NATRIURETIC PEPTIDES IN THE REGULATION OF THE HYPOTHALAMIC- PITUITARY-ADRENAL AXIS
Andrea Porzionato,* Veronica Macchi,* Marcin Rucinski,+ Ludwik K. Malendowicz,+ and Raffaele De Caro*
Contents
| 1. Introduction | 2 |
| 2. Biology of Natriuretic Peptides and Their Receptors | 2 |
| 2.1. Natriuretic peptides | 2 |
| 2.2. Natriuretic peptide receptors and their signaling mechanisms | 4 |
| 3. Expression of Natriuretic Peptides and Their Receptors in the | |
| HPA Axis | 4 |
| 3.1. Hypothalamus | 4 |
| 3.2. Pituitary gland | 8 |
| 3.3. Adrenal cortex | 10 |
| 3.4. Adrenal medulla | 11 |
| 4. Effects of Natriuretic Peptides on the HPA Axis | 12 |
| 4.1. Hypothalamus | 12 |
| 4.2. Pituitary gland | 15 |
| 4.3. Adrenal cortex | 18 |
| 4.4. Adrenal medulla | 20 |
| 5. Natriuretic Peptides and Pathophysiology of HPA Axis | 21 |
| 5.1. Adrenocortical adenomas and carcinomas | 21 |
| 5.2. Pheochromocytomas | 22 |
| 6. Concluding Remarks | 22 |
| Acknowledgment | 24 |
| References | 24 |
Abstract
Atrial (ANP), brain (BNP), and C-type (CNP) natriuretic peptides act by binding to three main subtypes of receptors, named NPR-A, -B, and -C. NPR-A and NPR-B are coupled with guanylate cyclase. Not only NPR-C is involved in removing natriuretic
* Department of Human Anatomy and Physiology, University of Padova, Padova, Italy
Ť Department of Histology and Embryology, Poznan University of Medical Sciences, Poznan, Poland
| International Review of Cell and Molecular Biology, Volume 280 | @ 2010 Elsevier Inc. |
|---|---|
| ISSN 1937-6448, DOI: 10.1016/S1937-6448(10)80001-2 | All rights reserved. |
peptides from the circulation but it also acts through inhibition of adenylyl cyclase. NPR-A binds ANP and BNP; NPR-B preferentially binds CNP; and NPR-C binds all natriuretic peptides with similar affinities. All natriuretic peptides and their recep- tors are widely present in the hypothalamus, pituitary, adrenal cortex, and medulla. In the hypothalamus, they reduce norepinephrine release, inhibit oxytocin, vaso- pressin, corticotropin-releasing factor, and luteinizing hormone-releasing hormone release. In the hypophysis, natriuretic peptides inhibit basal and induced ACTH release. Conversely, the effects of natriuretic peptides on secretion of growth, luteinizing, and follicle-stimulating hormones are not clear. Natriuretic peptides are known to inhibit basal and stimulated aldosterone secretion, through an increase of intracellular cGMP, and to inhibit the growth of zona glomerulosa. Inhibition or stimulation of glucocorticoid secretion by adrenocortical cells has been reported on the basis of the species involved, and an indirect effect mediated by adrenal- medullary cells has been hypothesized. In the adrenal medulla, natriuretic pep- tides inhibit catecholamine release and increase catecholamine uptake. It appears that natriuretic peptides may play a role in the pathophysiology of adrenocortical neoplasias and pheochromocytomas.
Key Words: Natriuretic peptides, Hypothalamic-pituitary-adrenal axis, ACTH secretion, Catecholamine secretion, Pheochromocytomas. @ 2010 Elsevier Inc.
1. INTRODUCTION
Numerous neuropeptides control the hypothalamic-pituitary-adrenal (HPA) axis, acting on both its central and peripheral branch. Natriuretic peptides are known to be included in this group of regulatory peptides, but only a few review articles have been published regarding the role of natriuretic peptides in the HPA axis, and mainly with reference to specific structures or specific pathological conditions (Gutkowska et al., 1997; Wiedemann et al., 2000). A comprehensive and updated review on the role of natriuretic peptides in all the levels of the HPA axis is still lacking. Thus, after a synthetic account on the biology of the natriuretic peptides system, we will herein review data indicating how natriuretic peptides and their receptors are expressed in all the anatomical components of the HPA axis, and are involved in the functional regulation of HPA axis under both physiological and pathological conditions.
2. BIOLOGY OF NATRIURETIC PEPTIDES AND THEIR RECEPTORS
2.1. Natriuretic peptides
Natriuretic peptides represent a family of three hormones called atrial natri- uretic peptides (ANP) (Kangawa and Matsuo, 1984), brain natriuretic peptides (BNP) (Sudoh et al., 1988), and C-type natriuretic peptides (CNP) (Sudoh
et al., 1990). ANP is a 28-amino acid peptide which has first been isolated from human atrial extract (Kangawa and Matsuo, 1984). BNP and CNP have been identified in the porcine brain (Sudoh et al., 1988, 1990). Figure 1.1 shows the sequences of natriuretic peptides. All peptides contain the conserved sequence FGXXXDRIGXXSGL. The flanking cysteines form a 17-amino acid disul- fide-linked ring that is required for biological activity. In some tissues, CNP-53 is cleaved to CNP-22.
ANP
1
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pro-ANP
2
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ANP-28 amw Como
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BNP
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pro-BNP
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g-BNP
(pro-BNP, in blood)
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BNP-32
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CNP
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126
pro-CNP
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CNP-53
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CNP-22
2.2. Natriuretic peptide receptors and their signaling mechanisms
The biological activity of the natriuretic peptides occurs via the activation of three different receptors, which have been cloned and pharmacologically characterized: NPR-A, NPR-B, and NPR-C. The first two receptors are coupled with guanylate cyclase. They consist of an extracellular ligand-binding domain, a short transmembrane region, a juxtamembranous protein kinase- homology domain, an alpha-helical or hinge region, and a C-terminal guanylyl cyclase catalytic domain, receptor dimerization being essential for the activation of the catalytic domain (reviewed in Anand-Srivastava and Trachte, 1993; Kuhn, 2003; Maack, 1992; Potter et al., 2006, 2009). Alternative splicing of NPR-A has recently been found to produce an isoform which does not bind ANP and may inhibit ligand-inducible cGMP generation by forming hetero- dimers with the wild-type receptor (Hartmann et al., 2008). NPR-A is acti- vated by ANP and BNP, ANP being more effective than BNP in stimulating cGMP production. NPR-B binds with higher affinity CNP (Fig. 1.2). All natriuretic peptide receptors are also known to be internalized and to some extent recycled as a result of ligand binding (reviewed in Pandey, 2009).
NPR-C binds all three natriuretic peptides with relatively similar affi- nities (Maack, 1992). It is a disulfide-linked homodimer with a single transmembrane domain which lacks the intracellular guanylate cyclase domain but is able to internalize natriuretic peptides after binding. Thus, it has first been considered to be involved in removing natriuretic peptides from the circulation (Fig. 1.2). Nevertheless, following studies suggested that NPR-C contains a 37-amino acid intracellular domain which is able to inhibit the adenylyl cyclase and activate phospholipase C, through activa- tion of Gi proteins. Moreover, NPR-C may also inhibit the mitogen- activated protein kinase pathway (signaling pathways of NPR-C reviewed in Anand-Srivastava, 2005).
3. EXPRESSION OF NATRIURETIC PEPTIDES AND THEIR RECEPTORS IN THE HPA AXIS
3.1. Hypothalamus
ANP has first been identified in the rat hypothalamus by radioimmunoassay (Glembotski et al., 1985; Tanaka et al., 1984) and its release in vitro from rat hypothalamus has also been demonstrated (Shibasaki et al., 1986a; Tanaka and Inagami, 1986). Although it must be considered that some authors reported cross-reactions with neurophysins in immunohistochemistry of the rat hypo- thalamus, suggesting absence of ANP immunostaining in the hypothalamus (Nilaver et al., 1989), ANP has been identified by immunohistochemistry in
ANP-28
BNP-32
CNP-22
S
L
S
K
S
K
S
G
G
R
G
L
G
G
L
F
G
L
G
L
G
F
G
HON-SLRRSS
C
HC
G
F
NSFRY-COOH
H2N-SPKMVOGSC G
C
C
KVLRRH-COOH
H2N-GLSKG
C
C
COOH
NPR-B
NPR-A
NPR-C
KHD
KHD
CGMP
GTP
CGMP
GTP
GC
GC
GTP
GTP
CGMP
CGMP
neurons of several mammal hypothalamic and nonhypothalamic brain struc- tures, such as the septum, anteroventral region of the third ventricle (AV3V), subfornical organum, paraventricular nucleus (PVN), preoptic, supraoptic (SON), infundibular and ventromedial nuclei, lateral hypothalamus, organum vasculosum lamina terminalis, median eminence, lamina terminalis, periaque- ductal gray matter, parabrachial nucleus, solitary tract nucleus, tegmental lateral dorsal nucleus, and periventricular regions (e.g., Chriguer et al., 2001; Gutkowska et al., 1997; Jirikowski et al., 1986; Kawata et al., 1985; Raidoo et al., 1998; Standaert et al., 1986a; Tanaka et al., 1984). Most ANP-immuno- reactive neurons in the PVN belong to the parvocellular division (Jirikowski et al., 1986; Kawata et al., 1985), but colocalization of ANP and oxytocin (OT) immunostaining has also been reported in some magnocellular neurons of the magnocellular division of the PVN and SON (Chriguer et al., 2001; Gutkowska et al., 1997; Jirikowski et al., 1986; Kawata et al., 1985). The densest terminal fields of ANP-containing fibers have been reported in the PVN of the hypothalamus, the bed nucleus of the stria terminalis, the inter- peduncular nucleus, and the median eminence (Standaert et al., 1986a), where ANP may modulate the release of anterior pituitary hormones (Franci et al., 1990, 1992; Gutkowska et al., 1997). It has also been reported that ANP- containing neurons in the PVN are the major source of ANP-containing nerve terminals in the median eminence (Palkovits et al., 1987). ANP-immunoreac- tive fibers have also been observed in close proximity with oxytocinergic fibers in the median eminence (Chriguer et al., 2001). In the hypophyseal portal blood, ANP has been found in 3-4 times higher concentrations than in the peripheral blood and the predominant species of IR-ANP in extracts of portal blood from adult rats is ANP(5-28), whereas in peripheral blood is ANP(1-28) (Lim et al., 1994). ANP mRNA has also been identified in the rat hypothala- mus (Chen et al., 1992; Dagnino et al., 1991; Gardner et al., 1987; Komatsu et al., 1992). The distribution of mRNA encoding prepro-ANP has also been investigated in rat brain by in situ hybridization and the highest relative con- centrations have been detected in the anteromedial preoptic nucleus of the medial preoptic area (Gundlach and Knobe, 1992; Ryan et al., 1997).
Analysis through RT-PCR in the rat and monkey hypothalamus did not identify BNP mRNA (Abdelalim et al., 2006; Langub et al., 1995). However, radioimmunoassay studies have detected BNP in porcine (Ueda et al., 1988), canine (Itoh et al., 1989), rat (Sone et al., 1991), human (Takahashi et al., 1992), and ovine (Pemberton et al., 2002) hypothalamus. BNP-immunoreactive fibers are also present in the PVN of the hypothalamus and many BNP-positive neurons have been retrogradely labeled in the tuberomammillary nucleus of the hypothalamus and in the pedunculopontine and laterodorsal tegmental nuclei (Moga and Saper, 1994; Saper et al., 1989). An immunohistochemical study on monkey hypothalamus revealed BNP-like immunoreactivity in the form of clusters of granules in the PVN, SON, and periventricular area (Abdelalim et al., 2006). These BNP-positive dots were located in neurons,
oligodendrocytes, astrocytes, and microglial cells. It has been suggested that BNP granules in the hypothalamus are originated from outside the hypothala- mus and reach the hypothalamus through the subfornical organ (Abdelalim et al., 2006) as high-density binding sites for BNP have been observed by autoradiography in rat subfornical organ, SON, and paraventricular hypotha- lamic nucleus (Brown and Czarnecki, 1990) and NPR-A mRNA has been found in the subfornical organ (Langub et al., 1995).
CNP has also been identified in the human hypothalamus in both high and low molecular weight forms by using radioimmunoassay (Totsune et al., 1994a). In the ovine hypothalamus, the concentration of CNP is much higher than that of ANP, similar amounts of CNP-53- and CNP-22-like immunore- active-CNP being present (Yandle et al., 1993). In the rat hypothalamus, the highest CNP tissue concentrations have been found in the arcuate nucleus and PVN (Herman et al., 1993; Minamino et al., 1993). Hybridization signals of lower intensity were reported in the medial, median, and periventricular preoptic area; the SON; dorsomedial, ventral premammillary, and lateral mammillary nuclei; and in the posterior hypothalamic area (Herman et al., 1993). Through in situ hybridization, prepro-CNP mRNA has also been detected in the rat hypothalamus, particularly in the anteromedial preoptic nucleus of the medial preoptic area (Ryan et al., 1997). CNP synthesis has also been identified in immortalized luteinizing hormone-releasing hormone (LHRH) neurons using RT-PCR, immunocytochemistry, and electron microscopic immunohistochemistry and in these cells CNP also elevated LHRH production in an autocrine manner (Middendorff et al., 1997). The concentration of CNP in the cerebrospinal fluid has been reported to be one order of magnitude greater than that of ANP (Kaneko et al., 1993).
Gibson et al. (1986) have found the highest levels of ANP binding in the rat subfornical organ, area postrema and olfactory apparatus; moderate ANP binding has been found throughout the brainstem and low levels in the forebrain, diencephalon, basal ganglia, cortex, and cerebellum. ANP-bind- ing sites have been identified in hypothalamic and nonhypothalamic struc- tures in both rat and guinea pig (Mantyh et al., 1987). ANP-binding sites have been identified in cerebral circumventricular organs, including the subfornical organ and organum vasculosum of the lamina terminalis (Mendelsohn et al., 1987). ANP-binding sites have also been reported in the SON and in the magnocellular and parvocellular subdivisions of the PVN in rat (Castrén and Saavedra, 1989). In particular, high numbers of ANP-binding sites have been reported in the circumventricular organs (the organon vasculosum laminae terminalis, subfornical organum, and area postrema) and selected hypothalamic (SON, median preoptic, and paraven- tricular) nuclei (Kurihara et al., 1987). ANP-binding sites have also been reported in the median eminence, pineal gland, subfornical organ, choroid plexus, but not in the magnocellular hypothalamic nuclei (Gerstberger et al., 1992).
NPR-B mRNA has been observed to be expressed throughout the hypo- thalamus, in the magnocellular and parvocellular paraventricular, the arcuate, and the SON, the median preoptic, anteroventral periventricular, tuberomam- millary, ventromedial, and suprachiasmatic nuclei (Langub et al., 1995). The three receptors have been identified in astrocyte glial and neuronal cultures from the hypothalamus and brain stem of 1-day-old rats, with astrocytes containing predominantly the ANP-A subtype and neurons predominantly the ANP-B subtype (Sumners and Tang, 1992). NPR-A and -B mRNA have also been identified in the GT1-7 cell line, an immortalized LHRH neuronal cell line. All the natriuretic peptides elevated cGMP production in this cell line with the following rank order of potency: CNP > ANP > BNP (Olcese et al., 1994). NPR-C expression has also been found in mammalian hypothal- amus (Peng et al., 1996; Sumners and Tang, 1992). In the human, ovine, and rat hypothalamus, higher expression of CNP and NPR-B have been found than of ANP, BNP, and NPR-A (Herman et al., 1993, 1996a; Komatsu et al., 1991; Langub et al., 1995; Minamino et al., 1993; Pemberton et al., 2002).
Natriuretic peptide expression in the rat hypothalamus has also been studied with reference to postnatal maturation. It has been found through radioimmunoassay that ANP concentrations show a first increase in the postnatal days 0-5 and a second one in the postnatal days 10-20, for a 16- fold final increase (Jankowski et al., 2004). Increments of ANP mRNA have also been found by in situ hybridization in the septohypothalamic, lateral, periventricular, and arcuate nuclei from postnatal day 4 until post- natal days 21-28 (Ryan and Gundlach, 1998). In rat SON and suprachias- matic nuclei, ANP peptide and mRNA have been identified starting from the 18th day of the fetal life (Lipari et al., 2005, 2007). CNP concentrations, instead, increased steadily until postnatal day 60, when they were 3.7-fold higher than at birth (Jankowski et al., 2004). As regards concentrations of the transcripts of the natriuretic peptides receptors in adult versus newborn rats, higher NPR-A concentrations, lower NPR-C concentrations, and no differences in NPR-B concentrations were found (Jankowski et al., 2004).
3.2. Pituitary gland
ANP has been identified in the rat anterior pituitary by radioimmunoassay (Gutkowska and Cantin, 1988) and ANP and BNP mRNA have been identified in human pituitary by PCR (Gerbes et al., 1994). The presence of all the three natriuretic peptides has been reported through radioimmu- noassay in the ovine pituitary, CNP (15.84 pmol/g wet weight) showing higher concentrations than ANP and BNP (0.25 and 0.26 pmol/g wet weight) (Pemberton et al., 2002). In the ovine hypophysis, the CNP-53- like IR-CNP was mainly present (Yandle et al., 1993). CNP has been identified by radioimmunoassay in the anterior lobe and neurointermediate lobe of the pituitary (Komatsu et al., 1991). ANP-like immunoreactivity has
been detected in the rat posterior hypophysis (Gutkowska et al., 1987). In particular, a low molecular weight peptide with a RP-HPLC pattern similar to that of the synthetic rat 28-amino acid C-terminal (Ser 99-Tyr 126) ANP was found, together with an unidentified higher molecular weight peptide (Gutkowska et al., 1987). An immunohistochemical study on rat pituitary gland has found ANP-, BNP-, and CNP-immunoreactive cells in the anterior lobe but not in the intermediate lobe of fetal and maternal glands on day 21 of gestation, fetal samples showing fewer and weakly stained cells (Chatelain et al., 2003). ANP has been localized by immunohistochemistry (Gutkowska and Cantin, 1988; Mckenzie et al., 1985) and in situ hybridization (Morel et al., 1989a) in rat gonadotroph cells. Its expression has also been reported through RT-PCR in LBT2 cells and primary mouse pituitary tissue (Thompson et al., 2009). An in vivo ultra- structural autoradiographic approach through intravenous injection of 125 I-ANP has also demonstrated internalization of extracellular ANP by gonadotroph cells (Morel et al., 1989a). BNP has not been found to be expressed in gonadotroph «T3-1 and LBT2 cells and rat and mouse pitui- taries (Thompson et al., 2009). Conversely, CNP has been localized in rat and mouse LH-positive cells of the anterior pituitary and in &T3-1 and LBT2 cells (McArdle et al., 1994; Thompson et al., 2009). Putative proces- sing enzymes of CNP (Furin and peptidyl &-amidating monoxygenase enzymes) have also been found to be expressed in «T3-1 cells and primary mouse pituitaries. Transcriptional analyses revealed that CNP expression is responsive to GNRH action in a protein kinase C and calcium-dependent manner (Thompson et al., 2009). The CNP promoter has been reported to work effectively also in somatomammotroph or somatotroph GH3 cells but not in corticotroph AtT20 cells (Ohta et al., 1993).
ANP-binding sites have also been reported in the anterior pituitary in rabbit (Gerstberger et al., 1992) and rat (Agui et al., 1989) and in the posterior pituitary in guinea pig (Mantyh et al., 1986) and rabbit (Gerstberger et al., 1992). NPR-A and -B have been isolated from a human pituitary cDNA library (Chang et al., 1989; Wilcox et al., 1991). In situ hybridization study in the anterior pituitary of rhesus monkey has revealed NPR-A and NPR-B mRNA (Wilcox et al., 1991). NPR-B mRNA has been identified in some cells of the anterior pituitary and in pituicytes in the neural lobe (Herman et al., 1996a). Northern blot analysis identified all three natriuretic peptide receptors in the mouse pituitary (Guild and Cramb, 1999). Analysis in alpha T3-1 and AtT-20 cell lines did not confirm the presence of NPR-A mRNA, suggesting cGMP accu- mulation occurring via NPR-B (Gilkes et al., 1994; McArdle et al., 1994). Ohta et al. (1993) have identified NPR-B in rat pituitary somatotroph and somatolactotroph progenitor cells. In situ hybridization in rat anterior pitui- tary gland has revealed NPR-A, -B, and -C mRNA in lactotroph, cortico- troph, and gonadotroph cells, but not in somatotroph or tyreotroph ones
(Grandclément et al., 1995; Thompson et al., 2009). NPR-C mRNA has been identified by in situ hybridization not only in the rat anterior lobe but also in the intermediate one (Herman et al., 1996b). Pituicytes cultured from adult rat neurohypophyses have been found to possess high-affinity binding sites for ANP, but ANP has been found not to modulate the basal or electrically stimulated release of OT or vasopressin (VP) from the isolated neurohypophysis in vitro (Luckman and Bicknell, 1991). NPR-B mRNA has also been found in the pars intermedia and posterior of the pituitary gland in the monkey (Wilcox et al., 1991) and rat (Konrad et al., 1992). NPR-B mRNA was also observed in the neural lobe of the pituitary gland, suggesting expression by pituicytes (Langub et al., 1995).
3.3. Adrenal cortex
Although Morel et al. (1988) did not report the presence of ANP mRNA in the rat adrenal cortex and Lee et al. (1994) did not report BNP mRNA and protein in the adrenal cortex by in situ hybridization and immunohisto- chemistry, ANP and BNP mRNA have been identified in human adrenal gland (without distinction between cortex and medulla) by PCR (Gerbes et al., 1994). Moreover, Lai et al. (2000) detected ANP mRNA and protein by in situ hybridization and immunohistochemistry in the rat zona glomer- ulosa and outer region of the zona fasciculata, but not in the remaining part of the zona fasciculata and in the zona reticularis. In bovine, CNP mRNA has also been demonstrated by RT-PCR in the zona glomerulosa tissue and cultured cells and CNP immunoreactivity has been localized in the outer- most region of the adrenal cortex but not in the inner portion of the zona fasciculata and zona reticularis (Kawai et al., 1996).
ANP-binding sites have been identified in the rat, guinea pig, rabbit, bovine, and tree shrew adrenal zona glomerulosa (e.g., Chai et al., 1986; De Lean et al., 1984; Fuchs et al., 1986; Gerstberger et al., 1992; Lynch et al., 1986; Mantyh et al., 1986; Mendelsohn et al., 1987; Morel et al., 1989b). In particular, internalization of ANP in rat adrenal glomerulosa cells was also demonstrated (Morel et al., 1989b). ANP-binding sites have also been observed in the rat zona fasciculata (Chai et al., 1986) and in the tree shrew and bovine zona fasciculata and reticularis (Fuchs et al., 1986; Nunez et al., 1990). Lynch et al. (1986) also reported the presence of ANP-binding sites in the rat zona fasciculata and reticularis, although at lower levels. Developmental changes have also been reported in the expres- sion of ANP receptors as in the 16-day-old rat ANP-binding sites are present throughout the cortical area but at 20 days gestation and 1 day postpartum ANP receptors are more numerous in the peripheral region (Scott and Jennes, 1989). Conversely, rat adrenocortical autotransplants regenerated from capsular-tissue fragments implanted in the musculus gra- cilis have been found not to significantly bind 125I-ANP (Belloni et al.,
1993). BNP-binding sites have also been identified in bovine adrenocortical membrane fractions (Higuchi et al., 1989).
In the rat zona glomerulosa cells, mRNA of the three natriuretic peptide receptors have been identified (Grandclément et al., 1997; Nagase et al., 1997; Vaillancourt et al., 1997). The amount of NPR-A mRNA has been found to be the highest (Grandclément et al., 1997) and Western analysis using poly- clonal anti-NPR-A and anti-NPR-B antibodies revealed the presence of NPR-A but not of NPR-B proteins (Vaillancourt et al., 1997). Wilcox et al. (1991) reported the presence of NPR-A but not NPR-B in the monkey zona glomerulosa by in situ hybridization and observed clusters of NPR-C-positive cells suggestive of endothelial, not necessarily secretory, cells. In the rat zona fasciculata cells, NPR-A but not NPR-B and -C receptor’s mRNA has been identified (Mulay et al., 1995; Vaillancourt et al., 1997). In the monkey zona fasciculata and reticularis, mRNA of the three receptors was not identified in secretory cells (Wilcox et al., 1991). NPR-A has also been identified in the H295R human adrenocortical cell line (Bodart et al., 1996).
Plasma ANP concentrations are known to decrease after water deprivation or hemorrhage and to increase after blood volume expansion. Conversely, data concerning plasma ANP concentrations in response to salt-overloading are contradictory. Water deprivation increases total number of ANP recep- tors in the adrenal gland of adult and maternal rats, but not of fetal ones (Deloof et al., 1999; Lynch et al., 1986). In particular, the density of NPR-C but not of NPR-B has been found to be increased (Deloof et al., 1999). Most studies, with few exceptions (Deloof et al., 2000) reported downregulation of the ANP receptors in the adrenal glands after salt-overloading (Lynch et al., 1986; Sessions et al., 1992).
3.4. Adrenal medulla
ANP, BNP, and CNP have been identified in rat, bovine, porcine, and human adrenal medulla cells (e.g., Babinski et al., 1992; Dagnino et al., 1991; De Léan et al., 1985; Komatsu et al., 1991; Lai et al., 2000; Lee et al., 1993, 1994; Mckenzie et al., 1985; Minamino et al., 1993; Morel et al., 1988; Nawata et al., 1991; Nguyen et al., 1990; Wolfensberger et al., 1995; reviewed in Kobayashi et al., 1998). In situ hybridization identified ANP mRNA in noradrenergic cells while immunohistochemistry identified ANP protein in both noradrenergic and adrenergic cells, suggesting ANP synthesis in noradrenergic cells and internalization in adrenergic ones (Morel et al., 1988). It has also been reported that the majority ANP-immunoreactive chromaffin cells are the adrenergic ones (Wolfensberger et al., 1995). Electrical stimulation of the splanchnic nerves has been found to cause the release of ANP-like immunoreactive material in isolated perfused calf adrenal glands (Duntas et al., 1993; Edwards et al., 1990) and enhance the uptake of ANP by chromaffin cells (Edwards et al., 1990).
It has been hypothesized that ANP produced in the adrenal medulla may act on the adrenal cortex (Lee et al., 1993, 1994; Nawata et al., 1991) and may be involved in the regulation of blood flow and even in the zonation of the adrenal cortex (Lee et al., 1994). 125I-ANP-binding sites have been identified by in vivo autoradiography in rat adrenal medulla and by in vitro autoradiography in bovine, guinea pig, tree shrew, rabbit, and rat adrenal medulla (Bormann et al., 1989; Fuchs et al., 1986; Gerstberger et al., 1992; Konrad et al., 1992; Maurer and Reubi, 1986; Morel et al., 1988; Niina et al., 1996). Specific binding sites for ANP have been identified in the phaeochromocytoma cell line PC12 (Boumezrag et al., 1988). 125I-ANP-binding sites, instead, have not been identified in mouse, hamster, monkey, human, and in other studies in bovine, guinea pig, and rat (Chai et al., 1986; Lynch et al., 1986; Mantyh et al., 1986; Maurer and Reubi, 1986; Stewart et al., 1988). In rat, 125I-BNP and125I-[Tyrº]-CNP-binding sites have also been identified (Konrad et al., 1992). The number of ANP-binding sites has also been found to increase regularly in fetal (day 17 of gestation and term) and neonatal (weeks 1 and 4) rats (Deloof et al., 1994).
NPR-A and NPR-B mRNA, but not NPR-C mRNA, have been iden- tified by in situ hybridization in adrenal chromaffin cells of monkey (Wilcox et al., 1991). This finding is in keeping with displacing of 125I-ANP and125I-BNP bindings by ANP and BNP but not by selective analogues for NPR-C in rat and bovine (Konrad et al., 1992; Niina et al., 1996). In rat adrenal medulla, the mRNA of the three subtypes has been found by in situ hybridization, the amount of NPR-A mRNA being the highest (Grandclément et al., 1997). The above receptors were selectively present in adrenaline-containing chromaffin cells and not in the noradrenaline- containing ones (Grandclément et al., 1997).
NPR-A mRNA expression has also been reported to be significantly increased in the adrenal medulla of adult pro-ANP gene-disrupted mice (O’Tierney et al., 2007).
4. EFFECTS OF NATRIURETIC PEPTIDES ON THE HPA AXIS
4.1. Hypothalamus
ANP has been found to modulate the membrane excitability of neurons of the lateral septal nucleus, lateral paraolfactory area, bed nucleus of the anterior commissure, and medial preoptic area (Wong et al., 1986). ANP has been found to produce significant increases in blood pressure and heart rate when injected into the preoptic suprachiasmatic nucleus, suggesting it may play an important role in central cardiovascular regulatory mechanisms (reviewed in Oparil et al., 1996). Moreover, intracerebroventricular injection of ANP has
been found to inhibit dehydration- and angiotensin II-induced water intake in conscious, unrestrained rats (Antunes-Rodrigues et al., 1985).
ANP, BNP, and CNP have been found to reduce both spontaneous and acetylcholine, K+ and angiotensin II-evoked norepinephrine release in slices of rat hypothalamus (Giridhar et al., 1992; Vatta et al., 1996). ANP has been found to increase neuronal norepinephrine uptake in hypothalamus (Fernandez et al., 1993) and in organum vasculosum lamina terminalis and organum subfornical (Vatta et al., 1995) of rat. BNP and CNP have also been found to increase neuronal norepinephrine uptake in slices of rat hypothalamus and, particularly, independently of the hypothalamic nucleus involved (pre- optic, periventricular, paraventricular, SON, and arcuate nuclei; median emi- nence) (Rodriguez Fermepin et al., 2000; Vatta et al., 1996). ANP has been found to diminish monoamine oxidase activity, but not catechol-O-methyl transferase activity and the formation of deaminates metabolites, in rat hypo- thalamus slices (Vatta et al., 1998). Moreover, centrally applied ANP has been reported to increase the hypothalamic content of NE, diminish its utilization and turnover, inhibit basal and KCl-evoked tyrosine hydroxylase activity, and increase cyclic GMP levels (Vatta et al., 1999).
Experimental studies on rats have shown that ANP microinjections into the third ventricle do not change basal levels of OT but attenuate the increase in OT secretion induced by hyperosmolarity (Chriguer et al., 2001; Gutkowska et al., 1997; Lewandowska et al., 1992; McCann et al., 1996; Poole et al., 1987). ANP has also been found to markedly inhibit OT release in vitro from the isolated neurointermediate lobe both under basal condition as well as during stimulation (Lewandowska et al., 1992; Poole et al., 1987).
ANP has been proven to be a potent inhibitor of VP neurons of the PVN in anesthetized rats (Okuya and Yamashita, 1987; Standaert et al., 1987). Intrave- nous infusion of ANP has been found to reduce dehydration and hemorrhage- induced VP release in the rat (Samson, 1985). ANP has been reported to inhibit the basal and stimulated release of VP in hypothalamushypophyseal slice preparations and in superfused rat posterior pituitary gland (Januszewicz et al., 1986; Obana et al., 1985). ANP has also been found to inhibit VP release in vitro from the neurointermediate lobes both under basal condition as well as during stimulation (Lewandowska et al., 1992; Poole et al., 1987). Intracerebroven- tricular injections of ANP, BNP, or CNP have been found to show inhibitory effects on the VP secretion (e.g., Iitake et al., 1986; Lewandowska et al., 1992; Makino et al., 1992; Poole et al., 1987; Samson et al., 1991; Shirakami et al., 1993). The three natriuretic peptides have also been reported to inhibit the basal secretion of VP from rat SON neurons in dissociated cell preparations, CNP being the most potent inhibitory factor (Yamamoto et al., 1997). Reduction of VP plasma levels due to central ANP stimulus has been observed in both euhydrated and dehydrated sheeps (Lee et al., 1987) and rats (Manzanares et al., 1990). In rats, inhibition of VP secretion was not accom- panied by modifications in the concentrations of 3,4-dihydroxyphenylacetic
acid and dopamine, indicating that ANP-induced suppression of VP secretion is not mediated by tuberohypophysial or tuberoinfundibular dopaminergic neurons (Manzanares et al., 1990). Conversely, in dehydrated but not in euhydrated rabbits, infusion of ANP has also been found to inhibit secretion of VP (Gerstberger et al., 1992). ANP and BNP have also been found to decrease the firing rate and hyperpolarize the membrane potential in phasically firing (putative VP) but not in nonphasically firing (putative OT) neurons of SON; inhibition of cGMP synthesis was also reported in neurons of SON (Akamatsu et al., 1993). ANP and BNP have been found to inhibit AV3V neurons, suggesting direct actions of the peptides on drinking, and in the SON, these peptides inhibited selectively putative VP neurons but not putative OT neurons, suggesting direct actions of the peptides on VP secretion (Yamamoto et al., 1995). The central inhibition of OT and VP release from the magno- cellular neurosecretory cells by ANP has been suggested to be mediated by presynaptic inhibition of glutamate release from osmoreceptor afferents derived from the organum vasculosum lamina terminalis (Richard and Bourque, 1996). Experiments through injection of highly specific antiserum against ANP into the third cerebral ventricle of rats also showed that the inhibitory role in suppressing ACTH release during stress is in part mediated by inhibition of VP release (Franci et al., 1992). Conversely, it has also been reported an increase of the plasma VP response to acute moderate hemorrhage after intracerebroventricular injection of CNP (Charles et al., 1995).
It has also been demonstrated that CNP has a potent and selective inhibitory effect on magnocellular cells of SON and PVN, which is mediated by NPR-C (Rose et al., 2005). Moreover, since NPR-C binds all natriuretic peptides with equal affinity (Levin et al., 1998), it has been suggested that this receptor could mediate the hypothalamic effects by the other natriuretic peptides (Rose et al., 2005).
It has been reported that intracerebroventricular injection of ANP in rats does not modify tuberoinfundibular dopaminergic neuronal activity and serum prolactin levels, but it attenuates the stimulatory effects of angiotensin II on tuberoinfundibular dopaminergic neuronal activity, negatively modulating also the inhibitory effect on serum prolactin level (Yen and Pan, 1997). ANP and BNP have been reported to cause a dose-dependent increase in dopamine accumulation in cultured rat hypothalamic cells through an increase in intra- cellular cGMP concentration (Kadowaki et al., 1992). Franci et al. (1992) also reported a role by ANP in augmenting the prolactin release in stress through a hypothalamic action. On the other hand, CNP has been found to stimulate prolactin secretion in rats by a hypothalamic site of action (Huang et al., 1992a; Samson et al., 1995).
In rat, ANP has been found to inhibit acetylcholine- and KCl-induced release of corticotrophin-releasing factor in vitro (Grossman et al., 1993; Ibanez-Santos et al., 1990; Takao et al., 1988) and to increase its immuno- reactivity in the hypothalamus in vivo (Biró et al., 1996). In humans,
intranasal administration of ANP has been shown to inhibit secretion of ACTH stimulated by hypoglycemia but not by CRH/VP, suggesting inhibition of central nervous mechanisms of HPA activation, probably at the level of the hypothalamus (Perras et al., 2004). High doses of BNP and CNP have been found to increase and decrease, respectively, corticotropin- releasing factor immunoreactivity in the hypothalamus (Gardi et al., 1997). Charles et al. (1992) reported suppression of the adrenocortical secretion in the sheep after intracerebroventricular injection of CNP, while ANP had no significant effect. The same research group in a following experiment reported increase of the plasma cortisol response to acute moderate hemor- rhage after intracerebroventricular injection of CNP, although the plasma ACTH response was not significantly different, probably for feedback inhibition (Charles et al., 1995). Intracerebroventricular injections of BNP and CNP have been found to inhibit the stress-induced corticosterone response, without changes of the basal secretion, thus suggesting a hypotha- lamic actions of these hormones (Jászberényi et al., 1998, 2000). Experi- ments through injection of highly specific antiserum against ANP into the third cerebral ventricle of rats to immunoneutralize hypothalamic ANP showed that ANP inhibits basal but not stress-induced GH release. The same study did not find a modulatory role by ANP in thyroid-stimulating hormone release (Franci et al., 1992).
ANP and CNP have been reported to inhibit LHRH release (Huang et al., 1992b; Samson et al., 1992, 1993). Microinjection of antisera against ANP into the third cerebral ventricle of rats produced elevation of plasma LH levels (Franci et al., 1990). Conversely, some authors reported a slight increase in LH serum levels after applying ANP into rat PO/AH by means of push-pull cannula, probably through reduction of preoptic GABA release rates (Rodriguez Lopez et al., 1993). Recent studies involving ricin A chain conjugated ANP suggest that ANP binding to clearance receptors in the hypothalamus displaces CNP from the shared clearance receptor, making more CNP available to inhibit LHRH release through binding to the ANPR-B receptor (Samson et al., 1992, 1993). The perfu- sion of hypothalamusohypophysial complex with ANP has also been found to increase the beta-endorphin concentration, whereas such an effect was not reported in isolated neurointermediate lobes of rat pituitary (Ikeda et al., 1989).
4.2. Pituitary gland
Although a first study in the rat did not report inhibition of basal and CRF-, VP-, and angiotensin II-induced ACTH release by ANP both in vivo and in vitro (Hashimoto et al., 1987), following studies in the adult rat, reported inhibition by ANP of ACTH release both in vivo (Antoni et al., 1992; Fink et al., 1991; Kovács and Antoni, 1990) and in vitro (King and Baertschi, 1989;
Kovács and Antoni, 1990; Shibasaki et al., 1986b). In cultured ovine and rat anterior pituitary cells, CRF- and VP-stimulated, but not basal, ACTH secretion has also been found to be inhibited by rat ANP (Dayanithi and Antoni, 1990; Engler et al., 1990). This effect was also confirmed for all three natriuretic peptides in vitro in mouse hemipituitary preparations over a concentration range of 10-12 - 10-10 M (Guild and Cramb, 1999) and in vivo in humans (Kellner et al., 1992). Inhibition of ACTH release was accompanied by stimulation of cGMP accumulation (Guild and Cramb, 1999). Conversely, it must also be considered that in the work by Ur et al. (1991) significant differences were not found in mean peak cortisol and ACTH levels between ANP and placebo infusion. In young healthy men exposed to ANP infusion and stimulation of ACTH secretion by CRH and/ or VP, Bierwolf et al. (1998) reported inhibition of ACTH/ cortisol secretory responses within the first hour after stimulation with secretagogues and augmentation of ACTH/cortisol response during the third hour after stimu- lation. The early suppression was ascribed to direct inhibitory actions of ANP on both adrenal release of cortisol and pituitary release of ACTH; the late effect was ascribed to secondary hypovolemic actions. Natriuretic peptides have been found to stimulate cGMP accumulation in AtT-20 cell line, CNP being the most effective hormone (Fowkes and McArdle, 2000), but not to affect basal or CRF-stimulated ACTH secretion (Gilkes et al., 1992, 1994). In AtT-20 cells, ANP has also been found to reduce POMC mRNA content, together with a modest reduction in the release and cell content of beta- endorphin-like immunoreactivity (Tan et al., 1994). ANP, BNP, and CNP have also been reported to inhibit CRF-stimulated ACTH secretion and proopiomelanocortin mRNA expression in in vitro fetal rat pituitary gland in late gestation (Chatelain et al., 2003). The three natriuretic peptides are equipotent in inhibiting the CRF-stimulated ACTH release (Chatelain et al., 2003; Guild and Cramb, 1999). Intracerebroventricular administration of BNP has also been found to suppress endothelin-induced ACTH secretion in rat (Makino et al., 1990). Other studies, instead, have not reported inhibition on ACTH secretion by ANP in cultured pituitary cells of rat, sheep, and horse (e.g., Bowman et al., 1997; Mulligan et al., 1997). Horvath et al. (1986) also reported a small but significant stimulation of ACTH release by ANP in superfused rat pituitary cells. Mulligan et al. (1997) also reported absence of inhibition on ACTH secretion by CNP in horse cultured pituitary cells. Such differences may be explained with reference to different in vitro models or concentrations of ANP.
The three natriuretic peptides have been reported to cause increases in cGMP content in GH3 cells (McArdle et al., 1993). Experimental studies on rat pituitary have reported ANP suppression of basal, growth hormone releasing factor-stimulated and stress-induced GH secretion (Shibasaki et al., 1986b). Conversely, other studies on superfused anterior pituitary cells did not revealed any effect by ANP on GH release (Horvath et al., 1986;
Shimekake et al., 1994) and central administration of ANP in rats (Murakami et al., 1988) stimulated GH release. In other studies, stimulation of GH release by natriuretic peptides has been reported from rat cultured anterior pituitary cells, such as GH3 cell line, ANP and CNP being the most effective hormones (Fowkes and McArdle, 2000; Hartt et al., 1995). Shimekake et al. (1994) reported stimulation of GH release by CNP, but not ANP, from GH3 cells. In conclusion, effects of natriuretic peptides on GH release seem to be equivocal.
ANP has been found to produce cGMP accumulation in rat anterior pituitary cells in culture, basal, and ANP-induced cGMP levels being higher in cell populations enriched in gonadotrophs compared to gonadotroph- impoverished preparations, but alteration of LH release was not reported (Simard et al., 1986). ANP, BNP, and CNP have also been found to stimulate cGMP accumulation in primary cultures of rat pituitary cells and &T3-1 and LBT2 gonadotroph-derived cells, ANP and CNP being the most effective hormones in stimulating LBT2 and «T3-1 cells, respectively (Fowkes and McArdle, 2000; McArdle et al., 1993; Thompson et al., 2009). Moreover, «T3-1 cells produced significantly more cGMP in response to CNP than other cell lines, that is, GH3, TtT-GF, and AfT-20 cells (Fowkes and McArdle, 2000). CNP has been found to inhibit GnRH-stimulated calcium mobilization in «T3-1 gonadotroph-derived cells (Fowkes et al., 1999). Moreover, CNP has been reported to stimulate the human glyco- protein hormone a-subunit promoter in LBT2 cells, although not in &T3-1 ones (Thompson et al., 2009). However, CNP had no measurable effects on basal and GnRH-stimulated LH release and on cell proliferation (McArdle et al., 1993; Thompson et al., 2009). Conversely, stimulation of LH and FSH release had been reported by ANP in anterior pituitary cells of rats (Horvath et al., 1986), although recently not confirmed (Thompson et al., 2009). Intracerebroventricular injection of ANP has also been reported to induce an increase in plasma LH levels without significantly affecting prolactin release (Steele, 1990). On the other hand, Standaert et al. (1986b) had reported in vivo inhibition of the release of LH by ANP. In conclusion, effects of natriuretic peptides on LH and FSH release will have to be better clarified in the future.
ANP has been found not to affect thyrotropin and PRL release from dispersed rat anterior pituitary cells, but central administration of high doses in rats has been reported to cause significant inhibition of PRL release (Horvath et al., 1986; Samson and Bianchi, 1988). ANP, BNP, and CNP have also been found to stimulate cGMP accumulation in TtT-GF cell line, a pituitary folliculo-stellate-like cell line derived from an isologously transplan- table pituitary thyrotropic tumor line, CNP being the most effective hormone (Fowkes and McArdle, 2000). Synthetic rat ANP has also been found to attenuate, in a dose-dependent manner, basal and CRF-induced secretion of
proopiomelanocortin-derived peptides from cultured intermediate lobe cells of rat pituitary (Shibasaki et al., 1986b).
4.3. Adrenal cortex
In the cells of the mammal adrenal zona glomerulosa, ANP has been found to inhibit basal and angiotensin II-, K+ -, PACAP-, calcium ionophores and ACTH-stimulated aldosterone secretion via a cGMP-mediated mechanism (e.g., Atarashi et al., 1984; Bodart et al., 1997; Chartier et al., 1984; Cozza et al., 1993; Deloff et al., 1992; Elliott et al., 1993; Isales et al., 1989; Kudo and Baird, 1984-1985; Lotshaw et al., 1991; Mazzocchi et al., 1987; Naruse et al., 1987; Nawata et al., 1991; Nussdorfer et al., 1988-1989; Spiessberger et al., 2009; Vesely et al., 1995; reviewed in Ganguly, 1992; Nussdorfer, 1996). Inhibition of aldosterone production in adrenal zona glomerulosa cells has also been reported by a specific ligand for NPR-C (Isales et al., 1992). Inhibition of angiotensin II-induced aldosterone production by a NPR-A agonist has also been demonstrated in H295R human adrenocortical cell line (Bodart et al., 1996). On the other hand, the pro-ANP 1-30 and 31-67 have been found not to affect angiotensin II-stimulated aldosterone secretion in calf adrenal cells (Denker et al., 1990). ANP-induced inhibition of aldosterone secretion has also been found to be mediated by inhibition of T-type calcium channels (McCarthy et al., 1990). ANP has also been found to diminish cAMP levels in glomerulosa cells through stimulation of a phosphodiesterase by cGMP (MacFarland et al., 1991; Nikolaev et al., 2005; Spiessberger et al., 2009). Moreover, ANP has been found to have no effect on ACTH-stimulated aldosterone levels in mice with a homozygous inactivation of the cGMP- dependent protein kinase II, suggesting involvement of this enzyme in ANP- mediated inhibition of aldosterone expression (Spiessberger et al., 2009). Inhibition of the phosphorylation of the myristoylated alanine-rich C-kinase substrate (MARCKS) and the synthesis and phosphorylation of the steroido- genic acute regulatory protein (StAR) has also been found to play a pivotal role in inhibition of aldosterone production (Calle et al., 2001; Cherradi et al., 1998). ANP has also been found to inhibit the phosphorylation of histone H3 in bovine adrenal glomerulosa cells (Elliott, 1990).
In cultured human and bovine adrenal cells, BNP has also been found to increase intracellular cGMP and inhibit ACTH- and angiotensin II-stimulated aldosterone secretion (Hashiguchi et al., 1989; Higuchi et al., 1989; Nawata et al., 1991). In calf adrenal zona glomerulosa cells in culture, BNP has also been found to inhibit AII-, K+,- and ACTH-stimulated increase in aldoste- rone, while CNP showed only weak effects (Cozza et al., 1993). In bovine adrenal zona glomerulosa cells in culture, CNP has also been found to increase the basal secretion of cGMP and inhibit ACTH-stimulated increase in aldoste- rone (Kawai et al., 1996). In primary human adrenocortical cells investigated through intracellular cGMP assay and cDNA microarray, BNP has been
reported to induce cGMP synthesis and oppose 49% of ANGII-regulated genes, with particular reference to genes involved in cell growth and differen- tiation, steroid synthesis, and cholesterol synthesis and transfer (Liang et al., 2007). Treatment with BNP alone, instead, produced downregulation only of a small number of genes. Moreover, BNP inhibited ANGII-induced stimula- tion of the binding of LDL and HDL and of the release of aldosterone, cortisol, and estradiol (Liang et al., 2007).
ANP has also been reported to inhibit the growth of rat zona glomerulosa (Mazzocchi et al., 1987; Rebuffat et al., 1988; Trejter et al., 2002); this action has been reported with both ANP and ANP antagonist, suggesting a non- receptor-mediated mechanism of action (Trejter et al., 2002).
ANP has been found to decrease basal and ACTH-stimulated glucocorti- coid production from cultured human and cow zona fasciculata cells (Carr and Mason, 1988; Hashiguchi et al., 1989; Naruse et al., 1987; Nawata et al., 1991). This effect was also observed in the Y1 mouse adrenocortical tumor cell line (Heisler et al., 1989). Other studies did not show effects of ANP on glucocor- ticoid secretion in rat (Cantin and Genest, 1985; Ganguly, 1992). It has also been found that isolated fasciculata cells of rat adrenal cortex, when incubated with ANP, stimulated the levels of cyclic GMP and corticosterone production in a concentration-dependent manner (Jaiswal et al., 1986). ANP treatment for 6 days has been reported to increase plasma concentrations of cortisol by about 20% in normal guinea pigs and by about 3.5-fold in dexamethasone/captopril administered animals, indicating a direct action on the adrenal gland. Although ANP has been found not to affect cortisol secretion from dispersed guinea pig zona fasciculata-reticularis cells, a raise in cortisol production has been reported in guinea pig adrenocortical slices containing adrenomedullary tissue, suggest- ing an indirect effect, mediated by medullary chromaffin cells, under the secretagogue action of ANP (Raha et al., 2006). In fact, the bulk of evidence indicates that catecholamines are able to stimulate steroidogenesis through binding beta-adrenoreceptors on adrenocortical cells (Lightly et al., 1990; Mazzocchi et al., 1998; Nussdorfer, 1996) and various peptides, such as neuromedin U (Malendowicz et al., 1994, 2009), VIP and PACAP (Nussdorfer and Malendowicz, 1998a), neuropeptide-Y (Spinazzi et al., 2005), tachykinins (Nussdorfer and Malendowicz, 1998b), endothelins (Malendowicz et al., 1998; Nussdorfer et al., 1999), and adrenomedullin (Nussdorfer, 2001), have been found to stimulate cortisol secretion by indirect action on the medullary chromaffin cells. Lastly, in the evaluation of ANP effects on adrenal gland, relevant species-specific differences must be considered.
BNP has also been found to inhibit basal and ACTH-stimulated cortisol production in cultured human, bovine, and guinea pig adrenal cells (Hashiguchi et al., 1989; Higuchi et al., 1989). Inhibition of basal and ACTH-stimulated dehydroepiandrosterone production by ANP and BNP, although less potent, has also been demonstrated in human and bovine adrenal cell cultures (Higuchi
et al., 1989; Nawata et al., 1991). Many in vitro studies have been performed on transformed cell lines and different findings in studies performed on cell cultures may derive from the fact that transformed cell lines may not appropriately reflect the features of primary human adrenal cells (Liang et al., 2007).
4.4. Adrenal medulla
In the literature, the three natriuretic peptides have been reported to increase cGMP content in the rat and bovine adrenal chromaffin cells (Fernández et al., 1997; Fethière et al., 1993; Tsutsui et al., 1994; Yanagihara et al., 1991). ANP has been reported to inhibit catecholamine release by adrenal medulla cells (e.g., Babinski et al., 1995; Fernández et al., 1997; Papouchado et al., 1995; Vatta et al., 1994; reviewed in Kobayashi et al., 1998). In particular, ANP has been demonstrated to inhibit acetyl- choline-induced membrane currents in bovine chromaffin cells (Bormann et al., 1989) and to enhance activity of potassium conductance (Ganz et al., 1994). ANP mediates also indirect sympathoinhibitory effects through antagonism of the renin-angiotensin (Atlas and Maack, 1987) and endothe- lin (Emori et al., 1993; Neuser et al., 1993) systems, which modulate catecholamine release from the adrenal medulla (Armando et al., 2004; Lange et al., 2000). ANP has also been found to reduce monoamine oxidase activity, but not catechol-O-methyl transferase activity and the formation of deaminates metabolites, in rat adrenal medulla slices (Vatta et al., 1998). In cultured bovine adrenal medullary cells ANP increases phosphorylation and activity of tyrosine hydroxylase (Yanagihara et al., 1991), whereas, in rat adrenal medulla, inhibition of both spontaneous and KCl-evoked TH activity has been reported (Fernández et al., 1997). In rat adrenal medullary cells, ANP has also been found to increase noradrenaline uptake (Vatta et al., 1992) and endogenous content and to diminish noradrenaline utilization (Fernández et al., 1997). Pro-ANP gene-disrupted mice have also found to show an increase in circulating catecholamine levels (Melo et al., 1999) and upregulation of tyrosine hydroxylase expression in sympathetic ganglia and adrenal medulla (O’Tierney et al., 2007). Conversely, in some studies ANP has been found to potentiate catecholamine secretion due to low concentra- tions (3 uM) of nicotine in bovine adrenal chromaffin cells (O’Sullivan and Burgoyne, 1990) and to enhance catecholamine release from bovine adre- nomedullary cultured cells of guinea pigs (Raha et al., 2006).
BNP has also been show to stimulate tyrosine hydroxylase activity, in cultured adrenomedullary cells (Yanagihara et al., 1991), and to decrease spontaneous and KCl-induced norepinephrine release and enhance nor- adrenaline uptake in rat adrenal medulla slices (Vatta et al., 1996, 1997). It has been suggested that BNP may contribute to increase adrenal tyrosine hydroxylase expression in ANP- - mice due to elevated levels of NPR-A (O’Tierney et al., 2007).
CNP has also been found to inhibit catecholamine secretion stimulated by nicotine (10 µM), acetylcholine (50 µM), or KCI (30 mM) in bovine chromaf- fin cells, through cGMP-dependent and -independent mechanisms (Babinski et al., 1995; Rodriguez-Pascual et al., 1996). Inhibition of spontaneous and KCl-induced catecholamine release has also been demonstrated in rat adrenal medulla slices, together with enhancement of noradrenaline uptake (Vatta et al., 1997). CNP has also been reported to stimulate catecholamine synthesis, through increasing of intracellular cGMP content and activation of tyrosine hydroxylase, in cultured bovine adrenal medullary cells (Tsutsui et al., 1994).
5. NATRIURETIC PEPTIDES AND PATHOPHYSIOLOGY OF HPA AXIS
5.1. Adrenocortical adenomas and carcinomas
Plasma levels of ANP and BNP have been found to be higher in patients with primary aldosteronism due to aldosterone-producing adrenal adenoma or bilateral adrenal hyperplasia, reduced levels being found after adenoma resection (Jakubik et al., 2006; Kato et al., 2005; Lapinski et al., 1991; Naruse et al., 1994; Tunny and Gordon, 1986; Yamaji et al., 1986). BNP was more closely correlated with blood volume, being a more sensitive marker of cardiac load or volume status in patients with primary aldoste- ronism (Kato et al., 2005).
In human adrenocortical tumors, CNP has been found by radioimmu- noassay in concentration of 0.69 ± 0.19 pmol/g wet tissue, with respect to 0.49 ± 0.22 pmol/g wet tissue in normal adrenal glands (cortex and medulla mixed) (Totsune et al., 1994b). BNP has been found by radioim- munoassay in concentrations of 0.203 ± 0.061 pmol/g wet tissue in normal adrenal glands (cortex and medulla mixed), 0.230 ± 0.062 pmol/g wet tissue in aldosteronomas, and 0.180 ± 0.054 pmol/g wet tissue in adreno- cortical adenomas with Cushing’s syndrome (Totsune et al., 1996). Multi- ple molecular forms of BNP have been reported in aldosteronomas (Totsune et al., 1996). Significant differences in the allelic frequencies of restriction fragment length polymorphisms in the ANP gene have been found between angiotensin II-unresponsive and -responsive aldosterone- producing tumors (Tunny et al., 1994). Enhanced expressions of ANP and BNP from adrenal medulla surrounding aldosteronomas have also been reported (Lee et al., 1993, 1994).
The inhibitory effect of natriuretic peptides on aldosterone production from aldosteronomas has been found to be less potent or even absent (Hirata et al., 1985; Mantero et al., 1987; Naruse et al., 1987; Nawata et al., 1991; Rocco et al., 1989; Shionoiri et al., 1988, 1989). Moreover, ANP has been found not to inhibit basal and ACTH-stimulated cortisol secretion in tissue
slices of Cushing’s adenoma (Shionoiri et al., 1989). Shionoiri et al. (1988, 1989) did not report NPR-A presence in aldosteronoma by binding assay and immunohistochemistry. mRNA of the three NPRs has been found in the aldosteronomas (Chen et al., 1995; Sarzani et al., 1999). NPR-B and -C mRNA, but not NPR-A mRNA, have been reported to be downregulated in aldosteronomas by Chen et al. (1995), while Sarzani et al. (1999) did not report significant differences. Moreover, ANP-binding sites have also been reported to be reduced in aldosteronomas (Ohashi et al., 1991; Sarzani et al., 1999).
5.2. Pheochromocytomas
In patients with pheochromocytoma, higher plasma ANP concentration has been found with respect to controls and patients with essential hypertension and ANP concentrations has been reported to decline after removal of the tumor, suggesting that catecholamines produced by the chromaffin tumor induce ANP secretion through stimulation of adrenergic receptors (Stepniakowski et al., 1992). In human pheochromocytomas, BNP and CNP have been found in concentrations of 0.205 ± 0.037 pmol/g wet tissue (Totsune et al., 1996) and 0.54 ± 0.40 pmol/g wet tissue, respec- tively (Totsune et al., 1994b). Multiple molecular forms of BNP have been reported in pheochromocytomas (Totsune et al., 1996).
Nakamaru et al. (1989) reported increases in plasma levels of catechola- mines after intravenous infusion of ANP in patients with pheochromocy- toma but they did not observe modifications of the basal release of catecholamines from isolated superfused pheochromocytoma tissue. Release of catecholamines from tissue slices of pheochromocytoma has been found to be inhibited by hANP in a dose-dependent manner, binding assays using 125I-ANP have revealed a single class of high-affinity binding sites for ANP and immunohistochemistry has also revealed the presence of ANP receptors (Shionoiri et al., 1987, 1989).
6. CONCLUDING REMARKS
The preceding sections of the paper have shown that a huge mass of data strongly suggests that natriuretic peptides play an important role in the regulation of the function of the HPA axis, although some important topics have not yet received adequate answers. The above data and doubts may be synthesized as follows. Natriuretic peptides and their receptors are widely expressed in the hypothalamus, although some doubts still remain if BNP is locally expressed or internalized through receptor binding. In the hypothal- amus, natriuretic peptides play different roles: reduction of norepinephrine
release; inhibition of OT, VP, corticotropin-releasing factor, growth hor- mone, and LHRH release. All the natriuretic peptides and their receptors are present in the hypophysis; in particular, the three subtypes of receptors seem to be present in lactotroph, corticotroph, gonadotroph cells, equivocal data being present regarding somatotroph ones. Nevertheless a huge mass of studies investigating the effects of natriuretic peptides on pituitary cell populations, some doubts are still present. Majority of literature (although not all the literature) reported inhibition of both basal and induced ACTH release by natriuretic peptides. Instead really contrasting data are present regarding effects of natriuretic peptides on GH, LH, and FSH release, being reported inhibition, stimulation, or absence of effects in different studies. Such differences may be explained with reference to different in vitro or in vivo models but surely request further analyses in the future. Natriuretic peptides have mainly been identified in the zona glomerulosa and adrenal medulla. They are known to inhibit aldosterone secretion and growth of zona glomerulosa. More problematic are data regarding effects of natriuretic peptides in the zona fasciculata. Inhibition or stimulation of glucocorticoid secretion by adrenocortical cells has been reported and these contradictory data may be explained with reference to the different species considered. Lastly, in the adrenal medulla, natriuretic peptides inhibit catecholamine release and increase catecholamine uptake.
Despite the extensive experimental investigations of the natriuretic peptide biology under both normal and pathological conditions many interesting problems remain to be addressed in the next years. It will have to be better investigated how the central nervous system control the natriuretic peptide system in the central and peripheral branches of the HPA axis. Moreover, natriuretic peptides modulate different hormonal systems and further experiments are needed to better ascertain the func- tional interrelationships between these systems. Data reviewed in Sections 5.1 and 5.2 indicate that the natriuretic peptide system is involved in the pathophysiology of adrenal cortical and medullary neoplasias but further studies will be necessary.
The study of these and many other basic topics, along with the develop- ment of new potent and selective agonists and antagonists of the different receptors, not only will open new frontiers in the knowledge of the physiology of the HPA axis, but also will shed light on new therapeutical perspectives. Moreover, in recent years new technologies have been devel- oped which could be used in order to specifically study the expression and action of natriuretic peptides in the different components of the HPA axis. Laser-capture microdissection has recently been applied to obtain homoge- neous cell populations from nervous and endocrine structures, such as the hypothalamus (Segal et al., 2005) and pituitary gland (Lloyd et al., 2005). Microarray and proteomic analyses have also been performed on mRNA and proteins extracted from these cell populations. Laser-capture
microdissection in conjunction with microarray analysis may allow genome-wide screening of transcripts from homogeneous cell populations of hypothalamus and pituitary in order to better analyze the expression of natriuretic peptides and receptors and to specifically study the effects of these peptides on different cell types. Microarray and proteomics studies could also provide complete and accurate profiles of expression in response to various environmental stimuli.
ACKNOWLEDGMENT
We thank Alberta Coi for secretarial support and invaluable help in the provision of bibliographic items.
REFERENCES
Abdelalim, E.M., Takada, T., Torii, R., Tooyama, I., 2006. Molecular cloning of BNP from heart and its immunohistochemical localization in the hypothalamus of monkey. Peptides 27, 1886-1893.
Agui, T., Kurihara, M., Saavedra, J.M., 1989. Multiple types of receptors for atrial natriuretic peptide. Eur. J. Pharmacol. 162, 301-307.
Akamatsu, N., Inenaga, K., Yamashita, H., 1993. Inhibitory effects of natriuretic peptides on VP neurons mediated through cGMP and cGMP-dependent protein kinase in vitro. J. Neuroendocrinol. 5, 517-522.
Anand-Srivastava, M.B., 2005. Natriuretic peptide receptor-C signaling and regulation. Peptides 26, 1044-1059.
Anand-Srivastava, M.B., Trachte, G.J., 1993. Atrial natriuretic factor receptors and signal transduction mechanisms. Pharmacol. Rev. 45, 455-497.
Antoni, F.A., Hunter, E.F., Lowry, P.J., Noble, J.M., Seckl, J.R., 1992. Atriopeptin: an endogenous corticotropin-release inhibiting hormone. Endocrinology 130, 1753-1755.
Antunes-Rodrigues, J., McCann, S.M., Rogers, L.C., Samson, W.K., 1985. Atrial natri- uretic factor inhibits dehydration- and angiotensin II-induced water intake in the conscious, unrestrained rat. Proc. Natl. Acad. Sci. USA 82, 8720-8723.
Armando, I., Jezova, M., Bregonzio, C., Baiardi, G., Saavedra, J.M., 2004. Angiotensin II AT1 and AT2 receptor types regulate basal and stress-induced adrenomedullary cate- cholamine production through transcriptional regulation of tyrosine hydroxylase. Ann. N. Y. Acad. Sci. 1018, 302-309.
Atarashi, K., Mulrow, P.J., Franco-Saenz, R., Snajdar, R., Rapp, J., 1984. Inhibition of aldosterone production by an atrial extract. Science 224, 992-994.
Atlas, S.A., Maack, T., 1987. Effects of atrial natriuretic factor on the kidney and the renin- angiotensin-aldosterone system. Endocrinol. Metab. Clin. North Am. 16, 107-143.
Babinski, K., Féthière, J., Roy, M., De Léan, A., Ong, H., 1992. C-type natriuretic peptide in bovine chromaffin cells. The regulation of its biosynthesis and secretion. FEBS Lett. 313, 300-302.
Babinski, K., Haddad, P., Vallerand, D., McNicoll, N., de Léan, A., Ong, H., 1995. Natriuretic peptides inhibit nicotine-induced whole-cell currents and catecholamine secretion in bovine chromaffin cells: evidence for the involvement of the atrial natriuretic factor R2 receptors. J. Neurochem. 64, 1080-1087.
Belloni, A.S., Neri, G., Andreis, P.G., Musajo, F.G., Gottardo, G., Mazzocchi, G., et al., 1993. A comparative study of the effect of atrial natriuretic peptide (ANP) on the secretory activity of rat adrenal cortex and angiotensin-II-responsive adrenocortical autotransplants. Exp. Toxicol. Pathol. 45, 341-344.
Bierwolf, C., Burgemeister, A., Luthke, K., Born, J., Fehm, H.L., 1998. Influence of exogenous atrial natriuretic peptide on the pituitary-adrenal response to corticotropin- releasing hormone and vasopressin in healthy men. J. Clin. Endocrinol. Metab. 83, 1151-1157.
Biró, E., Gardi, J., Vecsernyés, M., Julesz, J., Tóth, G., Telegdy, G., 1996. The effects of atrial natriuretic peptide (ANP1-28) on corticotropin releasing factor in brain of rats. Life Sci. 59, 1351-1356.
Bodart, V., Rainey, W.E., Fournier, A., Ong, H., De Léan, A., 1996. The H295R human adrenocortical cell line contains functional atrial natriuretic peptide receptors that inhibit aldosterone biosynthesis. Mol. Cell Endocrinol. 118, 137-144.
Bodart, V., Babinski, K., Ong, H., De Léan, A., 1997. Comparative effect of pituitary adenylate cyclase-activating polypeptide on aldosterone secretion in normal bovine and human tumorous adrenal cells. Endocrinology 138, 566-573.
Bormann, J., Flugge, G., Fuchs, E., 1989. Effect of atrial natriuretic factor (ANF) on nicotinic acetylcholine receptor channels in bovine chromaffin cells. Pflügers Arch. 414, 11-14.
Boumezrag, A., Lyall, F., Dow, J.A., 1988. Characterization of specific binding of atrial natriuretic peptide (ANP) to rat PC12 phaeochromocytoma cells. Life Sci. 43, 2035-2042.
Bowman, M.E., Robinson, P.J., Smith, R., 1997. Atrial natriuretic peptide, cyclic GMP analogues and modulation of guanylyl cyclase do not alter stimulated POMC peptide release from perifused rat or sheep corticotrophs. J. Neuroendocrinol. 9, 929-936.
Brown, J., Czarnecki, A., 1990. Autoradiographic localization of atrial and brain natriuretic peptide receptors in rat brain. Am. J. Physiol. 258, R57-R63.
Calle, R.A., Bollag, W.B., White, S., Betancourt-Calle, S., Kent, P., 2001. ANPs effect on MARCKS and StAR phosphorylation in agonist-stimulated glomerulosa cells. Mol. Cell. Endocrinol. 177, 71-79.
Cantin, M., Genest, J., 1985. The heart and the atrial natriuretic factor. Endocr. Rev. 6, 107-127.
Carr, B.R., Mason, J.I., 1988. The effects of alpha-human atrial natriuretic polypeptide on steroidogenesis by fetal zone cells of the human fetal adrenal gland. Am. J. Obstet. Gynecol. 159, 1361-1365.
Castrén, E., Saavedra, J.M., 1989. Lack of vasopressin increases hypothalamic atrial natri- uretic peptide binding sites. Am. J. Physiol. 257, R168-R 173.
Chai, S.Y., Sexton, P.M., Allen, A.M., Figdor, R., Mendelsohn, F.A.O., 1986. In vivo autoradiographic localization of ANP receptors in rat kidney and adrenal gland. Am. J. Physiol. 250, F753-F757.
Chang, M.S., Lowe, D.G., Lewis, M., Hellmiss, R., Chen, E., Goeddel, D.V., 1989. Differential activation by atrial and brain natriuretic peptides of two different receptor guanylate cyclases. Nature 341, 68-72.
Charles, C.J., Richards, A.M., Espiner, E.A., 1992. Central C-type natriuretic peptide but not atrial natriuretic factor lowers blood pressure and adrenocortical secretion in normal conscious sheep. Endocrinology 131, 1721-1726.
Charles, C.J., Espiner, E.A., Richards, A.M., Donald, R.A., 1995. Central C-type natri- uretic peptide augments the hormone response to hemorrhage in conscious sheep. Peptides 16, 129-132.
Chartier, L., Schiffrin, E., Thibault, G., Garcia, R., 1984. Atrial natriuretic factor inhibits the stimulation of aldosterone secretion by angiotensin II, ACTH and potassium in vitro and angiotensin II-induced steroidogenesis in vivo. Endocrinology 115, 2026-2028.
Chatelain, D., Lesage, J., Montel, V., Chatelain, A., Deloof, S., 2003. Effect of natriuretic peptides on in vitro stimulated adrenocorticotropic hormone release and pro-opiomela- nocortin mRNA expression by the fetal rat pituitary gland in late gestation. Horm. Res. 59, 142-148.
Chen, Y.F., Elton, T.S., Oparil, S., 1992. Quantitation of hypothalamic atrial natriuretic peptide messenger RNA in hypertensive rats. Hypertension 19, 296-300.
Chen, Y.M., Wu, K.D., Hung, K.Y., Pu, Y.S., Hsieh, B.S., 1995. Quantitative analysis of messenger ribonucleic acid encoding natriuretic peptide receptors in aldosterone-producing adenoma. Mol. Cell. Endocrinol. 111, 139-146.
Cherradi, N., Brandenburger, Y., Rossier, M.F., Vallotton, M.B., Stocco, D.M., Capponi, A.M., 1998. Atrial natriuretic peptide inhibits calcium-induced steroidogenic acute regulatory protein gene transcription in adrenal glomerulosa cells. Mol. Endocri- nol. 12, 962-972.
Chriguer, R.S., Rocha, M.J., Antunes-Rodrigues, J., Franci, C.R., 2001. Hypothalamic atrial natriuretic peptide and secretion of oxytocin. Brain Res. 889, 239-242.
Cozza, E.N., Foecking, M.F., Vila, M.C., Gomez-Sanchez, C.E., 1993. Adrenal receptors for natriuretic peptides and inhibition of aldosterone secretion in calf zona glomerulosa cells in culture. Acta Endocrinol. 129, 59-64.
Dagnino, L., Drouin, J., Nemer, M., 1991. Differential expression of natriuretic peptide genes in cardiac and extracardiac tissues. Mol. Endocrinol. 5, 1292-1300.
Dayanithi, G., Antoni, F.A., 1990. Atriopeptins are potent inhibitors of ACTH secretion by rat anterior pituitary cells in vitro: involvement of the atrial natriuretic factor receptor domain of membrane-bound guanylyl cyclase. J. Endocrinol. 125, 39-44.
De Léan, A., Gutkowska, J., McNicoll, N., Schiller, P.W., Cantin, M., Genest, J., 1984. Characterization of specific receptors for atrial natriuretic factor in bovine adrenal zona glomerulosa. Life Sci. 35, 2311-2318.
De Léan, A., Ong, H., McNicoll, N., Racz, K., Gutkowska, J., Cantin, M., 1985. Identifi- cation of aldosterone secretion inhibitory factor in bovine adrenal medulla. Life Sci. 36, 2375-2382.
Deloof, S., Chatelain, A., Dupouy, J.P., 1994. Characteristics and developmental changes of ANP-binding sites in rat adrenal glands during the perinatal period. Regul. Pept. 51, 199-206.
Deloof, S., De Seze, C., Montel, V., Chatelain, A., 1999. Effects of water deprivation on atrial natriuretic peptide secretion and density of binding sites in adrenal glands and kidneys of maternal and fetal rats in late gestation. Eur. J. Endocrinol. 141, 160-168.
Deloof, S., De Seze, C., Montel, V., Chatelain, A., 2000. Atrial natriuretic peptide and aldosterone secretions, and atrial natriuretic peptide-binding sites in kidneys and adrenal glands of pregnant and fetal rats in late gestation in response to a high-salt diet. Eur. J. Endocrinol. 142, 524-532.
Deloff, S., Leprêtre, A., Montel, V., Châtelain, A., 1992. Effect of rat atrial natriuretic factor on in vivo and in vitro aldosterone and corticosterone secretions in the rat during the perinatal period. Biol. Neonate 62, 145-154.
Denker, P.S., Vesely, D.L., Gómez-Sánchez, C.E., 1990. Effect of pro-atrial natriuretic peptides 1-30, 31-67 and 99-126 on angiotensin II-stimulated aldosterone production in calf adrenal cells. J. Steroid Biochem. Mol. Biol. 37, 617-619.
Duntas, L., Bornstein, S.R., Scherbaum, W.A., Holst, J.J., 1993. Atrial natriuretic peptide- like immunoreactive material (ANP-LI) is released from the adrenal gland by splanchnic nerve stimulation. Exp. Clin. Endocrinol. 101, 371-373.
Edwards, A.V., Ghatei, M.A., Bloom, S.R., 1990. The effect of splanchnic nerve stimulation on the uptake of atrial natriuretic peptide by the adrenal gland in conscious calves. J. Endocrinol. Invest. 13, 887-892.
Elliott, M.E., 1990. Phosphorylation of adrenal histone H3 is affected by angiotensin, ACTH, dibutyryl cAMP, and atrial natriuretic peptide. Life Sci. 46, 1479-1488.
Elliott, M.E., Goodfriend, T.L., Jefcoate, C.R., 1993. Bovine adrenal glomerulosa and fasciculata cells exhibit 28.5-kilodalton proteins sensitive to angiotensin, other agonists, and atrial natriuretic peptide. Endocrinology 133, 1669-1677.
Emori, T., Hirata, Y., Imai, T., Eguchi, S., Kanno, K., Marumo, F., 1993. Cellular mechanism of natriuretic peptides-induced inhibition of endothelin-1 biosynthesis in rat endothelial cells. Endocrinology 133, 2474-2480.
Engler, D., Pham, T., Liu, J.P., Fullerton, M.J., Clarke, I.J., Funder, J.W., 1990. Studies of the regulation of the hypothalamic-pituitary-adrenal axis in sheep with hypothalamic- pituitary disconnection. II. Evidence for in vivo ultradian hypersecretion of proopiome- lanocortin peptides by the isolated anterior and intermediate pituitary. Endocrinology 127, 1956-1966.
Fernandez, B.E., Vatta, M.S., Bianciotti, L.G., 1993. Comparative effects of bradykinin and atrial natriuretic factor on neuronal and non-neuronal noradrenaline uptake in the central nervous system of the rat. Arch. Int. Physiol. Biochim. Biophys. 101, 337-340.
Fernández, B.E., Leder, M., Fernández, G., Bianciotti, L.G., Vatta, M.S., 1997. Atrial natriuretic factor modifies the biosynthesis and turnover of norepinephrine in the rat adrenal medulla. Biochem. Biophys. Res. Commun. 238, 343-346.
Féthière, J., Graihle, R., Larose, L., Babinski, K., Ong, H., De Léan, A., 1993. Distribution and regulation of natriuretic factor-R 1C receptor subtypes in mammalian cell lines. Mol. Cell. Biochem. 124, 11-16.
Fink, G., Dow, R.C., Casley, D., Johnston, C.I., Lim, A.T., Copolov, D.L., et al., 1991. Atrial natriuretic peptide is a physiological inhibitor of ACTH release: evidence from immunoneutralization in vivo. J. Endocrinol. 131, R9-R12.
Fowkes, R.C., McArdle, C.A., 2000. C-type natriuretic peptide: an important neuroendo- crine regulator? Trends Endocrinol. Metab. 11, 333-338.
Fowkes, R.C., Forrest-Owen, W., Williams, B., McArdle, C.A., 1999. C-type natriuretic peptide (CNP) effects on intracellular calcium [Ca2+]i in mouse gonadotrope-derived alphaT3-1 cell line. Regul. Pept. 84, 43-49.
Franci, C.R., Anselmo-Franci, J.A., McCann, S.M., 1990. Opposite effects of central immunoneutralization of angiotensin II or atrial natriuretic peptide on luteinizing hor- mone release in ovariectomized rats. Neuroendocrinology 51, 683-687.
Franci, C.R., Anselmo-Franci, J.A., McCann, S.M., 1992. The role of endogenous atrial natriuretic peptide in resting and stress-induced release of corticotropin, prolactin, growth hormone, and thyroid-stimulating hormone. Proc. Natl. Acad. Sci. USA 89, 11391-11395.
Fuchs, E., Shigematsu, K., Saavedra, J.M., 1986. Binding sites of atrial natriuretic peptide in tree shrew adrenal gland. Peptides 7, 873-876.
Ganguly, A., 1992. Atrial natriuretic peptide-induced inhibition of aldosterone secretion: a quest for mediator(s). Am. J. Physiol. 263, E181-E194.
Ganz, M.B., Nee, J.J., Isales, C.M., Barrett, P.Q., 1994. Atrial natriuretic peptide enhances activity of potassium conductance in adrenal glomerulosa cells. Am. J. Physiol. 266, C1357-C1365.
Gardi, J., Bíró, E., Vecsernyés, M., Julesz, J., Nyári, T., Tóth, G., et al., 1997. The effects of brain and C-type natriuretic peptides on corticotropin-releasing factor in brain of rats. Life Sci. 60, 2111-2117.
Gardner, D.G., Vlasuk, G.P., Baxter, J.D., Fiddes, J.C., Lewicki, J.A., 1987. Identification of atrial natriuretic factor gene transcripts in the central nervous system of the rat. Proc. Natl. Acad. Sci. USA 84, 2175-2179.
Gerbes, A.L., Dagnino, L., Nguyen, T., Nemer, M., 1994. Transcription of brain natriuretic peptide and atrial natriuretic peptide genes in human tissues. J. Clin. Endocrinol. Metab. 78, 1307-1311.
Gerstberger, R., Schütz, H., Luther-Dyroff, D., Keil, R., Simon, E., 1992. Inhibition of vasopressin and aldosterone release by atrial natriuretic peptide in conscious rabbits. Exp. Physiol. 77, 587-600.
Gibson, T.R., Wildey, G.M., Manaker, S., Glembotski, C.C., 1986. Autoradiographic localization and characterization of atrial natriuretic peptide binding sites in the rat central nervous system and adrenal gland. J. Neurosci. 6, 2004-2011.
Gilkes, A.F., MacKay, K.B., Cramb, G., Guild, S.B., 1992. Atrial natriuretic peptide effects in AtT-20 pituitary tumour cells. Mol. Cell. Endocrinol. 89, 39-45.
Gilkes, A.F., Ogden, P.H., Guild, S.B., Cramb, G., 1994. Characterization of natriuretic peptide receptor subtypes in the AtT-20 pituitary tumour cell line. Biochem. J. 299, 481-487.
Giridhar, J., Peoples, R.W., Isom, G.E., 1992. Modulation of hypothalamic norepinephrine release by atrial natriuretic peptide: involvement of cyclic GMP. Eur. J. Pharmacol. 213, 317-321.
Glembotski, C.C., Wildey, G.M., Gibson, T.R., 1985. Molecular forms of immunoactive atrial natriuretic peptide in the rat hypothalamus and atrium. Biochem. Biophys. Res. Commun. 129, 671-678.
Grandclément, B., Brisson, C., Bayard, F., Tremblay, J., Gossard, F., Morel, G., 1995. Localization of mRNA coding for the three subtypes of atrial natriuretic factor (ANF) receptors in rat anterior pituitary gland cells. J. Neuroendocrinol. 7, 939-948.
Grandclément, B., Ronsin, B., Morel, G., 1997. The three subtypes of atrial natriuretic peptide (ANP) receptors are expressed in the rat adrenal gland. Biol. Cell. 89, 29-41.
Grossman, A., Costa, A., Navarra, P., Tsagarakis, S., 1993. The regulation of hypothalamic corticotropin-releasing factor release: in vitro studies. Ciba Found. Symp. 172, 129-150. Guild, S.B., Cramb, G., 1999. Characterisation of the effects of natriuretic peptides upon ACTH secretion from the mouse pituitary. Mol. Cell. Endocrinol. 152, 11-19.
Gundlach, A.L., Knobe, K.E., 1992. Distribution of preproatrial natriuretic peptide mRNA in rat brain detected by in situ hybridization of DNA oligonucleotides: enrichment in hypothalamic and limbic regions. J. Neurochem. 59, 758-761.
Gutkowska, J., Racz, K., Debinski, W., Thibault, G., Garcia, R., Kuchel, O., Cantin, M., Genest, J., 1987. An atrial natriuretic factor-like activity in rat posterior hypophysis. Peptides 8, 461-465.
Gutkowska, J., Cantin, M., 1988. Bioactive atrial natriuretic factor-like peptides in rat anterior pituitary. Can. J. Physiol. Pharmacol. 66, 270-275.
Gutkowska, J., Antunes-Rodrigues, J., McCann, S.M., 1997. Atrial natriuretic peptide in brain and pituitary gland. Physiol. Rev. 77, 465-515.
Hartmann, M., Skryabin, B.V., Müller, T., Gazinski, A., Schröter, J., Gassner, B., et al., 2008. Alternative splicing of the guanylyl cyclase-A receptor modulates atrial natriuretic peptide signaling. J. Biol. Chem. 283, 28313-28320.
Hartt, D.J., Ogiwara, T., Ho, A.K., Chik, C.L., 1995. Cyclic GMP stimulates growth hormone release in rat anterior pituitary cells. Biochem. Biophys. Res. Commun. 214, 918-926.
Hashiguchi, T., Higuchi, K., Ohashi, M., Takayanagi, R., Matsuo, H., Nawata, H., 1989. Effect of porcine brain natriuretic peptide (pBNP) on human adrenocortical steroido- genesis. Clin. Endocrinol. 31, 623-630.
Hashimoto, K., Hattori, T., Suemaru, S., Sugawara, M., Takao, T., Kageyama, J., et al., 1987. Atrial natriuretic peptide does not affect corticotropin-releasing factor-, arginine vasopressin- and angiotensin II-induced adrenocorticotropic hormone release in vivo or in vitro. Regul. Pept. 17, 53-60.
Heisler, S., Tallerico-Melnyk, T., Yip, C., Schimmer, B.P., 1989. Y-1 adrenocortical tumor cells contain atrial natriuretic peptide receptors which regulate cyclic nucleotide metab- olism and steroidogenesis. Endocrinology 125, 2235-2243.
Herman, J.P., Langub Jr., M.C., Watson Jr., R.E., 1993. Localization of C-type natriuretic peptide mRNA in rat hypothalamus. Endocrinology 133, 1903-1906.
Herman, J.P., Dolgas, C.M., Rucker, D., Langub Jr., M.C., 1996a. Localization of natri- uretic peptide-activated guanylate cyclase mRNAs in the rat brain. J. Comp. Neurol. 369, 165-187.
Herman, J.P., Dolgas, C.M., Marcinek, R., Langub Jr., M.C., 1996b. Expression and glucocorticoid regulation of natriuretic peptide clearance receptor (NPR-C) mRNA in rat brain and choroid plexus. J. Chem. Neuroanat. 11, 257-265.
Higuchi, K., Hashiguchi, T., Ohashi, M., Takayanagi, R., Haji, M., Matsuo, H., et al., 1989. Porcine brain natriuretic peptide receptor in bovine adrenal cortex. Life Sci. 44, 881-886.
Hirata, Y., Tomita, M., Yoshimi, H., Kuramochi, M., Ito, K., Ikeda, M., 1985. Effect of synthetic human atrial natriuretic peptide on aldosterone secretion by dispersed aldoste- rone-producing adenoma cells in vitro. J. Clin. Endocrinol. Metab. 61, 677-680.
Horvath, J., Ertl, T., Schally, A.V., 1986. Effect of atrial natriuretic peptide on gonadotropin release in superfused rat pituitary cells. Proc. Natl. Acad. Sci. USA 83, 3444-3446.
Huang, F.L.S., Skala, K.D., Samson, W.K., 1992a. C-type natriuretic peptide stimulates prolactin secretion by a hypothalamic site of action. J. Neuroendocrinol. 4, 593-597. Huang, F.L.S., Skala, K.D., Samson, W.K., 1992b. Hypothalamic effects of C-type natri- uretic peptide on luteinizing hormone secretion. J. Neuroendocrinol. 4, 325-330.
Ibanez-Santos, J., Tsagarakis, S., Rees, L.H., Besser, G.M., Grossman, A., 1990. Atrial natriuretic peptides inhibit the release of corticotrophin-releasing factor-41 from the rat hypothalamus in vitro. J. Endocrinol. 126, 223-228.
Iitake, K., Share, L., Crofton, J.T., Brooks, D.P., Ouchi, Y., Blaine, E.H., 1986. Central atrial natriuretic factor reduces vasopressin secretion in the rat. Endocrinology 119, 438-440.
Ikeda, Y., Tanaka, I., Oki, Y., Ikeda, Y., Yoshimi, T., 1989. Effect of atrial natriuretic peptide on the release of beta-endorphin from rat hypothalamusohypophysial com- plex. Endocrinol. Jpn. 36, 647-653.
Isales, C.M., Bollag, W.B., Kiernan, L.C., Barrett, P.Q., 1989. Effect of ANP on sustained aldosterone secretion stimulated by angiotensin II. Am. J. Physiol. 256, C89-C95.
Isales, C.M., Lewicki, J.A., Nee, J.J., Barrett, P.Q., 1992. ANP-(7-23) stimulates a DHP- sensitive Ca2+ conductance and reduces cellular cAMP via a cGMP-independent mechanism. Am. J. Physiol. 263, C334-C342.
Itoh, H., Nakao, K., Saito, Y., Yamada, T., Shirakami, G., Mukoyama, M., et al., 1989. Radioimmunoassay for brain natriuretic peptide (BNP) detection of BNP in canine brain. Biochem. Biophys. Res. Commun. 158, 120-128.
Jaiswal, N., Paul, A.K., Jaiswal, R.K., Sharma, R.K., 1986. Atrial natriuretic factor regula- tion of cyclic GMP levels and steroidogenesis in isolated fasciculata cells of rat adrenal cortex. FEBS Lett. 199, 121-124.
Jakubik, P., Janota, T., Widimsky Jr., J., Zelinka, T., Strauch, B., Petrak, O., et al., 2006. Impact of essential hypertension and primary aldosteronism on plasma brain natriuretic peptide concentration. Blood Press. 15, 302-307.
Jankowski, M., Marcinkiewicz, M., Bouanga, J.C., Gutkowska, J., 2004. Changes of atrial natriuretic peptide in rat supraoptic neurones during pregnancy. J. Neuroendocrinol. 16, 441-449.
Januszewicz, P., Thibault, G., Garcia, R., Gutkowska, J., Genest, J., Cantin, M., 1986. Effect of synthetic atrial natriuretic factor on arginine vasopressin release by the rat hypothalamusohypophysial complex in organ culture. Biochem. Biophys. Res. Commun. 134, 652-658.
Jászberényi, M., Bujdosó, E., Telegdy, G., 1998. Effects of C-type natriuretic peptide on pituitary-adrenal activation in rats. Neuroreport 9, 2601-2603.
Jászberényi, M., Bujdosó, E., Telegdy, G., 2000. Effects of brain natriuretic peptide on pituitary-adrenal activation in rats. Life Sci. 66, 1655-1661.
Jirikowski, G.F., Back, H., Forssmann, W.G., Stumpf, W.E., 1986. Coexistence of atrial natriuretic factor (ANF) and oxytocin in neurons of the rat hypothalamus. Neuropeptides 8, 243-249.
Kadowaki, K., Hirota, K., Koike, K., Ohmichi, M., Miyake, A., Tanizawa, O., 1992. Atrial and brain natriuretic peptides enhance dopamine accumulation in cultured rat hypotha- lamic cells including dopaminergic neurons. Neuroendocrinology 56, 11-17.
Kaneko, T., Shirakami, G., Nakao, K., Nagata, I., Nakagawa, O., Hama, N., et al., 1993. C-type natriuretic peptide (CNP) is the major natriuretic peptide in human cerebro- spinal fluid. Brain Res. 612, 104-109.
Kangawa, K., Matsuo, H., 1984. Purification and complete amino acid sequence of alpha- human atrial natriuretic polypeptide (alpha-hANP). Biochem. Biophys. Res. Commun. 118, 131-139.
Kato, J., Etoh, T., Kitamura, K., Eto, T., 2005. Atrial and brain natriuretic peptides as markers of cardiac load and volume retention in primary aldosteronism. Am. J. Hyper- tens. 18, 354-357.
Kawai, M., Naruse, M., Yoshimoto, T., Naruse, K., Shionoya, K., Tanaka, M., et al., 1996. C-type natriuretic peptide as a possible local modulator of aldosterone secretion in bovine adrenal zona glomerulosa. Endocrinology 137, 42-46.
Kawata, M., Ueda, S., Nakao, K., Morii, N., Kiso, Y., Imura, H., et al., 1985. Immuohis- tochemical demonstration of alpha-atrial natriretic plypeptide-containing neurons in the rat brain. Histochemistry 83, 1-3.
Kellner, M., Wiedemann, K., Holsboer, F., 1992. Atrial natriuretic factor inhibits the CRH- stimulated secretion of ACTH and cortisol in man. Life Sci. 50, 1835-1842.
King, M.S., Baertschi, A.J., 1989. Physiological concentrations of atrial natriuretic factors with intact N-terminal sequences inhibit corticotropin-releasing factor-stimulated adrenocortico- tropin secretion from cultured anterior pituitary cells. Endocrinology 124, 286-292.
Kobayashi, H., Niina, H., Yamamoto, R., Wada, A., 1998. Receptors for natriuretic peptides in adrenal chromaffin cells. Biochem. Pharmacol. 55, 1-7.
Komatsu, Y., Nakao, K., Suga, S., Ogawa, Y., Mukoyama, M., Arai, H., et al., 1991. C-type natriuretic peptide (CNP) in rats and humans. Endocrinology 129, 1104-1106.
Komatsu, K., Tanaka, I., Funai, T., Ichiyama, A., Yoshimi, T., 1992. Increased level of atrial natriuretic peptide messenger RNA in the hypothalamus and brainstem of spontaneously hypertensive rats. J. Hypertens. 10, 17-23.
Konrad, E.M., Thibault, G., Schiffrin, E.L., 1992. Autoradiographic visualization of the natriuretic peptide receptor-B in rat tissues. Regul. Pept. 39, 177-189.
Kovács, K.J., Antoni, F.A., 1990. Atriopeptin inhibits stimulated secretion of adrenocorti- cotropin in rats: evidence for a pituitary site of action. Endocrinology 127, 3003-3008. Kudo, T., Baird, A., 1984-1985. Inhibition of aldosterone production in the adrenal glomerulosa by atrial natriuretic factor. Nature 312, 756-757.
Kuhn, M., 2003. Structure, regulation, and function of mammalian membrane guanylyl cyclase receptors, with a focus on guanylyl cyclase-A. Circ. Res. 93, 700-709.
Kurihara, M., Saavedra, J.M., Shigematsu, K., 1987. Localization and characterization of atrial natriuretic peptide binding sites in discrete areas of rat brain and pituitary gland by quantitative autoradiography. Brain Res. 408, 31-39.
Lai, F.J., Shin, S.J., Lee, Y.J., Lin, S.R., Jou, W.Y., Tsai, J.H., 2000. Up-regulation of adrenal cortical and medullary atrial natriuretic peptide and gene expression in rats with deoxycorticosterone acetate-salt treatment. Endocrinology 141, 325-332.
Lange, D.L., Haywood, J.R., Hinojosa-Laborde, C., 2000. Endothelin enhances and inhi- bits adrenal catecholamine release in deoxycorticosterone acetate-salt hypertensive rats. Hypertension 35, 385-390.
Langub Jr., M.C., Dolgas, C.M., Watson Jr., R.E., Herman, J.P., 1995. The C-type natriuretic peptide receptor is the predominant natriuretic peptide receptor mRNA expressed in rat hypothalamus. J. Neuroendocrinol. 7, 305-309.
Lapinski, M., Stepniakowski, K., Januszewicz, A., Wocial, B., Chodakowska, J., Feltynowski, T., et al., 1991. Plasma atrial natriuretic peptide concentration in patients with primary aldosteronism. J. Hypertens. Suppl. 9, S260-S261.
Lee, J., Malvin, R.L., Claybaugh, J.R., Huang, B.S., 1987. Atrial natriuretic factor inhibits vasopressin secretion in conscious sheep. Proc. Soc. Exp. Biol. Med. 185, 272-276.
Lee, Y.J., Lin, S.R., Shin, S.J., Tsai, J.H., 1993. Increased adrenal medullary atrial natriuretic polypeptide synthesis in patients with primary aldosteronism. J. Clin. Endocrinol. Metab. 76, 1357-1362.
Lee, Y.J., Lin, S.R., Shin, S.J., Lai, Y.H., Lin, Y.T., Tsai, J.H., 1994. Brain natriuretic peptide is synthesized in the human adrenal medulla and its messenger ribonucleic acid expression along with that of atrial natriuretic peptide are enhanced in patients with primary aldosteronism. J. Clin. Endocrinol. Metab. 79, 1476-1482.
Levin, E.R., Gardner, D.G., Samson, W.K., 1998. Natriuretic peptides. N. Engl. J. Med. 339, 321-328.
Lewandowska, A., Szyburska, I., Guzek, J.W., 1992. Atrial natriuretic peptide inhibits neurohypophysial hormones’ release in the rat (in vitro and in vivo studies). J. Physiol. Pharmacol. 43, 79-88.
Liang, F., Kapoun, A.M., Lam, A., Damm, D.L., Quan, D., O’Connell, M., et al., 2007. B-Type natriuretic peptide inhibited angiotensin II-stimulated cholesterol biosynthesis, cholesterol transfer, and steroidogenesis in primary human adrenocortical cells. Endocri- nology 148, 3722-3729.
Lightly, E.R., Walker, S.W., Bird, I.M., Williams, B.C., 1990. Subclassification of beta- adrenoceptors responsible for steroidogenesis in primary cultures of bovine adrenocortical zona fasciculata/reticularis cells. Br. J. Pharmacol. 99, 709-712.
Lim, A.T., Dow, R.C., Yang, Z., Fink, G., 1994. ANP(5-28) is the major molecular species in hypophysial portal blood of the rat. Peptides 15, 1557-1559.
Lipari, F.E., Lipari, D., Dieli, F., Valentino, B., 2005. Atrial natriuretic peptide secretion during development of the rat supraoptic nucleus. Eur. J. Histochem. 49, 379-384.
Lipari, E.F., Lipari, A., Dieli, F., Valentino, B., 2007. ANP presence in the hypothalamic suprachiasmatic nucleus of developing rat. Ital. J. Anat. Embryol. 112, 19-25.
Lloyd, R.V., Qian, X., Jin, L., Ruebel, K., Bayliss, J., Zhang, S., et al., 2005. Analysis of pituitary cells by laser capture microdissection. Methods Mol. Biol. 293, 233-241.
Lotshaw, D.P., Franco-Saenz, R., Mulrow, P.J., 1991. Atrial natriuretic peptide inhibition of calcium ionophore A23187-stimulated aldosterone secretion in rat adrenal glomer- ulosa cells. Endocrinology 129, 2305-2310.
Luckman, S.M., Bicknell, R.J., 1991. Binding sites for atrial natriuretic peptide (ANP) on cultured pituicytes: lack of effect of ANP on release of neurohypophysial hormones in vitro. Neurosci. Lett. 123, 156-159.
Lynch, D.R., Braas, K.M., Snyder, S.H., 1986. Atrial natriuretic factor receptors in rat kidney, adrenal gland, and brain: autoradiographic localization and fluid balance depen- dent changes. Proc. Natl. Acad. Sci. USA 83, 3557-3561.
Maack, T., 1992. Receptors of atrial natriuretic factor. Annu. Rev. Physiol. 54, 11-27.
MacFarland, R.T., Zelus, B.D., Beavo, J.A., 1991. High concentrations of a cGMP- stimulated phosphodiesterase mediate ANP-induced decreases in cAMP and steroido- genesis in adrenal glomerulosa cells. J. Biol. Chem. 266, 136-142.
Makino, S., Hashimoto, K., Hirasawa, R., Hattori, T., Kageyama, J., Ota, Z., 1990. Central interaction between endothelin and brain natriuretic peptide on pressor and hormonal responses. Brain Res. 534, 117-121.
Makino, S., Hashimoto, K., Hirasawa, R., Hattori, T., Ota, Z., 1992. Central interaction between endothelin and brain natriuretic peptide on vasopressin secretion. J. Hypertens. 10, 25-28.
Malendowicz, L.K., Andreis, P.G., Markowska, A., Nowak, M., Warchol, J.B., Neri, G., et al., 1994. Effects of neuromedin U-8 on the secretory activity of the rat adrenal cortex: evidence for an indirect action requiring the presence of the zona medullaris. Res. Exp. Med. 194, 69-79.
Malendowicz, L.K., Brelinska, R., De Caro, R., Trejer, M., Nussdorfer, G.G., 1998. Endothelin-1, acting via the A receptor subtype, stimulates thymocyte proliferation in the rat. Life Sci. 62, 1959-1963.
Malendowicz, L.K., Guidolin, D., Trejter, M., Rucinski, M., Porzionato, A., De Caro, R., et al., 2009. Neuromedin-U inhibits unilateral adrenalectomy-induced compensatory adrenal growth in the rat. Peptides 30, 935-939.
Mantero, F., Rocco, S., Pertile, F., Carpenè, G., Fallo, F., Leone, L., et al., 1987. Effect of alpha-human atrial natriuretic peptide in low renin essential hypertension and primary aldosteronism. Clin. Exp. Hypertens. A 9, 1505-1513.
Mantyh, C.R., Kruger, L., Brecha, N.C., Mantyh, P.W., 1986. Localization of specific binding sites for atrial natriuretic factor in peripheral tissues of the guinea pig, rat, and human. Hypertension 8, 712-721.
Mantyh, C.R., Kruger, L., Brecha, N.C., Mantyh, P.W., 1987. Localization of specific binding sites for atrial natriuretic factor in the central nervous system of rat, guinea pig, cat and human. Brain Res. 412, 329-342.
Manzanares, J., Lookingland, K.J., Moore, K.E., 1990. Atrial natriuretic peptide-induced suppression of basal and dehydration-induced vasopressin secretion is not mediated by hypothalamic tuberohypophysial or tuberoinfundibular dopaminergic neurons. Brain Res. 527, 103-108.
Maurer, R., Reubi, J.C., 1986. Distribution and coregulation of three peptide receptors in adrenals. Eur. J. Pharmacol. 125, 241-247.
Mazzocchi, G., Rebuffat, P., Nussdorfer, G.G., 1987. Atrial natriuretic factor (ANF) inhibits the growth and the secretory activity of rat adrenal zona glomerulosa in vivo. J. Steroid Biochem. 28, 643-646.
Mazzocchi, G., Gottardo, G., Nussdorfer, G.G., 1998. Paracrine control of steroid hormone secretion by chromaffin cells in the adrenal gland of lower vertebrates. Histol. Histo- pathol. 13, 209-220.
McArdle, C.A., Poch, A., Käppler, K., 1993. Cyclic guanosine monophosphate production in the pituitary: stimulation by C-type natriuretic peptide and inhibition by gonadotro- pin-releasing hormone in alpha T3-1 cells. Endocrinology 132, 2065-2072.
McArdle, C.A., Olcese, J., Schmidt, C., Poch, A., Kratzmeier, M., Middendorff, R., 1994. C-type natriuretic peptide (CNP) in the pituitary: is CNP an autocrine regulator of gonadotropes? Endocrinology 135, 2794-2801.
McCann, S.M., Franci, C., Gutkowska, J., Favaretto, A.L., Antunes-Rodrigues, J., 1996. Neural control of atrial natriuretic peptide actions on fluid intake and excretion. Proc. Soc. Exp. Biol. Med. 213, 117-127.
McCarthy, R.T., Isales, C.M., Bollag, W.B., Rasmussen, H., Barrett, P.Q., 1990. Atrial natriuretic peptide differentially modulates T- and L-type calcium channels. Am. J. Physiol. 258, F473-F478.
Mckenzie, J.C., Tanaka, I., Misono, K.S., Inagami, T., 1985. Immunocytochemical locali- zation of atrial natriuretic factor in the kidney, adrenal medulla, pituitary, and atrium of rat. J. Histochem. Cytochem. 33, 828-832.
Melo, L.G., Veress, A.T., Ackermann, U., Pang, S.C., Flynn, T.G., Sonnenberg, H., 1999. Chronic hypertension in ANP knockout mice: contribution of peripheral resistance. Regul. Pept. 79, 109-115.
Mendelsohn, F.A., Allen, A.M., Chai, S.Y., Sexton, P.M., Figdor, R., 1987. Overlapping distributions of receptors for atrial natriuretic peptide and angiotensin II visualized by in vitro autoradiography: morphological basis of physiological antagonism. Can. J. Physiol. Pharmacol. 65, 1517-1521.
Middendorff, R., Paust, H.J., Davidoff, M.S., Olcese, J., 1997. Synthesis of C-type natri- uretic peptide (CNP) by immortalized LHRH cells. J. Neuroendocrinol. 9, 177-182.
Minamino, N., Aburaya, M., Kojima, M., Miyamoto, K., Kangawa, K., Matsuo, H., 1993. Distribution of C-type natriuretic peptide and its messenger RNA in rat central nervous system and peripheral tissue. Biochem. Biophys. Res. Commun. 197, 326-335.
Moga, M.M., Saper, C.B., 1994. Neuropeptide-immunoreactive neurons projecting to the paraventricular hypothalamic nucleus in the rat. J. Comp. Neurol. 346, 137-150.
Morel, G., Chabot, J.G., Garcia-Caballero, T., Gossard, F., Dihl, F., Belles-Isles, M., et al., 1988. Synthesis, internalization, and localization of atrial natriuretic peptide in rat adrenal medulla. Endocrinology 123, 149-158.
Morel, G., Chabot, J.G., Gossard, F., Heisler, S., 1989a. Is atrial natriuretic peptide synthe- sized and internalized by gonadotrophs? Endocrinology 124, 1703-1710.
Morel, G., Mesguich, P., Chabot, J.G., Belles-Isles, M., Jeandel, L., Heisler, S., 1989b. Internalization of atrial natriuretic peptide by adrenal glomerulosa cells. Biol. Cell. 65, 181-188.
Mulay, S., Vaillancourt, P., Omer, S., Varma, D.R., 1995. Hormonal modulation of atrial natriuretic factor receptors in adrenal fasciculata cells from female rats. Can. J. Physiol. Pharmacol. 73, 140-144.
Mulligan, R.S., Livesey, J.H., Evans, M.J., Ellis, M.J., Donald, R.A., 1997. Atrial natriuretic peptide and C-type natriuretic peptide do not acutely inhibit the release of adrenocorti- cotropin from equine pituitary cells in vitro. Neuroendocrinology 65, 64-69.
Murakami, Y., Kato, Y., Tojo, K., Inoue, T., Yanaihara, N., Imura, H., 1988. Stimulation of growth hormone secretion by central administration of atrial natriuretic polypeptide in the rat. Endocrinology 122, 2103-2108.
Nagase, M., Katafuchi, T., Hirose, S., Fujita, T., 1997. Tissue distribution and localization of natriuretic peptide receptor subtypes in stroke-prone spontaneously hypertensive rats. J. Hypertens. 15, 1235-1243.
Nakamaru, M., Ogihara, T., Saito, H., Rakugi, H., Hashizume, K., Yamatodani, A., et al., 1989. Effect of atrial natriuretic peptide on catecholamine release from human pheo- chromocytoma. Acta Endocrinol. 120, 107-112.
Naruse, M., Obana, K., Naruse, K., Yamaguchi, H., Demura, H., Inagami, T., et al., 1987. Atrial natriuretic polypeptide inhibits cortisol secretion as well as aldosterone secretion in vitro from human adrenal tissue. J. Clin. Endocrinol. Metab. 64, 10-16.
Naruse, M., Takeyama, Y., Tanabe, A., Hiroshige, J., Naruse, K., Yoshimoto, T., et al., 1994. Atrial and brain natriuretic peptides in cardiovascular diseases. Hypertension 23, I231-1234.
Nawata, H., Ohashi, M., Haji, M., Takayanagi, R., Higuchi, K., Fujio, N., et al., 1991. Atrial and brain natriuretic peptide in adrenal steroidogenesis. J. Steroid Biochem. Mol. Biol. 40, 367-379.
Neuser, D., Stasch, J.P., Knorr, A., Kazda, S., 1993. Inhibition by atrial natriuretic peptide of endothelin-1-stimulated proliferation of vascular smooth-muscle cells. J. Cardiovasc. Pharmacol. 22 (Suppl 8), S257-S261.
Nguyen, T.T., Babinski, K., Ong, H., De Lean, A., 1990. Differential regulation of natriuretic peptide biosynthesis in bovine adrenal chromaffin cells. Peptides 11, 973-978.
Niina, H., Kobayashi, H., Yamamoto, R., Yuhi, T., Yanagita, T., Wada, A., 1996. Receptors for atrial natriuretic peptide in adrenal chromaffin cells. Biochem. Pharmacol. 51, 855-858.
Nikolaev, V.O., Gambaryan, S., Engelhardt, S., Walter, U., Lohse, M.J., 2005. Real-time monitoring of the PDE2 activity of live cells: hormone-stimulated cAMP hydrolysis is faster than hormone-stimulated cAMP synthesis. J. Biol. Chem. 280, 1716-1719.
Nilaver, G., Rosenbaum, L.C., Fukui, K., Neuwelt, E.A., Samson, W.K., Zimmerman, E.A., et al., 1989. An antiserum to atrial natriuretic factor (ANF) cross-reacts with neurophysins in the hypothalamusohypophysial system of rat brain. Neuropeptides 14, 137-144.
Nunez, D.J., Davenport, A.P., Brown, M.J., 1990. Atrial natriuretic factor mRNA and binding sites in the adrenal gland. Biochem. J. 271, 555-558.
Nussdorfer, G.G., 1996. Paracrine control of adrenal cortical function by medullary chro- maffin cells. Pharmacol. Rev. 48, 495-530.
Nussdorfer, G.G., 2001. Proadrenomedullin-derived peptides in the paracrine control of the hypothalamicuitary-adrenal axis. Int. Rev. Cytol. 206, 249-284.
Nussdorfer, G.G., Malendowicz, L.K., 1998a. Role of VIP, PACAP, and related peptides in the regulation of the hypothalamicuitary-adrenal axis. Peptides 19, 1443-1467.
Nussdorfer, G.G., Malendowicz, L.K., 1998b. Role of tachykinins in the regulation of the hypothalamicuitary-adrenal axis. Peptides 19, 949-968.
Nussdorfer, G.G., Mazzocchi, G., Meneghelli, V., 1988-1989. Effect of atrial natriuretic factor (ANF) on the secretory activity of zona glomerulosa in sodium-restricted rats. Endocr. Res. 14, 293-303.
Nussdorfer, G.G., Rossi, G.P., Malendowicz, L.K., Mazzocchi, G., 1999. Autocrine- paracrine endothelin system in the physiology and pathology of steroid-secreting tissues. Pharmacol. Rev. 51, 403-438.
Obana, K., Naruse, M., Inagami, T., Brown, A.B., Naruse, K., Kurimoto, F., et al., 1985. Atrial natriuretic factor inhibits vasopressin secretion from rat posterior pituitary. Biochem. Biophys. Res. Commun. 132, 1088-1094.
Ohashi, M., Higuchi, K., Hashiguchi, T., Takayanagi, R., Nawata, H., 1991. Decreased binding capacity for alpha-human atrial natriuretic peptide in aldosterone-producing adrenocortical adenoma. Fukuoka Igaku Zasshi 82, 101-104.
Ohta, S., Shimekake, Y., Nagata, K., 1993. Cell-type-specific function of the C-type natriuretic peptide gene promoter in rat anterior pituitary-derived cultured cell lines. Mol. Cell. Biol. 13, 4077-4086.
Okuya, S., Yamashita, H., 1987. Effects of atrial natriuretic polypeptide on rat hypothalamic neurones in vitro. J. Physiol. 389, 717-728.
Olcese, J., Middendorff, R., Münker, M., Schmidt, C., McArdle, C.A., 1994. Natriuretic peptides stimulate cyclic GMP production in an immortalized LHRH neuronal cell line. J. Neuroendocrinol. 6, 127-130.
Oparil, S., Chen, Y.F., Peng, N., Wyss, J.M., 1996. Anterior hypothalamic norepinephrine, atrial natriuretic peptide, and hypertension. Front. Neuroendocrinol. 17, 212-246.
O’Sullivan, A.J., Burgoyne, R.D., 1990. Cyclic GMP regulates nicotine-induced secretion from cultured bovine adrenal chromaffin cells: effects of 8-bromo-cyclic GMP, atrial natriuretic peptide, and nitroprusside (nitric oxide). J. Neurochem. 54, 1805-1808.
O’Tierney, P.F., Tse, M.Y., Pang, S.C., 2007. Elevated renal norepinephrine in proANP gene-disrupted mice is associated with increased tyrosine hydroxylase expression in sympathetic ganglia. Regul. Pept. 143, 90-96.
Palkovits, M., Eskay, R.L., Antoni, F.A., 1987. Atrial natriuretic peptide in the median eminence is of paraventricular nucleus origin. Neuroendocrinology 46, 542-544.
Pandey, K.N., 2009. Ligand-mediated endocytosis and intracellular sequestration of guanylyl cyclase/natriuretic peptide receptors: role of GDAY motif. Mol. Cell. Biochem. 2009 Nov 26 [Epub ahead of print].
Papouchado, M.L., Vatta, M.S., Bianciotti, L.G., Fernández, B.E., 1995. Effects of atrial natriuretic factor on norepinephrine release evoked by angiotensins II and III in the rat adrenal medulla. Arch. Physiol. Biochem. 103, 55-58.
Pemberton, C.J., Yandle, T.G., Espiner, E.A., 2002. Immunoreactive forms of natriuretic peptides in ovine brain: response to heart failure. Peptides 23, 2235-2244.
Peng, N., Oparil, S., Meng, Q.C., Wyss, J.M., 1996. Atrial natriuretic peptide regulation of noradrenaline release in the anterior hypothalamic area of spontaneously hypertensive rats. J. Clin. Invest. 98, 2060-2065.
Perras, B., Schultes, B., Behn, B., Dodt, C., Born, J., Fehm, H.L., 2004. Intranasal atrial natriuretic peptide acts as central nervous inhibitor of the hypothalamicuitary-adrenal stress system in humans. J. Clin. Endocrinol. Metab. 89, 4642-4648.
Poole, C.J., Carter, D.A., Vallejo, M., Lightman, S.L., 1987. Atrial natriuretic factor inhibits the stimulated in-vivo and in-vitro release of vasopressin and oxytocin in the rat. J. Endocrinol. 112, 97-102.
Potter, L.R., Abbey-Hosch, S., Dickey, D.M., 2006. Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr. Rev. 27, 47-72.
Potter, L.R., Yoder, A.R., Flora, D.R., Antos, L.K., Dickey, D.M., 2009. Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications. Handb. Exp. Pharmacol. 191, 341-366.
Raha, D., Tortorella, C., Neri, G., Prasad, A., Raza, B., Raskar, R., et al., 2006. Atrial natriuretic peptide enhances cortisol secretion from guinea-pig adrenal gland: evidence for an indirect paracrine mechanism probably involving the local release of medullary catecholamines. Int. J. Mol. Med. 17, 633-636.
Raidoo, D.M., Narotam, P.K., van Dellen, J., Bhoola, K.D., 1998. Cellular orientation of atrial natriuretic peptide in the human brain. J. Chem. Neuroanat. 14, 207-213.
Rebuffat, P., Mazzocchi, G., Gottardo, G., Meneghelli, V., Nussdorfer, G.G., 1988. Further investigations on the atrial natriuretic factor (ANF)-induced inhibition of the growth and steroidogenic capacity of rat adrenal zona glomerulosa in vivo. J. Steroid Biochem. 29, 605-609.
Richard, D., Bourque, C.W., 1996. Atrial natriuretic peptide modulates synaptic transmis- sion from osmoreceptor afferents to the supraoptic nucleus. J. Neurosci. 16, 7526-7532. Rocco, S., Opocher, G., D’Agostino, D., Leone, L., Mantero, F., 1989. Lack of aldosterone inhibition by atrial natriuretic factor in primary aldosteronism: in vitro studies. J. Endo- crinol. Invest. 12, 13-17.
Rodriguez Fermepin, M., Vatta, M.S., Bianciotti, L.G., Wolovich, T.J., Fernandez, B.E., 2000. B-type and C-type natriuretic peptides modify norepinephrine uptake in discrete encephalic nuclei of the rat. Cell. Mol. Neurobiol. 20, 763-771.
Rodriguez Lopez, P., Ehlerding, A., Leonhardt, S., Jarry, H., Wuttke, W., 1993. Effects of angiotensin II and atrial natriuretic peptide on LH release are exerted in the preoptic area: possible involvement of gamma-aminobutyric acid (GABA). Exp. Clin. Endocrinol. 101, 350-355.
Rodriguez-Pascual, F., Miras-Portugal, M.T., Torres, M., 1996. Effect of cyclic GMP- increasing agents nitric oxide and C-type natriuretic peptide on bovine chromaffin cell function: inhibitory role mediated by cyclic GMP-dependent protein kinase. Mol. Pharmacol. 49, 1058-1070.
Rose, R.A., Anand-Srivastava, M.B., Giles, W.R., Bains, J.S., 2005. C-type natriuretic peptide inhibits L-type Ca2+ current in rat magnocellular neurosecretory cells by activating the NPR-C receptor. J. Neurophysiol. 94, 612-621.
Ryan, M.C., Gundlach, A.L., 1998. Ontogenic expression of natriuretic peptide mRNAs in postnatal rat brain: implications for development? Brain Res. Dev. Brain Res. 105, 251-268.
Ryan, M.C., Shen, P.J., Gundlach, A.L., 1997. Angiotensinogen and natriuretic peptide mRNAs in rat brain: localization and differential regulation by adrenal steroids in hypothalamus. Peptides 18, 495-504.
Samson, W.K., 1985. Atrial natriuretic factor inhibits dehydration and hemorrhage-induced vasopressin release. Neuroendocrinology 40, 277-279.
Samson, W.K., Bianchi, R., 1988. Further evidence for a hypothalamic site of action of atrial natriuretic factor: inhibition of prolactin secretion in the conscious rat. Can. J. Physiol. Pharmacol. 66, 301-305.
Samson, W.K., Skala, K.D., Huang, F.L., 1991. CNP-22 stimulates, rather than inhibits, water drinking in the rat: evidence for a unique biological action of the C-type natriuretic peptides. Brain Res. 568, 285-288.
Samson, W.K., Alexander, B.D., Skala, K.D., Huang, F.L., Fulton, R.J., 1992. Central peptidergic mechanisms controlling reproductive hormone secretion: novel methodol- ogy reveals a role for the natriuretic peptides. Can. J. Physiol. Pharmacol. 70, 773-778. Samson, W.K., Huang, F.L., Fulton, R.J., 1993. C-type natriuretic peptide mediates the hypothalamic actions of the natriuretic peptides to inhibit luteinizing hormone secretion. Endocrinology 132, 504-509.
Samson, W.K., Huang, F.L., Fulton, R.J., 1995. Opposing neuroendocrine actions of the natriuretic peptides: C-type and A-type natriuretic peptides do not interact with the same hypothalamic cells controlling prolactin secretion. J. Neuroendocrinol. 7, 759-763.
Saper, C.B., Hurley, K.M., Moga, M.M., Holmes, H.R., Adams, S.A., Leahy, K.M., et al., 1989. Brain natriuretic peptides: differential localization of a new family of neuropep- tides. Neurosci. Lett. 96, 29-34.
Sarzani, R., Opocher, G., Paci, M.V., Belloni, A.S., Mantero, F., Dessì-Fulgheri, P., et al., 1999. Natriuretic peptides receptors in human aldosterone-secreting adenomas. J. Endo- crinol. Invest. 22, 514-518.
Scott, J.N., Jennes, L.H., 1989. Ontogeny of atrial natriuretic peptide receptors in fetal rat kidney and adrenal gland. Histochemistry 91, 395-400.
Segal, J.P., Stallings, N.R., Lee, C.E., Zhao, L., Socci, N., Viale, A., et al., 2005. Use of laser-capture microdissection for the identification of marker genes for the ventromedial hypothalamic nucleus. J. Neurosci. 25, 4181-4188.
Sessions, C., Lawrence, D., Clinkingbeard, C., Shenker, Y., 1992. Regulation of adrenal atrial natriuretic hormone receptor subtypes. Life Sci. 50, 1087-1095.
Shibasaki, T., Naruse, M., Naruse, K., Masuda, A., Kim, Y.S., Imaki, T., et al., 1986a. Atrial natriuretic factor is released from rat hypothalamus in vitro. Biochem. Biophys. Res. Commun. 136, 590-595.
Shibasaki, T., Naruse, M., Yamauchi, N., Masuda, A., Imaki, T., Naruse, K., et al., 1986b. Rat atrial natriuretic factor suppresses proopiomelanocortin-derived peptides secretion from both anterior and intermediate lobe cells and growth hormone release from anterior lobe cells of rat pituitary in vitro. Biochem. Biophys. Res. Commun. 135, 1035-1041.
Shimekake, Y., Ohta, S., Nagata, K., 1994. C-type natriuretic peptide stimulates secretion of growth hormone from rat-pituitary-derived GH3 cells via a cyclic-GMP-mediated pathway. Eur. J. Biochem. 222, 645-650.
Shionoiri, H., Hirawa, N., Takasaki, I., Ishikawa, Y., Minamisawa, K., Miyajima, E., et al., 1987. Presence of functional receptors for atrial natriuretic peptide in human pheochro- mocytoma. Biochem. Biophys. Res. Commun. 148, 286-291.
Shionoiri, H., Hirawa, N., Takasaki, I., Ishikawa, Y., Oda, H., Gotoh, E., et al., 1988. Lack of atrial natriuretic peptide receptors in human aldosteronoma. Biochem. Biophys. Res. Commun. 152, 37-43.
Shionoiri, H., Hirawa, N., Takasaki, I., Ishikawa, Y., Oda, H., Minamisawa, K., et al., 1989. Functional atrial natriuretic peptide receptor in human adrenal tumor. J. Cardiovasc. Pharmacol. 13 (Suppl 6), S9-S12.
Shirakami, G., Itoh, H., Suga, S., Komatsu, Y., Hama, N., Mori, K., et al., 1993. Central action of C-type natriuretic peptide on vasopressin secretion in conscious rats. Neurosci. Lett. 159, 25-28.
Simard, J., Hubert, J.F., Labrie, F., Israël-Assayag, E., Heisler, S., 1986. Atrial natriuretic factor-induced cGMP accumulation in rat anterior pituitary cells in culture is not coupled to hormonal secretion. Regul. Pept. 15, 269-278.
Sone, M., Totsune, K., Takahashi, K., Ohneda, M., Itoi, K., Murakami, O., et al., 1991. Porcine brain natriuretic peptide-like immunoreactivity in rat tissues. Peptides 12, 1333-1335.
Spiessberger, B., Bernhard, D., Herrmann, S., Feil, S., Werner, C., Luppa, P.B., et al., 2009. cGMP-dependent protein kinase II and aldosterone secretion. FEBS J. 276, 1007-1013.
Spinazzi, R., Andreis, P.G., Nussdorfer, G.G., 2005. Neuropeptide-Y and Y-receptors in the autocrine-paracrine regulation of adrenal gland under physiological and pathophysi- ological conditions. Int. J. Mol. Med. 15, 3-13.
Standaert, D.G., Needleman, P., Saper, C.B., 1986a. Organization of atriopeptin-like immunoreactive neurons in the central nervous system of the rat. J. Comp. Neurol. 253, 315-341.
Standaert, D.G., Cicero, T., Needleman, P., 1986b. Atriopeptin inhibits the release of luteinizing hormone. Fed. Proc. 45, 174.
Standaert, D.G., Cechetto, D.F., Needleman, P., Saper, C.B., 1987. Inhibition of the firing of vasopressin neurons by atriopeptin. Nature 329, 151-153.
Steele, M.K., 1990. Additive effects of atrial natriuretic peptide and angiotensin II on luteinizing hormone and prolactin release in female rats. Neuroendocrinology 51, 345-350.
Stepniakowski, K., Januszewicz, A., Lapiński, M., Feltynowski, T., Chodakowska, J., Ignatowska-Switalska, H., et al., 1992. Plasma atrial natriuretic peptide (ANP) con- centration in patients with pheochromocytoma. Blood Press. 1, 157-161.
Stewart, R.E., Swithers, S.E., Plunkett, L.M., McCarty, R., 1988. ANF receptors: distribu- tion and regulation in central and peripheral tissues. Neurosci. Biobehav. Rev. 12, 151-168.
Sudoh, T., Kangawa, K., Minamino, N., Matsuo, H., 1988. A new natriuretic peptide in porcine brain. Nature 332, 78-81.
Sudoh, T., Minamino, N., Kangawa, K., Matsuo, H., 1990. C-type natriuretic peptide (CNP): a new member of natriuretic peptide family identified in porcine brain. Biochem. Biophys. Res. Commun. 168, 863-870.
Sumners, C., Tang, W., 1992. Atrial natriuretic peptide receptor subtypes in rat neuronal and astrocyte glial cultures. Am. J. Physiol. 262, C1134-C1143.
Takahashi, K., Totsune, K., Sone, M., Ohneda, M., Murakami, O., Itoi, K., et al., 1992. Human brain natriuretic peptide-like immunoreactivity in human brain. Peptides 13, 121-123.
Takao, T., Hashimoto, K., Ota, Z., 1988. Effect of atrial natriuretic peptide on acetylcho- line-induced release of corticotropin-releasing factor from rat hypothalamus in vitro. Life Sci. 42, 1199-1203.
Tan, T.T., Yang, Z., Huang, W., Lim, A.T., 1994. ANF(1-28) is a potent suppressor of pro- opiomelanocortin (POMC) mRNA but a weak inhibitor of beta EP-LI release from AtT-20 cells. J. Endocrinol. 143, R1-R4.
Tanaka, I., Inagami, T., 1986. Release of immunoreactive atrial natriuretic factor from rat hypothalamus in vitro. Eur. J. Pharmacol. 122, 353-355.
Tanaka, I., Misono, K.S., Inagami, T., 1984. Atrial natriuretic factor in rat hypothalamus, atria and plasma: determination by specific radioimmunoassay. Biochem. Biophys. Res. Commun. 124, 663-668.
Thompson, I.R., Chand, A.N., Jonas, K.C., Burrin, J.M., Steinhelper, M.E., Wheeler- Jones, C.P., et al., 2009. Molecular characterisation and functional interrogation of a local natriuretic peptide system in rodent pituitaries, alphaT3-1 and LbetaT2 gonadotroph cells. J. Endocrinol. 203, 215-229.
Totsune, K., Takahashi, K., Ohneda, M., Itoi, K., Murakami, O., Mouri, T., 1994a. C-type natriuretic peptide in the human central nervous system: distribution and molecular form. Peptides 15, 37-40.
Totsune, K., Takahashi, K., Murakami, O., Itoi, K., Sone, M., Ohneda, M., et al., 1994b. Immunoreactive C-type natriuretic peptide in human adrenal glands and adrenal tumors. Peptides 15, 287-290.
Totsune, K., Takahashi, K., Murakami, O., Satoh, F., Sone, M., Ohneda, M., et al., 1996. Immunoreactive brain natriuretic peptide in human adrenal glands and adrenal tumors. Eur. J. Endocrinol. 135, 352-356.
Trejter, M., Markowska, A., Belloni, A.S., Nussdorfer, G.G., Malendowicz, L.K., 2002. Investigation of the effect of different regulatory peptides on adrenocortical cell prolifer- ation in immature rats: evidence that endogenous adrenomedullin exerts a stimulating action. Int. J. Mol. Med. 10, 81-84.
Tsutsui, M., Yanagihara, N., Minami, K., Kobayashi, H., Nakashima, Y., Kuroiwa, A., et al., 1994. C-type natriuretic peptide stimulates catecholamine synthesis through the accumulation of cyclic GMP in cultured bovine adrenal medullary cells. J. Pharmacol. Exp. Ther. 268, 584-589.
Tunny, T.J., Gordon, R.D., 1986. Plasma atrial natriuretic peptide in primary aldosteronism (before and after treatment) and in Bartter’s and Gordon’s syndromes. Lancet 1, 272-273.
Tunny, T.J., Jonsson, J.R., Klemm, S.A., Ballantine, D.M., Stowasser, M., Gordon, R.D., 1994. Association of restriction fragment length polymorphism at the atrial natriuretic peptide gene locus with aldosterone responsiveness to angiotensin in aldosterone-pro- ducing adenoma. Biochem. Biophys. Res. Commun. 204, 1312-1317.
Ueda, S., Minamino, N., Sudoh, T., Kangawa, K., Matsuo, H., 1988. Regional distribution of immunoreactive brain natriuretic peptide in porcine brain and spinal cord. Biochem. Biophys. Res. Commun. 155, 733-739.
Ur, E., Faria, M., Tsagarakis, S., Anderson, J.V., Besser, G.M., Grossman, A., 1991. Atrial natriuretic peptide in physiological doses does not inhibit the ACTH or cortisol response to corticotrophin-releasing hormone-41 in normal human subjects. J. Endocrinol. 131, 163-167.
Vaillancourt, P., Omer, S., Palfree, R., Varma, D.R., Mulay, S., 1997. Downregulation of adrenal atrial natriuretic peptide receptor mRNAs and proteins by pregnancy in rats. J. Endocrinol. 155, 523-530.
Vatta, M.S., Bianciotti, L.G., Fernández, B.E., 1992. Effects of atrial natriuretic peptide, angiotensin II and III on norepinephrine uptake in the rat adrenal medulla. Rev. Esp. Fisiol. 48, 185-189.
Vatta, M.S., Papouchado, M.L., Bianciotti, L.G., Fernandez, B.E., 1994. Modulation of the rat adrenal medulla norepinephrine secretion in a sodium-free medium by atrial natri- uretic factor. Peptides 15, 709-712.
Vatta, M., Rodriguez-Fermepín, M., Bianciotti, L., Perazzo, J., Monserrat, A., Fernández, B., 1995. Atrial natriuretic factor enhances norepinephrine uptake in cir- cumventricular organs, locus coeruleus and nucleus tractus solitarii of the rat. Neurosci. Lett. 197, 29-32.
Vatta, M.S., Presas, M., Bianciotti, L.G., Zarrabeitia, V., Fernández, B.E., 1996. B and C types natriuretic peptides modulate norepinephrine uptake and release in the rat hypo- thalamus. Regul. Pept. 65, 175-184.
Vatta, M.S., Presas, M.F., Bianciotti, L.G., Rodriguez-Fermepin, M., Ambros, R., Fernandez, B.E., 1997. B and C types natriuretic peptides modify norepinephrine uptake and release in the rat adrenal medulla. Peptides 18, 1483-1489.
Vatta, M.S., Rubio, M., Bianciotti, L.G., Fernandez, B.E., 1998. Atrial natriuretic factor does not affect norepinephrine catabolismin rat hypothalamus and adrenal medulla. Neurosci. Lett. 253, 151-154.
Vatta, M.S., Rodriguez-Fermepin, M., Durante, G., Bianciotti, L.G., Fernandez, B.E., 1999. Atrial natriuretic factor inhibits norepinephrine biosynthesis and turnover in the rat hypothalamus. Regul. Pept. 85, 101-107.
Vesely, D.L., Chiou, S., Douglass, M.A., McCormick, M.T., Rodriguez-Paz, G., Schocken, D.D., 1995. Kaliuretic peptide and long acting natriuretic peptide as well as atrial natriuretic factor inhibit aldosterone secretion. J. Endocrinol. 146, 373-380.
Wiedemann, K., Jahn, H., Kellner, M., 2000. Effects of natriuretic peptides upon hypotha- lamo-pituitary-adrenocortical system activity and anxiety behaviour. Exp. Clin. Endocri- nol. Diabetes 108, 5-13.
Wilcox, J.N., Augustine, A., Goeddel, D.V., Lowe, D.G., 1991. Differential regional expression of three natriuretic peptide receptor genes within primate tissues. Mol. Cell. Biol. 11, 3454-3462.
Wolfensberger, M., Forssmann, W.G., Reinecke, M., 1995. Localization and coexistence of atrial natriuretic peptide (ANP) and neuropeptide Y (NPY) in vertebrate adrenal chro- maffin cells immunoreactive to TH, DBH and PNMT. Cell Tissue Res. 280, 267-276.
Wong, M., Samson, W.K., Dudley, C.A., Moss, R.L., 1986. Direct, neuronal action of atrial natriuretic factor in the rat brain. Neuroendocrinology 44, 49-53.
Yamaji, T., Ishibashi, M., Sekihara, H., Takaku, F., Nakaoka, H., Fujii, J., 1986. Plasma levels of atrial natriuretic peptide in primary aldosteronism and essential hypertension. J. Clin. Endocrinol. Metab. 63, 815-818.
Yamamoto, S., Inenaga, K., Eto, S., Yamashita, H., 1995. Cardiovascular-related peptides influence hypothalamic neurons involved in control of body water homeostasis. Obes. Res. 3 (Suppl. 5), 789S-794S.
Yamamoto, S., Morimoto, I., Yanagihara, N., Kangawa, K., Inenaga, K., Eto, S., et al., 1997. C-type natriuretic peptide suppresses arginine-vasopressin secretion from dissociated mag- nocellular neurons in newborn rat supraoptic nucleus. Neurosci. Lett. 229, 97-100.
Yanagihara, N., Okazaki, M., Terao, T., Uezono, Y., Wada, A., Izumi, F., 1991. Stimulatory effects of brain natriuretic peptide on cyclic GMP accumulation and tyrosine hydroxylase activity in cultured bovine adrenal medullary cells. Naunyn. Schmiedebergs Arch. Phar- macol. 343, 289-295.
Yandle, T.G., Fisher, S., Charles, C., Espiner, E.A., Richards, A.M., 1993. The ovine hypothalamus and pituitary have markedly different distribution of C-type natriuretic peptide forms. Peptides 14, 713-716.
Yen, S.H., Pan, J.T., 1997. Atrial natriuretic peptide negatively modulates the stimulatory effects of angiotensin II on tuberoinfundibular dopaminergic neuronal activity. Neuro- chemical and electrophysiological studies. Neuroendocrinology 66, 313-320.