The UALCAN and GEPIA Analyses of the TCGA Database Show a Strong Association Between Increased Expression of Stathmin 1 in Adrenocortical Carcinoma Tissues and Patient Survival
SHIN-NOSUKE YAMASHITA1*, YOSHIATSU TANAKA1*, SHAJEDUL ISLAM1,2,
TAKAO KITAGAWA1, KAZUHIRO TOKUDA3, DURGA PAUDEL1, SARITA GIRI1,
TOHRU OHTA1, FUMIYA HARADA4, HIROKI NAGAYASU4 and YASUHIRO KURAMITSU1,5
1Advanced Research Promotion Centre, 4Division of Oral and Maxillofacial Surgery School of Dentistry, and
5School of Medical Technology, Health Sciences University of Hokkaido, Ishikari-Tobetsu, Japan;
2Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX, U.S.A .; 3Graduate School of Health and Welfare, Yamaguchi Prefectural University, Yamaguchi, Japan
Abstract
Background/Aim: Adrenocortical carcinoma (ACC) arises from the adrenal cortex. This cancer is characterized by a very low incidence, poor prognosis and high mortality rate. Because early detection is extremely difficult and no effective treatment has been established, the five-year survival rate is very low. Therefore, there is an urgent need to identify biomarkers and therapeutic target molecules that can serve as early detection and prognostic factors. Stathmin 1 is a ubiquitously expressed 19 kDa cytosolic phosphoprotein, which induces microtubule depolymerization and regulates microtubule-dependent processes such as cell division and motility. Its over- expression has been linked to cell migration and invasion in sarcoma, malignant glioma, gastric cancer, colorectal cancer, and non-small cell lung cancer. However, the clinicopathological involvement of stathmin 1 in ACC, has not yet been reported.
Materials and Methods: The GEPIA and UALCAN platforms were used to analyze stathmin 1 mRNA expression and its association with survival in patients with ACC using TCGA data.
Results: TCGA analysis showed that the expression of stathmin 1 was significantly increased in ACC tissues, and patients with increased expression of stathmin 1 in cancer tissues had a significantly shorter survival time.
Conclusion: Stathmin 1 is highly expressed in ACC tissues and inversely correlated with patient prognosis, suggesting it may be a potential prognostic biomarker for patients with ACC. Furthermore, the GEPIA and UALCAN platforms proved to be highly effective in investigating the correlation between the expression levels of stathmin 1 in ACC tissues and the survival time of patients using the TCGA database.
Keywords: Stathmin 1, adrenocortical carcinoma, Kaplan-Meier survival plot, TCGA, prognosis.
*These Authors contributed equally to this study.
✉ ☒ Yasuhiro Kuramitsu, Advanced Research Promotion Center, Health Sciences University of Hokkaido, 1757 Kanazawa,
Ishikari-Tobetsu, Hokkaido 061-0293, Japan. Tel: +81 133231630, e-mail: climates@hoku-iryo-u.ac.jp
Introduction
Adrenocortical carcinoma (ACC) is one of the very rare cancers that develops in the adrenal cortex, and is known to occur frequently in children under the age of five and adults in their 40s and 50s. ACC not only causes symptoms such as abdominal pain and abdominal distension due to tumor growth, but can also cause other symptoms, including high blood pressure, hyperglycemia, muscle weakness, obesity, due to excessive secretion of hormones from the adrenal cortex. It is a rare tumor derived from the adrenal cortex. The annual worldwide incidence is estimated to be 0.5 to 2.0 cases per million people (1).
The prognosis for this cancer is poor. After surgery to remove the tumor, patients have a five-year survival rate of 38.6 percent, with a median survival time of 31.9 months (2). Furthermore, the 5-year survival rate for patients with metastatic disease is less than 15% (3). Therefore, there is an urgent need to select suitable prognostic biomarkers for the treatment of patients with ACC, but currently there are no clinically useful prognostic biomarkers for ACC.
Stathmin 1 is a ubiquitously expressed 18 kDa cytoplasmic phosphoprotein encoded by stathmin 1 (STMN1) gene. It is involved in the “relay” of multiple intracellular signaling pathways (4, 5). It has been reported to destabilize microtubules by interacting with tubulin. Serine residues 15, 24, 37, and 62 on the stathmin 1 molecule are phosphorylated, and this phosphorylation regulates its interaction with tubulin. PKA, CAMK, MAPK, Cdk and PKC catalyze these phosphorylations (6). We have previously analyzed heat stress-induced hyperphosphorylation of stathmin 1 at serine 37 (Ser37) in Jurkat cells using two- dimensional gel electrophoresis and tandem mass spectrometry. These results strongly suggest that heat stress activates Cdks that phosphorylate Ser37 of stathmin 1 in Jurkat cells, resulting in loss of microtubule sequestering activity and inducing cell cycle arrest and apoptosis (7, 8). Upregulation of stathmin 1 has been reported in various cancer tissues, including prostate cancer, oral squamous cell carcinoma, hepatocellular carcinoma, osteosarcoma,
malignant glioma, gastric cancer, colorectal cancer, esophageal cancer, non-small cell lung cancer (9-19). Aronova et al. reported increased expression of stathmin 1 in ACC tissues and demonstrated that upregulation of stathmin 1 was associated with a more aggressive phenotype in vitro (20). Furthermore, Passaia et al. showed that stathmin 1 was highly expressed in ACC tissues and was associated with survival outcomes in patients with ACC (21).
The Cancer Genome Atlas (TCGA) is a cancer genomics information database that contains information on more than 20,000 primary cancer and normal tissue samples from 33 cancer types (22). UALCAN is a cancer data analytics platform that uses data from TCGA to assess gene expression in 33 types of cancer and its impact on patient survival (23). Similar to UALCAN, GEPIA and GEPIA2 are also cancer data analysis platforms that provide key interactive and customizable features such as differential expression analysis, profiling plots, correlation analysis, patient survival analysis, similar gene detection, and dimensionality reduction analysis (24). We have used online bioinformatics tools, UALCAN, GEPIA and GEPIA 2, and clarified the expression and prognostic significance of DDX39 in patients with ACC using the TCGA database (25). In addition to ACC, we also identified DDX39 and STC-1 as genes associated with uveal melanoma prognosis using UALCAN and GEPIA (26, 27). Since these online bioinformatics tools are practical and useful, in this study, we investigated the relationship between increased expression of stathmin 1 in ACC tissues and the prognosis of patients with ACC.
Materials and Methods
Stathmin 1 mRNA expression in adrenocortical carcinoma tissues. We used GEPIA, a web server for cancer and normal gene expression profiling, to examine the expression levels of stathmin 1 mRNA in ACC tissues (28). We entered the gene name “STMN1” into the TCGA database and selected DIY Boxplot (cancer vs. normal tissue analysis) to obtain the results. This analysis showed a series of ACC studies and the expression of stathmin 1 in
cancer and normal tissues. The filters were set as follows: i) Gene: STMN1, ii) Threshold settings: Log2FC cutoff 2 with p-value of <0.05.
Assessment of stathmin-1 mRNA expression in cancer tissues from patients with different stages of adrenocortical carcinoma. By using the UALCAN platform, we investigated the expression levels of stathmin 1 mRNA in cancer tissues from patients with various stages of adrenocortical carcinoma registered in the TCGA database (23). The gene name “STMN1” was registered in the TCGA database.
Survival analysis according to the mRNA expression level of stathmin 1 in adrenocortical carcinoma tissues. By using the GEPIA platform, survival analysis was performed to investigate the mRNA expression of stathmin 1 in ACC. In the GEPIA platform, the gene name “STMN1” was entered, and median cutoff was selected to generate Kaplan-Meier curves for patients with ACC. Furthermore, the ULCAN platform was used to investigate the impact of stathmin 1 mRNA expression levels on the survival of patients with ACC. A p-value <0.05 was considered statistically significant.
Results
Stathmin 1 mRNA expression was higher in ACC tissues. The TCGA dataset was analyzed by using the GEPIA platform to investigate the expression of stathmin 1 mRNA in ACC tissues, and the results showed that stathmin 1 mRNA levels were higher in ACC tissues (n=77) compared to normal tissues (n=128) (p<0.05) (Figure 1). We next analyzed whether the increase in stathmin-1 mRNA expression levels was dependent on the stage of ACC. Figure 2 shows stathmin 1 mRNA expression in ACC tissues according to individual cancer stages [stage I (n=9), stage II (n=37), stage III (n=16), stage IV (n=15)]. Stathmin 1 mRNA expression gradually increased with the progression of ACC. Notably, stathmin 1 mRNA was significantly higher in ACC tissues from patients with stage IV ACC compared with patients at all other stages.
10
*
8
6
4
2
0
ACC
(num(T)=77; num(N)=128)
High expression of stathmin 1 correlates with shorter survival in patients with ACC. To analyze overall survival status, Kaplan-Meier survival plots were generated by using the GEPIA2 platform. Increased expression levels of stathmin 1 mRNA were found to correlate with shorter patient survival (p=0.0000041) (Figure 3A). Furthermore, increased expression levels of stathmin 1 mRNA correlated with shorter disease-free intervals (p=0.0000014) (Figure 3B). Additionally, we also generated Kaplan-Meier survival
Expression of STMN1 in ACC based on individual cancer stages
500
P= 5.663400E-03
P=6.767200E-04
400
P=2.987300E-04
Transcript per million
300
200
100
0
Stage1 (n=9)
Stage2 (n=37)
Stage3 (n=16)
Stage4 (n=15)
TCGA samples
plots for patients with ACC tissues with increased or decreased stathmin-1 using the UALCAN platform. The results showed that increased expression levels of stathmin 1 mRNA in ACC tissues correlated with shorter patient survival (p<0.0001) (Figure 4).
Discussion
In the present study, we used the GEPIA and UALCAN bioinformatics platforms to analyze stathmin 1 mRNA expression and Kaplan-Meier survival curves in patients with ACC. Stathmin 1 mRNA expression levels were significantly elevated in ACC tissues compared with normal adrenal tissues, and this elevated stathmin 1 expression was correlated with shorter patient survival.
Stathmin 1 has been reported to interact with tubulin to destabilize microtubules (29), which is thought to be a
very important function since it controls microtubule dynamics. Microtubules play a central role in cell division and are also strongly involved in the transport of molecules within cells (30). Microtubules are essential for the formation and function of invadosomes that play a key role in cancer cell invasion and metastasis (31). Therefore, the expression and function of stathmin 1, which plays an important role in microtubule dynamics, may be closely related to cancer prognosis. Stathmin 1, known as tumor protein 18, was first discovered as a tumor protein highly expressed in breast and ovarian cancers and leukemia (32- 34). Moreover, increased expression of stathmin 1 in various cancer tissues including prostate cancer, oral squamous cell carcinoma, hepatocellular carcinoma, osteosarcoma, esophageal cancer, and lung cancer has been reported (9-13, 17, 18). Furthermore, Passaia et al. reported that increased expression of stathmin 1 promotes
A
Overall survival
B
Disease-free survival
1.0
LOW STMN1 Group
1.0
High STMN1 Group
Low STMN1 TPM
High STMN1 TPM
Logrank p=4.1e-06
Logrank p=1.4e-06
0.8
HR(high)=7.3
p(HR)=7.2e-05
0.8
HR(high)=5.6
p(HR)=1.4e-05
n(high)=38
n(high)=38
Percent survival
0.6
n(low)=38
Percent survival
0.6
n(low)=38
0.4
0.4
0.2
0.2
0.0
0.0
0
50
100
150
0
50
100
150
Time (months)
Time (months)
a more aggressive phenotype in vitro, and stathmin 1 was highly expressed in ACC tissues and associated with survival outcomes in patients ACC (21). Considering the above, in ACC cells, stathmin 1 may regulate microtubule dynamics and favorably affect the formation and function of invadosomes, thereby promoting cancer cell invasion and metastasis, leading to poor prognosis.
The present study suggests that high expression of stathmin 1 may be associated with poor prognosis in patients with ACC, but it has not been reported whether prognosis can be determined by measuring stathmin 1 in the serum of patients with ACC, or whether autoantibodies against stathmin 1 are present in the serum of these patients. However, Yan et al. reported that serum stathmin concentrations were significantly elevated in patients with esophageal cancer compared with controls (35), and Biaoxue et al. reported that serum stathmin concentrations were elevated in patients with lung adenocarcinoma (36). Furthermore, Maroun et al. reported that anti-stathmin autoantibodies were detected in high levels in the serum of
patients with breast cancer (37). Taken together, these results suggest that stathmin 1 may promote the migration and invasion of ACC cells, increase metastasis to distant organs, and lead to poor prognosis.
We previously reported that heat stress activates Cdk that phosphorylates stathmin 1 at Ser37 in Jurkat cells, resulting in loss of microtubule sequestering activity and induction of cell cycle arrest and apoptosis. In this study, we used the correlation between stathmin 1 mRNA expression level and survival time as an index to evaluate the association with prognosis (7). It remains to be seen whether ACC cells can maintain their high proliferation, invasion, metastasis and survival potential even with high phosphorylation levels of stathmin 1 at Ser37. Future studies should focus on the correlation between phosphorylation levels of stathmin 1 and patient prognosis. Further studies are needed to clarify the exact mechanisms by which stathmin promotes the progression of ACC, and to investigate the possibility of stathmin 1 or anti-stathmin 1 autoantibodies in the patients’ sera are prognostic biomarkers for ACC.
Effect of STMN1 expression level on ACC patient survival
1.00
0.75
Survival probability
0.50
0.25
p<0.0001
Expression level
0.00
High expression (n=20)
1
Low/Medium expression (n=59)
0
1,000
2,000
3,000
4,000
Time (days)
Conflicts of Interest
The Authors declare no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Authors’ Contributions
All Authors contributed to the study’s conception and design. Data collection and analysis were performed by Shin-nosuke Yamashita, Yoshiatsu Tanaka, Shajedul Islam and Yasuhiro Kuramitsu. Shin-nosuke Yamashita and Yoshiatsu Tanaka wrote the first draft of the manuscript, Shajedul Islam and Yasuhiro Kuramitsu commented on
previous versions of the manuscript. All Authors read and approved the final manuscript.
Artificial Intelligence (AI) Disclosure
No artificial intelligence (AI) tools, including large language models or machine learning software, were used in the preparation, analysis, or presentation of this manuscript.
References
1 Sarrafan-Chaharsoughi Z, Yazdian Anari P, Malayeri AA, Naraev B, Del Rivero J: Update on adrenocortical carcinoma. Urol Clin North Am 52(2): 275-286, 2025. DOI: 10.1016/ j.ucl.2025.01.009
2 Bilimoria KY, Shen WT, Elaraj D, Bentrem DJ, Winchester DJ, Kebebew E, Sturgeon C: Adrenocortical carcinoma in the United States: treatment utilization and prognostic factors. Cancer 113(11): 3130-3136, 2008. DOI: 10.1002/cncr.23886
3 Libé R, Huillard O: Adrenocortical carcinoma: Diagnosis, prognostic classification and treatment of localized and advanced disease. Cancer Treat Res Commun 37: 100759, 2023. DOI: 10.1016/j.ctarc.2023.100759
4 Sobel A, Boutterm MC, Beretta L, Chneiweiss H, Doye V, Peyro- Saint-Paul H: Intracellular substrates for extracellular signaling. Characterization of a ubiquitous, neuron-enriched phosphoprotein (stathmin). J Biol Chem 264(7): 3765-3772, 1989.
5 Sobel A: Stathmin: a relay phosphoprotein for multiple signal transduction? Trends Biochem Sci 16(8): 301-305, 1991. DOI: 10.1016/0968-0004(91)90123-d
6 Curmi PA, Andersen SS, Lachkar S, Gavet O, Karsenti E, Knossow M, Sobel A: The stathmin/tubulin interaction in vitro. J Biol Chem 272(40): 25029-25036, 1997. DOI: 10.1074/jbc.272.40.25029
7 Nakamura K, Zhang X, Kuramitsu Y, Fujimoto M, Yuan X, Akada J, Aoshima-okuda M, Mitani N, Itoh Y, Katoh T, Morita Y, Nagasaka Y, Yamazaki Y, Kuriki T, Sobel A: Analysis on heat stress-induced hyperphosphorylation of stathmin at serine 37 in Jurkat cells by means of two-dimensional gel electrophoresis and tandem mass spectrometry. J Chromatogr A 1106(1-2): 181-189, 2006. DOI: 10.1016/j.chroma.2005.12.068
8 Nagasaka Y, Fijimoto M, Arai H, Nakamura K: Inhibition of heat-induced phosphorylation of stathmin by the bioflavonoid quercetin. Electrophoresis 23(4): 670-673, 2002. DOI: 10.1002/1522-2683(200202)23:4<670 :: AID- ELPS670>3.0.CO;2-3
9 Shi Y, Yeh YA, Cheng S, Gu X, Yang S, Li L, Khater NP, Kasper S, Yu X: Stathmin 1 expression in neuroendocrine and proliferating prostate cancer. Discov Oncol 16(1): 19, 2025. DOI: 10.1007/s12672-025-01754-6
10 Vadla P, Deepthi G, Julakanti V, Jahagirdar D, Meruva S, Tantravahi S: Association of stathmin (Op18) with TNM staging and grading of oral squamous cell carcinoma and its role in tumor progression. J Contemp Dent Pract 23(5): 497- 502, 2022.
11 Liu YP, Pan LL, Kong CC: Stathmin 1 promotes the progression of liver cancer through interacting with YAP1. Eur Rev Med Pharmacol Sci 24(13): 7335-7344, 2020. DOI: 10.26355/ eurrev_202007_21900
12 Zhao C, Li H, Wang L, Sun W: An immunohistochemical study of Stathmin 1 expression in osteosarcoma shows an association with metastases and poor patient prognosis. Med Sci Monit 24: 6070-6078, 2018. DOI: 10.12659/MSM.910953
13 Belletti B, Nicoloso MS, Schiappacassi M, Berton S, Lovat F, Wolf K, Canzonieri V, D’Andrea S, Zucchetto A, Friedl P, Colombatti A, Baldassarre G: Stathmin activity influences sarcoma cell shape, motility, and metastatic potential. Mol
Biol Cell 19(5): 2003-2013, 2008. DOI: 10.1091/mbc.e07-09- 0894
14 Liang XJ, Choi Y, Sackett DL, Park JK: Nitrosoureas inhibit the stathmin-mediated migration and invasion of malignant glioma cells. Cancer Res 68(13): 5267-5272, 2008. DOI: 10.1158/0008-5472.CAN-07-6482
15 Jeon TY, Han ME, Lee YW, Lee YS, Kim GH, Song GA, Hur GY, Kim JY, Kim HJ, Yoon S, Baek SY, Kim BS, Kim JB, Oh SO: Overexpression of stathmin1 in the diffuse type of gastric cancer and its roles in proliferation and migration of gastric cancer cells. Br J Cancer 102(4): 710-718, 2010. DOI: 10.1038/sj.bjc.6605537
16 Zheng P, Liu YX, Chen L, Liu XH, Xiao ZQ, Zhao L, Li GQ, Zhou J, Ding YQ, Li JM: Stathmin, a new target of PRL-3 identified by proteomic methods, plays a key role in progression and metastasis of colorectal cancer. J Proteome Res 9(10): 4897- 4905, 2010. DOI: 10.1021/pr100712t
17 Ni PZ, He JZ, Wu ZY, Ji X, Chen LQ, Xu XE, Liao LD, Wu JY, Li EM, Xu LY: Overexpression of Stathmin 1 correlates with poor prognosis and promotes cell migration and proliferation in oesophageal squamous cell carcinoma. Oncol Rep 38(6): 3608-3618, 2017. DOI: 10.3892/or.2017.6039
18 Bao P, Yokobori T, Altan B, Iijima M, Azuma Y, Onozato R, Yajima T, Watanabe A, Mogi A, Shimizu K, Nagashima T, Ohtaki Y, Obayashi K, Nakazawa S, Bai T, Kawabata-Iwakawa R, Asao T, Kaira K, Nishiyama M, Kuwano H: High STMN1 expression is associated with cancer progression and chemo-resistance in lung squamous cell carcinoma. Ann Surg Oncol 24(13): 4017-4024, 2017. DOI: 10.1245/s10434-017-6083-0
19 Singer S, Malz M, Herpel E, Warth A, Bissinger M, Keith M, Muley T, Meister M, Hoffmann H, Penzel R, Gdynia G, Ehemann V, Schnabel PA, Kuner R, Huber P, Schirmacher P, Breuhahn K: Coordinated expression of stathmin family members by far upstream sequence element-binding protein-1 increases motility in non-small cell lung cancer. Cancer Res 69(6): 2234-2243, 2009. DOI: 10.1158/0008- 5472.CAN-08-3338
20 Aronova A, Min IM, Crowley MJP, Panjwani SJ, Finnerty BM, Scognamiglio T, Liu YF, Whitsett TG, Garg S, Demeure MJ, Elemento O, Zarnegar R, Fahey TJ III: STMN1 is overexpressed in adrenocortical carcinoma and promotes a more aggressive phenotype in vitro. Ann Surg Oncol 25(3): 792-800, 2018. DOI: 10.1245/s10434-017-6296-2
21 Dos Santos Passaia B, Lima K, Kremer JL, da Conceição BB, de Paula Mariani BM, da Silva JCL, Zerbini MCN, Fragoso MCBV, Machado-Neto JA, Lotfi CFP: Stathmin 1 is highly expressed and associated with survival outcome in malignant adrenocortical tumours. Invest New Drugs 38(3): 899-908, 2020. DOI: 10.1007/s10637-019-00846-9
22 Peng L, Bian XW, Li DK, Xu C, Wang GM, Xia QY, Xiong Q: Large- scale RNA-Seq transcriptome analysis of 4043 cancers and 548 normal tissue controls across 12 TCGA cancer types. Sci Rep 5: 13413, 2015. DOI: 10.1038/srep13413
23 Chandrashekar DS, Karthikeyan SK, Korla PK, Patel H, Shovon AR, Athar M, Netto GJ, Qin ZS, Kumar S, Manne U, Creighton CJ, Varambally S: UALCAN: An update to the integrated cancer data analysis platform. Neoplasia 25: 18-27, 2022. DOI: 10.1016/j.neo.2022.01.001
24 Tang Z, Kang B, Li C, Chen T, Zhang Z: GEPIA2: an enhanced web server for large-scale expression profiling and interactive analysis. Nucleic Acids Res 47(W1): W556-W560, 2019. DOI: 10.1093/nar/gkz430
25 Tanaka Y, Yamashita S, Islam S, Kitagawa T, Tokuda K, Paudel D, Giri S, Ohta T, Harada F, Nagayasu H, Kuramitsu Y: Up- regulated DDX39 in adrenocortical carcinoma is associated with patient survival. Anticancer Res 45(2): 811-815, 2025. DOI: 10.21873/anticanres.17469
26 Yamashita SN, Tanaka Y, Islam S, Kitagawa T, Tokuda K, Paudel D, Giri S, Ohta T, Harada F, Nagayasu H, Kuramitsu Y: Increased expression of DDX39 in uveal melanoma is associated with patient prognosis. Anticancer Res 45(4): 1661-1666, 2025. DOI: 10.21873/anticanres.17547
27 Yamashita SN, Tanaka Y, Islam S, Kotake H, Tanaka M, Kitagawa T, Tokuda K, Paudel D, Giri S, Ohta T, Harada F, Nagayasu H, Kuramitsu Y: Elevated Stanniocalcin-1 expression in uveal melanoma predicts poor patient prognosis. Cancer Genomics Proteomics 22(4): 624-631, 2025. DOI: 10.21873/cgp.20526
28 Tang Z, Li C, Kang B, Gao G, Li C, Zhang Z: GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res 45(W1): W98-W102, 2017. DOI: 10.1093/nar/gkx247
29 Jourdain L, Curmi P, Sobel A, Pantaloni D, Carlier MF: Stathmin: a tubulin-sequestering protein which forms a ternary T2S complex with two tubulin molecules. Biochemistry 36(36): 10817-10821, 1997. DOI: 10.1021/bi971491b
30 Saadh MJ, Ahmed HH, Kareem RA, Chandra M, Monsi M, Walia C, Prasad GVS, Taher WM, Alwan M, Jawad MJ, Hamad AK: From motor proteins to oncogenic factors: the evolving role of kinesin superfamily proteins in breast cancer development. Mol Biotechnol, 2025. DOI: 10.1007/s12033-025-01428-2
31 Maurin J, Blangy A, Bompard G: Regulation of invadosomes by microtubules: Not only a matter of railways. Eur J Cell Biol 99(7): 151109, 2020. DOI: 10.1016/j.ejcb.2020.151109
32 Bièche I, Lachkar S, Becette V, Cifuentes-Diaz C, Sobel A, Lidereau R, Curmi PA: Overexpression of the stathmin gene in a subset of human breast cancer. Br J Cancer 78(6): 701- 709, 1998. DOI: 10.1038/bjc.1998.565
33 Price DK, Ball JR, Bahrani-Mostafavi Z, Vachris JC, Kaufman JS, Naumann RW, Higgins RV, Hall JB: The phosphoprotein Op18/Stathmin is differentially expressed in ovarian cancer. Cancer Invest 18(8): 722-730, 2000. DOI: 10.3109/0735790 0009012204
34 Roos G, Brattsand G, Landberg G, Marklund U, Gullberg M: Expression of oncoprotein 18 in human leukemias and lymphomas. Leukemia 7(10): 1538-1546, 1993.
35 Yan L, Dong X, Gao J, Liu F, Zhou L, Sun Y, Zhao X: A novel rapid quantitative method reveals stathmin-1 as a promising marker for esophageal squamous cell carcinoma. Cancer Med 7(5): 1802-1813, 2018. DOI: 10.1002/cam4.1449
36 Biaoxue R, Hua L, Tian F, Wenlong G: Increased stathmin in serum as a potential tumor marker for lung adenocarcinoma. Jpn J Clin Oncol 47(7): 668-668, 2017. DOI: 10.1093/jjco/ hyx078
37 Maroun MC, Olivero O, Lipovich L, Stark A, Tait L, Bandyopadhyay S, Burke M, Zarbo R, Chitale D, David Nathanson S, Long M, Peebles C, Madrid FF: Anti-centrosome antibodies in breast cancer are the expression of autoimmunity. Immunol Res 60(2-3): 339-347, 2014. DOI: 10.1007/s12026-014-8582-4