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Asian Journal of Surgery

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Asian Journal of Surgery

Letter to Editor

Prognostic value of spindle and kinetochore-related complex family and its correlation with immune cell infiltration in adrenocortical carcinoma

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To the Editor,

Adrenocortical carcinoma (ACC) originates from the adrenal cor- tex, with 0.5-2 new case per million people per year.1 Despite the low incidence of the ACC, many patients progress to metastasis at the initial diagnosis, which made them lose the precious chance of surgery.2 Thus, patients with ACC usually have a dismally poor prognosis. In order to solve this dilemma, scientists are striving to find powerful biomarkers and drugs to predict prognosis, and pro- vide new therapeutic options for patients with ACC. Spindle and kinetochore-related (SKA) complex family can establish and/or maintain the stability of kinetochore-microtubule interactions and spindle checkpoint silencing. However, the association of SKA family and adrenocortical carcinoma (ACC) has not been reported. To clarify the association of SKA family and ACC, we analyzed the expression, and diagnostic and prognostic value of the SKA family genes in patients with ACC using online database. In addition, GSCALite was used to screen drugs sensitive to SKA family.

We first reported that the expression level of SKA family genes was higher in ACC tumor tissues than normal adrenal tissue (Fig. 1A, P < 0.001). The expression of SKA family genes was signif- icantly different in metastasis, tumor status, pathological stage, T stage in patients with ACC (Table 1, P < 0.005). In particular, the SKA family genes not only had a high ROC value for the diagnosis of ACC (Fig. 1C), but also could distinguish the T stage (Fig. 1D) and the pathological stage (Fig. 1E). In terms of prognostic value,

the high expression of SKA family genes groups had significantly worse overall survival (OS) than the low expression groups (Fig. 1F-H).

Recently, tumor-associated immune cells have received wide- spread interest. In the present study, the expression of SKA family genes was negatively associated with the tumor infiltration of mast cells, cytotoxic cells, CD8+ T cells, and was positively corre- lated with Th2 cell level. In a study of childhood ACC, high CD8+ T cells counts was associated with younger patients and stage I dis- ease.3 Similarly, Landwehr et al4 reported that a high number of CD8+ T cells was also associated with better OS by analyzing 146 ACC samples. Our results indicated that the high expression of SKA family genes was strongly associated with a reduced infiltra- tion of CD8+ T cells. We might infer that overexpression of SKA family genes may inhibit the immune infiltration of CD8+ T cells.

Using the Gene Set Cancer Analysis (GSCA) database, we analyzed the associations between the expression of SKA family genes and their sensitivity to drug activity by calculating Pearson’s correlation coefficient (r > 0.2 and P < 0.001). Overall, trametinib was the only drug active against all genes in the SKA family (Fig. 1B).

Our findings suggested that the SKA family genes might serve as a new biomarker predicting diagnosis and overall survival for pa- tients with ACC. Trametinib might be the sensitive drug to SKA fam- ily. Moreover, SKA family were closely related to the infiltration of mast cells, CD8+ T cells, cytotoxic cells, and Th2 cells.

Fig. 1. (A) The expression of SKA family in the ACC and tumor-adjacent normal. (B) Correlation between GDSC drug sensitivity and mRNA expression of SKA family. The ROC curve of SKA family in ACC patients: (C) ACC, (D) Histological stage, (E) T stage tissues. The overall survival of SKA family in ACC patients: (F) SKA1, (G) SKA2, (H) SKA3. The correlative immune infiltration cells of (I) SKA1, (J) SKA2, (K) SKA3. ACC: adrenocortical carcinoma; SKA: spindle and kinetochore-associated.

A

B


Correlation between GDSC drug sensitivity and mRNA expression

6

J:

The expression levels Log2 (TPM+1)

SKA2

0

o

0

O

0

Correlation

4

Normal

-0.3

Tumor

0.0

Symbol

SKA1

0.4

FDR

2

== 0.05

>0.05

SKA3

0

17-AAG

PD-0325001

RDEA119

CI-1040

~BET-762

Mothobra

QL-2-24

AW/519

BMS345541

8X-912 CP466722

GSK1070816

GSK890693

Genentech Cod 10

W-7-24-

KIND01-102 NPK78-B-7KM

Nastoclax

OS1-02

PHA-793687

04-103 PIK.93

Qt-X-138

TG101348

TPCA-

Vorinostat

WZ3105

SKA1

SKA2

SKA3

THZ-2-102-

C

D

E

1.0

1.0

1.0

0.8

0.8

0.8

Sensitivity (TPR)

Sensitivity (TPR)

Sensitivity (TPR)

0.6

0.6

0.6

0.4

0.4

0.4

0.2

0.2

SKA1 (AUC = 0.709)

0.2

SKA1 (AUC = 0.818)

SKA1 (AUC = 0.702)

SKA2 (AUC = 0.755)

SKA2 (AUC = 0.684)

SKA2 (AUC = 0.713)

SKA3 (AUC = 0.780)

d

SKA3 (AUC = 0.772)

0.0

SKA3 (AUC = 0.834)

0.0

0.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

F

1-Specificity (FPR)

G

1-Specificity (FPR)

H

1-Specificity (FPR)

1.0

SKA1

1.0

SKA2

1.0

SKA3

Low

Low

Low

High

High

High

Survival probability

0.8

Survival probability

0.8

Survival probability

0.8

0.6

0.6

0.6

0.4

0.4

0.4

0.2

Overall Survival HR = 6.20 (2.48-15.47)

0.2

Overall Survival HR = 3.85 (1.67-8.84)

0.2

Overall Survival HR = 6.14 (2.46-15.30)

0.0

P < 0.001

0.0

P = 0.002

0.0

P < 0.001

0

50

100

150

0

50

100

150

0

50

100

150

Time (months)

J

Time (months)

K

Time (months)

Th2 cells

Th2 cells

The cells

T helper cells

T helper cells

T helper cells

aDC

Tgd

aDC

TReg

TReg

DC

aDC

TReg

Tgd

NK cells

NK cells

Tgd

P value

Tem

Tom

P value

DC

Tom

P value

PDC

0.75

0.75

Tem

Tem

0.75

NK CDG5dim cells

0.50

NK cells

0.50

PDC

0.25

NK CD56bright cells

0.50

Neutrophils

0 25

IDC

0.00

Th17 cells

Correlation

PDC

0.00

Eosinophils

0.25

0.00

IDC

02

Th17 cells

Neutrophils

Comolation

NK CD56dim cells

Comelation

Tom

0.4

0.2

DC

0.2

NK CD56dim cells

0.4

Neutrophils

0.4

Eosinophils

bud

T cells

Macrophages

DUB

DC

0.6

Thi cells

Eosinophils

TFH

NK CD56bright cells

B cells

Th17 cells

B cells

TFH

Thi cells

Macrophages

Thi cells

T cells

TFH

NK CD56bright cells

Macrophages

Mast cells

T cells

CDB T colls

CDS T cells

CD8 T cells

B cells

Cytotoxic cells

Cytotoxic cells

Mast cells

02

Mast cells

Cytotoxic cells

-0.4

-0.2

0.0

0.4

0.6

0.8

Correlation

-0.6

-0.4

-0.2

0.0

02

0.4

0.6

-0.4

-0.2

0.0

0.2

0.4

0.6

0.8

Correlation

Correlation

Table 1 The correlation between SKA1/2/3 expression and clinicopathological features in ACC patients in the UALCAN database.
Clinicopathologic featuresSKA1 (P value)SKA2 (P value)SKA3 (P value)
Age(years) ≤50 vs. >500.14210.907
Gender Female vs. Male10.1411
Laterality Left vs. Right0.7450.8970.745
T stage
T1-2 vs. T3-40.0080.0450.008
Lymph node involvement no vs. yes0.0870.1540.087
Metastasis no vs. yes0.0180.0250.018
Pathologic stage Stage I-II vs. Stage III-IV0.0130.0450.013
Tumor status Free vs. with tumor<0.001<0.001<0.001

ACC: adrenocortical carcinoma; SKA: spindle and kinetochore-associated; vs: versus.

Author contributions

QXY and DCF collected, reviewed the literature and wrote the manuscript. DXL and HHZ pointed out writing design and revised the manuscript. All authors read and approved the final manuscript.

Not applicable.

No consent is required because all data comes from online database.

Data availability statement

Not applicable.

Funding

None.

Declaration of competing interest

The authors declare that they have no known competing finan- cial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

None.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.asjsur.2022.10.098.

References

1. Fassnacht M, et al. Adrenocortical carcinomas and malignant phaeochromocyto- mas: ESMO-EURACAN Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2020;31(11):1476-1490.

2. Tian X, et al. Identification of tumor-infiltrating immune cells and prognostic validation of tumor-infiltrating mast cells in adrenocortical carcinoma: results from bioinformatics and real-world data. OncoImmunology. 2020;9(1), 1784529.

3. Parise IZS, et al. The prognostic role of CD8(+) T lymphocytes in childhood adre- nocortical carcinomas compared to ki-67, PD-1, PD-L1, and the weiss score. Can- cers. 2019;11(11).

4. Landwehr LS, et al. Interplay between glucocorticoids and tumor-infiltrating lymphocytes on the prognosis of adrenocortical carcinoma. J Immunother Cancer. 2020;8(1).

Qing-Xin Yu1

Department of Pathology, Taizhou Hospital, Wenzhou Medical University, Linhai, Zhejiang Province, 317000, China

De-Chao Feng1

Department of Urology, Institute of Urology, West China Hospital, Sichuan University, Chengdu, Sichuan Province, 610041, China

Deng-Xiong Li2,

Department of Urology, Institute of Urology, West China Hospital, Sichuan University, Chengdu, Sichuan Province, 610041, China

Hai-Hong Zheng”,2

Department of Pathology, Taizhou Hospital, Wenzhou Medical University, Linhai, Zhejiang Province, 317000, China

* Corresponding author.

Corresponding author.

E-mail address: lidengxiongwch@stu.scu.edu.cn (D .- X. Li).

E-mail address: zhenghh@enzemed.com (H .- H. Zheng).

14 October 2022 Available online 20 November 2022

1 These authors have contributed equally to this work and share first authorship.

2 These authors contributed equally to this work and should be consider as cor- responding authors.