Expression of the ChrXq27.3 MiRNA Cluster in Recurrent Ovarian Clear Cell Carcinoma and Its Impact on Cisplatin Resistance

Overview

Journal Oncogene

Specialties Molecular Biology
Oncology

Date 2021 Jan 9

PMID 33420363

Citations 12

Authors

Kosuke Yoshida

Akira Yokoi

Mai Sugiyama

Shingo Oda

Kazuhisa Kitami

Satoshi Tamauchi

Yoshiki Ikeda

Nobuhisa Yoshikawa

Kimihiro Nishino

Kaoru Niimi

Shiro Suzuki

Fumitaka Kikkawa

Tsuyoshi Yokoi

Hiroaki Kajiyama

Affiliations

Soon will be listed here.

Abstract

Ovarian clear cell carcinoma (OCCC) is a histological subtype of epithelial ovarian cancer and exhibits dismal prognosis due to chemoresistance. Moreover, only few effective therapeutic options exist for patients with recurrent OCCC, and an understanding of its molecular characteristics is essential for the development of novel therapeutic approaches. In the present study, we investigated unique MicroRNAs (miRNA) profiles in recurrent/metastatic OCCC and the role of miRNAs in cisplatin resistance. Comprehensive miRNA sequencing revealed that expression of several miRNAs, including miR-508-3p, miR-509-3p, miR-509-3-5p, and miR-514a-3p was remarkably less in recurrent cancer tissues when compared with that in paired primary cancer tissues. These miRNAs are located in the chrXq27.3 region on the genome. Moreover, its expression was negative in omental metastases in two patients with advanced OCCC. In vitro analyses revealed that overexpression of miR-509-3p and miR-509-3-5p reversed cisplatin resistance and yes-associated protein 1 (YAP1) was partially responsible for the resistance. Immunohistochemistry revealed that YAP1 expression was inversely correlated with the chrXq27.3 miRNA cluster expression. In conclusion, these findings suggest that alteration of the chrXq27.3 miRNA cluster could play a critical role in chemoresistance and miRNAs in the cluster and their target genes can be potential therapeutic targets.

Citing Articles

CypA/TAF15/STAT5A/miR-514a-3p feedback loop drives ovarian cancer metastasis.

Li Y, Yang H, Li A, Chen B, Wang Y, Song Z Oncogene. 2024; 43(49):3570-3585.

PMID: 39402372 DOI: 10.1038/s41388-024-03188-w.

Drug resistance in ovarian cancer: from mechanism to clinical trial.

Wang L, Wang X, Zhu X, Zhong L, Jiang Q, Wang Y Mol Cancer. 2024; 23(1):66.

PMID: 38539161 PMC: 10976737. DOI: 10.1186/s12943-024-01967-3.

Baicalein improves the chemoresistance of ovarian cancer through regulation of CirSLC7A6.

Li S, Yi Z, Li M, Zhu Z J Ovarian Res. 2023; 16(1):212.

PMID: 37940982 PMC: 10631197. DOI: 10.1186/s13048-023-01285-0.

Study of MicroRNA Cluster Located on Chromosome X in Serum and Breast Cancer Tissue.

Rasool A, Haghi M, Feizi M Biochem Genet. 2023; 62(2):1115-1135.

PMID: 37544000 DOI: 10.1007/s10528-023-10448-z.

The downregulation of miR-509-3p expression by collagen type XI alpha 1-regulated hypermethylation facilitates cancer progression and chemoresistance via the DNA methyltransferase 1/Small ubiquitin-like modifier-3 axis in ovarian cancer cells.

Wu Y, Huang Y, Wu P, Chang T, Huang S, Chou C J Ovarian Res. 2023; 16(1):124.

PMID: 37386587 PMC: 10308652. DOI: 10.1186/s13048-023-01191-5.

References

Torre L, Bray F, Siegel R, Ferlay J, Lortet-Tieulent J, Jemal A . Global cancer statistics, 2012. CA Cancer J Clin. 2015; 65(2):87-108. DOI: 10.3322/caac.21262. View

Anglesio M, Carey M, Kobel M, MacKay H, Huntsman D . Clear cell carcinoma of the ovary: a report from the first Ovarian Clear Cell Symposium, June 24th, 2010. Gynecol Oncol. 2011; 121(2):407-15. DOI: 10.1016/j.ygyno.2011.01.005. View

Jayson G, Kohn E, Kitchener H, Ledermann J . Ovarian cancer. Lancet. 2014; 384(9951):1376-88. DOI: 10.1016/S0140-6736(13)62146-7. View

Ambros V . The functions of animal microRNAs. Nature. 2004; 431(7006):350-5. DOI: 10.1038/nature02871. View

Calin G, Sevignani C, Dumitru C, Hyslop T, Noch E, Yendamuri S . Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci U S A. 2004; 101(9):2999-3004. PMC: 365734. DOI: 10.1073/pnas.0307323101. View

Esquela-Kerscher A, Slack F . Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer. 2006; 6(4):259-69. DOI: 10.1038/nrc1840. View

Mendes N, Freitas A, Sagot M . Current tools for the identification of miRNA genes and their targets. Nucleic Acids Res. 2009; 37(8):2419-33. PMC: 2677885. DOI: 10.1093/nar/gkp145. View

Garzon R, Calin G, Croce C . MicroRNAs in Cancer. Annu Rev Med. 2009; 60:167-79. DOI: 10.1146/annurev.med.59.053006.104707. View

Mihanfar A, Fattahi A, Nejabati H . MicroRNA-mediated drug resistance in ovarian cancer. J Cell Physiol. 2017; 234(4):3180-3191. DOI: 10.1002/jcp.26060. View

10.

Ghafouri-Fard S, Shoorei H, Taheri M . miRNA profile in ovarian cancer. Exp Mol Pathol. 2020; 113:104381. DOI: 10.1016/j.yexmp.2020.104381. View

11.

Ramaiah M, Tan K, Plank T, Song H, Chousal J, Jones S . A microRNA cluster in the Fragile-X region expressed during spermatogenesis targets FMR1. EMBO Rep. 2018; 20(2). PMC: 6362356. DOI: 10.15252/embr.201846566. View

12.

Zhou Y, Hu Y, Sun Q, Xie N . Non-coding RNA in Fragile X Syndrome and Converging Mechanisms Shared by Related Disorders. Front Genet. 2019; 10:139. PMC: 6405884. DOI: 10.3389/fgene.2019.00139. View

13.

Wang J, Haubrock M, Cao K, Hua X, Zhang C, Wingender E . Regulatory coordination of clustered microRNAs based on microRNA-transcription factor regulatory network. BMC Syst Biol. 2011; 5:199. PMC: 3262773. DOI: 10.1186/1752-0509-5-199. View

14.

Zhai Q, Zhou L, Zhao C, Wan J, Yu Z, Guo X . Identification of miR-508-3p and miR-509-3p that are associated with cell invasion and migration and involved in the apoptosis of renal cell carcinoma. Biochem Biophys Res Commun. 2012; 419(4):621-6. DOI: 10.1016/j.bbrc.2012.02.060. View

15.

Streicher K, Zhu W, Lehmann K, Georgantas R, Morehouse C, Brohawn P . A novel oncogenic role for the miRNA-506-514 cluster in initiating melanocyte transformation and promoting melanoma growth. Oncogene. 2011; 31(12):1558-70. DOI: 10.1038/onc.2011.345. View

16.

Ozata D, Li X, Lee L, Liu J, Warsito D, Hajeri P . Loss of miR-514a-3p regulation of PEG3 activates the NF-kappa B pathway in human testicular germ cell tumors. Cell Death Dis. 2017; 8(5):e2759. PMC: 5520681. DOI: 10.1038/cddis.2016.464. View

17.

Yan T, Ren L, Shen C, Wang Z, Yu Y, Liang Q . miR-508 Defines the Stem-like/Mesenchymal Subtype in Colorectal Cancer. Cancer Res. 2018; 78(7):1751-1765. DOI: 10.1158/0008-5472.CAN-17-2101. View

18.

Wang X, Lu Y, Liang J, Cao J, Jin Y, An G . MiR-509-3-5p causes aberrant mitosis and anti-proliferative effect by suppression of PLK1 in human lung cancer A549 cells. Biochem Biophys Res Commun. 2016; 478(2):676-82. DOI: 10.1016/j.bbrc.2016.08.006. View

19.

Bagnoli M, De Cecco L, Granata A, Nicoletti R, Marchesi E, Alberti P . Identification of a chrXq27.3 microRNA cluster associated with early relapse in advanced stage ovarian cancer patients. Oncotarget. 2012; 2(12):1265-78. PMC: 3282083. DOI: 10.18632/oncotarget.401. View

20.

Nam E, Kim S, Lee T, Kim H, Lee J, Kim S . Primary and recurrent ovarian high-grade serous carcinomas display similar microRNA expression patterns relative to those of normal ovarian tissue. Oncotarget. 2016; 7(43):70524-70534. PMC: 5342571. DOI: 10.18632/oncotarget.12045. View