miR-214 regulates papillary thyroid carcinoma cell proliferation and metastasis by targeting PSMD10

Liu,Fangzhou; Lou,Kexin; Zhao,Xiaotong; Zhang,Jia; Chen,Wei; Qian,Yichun; Zhao,Yanbin; Zhu,Yan; Zhang,Yuan

doi:10.3892/ijmm.2018.3902

miR-214 regulates papillary thyroid carcinoma cell proliferation and metastasis by targeting PSMD10

Authors:
- Fangzhou Liu
- Kexin Lou
- Xiaotong Zhao
- Jia Zhang
- Wei Chen
- Yichun Qian
- Yanbin Zhao
- Yan Zhu
- Yuan Zhang
View Affiliations

Affiliations: Department of Head and Neck Surgery, Jiangsu Cancer Hospital, Jiangsu Institute of Cancer Research, The Affiliated Cancer Hospital of Nanjing Medical University, Nanjing, Jiangsu 210000, P.R. China, Department of Pathology, Jiangsu Cancer Hospital, Jiangsu Institute of Cancer Research, The Affiliated Cancer Hospital of Nanjing Medical University, Nanjing, Jiangsu 210000, P.R. China, Department of Otorhinolaryngology and Head and Neck Surgery, Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu 221000, P.R. China, PET‑CT Center, Jiangsu Cancer Hospital, Jiangsu Institute of Cancer Research, The Affiliated Cancer Hospital of Nanjing Medical University, Nanjing, Jiangsu 210000, P.R. China, Department of Pathology, Jiangsu Province People's Hospital, Nanjing, Jiangsu 210000, P.R. China
Published online on: September 27, 2018 https://doi.org/10.3892/ijmm.2018.3902
Pages: 3027-3036
Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

MicroRNAs (miRNAs) have important effects on cancer occurrence and development by adjusting gene expression. The aim of the present study was to examine the role of miR‑214 in papillary thyroid carcinoma cell proliferation and metastasis, and its molecular mechanisms. miR‑214 was demonstrated to be markedly downregulated in papillary thyroid carcinoma tissues and cells compared with normal, and this was significantly associated with lymph node metastasis, tumor size and TNM stage. Upregulation of miR‑214 significantly decreased cell proliferation, and promoted cell apoptosis and cell cycle arrest in papillary thyroid carcinoma cell lines in vitro. By contrast, downregulation of miR‑214 resulted in the opposite effects. In addition, miR‑214 mimics significantly decreased papillary thyroid carcinoma cell migration and invasion, which was correlated with decreased expression levels of matrix metallopeptidase (MMP)‑2 and MMP‑9. Restoration of miR‑214 expression in papillary thyroid carcinoma cells decreased the activities associated with epithelial‑mesenchymal transition (EMT). Furthermore, proteasome 26S subunit non‑ATPase 10 (PSMD10) was predicted to be a target of miR‑214. Experimental results demonstrated that miR‑214 negatively regulated PSMD10 expression by targeting its 3' untranslated region directly. Knockdown of PSMD10 reduced papillary thyroid carcinoma cell clone formation, migration and invasion, most likely by repressing glycogen synthase kinase (GSK)‑3β/β‑catenin and AKT signaling. Finally, a negative correlation was observed between the expression levels of miR‑214 and PSMD10 in papillary thyroid carcinoma tissues. Taken together, these data suggested that miR‑214 might be a candidate target for the treatment of papillary thyroid carcinoma.

View Figures

View References

1	Chen AY, Jemal A and Ward EM: Increasing incidence of differentiated thyroid cancer in the United States, 1988–2005. Cancer. 115:3801–3807. 2009. View Article : Google Scholar : PubMed/NCBI
2	Davies L and Welch HG: Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA. 295:2164–2167. 2006. View Article : Google Scholar : PubMed/NCBI
3	Voutilainen PE, Multanen MM, Leppäniemi AK, Haglund CH, Haapiainen RK and Franssila KO: Prognosis after lymph node recurrence in papillary thyroid carcinoma depends on age. Thyroid. 11:953–957. 2001. View Article : Google Scholar : PubMed/NCBI
4	Chou CK, Chen RF, Chou FF, Chang HW, Chen YJ, Lee YF, Yang KD, Cheng JT, Huang CC and Liu RT: miR-146b is highly expressed in adult papillary thyroid carcinomas with high risk features including extrathyroidal invasion and the BRAF(V600E) mutation. Thyroid. 20:489–494. 2010. View Article : Google Scholar : PubMed/NCBI
5	Brown RL, de Souza JA and Cohen EE: Thyroid cancer: Burden of illness and management of disease. J Cancer. 2:193–199. 2011. View Article : Google Scholar : PubMed/NCBI
6	Chou CK, Yang KD, Chou FF, Huang CC, Lan YW, Lee YF, Kang HY and Liu RT: Prognostic implications of miR-146b expression and its functional role in papillary thyroid carcinoma. J Clin Endocrinol Metab. 98:E196–E205. 2013. View Article : Google Scholar
7	Jazdzewski K, Liyanarachchi S, Swierniak M, Pachucki J, Ringel MD, Jarzab B and de la Chapelle A: Polymorphic mature microRNAs from passenger strand of pre-miR-146a contribute to thyroid cancer. Proc Natl Acad Sci USA. 106:1502–1505. 2009. View Article : Google Scholar : PubMed/NCBI
8	Li M, Teruya-Feldstein J and Weinberg RA: Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 449:682–688. 2007. View Article : Google Scholar
9	Vriens MR, Weng JL, Suh I, Huynh N, Guerrero MA, Shen WT, Duh QY, Clark OH and Kebebew E: MicroRNA expression profiling is a potential diagnostic tool for thyroid cancer. Cancer. 118:3426–3432. 2012. View Article : Google Scholar
10	Zhong L, Sun S, Shi J, Cao F, Han X and Chen Z: MicroRNA-125a 5p plays a role as a tumor suppressor in lung carcinoma cells by directly targeting STAT3. Tumor Biol. 39:10104283176975792017. View Article : Google Scholar
11	Dong W, Li B, Wang J, Song Y, Zhang Z and Fu C: MicroRNA-337 inhibits cell proliferation and invasion of cervical cancer through directly targeting specificity protein 1. Tumor Biol. 39:10104283177113232017. View Article : Google Scholar
12	Wang P, Chen S, Fang H, Wu X, Chen D, Peng L, Gao Z and Xie C: miR-214/199a/199a^* cluster levels predict poor survival in hepatocellular carcinoma through interference with cell-cycle regulators. Oncotarget. 7:929–945. 2016.
13	Zhang J, Su B, Gong C, Xi Q and Chao T: miR-214 promotes apoptosis and sensitizes breast cancer cells to doxorubicin by targeting the RFWD2-p53 cascade. Biochem Bioph Res Co. 478:337–342. 2016. View Article : Google Scholar
14	Peng R, Men J, Ma R, Wang Q, Wang Y, Sun Y and Ren J: miR-214 down-regulates ARL2 and suppresses growth and invasion of cervical cancer cells. Biochem Bioph Res Co. 484:623–630. 2017. View Article : Google Scholar
15	Penna E, Orso F and Taverna D: miR-214 as a key hub that controls cancer networks: Small player, multiple functions. J Invest Dermatol. 135:960–969. 2015. View Article : Google Scholar
16	Hori T, Kato S, Saeki M, DeMartino GN, Slaughter CA, Takeuchi J, Toh-e A and Tanaka K: cDNA cloning and functional analysis of p28 (Nas6p) and p40.5 (Nas7p), two novel regulatory subunits of the 26S proteasome. Gene. 216:113–122. 1998. View Article : Google Scholar : PubMed/NCBI
17	Higashitsuji H, Itoh K, Nagao T, Dawson S, Nonoguchi K, Kido T, Mayer RJ, Arii S and Fujita J: Reduced stability of retinoblastoma protein by gankyrin, an oncogenic ankyrin-repeat protein overexpressed in hepatomas. Nat Med. 6:96–99. 2000. View Article : Google Scholar
18	Zhen C, Chen L, Zhao Q, Liang B, Gu YX, Bai ZF, Wang K, Xu X, Han QY, Fang DF, et al: Gankyrin promotes breast cancer cell metastasis by regulating Rac1 activity. Oncogene. 32:3452–3460. 2000. View Article : Google Scholar
19	Meng Y, He L, Guo X, Tang S, Zhao X, Du R, Jin J, Bi Q, Li H, Nie Y, et al: Gankyrin promotes the proliferation of human pancreatic cancer. Cancer Lett. 297:9–17. 2010. View Article : Google Scholar : PubMed/NCBI
20	Uddin MH, Choi MH, Kim WH, Jang JJ and Hong ST: Involvement of PSMD10, CDK4, and tumor suppressors in development of intrahepatic cholangiocarcinoma of syrian golden hamsters induced by clonorchis sinensis and N-Nitrosodimethylamine. PLoS Negl Trop Dis. 9:e00040082015. View Article : Google Scholar : PubMed/NCBI
21	Edge SB, Byrd DR, Compton CC, Fritz AG and Greene FL: AJCC cancer staging manual. 7th edition. Springer; New York, NY: 2010
22	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−delta delta C(T)) methods. Methods. 25:420–408. 2001. View Article : Google Scholar
23	Agarwal V, Bell GW, Nam J and Bartel DP: Predicting effective microRNA target sites in mammalian mRNAs. Elife. 4:e050052015. View Article : Google Scholar :
24	Xia H, Ooi LL and Hui KM: MiR-214 targets β-catenin pathway to suppress invasion, stem-like traits and recurrence of human hepatocellular harcinoma. PLoS One. 7:e442062012. View Article : Google Scholar
25	Mitra AK, Zillhardt M, Hua Y, Tiwari P, Murmann AE, Peter ME and Lengyel E: MicroRNAs reprogram normal fibroblasts into cancer-associated fibroblasts in ovarian cancer. Cancer Discov. 2:1100–1108. 2012. View Article : Google Scholar : PubMed/NCBI
26	Wang F, Liu M, Li X and Tang H: MiR-214 reduces cell survival and enhances cisplatin-induced cytotoxicity via down-regulation of Bcl2l2 in cervical cancer cells. FEBS Lett. 587:488–495. 2013. View Article : Google Scholar : PubMed/NCBI
27	Srivastava A, Goldberger H, Dimtchev A, Ramalinga M, Chijioke J, Marian C, Oermann EK, Uhm S, Kim JS, Chen LN, et al: MicroRNA profiling in prostate cancer-the diagnostic potential of urinary miR-205 and miR-214. PLoS One. 8:e769942013. View Article : Google Scholar
28	Yang TS, Yang XH, Wang XD, Wang YL, Zhou B and Song ZS: MiR-214 regulate gastric cancer cell proliferation, migration and invasion by targeting PTEN. Cancer Cell Int. 13:682013. View Article : Google Scholar : PubMed/NCBI
29	Derfoul A, Juan AH, Difilippantonio MJ, Palanisamy N, Ried T and Sartorelli V: Decreased microRNA-214 levels in breast cancer cells coincides with increased cell proliferation, invasion and accumulation of the Polycomb Ezh2 methyltransferase. Carcinogenesis. 32:1607–1614. 2011. View Article : Google Scholar : PubMed/NCBI
30	Duan Q, Wang X, Gong W, Ni L, Chen C, He X, Chen F, Yang L, Wang P and Wang DW: ER stress negatively modulates the expression of the miR-199a/214 cluster to regulates tumor survival and progression in human hepatocellular cancer. PLoS One. 7:e315182012. View Article : Google Scholar : PubMed/NCBI
31	Misiewicz-Krzeminska I, Sarasquete ME, Quwaider D, Krzeminski P, Ticona FV, Paino T, Delgado M, Aires A, Ocio EM, Garcia-Sanz R, et al: Restoration of microRNA-214 expression reduces growth of myeloma cells through positive regulation of P53 and inhibition of DNA replication. Haematologica. 98:640–648. 2013. View Article : Google Scholar :
32	Huang SD, Yuan Y, Zhuang CW, Li BL, Gong DJ, Wang SG, Zeng ZY and Cheng HZ: MicroRNA-98 and microRNA-214 post-transcriptionally regulate enhancer of zeste homolog 2 and inhibit migration and invasion in human esophageal squamous cell carcinoma. Mol Cancer. 11:512012. View Article : Google Scholar : PubMed/NCBI
33	Penna E, Orso F, Cimino D, Tenaglia E, Lembo A, Quaglino E, Poliseno L, Haimovic A, Osella-Abate S, De Pittà C, et al: microRNA-214 contributes to melanoma tumour progression through suppression of TFAP2C. EMBO J. 30:1990–2007. 2011. View Article : Google Scholar : PubMed/NCBI
34	Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, et al: A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 103:2257–2261. 2006. View Article : Google Scholar : PubMed/NCBI
35	Chen DL, Wang ZQ, Zeng ZL, Wu WJ, Zhang DS, Luo HY, Wang F, Qiu MZ, Wang DS, Ren C, et al: Identification of microRNA-214 as a negative regulator of colorectal cancer liver metastasis via regulation of fibroglast growth factor 1 expression. Hepatology. 60:598–609. 2014. View Article : Google Scholar : PubMed/NCBI
36	He F, Chen H, Yang P, Wu Q, Zhang T, Wang C, Wei J, Chen Z, Hu H, Li W and Cao J: Gankyrin sustains PI3K/GSK-3β/β-catenin signal activation and promotes colorectal cancer aggressiveness and progression. Oncotarget. 7:81156–81171. 2016. View Article : Google Scholar : PubMed/NCBI