Generic placeholder image

Current Cancer Drug Targets

Editor-in-Chief

ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

Research Article

PIWIL1 Promotes Malignant Progression of Papillary Thyroid Carcinoma by Inducing EVA1A Expression

Author(s): Lianyong Liu, Fengying Wu, Xiaoying Zhang* and Xiangqi Li*

Volume 24, Issue 2, 2024

Published on: 12 July, 2023

Page: [192 - 203] Pages: 12

DOI: 10.2174/1568009623666230703140510

Price: $65

conference banner
Abstract

Introduction: Papillary thyroid carcinoma (PTC) is the most common subtype of thyroid cancer. Previous studies have reported on the ectopic expression of P-element-induced wimpy testis ligand 1 (PIWIL1) in various human cancers, but its role in PTC progression has not been investigated.

Methods: In this study, we measured the expression levels of PIWIL1 and Eva-1 homolog A (EVA1A) in PTC using qPCR and WB. We performed a viability assay to evaluate PTC cell proliferation and used flow cytometry to investigate apoptosis. Moreover, we conducted a Transwell invasion assay to quantify cell invasion and assessed PTC growth in vivo using xenograft tumor models.

Results: Our findings showed PIWIL1 to be highly expressed in PTC and promote cell proliferation, cell cycle activity, and cell invasion, while suppressing apoptosis. Additionally, PIWIL1 accelerated tumor growth in PTC xenografts by modulating the EVA1A expression.

Conclusion: Our study suggests that PIWIL1 contributes to the progression of PTC through EVA1A signaling, indicating its potential role as a therapeutic target for PTC. These results provide valuable insights into PIWIL1 function and may lead to more effective treatments for PTC.

Graphical Abstract

[1]
Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2017. CA Cancer J. Clin., 2017, 67(1), 7-30.
[http://dx.doi.org/10.3322/caac.21387] [PMID: 28055103]
[2]
Haugen, B.R.; Alexander, E.K.; Bible, K.C.; Doherty, G.M.; Mandel, S.J.; Nikiforov, Y.E.; Pacini, F.; Randolph, G.W.; Sawka, A.M.; Schlumberger, M.; Schuff, K.G.; Sherman, S.I.; Sosa, J.A.; Steward, D.L.; Tuttle, R.M.; Wartofsky, L. 2015 American thyroid association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: The american thyroid association guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid, 2016, 26(1), 1-133.
[http://dx.doi.org/10.1089/thy.2015.0020] [PMID: 26462967]
[3]
Saiselet, M.; Gacquer, D.; Spinette, A.; Craciun, L.; Decaussin-Petrucci, M.; Andry, G.; Detours, V.; Maenhaut, C. New global analysis of the microRNA transcriptome of primary tumors and lymph node metastases of papillary thyroid cancer. BMC Genomics, 2015, 16(1), 828.
[http://dx.doi.org/10.1186/s12864-015-2082-3] [PMID: 26487287]
[4]
Lundgren, C.I.; Hall, P.; Dickman, P.W.; Zedenius, J. Clinically significant prognostic factors for differentiated thyroid carcinoma. Cancer, 2006, 106(3), 524-531.
[http://dx.doi.org/10.1002/cncr.21653] [PMID: 16369995]
[5]
Xing, M. Molecular pathogenesis and mechanisms of thyroid cancer. Nat. Rev. Cancer, 2013, 13(3), 184-199.
[http://dx.doi.org/10.1038/nrc3431] [PMID: 23429735]
[6]
Tan, Y.; Liu, L.; Liao, M.; Zhang, C.; Hu, S.; Zou, M.; Gu, M.; Li, X. Emerging roles for PIWI proteins in cancer. Acta Biochim. Biophys. Sin. (Shanghai), 2015, 47(5), 315-324.
[http://dx.doi.org/10.1093/abbs/gmv018] [PMID: 25854579]
[7]
Liu, L.; Ren, L.; Shen, L.; Zhang, C.; Zhu, H.; Gu, M.; Li, X. Decreased expression of piR-35413 in human papillary thyroid cancer. Acta Biochim. Biophys. Sin., 2019, 51(12), 1293-1295.
[http://dx.doi.org/10.1093/abbs/gmz117] [PMID: 31774911]
[8]
Soukup, S.F.; Verstreken, P. PIWIL1 protein power targets tau therapy. Nat. Neurosci., 2014, 17(3), 334-335.
[http://dx.doi.org/10.1038/nn.3659] [PMID: 24569826]
[9]
Shen, S.; Yu, H.; Liu, X.; Liu, Y.; Zheng, J.; Wang, P.; Gong, W.; Chen, J.; Zhao, L.; Xue, Y. PIWIL1/piRNA-DQ593109 regulates the permeability of the blood-tumor barrier via the MEG3/miR-330-5p/RUNX3 axis. Mol. Ther. Nucleic Acids, 2018, 10, 412-425.
[http://dx.doi.org/10.1016/j.omtn.2017.12.020] [PMID: 29499952]
[10]
Van Tongelen, A.; Loriot, A.; De Smet, C. Oncogenic roles of DNA hypomethylation through the activation of cancer-germline genes. Cancer Lett., 2017, 396, 130-137.
[http://dx.doi.org/10.1016/j.canlet.2017.03.029] [PMID: 28342986]
[11]
Burger, K.; Schlackow, M.; Potts, M.; Hester, S.; Mohammed, S.; Gullerova, M. Nuclear phosphorylated Dicer processes double-stranded RNA in response to DNA damage. J. Cell Biol., 2017, 216(8), 2373-2389.
[http://dx.doi.org/10.1083/jcb.201612131] [PMID: 28642363]
[12]
Lu, L.; Katsaros, D.; Risch, H.A.; Canuto, E.M.; Biglia, N.; Yu, H. MicroRNA let-7a modifies the effect of self-renewal gene HIWI on patient survival of epithelial ovarian cancer. Mol. Carcinog., 2016, 55(4), 357-365.
[http://dx.doi.org/10.1002/mc.22285] [PMID: 25630839]
[13]
Chattopadhyay, T.; Biswal, P.; Lalruatfela, A.; Mallick, B. Emerging roles of PIWI-interacting RNAs (piRNAs) and PIWI proteins in head and neck cancer and their potential clinical implications. Biochim. Biophys. Acta Rev. Cancer, 2022, 1877(5), 188772.
[http://dx.doi.org/10.1016/j.bbcan.2022.188772] [PMID: 35931391]
[14]
Wang, L.; Yu, C.; Lu, Y.; He, P.; Guo, J.; Zhang, C.; Song, Q.; Ma, D.; Shi, T.; Chen, Y. TMEM166, a novel transmembrane protein, regulates cell autophagy and apoptosis. Apoptosis, 2007, 12(8), 1489-1502.
[http://dx.doi.org/10.1007/s10495-007-0073-9] [PMID: 17492404]
[15]
Chang, Y.; Li, Y.; Hu, J.; Guo, J.; Xu, D.; Xie, H.; Lv, X.; Shi, T.; Chen, Y. Adenovirus vector-mediated expression of TMEM166 inhibits human cancer cell growth by autophagy and apoptosis in vitro and in vivo. Cancer Lett., 2013, 328(1), 126-134.
[http://dx.doi.org/10.1016/j.canlet.2012.08.032] [PMID: 22960574]
[16]
Xie, H.; Hu, J.; Pan, H.; Lou, Y.; Lv, P.; Chen, Y. Adenovirus vector-mediated FAM176A overexpression induces cell death in human H1299 non-small cell lung cancer cells. BMB Rep., 2014, 47(2), 104-109.
[http://dx.doi.org/10.5483/BMBRep.2014.47.2.090] [PMID: 24257118]
[17]
Ren, W.W.; Li, D.D.; Chen, X.; Li, X.L.; He, Y.P.; Guo, L.H.; Liu, L.N.; Sun, L.P.; Zhang, X.P. MicroRNA-125b reverses oxaliplatin resistance in hepatocellular carcinoma by negatively regulating EVA1A mediated autophagy. Cell Death Dis., 2018, 9(5), 547.
[http://dx.doi.org/10.1038/s41419-018-0592-z] [PMID: 29749374]
[18]
Lin, B.Y.; Wen, J.L.; Zheng, C.; Lin, L.Z.; Chen, C.Z.; Qu, J.M. Eva‐1 homolog A promotes papillary thyroid cancer progression and epithelial‐mesenchymal transition via the Hippo signalling pathway. J. Cell. Mol. Med., 2020, 24(22), 13070-13080.
[http://dx.doi.org/10.1111/jcmm.15909] [PMID: 32969138]
[19]
Yoon, S.G.; Yi, J.W.; Seong, C.Y.; Kim, J.K.; Kim, S.J.; Chai, Y.J.; Choi, J.Y.; Lee, K.E. Clinical characteristics of papillary thyroid carcinoma arising from the pyramidal lobe. Ann. Surg. Treat. Res., 2017, 92(3), 123-128.
[http://dx.doi.org/10.4174/astr.2017.92.3.123] [PMID: 28289665]
[20]
Qiu, J.; Zhang, W.; Xia, Q.; Liu, F.; Li, L.; Zhao, S.; Gao, X.; Zang, C.; Ge, R.; Sun, Y. RNA sequencing identifies crucial genes in papillary thyroid carcinoma (PTC) progression. Exp. Mol. Pathol., 2016, 100(1), 151-159.
[http://dx.doi.org/10.1016/j.yexmp.2015.12.011] [PMID: 26708423]
[21]
Qiao, D.; Zeeman, A.M.; Deng, W.; Looijenga, L.H.J.; Lin, H. Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomas. Oncogene, 2002, 21(25), 3988-3999.
[http://dx.doi.org/10.1038/sj.onc.1205505] [PMID: 12037681]
[22]
Yousefi, B.; Sadoughi, F.; Asemi, Z.; Mansournia, M.A.; Hallajzadeh, J. Novel perspectives for the diagnosis and treatment of gynecological cancers using dysregulation of PIWI protein and PiRNAs as biomarkers. Curr. Med. Chem., 2023.
[PMID: 36786140]
[23]
Wang, N.; Tan, H.Y.; Lu, Y.; Chan, Y.T.; Wang, D.; Guo, W.; Xu, Y.; Zhang, C.; Chen, F.; Tang, G.; Feng, Y. PIWIL1 governs the crosstalk of cancer cell metabolism and immunosuppressive microenvironment in hepatocellular carcinoma. Signal Transduct. Target. Ther., 2021, 6(1), 86.
[http://dx.doi.org/10.1038/s41392-021-00485-8] [PMID: 33633112]
[24]
Shen, X.; Kan, S.; Liu, Z.; Lu, G.; Zhang, X.; Chen, Y.; Bai, Y. EVA1A inhibits GBM cell proliferation by inducing autophagy and apoptosis. Exp. Cell Res., 2017, 352(1), 130-138.
[http://dx.doi.org/10.1016/j.yexcr.2017.02.003] [PMID: 28185834]
[25]
Tao, M.; Shi, X.Y.; Yuan, C.H.; Hu, J.; Ma, Z.L.; Jiang, B.; Xiu, D.R.; Chen, Y.Y. Expression profile and potential roles of EVA1A in normal and neoplastic pancreatic tissues. Asian Pac. J. Cancer Prev., 2015, 16(1), 373-376.
[http://dx.doi.org/10.7314/APJCP.2015.16.1.373] [PMID: 25640383]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy