Hostname: page-component-6b989bf9dc-pkhfk Total loading time: 0 Render date: 2024-04-14T09:46:04.220Z Has data issue: false hasContentIssue false

lncRNA SNHG14 promotes the proliferation, migration, and invasion of thyroid tumour cells by regulating miR-93-5p

Published online by Cambridge University Press:  12 August 2021

Fang Tian
Affiliation:
Department of Endocrinology, Hangzhou Xixi Hospital Affiliated to Zhejiang University of Traditional Chinese Medicine, Hangzhou, Zhejiang, China
Huimin Ying
Affiliation:
Department of Endocrinology, Hangzhou Xixi Hospital Affiliated to Zhejiang University of Traditional Chinese Medicine, Hangzhou, Zhejiang, China
Shuaiju Liao
Affiliation:
Department of Endocrinology, BenQ Medical Center, Nanjing, Jiangsu, China
Yuanyuan Wang
Affiliation:
Department of Endocrinology, Hangzhou Xixi Hospital Affiliated to Zhejiang University of Traditional Chinese Medicine, Hangzhou, Zhejiang, China
Quansheng Wang*
Affiliation:
Department of Endocrinology, BenQ Medical Center, Nanjing, Jiangsu, China
*
*Author for correspondence: Quansheng Wang, Department of Endocrinology, BenQ Medical Center, The Affiliated BenQ Hospital of Nanjing Medical University, 71 Hexi Street, Jianye District, Nanjing City, Jiangsu Province, 210019, China. E-mail: chenguanghi231@163.com

Summary

Long non-coding RNAs (lncRNAs) exert vital functions in the occurrence and development of various tumours. The aim of this study was to examine the regulatory effect and underlying molecular mechanism of lncRNA small nucleolar RNA host gene 14 (SNHG14) on the proliferation, invasion and migration of thyroid tumour cells. The expression of SNHG14 in thyroid tumour cell lines was determined using qRT-PCR. CCK-8 and western blot were used to detect the effects of SNHG14 on proliferation and apoptosis of thyroid tumour cells. The effect of SNHG14 on the migration and invasion of thyroid tumour cells was analyzed using immunofluorescence, wound-healing and transwell assays. A targeting relationship between SNHG14 and miR-93-5p was determined using bioinformatics software and luciferase reporter assays. In addition, CCK-8, immunofluorescence, wound-healing and transwell assays were applied to demonstrate that SNHG14 promoted the proliferation, migration and invasion of thyroid tumour cells by targeting miR-93-5p. The biological function of SNHG14 in vivo was explored through a xenograft model and immunohistochemistry. SNHG14 was upregulated in thyroid tumour cells compared with normal cells. Downregulation of SNHG14 effectively reduced the proliferation, migration and invasion of TPC-1 cells, and induced cell apoptosis. Moreover, SNHG14 directly targeted miR-93-5p and there was a negative correlation between them. Further functional experiments illustrated that miR-93-5p overexpression dramatically reversed the promoting role of SNHG14 in proliferation, migration and invasion of TPC-1 cells. Our results demonstrated that SNHG14 promotes the proliferation, invasion and migration of thyroid tumour cells by downregulating miR-93-5p.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Deng, PC, Chen, WB, Cai, HH, An, Y, Wu, XQ, Chen, XM, Sun, DL, Yang, Y, Shi, LQ and Yang, Y (2019). LncRNA SNHG14 potentiates pancreatic cancer progression via modulation of annexin A2 expression by acting as a competing endogenous RNA for miR-613. J Cell Mol Med 23, 7222–32.Google ScholarPubMed
Di, W, Weinan, X, Xin, L, Zhiwei, Y, Xinyue, G, Jinxue, T and Mingqi, L (2019). Long noncoding RNA SNHG14 facilitates colorectal cancer metastasis through targeting EZH2-regulated EPHA7. Cell Death Dis 10, 514.Google ScholarPubMed
Fang, C, Zhu, DX, Dong, HJ, Zhou, ZJ, Wang, YH, Liu, L, Fan, L, Miao, KR, Liu, P, Xu, W and Li, JY (2012). Serum microRNAs are promising novel biomarkers for diffuse large B cell lymphoma. Ann Hematol 91, 553–9.Google ScholarPubMed
Han, MA and Kim, JH (2018). Diagnostic X-ray exposure and thyroid cancer risk: systematic review and meta-analysis. Thyroid 28, 220–8.CrossRefGoogle ScholarPubMed
Janjua, N and Wreesmann, VB (2018). Aggressive differentiated thyroid cancer. Eur J Surg Oncol 44, 367–77.CrossRefGoogle ScholarPubMed
Ji, N, Wang, Y, Bao, G, Yan, J and Ji, S (2019). LncRNA SNHG14 promotes the progression of cervical cancer by regulating miR-206/YWHAZ. Pathol Res Pract 215, 668–75.CrossRefGoogle ScholarPubMed
Kaufmann, SH and Earnshaw, WC (2000). Induction of apoptosis by cancer chemotherapy. Exp Cell Res 256, 42–9.Google ScholarPubMed
Kwok, ZH and Tay, Y (2017). Long noncoding RNAs: lincs between human health and disease. Biochem Soc Trans 45, 805–12.CrossRefGoogle ScholarPubMed
Li, L, Zhang, R and Li, SJ (2020). Long noncoding RNA SNHG14 promotes ovarian cancer cell proliferation and metastasis via sponging miR-219a-5p. Eur Rev Med Pharmacol Sci 24, 7541.Google ScholarPubMed
Lin, C and Yang, L (2018). Long noncoding RNA in cancer: wiring signaling circuitry. Trends Cell Biol 28, 287301.Google ScholarPubMed
Liu, G, Ye, Z, Zhao, X and Ji, Z (2017). SP1-induced up-regulation of lncRNA SNHG14 as a ceRNA promotes migration and invasion of clear cell renal cell carcinoma by regulating N-WASP. Am J Cancer Res 7, 2515–25.Google ScholarPubMed
Liu, N and Olson, EN (2010). MicroRNA regulatory networks in cardiovascular development. Dev Cell 18, 510–25.Google ScholarPubMed
Liu, Z, Yan, Y, Cao, S and Chen, Y (2018). Long non-coding RNA SNHG14 contributes to gastric cancer development through targeting miR-145/SOX9 axis. J Cell Biochem 119, 6905–13.Google ScholarPubMed
Maldotti, M, Incarnato, D, Neri, F, Krepelova, A, Rapelli, S, Anselmi, F, Parlato, C, Basile, G, Dettori, D, Calogero, R and Oliviero, S (2016). The long intergenic non-coding RNA CCR492 functions as a let-7 competitive endogenous RNA to regulate c-Myc expression. Biochim Biophys Acta 1859, 1322–32.Google Scholar
Nicholson, KJ and Yip, L (2018). An update on the status of molecular testing for the indeterminate thyroid nodule and risk stratification of differentiated thyroid cancer. Curr Opin Oncol 30, 815.Google ScholarPubMed
Quinn, JJ and Chang, HY (2016). Unique features of long non-coding RNA biogenesis and function. Nat Rev Genet 17, 4762.Google ScholarPubMed
Sun, W, Lan, X, Wang, Z, Dong, W, He, L, Zhang, T and Zhang, H (2016). Overexpression of long non-coding RNA NR_036575.1 contributes to the proliferation and migration of papillary thyroid cancer. Med Oncol 33, 102.CrossRefGoogle Scholar
Sun, XY, Han, XM, Zhao, XL, Cheng, XM and Zhang, Y (2019). MiR-93-5p promotes cervical cancer progression by targeting THBS2/MMPS signal pathway. Eur Rev Med Pharmacol Sci 23, 5113–21.Google ScholarPubMed
Wang, LY and Ganly, I (2018). Post-treatment surveillance of thyroid cancer. Eur J Surg Oncol 44, 357366.Google ScholarPubMed
Yang, J, Lin, J, Liu, T, Chen, T, Pan, S, Huang, W and Li, S (2014). Analysis of lncRNA expression profiles in non-small cell lung cancers (NSCLC) and their clinical subtypes. Lung Cancer 85, 110–15.CrossRefGoogle ScholarPubMed
Yang, W, Bai, J, Liu, D, Wang, S, Zhao, N, Che, R and Zhang, H (2018). MiR-93-5p up-regulation is involved in non-small cell lung cancer cells proliferation and migration and poor prognosis. Gene 647, 1320.Google ScholarPubMed
Zhang, H, Cai, Y, Zheng, L, Zhang, Z, Lin, X and Jiang, N (2018). LncRNA BISPR promotes the progression of thyroid papillary carcinoma by regulating miR-21-5p. Int J Immunopathol Pharmacol 32, 2058738418772652.Google ScholarPubMed
Zhang, H, Xu, HB, Kurban, E and Luo, HW (2020a). LncRNA SNHG14 promotes hepatocellular carcinoma progression via H3K27 acetylation activated PABPC1 by PTEN signaling. Cell Death Dis 11, 646.Google ScholarPubMed
Zhang, K, Cai, Y, Zhou, Q, Sun, H and Wei, J (2020b). Long non-coding RNA SNHG14 impedes viability, migration and invasion of endometrial carcinoma cells through modulating miR-93-5p/ZBTB7A axis. Cancer Manag Res 12, 9515–25.Google ScholarPubMed
Zhang, P, Li, J, Qi, Y, Zou, Y, Liu, L, Tang, X, Duan, J, Liu, H and Zeng, G (2016). Vitamin C promotes the proliferation of human adipose-derived stem cells via p53-p21 pathway. Organogenesis 12, 143–51.CrossRefGoogle ScholarPubMed
Zhang, W, Duan, W, Mo, Z, Wang, J, Yang, W, Wu, W, Li, X, Lin, S, Tan, Y and Wei, W (2020c). Upregulation of SNHG14 suppresses cell proliferation and metastasis of colorectal cancer by targeting miR-92b-3p. J Cell Biochem 121, 19982008.Google ScholarPubMed
Zhang, X, Zhang, J, Liu, W, Wang, Y, Wu, J, Zhao, S, Zhao, M and Peng, S. (2020d). Exploring the action of RGDV-gemcitabine on tumor metastasis, tumor growth and possible action pathway. Sci Rep 10, 15729.Google ScholarPubMed
Zhang, Y and Weinberg, RA (2018). Epithelial-to-mesenchymal transition in cancer: complexity and opportunities. Front Med 12, 361–73.Google ScholarPubMed
Zhang, YY, Li, M, Xu, YD and Shang, J (2019a). LncRNA SNHG14 promotes the development of cervical cancer and predicts poor prognosis. Eur Rev Med Pharmacol Sci 23, 3664–71.Google ScholarPubMed
Zhang, Z, Wang, Y, Zhang, W, Li, J, Liu, W and Lu, W (2019b). Long non-coding RNA SNHG14 exerts oncogenic functions in non-small cell lung cancer through acting as an miR-340 sponge. Biosci Rep 39, BSR20180941.Google ScholarPubMed