Exosomal microRNA-301a-3p promotes the proliferation and invasion of nasopharyngeal carcinoma cells by targeting BTG1 mRNA

Cheng,Qiang; Li,Qiang; Xu,Lingen; Jiang,Hui

doi:10.3892/mmr.2021.11967

Exosomal microRNA-301a-3p promotes the proliferation and invasion of nasopharyngeal carcinoma cells by targeting BTG1 mRNA

Authors:
- Qiang Cheng
- Qiang Li
- Lingen Xu
- Hui Jiang
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Affiliations: Department of Otolaryngology, Jinshan Hospital Affiliated to Fudan University, Shanghai 201508, P.R. China
Published online on: March 8, 2021 https://doi.org/10.3892/mmr.2021.11967
Article Number: 328
Copyright: © Cheng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Aberrant microRNA (miRNA/miR) expression plays an important role in the pathogenesis of nasopharyngeal carcinoma (NPC). In the present study, the role and underlying molecular mechanism of miR‑301a‑3p in NPC cells were determined. It was observed that miR‑301a‑3p upregulation promoted NPC cell proliferation, migration, invasion and epithelial‑mesenchymal transition in vitro, whereas its downregulation resulted in the opposite effect. B‑cell translocation gene 1 (BTG1) mRNA was identified as the novel target of miR‑301a‑3p. BTG1 overexpression partially attenuated miR‑301a‑3p‑induced increase in cell proliferation and invasion. miR‑301a‑3p can be transferred by exosomes and positively regulate the proliferation and invasion of NPC cells. Altogether, the present study highlights that exosomal miR‑301a‑3p can promote NPC cell proliferation and invasion by repressing BTG1, thereby resulting in the development of NPC.

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1	Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ and He J: Cancer statistics in China, 2015. CA Cancer J Clin. 66:115–132. 2016. View Article : Google Scholar : PubMed/NCBI
2	Liang TS, Zheng YJ, Wang J, Zhao JY, Yang DK and Liu ZS: MicroRNA-506 inhibits tumor growth and metastasis in nasopharyngeal carcinoma through the inactivation of the Wnt/β-catenin signaling pathway by down-regulating LHX2. J Exp Clin Cancer Res. 38:972019. View Article : Google Scholar : PubMed/NCBI
3	Kong YW, Ferland-McCollough D, Jackson TJ and Bushell M: microRNAs in cancer management. Lancet Oncol. 13:e249–e258. 2012. View Article : Google Scholar : PubMed/NCBI
4	Filipowicz W, Bhattacharyya SN and Sonenberg N: Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat Rev Genet. 9:102–114. 2008. View Article : Google Scholar : PubMed/NCBI
5	Li B, Xu WW, Han L, Chan KT, Tsao SW, Lee NP, Law S, Xu LY, Li EM, Chan KW, et al: MicroRNA-377 suppresses initiation and progression of esophageal cancer by inhibiting CD133 and VEGF. Oncogene. 36:3986–4000. 2017. View Article : Google Scholar : PubMed/NCBI
6	Zheng Z, Qu JQ, Yi HM, Ye X, Huang W, Xiao T, Li JY, Wang YY, Feng J, Zhu JF, et al: MiR-125b regulates proliferation and apoptosis of nasopharyngeal carcinoma by targeting A20/NF-κB signaling pathway. Cell Death Dis. 8:e28552017. View Article : Google Scholar : PubMed/NCBI
7	Ye SB, Zhang H, Cai TT, Liu YN, Ni JJ, He J, Peng JY, Chen QY, Mo HY, Jun-Cui, et al: Exosomal miR-24-3p impedes T-cell function by targeting FGF11 and serves as a potential prognostic biomarker for nasopharyngeal carcinoma. J Pathol. 240:329–340. 2016. View Article : Google Scholar : PubMed/NCBI
8	Bao L, You B, Shi S, Shan Y, Zhang Q, Yue H, Zhang J, Zhang W, Shi Y, Liu Y, et al: Metastasis-associated miR-23a from nasopharyngeal carcinoma-derived exosomes mediates angiogenesis by repressing a novel target gene TSGA10. Oncogene. 37:2873–2889. 2018. View Article : Google Scholar : PubMed/NCBI
9	Li X, Zhong M, Wang J, Wang L, Lin Z, Cao Z, Huang Z, Zhang F, Li Y, Liu M, et al: miR-301a promotes lung tumorigenesis by suppressing Runx3. Mol Cancer. 18:992019. View Article : Google Scholar : PubMed/NCBI
10	Hu H, Zhang Q, Chen W, Wu T, Liu S, Li X, Luo B, Zhang T, Yan G, Lu H, et al: MicroRNA-301a promotes pancreatic cancer invasion and metastasis through the JAK/STAT3 signaling pathway by targeting SOCS5. Carcinogenesis. 41:502–514. 2020. View Article : Google Scholar : PubMed/NCBI
11	Li X, Li J, Cai Y, Peng S, Wang J, Xiao Z, Wang Y, Tao Y, Li J, Leng Q, et al: Hyperglycaemia-induced miR-301a promotes cell proliferation by repressing p21 and Smad4 in prostate cancer. Cancer Lett. 418:211–220. 2018. View Article : Google Scholar : PubMed/NCBI
12	Yue X, Lan F and Xia T: Hypoxic glioma cell-secreted exosomal miR-301a activates Wnt/β-catenin signaling and promotes radiation resistance by targeting TCEAL7. Mol Ther. 27:1939–1949. 2019. View Article : Google Scholar : PubMed/NCBI
13	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
14	Lu J, Liu QH, Wang F, Tan JJ, Deng YQ, Peng XH, Liu X, Zhang B, Xu X and Li XP: Exosomal miR-9 inhibits angiogenesis by targeting MDK and regulating PDK/AKT pathway in nasopharyngeal carcinoma. J Exp Clin Cancer Res. 37:1472018. View Article : Google Scholar : PubMed/NCBI
15	Wang YG, Wang T, Shi M and Zhai B: Long noncoding RNA EPB41L4A-AS2 inhibits hepatocellular carcinoma development by sponging miR-301a-5p and targeting FOXL1. J Exp Clin Cancer Res. 38:1532019. View Article : Google Scholar : PubMed/NCBI
16	Lettlova S, Brynychova V, Blecha J, Vrana D, Vondrusova M, Soucek P and Truksa J: MiR-301a-3p suppresses estrogen signaling by directly inhibiting ESR1 in ERα positive breast cancer. Cell Physiol Biochem. 46:2601–2615. 2018. View Article : Google Scholar : PubMed/NCBI
17	Xia X, Zhang K, Luo G, Cen G, Cao J, Huang K and Qiu Z: Downregulation of miR-301a-3p sensitizes pancreatic cancer cells to gemcitabine treatment via PTEN. Am J Transl Res. 9:1886–1895. 2017.PubMed/NCBI
18	Yuniati L, Scheijen B, van der Meer LT and van Leeuwen FN: Tumor suppressors BTG1 and BTG2: Beyond growth control. J Cell Physiol. 234:5379–5389. 2019. View Article : Google Scholar : PubMed/NCBI
19	Sun GG, Wang YD, Cheng YJ and Hu WN: The expression of BTG1 is downregulated in nasopharyngeal carcinoma and possibly associated with tumour metastasis. Mol Biol Rep. 41:5979–5988. 2014. View Article : Google Scholar : PubMed/NCBI
20	Kalluri R and LeBleu VS: The biology, function, and biomedical applications of exosomes. Science. 367:eaau69772020. View Article : Google Scholar : PubMed/NCBI
21	Kalluri R: The biology and function of exosomes in cancer. J Clin Invest. 126:1208–1215. 2016. View Article : Google Scholar : PubMed/NCBI
22	Wang X, Luo G, Zhang K, Cao J, Huang C, Jiang T, Liu B, Su L and Qiu Z: Hypoxic tumor-derived exosomal miR-301a mediates M2 macrophage polarization via PTEN/PI3Kγ to promote pancreatic cancer metastasis. Cancer Res. 78:4586–4598. 2018. View Article : Google Scholar : PubMed/NCBI
23	Lan F, Qing Q, Pan Q, Hu M, Yu H and Yue X: Serum exosomal miR-301a as a potential diagnostic and prognostic biomarker for human glioma. Cell Oncol (Dordr). 41:25–33. 2018. View Article : Google Scholar : PubMed/NCBI