OIP5‑AS1 modulates epigenetic regulator HDAC7 to enhance non‑small cell lung cancer metastasis via miR‑140‑5p

Mei,Jiazhuan; Liu,Guiju; Wang,Wenhui; Xiao,Peng; Yang,Dan; Bai,Hua; Li,Ruijun

doi:10.3892/ol.2020.11868

OIP5‑AS1 modulates epigenetic regulator HDAC7 to enhance non‑small cell lung cancer metastasis via miR‑140‑5p

Authors:
- Jiazhuan Mei
- Guiju Liu
- Wenhui Wang
- Peng Xiao
- Dan Yang
- Hua Bai
- Ruijun Li
View Affiliations

Affiliations: Department of Oncology, People's Hospital of Zhengzhou, Zhengzhou, Henan 450000, P.R. China
Published online on: July 15, 2020 https://doi.org/10.3892/ol.2020.11868
Article Number: 7
Copyright: © Mei 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

Long non‑coding RNAs have been reported to be involved in non‑small cell lung cancer (NSCLC) progression. However, whether Opa‑interacting protein 5 antisense RNA 1 (OIP5‑AS1) serves a role in NSCLC remains unclear. Bioinformatics analysis of The Cancer Genome Atlas datasets showed clinical significance and relevance of OIP5‑AS1 in NSCLC. Western blotting and reverse transcription‑quantitative PCR revealed protein and RNA expression levels of the genes [including OIP5‑AS1, microRNA (miR)‑140‑5p, histone deacetylase 7 (HDAC7) and vascular endothelial growth factor A (VEGFA)]. Direct associations between the genes (miR‑140‑5p and OIP5‑AS1, or miR‑140‑5p and HDAC7) were confirmed using a dual‑luciferase reporter assay. Lymphatic vessel formation and invasion ability were detected using a lymphatic vessel formation assay and Transwell invasion assay. OIP5‑AS1 knockdown attenuated lymphatic vessel length and invasion. The role of OIP5‑AS1 was reverted by miR‑140‑5p. HDAC7 and VEGFA are downstream effectors of miR‑140‑5p‑mediated NSCLC metastasis. OIP5‑AS1, miR‑140‑5p, HDAC7 and VEGFA were all dysregulated in human clinical NSCLC tumor tissues. In conclusion, the present results demonstrated a novel mechanism for OIP5‑AS1‑induced metastatic phenotypes of NSCLC via the miR‑140‑5p/HDAC7/VEGFA axis.

View Figures

View References

1	Zhuang Y, Jiang H, Li H, Dai J, Liu Y, Li Y, Miao L, Cai H, Xiao Y, Xia H, et al: Down-regulation of long non-coding RNA AFAP1-AS1 inhibits tumor cell growth and invasion in lung adenocarcinoma. Am J Transl Res. 9:2997–3005. 2017.PubMed/NCBI
2	Herbst RS, Morgensztern D and Boshoff C: The biology and management of non-small cell lung cancer. Nature. 553:446–454. 2018. View Article : Google Scholar : PubMed/NCBI
3	Zhou C, Wu YL, Chen G, Feng J, Liu XQ, Wang C, Zhang S, Wang J, Zhou S, Ren S, et al: Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): A multicentre, open-label, randomised, phase 3 study. Lancet Oncol. 12:735–742. 2011. View Article : Google Scholar : PubMed/NCBI
4	Morgensztern D, Ng SH, Gao F and Govindan R: Trends in stage distribution for patients with non-small cell lung cancer: A national cancer database survey. J Thorac Oncol. 5:29–33. 2010. View Article : Google Scholar : PubMed/NCBI
5	Xu G, Chen J, Pan Q, Huang K, Pan J, Zhang W, Chen J, Yu F, Zhou T and Wang Y: Long noncoding RNA expression profiles of lung adenocarcinoma ascertained by microarray analysis. PLoS One. 9:e1040442014. View Article : Google Scholar : PubMed/NCBI
6	Li M, Ning J, Li Z, Fei Q, Zhao C, Ge Y and Wang L: Long noncoding RNA OIP5-AS1 promotes the progression of oral squamous cell carcinoma via regulating miR-338-3p/NRP1 axis. Biomed Pharmacother. 118:1092592019. View Article : Google Scholar : PubMed/NCBI
7	Wang Y, Shi F, Xia Y and Zhao H: LncRNA OIP5-AS1 predicts poor prognosis and regulates cell proliferation and apoptosis in bladder cancer. J Cell Biochem. 2018.(Online ahead of print).
8	Zhang J, Zhao T, Tian L and Li Y: LncRNA OIP5-AS1 promotes the proliferation of hemangioma vascular endothelial cells via regulating miR-195-5p/NOB1 axis. Front Pharmacol. 10:4492019. View Article : Google Scholar : PubMed/NCBI
9	Deng J, Deng H, Liu C, Liang Y and Wang S: Long non-coding RNA OIP5-AS1 functions as an oncogene in lung adenocarcinoma through targeting miR-448/Bcl-2. Biomed Pharmacother. 98:102–110. 2018. View Article : Google Scholar : PubMed/NCBI
10	Wang M, Sun X, Yang Y and Jiao W: Long non-coding RNA OIP5-AS1 promotes proliferation of lung cancer cells and leads to poor prognosis by targeting miR-378a-3p. Thorac Cancer. 9:939–949. 2018. View Article : Google Scholar : PubMed/NCBI
11	Acunzo M, Romano G, Wernicke D and Croce CM: MicroRNA and cancer-a brief overview. Adv Biol Regul. 57:1–9. 2015. View Article : Google Scholar : PubMed/NCBI
12	Yao Y, Ma J, Xue Y, Wang P, Li Z, Liu J, Chen L, Xi Z, Teng H, Wang Z, et al: Knockdown of long non-coding RNA XIST exerts tumor-suppressive functions in human glioblastoma stem cells by up-regulating miR-152. Cancer Lett. 359:75–86. 2015. View Article : Google Scholar : PubMed/NCBI
13	Sun Y and Qin B: Long noncoding RNA MALAT1 regulates HDAC4-mediated proliferation and apoptosis via decoying of miR-140-5p in osteosarcoma cells. Cancer Med. 7:4584–4597. 2018. View Article : Google Scholar : PubMed/NCBI
14	Zhou W, Wang X, Yin D, Xue L, Ma Z, Wang Z, Zhang Q, Zhao Z, Wang H, Sun Y and Yang Y: Effect of miR-140-5p on the regulation of proliferation and apoptosis in NSCLC and its underlying mechanism. Exp Ther Med. 18:1350–1356. 2019.PubMed/NCBI
15	Shi SL and Zhang ZH: Long non-coding RNA SNHG1 contributes to cisplatin resistance in non-small cell lung cancer by regulating miR-140-5p/Wnt/β-catenin pathway. Neoplasma. 66:756–765. 2019. View Article : Google Scholar : PubMed/NCBI
16	Yang P, Xiong J, Zuo L, Liu K and Zhang H: miR1405p regulates cell migration and invasion of nonsmall cell lung cancer cells through targeting VEGFA. Mol Med Rep. 18:2866–2872. 2018.PubMed/NCBI
17	Witt O, Deubzer HE, Milde T and Oehme I: HDAC family: What are the cancer relevant targets? Cancer Lett. 277:8–21. 2009. View Article : Google Scholar : PubMed/NCBI
18	Jensen ED, Schroeder TM, Bailey J, Gopalakrishnan R and Westendorf JJ: Histone deacetylase 7 associates with Runx2 and represses its activity during osteoblast maturation in a deacetylation-independent manner. J Bone Miner Res. 23:361–372. 2008. View Article : Google Scholar : PubMed/NCBI
19	Kato H, Tamamizu-Kato S and Shibasaki F: Histone deacetylase 7 associates with hypoxia-inducible factor 1alpha and increases transcriptional activity. J Biol Chem. 279:41966–41974. 2004. View Article : Google Scholar : PubMed/NCBI
20	Li B, Samanta A, Song X, Iacono KT, Bembas K, Tao R, Basu S, Riley JL, Hancock WW, Shen Y, et al: FOXP3 interactions with histone acetyltransferase and class II histone deacetylases are required for repression. Proc Natl Acad Sci USA. 104:4571–4576. 2007. View Article : Google Scholar : PubMed/NCBI
21	Caslini C, Hong S, Ban YJ, Chen XS and Ince TA: HDAC7 regulates histone 3 lysine 27 acetylation and transcriptional activity at super-enhancer-associated genes in breast cancer stem cells. Oncogene. 38:6599–6614. 2019. View Article : Google Scholar : PubMed/NCBI
22	Wei Y, Zhou F, Zhou H, Huang J, Yu D and Wu G: Endothelial progenitor cells contribute to neovascularization of non-small cell lung cancer via histone deacetylase 7-mediated cytoskeleton regulation and angiogenic genes transcription. Int J Cancer. 143:657–667. 2018. View Article : Google Scholar : PubMed/NCBI
23	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
24	Lei H, Gao Y and Xu X: LncRNA TUG1 influences papillary thyroid cancer cell proliferation, migration and EMT formation through targeting miR-145. Acta Biochim Biophys Sin (Shanghai). 49:588–597. 2017. View Article : Google Scholar : PubMed/NCBI
25	Yu Y, Shen HM, Fang DM, Meng QJ and Xin YH: LncRNA HCP5 promotes the development of cervical cancer by regulating MACC1 via suppression of microRNA-15a. Eur Rev Med Pharmacol Sci. 22:4812–4819. 2018.PubMed/NCBI
26	Yao N, Yu L, Zhu B, Gan HY and Guo BQ: LncRNA GIHCG promotes development of ovarian cancer by regulating microRNA-429. Eur Rev Med Pharmacol Sci. 22:8127–8134. 2018.PubMed/NCBI
27	Gobillot TA, Humes D, Sharma A, Kikawa C and Overbaugh J: The robust restriction of zika virus by type-I interferon in A549 cells varies by viral lineage and is not determined by IFITM3. Viruses. 12:5032020. View Article : Google Scholar
28	Massa D, Baran M, Bengoechea JA and Bowie AG: PYHIN1 regulates pro-inflammatory cytokine induction rather than innate immune DNA sensing in airway epithelial cells. J Biol Chem. 295:4438–4450. 2020. View Article : Google Scholar : PubMed/NCBI
29	Zhang Q, Lu S, Li T, Yu L, Zhang Y, Zeng H, Qian X, Bi J and Lin Y: ACE2 inhibits breast cancer angiogenesis via suppressing the VEGFa/VEGFR2/ERK pathway. J Exp Clin Cancer Res. 38:1732019. View Article : Google Scholar : PubMed/NCBI
30	Guo J, Chen M, Ai G, Mao W, Li H and Zhou J: Hsa_circ_0023404 enhances cervical cancer metastasis and chemoresistance through VEGFA and autophagy signaling by sponging miR-5047. Biomed Pharmacother. 115:1089572019. View Article : Google Scholar : PubMed/NCBI
31	Duma N, Santana-Davila R and Molina JR: Non-small cell lung cancer: Epidemiology, screening, diagnosis, and treatment. Mayo Clin Proc. 94:1623–1640. 2019. View Article : Google Scholar : PubMed/NCBI
32	Schiller JH, Harrington D, Belani CP, Langer C, Sandler A, Krook J, Zhu J and Johnson DH; Eastern Cooperative Oncology, : Comparison of four chemotherapy regimens for advanced non-small-cell lung cancer. N Engl J Med. 346:92–98. 2002. View Article : Google Scholar : PubMed/NCBI
33	Kumarakulasinghe NB, van Zanwijk N and Soo RA: Molecular targeted therapy in the treatment of advanced stage non-small cell lung cancer (NSCLC). Respirology. 20:370–378. 2015. View Article : Google Scholar : PubMed/NCBI
34	Cao MX, Jiang YP, Tang YL and Liang XH: The crosstalk between lncRNA and microRNA in cancer metastasis: Orchestrating the epithelial-mesenchymal plasticity. Oncotarget. 8:12472–12483. 2017. View Article : Google Scholar : PubMed/NCBI
35	Li SJ, Wu YX, Liang YH, Gao Y, Wu AB, Zheng HY and Yang ZX: LncRNA HANR aggravates the progression of non-small cell lung cancer via mediating miRNA-140-5p. Eur Rev Med Pharmacol Sci. 24:704–711. 2020.PubMed/NCBI
36	Dressel U, Bailey PJ, Wang SC, Downes M, Evans RM and Muscat GE: A dynamic role for HDAC7 in MEF2-mediated muscle differentiation. J Biol Chem. 276:17007–17013. 2001. View Article : Google Scholar : PubMed/NCBI
37	Ma C and D'Mello SR: Neuroprotection by histone deacetylase-7 (HDAC7) occurs by inhibition of c-jun expression through a deacetylase-independent mechanism. J Biol Chem. 286:4819–4828. 2011. View Article : Google Scholar : PubMed/NCBI
38	Saharinen P, Eklund L, Pulkki K, Bono P and Alitalo K: VEGF and angiopoietin signaling in tumor angiogenesis and metastasis. Trends Mol Med. 17:347–362. 2011. View Article : Google Scholar : PubMed/NCBI
39	Xu H, Zhang Y, Pena MM, Pirisi L and Creek KE: Six1 promotes colorectal cancer growth and metastasis by stimulating angiogenesis and recruiting tumor-associated macrophages. Carcinogenesis. 38:281–292. 2017. View Article : Google Scholar : PubMed/NCBI
40	Liu H, Chen Y, Li Y, Li C, Qin T, Bai M, Zhang Z, Jia R, Su Y and Wang C: miR195 suppresses metastasis and angiogenesis of squamous cell lung cancer by inhibiting the expression of VEGF. Mol Med Rep. 20:2625–2632. 2019.PubMed/NCBI
41	Sinha S, Khan S, Shukla S, Lakra AD, Kumar S, Das G, Maurya R and Meeran SM: Cucurbitacin B inhibits breast cancer metastasis and angiogenesis through VEGF-mediated suppression of FAK/MMP-9 signaling axis. Int J Biochem Cell Biol. 77:41–56. 2016. View Article : Google Scholar : PubMed/NCBI