Long non‑coding RNA LINC00887 promotes progression of lung carcinoma by targeting the microRNA‑206/NRP1 axis

Xu,Ling-Bin; Bo,Bian-Xin; Xiong,Jie; Ren,Ya-Juan; Han,Dong; Wei,Sheng-Hong; Ren,Xiao-Ping

doi:10.3892/ol.2020.12348

Long non‑coding RNA LINC00887 promotes progression of lung carcinoma by targeting the microRNA‑206/NRP1 axis

Authors:
- Ling-Bin Xu
- Bian-Xin Bo
- Jie Xiong
- Ya-Juan Ren
- Dong Han
- Sheng-Hong Wei
- Xiao-Ping Ren
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Affiliations: The Second Department of Pulmonary and Critical Care Medicine, Shaanxi Provincial People's Hospital, Xi'an, Shaanxi 710068, P.R. China, Department of Critical Care Medicine, Zhouzhi Country People's Hospital, Xi'an, Shaanxi 710407, P.R. China
Published online on: December 6, 2020 https://doi.org/10.3892/ol.2020.12348
Article Number: 87
Copyright: © Xu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Long non‑coding RNAs (lncRNAs) have been reported to participate in multiple biological processes, including tumorigenesis. In the current study, the function of a novel lncRNA LINC00887 was investigated in lung carcinoma. For this purpose, LINC00887 expression was assessed by reverse‑transcription quantitative PCR. Cell viability was determined by the CCK‑8 and EdU assays. Cell invasion, migration were assessed by the transwell and wound healing assays, respectively. A dual luciferase assay was used for analysis of the interaction between LINC00887 and miR‑206, as well as the relationship of miR‑206 with NRP1. A tumor xenograft study was performed to investigate the LINC00887‑miR‑206‑NRP1 axis in vivo. The expression levels of LINC00887 were upregulated in lung carcinoma tissues and cells compared with adjacent tissues or normal cells (BEAS‑2B). Knockdown LINC00887 significantly inhibited the proliferation, migration and invasion of lung carcinoma A549 and NCI‑H460 cells. Furthermore, LINC00887 was identified as a competing endogenous RNA and to directly interact with miR‑206. Mechanistically, miR‑206 was demonstrated to regulate neuropilin‑1 (NRP1) expression by targeting the NRP1 3'‑untranslated region. The results of the present study suggested that the LINC00887‑miR‑206‑NRP1 axis served a critical role in regulating lung carcinoma cell proliferation, migration and invasion. In addition, xenograft tumor model experiments revealed that silencing LINC00887 suppressed lung carcinoma tumor growth of in vivo. In summary, our results suggest that LINC00887 may serve an oncogenic role in lung carcinoma by targeting the miR‑206/NRP1 axis, providing a potential therapeutic target for patients with lung carcinoma.

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1	Siegel RL, Miller KD and Jemal A: Cancer statistics, 2018. CA Cancer J Clin. 68:7–30. 2018. View Article : Google Scholar : PubMed/NCBI
2	Dela Cruz CS, Tanoue LT and Matthay RA: Lung cancer: Epidemiology, etiology, and prevention. Clin Chest Med. 32:605–644. 2011. View Article : Google Scholar : PubMed/NCBI
3	Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA and Jemal A: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68:394–424. 2018. View Article : Google Scholar : PubMed/NCBI
4	Tanase A, Colita A, Ianosi G, Neagoe D, Branisteanu DE, Calina D, Docea AO, Tsatsakis A and Ianosi SL: Rare case of disseminated fusariosis in a young patient with graft vs. host disease following an allogeneic transplant. Exp Ther Med. 12:2078–2082. 2016. View Article : Google Scholar : PubMed/NCBI
5	Ungureanu A, Zlatian O, Mitroi G, Drocaş A, Ţîrcă T, Călina D, Dehelean C, Docea AO, Izotov BN, Rakitskii VN, et al: Staphylococcus aureus colonisation in patients from a primary regional hospital. Mol Med Rep. 16:8771–8780. 2017. View Article : Google Scholar : PubMed/NCBI
6	Calina D, Rosu L, Roșu AF, Ianoşi G, Ianoşi S, Zlatian O, Mitruț R, Docea AO, Rogoveanu O, Mitruț P, et al: Etiological diagnosis and pharmacotherapeutic management of parapneumonic pleurisy. Farmacia. 64:946–952. 2016.
7	Lemjabbar-Alaoui H, Hassan OU, Yang YW and Buchanan P: Lung cancer: Biology and treatment options. Biochim Biophys Acta. 1856:189–210. 2015.PubMed/NCBI
8	Siegel RL, Miller KD and Jemal A: Cancer statistics, 2019. CA Cancer J Clin. 69:7–34. 2019. View Article : Google Scholar : PubMed/NCBI
9	Knight SB, Crosbie PA, Balata H, Chudziak J, Hussell T and Dive C: Progress and prospects of early detection in lung cancer. Open Biol. 7:1700702017. View Article : Google Scholar : PubMed/NCBI
10	Daphedar A and Taranath TC: Characterization and cytotoxic effect of biogenic silver nanoparticles on mitotic chromosomes of drimia polyantha (Blatt. & McCann) stearn. Toxicol Rep. 5:910–918. 2018. View Article : Google Scholar : PubMed/NCBI
11	Sani TA, Mohammadpour E, Mohammadi A, Memariani T, Yazd MV, Ramin R, Daniela C, Anca OD, Marina G, Etemad L and Shahsavand S: Cytotoxic and apoptogenic properties of Dracocephalum kotschyi aerial part different fractions on calu-6 and mehr-80 lung cancer cell lines. Farmacia. 65:189–199. 2017.
12	Saab AM, Guerrini A, Sacchetti G, Maietti S, Zeino M, Arend J, Gambari R, Bernardi F and Efferth T: Phytochemical analysis and cytotoxicity towards multidrug-resistant leukemia cells of essential oils derived from lebanese medicinal plants. Planta Med. 78:1927–1931. 2012. View Article : Google Scholar : PubMed/NCBI
13	Shao H, Jing K, Mahmoud E, Huang H, Fang X and Yu C: Apigenin sensitizes colon cancer cells to antitumor activity of ABT-263. Mol Cancer Ther. 12:2640–2650. 2013. View Article : Google Scholar : PubMed/NCBI
14	Zeng S, Kapur A, Patankar MS and Xiong MP: Formulation, characterization, and antitumor properties of trans- and cis-citral in the 4T1 breast cancer xenograft mouse model. Pharm Res. 32:2548–2558. 2015.PubMed/NCBI
15	Forde PM, Brahmer JR and Kelly RJ: New strategies in lung cancer: Epigenetic therapy for non-small cell lung cancer. Clin Cancer Res. 20:2244–2248. 2014. View Article : Google Scholar : PubMed/NCBI
16	Mercer TR, Dinger ME and Mattick JS: Long non-coding RNAs: Insights into functions. Nat Rev Genet. 10:155–159. 2009. View Article : Google Scholar : PubMed/NCBI
17	Calle AS, Kawamura Y, Yamamoto Y, Takeshita F and Ochiya T: Emerging roles of long non-coding RNA in cancer. Cancer Sci. 109:2093–2100. 2018. View Article : Google Scholar : PubMed/NCBI
18	Sun H, Huang Z, Sheng W and Xu MD: Emerging roles of long non-coding RNAs in tumor metabolism. J Hematol Oncol. 11:1062018. View Article : Google Scholar : PubMed/NCBI
19	Sun M, Gadad SS, Kim DS and Kraus WL: Discovery, annotation, and functional analysis of long noncoding rnas controlling cell-cycle gene expression and proliferation in breast cancer cells. Mol Cell. 59:698–711. 2015. View Article : Google Scholar : PubMed/NCBI
20	Chakravarty D, Sboner A, Nair SS, Giannopoulou E, Li R, Hennig S, Mosquera JM, Pauwels J, Park K, Kossai M, et al: The oestrogen receptor alpha-regulated lncRNA NEAT1 is a critical modulator of prostate cancer. Nat Commun. 5:53832014. View Article : Google Scholar : PubMed/NCBI
21	She K, Huang J, Zhou H, Huang T, Chen G and He J: lncRNA-SNHG7 promotes the proliferation, migration and invasion and inhibits apoptosis of lung cancer cells by enhancing the FAIM2 expression. Oncol Rep. 36:2673–2680. 2016. View Article : Google Scholar : PubMed/NCBI
22	Wu WK, Lee CW, Cho CH, Fan D, Wu K, Yu J and Sung JJ: MicroRNA dysregulation in gastric cancer: A new player enters the game. Oncogene. 29:5761–5771. 2010. View Article : Google Scholar : PubMed/NCBI
23	Lin C and Yang L: Long noncoding RNA in Cancer: Wiring signaling circuitry. Trends Cell Biol. 28:287–301. 2018. View Article : Google Scholar : PubMed/NCBI
24	Zhang C, Wang C, Jia Z, Tong W, Liu D, He C, Huang X and Xu W: Differentially expressed mRNAs, lncRNAs, and miRNAs with associated co-expression and ceRNA networks in ankylosing spondylitis. Oncotarget. 8:113543–113557. 2017. View Article : Google Scholar : PubMed/NCBI
25	Fan CN, Ma L and Liu N: Systematic analysis of lncRNA-miRNA-mRNA competing endogenous RNA network identifies four-lncRNA signature as a prognostic biomarker for breast cancer. J Transl Med. 16:2642018. View Article : Google Scholar : PubMed/NCBI
26	Cong Z, Diao Y, Xu Y, Li X, Jiang Z, Shao C, Ji S, Shen Y, De W and Qiang Y: Long non-coding RNA linc00665 promotes lung adenocarcinoma progression and functions as ceRNA to regulate AKR1B10-ERK signaling by sponging miR-98. Cell Death Dis. 10:842019. View Article : Google Scholar : PubMed/NCBI
27	Guo T, Li J, Zhang L, Hou W, Wang R, Zhang J and Gao P: Multidimensional communication of microRNAs and long non-coding RNAs in lung cancer. J Cancer Res Clin Oncol. 145:31–48. 2019. View Article : Google Scholar : PubMed/NCBI
28	Liu S, Yan G, Zhang J and Yu L: Knockdown of long noncoding RNA (lncRNA) metastasis-associated lung adenocarcinoma transcript 1 (MALAT1) inhibits proliferation, migration, and invasion and promotes apoptosis by targeting miR-124 in retinoblastoma. Oncol Res. 26:581–591. 2018. View Article : Google Scholar : PubMed/NCBI
29	Wang D and Hu Y: Long non-coding RNA PVT1 competitively binds microRNA-424-5p to regulate CARM1 in radiosensitivity of non-small-cell lung cancer. Mol Ther Nucleic Acids. 16:130–140. 2018. View Article : Google Scholar : PubMed/NCBI
30	Yang X, Zhang W, Cheng SQ and Yang RL: High expression of lncRNA GACAT3 inhibits invasion and metastasis of non-small cell lung cancer to enhance the effect of radiotherapy. Eur Rev Med Pharmacol Sci. 22:1315–1322. 2018.PubMed/NCBI
31	Yang J, Du YM and Li B: LncRNA BX357664 inhibits the proliferation and invasion of non-small cell lung cancer cells. Eur Rev Med Pharmacol Sci. 23:660–669. 2019.PubMed/NCBI
32	Tian Y, Yu M, Sun L, Liu L, Huo S, Shang W, Sheng S, Wang J, Sun J, Hu Q, et al: Long noncoding RNA00887 reduces the invasion and metastasis of nonsmall cell lung cancer by causing the degradation of miRNAs. Oncol Rep. 42:1173–1182. 2019.PubMed/NCBI
33	Ali MM, Akhade VS, Kosalai ST, Subhash S, Statello L, Meryet-Figuiere M, Abrahamsson J, Mondal T and Kanduri C: PAN-Cancer analysis of S-phase enriched lncRNAs identifies oncogenic drivers and biomarkers. Nat Commun. 9:8832018. View Article : Google Scholar : PubMed/NCBI
34	Travis WD, Brambilla E, Nicholson AG, Yatabe Y, Austin JH, Beasley MB, Chirieac LR, Dacic S, Duhig E, Flieder DB, et al: The 2015 world health organization classification of lung tumors: Impact of genetic, clinical and radiologic advances since the 2004 classification. J Thorac Oncol. 10:1243–1260. 2015. View Article : Google Scholar : PubMed/NCBI
35	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
36	Salmena L, Poliseno L, Tay Y, Kats L and Pandolfi PP: A ceRNA hypothesis: The rosetta stone of a hidden RNA language? Cell. 146:353–358. 2011. View Article : Google Scholar : PubMed/NCBI
37	Kartha RV and Subramanian S: Competing endogenous RNAs (ceRNAs): New entrants to the intricacies of gene regulation. Front Genet. 5:82014. View Article : Google Scholar : PubMed/NCBI
38	Paraskevopoulou MD, Vlachos IS, Karagkouni D, Georgakilas G, Kanellos I, Vergoulis T, Zagganas K, Tsanakas P, Floros E, Dalamagas T and Hatzigeorgiou AG: DIANA-LncBase v2: Indexing microRNA targets on non-coding transcripts. Nucleic Acids Res. 44:D231–D238. 2016. View Article : Google Scholar : PubMed/NCBI
39	Balas MM and Johnson AM: Exploring the mechanisms behind long noncoding RNAs and cancer. Noncoding RNA Res. 3:108–117. 2018. View Article : Google Scholar : PubMed/NCBI
40	Jin Y, Feng SJ, Qiu S, Shao N and Zheng JH: LncRNA MALAT1 promotes proliferation and metastasis in epithelial ovarian cancer via the PI3K-AKT pathway. Eur Rev Med Pharmacol Sci. 21:3176–3184. 2017.PubMed/NCBI
41	Ji Q, Zhang L, Liu X, Zhou L, Wang W, Han Z, Sui H, Tang Y, Wang Y, Liu N, et al: Long non-coding RNA MALAT1 promotes tumour growth and metastasis in colorectal cancer through binding to SFPQ and releasing oncogene PTBP2 from SFPQ/PTBP2 complex. Br J Cancer. 111:736–748. 2014. View Article : Google Scholar : PubMed/NCBI
42	Zhang J, Yao T, Wang Y, Yu J, Liu Y and Lin Z: Long noncoding RNA MEG3 is downregulated in cervical cancer and affects cell proliferation and apoptosis by regulating miR-21. Cancer Biol Ther. 17:104–113. 2016. View Article : Google Scholar : PubMed/NCBI
43	Celestino R, Nome T, Pestana A, Hoff AM, Gonçalves AP, Pereira L, Cavadas B, Eloy C, Bjøro T, Sobrinho-Simões M, et al: CRABP1, C1QL1 and LCN2 are biomarkers of differentiated thyroid carcinoma, and predict extrathyroidal extension. BMC Cancer. 18:682018. View Article : Google Scholar : PubMed/NCBI
44	Zhu H, Yu J, Zhu H, Guo Y and Feng S: Identification of key lncRNAs in colorectal cancer progression based on associated protein-protein interaction analysis. World J Surg Oncol. 15:1532017. View Article : Google Scholar : PubMed/NCBI
45	You X, Zhao Y, Sui J, Shi X, Sun Y, Xu J, Liang G, Xu Q and Yao Y: Integrated analysis of long noncoding RNA interactions reveals the potential role in progression of human papillary thyroid cancer. Cancer Med. 7:5394–5410. 2018. View Article : Google Scholar : PubMed/NCBI
46	Deng M, Qin Y, Chen X, Wang Q and Wang J: MiR-206 inhibits proliferation, migration, and invasion of gastric cancer cells by targeting the MUC1 gene. Onco Targets Ther. 12:849–859. 2019. View Article : Google Scholar : PubMed/NCBI
47	Sun P, Sun D, Wang X, Liu T, Ma Z and Duan L: MiR-206 is an independent prognostic factor and inhibits tumor invasion and migration in colorectal cancer. Cancer Biomark. 15:391–396. 2015. View Article : Google Scholar : PubMed/NCBI
48	Fu Y, Shao ZM, He QZ, Jiang BQ, Wu Y and Zhuang ZG: Hsa-MiR-206 represses the proliferation and invasion of breast cancer cells by targeting Cx43. Eur Rev Med Pharmacol Sci. 19:2091–2104. 2015.PubMed/NCBI
49	Zhang T, Liu M, Wang C, Lin C, Sun Y and Jin D: Down-Regulation of miR-206 promotes proliferation and invasion of laryngeal cancer by regulating VEGF expression. Anticancer Res. 31:3859–3863. 2011.PubMed/NCBI
50	Samaeekia R, Adorno-Cruz V, Bockhorn J, Chang YF, Huang S, Prat A, Ha N, Kibria G, Huo D, Zheng H, et al: MiR-206 inhibits stemness and metastasis of breast cancer by targeting MKL1/IL11 pathway. Clin Cancer Res. 23:1091–1103. 2017. View Article : Google Scholar : PubMed/NCBI
51	Chaudhary B, Khaled YS, Ammori BJ and Elkord E: Neuropilin 1: Function and therapeutic potential in cancer. Cancer Immunol Immunother. 63:81–99. 2014. View Article : Google Scholar : PubMed/NCBI
52	Chen C, Hu Y and Li L: NRP1 is targeted by miR-130a and miR-130b, and is associated with multidrug resistance in epithelial ovarian cancer based on integrated gene network analysis. Mol Med Rep. 13:188–196. 2016. View Article : Google Scholar : PubMed/NCBI
53	Peng Y, Liu YM, Li LC, Wang LL and Wu XL: MicroRNA-338 inhibits growth, invasion and metastasis of gastric cancer by targeting NRP1 expression. PLoS One. 9:e944222014. View Article : Google Scholar : PubMed/NCBI
54	Ma L, Zhai B, Zhu H, Li W, Jiang W, Lei L, Zhang S, Qiao H, Jiang X and Sun X: The miR-141/neuropilin-1 axis is associated with the clinicopathology and contributes to the growth and metastasis of pancreatic cancer. Cancer Cell Int. 19:2482019. View Article : Google Scholar : PubMed/NCBI
55	Seifi-Alan M, Shams R, Bandehpour M, Mirfakhraie R and Ghafouri-Fard S: Neuropilin-1 expression is associated with lymph node metastasis in breast cancer tissues. Cancer Manag Res. 10:1969–1974. 2018. View Article : Google Scholar : PubMed/NCBI