Comprehensive identification of microRNA arm selection preference in lung cancer: miR‑324‑5p and ‑3p serve oncogenic functions in lung cancer

Lin,Min‑Hsi; Chen,You‑Zuo; Lee,Mei‑Yu; Weng,Ken‑Pen; Chang,Hong‑Tai; Yu,Shou‑Yu; Dong,Bo‑Jhu; Kuo,Fan‑Rong; Hung,Li‑Tzu; Liu,Li‑Feng; Chen,Wei‑Shone; Tsai,Kuo‑Wang

doi:10.3892/ol.2018.8557

Comprehensive identification of microRNA arm selection preference in lung cancer: miR‑324‑5p and ‑3p serve oncogenic functions in lung cancer

Authors:
- Min‑Hsi Lin
- You‑Zuo Chen
- Mei‑Yu Lee
- Ken‑Pen Weng
- Hong‑Tai Chang
- Shou‑Yu Yu
- Bo‑Jhu Dong
- Fan‑Rong Kuo
- Li‑Tzu Hung
- Li‑Feng Liu
- Wei‑Shone Chen
- Kuo‑Wang Tsai
View Affiliations

Affiliations: Division of Chest Medicine, Kaohsiung Veterans General Hospital, Kaohsiung 813, Taiwan, R.O.C., Department of Medical Education and Research, Kaohsiung Veterans General Hospital, Kaohsiung 813, Taiwan, R.O.C., School of Medicine, National Yang‑Ming University, Taipei 112, Taiwan, R.O.C., Center for Geriatrics and Gerontology, Kaohsiung Veterans General Hospital, Kaohsiung 813, Taiwan, R.O.C., Department of Chemical Biology, National Pingtung University of Education, Pingtung 900, Taiwan, R.O.C., Department of Biological Science and Technology, I‑Shou University, Kaohsiung 813, Taiwan, R.O.C.
Published online on: April 24, 2018 https://doi.org/10.3892/ol.2018.8557
Pages: 9818-9826
Copyright: © Lin 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

MicroRNA (miRNA/miR) dysfunction is a hallmark of lung cancer, and results in the dysregulation of tumor suppressors and oncogenes during lung cancer progression. Selection of the 5p and 3p arms of miRNA is a mechanism that improves the modulation of miRNA biological functions and complicates the regulatory network in human types of cancer. However, the involvement of arm selection preference of miRNA in lung cancer remains unclear. In the present study, changes in miRNA arm selection preference were comprehensively identified in lung cancer and corresponding adjacent normal tissues by analyzing The Cancer Genome Atlas. Arm selection was revealed to be consistent in the majority of miRNAs in lung cancer. Only a few miRNAs had significantly altered arm selection preference in lung cancer. Among these, the biological functions of the individual arms of miR‑324 were investigated further. The data revealed that miR‑324‑5p and ‑3p were significantly overexpressed in lung cancer cells. Ectopic expression of miR‑324‑5p significantly promoted cell proliferation and invasion in lung cancer cells, while miR‑324‑3p overexpression significantly increased cell proliferation but did not alter the invasion of lung cancer cells. In conclusion, the arm selection preference of miRNA may be an additional mechanism through which biological functions are modulated. The results of the present study provide a novel insight into the underlying mechanisms of lung cancer and may direct research into future therapies.

View Figures

View References

1	Siegel R, Ma J, Zou Z and Jemal A: Cancer statistics, 2014. CA Cancer J Clin. 64:9–29. 2014. View Article : Google Scholar : PubMed/NCBI
2	Ferlay J, Shin HR, Bray F, Forman D, Mathers C and Parkin DM: Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 127:2893–2917. 2010. View Article : Google Scholar : PubMed/NCBI
3	Socinski MA, Crowell R, Hensing TE, Langer CJ, Lilenbaum R, Sandler AB and Morris D: American College of Chest Physicians: Treatment of non-small cell lung cancer, stage IV: ACCP evidence-based clinical practice guidelines (2nd edition). Chest. 132 Suppl 3:277S–289S. 2007. View Article : Google Scholar : PubMed/NCBI
4	Hanahan D and Weinberg RA: The hallmarks of cancer. Cell. 100:57–70. 2000. View Article : Google Scholar : PubMed/NCBI
5	Nowell PC: The clonal evolution of tumor cell populations. Science. 194:23–28. 1976. View Article : Google Scholar : PubMed/NCBI
6	Wu HH, Lin WC and Tsai KW: Advances in molecular biomarkers for gastric cancer: miRNAs as emerging novel cancer markers. Expert Rev Mol Med. 16:e12014. View Article : Google Scholar : PubMed/NCBI
7	Yekta S, Shih IH and Bartel DP: MicroRNA-directed cleavage of HOXB8 mRNA. Science. 304:594–596. 2004. View Article : Google Scholar : PubMed/NCBI
8	Trabucchi M, Briata P, Filipowicz W, Rosenfeld MG, Ramos A and Gherzi R: How to control miRNA maturation? RNA Biol. 6:536–540. 2009. View Article : Google Scholar : PubMed/NCBI
9	Newman MA and Hammond SM: Emerging paradigms of regulated microRNA processing. Genes Dev. 24:1086–1092. 2010. View Article : Google Scholar : PubMed/NCBI
10	Chen WS, Chen TW, Yang TH, Hu LY, Pan HW, Leung CM, Li SC, Ho MR, Shu CW, Liu PF, et al: Co-modulated behavior and effects of differentially expressed miRNA in colorectal cancer. BMC Genomics. 14 Suppl 5:S122013. View Article : Google Scholar : PubMed/NCBI
11	Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S, Yatabe Y, Kawahara K, Sekido Y and Takahashi T: A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res. 65:9628–9632. 2005. View Article : Google Scholar : PubMed/NCBI
12	Lee YS and Dutta A: The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 21:1025–1030. 2007. View Article : Google Scholar : PubMed/NCBI
13	Matsubara H, Takeuchi T, Nishikawa E, Yanagisawa K, Hayashita Y, Ebi H, Yamada H, Suzuki M, Nagino M, Nimura Y, et al: Apoptosis induction by antisense oligonucleotides against miR-17-5p and miR-20a in lung cancers overexpressing miR-17-92. Oncogene. 26:6099–6105. 2007. View Article : Google Scholar : PubMed/NCBI
14	Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E, Liu S, Alder H, Costinean S, Fernandez-Cymering C, et al: MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci USA. 104:15805–15810. 2007. View Article : Google Scholar : PubMed/NCBI
15	Liu B, Peng XC, Zheng XL, Wang J and Qin YW: MiR-126 restoration down-regulate VEGF and inhibit the growth of lung cancer cell lines in vitro and in vivo. Lung Cancer. 66:169–175. 2009. View Article : Google Scholar : PubMed/NCBI
16	Takahashi Y, Forrest AR, Maeno E, Hashimoto T, Daub CO and Yasuda J: miR-107 and MiR-185 can induce cell cycle arrest in human non small cell lung cancer cell lines. PLoS One. 4:e66772009. View Article : Google Scholar : PubMed/NCBI
17	Xiao L, Zhou H, Li XP, Chen J, Fang C, Mao CX, Cui JJ, Zhang W, Zhou HH, Yin JY and Liu ZQ: MicroRNA-138 acts as a tumor suppressor in non small cell lung cancer via targeting YAP1. Oncotarget. 7:40038–40046. 2016. View Article : Google Scholar : PubMed/NCBI
18	Leung CM, Li SC, Chen TW, Ho MR, Hu LY, Liu WS, Wu TT, Hsu PC, Chang HT and Tsai KW: Comprehensive microRNA profiling of prostate cancer cells after ionizing radiation treatment. Oncol Rep. 31:1067–1078. 2014. View Article : Google Scholar : PubMed/NCBI
19	Cheng WC, Chung IF, Huang TS, Chang ST, Sun HJ, Tsai CF, Liang ML, Wong TT and Wang HW: YM500: A small RNA sequencing (smRNA-seq) database for microRNA research. Nucleic Acids Res. 41:(Database Issue). D285–D294. 2013. View Article : Google Scholar : PubMed/NCBI
20	Li SC, Liao YL, Ho MR, Tsai KW, Lai CH and Lin WC: miRNA arm selection and isomiR distribution in gastric cancer. BMC Genomics. 13 Suppl 1:S132012. View Article : Google Scholar : PubMed/NCBI
21	Chang HT, Li SC, Ho MR, Pan HW, Ger LP, Hu LY, Yu SY, Li WH and Tsai KW: Comprehensive analysis of microRNAs in breast cancer. BMC Genomics. 13 Suppl 7:S182012.PubMed/NCBI
22	Li SC, Liao YL, Chan WC, Ho MR, Tsai KW, Hu LY, Lai CH, Hsu CN and Lin WC: Interrogation of rabbit miRNAs and their isomiRs. Genomics. 98:453–459. 2011. View Article : Google Scholar : PubMed/NCBI
23	Griffiths-Jones S, Hui JH, Marco A and Ronshaugen M: MicroRNA evolution by arm switching. EMBO Rep. 12:172–177. 2011. View Article : Google Scholar : PubMed/NCBI
24	Cloonan N, Wani S, Xu Q, Gu J, Lea K, Heater S, Barbacioru C, Steptoe AL, Martin HC, Nourbakhsh E, et al: MicroRNAs and their isomiRs function cooperatively to target common biological pathways. Genome Biol. 12:R1262011. View Article : Google Scholar : PubMed/NCBI
25	Marco A, Hui JH, Ronshaugen M and Griffiths-Jones S: Functional shifts in insect microRNA evolution. Genome Biol Evol. 2:686–696. 2010.PubMed/NCBI
26	Guo L, Li H, Liang T, Lu J, Yang Q, Ge Q and Lu Z: Consistent isomiR expression patterns and 3′ addition events in miRNA gene clusters and families implicate functional and evolutionary relationships. Mol Biol Rep. 39:6699–6706. 2012. View Article : Google Scholar : PubMed/NCBI
27	Tsai KW, Leung CM, Lo YH, Chen TW, Chan WC, Yu SY, Tu YT, Lam HC, Li SC, Ger LP, et al: Arm selection preference of MicroRNA-193a varies in breast cancer. Sci Rep. 6:281762016. View Article : Google Scholar : PubMed/NCBI
28	Kuo WT, Yu SY, Li SC, Lam HC, Chang HT, Chen WS, Yeh CY, Hung SF, Liu TC, Wu T, et al: MicroRNA-324 in Human cancer: miR-324-5p and miR-324-3p have distinct biological functions in human cancer. Anticancer Res. 36:5189–5196. 2016. View Article : Google Scholar : PubMed/NCBI
29	Lewis BP, Burge CB and Bartel DP: Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 120:15–20. 2005. View Article : Google Scholar : PubMed/NCBI
30	Oliveros JC: Venny. An interactive tool for comparing lists with Venn's diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html2007–2015.
31	Griffiths-Jones S, Saini HK, van Dongen S and Enright AJ: miRBase: Tools for microRNA genomics. Nucleic Acids Res. 36:(Database issue). D154–D158. 2008. View Article : Google Scholar : PubMed/NCBI
32	Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A and Enright AJ: miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34:(Database issue). D140–D144. 2006. View Article : Google Scholar : PubMed/NCBI
33	Kozomara A and Griffiths-Jones S: miRBase: Annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42:(Database issue). D68–D73. 2014. View Article : Google Scholar : PubMed/NCBI
34	Kozomara A and Griffiths-Jones S: miRBase: Integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39:(Database issue). D152–D157. 2011. View Article : Google Scholar : PubMed/NCBI
35	Griffiths-Jones S: The microRNA registry. Nucleic Acids Res. 32:(Database issue). D109–D111. 2004. View Article : Google Scholar : PubMed/NCBI
36	Liu C, Zheng L, Wang H, Ran X, Liu H and Sun X: The RCAN1 inhibits NF-κB and suppresses lymphoma growth in mice. Cell Death Dis. 6:e19292015. View Article : Google Scholar : PubMed/NCBI
37	Kohler RS, Anugraham M, López MN, Xiao C, Schoetzau A, Hettich T, Schlotterbeck G, Fedier A, Jacob F and Heinzelmann-Schwarz V: Epigenetic activation of MGAT3 and corresponding bisecting GlcNAc shortens the survival of cancer patients. Oncotarget. 7:51674–51686. 2016. View Article : Google Scholar : PubMed/NCBI
38	Chang SN, Lee JM, Oh H and Park JH: Glutathione peroxidase 3 inhibits prostate tumorigenesis in TRAMP mice. Prostate. 76:1387–1398. 2016. View Article : Google Scholar : PubMed/NCBI
39	An BC, Jung NK, Park CY, Oh IJ, Choi YD, Park JI and Lee SW: Epigenetic and glucocorticoid receptor-mediated regulation of glutathione peroxidase 3 in lung cancer cells. Mol Cells. 39:631–638. 2016. View Article : Google Scholar : PubMed/NCBI
40	Slezak-Prochazka I, Durmus S, Kroesen BJ and van den Berg A: MicroRNAs, macrocontrol: Regulation of miRNA processing. Rna. 16:1087–1095. 2010. View Article : Google Scholar : PubMed/NCBI
41	Li SC, Tsai KW, Pan HW, Jeng YM, Ho MR and Li WH: MicroRNA 3′ end nucleotide modification patterns and arm selection preference in liver tissues. BMC Syst Biol. 6 Suppl 2:S142012. View Article : Google Scholar
42	Dixon-McIver A, East P, Mein CA, Cazier JB, Molloy G, Chaplin T, Lister Andrew T, Young BD and Debernardi S: Distinctive patterns of microRNA expression associated with karyotype in acute myeloid leukaemia. PLoS One. 3:e21412008. View Article : Google Scholar : PubMed/NCBI
43	Ferretti E, De Smaele E, Miele E, Laneve P, Po A, Pelloni M, Paganelli A, Di Marcotullio L, Caffarelli E, Screpanti I, et al: Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J. 27:2616–2627. 2008. View Article : Google Scholar : PubMed/NCBI
44	Schultz J, Lorenz P, Gross G, Ibrahim S and Kunz M: MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growth. Cell Res. 18:549–557. 2008. View Article : Google Scholar : PubMed/NCBI
45	Wang Y, Lee AT, Ma JZ, Wang J, Ren J, Yang Y, Tantoso E, Li KB, Ooi LL, Tan P and Lee CG: Profiling microRNA expression in hepatocellular carcinoma reveals microRNA-224 up-regulation and apoptosis inhibitor-5 as a microRNA-224-specific target. J Biol Chem. 283:13205–13215. 2008. View Article : Google Scholar : PubMed/NCBI
46	Crawford M, Batte K, Yu L, Wu X, Nuovo GJ, Marsh CB, Otterson GA and Nana-Sinkam SP: MicroRNA 133B targets pro-survival molecules MCL-1 and BCL2L2 in lung cancer. Biochem Biophys Res Commun. 388:483–489. 2009. View Article : Google Scholar : PubMed/NCBI
47	Xu HS, Zong HL, Shang M, Ming X, Zhao JP, Ma C and Cao L: MiR-324-5p inhibits proliferation of glioma by target regulation of GLI1. Eur Rev Med Pharmacol Sci. 18:828–832. 2014.PubMed/NCBI