Inhibition of microRNA-25 by tumor necrosis factor α is critical in the modulation of vascular smooth muscle cell proliferation

Qi,Lichun; Zhi,Jixin; Zhang,Tong; Cao,Xue; Sun,Lixiu; Xu,Yuanyuan; Li,Xueqi

doi:10.3892/mmr.2015.3329

Inhibition of microRNA-25 by tumor necrosis factor α is critical in the modulation of vascular smooth muscle cell proliferation

Authors:
- Lichun Qi
- Jixin Zhi
- Tong Zhang
- Xue Cao
- Lixiu Sun
- Yuanyuan Xu
- Xueqi Li
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Affiliations: Cardiovascular Department, The Fourth Affiliated Hospital, Harbin Medical University, Harbin, Heilongjiang 150001, P.R. China
Published online on: February 11, 2015 https://doi.org/10.3892/mmr.2015.3329
Pages: 4353-4358

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Abstract

Atherosclerosis and coronary heart disease are characterized by a hyperplastic neointima and inflammation involving cytokines, such as tumor necrosis factor‑α (TNF‑α). TNF‑α is pleiotropic and mediates inflammation and proliferation in various cell types, such as vascular smooth muscle cells (VSMCs). The molecular mechanism for the pleiotropic effects of TNF‑α has not previously been fully elucidated. The current study identified that the expression of microRNA‑25 (miR‑25), a small noncoding RNA, was reduced in response to TNF‑α signaling in VSMCs. Restored miR‑25 expression inhibited cell proliferation and Ki‑67 expression. The present study indicated that cyclin‑dependent kinase 6 (CDK6) was the direct target gene of miR‑25 using mRNA and protein expression analysis, and luciferase assays. It was also observed that restored CDK6 expression in the miR‑25 mimic‑treated VSMCs partly reduced miR‑25‑mediated VSMC proliferation. In conclusion, miR‑25 is suggested to be important in TNF‑α‑induced abnormal proliferation of VSMCs.

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1	Zeidan A, Purdham DM, Rajapurohitam V, Javadov S, Chakrabarti S and Karmazyn M: Leptin induces vascular smooth muscle cell hypertrophy through angiotensin II- and endothelin-1-dependent mechanisms and mediates stretch-induced hypertrophy. J Pharmacol Exp Ther. 315:1075–1084. 2005. View Article : Google Scholar : PubMed/NCBI
2	Chen NX, Kiattisunthorn K, O’Neill KD, et al: Decreased microRNA is involved in the vascular remodeling abnormalities in chronic kidney disease (CKD). PloS One. 8:e645582013. View Article : Google Scholar : PubMed/NCBI
3	Davis-Dusenbery BN, Wu C and Hata A: Micromanaging vascular smooth muscle cell differentiation and phenotypic modulation. Arterioscler Thromb Vasc Biol. 31:2370–2377. 2011. View Article : Google Scholar : PubMed/NCBI
4	Kothapalli D, Castagnino P, Rader DJ, Phillips MC, Lund-Katz S and Assoian RK: Apolipoprotein E-mediated cell cycle arrest linked to p27 and the Cox2-dependent repression of miR221/222. Atherosclerosis. 227:65–71. 2013. View Article : Google Scholar : PubMed/NCBI
5	Bohlen F, Kratzsch J, Mueller M, et al: Leptin inhibits cell growth of human vascular smooth muscle cells. Vascul Pharmacol. 46:67–71. 2007. View Article : Google Scholar
6	Bodary PF, Shen Y, Ohman M, et al: Leptin regulates neointima formation after arterial injury through mechanisms independent of blood pressure and the leptin receptor/STAT3 signaling pathways involved in energy balance. Arterioscler Thromb Vasc Biol. 27:70–76. 2007. View Article : Google Scholar
7	Beltowski J: Leptin and atherosclerosis. Atherosclerosis. 189:47–60. 2006. View Article : Google Scholar : PubMed/NCBI
8	Davis R, Pillai S, Lawrence N, Sebti S and Chellappan SP: TNF-α-mediated proliferation of vascular smooth muscle cells involves Raf-1-mediated inactivation of Rb and transcription of E2F1-regulated genes. Cell Cycle. 11:109–118. 2012. View Article : Google Scholar :
9	Gao X, Belmadani S, Picchi A, et al: Tumor necrosis factor-alpha induces endothelial dysfunction in Lepr(db) mice. Circulation. 115:245–254. 2007. View Article : Google Scholar : PubMed/NCBI
10	Rajesh M, Mukhopadhyay P, Haskó G, Huffman JW, Mackie K and Pacher P: CB2 cannabinoid receptor agonists attenuate TNF-alpha-induced human vascular smooth muscle cell proliferation and migration. Br J Pharmacol. 153:347–357. 2008. View Article : Google Scholar
11	Lee SJ, Kim WJ and Moon SK: TNF-alpha regulates vascular smooth muscle cell responses in genetic hypertension. Int Immunopharmacol. 9:837–843. 2009. View Article : Google Scholar : PubMed/NCBI
12	Rho MC, Ah Lee K, Mi Kim S, et al: Sensitization of vascular smooth muscle cell to TNF-alpha-mediated death in the presence of palmitate. Toxicol Appl Pharmacol. 220:311–319. 2007. View Article : Google Scholar : PubMed/NCBI
13	Song B, Wang Y, Xi Y, et al: Mechanism of chemoresistance mediated by miR-140 in human osteosarcoma and colon cancer cells. Oncogene. 28:4065–4074. 2009. View Article : Google Scholar : PubMed/NCBI
14	Yu X, Li Z, Shen J, et al: MicroRNA-10b promotes nucleus pulposus cell proliferation through RhoC-Akt pathway by targeting HOXD10 in intervetebral disc degeneration. PloS One. 8:e830802013. View Article : Google Scholar :
15	Hutcheson R, Terry R, Chaplin J, et al: MicroRNA-145 restores contractile vascular smooth muscle phenotype and coronary collateral growth in the metabolic syndrome. Arterioscler Thromb Vasc Biol. 33:727–736. 2013. View Article : Google Scholar : PubMed/NCBI
16	Martello G, Rosato A, Ferrari F, et al: A MicroRNA targeting dicer for metastasis control. Cell. 141:1195–1207. 2010. View Article : Google Scholar : PubMed/NCBI
17	Majid S, Dar AA, Saini S, et al: MicroRNA-23b functions as a tumor suppressor by regulating Zeb1 in bladder cancer. PloS One. 8:e676862013. View Article : Google Scholar : PubMed/NCBI
18	Wu WK, Lee CW, Cho CH, et al: MicroRNA dysregulation in gastric cancer: a new player enters the game. Oncogene. 29:5761–5771. 2010. View Article : Google Scholar : PubMed/NCBI
19	Brenner B, Hoshen MB, Purim O, et al: MicroRNAs as a potential prognostic factor in gastric cancer. World J Gastroenterol. 17:3976–3985. 2011. View Article : Google Scholar : PubMed/NCBI
20	Cullen BR: MicroRNAs as mediators of viral evasion of the immune system. Nat Immunol. 14:205–210. 2013. View Article : Google Scholar : PubMed/NCBI
21	Rotllan N and Fernández-Hernando C: MicroRNA regulation of cholesterol metabolism. Cholesterol. 2012:8478492012. View Article : Google Scholar : PubMed/NCBI
22	Chen KC and Juo SH: MicroRNAs in atherosclerosis. Kaohsiung J Med Sci. 28:631–640. 2012. View Article : Google Scholar : PubMed/NCBI
23	Chen LJ, Lim SH, Yeh YT, Lien SC and Chiu JJ: Roles of microRNAs in atherosclerosis and restenosis. J Biomed Sci. 19:792012. View Article : Google Scholar : PubMed/NCBI
24	Sun Y, Chen D, Cao L, et al: MiR-490-3p modulates the proliferation of vascular smooth muscle cells induced by ox-LDL through targeting PAPP-A. Cardiovasc Res. 100:272–279. 2013. View Article : Google Scholar : PubMed/NCBI
25	Yu ML, Wang JF, Wang GK, et al: Vascular smooth muscle cell proliferation is influenced by let-7d microRNA and its interaction with KRAS. Circ J. 75:703–709. 2011. View Article : Google Scholar : PubMed/NCBI
26	Kim S and Kang H: miR-15b induced by platelet-derived growth factor signaling is required for vascular smooth muscle cell proliferation. BMB Rep. 46:550–554. 2013. View Article : Google Scholar : PubMed/NCBI
27	Li P, Liu Y, Yi B, et al: MicroRNA-638 is highly expressed in human vascular smooth muscle cells and inhibits PDGF-BB-induced cell proliferation and migration through targeting orphan nuclear receptor NOR1. Cardiovasc Res. 99:185–193. 2013. View Article : Google Scholar : PubMed/NCBI
28	Gómez-Hernández A, Escribano Ó, Perdomo L, et al: Implication of insulin receptor A isoform and IRA/IGF-IR hybrid receptors in the aortic vascular smooth muscle cell proliferation: role of TNF-α and IGF-II. Endocrinology. 154:2352–2364. 2013. View Article : Google Scholar
29	Jiang F, Jiang R, Zhu X, Zhang X and Zhan Z: Genipin inhibits TNF-α-induced vascular smooth muscle cell proliferation and migration via induction of HO-1. PloS One. 8:e748262013. View Article : Google Scholar
30	Kim HH and Kim K: Enhancement of TNF-alpha-mediated cell death in vascular smooth muscle cells through cytochrome c-independent pathway by the proteasome inhibitor. FEBS Lett. 535:190–194. 2003. View Article : Google Scholar : PubMed/NCBI
31	Li Q, Zou C, Han Z, et al: MicroRNA-25 functions as a potential tumor suppressor in colon cancer by targeting Smad7. Cancer Lett. 335:168–174. 2013. View Article : Google Scholar : PubMed/NCBI
32	Razumilava N, Bronk SF, Smoot RL, et al: miR-25 targets TNF-related apoptosis inducing ligand (TRAIL) death receptor-4 and promotes apoptosis resistance in cholangiocarcinoma. Hepatology. 55:465–475. 2012. View Article : Google Scholar :
33	Lu D, Davis MP, Abreu-Goodger C, et al: MiR-25 regulates Wwp2 and Fbxw7 and promotes reprogramming of mouse fibroblast cells to iPSCs. PloS One. 7:e409382012. View Article : Google Scholar : PubMed/NCBI
34	Su ZX, Zhao J, Rong ZH, Geng WM, Wu YG and Qin CK: Upregulation of microRNA-25 associates with prognosis in hepatocellular carcinoma. Diagn Pathol. 9:472014. View Article : Google Scholar : PubMed/NCBI
35	Xu FX, Su YL, Zhang H, Kong JY, Yu H and Qian BY: Prognostic implications for high expression of MiR-25 in lung adenocarcinomas of female non-smokers. Asian Pac J Cancer Prev. 15:1197–1203. 2014. View Article : Google Scholar : PubMed/NCBI
36	Esposito F, Tornincasa M, Pallante P, et al: Down-regulation of the miR-25 and miR-30d contributes to the development of anaplastic thyroid carcinoma targeting the polycomb protein EZH2. J Clin Endocrinol Metab. 97:E710–E718. 2012. View Article : Google Scholar : PubMed/NCBI
37	Li X, Yang C, Wang X, Zhang J, Zhang R and Liu R: The expression of miR-25 is increased in colorectal cancer and is associated with patient prognosis. Med Oncol. 31:7812014. View Article : Google Scholar
38	Wahlquist C, Jeong D, Rojas-Muñoz A, et al: Inhibition of miR-25 improves cardiac contractility in the failing heart. Nature. 508:531–535. 2014. View Article : Google Scholar : PubMed/NCBI
39	Setyowati Karolina D, Sepramaniam S, Tan HZ, Armugam A and Jeyaseelan K: miR-25 and miR-92a regulate insulin I biosynthesis in rats. RNA Biol. 10:1365–1378. 2013. View Article : Google Scholar : PubMed/NCBI
40	Zhang H, Zuo Z, Lu X, Wang L, Wang H and Zhu Z: MiR-25 regulates apoptosis by targeting Bim in human ovarian cancer. Oncol Rep. 27:594–598. 2012.
41	Grossel MJ and Hinds PW: Beyond the cell cycle: a new role for Cdk6 in differentiation. J Cell Biochem. 97:485–493. 2006. View Article : Google Scholar
42	Pauls E, Ruiz A, Badia R, et al: Cell cycle control and HIV-1 susceptibility are linked by CDK6-dependent CDK2 phosphorylation of SAMHD1 in myeloid and lymphoid cells. J Immunol. 193:1988–1997. 2014. View Article : Google Scholar : PubMed/NCBI
43	Kohrt D, Crary J, Zimmer M, et al: CDK6 binds and promotes the degradation of the EYA2 protein. Cell Cycle. 13:62–71. 2014. View Article : Google Scholar :
44	Wu J, Qian J, Li C, et al: miR-129 regulates cell proliferation by downregulating Cdk6 expression. Cell Cycle. 9:1809–1818. 2010. View Article : Google Scholar : PubMed/NCBI
45	Dauphinot L, De Oliveira C, Melot T, et al: Analysis of the expression of cell cycle regulators in Ewing cell lines: EWS-FLI-1 modulates p57KIP2and c-Myc expression. Oncogene. 20:3258–3265. 2001. View Article : Google Scholar : PubMed/NCBI
46	Kollmann K and Sexl V: CDK6 and p16INK4A in lymphoid malignancies. Oncotarget. 4:1858–1859. 2013.PubMed/NCBI
47	Liu B, Han M, Sun RH, Wang JJ, Liu YP and Wen JK: Acetylbritannilactone induces G1 arrest and apoptosis in vascular smooth muscle cells. Int J Cardiol. 149:30–38. 2011. View Article : Google Scholar