MicroRNA-34a Induces Vascular Smooth Muscle Cells Senescence by SIRT1 Downregulation and Promotes the Expression of Age-Associated Pro-inflammatory Secretory Factors

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 70, Issue 11, 2015, Pages 1304-1311

  Badi, Ileana ^a   Burba, Ilaria ^a,b   Ruggeri, Clarissa ^a   Zeni, Filippo ^a   Bertolotti, Matteo ^a   Scopece, Alessandro ^a   Pompilio, Giulio ^a   Raucci, Angela ^a  

^a CENTRO CARDIOLOGICO MONZINO   (Italy)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Inflammation; MiR 34a; SASP; SIRT1; Vascular aging

Indexed keywords

MICRORNA; MIRN34 MICRORNA, HUMAN; MIRN34 MICRORNA, MOUSE; SIRT1 PROTEIN, HUMAN; SIRT1 PROTEIN, MOUSE; SIRTUIN 1;

ANIMAL; AORTA; CELL AGING; CULTURE TECHNIQUE; ENDOTHELIUM CELL; GENETICS; HUMAN; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; SMOOTH MUSCLE FIBER;

ANIMALS; AORTA; CELL AGING; CELL CULTURE TECHNIQUES; ENDOTHELIAL CELLS; HUMANS; MICE; MICRORNAS; MYOCYTES, SMOOTH MUSCLE; SIRTUIN 1;

EID: 84946616107     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glu180     Document Type: Article

References (56)

1. Lakatta EG, Levy D. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: Part I: aging arteries: a "set up" for vascular disease. Circulation. 2003;107:139-146. doi:10.1161/01. CIR.0000048892.83521.58
2. Wang M, Jiang L, Monticone RE, Lakatta EG. Proinflammation: the key to arterial aging. Trends Endocrinol Metab. 2014;25:72-79. doi:10.1016/j. tem.2013.10.002
3. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS. The essence of senescence. Genes Dev. 2010;24:2463-2479. doi:10.1101/gad.1971610
4. Salama R, Sadaie M, Hoare M, Narita M. Cellular senescence and its effector programs. Genes Dev. 2014;28:99-114. doi:10.1101/gad.235184.113
5. Campisi J. Cellular senescence: putting the paradoxes in perspective. Curr Opin Genet Dev. 2011;21:107-112. doi:10.1016/j.gde.2010.10.005
6. Song Y, Shen H, Schenten D, Shan P, Lee PJ, Goldstein DR. Aging enhances the basal production of IL-6 and CCL2 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2012;32:103-109. doi:10.1161/ATVBAHA.111.236349
7. Bartel DP. Micro RNAs: target recognition and regulatory functions. Cell. 2009;136:215-233. doi:10.1016/j.cell.2009.01.002
8. Thum T. Micro RNA therapeutics in cardiovascular medicine. EMBO Mol Med. 2012;4:3-14. doi:10.1002/emmm.201100191
9. van Rooij E, Olson EN. Micro RNA therapeutics for cardiovascular disease: opportunities and obstacles. Nat Rev Drug Discov. 2012;11:860-872. doi:10.1038/nrd3864
10. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ. 2010;17:193-199. doi:10.1038/cdd.2009.56
11. Concepcion CP, Han YC, Mu P, et al.et al. Intact p53-dependent responses in miR-34-deficient mice. PLoS Genet. 2012;8:e1002797. doi:10.1371/journal.pgen.1002797
12. Okada N, Lin CP, Ribeiro MC, et al.et al. A positive feedback between p53 and miR-34 miRNAs mediates tumor suppression. Genes Dev. 2014;28:438-450. doi:10.1101/gad.233585.113
13. Dimmeler S, Nicotera P. Micro RNAs in age-related diseases. EMBO Mol Med. 2013;5:180-190. doi:10.1002/emmm.201201986
14. Boon RA, Iekushi K, Lechner S, et al.et al. Micro RNA-34a regulates cardiac ageing and function. Nature. 2013;495:107-110. doi:10.1038/nature11919
15. Ito T, Yagi S, Yamakuchi M. Micro RNA-34a regulation of endothelial senescence. Biochem Biophys Res Commun. 2010;398:735-740. doi:10.1016/j.bbrc.2010.07.012
16. Li X, Khanna A, Li N, Wang E. Circulatory miR34a as an RNAbased, noninvasive biomarker for brain aging. Aging (Albany NY). 2011;3:985-1002.
17. Xu Q, Seeger FH, Castillo J, et al.et al. Micro-RNA-34a contributes to the impaired function of bone marrow-derived mononuclear cells from patients with cardiovascular disease. J Am Coll Cardiol. 2012;59:2107-2117. doi:10.1016/j.jacc.2012.02.033
18. Mudduluru G, Ceppi P, Kumarswamy R, Scagliotti GV, Papotti M, Allgayer H. Regulation of Axl receptor tyrosine kinase expression by miR- 34a and miR-199a/b in solid cancer. Oncogene. 2011;30:2888-2899. doi:10.1038/onc.2011.13
19. Melaragno MG, Fridell YW, Berk BC. The Gas6/Axl system: a novel regulator of vascular cell function. Trends Cardiovasc Med. 1999;9:250-253. doi:10.1016/S1050-1738(00)00027-X
20. Nishio E, Watanabe Y. Oxysterols induced apoptosis in cultured smooth muscle cells through CPP32 protease activation and bcl-2 protein downregulation. Biochem Biophys Res Commun. 1996;226:928-934. doi:10.1006/bbrc.1996.1452
21. Chang TC, Wentzel EA, Kent OA, et al.et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell. 2007;26:745-752. doi:10.1016/j.molcel.2007.05.010
22. Yamakuchi M, Ferlito M, Lowenstein CJ. miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci USA. 2008;105:13421-13426. doi:10.1073/pnas.0801613105
23. Stein S, Matter CM. Protective roles of SIRT1 in atherosclerosis. Cell Cycle. 2011;10:640-647. doi:10.4161/cc.10.4.14863
24. Dimri GP, Lee X, Basile G, et al.et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA. 1995;92:9363-9367.
25. Burton DG, Giles PJ, Sheerin AN, et al.et al. Microarray analysis of senescent vascular smooth muscle cells: a link to atherosclerosis and vascular calcification. Exp Gerontol. 2009;44:659-665. doi:10.1016/j.exger.2009.07. 004
26. Tanner FC, Boehm M, Akyürek LM, et al.et al. Differential effects of the cyclin-dependent kinase inhibitors p27(Kip1), p21(Cip1), and p16(Ink4) on vascular smooth muscle cell proliferation. Circulation. 2000;101:2022-2025. doi:10.1161/01.CIR.101.17.2022
27. Gorenne I, Kumar S, Gray K, et al.et al. Vascular smooth muscle cell sirtuin 1 protects against DNA damage and inhibits atherosclerosis. Circulation. 2013;127:386-396. doi:10.1161/CIRCULATIONAHA.112.124404
28. Yoshizaki T, Milne JC, Imamura T, et al.et al. SIRT1 exerts anti-inflammatory effects and improves insulin sensitivity in adipocytes. Mol Cell Biol. 2009;29:1363-1374. doi:10.1128/MCB.00705-08
29. Csiszar A, Sosnowska D, Wang M, Lakatta EG, Sonntag WE, Ungvari Z. Age-associated proinflammatory secretory phenotype in vascular smooth muscle cells from the non-human primate Macaca mulatta: reversal by resveratrol treatment. J Gerontol A Biol Sci Med Sci. 2012;67:811-820. doi:10.1093/gerona/glr228
30. Wang JC, Bennett M. Aging and atherosclerosis: mechanisms, functional consequences, and potential therapeutics for cellular senescence. Circ Res. 2012;111:245-259. doi:10.1161/CIRCRESAHA
31. Feil S, Hofmann F, Feil R. SM22alpha modulates vascular smooth muscle cell phenotype during atherogenesis. Circ Res. 2004;94:863-865. doi:10.1161/01.RES.0000126417.38728.F6
32. Han M, Dong LH, Zheng B, Shi JH, Wen JK, Cheng Y. Smooth muscle 22 alpha maintains the differentiated phenotype of vascular smooth muscle cells by inducing filamentous actin bundling. Life Sci. 2009;84:394-401. doi:10.1016/j.lfs.2008.11.017
33. Yao H, Chung S, Hwang JW, et al.et al. SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice. J Clin Invest. 2012;122:2032-2045. doi:10.1172/JCI60132
34. Yamamoto H, Schoonjans K, Auwerx J. Sirtuin functions in health and disease. Mol Endocrinol. 2007;21:1745-1755. doi:10.1210/me.2007-0079
35. Borradaile NM, Pickering JG. NAD(+), sirtuins, and cardiovascular disease. Curr Pharm Des. 2009;15:110-117. doi:10.2174/138161209787185742
36. Takemura A, Iijima K, Ota H, et al.et al. Sirtuin 1 retards hyperphosphatemia-induced calcification of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2011;31:2054-2062. doi:10.1161/ATVBAHA.110.216739
37. Nakano-Kurimoto R, Ikeda K, Uraoka M, et al.et al. Replicative senescence of vascular smooth muscle cells enhances the calcification through initiating the osteoblastic transition. Am J Physiol Heart Circ Physiol. 2009;297:H1673-H1684. doi:10.1152/ajpheart.00455.2009
38. Ho C, van der Veer E, Akawi O, Pickering JG. SIRT1 markedly extends replicative lifespan if the NAD+ salvage pathway is enhanced. FEBS Lett. 2009;583:3081-3085. doi:10.1016/j.febslet.2009.08.031
39. Li L, Zhang HN, Chen HZ, et al.et al. SIRT1 acts as a modulator of neointima formation following vascular injury in mice. Circ Res. 2011;108:1180-1189. doi:10.1161/CIRCRESAHA.110.237875
40. Qiang L, Lin HV, Kim-Muller JY, Welch CL, Gu W, Accili D. Proatherogenic abnormalities of lipid metabolism in SirT1 transgenic mice are mediated through Creb deacetylation. Cell Metab. 2011;14:758-767. doi:10.1016/j.cmet.2011.10.007
41. van Rooij E, Purcell AL, Levin AA. Developing micro RNA therapeutics. Circ Res. 2012;110:496-507. doi:10.1161/CIRCRESAHA.111.247916
42. Breland UM, Halvorsen B, Hol J, et al.et al. A potential role of the CXC chemokine GROalpha in atherosclerosis and plaque destabilization: downregulatory effects of statins. Arterioscler Thromb Vasc Biol. 2008;28:1005-1011. doi:10.1161/ATVBAHA.108.162305
43. Xie L, Tsaprailis G, Chen QM. Proteomic identification of insulin-like growth factor-binding protein-6 induced by sublethal H2O2 stress from human diploid fibroblasts. Mol Cell Proteomics. 2005;4:1273-1283. doi:10.1074/mcp.M500032-MCP200
44. Liu Y, Drozdov I, Shroff R, Beltran LE, Shanahan CM. Prelamin A accelerates vascular calcification via activation of the DNA damage response and senescence-associated secretory phenotype in vascular smooth muscle cells. Circ Res. 2013;112:e99-e109. doi:10.1161/CIRCRESAHA.111.300543
45. Acosta JC, O'Loghlen A, Banito A, et al.et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell. 2008;133:1006-1018. doi:10.1016/j.cell.2008.03.038
46. Abedin M, Lim J, Tang TB, Park D, Demer LL, Tintut Y. N-3 fatty acids inhibit vascular calcification via the p38-mitogen-activated protein kinase and peroxisome proliferator-activated receptor-gamma pathways. Circ Res. 2006;98:727-729. doi:10.1161/01.RES.0000216009.68958.e6
47. Couffinhal T, Duplàa C, Moreau C, Lamazière JM, Bonnet J. Regulation of vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 in human vascular smooth muscle cells. Circ Res. 1994;74:225-234. doi:10.1161/01.RES.74.2.225
48. Massberg S, Vogt F, Dickfeld T, Brand K, Page S, Gawaz M. Activated platelets trigger an inflammatory response and enhance migration of aortic smooth muscle cells. Thromb Res. 2003;110:187-194. doi:10.1016/S0049-3848(03)00342-6
49. Clément N, Gueguen M, Glorian M, et al.et al. Notch3 and IL-1beta exert opposing effects on a vascular smooth muscle cell inflammatory pathway in which NF-kappaB drives crosstalk. J Cell Sci. 2007;120(Pt 19):3352-3361. doi:10.1242/jcs.007872
50. Bennett BJ, Scatena M, Kirk EA, et al.et al. Osteoprotegerin inactivation accelerates advanced atherosclerotic lesion progression and calcification in older ApoE-/- mice. Arterioscler Thromb Vasc Biol. 2006;26:2117-2124. doi:10.1161/01.ATV.0000236428.91125.e6
51. Callegari A, Coons ML, Ricks JL, Rosenfeld ME, Scatena M. Increased calcification in osteoprotegerin-deficient smooth muscle cells: dependence on receptor activator of NF-κB ligand and interleukin 6. J Vasc Res. 2014;51:118-131. doi:10.1159/000358920
52. Shan Z, Yao C, Li ZL, et al.et al. Differentially expressed micro RNAs at different stages of atherosclerosis in ApoE-deficient mice. Chin Med J (Engl). 2013;126:515-520.
53. Raitoharju E, Lyytikäinen LP, Levula M, et al.et al. miR-21, miR-210, miR- 34a, and miR-146a/b are up-regulated in human atherosclerotic plaques in the Tampere Vascular Study. Atherosclerosis. 2011;219:211-217. doi:10.1016/j.atherosclerosis.2011.07.020
54. Fabbri M, Paone A, Calore F, et al.et al. Micro RNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA. 2012;109:E2110-E2116. doi:10.1073/pnas.1209414109
55. Fabbri M, Paone A, Calore F, Galli R, Croce CM. A new role for microRNAs, as ligands of Toll-like receptors. RNA Biol. 2013;10:169-174. doi:10.4161/rna.23144
56. He WA, Calore F, Londhe P, Canella A, Guttridge DC, Croce CM. Microvesicles containing miRNAs promote muscle cell death in cancer cachexia via TLR7. Proc Natl Acad Sci USA. 2014;111:4525-4529. doi:10.1073/pnas.1402714111