Regulation of connective tissue growth factor and cardiac fibrosis by an SRF/MicroRNA-133a Axis

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Angelini, Aude ^a,b,c   Li, Zhenlin ^a,b,c   Mericskay, Mathias ^a,b,c   Decaux, Jean François ^a,b,c   Samuel, Jane Lise ^c  

^a SORBONNE UNIVERSITÉ   (France)

^b Université Pierre et Marie Curie   (France)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; DYE; FIBRONECTIN; MICRORNA; MICRORNA 133A; PROCOLLAGEN; PROCOLLAGEN TYPE 1 ALPHA1; PROCOLLAGEN TYPE 3 ALPHA1; SIRIUS RED; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SRF; UNCLASSIFIED DRUG; MIRN133 MICRORNA, MOUSE; SCLEROPROTEIN; SERUM RESPONSE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; ENZYME INHIBITION; ENZYME REGULATION; GENE EXPRESSION; HEART FAILURE; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RAT; STAINING; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CELL LINE; FIBROSIS; GENE EXPRESSION REGULATION; GENETICS; HEART DISEASE; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELL LINE; CONNECTIVE TISSUE GROWTH FACTOR; EXTRACELLULAR MATRIX PROTEINS; FIBROSIS; GENE EXPRESSION REGULATION; HEART DISEASES; MICE; MICE, TRANSGENIC; MICRORNAS; MYOCARDIUM; MYOCYTES, CARDIAC; RATS; SERUM RESPONSE FACTOR;

EID: 84947744763     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0139858     Document Type: Article

References (52)

1. Brower GL, Chancey AL, Thanigaraj S, Matsubara B.B., Janicki JS. Cause and effect relationship between myocardial mast cell number and matrix metalloproteinase activity. Am J Physiol Heart Circ Physiol. 2002 Aug; 283(2):H518-25. PMID: 12124196
2. Chancey AL, Brower GL, Janicki JS Cardiac mast cell-mediated activation of gelatinase and alteration of ventricular diastolic function. Am J Physiol Heart Circ Physiol. 2002 Jun; 282(6):H2152-8. PMID: 12003823
3. Stewart JA J.r., Wei CC, Brower G.L., Rynders PE, Hankes GH, Dillon AR, et al Cardiac mast cell-and chymase-mediated matrix metalloproteinase activity and left ventricular remodeling in mitral regurgitation in the dog. J Mol Cell Cardiol. 2003 Mar; 35(3):311-9. PMID: 12676546
4. Baudino TA, Carver W, Giles W., Borg TK. Cardiac fibroblasts: friend or foe? Am J Physiol Heart Circ Physiol. 2006 Sep; 291(3):H1015-26. PMID: 16617141
5. Kakkar R, Lee RT Intramyocardial fibroblast myocyte communication. Circ Res. 2010 Jan 8; 106 (1):47-57. doi: 10.1161/CIRCRESAHA.109.207456 PMID: 20056945
6. Manabe I, Shindo T, Nagai R. Gene expression in fibroblasts and fibrosis: involvement in cardiac hypertrophy. Circ Res. 2002 Dec 13; 91(12):1103-13. PMID: 12480810
7. Abreu JG, Ketpura NI, Reversade B, De Robertis EM. Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta. Nat Cell Biol. 2002 Aug; 4(8):599-604. PMID: 12134160
8. Blom IE, Goldschmeding R, Leask A. Gene regulation of connective tissue growth factor: new targets for antifibrotic therapy? Matrix Biol. 2002 Oct; 21(6):473-82. PMID: 12392758
9. Kuwahara K, Teg Pipes GC, McAnally J, Richardson JA, Hill J.A., Bassel-Duby R, et al. Modulation of adverse cardiac remodeling by STARS, a mediator of MEF2 signaling and SRF activity. J Clin Invest. 2007 May; 117(5):1324-34. PMID: 17415416
10. Miano JM, Ramanan N, Georger M.A., de Mesy Bentley KL, Emerson RL, Balza RO Jr, et al. Restricted inactivation of serum response factor to the cardiovascular system. Proc Natl Acad Sci USA. 2004 Dec 7; 101(49):17132-7. PMID: 15569937
11. Parlakian A, Tuil D, Hamard G., Tavernier G, Hentzen D., Concordet JP, et al. Targeted inactivation of serum response factor in the developing heart results in myocardial defects and embryonic lethality. Mol Cell Biol. 2004; 24:5281-9. PMID: 15169892
12. Zhang X, Chai J, Azhar G, Sheridan P., Borras AM, Furr MC, et al. Early postnatal cardiac changes and premature death in transgenic mice overexpressing a mutant form of serum response factor. J Biol Chem. 2001; 276:40033-40. PMID: 11514558
13. Parlakian A, Charvet C, Escoubet B., Mericskay M, Molkentin JD, Gary-Bobo G, et al. Temporally controlled onset of dilated cardiomyopathy through disruption of the SRF gene in adult heart. Circulation. 2005; 112:2930-9. PMID: 16260633
14. Diguet N, Mallat Y, Ladouce R., Clodic G, Prola A., Tritsch E, et al. Muscle creatine kinase deficiency triggers both actin depolymerization and desmin disorganization by advanced glycation end products in dilated cardiomyopathy. J Biol Chem. 2011 Oct 7; 286(40):35007-19. doi: 10.1074/jbc.M111.252395 PMID: 21768101
15. Touvron M, Escoubet B, Mericskay M., Angelini A, Lamotte L, Santini M.P., et al. Locally expressed IGF1 propeptide improves mouse heart function in induced dilated cardiomyopathy by blocking myocardial fibrosis and SRF-dependentCTGF induction. Dis Model Mech. 2012 Jul; 5(4):481-91. doi: 10.1242/dmm.009456 PMID: 22563064
16. Tritsch E, Mallat Y, Lefebvre F., Diguet N, Escoubet B, Blanc J., et al. An SRF/miR-1 axis regulates NCX1 and annexin A5 protein levels in the normal and failing heart. Cardiovasc Res. 2013 Jun 1; 98 (3):372-80. doi: 10.1093/cvr/cvt042 PMID: 23436819
17. Zhang X, Azhar G, Furr M.C., Zhong Y., Wei JY. Model of functional cardiac aging: young adult mice with mild overexpression of serum response factor. Am J Physiol Regul IntegrComp Physiol. 2003; 285: R552-R60. PMID: 12909581
18. Muehlich S, Cicha I, Garlichs C.D., Krueger B., Posern G, Goppelt-Struebe M. Actin-dependent regulation of connective tissue growth factor. Am J Physiol Cell Physiol. 2007 May; 292(5):C1732-8. PMID: 17215322
19. Spencer JA, Misra RP Expression of the serum response factor gene is regulated by serum response factor binding sites. J Biol Chem. 1996 Jul 12; 271(28):16535-43. PMID: 8663310
20. Chen JF, Mandel EM, Thomson J.M., Wu Q, Callis T.E., Hammond SM, et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet. 2006 Feb; 38 (2):228-33. PMID: 16380711
21. Duisters RF, Tijsen AJ, Schroen B, Leenders J.J., Lentink V, van der Made I, et al. miR-133andmiR-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodeling. Circ Res. 2009 Jan 30; 104(2):170-8. doi: 10.1161/CIRCRESAHA.108.182535 PMID: 19096030
22. Zhang X, Azhar G, Chai J., Sheridan P, Nagano K, Brown T., et al. Cardiomyopathy in transgenic mice with cardiac-specific overexpression of serum response factor. Am J Physiol Heart Circ Physiol. 2001; 280:H1782-H92. PMID: 11247792
23. Lin H, McGrath J, Wang P., Lee T. Cellular toxicity induced by SRF-mediated transcriptional squelching. Toxicol Sci. 2007 Mar; 96(1):83-91. PMID: 17116645
24. Prywes R, Zhu H. In vitro squelching of activated transcription by serum response factor: evidence for a common coactivator used by multiple transcriptional activators. Nucleic acids research. 1992 Feb 11; 20(3):513-20. PMID: 1531519
25. Belaguli NS, Sepulveda JL, Nigam V, Charron F., Nemer M, Schwartz RJ. Cardiac tissue enriched factors serum response factor and GATA-4 are mutual coregulators. Mol Cell Biol. 2000 Oct; 20 (20):7550-8. PMID: 11003651.
26. Chen CY, Schwartz RJ Recruitment of the tinman homolog Nkx-2.5 by serum response factor activates cardiac alpha-actin gene transcription. Mol Cell Biol. 1996 Nov; 16(11):6372-84. PMID: 8887666
27. Miano JM. Role of serum response factor in the pathogenesis of disease. Laboratory investigation; a journal of technical methods and pathology. 2010 Sep; 90(9):1274-84. doi: 10.1038/labinvest.2010.104 PMID: 20498652
28. Olson EN, Nordheim A. Linking actin dynamics and gene transcription to drive cellular motile functions. Nature reviews Molecular cell biology. 2010 May; 11(5):353-65. doi: 10.1038/nrm2890 PMID: 20414257
29. Menick DR, Renaud L, Buchholz A., Muller JG, Zhou H, Kappler CS, et al Regulation of Ncx1 gene expression in the normal and hypertrophic heart. Annals of the New York Academy of Sciences. 2007 Mar; 1099:195-203. PMID: 17446459
30. Stritt C, Stern S, Harting K., Manke T, Sinske D, Schwarz H., et al. Paracrine control of oligodendrocyte differentiation by SRF-directed neuronal gene expression. Nat Neurosci. 2009 Apr; 12(4):418-27. doi: 10.1038/nn.2280 PMID: 19270689
31. Sun Q, Chen G, Streb J.W., Long X, Yang Y., StoeckertCJ Jr, et al. Defining the mammalian CArGome. Genome Res. 2006 Feb; 16(2):197-207. PMID: 16365378
32. van Rooij E., Marshall WS, Olson EN Toward microRNA-based therapeutics for heart disease: the sense in antisense. Circ Res. 2008 Oct 24; 103(9):919-28. doi: 10.1161/CIRCRESAHA.108.183426 PMID: 18948630
33. van Rooij E., Olson EN MicroRNAs: powerful new regulators of heart disease and provocative therapeutic targets. J Clin Invest. 2007 Sep; 117(9):2369-76. PMID: 17786230.
34. Care A, Catalucci D, Felicetti F., Bonci D, Addario A, Gallo P., et al. MicroRNA-133 controls cardiac hypertrophy. Nat Med. 2007 May; 13(5):613-8. PMID: 17468766
35. Danowski N, Manthey I, Jakob H.G., Siffert W, Peters J., Frey UH. Decreased expression of miR-133a but not of miR-1 is associated with signs of heart failure in patients undergoing coronary bypass surgery. Cardiology. 2013; 125(2):125-30. doi: 10.1159/000348563 PMID: 23711953
36. Liu N, Bezprozvannaya S, Williams A.H., Qi X., Richardson JA, Bassel-Duby R, et al. microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev. 2008 Dec 1; 22(23):3242-54. doi: 10.1101/gad.1738708 PMID: 19015276
37. Matkovich SJ, Wang W, Tu Y., Eschenbacher WH, Dorn LE, Condorelli G, et al MicroRNA-133a protects against myocardial fibrosis and modulates electrical repolarization without affecting hypertrophy in pressure-overloaded adult hearts. Circ Res. 2010 Jan 8; 106(1):166-75. doi: 10.1161/CIRCRESAHA.109.202176 PMID: 19893015
38. Liu N, Olson EN MicroRNA regulatory networks in cardiovascular development. Dev Cell. 2010 Apr 20; 18(4):510-25. doi: 10.1016/j.devcel.2010.03.010 PMID: 20412767
39. Koitabashi N, Arai M, Kogure S., Niwano K, Watanabe A, Aoki Y., et al. Increased connective tissue growth factor relative to brain natriuretic peptide as a determinant of myocardial fibrosis. Hypertension. 2007 May; 49(5):1120-7. PMID: 17372041
40. Matsui Y, Sadoshima J. Rapid upregulation of CTGF in cardiac myocytes by hypertrophic stimuli: implication for cardiac fibrosis and hypertrophy. J Mol Cell Cardiol. 2004 Aug; 37(2):477-81. PMID: 15276017
41. Ohnishi H, Oka T, Kusachi S., Nakanishi T, Takeda K, Nakahama M., et al. Increased expression of connective tissue growth factor in the infarct zone of experimentally induced myocardial infarction in rats. J Mol Cell Cardiol. 1998 Nov; 30(11):2411-22. PMID: 9925376
42. Shi-Wen X., Leask A, Abraham D. Regulation and function of connective tissue growth factor/CCN2 in tissue repair, scarring and fibrosis. Cytokine Growth Factor Rev. 2008 Apr; 19(2): 133-44. doi: 10.1016/j.cytogfr.2008.01.002 PMID: 18358427
43. Daniels JT, Schultz GS, Blalock TD, Garrett Q, Grotendorst G.R., Dean NM, et al. Mediation of transforming growth factor-beta(1)-stimulated matrix contraction by fibroblasts: a role for connective tissue growth factor in contractile scarring. Am J Pathol. 2003 Nov; 163(5):2043-52. PMID: 14578203
44. Frazier K, Williams S, Kothapalli D., Klapper H, Grotendorst GR. Stimulation of fibroblast cell growth, matrix production, and granulation tissue formation by connective tissue growth factor. The Journal of investigative dermatology. 1996 Sep; 107(3):404-11. PMID: 8751978
45. Grotendorst GR, Rahmanie H, Duncan MR Combinatorial signaling pathways determine fibroblast proliferation and myofibroblast differentiation. FASEB J. 2004 Mar; 18(3):469-79. PMID: 15003992
46. Szabo Z, Magga J, Alakoski T., Ulvila J, Piuhola J, Vainio L., et al. Connective tissue growth factor inhibition attenuates left ventricular remodeling and dysfunction in pressure overload-induced heart failure. Hypertension. 2014 Jun; 63(6):1235-40. doi: 10.1161/HYPERTENSIONAHA.114.03279 PMID: 24688123
47. Yang M, Huang H, Li J., Li D, Wang H. Tyrosine phosphorylation of the LDL receptor-related protein (LRP) and activation of the ERK pathway are required for connective tissue growth factor to potentiate myofibroblast differentiation. FASEB J. 2004 Dec; 18(15):1920-1. PMID: 15469966
48. Zhang C, Meng X, Zhu Z., Yang X, Deng A. Role of connective tissue growth factor in renal tubular epithelial-myofibroblasttransdifferentiation and extracellular matrix accumulation in vitro. Life sciences. 2004 Jun 4; 75(3):367-79. PMID: 15135656
49. Camelliti P, Borg TK, Kohl P. Structural and functional characterisation of cardiac fibroblasts. Cardiovasc Res. 2005 Jan 1; 65(1):40-51. PMID: 15621032
50. Chen MM, Lam A, Abraham J.A., Schreiner GF, Joly AH. CTGF expression is induced byTGF-betain cardiac fibroblasts and cardiac myocytes: a potential role in heart fibrosis. J Mol Cell Cardiol. 2000 Oct; 32(10):1805-19. PMID: 11013125
51. Arimura T, Takeya R, Ishikawa T, Yamano T., Matsuo A, Tatsumi T, et al Dilated cardiomyopathy-asso-ciated FHOD3 variant impairs the ability to induce activation of transcription factor serum response factor. Circulation journal: official journal of the Japanese Circulation Society. 2013; 77(12):2990-6.
52. Ho CY, Jaalouk DE, Vartiainen M.K., Lammerding J. Lamin A/C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature. 2013 May 23; 497 (7450):507-11. doi: 10.1038/nature12105 PMID: 23644458