MicroRNA-150 Inhibits the Activation of Cardiac Fibroblasts by Regulating c-Myb

Cellular Physiology and Biochemistry

Volumn 38, Issue 6, 2016, Pages 2103-2122

  Deng, Peng ^a   Chen, Ling ^b   Liu, Zheng ^c   Ye, Ping ^d   Wang, Sihua ^a   Wu, Jie ^a   Yao, Yufeng ^e   Sun, Yuan ^a   Huang, Xiaofan ^a   Ren, Linyun ^a   Zhang, Anchen ^a   Wang, Ke ^a   Wu, Chuangyan ^a   Yue, Zhang ^a   Xu, Xuezeng ^d   Chen, Manhua ^b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b CENTRAL HOSPITAL OF WUHAN   (China)

^c SICHUAN UNIVERSITY   (China)

^d FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^e HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

c Myb; Cardiac fibroblast; Cardiac fibrosis; Mir 150; Myofibroblast

Indexed keywords

MICRORNA; MICRORNA 150; PROTEIN C MYB; UNCLASSIFIED DRUG; MIRN150 MICRORNA, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL MIGRATION; CELL PROLIFERATION; DOWN REGULATION; HEART FIBROBLAST; HEART MUSCLE FIBROSIS; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSTHORACIC ECHOCARDIOGRAPHY; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; CARDIOMYOPATHY; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DISEASE MODEL; FIBROBLAST; FIBROSIS; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; MYOFIBROBLAST; PATHOLOGY;

ANIMALS; CARDIOMYOPATHIES; CELL DIFFERENTIATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FIBROBLASTS; FIBROSIS; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; MYOCARDIUM; MYOFIBROBLASTS; PROTO-ONCOGENE PROTEINS C-MYB;

EID: 84969631872     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000445568     Document Type: Article

References (56)

1. Camelliti P, Borg TK, Kohl P: Structural and functional characterisation of cardiac fibroblasts. Circ Res 2005;65:40-51.
2. Souders CA, Bowers SL, Baudino TA: Cardiac fibroblast: The renaissance cell. Circ Res 2009;105:1164-1176.
3. Abramochkin DV, Lozinsky IT, Kamkin A: Influence of mechanical stress on fibroblast-myocyte interactions in mammalian heart. J Mol cell Cardiol 2014;70:27-36.
4. Porter KE, Turner NA: Cardiac fibroblasts: At the heart of myocardial remodeling. Pharmacol Ther 2009;123:255-278.
5. Ubil E, Duan J, Pillai IC, Rosa-Garrido M, Wu Y, Bargiacchi F, Lu Y, Stanbouly S, Huang J, Rojas M, Vondriska TM, Stefani E, Deb A: Mesenchymal-endothelial transition contributes to cardiac neovascularization. Nature 2014;514:585-590.
6. Shinde AV, Frangogiannis NG: Fibroblasts in myocardial infarction: A role in inflammation and repair. J Mol Cell Cardiol 2014;70:74-82.
7. Chaturvedi RR, Herron T, Simmons R, Shore D, Kumar P, Sethia B, Chua F, Vassiliadis E, Kentish JC: Passive stiffness of myocardium from congenital heart disease and implications for diastole. Circulation 2010;121:979-988.
8. Kai H, Mori T, Tokuda K, Takayama N, Tahara N, Takemiya K, Kudo H, Sugi Y, Fukui D, Yasukawa H, Kuwahara F, Imaizumi T: Pressure overload-induced transient oxidative stress mediates perivascular inflammation and cardiac fibrosis through angiotensin II. Hypertens Res 2006;29:711-718.
9. Bartel DP: Micrornas: Genomics, biogenesis, mechanism, and function. Cell 2004;116:281-297.
10. Lewis BP, Burge CB, Bartel DP: Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microrna targets. Cell 2005;120:15-20.
11. Ambros V: The functions of animal micrornas. Nature 2004;431:350-355.
12. Kloosterman WP, Plasterk RH: The diverse functions of micrornas in animal development and disease. Dev Cell 2006;11:441-450.
13. Hata A: Functions of micrornas in cardiovascular biology and disease. Annu Rev Physiol 2013;75:69-93.
14. Condorelli G, Latronico MV, Cavarretta E: Micrornas in cardiovascular diseases: Current knowledge and the road ahead. J Am Coll Cardiol 2014;63:2177-2187.
15. Zhao X, Wang K, Liao Y, Zeng Q, Li Y, Hu F, Liu Y, Meng K, Qian C, Zhang Q, Guan H, Feng K, Zhou Y, Du Y, Chen Z: Microrna-lOla inhibits cardiac fibrosis induced by hypoxia via targeting tgfbetari on cardiac fibroblasts. Cell Physiol Biochem 2015;35:213-226.
16. Melo SF, Fernandes T, Barauna VG, Matos KC, Santos AA, Tucci PJ, Oliveira EM: Expression of microrna-29 and collagen in cardiac muscle after swimming training in myocardial-infarcted rats. Cell Physiol Biochem 2014;33:657-669.
17. van Rooij E, Olson EN: Micrornas: Powerful new regulators of heart disease and provocative therapeutic targets. J Clin Invest 2007;117:2369-2376.
18. Tijsen AJ, Pinto YM, Creemers EE: Circulating micrornas as diagnostic biomarkers for cardiovascular diseases. Am J Physiol Heart Circ Physiol 2012;303:H1085-1095.
19. Gupta SK, Bang C, Thum T: Circulating micrornas as biomarkers and potential paracrine mediators of cardiovascular disease. Circ Cardiovasc Genet 2010;3:484-488.
20. van Rooij E, Sutherland LB, Liu N, Williams AH, McAnally J, Gerard RD, Richardson JA, Olson EN: A signature pattern of stress-responsive micrornas that can evoke cardiac hypertrophy and heart failure. Proc Natl Acad Sci U S A 2006;103:18255-18260.
21. Devaux Y, Vausort M, McCann GP, Zangrando J, Kelly D, Razvi N, Zhang L, Ng LL, Wagner DR, Squire IB: Microrna-150: A novel marker of left ventricular remodeling after acute myocardial infarction. Circ Cardiovasc Genet 2013;6:290-298.
22. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, Hill JA, Olson EN: Dysregulation of micrornas after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 2008;105:13027-13032.
23. Liu Z, Zhou C, Liu Y, Wang S, Ye P, Miao X, Xia J: The expression levels of plasma micornas in atrial fibrillation patients. PLoS One 2012;7:e44906.
24. Liu Z, Ye P, Wang S, Wu J, Sun Y, Zhang A, Ren L, Cheng C, Huang X, Wang K, Deng P, Wu C, Yue Z, Xia J: Microrna-150 protects the heart from injury by inhibiting monocyte accumulation in a mouse model of acute myocardial infarction. Circ Cardiovasc Genet 2015;8:11-20.
25. Huang ZP, Chen J, Seok HY, Zhang Z, Kataoka M, Hu X, Wang DZ: Microrna-22 regulates cardiac hypertrophy and remodeling in response to stress. Circ Res 2013;112:1234-1243.
26. Pan Z, Sun X, Shan H, Wang N, Wang J, Ren J, Feng S, Xie L, Lu C, Yuan Y, Zhang Y, Wang Y, Lu Y, Yang B: Microrna-101 inhibited postinfarct cardiac fibrosis and improved left ventricular compliance via the fbj osteosarcoma oncogene/transforming growth factor-betal pathway. Circulation 2012;126:840-850.
27. Yin K, Zhao L, Feng D, Ma W, Liu Y, Wang Y, Liang J, Yang F, Bi C, Chen H, Li X, Lu Y, Cai B: Resveratrol attenuated low ambient temperature-induced myocardial hypertrophy via inhibiting cardiomyocyte apoptosis. Cell Physiol Biochem 2015;35:2451-2462.
28. Sayed D, Hong C, Chen IY, Lypowy J, Abdellatif M: Micrornas play an essential role in the development of cardiac hypertrophy. Circ Res 2007;100:416-424.
29. Cheng Y, Ji R, Yue J, Yang J, Liu X, Chen H, Dean DB, Zhang C: Micrornas are aberrantly expressed in hypertrophic heart: Do they play a role in cardiac hypertrophy? Am J Pathol 2007;170:1831-1840.
30. Tatsuguchi M, Seok HY, Callis TE, Thomson JM, Chen JF, Newman M, Rojas M, Hammond SM, Wang DZ: Expression of micrornas is dynamically regulated during cardiomyocyte hypertrophy. J Mol Cell Cardiol 2007;42:1137-1141.
31. Xiao C, Calado DP, Galler G, Thai TH, Patterson HC, Wang J, Rajewsky N, Bender TP, Rajewsky K: Mir-150 controls b cell differentiation by targeting the transcription factor c-myb. Cell 2007;131:146-159.
32. Bezman NA, Chakraborty T, Bender T, Lanier LL: Mir-150 regulates the development of nk and inkt cells. J Exp Med 2011;208:2717-2731.
33. Pimentel DR, Adachi T, Ido Y, Heibeck T, Jiang B, Lee Y, Melendez JA, Cohen RA, Colucci WS: Strain-stimulated hypertrophy in cardiac myocytes is mediated by reactive oxygen species-dependent ras s-glutathiolation. J Mol Cell Cardiol 2006;41:613-622.
34. Oka T, Komuro I: Molecular mechanisms underlying the transition of cardiac hypertrophy to heart failure. Circ J 2008;72 Suppl AA13-16.
35. Carver W, Nagpal ML, Nachtigal M, Borg TK, Terracio L: Collagen expression in mechanically stimulated cardiac fibroblasts. Circ Res 1991;69:116-122.
36. Takeda N, Manabe I, Uchino Y, Eguchi K, Matsumoto S, Nishimura S, Shindo T, Sano M, Otsu K, Snider R Conway SJ, Nagai R: Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J Clin Invest 2010;120:254-265.
37. Kakkar R, Lee RT: Intramyocardial fibroblast myocyte communication. Circ Res 2010;106:47-57.
38. Fredj S, Bescond J, Louault C, Potreau D: Interactions between cardiac cells enhance cardiomyocyte hypertrophy and increase fibroblast proliferation. J Cell Physiol 2005;202:891-899.
39. LaFramboise WA, Scalise D, Stoodley P, Graner SR, Guthrie RD, Magovern JA, Becich MJ: Cardiac fibroblasts influence cardiomyocyte phenotype in vitro. Am J Physiol Cell Physiol 2007;292:C1799-1808.
40. Bang C, Batkai S, Dangwal S, Gupta SK, Foinquinos A, Holzmann A, Just A, Remke J, Zimmer K, Zeug A, Ponimaskin E, Schmiedl A, Yin X, Mayr M, Haider R, Fischer A, Engelhardt S, Wei Y, Schober A, Fiedler J, Thum T: Cardiac fibroblast-derived microrna passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J Clin Invest 2014;124:2136-2146.
41. Lajiness JD, Conway SJ: Origin, development, and differentiation of cardiac fibroblasts. J Mol Cell Cardiol 2014;70:2-8.
42. Moore-Morris T, Guimaraes-Camboa N, Banerjee I, Zambon AC, Kisseleva T, Velayoudon A, Stallcup WB, Gu Y, Dalton ND, Cedenilla M, Gomez-Amaro R, Zhou B, Brenner DA, Peterson KL, Chen J, Evans SM: Resident fibroblast lineages mediate pressure overload-induced cardiac fibrosis. J Clin Invest 2014;124:2921-2934.
43. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N: Combinatorial microrna target predictions. Nat Genet 2005;37:495-500.
44. Bender TP, Kremer CS, Kraus M, Buch T, Rajewsky K: Critical functions for c-myb at three checkpoints during thymocyte development. Nat Immunol 2004;5:721-729.
45. Thomas MD, Kremer CS, Ravichandran KS, Rajewsky K, Bender TP: C-myb is critical for b cell development and maintenance of follicular b cells. Immunity 2005;23:275-286.
46. Piccinini G, Golay J, Flora A, Songia S, Luchetti M, Gabrielli A, Introna M: C-myb, but not b-myb, upregulates type i collagen gene expression in human fibroblasts. J Invest Dermatol 1999;112:191-196.
47. Luchetti MM, Paroncini P, Majlingova P, Frampton J, Mucenski M, Baroni SS, Sambo P, Golay J, Introna M, Gabrielli A: Characterization of the c-myb-responsive region and regulation of the human type i collagen alpha 2 chain gene by c-myb. J Biol Chem 2003;278:1533-1541.
48. Kopecki Z, Luchetti MM, Adams DH, Strudwick X, Mantamadiotis T, Stoppacciaro A, Gabrielli A, Ramsay RG, Cowin AJ: Collagen loss and impaired wound healing is associated with c-myb deficiency. J Pathol 2007;211:351-361.
49. Ma HH, Yao JL, Li G, Yao CL, Chen XJ, Yang SJ: Effects of c-myb antisense rna on tgf-betal and betal-i collagen expression in cultured hepatic stellate cells. World J Gastroenterol 2004;10:3662-3665.
50. van den Borne SW, Diez J, Blankesteijn WM, Verjans J, Hofstra L, Narula J: Myocardial remodeling after infarction: The role of myofibroblasts. Nat Rev Cardiol 2010;7:30-37.
51. Buck M, Kim DJ, Houglum K, Hassanein T, Chojkier M: C-myb modulates transcription of the alpha-smooth muscle actin gene in activated hepatic stellate cells. Am j Physiol Gastrointest Liver Physiol 2000;278:G321-328.
52. Kolodziejska KM, Noyan-Ashraf MH, Nagy A, Bacon A, Frampton J, Xin HB, Kotlikoff MI, Husain M: C-myb-dependent smooth muscle cell differentiation. Circ Res 2008;102:554-561.
53. Liu W, Liu Y, Zhang Y, Zhu X, Zhang R, Guan L, Tang Q, Jiang H, Huang C, Huang H: Microrna-150 protects against pressure overload-induced cardiac hypertrophy. J Cell Biochem 2015;116:2166-76.
54. Tang Y, Wang Y, Park KM, Hu Q, Teoh JP, Broskova Z, Ranganathan P, Jayakumar C, Li J, Su H, Tang Y, Ramesh G, Kim IM: Microrna-150 protects the mouse heart from ischaemic injury by regulating cell death. Cardiovasc Res 2015;106:387-397.
55. Tardiff JC: Sarcomeric proteins and familial hypertrophic cardiomyopathy: Linking mutations in structural proteins to complex cardiovascular phenotypes. Heart Fail Rev 2005;10:237-248.
56. Debold EP, Schmitt JP, Patlak JB, Beck SE, Moore JR, Seidman JG, Seidman C, Warshaw DM: Hypertrophic and dilated cardiomyopathy mutations differentially affect the molecular force generation of mouse alpha-cardiac myosin in the laser trap assay. Am J Physiol Heart Circ Physiol 2007;293:H284-291.