Journal of Molecular and Cellular Cardiology
Volume 48, Issue 3 , Pages 461-467 , March 2010

Extracellular matrix remodeling in atrial fibrosis: Mechanisms and implications in atrial fibrillation

Received 29 May 2009 ,Revised 29 August 2009 ,Accepted 2 September 2009.

References 

  1. Weber KT, Brilla CG. Pathological hypertrophy and cardiac interstitium. Fibrosis and renin–angiotensin–aldosterone system. Circulation. 1991;83:1849–1865
  2. Mazzini MJ, Monahan KM. Pharmacotherapy for atrial arrhythmias: present and future. Heart Rhythm. 2008;5:S26–31
  3. Callans DJ. Apples and oranges: comparing antiarrhythmic drugs and catheter ablation for treatment of atrial fibrillation. Circulation. 2008;118:2488–2490
  4. Bajpai A, Savelieva I, Camm AJ. Treatment of atrial fibrillation. Br. Med. Bull. 2008;88:75–94
  5. Kagitani S, Ueno H, Hirade S, Takahashi T, Takata M, Inoue H. Tranilast attenuates myocardial fibrosis in association with suppression of monocyte/macrophage infiltration in DOCA/salt hypertensive rats. J. Hypertens. 2004;22:1007–1015
  6. Brilla CG, Matsubara LS, Weber KT. Anti-aldosterone treatment and the prevention of myocardial fibrosis in primary and secondary hyperaldosteronism. J. Mol. Cell. Cardiol. 1993;25:563–575
  7. Brilla CG, Pick R, Tan LB, Janicki JS, Weber KT. Remodeling of the rat right and left ventricles in experimental hypertension. Circ. Res. 1990;67:1355–1364
  8. Yang SS, Han W, Zhou HY, Dong G, Wang BC, Huo H, et al. Effects of spironolactone on electrical and structural remodeling of atrium in congestive heart failure dogs. Chin. Med. J. (Engl). 2008;121:38–42
  9. Robert V, Heymes C, Silvestre JS, Sabri A, Swynghedauw B, Delcayre C. Angiotensin AT1 receptor subtype as a cardiac target of aldosterone: role in aldosterone-salt-induced fibrosis. Hypertension. 1999;33:981–986
  10. Johar S, Cave AC, Narayanapanicker A, Grieve DJ, Shah AM. Aldosterone mediates angiotensin II-induced interstitial cardiac fibrosis via a Nox2-containing NADPH oxidase. FASEB J. 2006;20:1546–1548
  11. Thiedemann KU, Ferrans VJ. Left atrial ultrastructure in mitral valvular disease. Am. J. Pathol. 1977;89:575–604
  12. Frustaci A, Chimenti C, Bellocci F, Morgante E, Russo MA, Maseri A. Histological substrate of atrial biopsies in patients with lone atrial fibrillation. Circulation. 1997;96:1180–1184
  13. Remes J, van Brakel TJ, Bolotin G, Garber C, de Jong MM, van der Veen FH, et al. Persistent atrial fibrillation in a goat model of chronic left atrial overload. J. Thorac. Cardiovasc. Surg. 2008;136:1005–1011
  14. Verheule S, Sato T, Everett Tt, Engle SK, Otten D, Rubart-von der Lohe M, et al. Increased vulnerability to atrial fibrillation in transgenic mice with selective atrial fibrosis caused by overexpression of TGF-beta1. Circ. Res. 2004;94:1458–1465
  15. Sanfilippo AJ, Abascal VM, Sheehan M, Oertel LB, Harrigan P, Hughes RA, et al. Atrial enlargement as a consequence of atrial fibrillation. A prospective echocardiographic study. Circulation. 1990;82:792–797
  16. Verheule S, Wilson E, Everett Tt, Shanbhag S, Golden C, Olgin J. Alterations in atrial electrophysiology and tissue structure in a canine model of chronic atrial dilatation due to mitral regurgitation. Circulation. 2003;107:2615–2622
  17. Knackstedt C, Gramley F, Schimpf T, Mischke K, Zarse M, Plisiene J, et al. Association of echocardiographic atrial size and atrial fibrosis in a sequential model of congestive heart failure and atrial fibrillation. Cardiovasc. Pathol. 2008;17:318–324
  18. Van Wagoner DR. Electrophysiological remodeling in human atrial fibrillation. Pacing Clin. Electrophysiol. 2003;26:1572–1575
  19. Wijffels MC, Kirchhof CJ, Dorland R, Allessie MA. Atrial fibrillation begets atrial fibrillation. A study in awake chronically instrumented goats. Circulation. 1995;92:1954–1968
  20. Dhein S. Role of connexins in atrial fibrillation. Adv. Cardiol. 2006;42:161–174
  21. Luo MH, Li YS, Yang KP. Fibrosis of collagen I and remodeling of connexin 43 in atrial myocardium of patients with atrial fibrillation. Cardiology. 2007;107:248–253
  22. Dhein S, Polontchouk L, Salameh A, Haefliger JA. Pharmacological modulation and differential regulation of the cardiac gap junction proteins connexin 43 and connexin 40. Biol. Cell. 2002;94:409–422
  23. Cha TJ, Ehrlich JR, Zhang L, Shi YF, Tardif JC, Leung TK, et al. Dissociation between ionic remodeling and ability to sustain atrial fibrillation during recovery from experimental congestive heart failure. Circulation. 2004;109:412–418
  24. Tsai CT, Lai LP, Hwang JJ, Lin JL, Chiang FT. Molecular genetics of atrial fibrillation. J. Am. Coll. Cardiol. 2008;52:241–250
  25. Schotten U, de Haan S, Neuberger HR, Eijsbouts S, Blaauw Y, Tieleman R, et al. Loss of atrial contractility is primary cause of atrial dilatation during first days of atrial fibrillation. Am. J. Physiol., Heart Circ. Physiol. 2004;287:H2324–2331
  26. Li X, Zima AV, Sheikh F, Blatter LA, Chen J. Endothelin-1-induced arrhythmogenic Ca2+ signaling is abolished in atrial myocytes of inositol-1,4,5-trisphosphate(IP3)-receptor type 2-deficient mice. Circ. Res. 2005;96:1274–1281
  27. Eckstein J, Verheule S, de Groot NM, Allessie M, Schotten U. Mechanisms of perpetuation of atrial fibrillation in chronically dilated atria. Prog. Biophys. Mol. Biol. 2008;97:435–451
  28. Young MJ. Mechanisms of mineralocorticoid receptor-mediated cardiac fibrosis and vascular inflammation. Curr. Opin. Nephrol. Hypertens. 2008;17:174–180
  29. Brilla CG, Weber KT. Mineralocorticoid excess, dietary sodium, and myocardial fibrosis. J. Lab. Clin. Med. 1992;120:893–901
  30. Sun Y, Ramires FJ, Weber KT. Fibrosis of atria and great vessels in response to angiotensin II or aldosterone infusion. Cardiovasc. Res. 1997;35:138–147
  31. Schmidt BM, Schmieder RE. Aldosterone-induced cardiac damage: focus on blood pressure independent effects. Am. J. Hypertens. 2003;16:80–86
  32. Silvestre JS, Robert V, Heymes C, Aupetit-Faisant B, Mouas C, Moalic JM, et al. Myocardial production of aldosterone and corticosterone in the rat. Physiological regulation. J. Biol. Chem. 1998;273:4883–4891
  33. Rocha R, Stier CT, Kifor I, Ochoa-Maya MR, Rennke HG, Williams GH, et al. Aldosterone: a mediator of myocardial necrosis and renal arteriopathy. Endocrinology. 2000;141:3871–3878
  34. Hood WG, Hill R, Pittman JA, Farmer TA. Studies on the metabolic effects of spironolactone in man. Ann. N.Y. Acad. Sci. 1960;88:864–880
  35. Pitt B, Zannad F, Remme WJ, Cody R, Castaigne A, Perez A, et al. The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. N. Engl. J. Med. 1999;341:709–717
  36. Zannad F, Alla F, Dousset B, Perez A, Pitt B. Limitation of excessive extracellular matrix turnover may contribute to survival benefit of spironolactone therapy in patients with congestive heart failure: insights from the Randomized Aldactone Evaluation Study (RALES). Rales Investigators. Circulation. 2000;102:2700–2706
  37. Shehab A, Elnour AA, Struthers AD. A randomised, controlled, double-blind, cross-over pilot study assessing the effects of spironolactone, losartan and their combination on heart rate variability and QT dispersion in patients with chronic heart failure. Cardiovasc. J. Afr. 2008;19:292–296
  38. Milliez P, Deangelis N, Rucker-Martin C, Leenhardt A, Vicaut E, Robidel E, et al. Spironolactone reduces fibrosis of dilated atria during heart failure in rats with myocardial infarction. Eur. Heart J. 2005;26:2193–2199
  39. Bunda S, Wang Y, Mitts TF, Liu P, Arab S, Arabkhari M, et al. Aldosterone stimulates elastogenesis in cardiac fibroblasts via mineralocorticoid receptor-independent action involving the consecutive activation of Galpha13, c-Src, the insulin-like growth factor-I receptor, and phosphatidylinositol 3-kinase/Akt. J. Biol. Chem. 2009;284:16633–16647
  40. Nishioka T, Suzuki M, Onishi K, Takakura N, Inada H, Yoshida T, et al. Eplerenone attenuates myocardial fibrosis in the angiotensin II-induced hypertensive mouse: involvement of tenascin-C induced by aldosterone-mediated inflammation. J. Cardiovasc. Pharmacol. 2007;49:261–268
  41. Barnes BJ, Howard PA. Eplerenone: a selective aldosterone receptor antagonist for patients with heart failure. Ann. Pharmacother. 2005;39:68–76
  42. Pitt B, Remme W, Zannad F, Neaton J, Martinez F, Roniker B, et al. Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N. Engl. J. Med. 2003;348:1309–1321
  43. Akashiba A, Ono H, Ono Y, Ishimitsu T, Matsuoka H. Valsartan improves l-NAME-exacerbated cardiac fibrosis with TGF-beta inhibition and apoptosis induction in spontaneously hypertensive rats. J. Cardiol. 2008;52:239–246
  44. Kumagai K, Nakashima H, Urata H, Gondo N, Arakawa K, Saku K. Effects of angiotensin II type 1 receptor antagonist on electrical and structural remodeling in atrial fibrillation. J. Am. Coll. Cardiol. 2003;41:2197–2204
  45. Disertori M, Latini R, Barlera S, Franzosi MG, Staszewsky L, Maggioni AP, et al. Valsartan for prevention of recurrent atrial fibrillation. N. Engl. J. Med. 2009;360:1606–1617
  46. Zhao W, Zhao T, Chen Y, Ahokas RA, Sun Y. Oxidative stress mediates cardiac fibrosis by enhancing transforming growth factor-beta1 in hypertensive rats. Mol. Cell. Biochem. 2008;317:43–50
  47. Shimano M, Tsuji Y, Inden Y, Kitamura K, Uchikawa T, Harata S, et al. Pioglitazone, a peroxisome proliferator-activated receptor-gamma activator, attenuates atrial fibrosis and atrial fibrillation promotion in rabbits with congestive heart failure. Heart Rhythm. 2008;5:451–459
  48. Xiao HD, Fuchs S, Campbell DJ, Lewis W, Dudley SC, Kasi VS, et al. Mice with cardiac-restricted angiotensin-converting enzyme (ACE) have atrial enlargement, cardiac arrhythmia, and sudden death. Am. J. Pathol. 2004;165:1019–1032
  49. Nakajima H, Nakajima HO, Salcher O, Dittie AS, Dembowsky K, Jing S, et al. Atrial but not ventricular fibrosis in mice expressing a mutant transforming growth factor-beta(1) transgene in the heart. Circ. Res. 2000;86:571–579
  50. Paradis P, Dali-Youcef N, Paradis FW, Thibault G, Nemer M. Overexpression of angiotensin II type I receptor in cardiomyocytes induces cardiac hypertrophy and remodeling. Proc. Natl. Acad. Sci. U. S. A. 2000;97:931–936
  51. Bauer P, Regitz-Zagrosek V, Kallisch H, Linz W, Schoelkens B, Hildebrandt AG, et al. Myocardial angiotensin receptor type 1 gene expression in a rat model of cardiac volume overload. Basic Res. Cardiol. 1997;92:139–146
  52. Burstein B, Libby E, Calderone A, Nattel S. Differential behaviors of atrial versus ventricular fibroblasts: a potential role for platelet-derived growth factor in atrial-ventricular remodeling differences. Circulation. 2008;117:1630–1641
  53. de Gasparo M, Catt KJ, Inagami T, Wright JW, Unger T. International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol. Rev. 2000;52:415–472
  54. Lymperopoulos A, Rengo G, Zincarelli C, Kim J, Soltys S, Koch WJ. An adrenal beta-arrestin 1-mediated signaling pathway underlies angiotensin II-induced aldosterone production in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 2009;106:5825–5830
  55. Kassiri Z, Khokha R. Myocardial extra-cellular matrix and its regulation by metalloproteinases and their inhibitors. Thromb. Haemost. 2005;93:212–219
  56. Herpel E, Pritsch M, Koch A, Dengler TJ, Schirmacher P, Schnabel PA. Interstitial fibrosis in the heart: differences in extracellular matrix proteins and matrix metalloproteinases in end-stage dilated, ischaemic and valvular cardiomyopathy. Histopathology. 2006;48:736–747
  57. Cardin S, Libby E, Pelletier P, Le Bouter S, Shiroshita-Takeshita A, Le Meur N, et al. Contrasting gene expression profiles in two canine models of atrial fibrillation. Circ. Res. 2007;100:425–433
  58. Bouzeghrane F, Reinhardt DP, Reudelhuber TL, Thibault G. Enhanced expression of fibrillin-1, a constituent of the myocardial extracellular matrix in fibrosis. Am. J. Physiol., Heart Circ. Physiol. 2005;289:H982–991
  59. Lin CS, Lai LP, Lin JL, Sun YL, Hsu CW, Chen CL, et al. Increased expression of extracellular matrix proteins in rapid atrial pacing-induced atrial fibrillation. Heart Rhythm. 2007;4:938–949
  60. Ramirez F, Rifkin DB. Extracellular microfibrils: contextual platforms for TGFbeta and BMP signaling. Curr. Opin. Cell Biol. 2009;
  61. Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol. Rev. 2007;87:1285–1342
  62. Mukherjee R, Herron AR, Lowry AS, Stroud RE, Stroud MR, Wharton JM, et al. Selective induction of matrix metalloproteinases and tissue inhibitor of metalloproteinases in atrial and ventricular myocardium in patients with atrial fibrillation. Am. J. Cardiol. 2006;97:532–537
  63. Moe GW, Laurent G, Doumanovskaia L, Konig A, Hu X, Dorian P. Matrix metalloproteinase inhibition attenuates atrial remodeling and vulnerability to atrial fibrillation in a canine model of heart failure. J. Card. Fail. 2008;14:768–776
  64. Baudino TA, McFadden A, Fix C, Hastings J, Price R, Borg TK. Cell patterning: interaction of cardiac myocytes and fibroblasts in three-dimensional culture. Microsc. Microanal. 2008;14:117–125
  65. Hirose M, Takeishi Y, Niizeki T, Shimojo H, Nakada T, Kubota I, et al. Diacylglycerol kinase zeta inhibits G(alpha)q-induced atrial remodeling in transgenic mice. Heart Rhythm. 2009;6:78–84
  66. Zaman AK, French CJ, Schneider DJ, Sobel BE. A profibrotic effect of plasminogen activator inhibitor type-1 (PAI-1) in the heart. Exp. Biol. Med. (Maywood). 2009;234:246–254
  67. Duisters RF, Tijsen AJ, Schroen B, Leenders JJ, Lentink V, van der Made I, et al. miR-133 and miR-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodeling. Circ. Res. 2009;104:170–1786p following 8
  68. Recchia AG, Filice E, Pellegrino D, Dobrina A, Cerra MC, Maggiolini M. Endothelin-1 induces connective tissue growth factor expression in cardiomyocytes. J. Mol. Cell. Cardiol. 2009;46:352–359

PII: S0022-2828(09)00377-0

doi: 10.1016/j.yjmcc.2009.09.001

Journal of Molecular and Cellular Cardiology
Volume 48, Issue 3 , Pages 461-467 , March 2010

Article Tools

* Image Usage & Resolution