Journal of Molecular and Cellular Cardiology
Volume 48, Issue 3 , Pages 504-511 , March 2010

The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction

Received 16 April 2009 ,Revised 9 July 2009 ,Accepted 14 July 2009.

References 

  1. Berk BC, Fujiwara K, Lehoux S. ECM remodeling in hypertensive heart disease. J. Clin. Invest. 2007;117:568–575
  2. Kim HE, Dalal SS, Young E, Legato MJ, Weisfeldt ML, D'Armiento J. Disruption of the myocardial extracellular matrix leads to cardiac dysfunction. J. Clin. Invest. 2000;106:857–866
  3. Senzaki H, Paolocci N, Gluzband YA, Lindsey ML, Janicki JS, Crow MT, et al. beta-blockade prevents sustained metalloproteinase activation and diastolic stiffening induced by angiotensin II combined with evolving cardiac dysfunction. Circ. Res. 2000;86:807–815
  4. Opie LH, Commerford PJ, Gersh BJ, Pfeffer MA. Controversies in ventricular remodelling. Lancet. 2006;367:356–367
  5. Siwik DA, Chang DL, Colucci WS. Interleukin-1beta and tumor necrosis factor-alpha decrease collagen synthesis and increase matrix metalloproteinase activity in cardiac fibroblasts in vitro. Circ. Res. 2000;86:1259–1265
  6. Bujak M, Dobaczewski M, Chatila K, Mendoza LH, Li N, Reddy A, et al. Interleukin-1 receptor type I signaling critically regulates infarct healing and cardiac remodeling. Am. J. Pathol. 2008;173:57–67
  7. Frangogiannis NG, Mendoza LH, Lindsey ML, Ballantyne CM, Michael LH, Smith CW, et al. IL-10 is induced in the reperfused myocardium and may modulate the reaction to injury. J. Immunol. 2000;165:2798–2808
  8. Bujak M, Frangogiannis NG. The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc. Res. 2007;74:184–195
  9. Frangogiannis NG. The immune system and cardiac repair. Pharmacol. Res. 2008;58:88–111
  10. Cannon RO, Butany JW, McManus BM, Speir E, Kravitz AB, Bolli R, et al. Early degradation of collagen after acute myocardial infarction in the rat. Am. J. Cardiol. 1983;52:390–395
  11. Whittaker P, Boughner DR, Kloner RA. Role of collagen in acute myocardial infarct expansion. Circulation. 1991;84:2123–2134
  12. Etoh T, Joffs C, Deschamps AM, Davis J, Dowdy K, Hendrick J, et al. Myocardial and interstitial matrix metalloproteinase activity after acute myocardial infarction in pigs. Am. J. Physiol. Heart Circ. Physiol. 2001;281:H987–H994
  13. Takahashi S, Barry AC, Factor SM. Collagen degradation in ischaemic rat hearts. Biochem. J. 1990;265:233–241
  14. Cleutjens JP, Verluyten MJ, Smiths JF, Daemen MJ. Collagen remodeling after myocardial infarction in the rat heart. Am. J. Pathol. 1995;147:325–338
  15. Villarreal FJ, Griffin M, Omens J, Dillmann W, Nguyen J, Covell J. Early short-term treatment with doxycycline modulates postinfarction left ventricular remodeling. Circulation. 2003;108:1487–1492
  16. Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol. Rev. 2007;87:1285–1342
  17. Cleutjens JP, Kandala JC, Guarda E, Guntaka RV, Weber KT. Regulation of collagen degradation in the rat myocardium after infarction. J. Mol. Cell. Cardiol. 1995;27:1281–1292
  18. Villarreal F, Omens J, Dillmann W, Risteli J, Nguyen J, Covell J. Early degradation and serum appearance of type I collagen fragments after myocardial infarction. J. Mol. Cell. Cardiol. 2004;36:597–601
  19. Dobaczewski M, Bujak M, Zymek P, Ren G, Entman ML, Frangogiannis NG. Extracellular matrix remodeling in canine and mouse myocardial infarcts. Cell Tissue Res. 2006;324:475–488
  20. Huebener P, Abou-Khamis T, Zymek P, Bujak M, Ying X, Chatila K, et al. CD44 is critically involved in infarct healing by regulating the inflammatory and fibrotic response. J. Immunol. 2008;180:2625–2633
  21. Gearing AJ, Beckett P, Christodoulou M, Churchill M, Clements JM, Crimmin M, et al. Matrix metalloproteinases and processing of pro-TNF-alpha. J. Leukoc. Biol. 1995;57:774–777
  22. Van Lint P, Libert C. Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation. J. Leukoc. Biol. 2007;82:1375–1381
  23. Adair-Kirk TL, Senior RM. Fragments of extracellular matrix as mediators of inflammation. Int. J. Biochem. Cell Biol. 2008;40:1101–1110
  24. Senior RM, Griffin GL, Mecham RP. Chemotactic activity of elastin-derived peptides. J. Clin. Invest. 1980;66:859–862
  25. Weathington NM, van Houwelingen AH, Noerager BD, Jackson PL, Kraneveld AD, Galin FS, et al. A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat. Med. 2006;12:317–323
  26. Gaggar A, Jackson PL, Noerager BD, O'Reilly PJ, McQuaid DB, Rowe SM, et al. A novel proteolytic cascade generates an extracellular matrix-derived chemoattractant in chronic neutrophilic inflammation. J. Immunol. 2008;180:5662–5669
  27. Taylor KR, Trowbridge JM, Rudisill JA, Termeer CC, Simon JC, Gallo RL. Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J. Biol. Chem. 2004;279:17079–17084
  28. Teder P, Vandivier RW, Jiang D, Liang J, Cohn L, Pure E, et al. Resolution of lung inflammation by CD44. Science. 2002;296:155–158
  29. Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 2003;4:33–45
  30. Clark RA. Wound repair. Overview and general considerations. In: R.A. Clark editors. The molecular and cellular biology of wound repair. New York: Plenum Press; 1995;p. 3–50
  31. Corbett SA, Schwarzbauer JE. Fibronectin-fibrin cross-linking: a regulator of cell behavior. Trends Cardiovasc. Med. 1998;8:357–362
  32. Petzelbauer P, Zacharowski PA, Miyazaki Y, Friedl P, Wickenhauser G, Castellino FJ, et al. The fibrin-derived peptide Bbeta15-42 protects the myocardium against ischemia-reperfusion injury. Nat. Med. 2005;11:298–304
  33. Atar D, Petzelbauer P, Schwitter J, Huber K, Rensing B, Kasprzak JD, et al. Effect of intravenous FX06 as an adjunct to primary percutaneous coronary intervention for acute ST-segment elevation myocardial infarction results of the F.I.R.E. (Efficacy of FX06 in the Prevention of Myocardial Reperfusion Injury) trial. J. Am. Coll. Cardiol. 2009;53:720–729
  34. Drew AF, Liu H, Davidson JM, Daugherty CC, Degen JL. Wound-healing defects in mice lacking fibrinogen. Blood. 2001;97:3691–3698
  35. Creemers E, Cleutjens J, Smits J, Heymans S, Moons L, Collen D, et al. Disruption of the plasminogen gene in mice abolishes wound healing after myocardial infarction. Am. J. Pathol. 2000;156:1865–1873
  36. Brown LF, Dubin D, Lavigne L, Logan B, Dvorak HF, Van de Water L. Macrophages and fibroblasts express embryonic fibronectins during cutaneous wound healing. Am. J. Pathol. 1993;142:793–801
  37. Ulrich MM, Janssen AM, Daemen MJ, Rappaport L, Samuel JL, Contard F, et al. Increased expression of fibronectin isoforms after myocardial infarction in rats. J. Mol. Cell. Cardiol. 1997;29:2533–2543
  38. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J. Pathol. 2003;200:500–503
  39. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function, multiple origins. Am. J. Pathol. 2007;170:1807–1816
  40. Serini G, Bochaton-Piallat ML, Ropraz P, Geinoz A, Borsi L, Zardi L, et al. The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1. J. Cell Biol. 1998;142:873–881
  41. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 2002;3:349–363
  42. Sottile J, Hocking DC. Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell–matrix adhesions. Mol. Biol. Cell. 2002;13:3546–3559
  43. Willems IE, Arends JW, Daemen MJ. Tenascin and fibronectin expression in healing human myocardial scars. J. Pathol. 1996;179:321–325
  44. Imanaka-Yoshida K, Hiroe M, Nishikawa T, Ishiyama S, Shimojo T, Ohta Y, et al. Tenascin-C modulates adhesion of cardiomyocytes to extracellular matrix during tissue remodeling after myocardial infarction. Lab. Invest. 2001;81:1015–1024
  45. Mackie EJ, Scott-Burden T, Hahn AW, Kern F, Bernhardt J, Regenass S, et al. Expression of tenascin by vascular smooth muscle cells. Alterations in hypertensive rats and stimulation by angiotensin II. Am. J. Pathol. 1992;141:377–388
  46. Tamaoki M, Imanaka-Yoshida K, Yokoyama K, Nishioka T, Inada H, Hiroe M, et al. Tenascin-C regulates recruitment of myofibroblasts during tissue repair after myocardial injury. Am. J. Pathol. 2005;167:71–80
  47. Frangogiannis NG, Ren G, Dewald O, Zymek P, Haudek S, Koerting A, et al. The critical role of endogenous thrombospondin (TSP)-1 in preventing expansion of healing myocardial infarcts. Circulation. 2005;111:2935–2942
  48. Schellings MW, Pinto YM, Heymans S. Matricellular proteins in the heart: possible role during stress and remodeling. Cardiovasc. Res. 2004;64:24–31
  49. Murry CE, Giachelli CM, Schwartz SM, Vracko R. Macrophages express osteopontin during repair of myocardial necrosis. Am. J. Pathol. 1994;145:1450–1462
  50. Dewald O, Ren G, Duerr GD, Zoerlein M, Klemm C, Gersch C, et al. Of mice and dogs: species-specific differences in the inflammatory response following myocardial infarction. Am. J. Pathol. 2004;164:665–677
  51. Hashimoto S, Suzuki T, Dong HY, Yamazaki N, Matsushima K. Serial analysis of gene expression in human monocytes and macrophages. Blood. 1999;94:837–844
  52. Krishnamurthy P, Peterson JT, Subramanian V, Singh M, Singh K. Inhibition of matrix metalloproteinases improves left ventricular function in mice lacking osteopontin after myocardial infarction. Mol. Cell. Biochem. 2009;322:53–62
  53. Trueblood NA, Xie Z, Communal C, Sam F, Ngoy S, Liaw L, et al. Exaggerated left ventricular dilation and reduced collagen deposition after myocardial infarction in mice lacking osteopontin. Circ. Res. 2001;88:1080–1087
  54. Schellings MW, Vanhoutte D, Swinnen M, Cleutjens JP, Debets J, van Leeuwen RE, et al. Absence of SPARC results in increased cardiac rupture and dysfunction after acute myocardial infarction. J. Exp. Med. 2009;206:113–123
  55. Shimazaki M, Nakamura K, Kii I, Kashima T, Amizuka N, Li M, et al. Periostin is essential for cardiac healing after acute myocardial infarction. J. Exp. Med. 2008;205:295–303
  56. Oka T, Xu J, Kaiser RA, Melendez J, Hambleton M, Sargent MA, et al. Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ. Res. 2007;101:313–321
  57. Jugdutt BI, Amy RW. Healing after myocardial infarction in the dog: changes in infarct hydroxyproline and topography. J. Am. Coll. Cardiol. 1986;7:91–102
  58. Lerman RH, Apstein CS, Kagan HM, Osmers EL, Chichester CO, Vogel WM, et al. Myocardial healing and repair after experimental infarction in the rabbit. Circ. Res. 1983;53:378–388
  59. Holmes JW, Borg TK, Covell JW. Structure and mechanics of healing myocardial infarcts. Annu. Rev. Biomed. Eng. 2005;7:223–253
  60. Ren G, Michael LH, Entman ML, Frangogiannis NG. Morphological characteristics of the microvasculature in healing myocardial infarcts. J. Histochem. Cytochem. 2002;50:71–79
  61. Zhao W, Lu L, Chen SS, Sun Y. Temporal and spatial characteristics of apoptosis in the infarcted rat heart. Biochem. Biophys. Res. Commun. 2004;325:605–611
  62. Takemura G, Ohno M, Hayakawa Y, Misao J, Kanoh M, Ohno A, et al. Role of apoptosis in the disappearance of infiltrated and proliferated interstitial cells after myocardial infarction. Circ. Res. 1998;82:1130–1138
  63. Hinz B. Formation and function of the myofibroblast during tissue repair. J. Invest. Dermatol. 2007;127:526–537
  64. Lindsey ML, Gannon J, Aikawa M, Schoen FJ, Rabkin E, Lopresti-Morrow L, et al. Selective matrix metalloproteinase inhibition reduces left ventricular remodeling but does not inhibit angiogenesis after myocardial infarction. Circulation. 2002;105:753–758
  65. Lindsey ML. MMP induction and inhibition in myocardial infarction. Heart Fail. Rev. 2004;9:7–19
  66. Hudson MP, Armstrong PW, Ruzyllo W, Brum J, Cusmano L, Krzeski P, et al. Effects of selective matrix metalloproteinase inhibitor (PG-116800) to prevent ventricular remodeling after myocardial infarction: results of the PREMIER (Prevention of Myocardial Infarction Early Remodeling) trial. J. Am. Coll. Cardiol. 2006;48:15–20

PII: S0022-2828(09)00308-3

doi: 10.1016/j.yjmcc.2009.07.015

Journal of Molecular and Cellular Cardiology
Volume 48, Issue 3 , Pages 504-511 , March 2010