Translating Koch's postulates to identify matrix metalloproteinase roles in postmyocardial infarction remodeling: Cardiac metalloproteinase actions (carMA) postulates

Circulation Research

Volumn 114, Issue 5, 2014, Pages 860-871

  Iyer, Rugmani Padmanabhan ^a   De Castro Brás, Lisandra E ^a   Jin, Yu Fang ^a,b   Lindsey, Merry L ^a,c  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^b The University of Texas at San Antonio   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Extracellular matrix; fibrosis; inflammation; matrix metalloproteinases; proteomics; ventricular remodeling

Indexed keywords

COLLAGENASE 3; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MACROPHAGE DERIVED MMP 28 PROTEIN; MACROPHAGE ELASTASE; MATRILYSIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 15; MATRIX METALLOPROTEINASE 16; MATRIX METALLOPROTEINASE 26; MMP 23 PROTEIN; MMP 27 PROTEIN; MYOCYTE DERIVED MMP 28 PROTEIN; NEUTROPHIL COLLAGENASE; SCLEROPROTEIN; STROMELYSIN; STROMELYSIN 2; STROMELYSIN 3; UNCLASSIFIED DRUG;

CARDIOVASCULAR FUNCTION; CELL FUNCTION; DISEASE ASSOCIATION; ENZYME INHIBITION; EXTRACELLULAR MATRIX; FIBROBLAST; GENE OVEREXPRESSION; HEART FUNCTION; HEART INFARCTION; HEART VENTRICLE REMODELING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MOLECULAR EPIDEMIOLOGY; MOLECULAR PATHOLOGY; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW;

EXTRACELLULAR MATRIX; FIBROSIS; INFLAMMATION; MATRIX METALLOPROTEINASES; PROTEOMICS; VENTRICULAR REMODELING;

ANIMALS; EXTRACELLULAR MATRIX; HUMANS; MATRIX METALLOPROTEINASES; MYOCARDIAL INFARCTION; PROTEOMICS; VENTRICULAR DYSFUNCTION, LEFT;

EID: 84896780190     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.114.301673     Document Type: Review

References (140)

1. Long CG, Braswell E, Zhu D, Apigo J, Baum J, Brodsky B. Characterization of collagen-like peptides containing interruptions in the repeating Gly-X-Y sequence. Biochemistry. 1993;32:11688-11695.
2. Zamilpa R, Ibarra J, De Castro Brs LE, Ramirez TA, Nguyen N, Halade GV, Zhang J, Dai Q, Dayah T, Chiao YA, Lowell W, Ahuja SS, DArmiento J, Jin YF, Lindsey ML. Transgenic overexpression of matrix metalloproteinase-9 in macrophages attenuates the inflammatory response and improves left ventricular function post-myocardial infarction. J Mol Cell Cardiol. 2012;53:599-608.
3. Jourdan-Lesaux C, Zhang J, Lindsey ML. Extracellular matrix roles during cardiac repair. Life Sci. 2010;87:391-400.
4. Mllmann H, Nef HM, Kostin S, von Kalle C, Pilz I, Weber M, Schaper J, Hamm CW, Elssser A. Bone marrow-derived cells contribute to infarct remodelling. Cardiovasc Res. 2006;71:661-671.
5. Van Amerongen MJ, Harmsen MC, Van Rooijen N, Petersen AH, Van Luyn MJ. Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice. Am J Pathol. 2007;170:818-829.
6. Amerongen Mv, Bou-Gharios G, Popa ER, Ark Jv, Petersen AH, Dam GMv, Luyn MJAv, Harmsen MC. Bone marrow-derived myofibroblasts contribute functionally to scar formation after myocardial infarction. J Pathol. 2008;214:377-386
7. Daskalopoulos EP, Janssen B, Blankesteijn WM. Myofibroblasts in the infarct area: Concepts and challenges. Microsc Microanal. 2012;18:35-49. doi:10.1017/S143192761101227X.
8. Marchant DJ, Boyd JH, Lin DC, Granville DJ, Garmaroudi FS, McManus BM. Inflammation in myocardial diseases. Circ Res. 2012;110:126-144.
9. Janicki JS, Brower GL. The role of myocardial fibrillar collagen in ventricular remodeling and function. J Card Fail. 2002;8:S319-S325.
10. Lindsey ML, Mann DL, Entman ML, Spinale FG. Extracellular matrix remodeling following myocardial injury. Ann Med. 2003;35:316-326.
11. Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: Influence on cardiac form and function. Physiol Rev. 2007;87:1285-1342.
12. Fredericks DN, Relman DA. Sequence-based identification of microbial pathogens: A reconsideration of Kochs postulates. Clin Microbiol Rev. 1996;9:18-33.
13. Marqusee S, Robbins VH, Baldwin RL. Unusually stable helix formation in short alanine-based peptides. Proc Natl Acad Sci USA. 1989;86:5286-5290.
14. Lindsey ML, Escobar GP, Mukherjee R, Goshorn DK, Sheats NJ, Bruce JA, Mains IM, Hendrick JK, Hewett KW, Gourdie RG, Matrisian LM, Spinale FG. Matrix metalloproteinase-7 affects connexin-43 levels, electrical conduction, and survival after myocardial infarction. Circulation. 2006;113:2919-2928.
15. Ma Y, Chiao YA, Zhang J, Manicone AM, Jin YF, Lindsey ML. Matrix metalloproteinase-28 deletion amplifies inflammatory and extracellular matrix responses to cardiac aging. Microsc Microanal. 2012;18:81-90.
16. Peterson JT, Li H, Dillon L, Bryant JW. Evolution of matrix metalloprotease and tissue inhibitor expression during heart failure progression in the infarcted rat. Cardiovasc Res. 2000;46:307-315.
17. 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.
18. Cleutjens JP. The role of matrix metalloproteinases in heart disease. Cardiovasc Res. 1996;32:816-821.
19. Ma Y, Halade GV, Zhang J, Ramirez TA, Levin D, Voorhees A, Jin YF, Han HC, Manicone AM, Lindsey ML. Matrix metalloproteinase-28 deletion exacerbates cardiac dysfunction and rupture after myocardial infarction in mice by inhibiting M2 macrophage activation. Circ Res. 2013;112:675-688.
20. Orn S, Manhenke C, Squire IB, Ng L, Anand I, Dickstein K. Plasma MMP-2, MMP-9 and N-BNP in long-term survivors following complicated myocardial infarction: Relation to cardiac magnetic resonance imaging measures of left ventricular structure and function. J Card Fail. 2007;13:843-849.
21. Chiao YA, Dai Q, Zhang J, Lin J, Lopez EF, Ahuja SS, Chou YM, Lindsey ML, Jin YF. Multi-analyte profiling reveals matrix metalloproteinase-9 and monocyte chemotactic protein-1 as plasma biomarkers of cardiac aging. Circ Cardiovasc Genet. 2011;4:455-462.
22. Bradham WS, Gunasinghe H, Holder JR, Multani M, Killip D, Anderson M, Meyer D, Spencer WH 3rd, Torre-Amione G, Spinale FG. Release of matrix metalloproteinases following alcohol septal ablation in hypertrophic obstructive cardiomyopathy. J Am Coll Cardiol. 2002;40:2165-2173.
23. Tanindi A, Sahinarslan A, Elbeg S, Cemri M. Association of matrix metalloproteinase-1, matrix metalloproteinase-9, tissue inhibitor of matrix metalloproteinase-1, and interleukin-6 with epicardial and myocardial perfusion. Coron Artery Dis. 2011;22:253-258.
24. Lehrke M, Greif M, Broedl UC, Lebherz C, Laubender RP, Becker A, von Ziegler F, Tittus J, Reiser M, Becker C, Gke B, Steinbeck G, Leber AW, Parhofer KG. MMP-1 serum levels predict coronary atherosclerosis in humans. Cardiovasc Diabetol. 2009;8:50.
25. Halapas A, Zacharoulis A, Theocharis S, Karavidas A, Korres D, Papadopoulos K, Katopodis H, Stavropoulou A, Lembessis P, Xiromeritis C, Zacharoulis A, Koutsilieris M. Serum levels of the osteoprotegerin, receptor activator of nuclear factor kappa-B ligand, metalloproteinase-1 (MMP-1) and tissue inhibitors of MMP-1 levels are increased in men 6 months after acute myocardial infarction. Clin Chem Lab Med. 2008;46:510-516.
26. Scholtz JM, Baldwin RL. The mechanism of -helix formation by peptides. Annu Rev Biophys Biomol Struct. 1992;21:95-118.
27. Lindsey ML, Zamilpa R. Temporal and spatial expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases following myocardial infarction. Cardiovasc Ther. 2012;30:31-41.
28. 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.
29. Van Den Berg JM, Weyer S, Weening JJ, Roos D, Kuijpers TW. Divergent effects of tumor necrosis factor alpha on apoptosis of human neutrophils. J Leukoc Biol. 2001;69:467-473.
30. Balbn M, Fueyo A, Knuper V, Lpez JM, Alvarez J, Snchez LM, Quesada V, Bordallo J, Murphy G, Lpez-Otn C. Identification and enzymatic characterization of two diverging murine counterparts of human interstitial collagenase (MMP-1) expressed at sites of embryo implantation. J Biol Chem. 2001;276:10253-10262.
31. Lindsey ML, Goshorn DK, Squires CE, Escobar GP, Hendrick JW, Mingoia JT, Sweterlitsch SE, Spinale FG. Age-dependent changes in myocardial matrix metalloproteinase/tissue inhibitor of metalloproteinase profiles and fibroblast function. Cardiovasc Res. 2005;66:410-419.
32. Porter KE, Turner NA. Cardiac fibroblasts: At the heart of myocardial remodeling. Pharmacol Ther. 2009;123:255-278.
33. Chow AK, Cena J, Schulz R. Acute actions and novel targets of matrix metalloproteinases in the heart and vasculature. Br J Pharmacol. 2007;152:189-205.
34. Tyagi SC, Campbell SE, Reddy HK, Tjahja E, Voelker DJ. Matrix metalloproteinase activity expression in infarcted, noninfarcted and dilated cardiomyopathic human hearts. Mol Cell Biochem. 1996;155:13-21.
35. Vanhoutte D, Schellings M, Pinto Y, Heymans S. Relevance of matrix metalloproteinases and their inhibitors after myocardial infarction: A temporal and spatial window. Cardiovasc Res. 2006;69:604-613.
36. Segawa S, Sugihara M. Characterization of the transition state of lysozyme unfolding. I. Effect of protein-solvent interactions on the transition state. Biopolymers. 1984;23:2473-2488.
37. Serrano L, Kellis JT Jr, Cann P, Matouschek A, Fersht AR. The folding of an enzyme. II. Substructure of barnase and the contribution of different interactions to protein stability. J Mol Biol. 1992;224:783-804.
38. Tao ZY, Cavasin MA, Yang F, Liu YH, Yang XP. Temporal changes in matrix metalloproteinase expression and inflammatory response associated with cardiac rupture after myocardial infarction in mice. Life Sci. 2004;74:1561-1572.
39. Sakowicz A, Fendler W, Lelonek M, Sakowicz B, Pietrucha T. Genetic polymorphisms and the risk of myocardial infarction in patients under 45 years of age. Biochem Genet. 2013;51:230-242.
40. Shoemaker KR, Kim PS, Brems DN, Marqusee S, York EJ, Chaiken IM, Stewart JM, Baldwin RL. Nature of the charged-group effect on the stability of the C-peptide helix. Proc Natl Acad Sci USA. 1985;82:2349-2353.
41. Romanic AM, Burns-Kurtis CL, Gout B, Berrebi-Bertrand I, Ohlstein EH. Matrix metalloproteinase expression in cardiac myocytes following myocardial infarction in the rabbit. Life Sci. 2001;68:799-814.
42. Zile MR, Desantis SM, Baicu CF, Stroud RE, Thompson SB, McClure CD, Mehurg SM, Spinale FG. Plasma biomarkers that reflect determinants of matrix composition identify the presence of left ventricular hypertrophy and diastolic heart failure. Circ Heart Fail. 2011;4:246-256.
43. Rao G, Tam JP. Synthesis of peptide dendrimer. J. Am. Chem. Soc. 1994;116:6975-6976.
44. Webb CS, Bonnema DD, Ahmed SH, Leonardi AH, McClure CD, Clark LL, Stroud RE, Corn WC, Finklea L, Zile MR, Spinale FG. Specific temporal profile of matrix metalloproteinase release occurs in patients after myocardial infarction: Relation to left ventricular remodeling. Circulation. 2006;114:1020-1027.
45. Deten A, Volz HC, Holzl A, Briest W, Zimmer HG. Effect of propranolol on cardiac cytokine expression after myocardial infarction in rats. Mol Cell Biochem. 2003;251:127-137.
46. Wilson EM, Moainie SL, Baskin JM, Lowry AS, Deschamps AM, Mukherjee R, Guy TS, St John-Sutton MG, Gorman JH 3rd, Edmunds LH Jr, Gorman RC, Spinale FG. Region-and type-specific induction of matrix metalloproteinases in post-myocardial infarction remodeling. Circulation. 2003;107:2857-2863.
47. Squire IB, Evans J, Ng LL, Loftus IM, Thompson MM. Plasma MMP-9 and MMP-2 following acute myocardial infarction in man: Correlation with echocardiographic and neurohumoral parameters of left ventricular dysfunction. J Card Fail. 2004;10:328-333.
48. Phatharajaree W, Phrommintikul A, Chattipakorn N. Matrix metalloproteinases and myocardial infarction. Can J Cardiol. 2007;23:727-733.
49. Blankenberg S, Rupprecht HJ, Poirier O, Bickel C, Smieja M, Hafner G, Meyer J, Cambien F, Tiret L; AtheroGene Investigators. Plasma concentrations and genetic variation of matrix metalloproteinase 9 and prognosis of patients with cardiovascular disease. Circulation. 2003;107:1579-1585.
50. Kelly D, Cockerill G, Ng LL, Thompson M, Khan S, Samani NJ, Squire IB. Plasma matrix metalloproteinase-9 and left ventricular remodelling after acute myocardial infarction in man: A prospective cohort study. Eur Heart J. 2007;28:711-718.
51. Patterson NL, Iyer RP, De Castro Brs LE, Li Y, Andrews TG, Aune GJ, Lange RA, Lindsey ML. Using proteomics to uncover extracellular matrix interactions during cardiac remodeling. Proteomics Clin Appl. 2013;7:516-527.
52. Polyakova V, Hein S, Kostin S, Ziegelhoeffer T, Schaper J. Matrix metalloproteinases and their tissue inhibitors in pressure-overloaded human myocardium during heart failure progression. J Am Coll Cardiol. 2004;44:1609-1618.
53. Spinale FG, Coker ML, Heung LJ, Bond BR, Gunasinghe HR, Etoh T, Goldberg AT, Zellner JL, Crumbley AJ. A matrix metalloproteinase induction/activation system exists in the human left ventricular myocardium and is upregulated in heart failure. Circulation. 2000;102:1944-1949.
54. Regan L, Clarke ND. A tetrahedral zinc(II)-binding site introduced into a designed protein. Biochemistry. 1990;29:10878-10883.
55. Matouschek A, Kellis JJ, Serrano L, Fersht AR. Mapping the transient state-pathway of protein folding by protein engineering. Nature. 1989;340:122-126
56. Turner NA, Porter KE. Regulation of myocardial matrix metalloproteinase expression and activity by cardiac fibroblasts. IUBMB Life. 2012;64:143-150.
57. Lindner D, Zietsch C, Becher PM, Schulze K, Schultheiss HP, Tschpe C, Westermann D. Differential expression of matrix metalloproteases in human fibroblasts with different origins. Biochem Res Int. 2012;2012:875742. doi: 10.1155/2012/875742.
58. Matthews BW. Genetic and structural analysis of the protein stabilizing problem. Biochemistry. 1987;26:6885-6888.
59. ONeil KT, DeGrado WF. A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. Science. 1990;250: 646-651.
60. Raleigh DP, DeGrado WF. A De novo designed protein shows a thermally induced transition from a native to a molten globule-like state. J. Am. Chem. Soc. 1992;114:10079-10081.
61. Stawowy P, Margeta C, Kallisch H, Seidah NG, Chrtien M, Fleck E, Graf K. Regulation of matrix metalloproteinase MT1-MMP/MMP-2 in cardiac fibroblasts by TGF-beta1 involves furin-convertase. Cardiovasc Res. 2004;63:87-97.
62. Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 2000;14:163-176.
63. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: Regulators of the tumor microenvironment. Cell. 2010;141:52-67.
64. Ptitsyn OB. How does protein synthesis give rise to the 3D-structure FEBS Lett. 1991;285:176-181.
65. Leicht M, Briest W, Hlzl A, Zimmer HG. Serum depletion induces cell loss of rat cardiac fibroblasts and increased expression of extracellular matrix proteins in surviving cells. Cardiovasc Res. 2001;52:429-437.
66. Morley ME, Riches K, Peers C, Porter KE. Hypoxic inhibition of human cardiac fibroblast invasion and MMP-2 activation may impair adaptive myocardial remodelling. Biochem Soc Trans. 2007;35:905-907.
67. Sabeh F, Li XY, Saunders TL, Rowe RG, Weiss SJ. Secreted versus membrane-anchored collagenases: Relative roles in fibroblast-dependent collagenolysis and invasion. J Biol Chem. 2009;284:23001-23011.
68. Ptitsyn OB, Pain RH, Semisotnov GV, Zerovnik E, Razgulyaev OI. Evidence for a molten globule state as a general intermediate in protein folding. FEBS Lett. 1990;262:20-24.
69. Diaz-Araya G, Borg TK, Lavandero S, Loftis MJ, Carver W. IGF-1 modulation of rat cardiac fibroblast behavior and gene expression is age-dependent. Cell Commun Adhes. 2003;10:155-165.
70. Lindsey M, Wedin K, Brown MD, Keller C, Evans AJ, Smolen J, Burns AR, Rossen RD, Michael L, Entman M. Matrix-dependent mechanism of neutrophil-mediated release and activation of matrix metalloproteinase 9 in myocardial ischemia/reperfusion. Circulation. 2001;103:2181-2187.
71. Tester AM, Cox JH, Connor AR, Starr AE, Dean RA, Puente XS, Lpez-Otn C, Overall CM. LPS responsiveness and neutrophil chemotaxis in vivo require PMN MMP-8 activity. PLoS One. 2007;2:e312.
72. Owen CA, Hu Z, Lopez-Otin C, Shapiro SD. Membrane-bound matrix metalloproteinase-8 on activated polymorphonuclear cells is a potent, tissue inhibitor of metalloproteinase-resistant collagenase and serpinase. J Immunol. 2004;172:7791-7803.
73. Ernens I, Rouy D, Velot E, Devaux Y, Wagner DR. Adenosine inhibits matrix metalloproteinase-9 secretion by neutrophils: Implication of A2a receptor and cAMP/PKA/Ca2+ pathway. Circ Res. 2006;99:590-597.
74. OShea EK, Rutkowski R, Stafford WF 3rd, Kim PS. Preferential heterodimer formation by isolated leucine zippers from fos and jun. Science. 1989;245:646-648.
75. Chakrabarti S, Patel KD. Regulation of matrix metalloproteinase-9 release from IL-8-stimulated human neutrophils. J Leukoc Biol. 2005;78:279-288.
76. Owen CA, Hu Z, Barrick B, Shapiro SD. Inducible expression of tissue inhibitor of metalloproteinases-resistant matrix metalloproteinase-9 on the cell surface of neutrophils. Am J Respir Cell Mol Biol. 2003;29:283-294.
77. Huang WC, Sala-Newby GB, Susana A, Johnson JL, Newby AC. Classical macrophage activation up-regulates several matrix metalloproteinases through mitogen activated protein kinases and nuclear factor-B. PLoS One. 2012;7:e42507.
78. Osterhout JJJ, Handel T, Na G, Toumadje A, Long RC, Connolly PJ, Hoch JC, Johnson WC, Live D, DeGrado WF. Characterization of the structural properties of 11, a peptide designed to form a four-helix bundle. J Am Chem Soc. 1992;114:331-337.
79. Chase AJ, Bond M, Crook MF, Newby AC. Role of nuclear factor-kappa B activation in metalloproteinase-1,-3, and-9 secretion by human macrophages in vitro and rabbit foam cells produced in vivo. Arterioscler Thromb Vasc Biol. 2002;22:765-771.
80. Gong Y, Hart E, Shchurin A, Hoover-Plow J. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J Clin Invest. 2008;118:3012-3024.
81. Rohde LE, Ducharme A, Arroyo LH, Aikawa M, Sukhova GH, Lopez-Anaya A, McClure KF, Mitchell PG, Libby P, Lee RT. Matrix metalloproteinase inhibition attenuates early left ventricular enlargement after experimental myocardial infarction in mice. Circulation. 1999;99:3063-3070.
82. Mukherjee R, Brinsa TA, Dowdy KB, Scott AA, Baskin JM, Deschamps AM, Lowry AS, Escobar GP, Lucas DG, Yarbrough WM, Zile MR, Spinale FG. Myocardial infarct expansion and matrix metalloproteinase inhibition. Circulation. 2003;107:618-625.
83. Kaludercic N, Lindsey ML, Tavazzi B, Lazzarino G, Paolocci N. Inhibiting metalloproteases with PD 166793 in heart failure: Impact on cardiac remodeling and beyond. Cardiovasc Ther. 2008;26:24-37.
84. Yarbrough WM, Mukherjee R, Escobar GP, Mingoia JT, Sample JA, Hendrick JW, Dowdy KB, McLean JE, Lowry AS, ONeill TP, Spinale FG. Selective targeting and timing of matrix metalloproteinase inhibition in post-myocardial infarction remodeling. Circulation. 2003;108:1753-1759.
85. Robertson DE, Farid RS, Moser CC, Urbauer JL, Mulholland SE, Pidikiti R, Lear JD, Wand AJ, DeGrado WF, Dutton PL. Design and synthesis of multi-haem proteins. Nature. 1994;368:425-432.
86. Matsumura S, Iwanaga S, Mochizuki S, Okamoto H, Ogawa S, Okada Y. Targeted deletion or pharmacological inhibition of MMP-2 prevents cardiac rupture after myocardial infarction in mice. J Clin Invest. 2005;115:599-609.
87. Bench TJ, Jeremias A, Brown DL. Matrix metalloproteinase inhibition with tetracyclines for the treatment of coronary artery disease. Pharmacol Res. 2011;64:561-566.
88. Smith GN Jr, Mickler EA, Hasty KA, Brandt KD. Specificity of inhibition of matrix metalloproteinase activity by doxycycline: Relationship to structure of the enzyme. Arthritis Rheum. 1999;42:1140-1146.
89. Liu J, Xiong W, Baca-Regen L, Nagase H, Baxter BT. Mechanism of inhibition of matrix metalloproteinase-2 expression by doxycycline in human aortic smooth muscle cells. J Vasc Surg. 2003;38:1376-1383.
90. Morii H, Ichimura K, Uedaira H. Asymmetric inclusion by De novo designed proteins: Fluorescence probe studies on amphiphilic alpha-helix bundles. Proteins. 1991;11:133-141.
91. Jiang B, Chen J, Xu L, Gao Z, Deng Y, Wang Y, Xu F, Shen X, Guo DA. Salvianolic acid B functioned as a competitive inhibitor of matrix metalloproteinase-9 and efficiently prevented cardiac remodeling. BMC Pharmacol. 2010;10:10.
92. Morii H, Honda S, Ohashi S, Uedaira H. Alpha-helical assembly of biologically active peptides and designed helix bundle protein. Biopolymers. 1994;34:481-488.
93. Bristow MR, Larrabee P, Minobe W, Roden R, Skerl L, Klein J, Handwerger D, Port JD, Mller-Beckmann B. Receptor pharmacology of carvedilol in the human heart. J Cardiovasc Pharmacol. 1992;19(suppl 1):S68-S80.
94. Pauschinger M, Rutschow S, Chandrasekharan K, Westermann D, Weitz A, Peter Schwimmbeck L, Zeichhardt H, Poller W, Noutsias M, Li J. Carvedilol improves left ventricular function in murine coxsackievirus-induced acute myocarditis: Association with reduced myocardial interleukin-1[beta] and MMP-8 expression and a modulated immune response. Eur J Heart Fail. 2005;7:444-452.
95. Podesser BK, Siwik DA, Eberli FR, Sam F, Ngoy S, Lambert J, Ngo K, Apstein CS, Colucci WS. ET(A)-receptor blockade prevents matrix metalloproteinase activation late postmyocardial infarction in the rat. Am J Physiol Heart Circ Physiol. 2001;280:H984-H991.
96. Fraccarollo D, Galuppo P, Bauersachs J, Ertl G. Collagen accumulation after myocardial infarction: Effects of ETA receptor blockade and implications for early remodeling. Cardiovasc Res. 2002;54:559-567.
97. Creemers EE, Cleutjens JP, Smits JF, Daemen MJ. Matrix metalloproteinase inhibition after myocardial infarction: A new approach to prevent heart failure Circ Res. 2001;89:201-210.
98. Lindsey ML. MMP induction and inhibition in myocardial infarction. Heart Fail Rev. 2004;9:7-19.
99. Iyer RP, Patterson NL, Fields GB, Lindsey ML.. The history of matrix metalloproteinases: Milestones, myths, and misperceptions. Am J Physiol Heart Circ Physiol. 2012;303:H919-H930.
100. Hayashidani S, Tsutsui H, Ikeuchi M, Shiomi T, Matsusaka H, Kubota T, Imanaka-Yoshida K, Itoh T, Takeshita A. Targeted deletion of MMP-2 attenuates early LV rupture and late remodeling after experimental myocardial infarction. Am J Physiol Heart Circ Physiol. 2003;285:H1229-H1235.
101. Ducharme A, Frantz S, Aikawa M, Rabkin E, Lindsey M, Rohde LE, Schoen FJ, Kelly RA, Werb Z, Libby P, Lee RT. Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J Clin Invest. 2000;106:55-62.
102. Lematre V, OByrne TK, Dalal SS, Tall AR, DArmiento JM. Macrophage-specific expression of human collagenase (MMP-1) in transgenic mice. Ann N Y Acad Sci. 1999;878:736-739.
103. Wang GY, Bergman MR, Nguyen AP, Turcato S, Swigart PM, Rodrigo MC, Simpson PC, Karliner JS, Lovett DH, Baker AJ. Cardiac transgenic matrix metalloproteinase-2 expression directly induces impaired contractility. Cardiovasc Res. 2006;69:688-696.
104. Bergman MR, Teerlink JR, Mahimkar R, Li L, Zhu BQ, Nguyen A, Dahi S, Karliner JS, Lovett DH. Cardiac matrix metalloproteinase-2 expression independently induces marked ventricular remodeling and systolic dysfunction. Am J Physiol Heart Circ Physiol. 2007;292:H1847-H1860.
105. Spinale FG, Mukherjee R, Zavadzkas JA, Koval CN, Bouges S, Stroud RE, Dobrucki LW, Sinusas AJ. Cardiac restricted overexpression of membrane type-1 matrix metalloproteinase causes adverse myocardial remodeling following myocardial infarction. J Biol Chem. 2010;285:30316-30327.
106. Nie R, Xie S, Du B, Liu X, Deng B, Wang J. Extracellular matrix metalloproteinase inducer (EMMPRIN) is increased in human left ventricle after acute myocardial infarction. Arch Med Res. 2009;40:605-611.
107. Kandalam V, Basu R, Abraham T, Wang X, Soloway PD, Jaworski DM, Oudit GY, Kassiri Z. TIMP2 deficiency accelerates adverse post-myocardial infarction remodeling because of enhanced MT1-MMP activity despite lack of MMP2 activation. Circ Res. 2010;106:796-808.
108. Hammoud L, Lu X, Lei M, Feng Q. Deficiency in TIMP-3 increases cardiac rupture and mortality post-myocardial infarction via EGFR signaling: Beneficial effects of cetuximab. Basic Res Cardiol. 2011;106:459-471.
109. Koskivirta I, Kassiri Z, Rahkonen O, Kiviranta R, Oudit GY, McKee TD, Kyt V, Saraste A, Jokinen E, Liu PP, Vuorio E, Khokha R. Mice with tissue inhibitor of metalloproteinases 4 (Timp4) deletion succumb to induced myocardial infarction but not to cardiac pressure overload. J Biol Chem. 2010;285:24487-24493.
110. Mutter M. Natures rules and chemists tools: A way for creating novel proteins. Trends Biochem Sci. 1988;13:260-265.
111. Chiao YA, Zamilpa R, Lopez EF, Dai Q, Escobar GP, Hakala K, Weintraub ST, Lindsey ML. In vivo matrix metalloproteinase-7 substrates identified in the left ventricle post-myocardial infarction using proteomics. J Proteome Res. 2010;9:2649-2657.
112. Mukherjee R, Akar JG, Wharton JM, Adams DK, McClure CD, Stroud RE, Rice AD, DeSantis SM, Spinale FG, Gold MR. Plasma profiles of matrix metalloproteinases and tissue inhibitors of the metalloproteinases predict recurrence of atrial fibrillation following cardioversion. J Cardiovasc Transl Res. 2013;6:528-535.
113. Rose GD, Gierasch LM, Smith JA. Turns in peptides and proteins. Adv Protein Chem. 1985;37:1-109.
114. Webb CS, Bonnema DD, Ahmed SH, Leonardi AH, McClure CD, Clark LL, Stroud RE, Corn WC, Finklea L, Zile MR, Spinale FG. Specific temporal profile of matrix metalloproteinase release occurs in patients after myocardial infarction: Relation to left ventricular remodeling. Circulation. 2006;114:1020-1027.
115. Li YY, McTiernan CF, Feldman AM. Interplay of matrix metalloproteinases, tissue inhibitors of metalloproteinases and their regulators in cardiac matrix remodeling. Cardiovasc Res. 2000;46:214-224.
116. Zamilpa R, Lindsey ML. Extracellular matrix turnover and signaling during cardiac remodeling following MI: Causes and consequences. J Mol Cell Cardiol. 2010;48:558-563.
117. Mutter M, Tuchscherer G. The construction of new proteins: Template-assembled synthetic 4-helix bundle protein. Makromol Chem Rapid Commun. 1988;9:437-443.
118. Ulrich MM, Janssen AM, Daemen MJ, Rappaport L, Samuel JL, Contard F, Smits JF, Cleutjens JP. Increased expression of fibronectin isoforms after myocardial infarction in rats. J Mol Cell Cardiol. 1997;29:2533-2543.
119. Zamilpa R, Lopez EF, Chiao YA, Dai Q, Escobar GP, Hakala K, Weintraub ST, Lindsey ML. Proteomic analysis identifies in vivo candidate matrix metalloproteinase-9 substrates in the left ventricle postmyocardial infarction. Proteomics. 2010;10:2214-2223.
120. Trial J, Rossen RD, Rubio J, Knowlton AA. Inflammation and ischemia: Macrophages activated by fibronectin fragments enhance the survival of injured cardiac myocytes. Exp Biol Med (Maywood). 2004;229:538-545.
121. Arslan F, Smeets MB, Riem Vis PW, Karper JC, Quax PH, Bongartz LG, Peters JH, Hoefer IE, Doevendans PA, Pasterkamp G, De Kleijn DP. Lack of fibronectin-EDA promotes survival and prevents adverse remodeling and heart function deterioration after myocardial infarction. Circ Res. 2011;108:582-592.
122. Schnbeck U, Mach F, Libby P. Generation of biologically active IL-1 beta by matrix metalloproteinases: A novel caspase-1-independent pathway of IL-1 beta processing. J Immunol. 1998;161:3340-3346.
123. Hwang MW, Matsumori A, Furukawa Y, Ono K, Okada M, Iwasaki A, Hara M, Miyamoto T, Touma M, Sasayama S. Neutralization of interleukin-1beta in the acute phase of myocardial infarction promotes the progression of left ventricular remodeling. J Am Coll Cardiol. 2001;38:1546-1553.
124. Mitchell MD, Laird RE, Brown RD, Long CS. IL-1 beta stimulates rat cardiac fibroblast migration via MAP kinase pathways. Am J Physiol Heart Circ Physiol. 2007;292:H1139-1147.
125. Gurantz D, Cowling RT, Varki N, Frikovsky E, Moore CD, Greenberg BH. IL-1beta and TNF-alpha upregulate angiotensin II type 1 (AT1) receptors on cardiac fibroblasts and are associated with increased AT1 density in the post-MI heart. J Mol Cell Cardiol. 2005;38:505-515.
126. Sasaki T, Kaiser ET. Synthesis and structural stability of helichrome as an artificial hemeproteins. Biopolymers. 1990;29:79-88.
127. Parks WC, Wilson CL, Lpez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol. 2004;4:617-629.
128. Kandasamy AD, Chow AK, Ali MA, Schulz R. Matrix metalloproteinase-2 and myocardial oxidative stress injury: Beyond the matrix. Cardiovasc Res. 2010;85:413-423.
129. Dai W, Wold LE, Dow JS, Kloner RA. Thickening of the infarcted wall by collagen injection improves left ventricular function in rats: A novel approach to preserve cardiac function after myocardial infarction. J Am Coll Cardiol. 2005;46:714-719.
130. Sasaki T, Lieberman M. Between the secondary structure and the tertiary structure falls the globule: A problem in De novo protein design. Tetrahedron. 1993;49:3677-3689.
131. Lindsey ML, Weintraub ST, Lange RA. Using extracellular matrix proteomics to understand left ventricular remodeling. Circ Cardiovasc Genet. 2012;5:o1-o7.
132. Herzog E, Gu A, Kohmoto T, Burkhoff D, Hochman JS. Early activation of metalloproteinases after experimental myocardial infarction occurs in infarct and non-infarct zones. Cardiovasc Pathol. 1998;7:307-312.
133. Chen J, Tung CH, Allport JR, Chen S, Weissleder R, Huang PL. Near-infrared fluorescent imaging of matrix metalloproteinase activity after myocardial infarction. Circulation. 2005;111:1800-1805.
134. Eckart RE, Uyehara CF, Shry EA, Furgerson JL, Krasuski RA. Matrix metalloproteinases in patients with myocardial infarction and percutaneous revascularization. J Interv Cardiol. 2004;17:27-31.
135. Kai H, Ikeda H, Yasukawa H, Kai M, Seki Y, Kuwahara F, Ueno T, Sugi K, Imaizumi T. Peripheral blood levels of matrix metalloproteases-2 and-9 are elevated in patients with acute coronary syndromes. J Am Coll Cardiol. 1998;32:368-372.
136. Wagner DR, Delagardelle C, Ernens I, Rouy D, Vaillant M, Beissel J. Matrix metalloproteinase-9 is a marker of heart failure after acute myocardial infarction. J Card Fail. 2006;12:66-72.
137. Lindsey ML, Escobar GP, Dobrucki LW, Goshorn DK, Bouges S, Mingoia JT, McClister DM Jr, Su H, Gannon J, MacGillivray C, Lee RT, Sinusas AJ, Spinale FG. Matrix metalloproteinase-9 gene deletion facilitates angiogenesis after myocardial infarction. Am J Physiol Heart Circ Physiol. 2006;290:H232-H239.
138. Hlatky MA, Ashley E, Quertermous T, Boothroyd DB, Ridker P, Southwick A, Myers RM, Iribarren C, Fortmann SP, Go AS; Atherosclerotic Disease, Vascular Function and Genetic Epidemiology (ADVANCE) Study. Matrix metalloproteinase circulating levels, genetic polymorphisms, and susceptibility to acute myocardial infarction among patients with coronary artery disease. Am Heart J. 2007;154:1043-1051.
139. Lindsey ML, Gannon J, Aikawa M, Schoen FJ, Rabkin E, Lopresti-Morrow L, Crawford J, Black S, Libby P, Mitchell PG, Lee RT. Selective matrix metalloproteinase inhibition reduces left ventricular remodeling but does not inhibit angiogenesis after myocardial infarction. Circulation. 2002;105:753-758.
140. Kandalam V, Basu R, Abraham T, Wang X, Awad A, Wang W, Lopaschuk GD, Maeda N, Oudit GY, Kassiri Z. Early activation of matrix metalloproteinases underlies the exacerbated systolic and diastolic dysfunction in mice lacking TIMP3 following myocardial infarction. Am J Physiol Heart Circ Physiol. 2010;299:H1012-H1023.