Mechanistic relationship between membrane type-1 matrix metalloproteinase and the myocardial response to pressure overload

Circulation: Heart Failure

Volumn 7, Issue 2, 2014, Pages 340-350

  Zile, Michael R ^a   Baicu, Catalin F ^a   Stroud, Robert E ^a   Van Laer, An O ^a   Jones, Jeffrey A ^a   Patel, Risha ^a   Mukherjee, Rupak ^a   Spinale, Francis G ^b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Hypertrophy; Left ventricular; Matrix metalloproteinases

Indexed keywords

BINDING PROTEIN; COLLAGEN; LATENCY ASSOCIATED TRANSFORMING GROWTH FACTOR BINDING PROTEIN 1; MATRIX METALLOPROTEINASE 14; UNCLASSIFIED DRUG; MATRIX METALLOPROTEINASE; RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEART LEFT VENTRICLE MASS; HEART LEFT VENTRICLE OVERLOAD; HYDROLYSIS; LEFT VENTRICULAR DIASTOLIC DYSFUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; ANIMAL; BIOSYNTHESIS; DISEASE MODEL; ECHOCARDIOGRAPHY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEART LEFT VENTRICLE HYPERTROPHY; HEART MUSCLE; HEART VENTRICLE PRESSURE; HEART VENTRICLE REMODELING; HYPERTROPHY; IMMUNOBLOTTING; LEFT VENTRICULAR; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

HYPERTROPHY; LEFT VENTRICULAR; MATRIX METALLOPROTEINASES;

ANIMALS; DISEASE MODELS, ANIMAL; ECHOCARDIOGRAPHY; GENE EXPRESSION REGULATION; HYPERTROPHY, LEFT VENTRICULAR; IMMUNOBLOTTING; MATRIX METALLOPROTEINASE 14; MICE; MICE, TRANSGENIC; MYOCARDIUM; REAL-TIME POLYMERASE CHAIN REACTION; RNA; VENTRICULAR PRESSURE; VENTRICULAR REMODELING;

EID: 84899905661     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.113.000984     Document Type: Article

References (53)

1. Zile MR, Baicu CF, Stroud RE, Van Laer A, Arroyo J, Mukherjee R, Jones JA, Spinale FG. Pressure overload-dependent membrane type 1-matrix metalloproteinase induction: relationship to LV remodeling and fibrosis. Am J Physiol Heart Circ Physiol. 2012;302:H1429-H1437.
2. Zile MR, Gottdiener JS, Hetzel SJ, McMurray JJ, Komajda M, McKelvie R, Baicu CF, Massie BM, Carson PE; I-PRESERVE Investigators. Prevalence and significance of alterations in cardiac structure and function in patients with heart failure and a preserved ejection fraction. Circulation. 2011;124:2491-2501.
3. Zile MR, Baicu CF, Gaasch WH. Diastolic heart failure-abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med. 2004;350:1953-1959.
4. Westermann D, Kasner M, Steendijk P, Spillmann F, Riad A, Weitmann K, Hoffmann W, Poller W, Pauschinger M, Schultheiss HP, Tschöpe C. Role of left ventricular stiffness in heart failure with normal ejection fraction. Circulation. 2008;117:2051-2060.
5. Weidemann F, Herrmann S, Störk S, Niemann M, Frantz S, Lange V, Beer M, Gattenlöhner S, Voelker W, Ertl G, Strotmann JM. Impact of myocardial fibrosis in patients with symptomatic severe aortic stenosis. Circulation. 2009;120:577-584.
6. Azevedo CF, Nigri M, Higuchi ML, Pomerantzeff PM, Spina GS, Sampaio RO, Tarasoutchi F, Grinberg M, Rochitte CE. Prognostic significance of myocardial fibrosis quantification by histopathology and magnetic resonance imaging in patients with severe aortic valve disease. J Am Coll Cardiol. 2010;56:278-287.
7. Kasner M, Westermann D, Lopez B, Gaub R, Escher F, KÜhl U, Schultheiss HP, Tschöpe C. Diastolic tissue Doppler indexes correlate with the degree of collagen expression and cross-linking in heart failure and normal ejection fraction. J Am Coll Cardiol. 2011;57:977-985.
8. Baicu CF, Li J, Zhang Y, Kasiganesan H, Cooper G 4th, Zile MR, Bradshaw AD. Time course of right ventricular pressure-overload induced myocardial fibrosis: relationship to changes in fibroblast postsynthetic procollagen processing. Am J Physiol Heart Circ Physiol. 2012;303:H1128-H1134.
9. Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev. 2007;87:1285-1342.
10. Creemers EE, Pinto YM. Molecular mechanisms that control interstitial fibrosis in the pressure-overloaded heart. Cardiovasc Res. 2011;89:265-272.
11. Goldsmith EC, Bradshaw AD, Spinale FG. Cellular mechanisms of tissue fibrosis. 2. Contributory pathways leading to myocardial fibrosis: moving beyond collagen expression. Am J Physiol Cell Physiol. 2013;304:C393-C402.
12. 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.
13. Malemud CJ. Matrix metalloproteinases (MMPs) in health and disease: An overview. Front Biosci. 2006;11:1696-1701.
14. Spinale FG, Janicki JS, Zile MR. Membrane-associated matrix proteolysis and heart failure. Circ Res. 2013;112:195-208.
15. Spinale FG, Zile MR. Integrating the myocardial matrix into heart failure recognition and management. Circ Res. 2013;113:725-738.
16. Karsdal MA, Larsen L, Engsig MT, Lou H, Ferreras M, Lochter A, Delaissé JM, Foged NT. Matrix metalloproteinase-dependent activation of latent transforming growth factor-beta controls the conversion of osteoblasts into osteocytes by blocking osteoblast apoptosis. J Biol Chem. 2002;277:44061-44067.
17. Spinale FG, Escobar GP, Mukherjee R, Zavadzkas JA, Saunders SM, Jeffords LB, Leone AM, Beck C, Bouges S, Stroud RE. Cardiac-restricted overexpression of membrane type-1 matrix metalloproteinase in mice: effects on myocardial remodeling with aging. Circ Heart Fail. 2009;2:351-360.
18. Zhou Z, Apte SS, Soininen R, Cao R, Baaklini GY, Rauser RW, Wang J, Cao Y, Tryggvason K. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci U S A. 2000;97:4052-4057.
19. Zavadzkas JA, Mukherjee R, Rivers WT, Patel RK, Meyer EC, Black LE, McKinney RA, Oelsen JM, Stroud RE, Spinale FG. Direct regulation of membrane type 1 matrix metalloproteinase following myocardial infarction causes changes in survival, cardiac function, and remodeling. Am J Physiol Heart Circ Physiol. 2011;301:H1656-H1666.
20. Bradshaw AD, Baicu CF, Rentz TJ, Van Laer AO, Boggs J, Lacy JM, Zile MR. Pressure overload-induced alterations in fibrillar collagen content and myocardial diastolic function: role of secreted protein acidic and rich in cysteine (SPARC) in post-synthetic procollagen processing. Circulation. 2009;119:269-280.
21. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, John Sutton M, Stewart WJ. Recommendations for chamber quantification: A report from the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a Branch of the European Society of Cardiology. J Am Soc Echocardiogr. 2005;18:1440-1463.
22. Lam CS, Roger VL, Rodeheffer RJ, Bursi F, Borlaug BA, Ommen SR, Kass DA, Redfield MM. Cardiac structure and ventricular-vascular function in persons with heart failure and preserved ejection fraction from Olmsted County, Minnesota. Circulation. 2007;115:1982-1990.
23. Melenovsky V, Borlaug BA, Rosen B, Hay I, Ferruci L, Morell CH, Lakatta EG, Najjar SS, Kass DA. Cardiovascular features of heart failure with preserved ejection fraction versus nonfailing hypertensive left ventricular hypertrophy in the urban Baltimore community: The role of atrial remodeling/dysfunction. J Am Coll Cardiol. 2007;49:198-207.
24. Blom AS, Mukherjee R, Pilla JJ, Lowry AS, Yarbrough WM, Mingoia JT, Hendrick JW, Stroud RE, McLean JE, Affuso J, Gorman RC, Gorman JH 3rd, Acker MA, Spinale FG. Cardiac support device modifies left ventricular geometry and myocardial structure after myocardial infarction. Circulation. 2005;112:1274-1283.
25. Deschamps AM, Yarbrough WM, Squires CE, Allen RA, McClister DM, Dowdy KB, McLean JE, Mingoia JT, Sample JA, Mukherjee R, Spinale FG. Trafficking of the membrane type-1 matrix metalloproteinase in ischemia and reperfusion: relation to interstitial membrane type-1 matrix metalloproteinase activity. Circulation. 2005;111:1166-1174.
26. Dixon JA, Gaillard WF 2nd, Rivers WT, Koval CN, Stroud RE, Mukherjee R, Spinale FG. Heterogeneity in MT1-MMP activity with ischemia-reperfusion and previous myocardial infarction: relation to regional myocardial function. Am J Physiol Heart Circ Physiol. 2010;299:H1947-H1958.
27. 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.
28. Ruddy JM, Jones JA, Stroud RE, Mukherjee R, Spinale FG, Ikonomidis JS. Differential effects of mechanical and biological stimuli on matrix metalloproteinase promoter activation in the thoracic aorta. Circulation. 2009;120(suppl 11):S262-S268.
29. van Heerebeek L, Franssen CP, Hamdani N, Verheugt FW, Somsen GA, Paulus WJ. Molecular and cellular basis for diastolic dysfunction. Curr Heart Fail Rep. 2012;9:293-302.
30. Hamdani N, Paulus WJ. Myocardial titin and collagen in cardiac diastolic dysfunction: partners in crime. Circulation. 2013;128:5-8.
31. Zile MR, Baicu CF. Alterations in ventricular function: diastolic heart failure, Chapter 14. In: Mann DL, ed. Heart Failure: A Companion to Braunwald's Heart Disease, 2nd ed. Philadelphia, PA: Elsevier; 2010.
32. Gaasch WH, Zile MR. Left ventricular structural remodeling in health and disease: with special emphasis on volume, mass, and geometry. J Am Coll Cardiol. 2011;58:1733-1740.
33. Villar AV, Garc?a R, Llano M, Cobo M, Merino D, Lantero A, Tramullas M, Hurl? JM, Hurl? MA, Nistal JF. BAMBI (BMP and activin membrane-bound inhibitor) protects the murine heart from pressure-overload biomechanical stress by restraining TGF-β signaling. Biochim Biophys Acta. 2013;1832:323-335.
34. Dobaczewski M, Chen W, Frangogiannis NG. Transforming growth factor (TGF)-β signaling in cardiac remodeling. J Mol Cell Cardiol. 2011;51:600-606.
35. Villar AV, Cobo M, Llano M, Montalvo C, González-Vílchez F, Martín-Durán R, Hurlé MA, Nistal JF. Plasma levels of transforming growth factor-beta1 reflect left ventricular remodeling in aortic stenosis. PLoS One. 2009;4:e8476.
36. Gordon KJ, Blobe GC. Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim Biophys Acta. 2008;1782:197-228.
37. Bjørnstad JL, Skrbic B, Marstein HS, Hasic A, Sjaastad I, Louch WE, Florholmen G, Christensen G, Tønnessen T. Inhibition of SMAD2 phosphorylation preserves cardiac function during pressure overload. Cardiovasc Res. 2012;93:100-110.
38. Bujak M, Ren G, Kweon HJ, Dobaczewski M, Reddy A, Taffet G, Wang XF, Frangogiannis NG. Essential role of Smad3 in infarct healing and in the pathogenesis of cardiac remodeling. Circulation. 2007;116:2127-2138.
39. Koshikawa N, Minegishi T, Sharabi A, Quaranta V, Seiki M. Membrane-type matrix metalloproteinase-1 (MT1-MMP) is a processing enzyme for human laminin gamma 2 chain. J Biol Chem. 2005;280:88-93.
40. Kridel SJ, Sawai H, Ratnikov BI, Chen EI, Li W, Godzik A, Strongin AY, Smith JW. A unique substrate binding mode discriminates membrane type-1 matrix metalloproteinase from other matrix metalloproteinases. J Biol Chem. 2002;277:23788-23793.
41. Kudo T, Takino T, Miyamori H, Thompson EW, Sato H. Substrate choice of membrane-type 1 matrix metalloproteinase is dictated by tissue inhibitor of metalloproteinase-2 levels. Cancer Sci. 2007;98:563-568.
42. Newby AC. Matrix metalloproteinases regulate migration, proliferation, and death of vascular smooth muscle cells by degrading matrix and non-matrix substrates. Cardiovasc Res. 2006;69:614-624.
43. Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, Okada Y. Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem. 1997;272:2446-2451.
44. Williams LM, Gibbons DL, Gearing A, Maini RN, Feldmann M, Brennan FM. Paradoxical effects of a synthetic metalloproteinase inhibitor that blocks both p55 and p75 TNF receptor shedding and TNF alpha processing in RA synovial membrane cell cultures. J Clin Invest. 1996;97:2833-2841.
45. Guo C, Piacentini L. Type I collagen-induced MMP-2 activation coincides with up-regulation of membrane type 1-matrix metalloproteinase and TIMP-2 in cardiac fibroblasts. J Biol Chem. 2003;278:46699-46708.
46. Dallas SL, Rosser JL, Mundy GR, Bonewald LF. Proteolysis of latent transforming growth factor-beta (TGF-beta)-binding protein-1 by osteoclasts. A cellular mechanism for release of TGF-beta from bone matrix. J Biol Chem. 2002;277:21352-21360.
47. Tatti O, Vehviläinen P, Lehti K, Keski-Oja J. MT1-MMP releases latent TGF-beta1 from endothelial cell extracellular matrix via proteolytic processing of LTBP-1. Exp Cell Res. 2008;314:2501-2514.
48. Hawinkels LJ, Kuiper P, Wiercinska E, Verspaget HW, Liu Z, Pardali E, Sier CF, ten Dijke P. Matrix metalloproteinase-14 (MT1-MMP)-mediated endoglin shedding inhibits tumor angiogenesis. Cancer Res. 2010;70:4141-4150.
49. Koitabashi N, Danner T, Zaiman AL, Pinto YM, Rowell J, Mankowski J, Zhang D, Nakamura T, Takimoto E, Kass DA. Koitabashi N, Danner T, Zaiman AL, Pinto YM, Rowell J, Mankowski J, Zhang D, Nakamura T, Takimoto E, Kass DA. Pivotal role of cardiomyocyte TGF-beta signaling in the murine pathological response to sustained pressure overload. J Clin Invest. 2011; 121:2301-12.
50. 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.
51. Zhao H, Bernardo MM, Osenkowski P, Sohail A, Pei D, Nagase H, Kashiwagi M, Soloway PD, DeClerck YA, Fridman R. Differential inhibition of membrane type 3 (MT3)-matrix metalloproteinase (MMP) and MT1-MMP by tissue inhibitor of metalloproteinase (TIMP)-2 and TIMP-3 rgulates pro-MMP-2 activation. J Biol Chem. 2004;279:8592-8601.
52. Gomez DE, Alonso DF, Yoshiji H, Thorgeirsson UP. Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol. 1997;74:111-122.
53. Coppola JM, Bhojani MS, Ross BD, Rehemtulla A. A small-molecule furin inhibitor inhibits cancer cell motility and invasiveness. Neoplasia. 2008;10:363-370.