A Disintegrin and Metalloprotease-17 Regulates Pressure Overload-Induced Myocardial Hypertrophy and Dysfunction Through Proteolytic Processing of Integrin β1

Hypertension

Volumn 68, Issue 4, 2016, Pages 937-948

  Fan, Dong ^a,d   Takawale, Abhijit ^a,d   Shen, Mengcheng ^a,d   Samokhvalov, Victor ^a,d   Basu, Ratnadeep ^c,d   Patel, Vaibhav ^c,d   Wang, Xiuhua ^a,d   Fernandez Patron, Carlos ^b,d   Seubert, John M ^a,d   Oudit, Gavin Y ^c,d   Kassiri, Zamaneh ^a,d  

^a UNIVERSITY OF ALBERTA   (Canada)

^b Department of Biochemistry ^*  (United States)

^c Faculty of Medicine and Dentistry   (Canada)

^d MAZANKOWSKI ALBERTA HEART INSTITUTE   (Canada)

Author keywords

angiotensin II; dilated cardiomyopathy; disintegrin; hypertrophy; upregulation

Indexed keywords

ALPHA5 INTEGRIN; ALPHA7 INTEGRIN; BETA1 INTEGRIN; DISINTEGRIN; FOCAL ADHESION KINASE; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; MATRIX METALLOPROTEINASE 17; ANGIOTENSIN II; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; CARDIAC MUSCLE CELL; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENZYME ACTIVATION; GENE SILENCING; HEART LEFT VENTRICLE OVERLOAD; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; IN VITRO STUDY; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; RAT; STRETCHING; SYSTOLIC DYSFUNCTION; UPREGULATION; ANIMAL; CELL CULTURE; CHEMICALLY INDUCED; COMPARATIVE STUDY; COMPLICATION; CYTOLOGY; DIAGNOSTIC IMAGING; DISEASE MODEL; DOPPLER ECHOCARDIOGRAPHY; HEART LEFT VENTRICLE FUNCTION; HEART LEFT VENTRICLE HYPERTROPHY; HYPERTENSION; HYPERTROPHIC CARDIOMYOPATHY; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; RANDOMIZATION;

ADAM17 PROTEIN; ANGIOTENSIN II; ANIMALS; CARDIOMYOPATHY, HYPERTROPHIC; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DISINTEGRINS; ECHOCARDIOGRAPHY, DOPPLER; HYPERTENSION; HYPERTROPHY, LEFT VENTRICULAR; MICE; MICE, KNOCKOUT; MYOCYTES, CARDIAC; PROTEOLYSIS; RANDOM ALLOCATION; RATS; VENTRICULAR DYSFUNCTION, LEFT;

EID: 84983362338     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.116.07566     Document Type: Article

References (46)

1. Spinale FG, Zile MR. Integrating the myocardial matrix into heart failure recognition and management. Circ Res. 2013;113:725-738. doi: 10.1161/CIRCRESAHA.113.300309.
2. Díez J, Frohlich ED. A translational approach to hypertensive heart disease. Hypertension. 2010;55:1-8. doi: 10.1161/HYPERTENSIONAHA.109.141887.
3. Fan D, Creemers EE, Kassiri Z. Matrix as an interstitial transport system. Circ Res. 2014;114:889-902. doi: 10.1161/CIRCRESAHA.114.302335.
4. Zhang P, Shen M, Fernandez-Patron C, Kassiri Z. ADAMs family and relatives in cardiovascular physiology and pathology. J Mol Cell Cardiol. 2016;93:186-199. doi: 10.1016/j.yjmcc.2015.10.031.
5. Israeli-Rosenberg S, Manso AM, Okada H, Ross RS. Integrins and integrin-associated proteins in the cardiac myocyte. Circ Res. 2014;114:572-586. doi: 10.1161/CIRCRESAHA.114.301275.
6. Chen C, Li R, Ross RS, Manso AM. Integrins and integrin-related proteins in cardiac fibrosis. J Mol Cell Cardiol. 2016;93:162-174. doi: 10.1016/j. yjmcc.2015.11.010.
7. Ross RS, Pham C, Shai SY, Goldhaber JI, Fenczik C, Glembotski CC, Ginsberg MH, Loftus JC. Beta1 integrins participate in the hypertrophic response of rat ventricular myocytes. Circ Res. 1998;82:1160-1172.
8. Shai SY, Harpf AE, Babbitt CJ, Jordan MC, Fishbein MC, Chen J, Omura M, Leil TA, Becker KD, Jiang M, Smith DJ, Cherry SR, Loftus JC, Ross RS. Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ Res. 2002;90:458-464.
9. Asakura M, Kitakaze M, Takashima S, et al. Cardiac hypertrophy is inhibited by antagonism of ADAM12 processing of HB-EGF: metalloproteinase inhibitors as a new therapy. Nat Med. 2002;8:35-40. doi: 10.1038/nm0102-35.
10. Fedak PW, Moravec CS, McCarthy PM, Altamentova SM, Wong AP, Skrtic M, Verma S, Weisel RD, Li RK. Altered expression of disintegrin metalloproteinases and their inhibitor in human dilated cardiomyopathy. Circulation. 2006;113:238-245. doi: 10.1161/CIRCULATIONAHA.105.571414.
11. Wang X, Oka T, Chow FL, Cooper SB, Odenbach J, Lopaschuk GD, Kassiri Z, Fernandez-Patron C. Tumor necrosis factor-alpha-converting enzyme is a key regulator of agonist-induced cardiac hypertrophy and fibrosis. Hypertension. 2009;54:575-582. doi: 10.1161/HYPERTENSIONAHA.108.127670.
12. Peschon JJ, Slack JL, Reddy P, et al. An essential role for ectodomain shedding in mammalian development. Science. 1998;282:1281-1284.
13. Fan D, Takawale A, Shen M, Wang W, Wang X, Basu R, Oudit GY, Kassiri Z. Cardiomyocyte a disintegrin and metalloproteinase 17 (ADAM17) is essential in post-myocardial infarction repair by regulating angiogenesis. Circ Heart Fail. 2015;8:970-979. doi: 10.1161/CIRCHEARTFAILURE.114.002029.
14. Kandalam V, Basu R, Moore L, Fan D, Wang X, Jaworski DM, Oudit GY, Kassiri Z. Lack of tissue inhibitor of metalloproteinases 2 leads to exacerbated left ventricular dysfunction and adverse extracellular matrix remodeling in response to biomechanical stress. Circulation. 2011;124:2094-2105. doi: 10.1161/CIRCULATIONAHA.111.030338.
15. Patel VB, Wang Z, Fan D, Zhabyeyev P, Basu R, Das SK, Wang W, Desaulniers J, Holland SM, Kassiri Z, Oudit GY. Loss of p47phox subunit enhances susceptibility to biomechanical stress and heart failure because of dysregulation of cortactin and actin filaments. Circ Res. 2013;112:1542-1556. doi: 10.1161/CIRCRESAHA.111.300299.
16. Zhong J, Basu R, Guo D, Chow FL, Byrns S, Schuster M, Loibner H, Wang XH, Penninger JM, Kassiri Z, Oudit GY. Angiotensin-converting enzyme 2 suppresses pathological hypertrophy, myocardial fibrosis, and cardiac dysfunction. Circulation. 2010;122:717-728. doi: 10.1161/CIRCULATIONAHA.110.955369.
17. Zhong J, Guo D, Chen CB, Wang W, Schuster M, Loibner H, Penninger JM, Scholey JW, Kassiri Z, Oudit GY. Prevention of angiotensin II-mediated renal oxidative stress, inflammation, and fibrosis by angiotensin-converting enzyme 2. Hypertension. 2011;57:314-322. doi: 10.1161/HYPERTENSIONAHA.110.164244.
18. Mori J, Basu R, McLean BA, Das SK, Zhang L, Patel VB, Wagg CS, Kassiri Z, Lopaschuk GD, Oudit GY. Agonist-induced hypertrophy and diastolic dysfunction are associated with selective reduction in glucose oxidation: a metabolic contribution to heart failure with normal ejection fraction. Circ Heart Fail. 2012;5:493-503. doi: 10.1161/CIRCHEARTFAILURE.112.966705.
19. Fan D, Takawale A, Basu R, Patel V, Lee J, Kandalam V, Wang X, Oudit GY, Kassiri Z. Differential role of TIMP2 and TIMP3 in cardiac hypertrophy, fibrosis, and diastolic dysfunction. Cardiovasc Res. 2014;103:268-280. doi: 10.1093/cvr/cvu072.
20. 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. doi: 10.1152/ajpheart.00246.2010.
21. 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. doi: 10.1161/CIRCRESAHA.109.209189.
22. Basu R, Oudit GY, Wang X, Zhang L, Ussher JR, Lopaschuk GD, Kassiri Z. Type 1 diabetic cardiomyopathy in the Akita (Ins2WT/C96Y) mouse model is characterized by lipotoxicity and diastolic dysfunction with preserved systolic function. Am J Physiol Heart Circ Physiol. 2009;297:H2096-H2108. doi: 10.1152/ajpheart.00452.2009.
23. Samokhvalov V, Zlobine I, Jamieson KL, Jurasz P, Chen C, Lee KS, Hammock BD, Seubert JM. PPAR? signaling mediates the cytotoxicity of DHA in H9c2 cells. Toxicol Lett. 2015;232:10-20. doi: 10.1016/j. toxlet.2014.09.029.
24. Kassiri Z, Zobel C, Nguyen TT, Molkentin JD, Backx PH. Reduction of I(to) causes hypertrophy in neonatal rat ventricular myocytes. Circ Res. 2002;90:578-585.
25. Frank D, Kuhn C, Brors B, Hanselmann C, Lüdde M, Katus HA, Frey N. Gene expression pattern in biomechanically stretched cardiomyocytes: evidence for a stretch-specific gene program. Hypertension. 2008;51:309-318. doi: 10.1161/HYPERTENSIONAHA.107.098046.
26. Das SK, Wang W, Zhabyeyev P, Basu R, McLean B, Fan D, Parajuli N, DesAulniers J, Patel VB, Hajjar RJ, Dyck JR, Kassiri Z, Oudit GY. Ironoverload injury and cardiomyopathy in acquired and genetic models is attenuated by resveratrol therapy. Sci Rep. 2015;5:18132. doi: 10.1038/srep18132.
27. Pérez-Martínez L, Jaworski DM. Tissue inhibitor of metalloproteinase-2 promotes neuronal differentiation by acting as an anti-mitogenic signal. J Neurosci. 2005;25:4917-4929. doi: 10.1523/JNEUROSCI.5066-04.2005.
28. Wang W, McKinnie SM, Patel VB, Haddad G, Wang Z, Zhabyeyev P, Das SK, Basu R, McLean B, Kandalam V, Penninger JM, Kassiri Z, Vederas JC, Murray AG, Oudit GY. Loss of apelin exacerbates myocardial infarction adverse remodeling and ischemia-reperfusion injury: therapeutic potential of synthetic apelin analogues. J Am Heart Assoc. 2013;2:e000249. doi: 10.1161/JAHA.113.000249.
29. Kassiri Z, Oudit GY, Sanchez O, Dawood F, Mohammed FF, Nuttall RK, Edwards DR, Liu PP, Backx PH, Khokha R. Combination of tumor necrosis factor-alpha ablation and matrix metalloproteinase inhibition prevents heart failure after pressure overload in tissue inhibitor of metalloproteinase-3 knock-out mice. Circ Res. 2005;97:380-390. doi: 10.1161/01. RES.0000178789.16929.c.f.
30. Shiojima I, Sato K, Izumiya Y, Schiekofer S, Ito M, Liao R, Colucci WS, Walsh K. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J Clin Invest. 2005;115:2108-2118. doi: 10.1172/JCI24682.
31. Oka T, Akazawa H, Naito AT, Komuro I. Angiogenesis and cardiac hypertrophy: maintenance of cardiac function and causative roles in heart failure. Circ Res. 2014;114:565-571. doi: 10.1161/CIRCRESAHA.114.300507.
32. Li R, Wu Y, Manso AM, Gu Y, Liao P, Israeli S, Yajima T, Nguyen U, Huang MS, Dalton ND, Peterson KL, Ross RS. 1 integrin gene excision in the adult murine cardiac myocyte causes defective mechanical and signaling responses. Am J Pathol. 2012;180:952-962. doi: 10.1016/j. ajpath.2011.12.007.
33. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389-3402.
34. Tucher J, Linke D, Koudelka T, Cassidy L, Tredup C, Wichert R, Pietrzik C, Becker-Pauly C, Tholey A. LC-MS based cleavage site profiling of the proteases ADAM10 and ADAM17 using proteome-derived peptide libraries. J Proteome Res. 2014;13:2205-2214. doi: 10.1021/pr401135u.
35. Levy D, Larson MG, Vasan RS, Kannel WB, Ho KK. The progression from hypertension to congestive heart failure. JAMA. 1996;275:1557-1562.
36. Clemente CF, Tornatore TF, Theizen TH, Deckmann AC, Pereira TC, Lopes-Cendes I, Souza JR, Franchini KG. Targeting focal adhesion kinase with small interfering RNA prevents and reverses load-induced cardiac hypertrophy in mice. Circ Res. 2007;101:1339-1348. doi: 10.1161/CIRCRESAHA.107.160978.
37. Franchini KG. Focal adhesion kinase-the basis of local hypertrophic signaling domains. J Mol Cell Cardiol. 2012;52:485-492. doi: 10.1016/j. yjmcc.2011.06.021.
38. DiMichele LA, Doherty JT, Rojas M, Beggs HE, Reichardt LF, Mack CP, Taylor JM. Myocyte-restricted focal adhesion kinase deletion attenuates pressure overload-induced hypertrophy. Circ Res. 2006;99:636-645. doi: 10.1161/01.RES.0000240498.44752.d6.
39. Okada H, Lai NC, Kawaraguchi Y, et al. Integrins protect cardiomyocytes from ischemia/reperfusion injury. J Clin Invest. 2013;123:4294-4308. doi: 10.1172/JCI64216.
40. Pugach EK, Richmond PA, Azofeifa JG, Dowell RD, Leinwand LA. Prolonged Cre expression driven by the ?-myosin heavy chain promoter can be cardiotoxic. J Mol Cell Cardiol. 2015;86:54-61. doi: 10.1016/j. yjmcc.2015.06.019.
41. Guo J, Mihic A, Wu J, Zhang Y, Singh K, Dhingra S, Weisel RD, Li RK. Canopy 2 attenuates the transition from compensatory hypertrophy to dilated heart failure in hypertrophic cardiomyopathy. Eur Heart J. 2015;36:2530-2540. doi: 10.1093/eurheartj/ehv294.
42. Takawale A, Sakamuri SS, Kassiri Z. Extracellular matrix communication and turnover in cardiac physiology and pathology. Compr Physiol. 2015;5:687-719. doi: 10.1002/cphy.c140045.
43. Wipff PJ, Hinz B. Integrins and the activation of latent transforming growth factor beta1-an intimate relationship. Eur J Cell Biol. 2008;87:601-615. doi: 10.1016/j.ejcb.2008.01.012.
44. Manso AM, Elsherif L, Kang SM, Ross RS. Integrins, membrane-type matrix metalloproteinases and ADAMs: potential implications for cardiac remodeling. Cardiovasc Res. 2006;69:574-584. doi: 10.1016/j. cardiores.2005.09.004.
45. Bax DV, Messent AJ, Tart J, van Hoang M, Kott J, Maciewicz RA, Humphries MJ. Integrin alpha5beta1 and ADAM-17 interact in vitro and co-localize in migrating HeLa cells. J Biol Chem. 2004;279:22377-22386. doi: 10.1074/jbc.M400180200.
46. Gooz P, Dang Y, Higashiyama S, Twal WO, Haycraft CJ, Gooz M. A disintegrin and metalloenzyme (ADAM) 17 activation is regulated by 51 integrin in kidney mesangial cells. PLoS One. 2012;7:e33350. doi: 10.1371/journal.pone.0033350.