Enhanced susceptibility to biomechanical stress in ACE2 null mice is prevented by loss of the p47phox NADPH oxidase subunit

Cardiovascular Research

Volumn 91, Issue 1, 2011, Pages 151-161

  Bodiga, Sreedhar ^a   Zhong, Jiu Chang ^a   Wang, Wang ^a   Basu, Ratnadeep ^a   Lo, Jennifer ^a   Liu, George C ^b   Guo, Danny ^a   Holland, Steven M ^c   Scholey, James W ^a   Penninger, Josef M ^d   Kassiri, Zamaneh ^a   Oudit, Gavin Y ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

Author keywords

Angiotensin 17; Angiotensin converting enzyme 2; NADPH oxidase; Reninangiotensin system; Signalling

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN II; ANGIOTENSIN[1-7]; MATRIX METALLOPROTEINASE; PROTEIN P47; PROTEIN P47PHOX; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA CONSTRICTION; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENZYME ACTIVATION; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GENE EXPRESSION; HEART FUNCTION; HEART MUSCLE; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; STRESS; SYSTOLE;

ANALYSIS OF VARIANCE; ANGIOTENSIN II; ANIMALS; BLOOD PRESSURE; CARDIOMYOPATHY, DILATED; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; HEART FAILURE; MALE; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIUM; NADPH OXIDASE; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PEPTIDYL-DIPEPTIDASE A; PHOSPHORYLATION; STRESS, MECHANICAL; SUPEROXIDES; TIME FACTORS; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 79958820082     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvr036     Document Type: Article

References (44)

1. Mazzolai L, Pedrazzini T, Nicoud F, Gabbiani G, Brunner HR, Nussberger J. Increased cardiac angiotensin II levels induce right and left ventricular hypertrophy in normotensive mice. Hypertension 2000;35:985-991. (Pubitemid 30303962)
2. Billet S, Bardin S, Verp S, Baudrie V, Michaud A, Conchon S et al. Gain-of-function mutant of angiotensin II receptor, type 1A, causes hypertension and cardiovascular fibrosis in mice. J Clin Invest 2007;117:1914-1925. (Pubitemid 47036325)
3. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 1994;74:1141-1148. (Pubitemid 24176909)
4. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 2000;86:494-501. (Pubitemid 30165039)
5. Landmesser U, Cai H, Dikalov S, McCann L, Hwang J, Jo H et al. Role of p47(phox) in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension 2002; 40:511-515.
6. Li JM, Shah AM. Mechanism of endothelial cell NADPH oxidase activation by angiotensin II. Role of the p47phox subunit. J Biol Chem 2003;278:12094-12100. (Pubitemid 36800187)
7. Li JM, Wheatcroft S, Fan LM, Kearney MT, Shah AM. Opposing roles of p47phox in basal versus angiotensin II-stimulated alterations in vascular O2- production, vascular tone, and mitogen-activated protein kinase activation. Circulation 2004;109: 1307-1313. (Pubitemid 38372791)
8. Mehta PK, Griendling KK. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 2007;292:C82-C97. (Pubitemid 46127306)
9. Li JM, Gall NP, Grieve DJ, Chen M, Shah AM. Activation of NADPH oxidase during progression of cardiac hypertrophy to failure. Hypertension 2002;40:477-484.
10. Heymes C, Bendall JK, Ratajczak P, Cave AC, Samuel JL, Hasenfuss G et al. Increased myocardial NADPH oxidase activity in human heart failure. J Am Coll Cardiol 2003;41: 2164-2171. (Pubitemid 36724261)
11. Griendling KK, FitzGerald GA. Oxidative stress and cardiovascular injury: Part II: animal and human studies. Circulation 2003;108:2034-2040. (Pubitemid 37337574)
12. Murdoch CE, Zhang M, Cave AC, Shah AM. NADPH oxidase-dependent redox signalling in cardiac hypertrophy, remodelling and failure. Cardiovasc Res 2006;71: 208-215.
13. Takimoto E, Kass DA. Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension 2007;49:241-248. (Pubitemid 46142995)
14. Imai Y, Kuba K, Rao S, Huan Y, Guo F, Guan B et al. Angiotensin- converting enzyme 2 protects from severe acute lung failure. Nature 2005;436:112-116. (Pubitemid 40966195)
15. Oudit GY, Herzenberg AM, Kassiri Z, Wong D, Reich H, Khokha R et al. Loss of angiotensin-converting enzyme-2 leads to the late development of angiotensin II-dependent glomerulosclerosis. Am J Pathol 2006;168:1808-1820. (Pubitemid 43825302)
16. Garabelli PJ, Modrall JG, Penninger JM, Ferrario CM, Chappell MC. Distinct roles for angiotensin-converting enzyme 2 and carboxypeptidase A in the processing of angiotensins within the murine heart. Exp Physiol 2008;93:613-621. (Pubitemid 351595064)
17. Wysocki J, Ye M, Rodriguez E, Gonzalez-Pacheco FR, Barrios C, Evora K et al. Targeting the degradation of angiotensin II with recombinant angiotensin-converting enzyme 2: prevention of angiotensin II-dependent hypertension. Hypertension 2009;55:90-98.
18. Oudit GY, Liu GC, Zhong J, Basu R, Chow FL, Zhou J et al. Human recombinant ACE2 reduces the progression of diabetic nephropathy. Diabetes 2010;59:529-538.
19. Zhong JC, Basu R, Guo D, Chow FL, Byrns S, Shuster M et al. Angiotensin converting enzyme 2 suppresses pathological hypertrophy, myocardial fibrosis and cardiac dysfunction. Circulation 2010;122:717-728.
20. Gallagher PE, Ferrario CM, Tallant EA. Regulation of ACE2 in cardiac myocytes and fibroblasts. Am J Physiol Heart Circ Physiol 2008;295:H2373-H2379.
21. Lovren F, Pan Y, Quan A, Teoh H, Wang G, Shukla PC et al. Angiotensin converting enzyme-2 confers endothelial protection and attenuates atherosclerosis. Am J Physiol Heart Circ Physiol 2008;295:H1377-H1384.
22. Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, Scanga SE et al. Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature 2002;417:822-828. (Pubitemid 34670323)
23. Oudit GY, Kassiri Z, Patel MP, Chappell M, Butany J, Backx PH et al. Angiotensin II-mediated oxidative stress and inflammation mediate the age-dependent cardiomyopathy in ACE2 null mice. Cardiovasc Res 2007;75:29-39. (Pubitemid 46873522)
24. Kassiri Z, Zhong J, Guo D, Basu R, Wang X, Liu PP et al. Loss of angiotensinconverting enzyme 2 accelerates maladaptive left ventricular remodeling in response to myocardial infarction. Circ Heart Fail 2009;2:446-455.
25. Kim MA, Yang D, Kida K, Molotkova N, Yeo SJ, Varki N et al. Effects of ACE2 inhibition in the post-myocardial infarction heart. J Card Fail 2010;16:777-785.
26. Yamamoto K, Ohishi M, Katsuya T, Ito N, Ikushima M, Kaibe M et al. Deletion of angiotensin-converting enzyme 2 accelerates pressure overload-induced cardiac dysfunction by increasing local angiotensin II. Hypertension 2006;47:718-726. (Pubitemid 43740244)
27. Epelman S, Tang WH, Chen SY, Van Lente F, Francis GS, Sen S. Detection of soluble angiotensin-converting enzyme 2 in heart failure: insights into the endogenous counter-regulatory pathway of the renin-angiotensin-aldosterone system. J Am Coll Cardiol 2008;52:750-754.
28. Epelman S, Shrestha K, Troughton RW, Francis GS, Sen S, Klein AL et al. Soluble angiotensin-converting enzyme 2 in human heart failure: relation with myocardial function and clinical outcomes. J Card Fail 2009;15:565-571.
29. Wang Y, Moreira Mda C, Heringer-Walther S, Ebermann L, Schultheiss HP,Wessel N et al. Plasma ACE2 activity is an independent prognostic marker in Chagas' disease and equally potent as BNP. J Card Fail 2010;16:157-163.
30. Doerries C, Grote K, Hilfiker-Kleiner D, Luchtefeld M, Schaefer A, Holland SM et al. Critical role of the NAD(P)H oxidase subunit p47phox for left ventricular remodeling/dysfunction and survival after myocardial infarction. Circ Res 2007;100:894-903. (Pubitemid 46555695)
31. Oudit GY, Kassiri Z, Zhou J, Liu QC, Liu PP, Backx PH et al. Loss of PTEN attenuates the development of pathological hypertrophy and heart failure in response to biomechanical stress. Cardiovasc Res 2008;78:505-514. (Pubitemid 351769769)
32. Kassiri Z, Oudit GY, Sanchez O, Dawood F, Mohammed FF, Nuttall RK et al. 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. (Pubitemid 41216143)
33. Rey FE, Cifuentes ME, Kiarash A, Quinn MT, Pagano PJ. Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O(2)(-) and systolic blood pressure in mice. Circ Res 2001;89:408-414. (Pubitemid 34132656)
34. Guo D, Kassiri Z, Basu R, Chow FL, Kandalam V, Damilano F et al. Loss of PI3Kg enhances cAMP-dependent MMP remodeling of the myocardial N-cadherin adhesion complexes and extracellular matrix in response to early biomechanical stress. Circ Res 2010;107:1275-1289.
35. Lin Q, Keller RS, Weaver B, Zisman LS. Interaction of ACE2 and integrin beta1 in failing human heart. Biochim Biophys Acta 2004;1689:175-178. (Pubitemid 38981593)
36. Loukogeorgakis SP, van den Berg MJ, Sofat R, Nitsch D, Charakida M, Haiyee B et al. Role of NADPH oxidase in endothelial ischemia/reperfusion injury in humans. Circulation 2010;121:2310-2316.
37. Mercure C, Yogi A, Callera GE, Aranha AB, Bader M, Ferreira AJ et al. Angiotensin(1-7) blunts hypertensive cardiac remodeling by a direct effect on the heart. Circ Res 2008; 103:1319-1326.
38. Tallant EA, Ferrario CM, Gallagher PE. Angiotensin-(1-7) inhibits growth of cardiac myocytes through activation of the mas receptor. Am J Physiol Heart Circ Physiol 2005;289:H1560-1566. (Pubitemid 41368998)
39. Ni W, Zhan Y, He H, Maynard E, Balschi JA, Oettgen P. Ets-1 is a critical transcriptional regulator of reactive oxygen species and p47(phox) gene expression in response to angiotensin II. Circ Res 2007;101:985-994. (Pubitemid 350084976)
40. Grote K, Flach I, Luchtefeld M, Akin E, Holland SM, Drexler H et al. Mechanical stretch enhances mRNA expression and proenzyme release of matrix metalloproteinase-2 (MMP-2) via NAD(P)H oxidase-derived reactive oxygen species. Circ Res 2003;92:e80-e86.
41. Luchtefeld M, Grote K, Grothusen C, Bley S, Bandlow N, Selle T et al. Angiotensin II induces MMP-2 in a p47phox-dependent manner. Biochem Biophys Res Commun 2005; 328:183-188. (Pubitemid 40164653)
42. Thomas M, Gavrila D, McCormick ML, Miller FJ Jr, Daugherty A, Cassis LA et al. Deletion of p47phox attenuates angiotensin II-induced abdominal aortic aneurysm formation in apolipoprotein E-deficient mice. Circulation 2006;114:404-413. (Pubitemid 44264822)
43. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003;92:827-839. (Pubitemid 36542523)
44. Rajagopalan S, Meng XP, Ramasamy S, Harrison DG, Galis ZS. Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J Clin Invest 1996;98:2572-2579. (Pubitemid 26415078)