Cardiac protective effects of irbesartan via the PPAR-gamma signaling pathway in angiotensin-converting enzyme 2-deficient mice

Journal of Translational Medicine

Volumn 11, Issue 1, 2013, Pages

  Zhang, Zhen Zhou ^a,b   Shang, Qian Hui ^c   Jin, Hai Yan ^a   Song, Bei ^a,b   Oudit, Gavin Y ^d   Lu, Lin ^a   Zhou, Tong ^a   Xu, Ying Le ^a,b   Gao, Ping Jin ^a,b   Zhu, Ding Liang ^a,b   Penninger, Josef M ^e   Zhong, Jiu Chang ^a,b  

^a SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

^b Shanghai Institute of Hypertension   (China)

^c ZUNYI MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF ALBERTA   (Canada)

^e INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

Author keywords

Angiotensin converting enzyme 2; Connective tissue growth factor; Irbesartan; Myocardial injury; Peroxisome proliferator activated receptor

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN[1-7]; ATRIAL NATRIURETIC FACTOR; COLLAGEN TYPE 1; COLLAGEN TYPE 3; CONNECTIVE TISSUE GROWTH FACTOR; FIBRONECTIN; IRBESARTAN; MITOGEN ACTIVATED PROTEIN KINASE 1; MYOSIN HEAVY CHAIN BETA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2;

ANIMAL EXPERIMENT; ARTICLE; COLLAGEN VOLUME FRACTION; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE REPRESSION; HEART FUNCTION; HEART INJURY; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; KNOCKOUT MOUSE; MALE; MORPHOMETRICS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAINING; TRANSMISSION ELECTRON MICROSCOPY; TREATMENT RESPONSE; WESTERN BLOTTING; WILD TYPE;

ANGIOTENSIN I; ANGIOTENSIN II; ANIMALS; BIPHENYL COMPOUNDS; CARDIOMEGALY; CARDIOTONIC AGENTS; COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROSIS; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIUM; PEPTIDE FRAGMENTS; PEPTIDYL-DIPEPTIDASE A; PHOSPHORYLATION; PPAR ALPHA; PPAR DELTA; PPAR GAMMA; RECEPTOR, ANGIOTENSIN, TYPE 1; RNA, MESSENGER; SIGNAL TRANSDUCTION; TETRAZOLES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84884522353     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-11-229     Document Type: Article

References (29)

1. Wang M, Zhang J, Walker SJ, Dworakowski R, Lakatta EG, Shah AM. Involvement of NADPH oxidase in age-associated cardiac remodeling. J Mol Cell Cardiol 2010, 48:765-772. 10.1016/j.yjmcc.2010.01.006, 2877878, 20079746.
2. 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. 10.1161/CIRCULATIONAHA.110.955369, 20679547.
3. Zhong JC, Ye JY, Jin HY, Yu X, Yu HM, Zhu DL, Gao PJ, Huang DY, Shuster M, Loibner H, Guo JM, Yu XY, Xiao BX, Gong ZH, Penninger JM, Oudit GY. Telmisartan attenuates aortic hypertrophy in hypertensive rats by the modulation of ACE2 and profilin-1 expression. Regul Pept 2011, 166:90-97. 10.1016/j.regpep.2010.09.005, 20854846.
4. Zhang HF, Xie SL, Chen YX, Mai JT, Wang JF, Zhu WL, Zhu LG. Altered serum levels of IL-33 in patients with advanced systolic chronic heart failure: correlation with oxidative stress. J Transl Med 2012, 10:120. 10.1186/1479-5876-10-120, 3514300, 22682001.
5. Ebrahimian T, Li MW, Lemarié CA, Simeone SM, Pagano PJ, Gaestel M, Paradis P, Wassmann S, Schiffrin EL. Mitogen-activated protein kinase-activated protein kinase 2 in angiotensin II-induced inflammation and hypertension: regulation of oxidative stress. Hypertension 2011, 57:245-254. 10.1161/HYPERTENSIONAHA.110.159889, 21173344.
6. Wu SH, Lu C, Dong L, Chen ZQ. Signal transduction involved in CTGF-induced production of chemokines in mesangial cells. Growth Factors 2008, 26:192-200. 10.1080/08977190802227828, 19378419.
7. Iwai M, Nakaoka H, Senba I, Kanno H, Moritani T, Horiuchi M. Possible involvement of angiotensin-converting enzyme 2 and Mas activation in inhibitory effects of angiotensin II Type 1 receptor blockade on vascular remodeling. Hypertension 2012, 60:137-144. 10.1161/HYPERTENSIONAHA.112.191452, 22665126.
8. Moritani T, Iwai M, Kanno H, Nakaoka H, Iwanami J, Higaki T, Ishii E, Horiuchi M. ACE2 deficiency induced perivascular fibrosis and cardiac hypertrophy during postnatal development in mice. J Am Soc Hypert 2013, 7:259-266.
9. Jin HY, Song B, Oudit GY, Davidge ST, Yu HM, Jiang YY, Gao PJ, Zhu DL, Ning G, Kassiri Z, Penninger JM, Zhong JC. ACE2 deficiency enhances angiotensin II-mediated aortic profilin-1 expression, inflammation and peroxynitrite production. PLoS One 2012, 7:e38502. 10.1371/journal.pone.0038502, 3367919, 22693641.
10. Patel VB, Bodiga S, Fan D, Das SK, Wang Z, Wang W, Basu R, Zhong J, Kassiri Z, Oudit GY. Cardioprotective effects mediated by angiotensin II type 1 receptor blockade and enhancing angiotensin 1-7 in experimental heart failure in angiotensin-converting enzyme 2-null mice. Hypertension 2012, 59:1195-1203. 10.1161/HYPERTENSIONAHA.112.191650, 22508831.
11. Zhong JC, Huang DY, Yang YM, Li YF, Liu GF, Song XH, Du K. Upregulation of angiotensin-converting enzyme 2 by all-trans retinoic acid in spontaneously hypertensive rats. Hypertension 2004, 44:907-912. 10.1161/01.HYP.0000146400.57221.74, 15477383.
12. 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. 10.1161/HYPERTENSIONAHA.110.164244, 21189404.
13. Kusunoki H, Taniyama Y, Rakugi H, Morishita R. Cardiac and renal protective effects of irbesartan via peroxisome proliferator-activated receptorγ-hepatocyte growth factor pathway independent of angiotensin II Type 1a receptor blockade in mouse model of salt-sensitive hypertension. J Am Heart Assoc 2013, 2:e000103. 10.1161/JAHA.113.000103, 3647265, 23608606.
14. Drosatos K, Khan RS, Trent CM, Jiang H, Son NH, Blaner WS, Homma S, Schulze PC, Goldberg IJ. Peroxisome proliferator-activated receptor-γ activation prevents sepsis-related cardiac dysfunction and mortality in mice. Circ Heart Fail 2013, 6:550-562. 10.1161/CIRCHEARTFAILURE.112.000177, 23572494.
15. Koh EJ, Yoon SJ, Lee SM. Losartan protects liver against ischaemia/reperfusion injury through PPAR-γ activation and receptor for advanced glycation end-products down-regulation. Br J Pharmacol 2013, 169:1404-1416. 10.1111/bph.12229, 23647130.
16. Lee SW, Won JY, Kim WJ, Lee J, Kim KH, Youn SW, Kim JY, Lee EJ, Kim YJ, Kim KW, Kim HS. Snail as a potential target molecule in cardiac fibrosis: paracrine action of endothelial cells on fibroblasts through snail and CTGF axis. Mol Ther 2013, 10.1038/mt.2013.146. Epub ahead of print.
17. Kassiri Z, Zhong J, Guo D, Basu R, Wang X, Liu PP, Scholey JW, Penninger JM, Oudit GY. Loss of angiotensin-converting enzyme 2 accelerates maladaptive left ventricular remodeling in response to myocardial infarction. Circ Heart Fail 2009, 2:446-455. 10.1161/CIRCHEARTFAILURE.108.840124, 19808375.
18. Bodiga S, Zhong JC, Wang W, Basu R, Lo J, Liu GC, Guo D, Holland SM, Scholey JW, Penninger JM, Kassiri Z, Oudit GY. Enhanced susceptibility to biomechanical stress in ACE2 null mice is prevented by loss of the p47(phox) NADPH oxidase subunit. Cardiovasc Res 2011, 91:151-161. 10.1093/cvr/cvr036, 3151662, 21285291.
19. Cai M, Wu J, Mao C, Ren J, Li P, Li X, Zhong J, Xu C, Zhou T. A Lectin-EGF antibody promotes regulatory T cells and attenuates nephrotoxic nephritis via DC-SIGN on dendritic cells. J Transl Med 2013, 11:103. 10.1186/1479-5876-11-103, 3651349, 23627732.
20. Song B, Jin H, Yu X, Zhang Z, Yu H, Ye J, Xu Y, Zhou T, Oudit GY, Ye JY, Chen C, Gao P, Zhu D, Penninger JM, Zhong JC. Angiotensin-converting enzyme 2 attenuates oxidative stress and VSMC proliferation via the JAK2/STAT3/SOCS3 and profilin-1/MAPK signaling pathways. Regul Pept 2013, 185:44-51. 10.1016/j.regpep.2013. 06.007. Epub ahead of print.
21. Ares-Carrasco S, Picatoste B, Camafeita E, Carrasco-Navarro S, Zubiri I, Ortiz A, Egido J, López JA, Tuñón J, Lorenzo O. Proteome changes in the myocardium of experimental chronic diabetes and hypertension: role of PPARα in the associated hypertrophy. J Proteomics 2012, 75:1816-1829. 10.1016/j.jprot.2011.12.023, 22234359.
22. Asakawa M, Takano H, Nagai T, Uozumi H, Hasegawa H, Kubota N, Saito T, Masuda Y, Kadowaki T, Komuro I. Peroxisome proliferator-activated receptor gamma plays a critical role in inhibition of cardiac hypertrophy in vitro and in vivo. Circulation 2002, 105:1240-1246. 10.1161/hc1002.105225, 11889020.
23. Kis A, Murdoch C, Zhang M, Siva A, Rodriguez-Cuenca S, Carobbio S, Lukasik A, Blount M, O'Rahilly S, Gray SL, Shah AM, Vidal-Puig A. Defective peroxisomal proliferators activated receptor gamma activity due to dominant-negative mutation synergizes with hypertension to accelerate cardiac fibrosis in mice. Eur J Heart Fail 2009, 11:533-541. 10.1093/eurjhf/hfp048, 2686026, 19395708.
24. Hashimoto T, Perlot T, Rehman A, Trichereau J, Ishiguro H, Paolino M, Sigl V, Hanada T, Hanada R, Lipinski S, Wild B, Camargo SM, Singer D, Richter A, Kuba K, Fukamizu A, Schreiber S, Clevers H, Verrey F, Rosenstiel P, Penninger JM. ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation. Nature 2012, 487:477-481. 10.1038/nature11228, 22837003.
25. Zhong JC, Yu XY, Lin QX, Li XH, Huang XZ, Xiao DZ, Lin SG. Enhanced angiotensin converting enzyme 2 regulates the insulin/Akt signalling pathway by blockade of macrophage migration inhibitory factor expression. Br J Pharmacol 2008, 153:66-74. 10.1038/sj.bjp.0707482, 2199394, 17906677.
26. Kuba K, Imai Y, Penninger JM. Multiple functions of angiotensin-converting enzyme 2 and its relevance in cardiovascular diseases. Circ J 2013, 77:301-308. 10.1253/circj.CJ-12-1544, 23328447.
27. Ko WC, Hong CY, Hou SM, Lin CH, Ong ET, Lee CF, Tsai CT, Lai LP. Elevated expression of connective tissue growth factor in human atrial fibrillation and angiotensin II-treated cardiomyocytes. Circ J 2011, 75:1592-1600. 10.1253/circj.CJ-10-0892, 21576830.
28. Leask A. Potential therapeutic targets for cardiac fibrosis: TGFbeta, angiotensin, endothelin, CCN2, and PDGF, partners in fibroblast activation. Circ Res 2010, 106:1675-1680. 10.1161/CIRCRESAHA.110.217737, 20538689.
29. Morrow JP, Katchman A, Son NH, Trent CM, Khan R, Shiomi T, Huang H, Amin V, Lader JM, Vasquez C, Morley GE, D'Armiento J, Homma S, Goldberg IJ, Marx SO. Mice with cardiac overexpression of peroxisome proliferator-activated receptor γ have impaired repolarization and spontaneous fatal ventricular arrhythmias. Circulation 2011, 124:2812-2821. 10.1161/CIRCULATIONAHA.111.056309, 3258098, 22124376.