Heme oxygenase-1 induction protects the heart and modulates cellular and extracellular remodelling after myocardial infarction in rats

Experimental Biology and Medicine

Volumn 236, Issue 12, 2011, Pages 1437-1448

  Lakkisto, Päivi ^a,b,c   Siren, Juha Matti ^c   Kytö, Ville ^d   Forsten, Hanna ^c   Laine, Mika ^a,c   Pulkki, Kari ^e   Tikkanen, Ilkka ^a,c  

^a HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c MINERVA FOUNDATION INSTITUTE FOR MEDICAL RESEARCH   (Finland)

^d TURKU UNIVERSITY HOSPITAL   (Finland)

^e UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Cardiac fibrosis; Cardiomyocyte apoptosis; Cardiomyocyte proliferation; Heme oxygenase 1; Myocardial infarction

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; CYCLINE; HEME OXYGENASE 1; KI 67 ANTIGEN; PROCOLLAGEN; PROCOLLAGEN TYPE 1; PROTOPORPHYRIN COBALT; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ACUTE HEART INFARCTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL REGENERATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; HEART FAILURE; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART PROTECTION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT;

ANIMALS; APOPTOSIS; CARDIOTONIC AGENTS; CELL PROLIFERATION; COLLAGEN; ENZYME INDUCTION; FIBRONECTINS; HEME OXYGENASE-1; MALE; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; PROTOPORPHYRINS; RATS; RATS, WISTAR; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA1; VIMENTIN;

EID: 82755179957     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1258/ebm.2011.011148     Document Type: Article

References (55)

1. Maines MD. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 1988;2:2557-68
2. Otterbein LE, Soares MP, Yamashita K, Bach FH. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 2003;24:449-55
3. Otterbein LE, Choi AM. Heme oxygenase: colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol 2000;279:L1029-37
4. Gozzelino R, Jeney V, Soares MP. Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol 2010;50:323-54
5. Idriss NK, Blann AD, Lip GY. Hemoxygenase-1 in cardiovascular disease. J Am Coll Cardiol 2008;52:971-8
6. Peterson SJ, Frishman WH, Abraham NG. Targeting heme oxygenase: therapeutic implications for diseases of the cardiovascular system. Cardiol Rev 2009;17:99-111
7. Dulak J, Deshane J, Jozkowicz A, Agarwal A. Heme oxygenase-1 and carbon monoxide in vascular pathobiology: focus on angiogenesis. Circulation 2008;117:231-41
8. Lakkisto P, Kyto V, Forsten H, Siren JM, Segersvard H, Voipio-Pulkki LM, Laine M, Pulkki K, Tikkanen I. Heme oxygenase-1 and carbon monoxide promote neovascularization after myocardial infarction by modulating the expression of HIF-1alpha, SDF-1alpha and VEGF-B. Eur J Pharmacol 2010;635:156-64
9. Foo RS, Siow RC, Brown MJ, Bennett MR. Heme oxygenase-1 gene transfer inhibits angiotensin II-mediated rat cardiac myocyte apoptosis but not hypertrophy. J Cell Physiol 2006;209:1-7
10. Pachori AS, Melo LG, Zhang L, Solomon SD, Dzau VJ. Chronic recurrent myocardial ischemic injury is significantly attenuated by pre-emptive adeno-associated virus heme oxygenase-1 gene delivery. J Am Coll Cardiol 2006;47:635-43
11. Ndisang JF, Jadhav A. Upregulating the heme oxygenase system suppresses left ventricular hypertrophy in adult spontaneously hypertensive rats for 3 months. J Card Fail 2009;15:616-28
12. Duckers HJ, Boehm M, True AL, Yet SF, San H, Park JL, Clinton Webb R, Lee ME, Nabel GJ, Nabel EG. Heme oxygenase-1 protects against vascular constriction and proliferation. Nat Med 2001;7:693-8
13. Zhou Z, Song R, Fattman CL, Greenhill S, Alber S, Oury TD, Choi AM, Morse D. Carbon monoxide suppresses bleomycin-induced lung fibrosis. Am J Pathol 2005;166:27-37
14. Liu X, Pachori AS, Ward CA, Davis JP, Gnecchi M, Kong D, Zhang L, Murduck J, Yet SF, Perrella MA, Pratt RE, Dzau VJ, Melo LG. Heme oxygenase-1 (HO-1) inhibits postmyocardial infarct remodelling and restores ventricular function. FASEB J 2006;20:207-16
15. Wegiel B, Chin BY, Otterbein LE. Inhale to survive, cycle or die? Carbon monoxide and cellular proliferation. Cell Cycle 2008;7:1379-84
16. Li Volti G, Wang J, Traganos F, Kappas A, Abraham NG. Differential effect of heme oxygenase-1 in endothelial and smooth muscle cell cycle progression. Biochem Biophys Res Commun 2002;296:1077-82
17. Pfeffer MA, Pfeffer JM, Fishbein MC, Fletcher PJ, Spadaro J, Kloner RA, Braunwald E. Myocardial infarct size and ventricular function in rats. Circ Res 1979;44:503-12
18. Saraste A, Pulkki K, Kallajoki M, Henriksen K, Parvinen M, Voipio-Pulkki LM. Apoptosis in human acute myocardial infarction. Circulation 1997;95:320-3
19. Lakkisto P, Palojoki E, Backlund T, Saraste A, Tikkanen I, Voipio-Pulkki LM, Pulkki K. Expression of heme oxygenase-1 in response to myocardial infarction in rats. J Mol Cell Cardiol 2002;34:1357-65
20. Amersi F, Buelow R, Kato H, Ke B, Coito AJ, Shen XD, Zhao D, Zaky J, Melinek J, Lassman CR, Kolls JK, Alam J, Ritter T, Volk HD, Farmer DG, Ghobrial RM, Busuttil RW, Kupiec-Weglinski JW. Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/ reperfusion injury. J Clin Invest 1999;104:1631-9
21. Peyton KJ, Reyna SV, Chapman GB, Ensenat D, Liu XM, Wang H, Schafer AI, Durante W. Heme oxygenase-1-derived carbon monoxide is an autocrine inhibitor of vascular smooth muscle cell growth. Blood 2002;99:4443-8
22. Song R, Mahidhara RS, Liu F, Ning W, Otterbein LE, Choi AM. Carbon monoxide inhibits human airway smooth muscle cell proliferation via mitogen-activated protein kinase pathway. Am J Respir Cell Mol Biol 2002;27:603-10
23. Schwer CI, Mutschler M, Stoll P, Goebel U, Humar M, Hoetzel A, Schmidt R. Carbon monoxide releasing molecule-2 inhibits pancreatic stellate cell proliferation by activating p38 mitogen-activated protein kinase/heme oxygenase-1 signaling. Mol Pharmacol 2010;77:660-9
24. Chen X, Wilson RM, Kubo H, Berretta RM, Harris DM, Zhang X, Jaleel N, MacDonnell SM, Bearzi C, Tillmanns J, Trofimova I, Hosoda T, Mosna F, Cribbs L, Leri A, Kajstura J, Anversa P, Houser SR. Adolescent feline heart contains a population of small, proliferative ventricular myocytes with immature physiological properties. Circ Res 2007;100:536-44
25. Beltrami AP, Urbanek K, Kajstura J, Yan SM, Finato N, Bussani R, Nadal-Ginard B, Silvestri F, Leri A, Beltrami CA, Anversa P. Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med 2001;344:1750-7
26. Yuasa S, Fukuda K, Tomita Y, Fujita J, Ieda M, Tahara S, Itabashi Y, Yagi T, Kawaguchi H, Hisaka Y, Ogawa S. Cardiomyocytes undergo cells division following myocardial infarction is a spatially and temporally restricted event in rats. Mol Cell Biochem 2004;259:177-81
27. Clark JE, Foresti R, Sarathchandra P, Kaur H, Green CJ, Motterlini R. Heme oxygenase-1-derived bilirubin ameliorates postischemic myocardial dysfunction. Am J Physiol Heart Circ Physiol 2000;278:H643-51
28. Savio M, Stivala LA, Bianchi L, Vannini V, Prosperi E. Involvement of the proliferating cell nuclear antigen (PCNA) in DNA repair induced by alkylating agents and oxidative damage in human fibroblasts. Carcinogenesis 1998;19:591-6
29. Sawhney N, Hall PA. Ki67 - structure, function, and new antibodies. J Pathol 1992;168:161-2
30. Bartunek J, Vanderheyden M, Knaapen MW, Tack W, Kockx MM, Goethals M. Deoxyribonucleic acid damage/repair proteins are elevated in the failing human myocardium due to idiopathic dilated cardiomyopathy. J Am Coll Cardiol 2002;40:1097-103
31. Francis GS, Anwar F, Bank AJ, Kubo SH, Jessurun J. Apoptosis, Bcl-2, and proliferating cell nuclear antigen in the failing human heart: observations made after implantation of left ventricular assist device. J Card Fail 1999;5:308-15
32. Vulapalli SR, Chen Z, Chua BH, Wang T, Liang CS. Cardioselective overexpression of HO-1 prevents I/R-induced cardiac dysfunction and apoptosis. Am J Physiol Heart Circ Physiol 2002;283:H688-94
33. Katori M, Buelow R, Ke B, Ma J, Coito AJ, Iyer S, Southard D, Busuttil RW, Kupiec-Weglinski JW. Heme oxygenase-1 overexpression protects rat hearts from cold ischemia/reperfusion injury via an antiapoptotic pathway. Transplantation 2002;73:287-92
34. Banerjee I, Fuseler JW, Price RL, Borg TK, Baudino TA. Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am J Physiol Heart Circ Physiol 2007;293:H1883-91
35. Porter KE, Turner NA. Cardiac fibroblasts: at the heart of myocardial remodelling. Pharmacol Ther 2009;123:255-78
36. Sun Y, Weber KT. Infarct scar: a dynamic tissue. Cardiovasc Res 2000;46:250-6
37. Gaedeke J, Noble NA, Border WA. Curcumin blocks fibrosis in anti-Thy 1 glomerulonephritis through up-regulation of heme oxygenase 1. Kidney Int 2005;68:2042-9
38. Tsui TY, Lau CK, Ma J, Wu X, Wang YQ, Farkas S, Xu R, Schlitt HJ, Fan ST. rAAV-mediated stable expression of heme oxygenase-1 in stellate cells: a new approach to attenuate liver fibrosis in rats. Hepatology 2005;42:335-42
39. Tsuburai T, Suzuki M, Nagashima Y, Suzuki S, Inoue S, Hasiba T, Ueda A, Ikehara K, Matsuse T, Ishigatsubo Y. Adenovirus-mediated transfer and overexpression of heme oxygenase 1 cDNA in lung prevents bleomycin-induced pulmonary fibrosis via a Fas-Fas ligand-independent pathway. Hum Gene Ther 2002;13:1945-60
40. Backlund T, Palojoki E, Saraste A, Eriksson A, Finckenberg P, Kyto V, Lakkisto P, Mervaala E, Voipio-Pulkki LM, Laine M, Tikkanen I. Sustained cardiomyocyte apoptosis and left ventricular remodelling after myocardial infarction in experimental diabetes. Diabetologia 2004;47:325-30
41. Bujak M, Frangogiannis NG. The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc Res 2007;74:184-95
42. Frangogiannis NG, Ren G, Dewald O, Zymek P, Haudek S, Koerting A, Winkelmann K, Michael LH, Lawler J, Entman ML. Critical role of endogenous thrombospondin-1 in preventing expansion of healing myocardial infarcts. Circulation 2005;111:2935-42
43. Xia ZW, Xu LQ, Zhong WW, Wei JJ, Li NL, Shao J, Li YZ, Yu SC, Zhang ZL. Heme oxygenase-1 attenuates ovalbumin-induced airway inflammation by up-regulation of foxp3T-regulatory cells, interleukin-10, and membrane-bound transforming growth factor- 1. Am J Pathol 2007;171:1904-14
44. Jadhav A, Ndisang JF. Heme arginate suppresses cardiac lesions and hypertrophy in deoxycorticosterone acetate-salt hypertension. Exp Biol Med (Maywood) 2009;234:764-78
45. Nishikimi T, Maeda N, Matsuoka H. The role of natriuretic peptides in cardioprotection. Cardiovasc Res 2006;69:318-28
46. Vollmar AM. The role of atrial natriuretic peptide in the immune system. Peptides 2005;26:1086-94
47. Houng AK, McNamee RA, Kerner A, Sharma P, Mohamad A, Tronolone J, Reed GL. Atrial natriuretic peptide increases inflammation, infarct size, and mortality after experimental coronary occlusion. Am J Physiol Heart Circ Physiol 2009;296:H655-61
48. Kiemer AK, Bildner N, Weber NC, Vollmar AM. Characterization of heme oxygenase 1 (heat shock protein 32) induction by atrial natriuretic peptide in human endothelial cells. Endocrinology 2003;144:802-12
49. Kiemer AK, Gerwig T, Gerbes AL, Meissner H, Bilzer M, Vollmar AM. Kupffer-cell specific induction of heme oxygenase 1 (hsp32) by the atrial natriuretic peptide - role of cGMP. J Hepatol 2003;38:490-8
50. Mito S, Ozono R, Oshima T, Yano Y, Watari Y, Yamamoto Y, Brydun A, Igarashi K, Yoshizumi M. Myocardial protection against pressure overload in mice lacking Bach1, a transcriptional repressor of heme oxygenase-1. Hypertension 2008;51:1570-7
51. Wang G, Hamid T, Keith RJ, Zhou G, Partridge CR, Xiang X, Kingery JR, Lewis RK, Li Q, Rokosh DG, Ford R, Spinale FG, Riggs DW, Srivastava S, Bhatnagar A, Bolli R, Prabhu SD. Cardioprotective and antiapoptotic effects of heme oxygenase-1 in the failing heart. Circulation 2010;121:1912-25
52. Ahmad M, Turkseven S, Mingone CJ, Gupte SA, Wolin MS, Abraham NG. Heme oxygenase-1 gene expression increases vascular relaxation and decreases inducible nitric oxide synthase in diabetic rats. Cell Mol Biol (Noisy-Le-Grand) 2005;51:371-6
53. Haider A, Olszanecki R, Gryglewski R, Schwartzman ML, Lianos E, Kappas A, Nasjletti A, Abraham NG. Regulation of cyclooxygenase by the heme-heme oxygenase system in microvessel endothelial cells. J Pharmacol Exp Ther 2002;300:188-94
54. Srisook K, Han SS, Choi HS, Li MH, Ueda H, Kim C, Cha YN. CO from enhanced HO activity or from CORM-2 inhibits both O2- and NO production and downregulates HO-1 expression in LPS-stimulated macrophages. Biochem Pharmacol 2006;71:307-18
55. Taille C, El-Benna J, Lanone S, Dang MC, Ogier-Denis E, Aubier M, Boczkowski J. Induction of heme oxygenase-1 inhibits NAD(P)H oxidase activity by down-regulating cytochrome b558 expression via the reduction of heme availability. J Biol Chem 2004;279:28681-8