Heme Oxygenase-1 Prevents Cardiac Dysfunction in Streptozotocin-Diabetic Mice by Reducing Inflammation, Oxidative Stress, Apoptosis and Enhancing Autophagy

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Zhao, Yanli ^a,b   Zhang, Lina ^a,c   Qiao, Yu ^a   Zhou, Xiaoling ^a   Wu, Guodong ^a   Wang, Lujing ^a   Peng, Yahui ^a   Dong, Xingli ^a   Huang, Hui ^a   Si, Lining ^b   Zhang, Xueying ^a   Zhang, Lei ^a   Li, Jihong ^a   Wang, Wei ^a   Zhou, Lingyun ^a   Gao, Xu ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b QINGHAI UNIVERSITY   (China)

^c DAQING OILFIELD CO LTD   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HEME OXYGENASE 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MUTANT PROTEIN; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DIABETES MELLITUS; DIABETOGENESIS; DISEASE MARKER; DISEASE SEVERITY; ECHOCARDIOGRAPHY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; HEART LEFT VENTRICLE FAILURE; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CELL; HO 1 GENE; INFLAMMATION; MOUSE; MUSCLE FIBRIL; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; STREPTOZOCIN DIABETES;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; DNA PRIMERS; ECHOCARDIOGRAPHY; GENE EXPRESSION REGULATION; HEART DISEASES; HEME OXYGENASE-1; MICE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STREPTOZOCIN; VENTRICULAR FUNCTION, LEFT;

EID: 84884562299     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075927     Document Type: Article

References (73)

1. King H, Aubert RE, Herman WH, (1998) Global burden of diabetes, 1995-2025: prevalence, numerical estimates, and projections. Diabetes Care 21: 1414-1431. doi:10.2337/diacare.21.9.1414. PubMed: 9727886.
2. Boudina S, Abel ED, (2007) Diabetic cardiomyopathy revisited. Circulation 115: 3213-3223. doi:10.1161/CIRCULATIONAHA.106.679597. PubMed: 17592090.
3. Pereira L, Matthes J, Schuster I, Valdivia HH, Herzig S, et al. (2006) Mechanisms of [Ca2+]i transient decrease in cardiomyopathy of db/db type 2 diabetic mice. Diabetes 55: 608-615. doi:10.2337/diabetes.55.03.06.db05-1284. PubMed: 16505222.
4. Lacombe VA, Viatchenko-Karpinski S, Terentyev D, Sridhar A, Emani S, et al. (2007) Mechanisms of impaired calcium handling underlying subclinical diastolic dysfunction in diabetes. Am J Physiol Regul Integr Comp Physiol 293: R1787-R1797. doi:10.1152/ajpregu.00059.2007. PubMed: 17761517.
5. Gallego M, Alday A, Urrutia J, Casis O, (2009) Transient outward potassium channel regulation in healthy and diabetic hearts. Can J Physiol Pharmacol 87: 77-83. doi:10.1139/Y08-106. PubMed: 19234570.
6. Huynh K, Kiriazis H, Du XJ, Love JE, Gray SP, et al. (2013) Targeting the upregulation of reactive oxygen species subsequent to hyperglycemia prevents type 1 diabetic cardiomyopathy in mice. Free Radic Biol Med 60C: 307-317. PubMed: 23454064.
7. Yu W, Wu J, Cai F, Xiang J, Zha W, et al. (2012) Curcumin alleviates diabetic cardiomyopathy in experimental diabetic rats. PLOS ONE 7: e52013. doi:10.1371/journal.pone.0052013. PubMed: 23251674.
8. Selvaraju V, Joshi M, Suresh S, Sanchez JA, Maulik N, et al. (2012) Diabetes, oxidative stress, molecular mechanism, and cardiovascular disease--an overview. Toxicol Mech Methods 22: 330-335. doi:10.3109/15376516.2012.666648. PubMed: 22394340.
9. Yu XY, Chen HM, Liang JL, Lin QX, Tan HH, et al. (2011) Hyperglycemic myocardial damage is mediated by proinflammatory cytokine: macrophage migration inhibitory factor. PLOS ONE 6: e16239. doi:10.1371/journal.pone.0016239. PubMed: 21283592.
10. Schilling JD, Machkovech HM, Kim AH, Schwendener R, Schaffer JE, (2012) Macrophages modulate cardiac function in lipotoxic cardiomyopathy. Am J Physiol Heart Circ Physiol 303: H1366-H1373. doi:10.1152/ajpheart.00111.2012. PubMed: 23042950.
11. El-Remessy AB, Rajesh M, Mukhopadhyay P, Horváth B, Patel V, et al. (2011) Cannabinoid 1 receptor activation contributes to vascular inflammation and cell death in a mouse model of diabetic retinopathy and a human retinal cell line. Diabetologia 54: 1567-1578. doi:10.1007/s00125-011-2061-4. PubMed: 21373835.
12. Delucchi F, Berni R, Frati C, Cavalli S, Graiani G, et al. (2012) Resveratrol treatment reduces cardiac progenitor cell dysfunction and prevents morpho-functional ventricular remodeling in type-1 diabetic rats. PLOS ONE 7: e39836. doi:10.1371/journal.pone.0039836. PubMed: 22768138.
13. Xie Z, Lau K, Eby B, Lozano P, He C, et al. (2011) Improvement of cardiac functions by chronic metformin treatment is associated with enhanced cardiac autophagy in diabetic OVE26 mice. Diabetes 60: 1770-1778. doi:10.2337/db10-0351. PubMed: 21562078.
14. He C, Zhu H, Li H, Zou MH, Xie Z, (2013) Dissociation of Bcl-2-Beclin1 Complex by Activated AMPK Enhances Cardiac Autophagy and Protects Against Cardiomyocyte Apoptosis in Diabetes. Diabetes 62: 1270-1281. doi:10.2337/db12-0533. PubMed: 23223177.
15. Zou MH, Xie Z, (2013) Regulation of interplay between autophagy and apoptosis in the diabetic heart: New role of AMPK. Autophagy 9: 624-625. doi:10.4161/auto.23577. PubMed: 23380689.
16. Bodiga VL, Eda SR, Bodiga S, (2013) Advanced glycation end products: role in pathology of diabetic cardiomyopathy. Heart Fail Rev. PubMed: 23404649.
17. Hofmann Bowman MA, Fedson S, Schmidt AM, (2011) Advanced glycation end products in diabetic cardiomyopathy: an alternative hypothesis. J Heart Lung Transplant 30: 1303; discussion 1303-1304 doi:10.1016/j.healun.2011.07.011. PubMed: 21723747.
18. Watanabe K, Thandavarayan RA, Harima M, Sari FR, Gurusamy N, et al. (2010) Role of differential signaling pathways and oxidative stress in diabetic cardiomyopathy. Curr Cardiol. Rev 6: 280-290.
19. Fang ZY, Prins JB, Marwick TH, (2004) Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev 25: 543-567. doi:10.1210/er.2003-0012. PubMed: 15294881.
20. Bao W, Song F, Li X, Rong S, Yang W, et al. (2010) Plasma heme oxygenase-1 concentration is elevated in individuals with type 2 diabetes mellitus. PLOS ONE 5: e12371. doi:10.1371/journal.pone.0012371. PubMed: 20811623.
21. Avogaro A, Pagnin E, Calò L, (2003) Monocyte NADPH oxidase subunit p22(phox) and inducible hemeoxygenase-1 gene expressions are increased in type II diabetic patients: relationship with oxidative stress. J Clin Endocrinol Metab 88: 1753-1759. doi:10.1210/jc.2002-021025. PubMed: 12679469.
22. Maines MD, (1988) Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 2: 2557-2568. PubMed: 3290025.
23. Ryter SW, Alam J, Choi AM, (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86: 583-650. doi:10.1152/physrev.00011.2005. PubMed: 16601269.
24. Abraham NG, Kushida T, McClung J, Weiss M, Quan S, et al. (2003) Heme oxygenase-1 attenuates glucose-mediated cell growth arrest and apoptosis in human microvessel endothelial cells. Circ Res 93: 507-514. doi:10.1161/01.RES.0000091828.36599.34. PubMed: 12933701.
25. Abraham NG, Rezzani R, Rodella L, Kruger A, Taller D, et al. (2004) Overexpression of human heme oxygenase-1 attenuates endothelial cell sloughing in experimental diabetes. Am J Physiol Heart Circ Physiol 287: H2468-H2477. doi:10.1152/ajpheart.01187.2003. PubMed: 15284058.
26. Cao J, Vecoli C, Neglia D, Tavazzi B, Lazzarino G, et al. (2012) Cobalt-Protoporphyrin Improves Heart Function by Blunting Oxidative Stress and Restoring NO Synthase Equilibrium in an Animal Model of Experimental Diabetes. Front. Physiol (Bethesda Md.) 3: 160.
27. Chen S, Khan ZA, Barbin Y, Chakrabarti S, (2004) Pro-oxidant role of heme oxygenase in mediating glucose-induced endothelial cell damage. Free Radic Res 38: 1301-1310. doi:10.1080/10715760400017228. PubMed: 15763954.
28. Farhangkhoee H, Khan ZA, Mukherjee S, Cukiernik M, Barbin YP, et al. (2003) Heme oxygenase in diabetes-induced oxidative stress in the heart. J Mol Cell Cardiol 35: 1439-1448. doi:10.1016/j.yjmcc.2003.09.007. PubMed: 14654370.
29. Niwa H, Yamamura K, Miyazaki J, (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199. doi:10.1016/0378-1119(91)90434-D. PubMed: 1660837.
30. Gao X, Liu HB, Wu JC, Liang J, Zhou LY, et al. (2011) Heme oxygenase-1 transgenic overexpression did not prevent artery injury induced by electric stimulation and pressure overload in mice. Eur J Pharmacol 659: 199-205. doi:10.1016/j.ejphar.2011.03.021. PubMed: 21458444.
31. Zhou L, Liu Y, Zou C, Ma N, Hui Y, et al. (2011) The effect of the Gly139His, Gly143His, and Ser142His mouse heme oxygenase-1 mutant on the HO reaction in vivo and in vitro. Anat Rec (Hoboken) 294: 112-118. doi:10.1002/ar.21284.
32. Hsueh W, Abel ED, Breslow JL, Maeda N, Davis RC, et al. (2007) Recipes for creating animal models of diabetic cardiovascular disease. Circ Res 100: 1415-1427. doi:10.1161/01.RES.0000266449.37396.1f. PubMed: 17525381.
33. Hui Y, Zhao Y, Ma N, Peng Y, Pan Z, et al. (2012) M3-mAChR stimulation exerts anti-apoptotic effect via activating the HIF-1alpha/HO-1/VEGF signaling pathway in H9c2 rat ventricular cells. J Cardiovasc Pharmacol 60: 474-482. doi:10.1097/FJC.0b013e31826c1c13. PubMed: 22932708.
34. Luchner A, Muders F, Dietl O, Friedrich E, Blumberg F, et al. (2001) Differential expression of cardiac ANP and BNP in a rabbit model of progressive left ventricular dysfunction. Cardiovasc Res 51: 601-607. doi:10.1016/S0008-6363(01)00316-9. PubMed: 11476751.
35. Yoon YS, Uchida S, Masuo O, Cejna M, Park JS, et al. (2005) Progressive attenuation of myocardial vascular endothelial groWth factor expression is a seminal event in diabetic cardiomyopathy: restoration of microvascular homeostasis and recovery of cardiac function in diabetic cardiomyopathy after replenishment of local vascular endothelial groWth factor. Circulation 111: 2073-2085. doi:10.1161/01.CIR.0000162472.52990.36. PubMed: 15851615.
36. Rajesh M, Bátkai S, Kechrid M, Mukhopadhyay P, Lee WS, et al. (2012) Cannabinoid 1 receptor promotes cardiac dysfunction, oxidative stress, inflammation, and fibrosis in diabetic cardiomyopathy. Diabetes 61: 716-727. doi:10.2337/db11-0477. PubMed: 22315315.
37. Van Linthout S, Riad A, Dhayat N, Spillmann F, Du J, et al. (2007) Anti-inflammatory effects of atorvastatin improve left ventricular function in experimental diabetic cardiomyopathy. Diabetologia 50: 1977-1986. doi:10.1007/s00125-007-0719-8. PubMed: 17589825.
38. Son SM, (2007) Role of vascular reactive oxygen species in development of vascular abnormalities in diabetes. Diabetes Res Clin Pract 77 (Suppl 1):: S65-S70. doi:10.1016/j.diabres.2007.01.036. PubMed: 17467110.
39. Lewis P, Stefanovic N, Pete J, Calkin AC, Giunti S, et al. (2007) Lack of the antioxidant enzyme glutathione peroxidase-1 accelerates atherosclerosis in diabetic apolipoprotein E-deficient mice. Circulation 115: 2178-2187. doi:10.1161/CIRCULATIONAHA.106.664250. PubMed: 17420349.
40. Lorenzo O, Picatoste B, Ares-Carrasco S, Ramirez E, Egido J, et al. (2011) Potential role of nuclear factor kappa B in diabetic cardiomyopathy. Mediat Inflamm: pp. 2011: 652097.
41. Khullar M, Al-Shudiefat AA, Ludke A, Binepal G, Singal PK, (2010) Oxidative stress: a key contributor to diabetic cardiomyopathy. Can J Physiol Pharmacol 88: 233-240. doi:10.1139/Y10-016. PubMed: 20393588.
42. Xie Z, He C, Zou MH, (2011) AMP-activated protein kinase modulates cardiac autophagy in diabetic cardiomyopathy. Autophagy 7: 1254-1255. doi:10.4161/auto.7.10.16740. PubMed: 21685727.
43. Kim AS, Miller EJ, Young LH, (2009) AMP-activated protein kinase: a core signalling pathway in the heart. Acta Physiol (Oxf) 196: 37-53. doi:10.1111/j.1748-1716.2009.01978.x. PubMed: 19239414.
44. Falcão-Pires I, Leite-Moreira AF, (2012) Diabetic cardiomyopathy: understanding the molecular and cellular basis to progress in diagnosis and treatment. Heart Fail Rev 17: 325-344. doi:10.1007/s10741-011-9257-z. PubMed: 21626163.
45. Soliman H, Gador A, Lu YH, Lin G, Bankar G, et al. (2012) Diabetes-induced increased oxidative stress in cardiomyocytes is sustained by a positive feedback loop involving Rho kinase and PKCbeta2. Am J Physiol Heart Circ Physiol 303: H989-H1000. doi:10.1152/ajpheart.00416.2012. PubMed: 22865386.
46. Khong FL, Zhang Y, Edgley AJ, Qi W, Connelly KA, et al. (2011) 3',4'-Dihydroxyflavonol antioxidant attenuates diastolic dysfunction and cardiac remodeling in streptozotocin-induced diabetic m(Ren2)27 rats. PLOS ONE 6: e22777. doi:10.1371/journal.pone.0022777. PubMed: 21829510.
47. Ren J, Ceylan-Isik AF, (2004) Diabetic cardiomyopathy: do women differ from men? Endocrine 25: 73-83. doi:10.1385/ENDO:25:2:073. PubMed: 15711018.
48. Haines DD, Lekli I, Teissier P, Bak I, Tosaki A, (2012) Role of haeme oxygenase-1 in resolution of oxidative stress-related pathologies: focus on cardiovascular, lung, neurological and kidney disorders. Acta Physiol (Oxf) 204: 487-501. doi:10.1111/j.1748-1716.2011.02387.x. PubMed: 22118298.
49. Kim YM, Pae HO, Park JE, Lee YC, Woo JM, et al. (2011) Heme oxygenase in the regulation of vascular biology: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 14: 137-167. doi:10.1089/ars.2010.3153. PubMed: 20624029.
50. Cao J, Sodhi K, Puri N, Monu SR, Rezzani R, et al. (2011) High fat diet enhances cardiac abnormalities in SHR rats: Protective role of heme oxygenase-adiponectin axis. Diabetol Metab Syndr 3: 37. doi:10.1186/1758-5996-3-37. PubMed: 22196253.
51. Kwak JY, Takeshige K, Cheung BS, Minakami S, (1991) Bilirubin inhibits the activation of superoxide-producing NADPH oxidase in a neutrophil cell-free system. Biochim Biophys Acta 1076: 369-373. doi:10.1016/0167-4838(91)90478-I. PubMed: 1848104.
52. Mano Y, Anzai T, Kaneko H, Nagatomo Y, Nagai T, et al. (2011) Overexpression of human C-reactive protein exacerbates left ventricular remodeling in diabetic cardiomyopathy. Circ J 75: 1717-1727. doi:10.1253/circj.CJ-10-1199. PubMed: 21519150.
53. Octavia Y, Brunner-La Rocca HP, Moens AL, (2012) NADPH oxidase-dependent oxidative stress in the failing heart: From pathogenic roles to therapeutic approach. Free Radic Biol Med 52: 291-297. doi:10.1016/j.freeradbiomed.2011.10.482. PubMed: 22080085.
54. Rajesh M, Mukhopadhyay P, Bátkai S, Patel V, Saito K, et al. (2010) Cannabidiol attenuates cardiac dysfunction, oxidative stress, fibrosis, and inflammatory and cell death signaling pathways in diabetic cardiomyopathy. J Am Coll Cardiol 56: 2115-2125. doi:10.1016/j.jacc.2010.07.033. PubMed: 21144973.
55. Deswal A, Petersen NJ, Feldman AM, Young JB, White BG, et al. (2001) Cytokines and cytokine receptors in advanced heart failure: an analysis of the cytokine database from the Vesnarinone trial (VEST). Circulation 103: 2055-2059. doi:10.1161/01.CIR.103.16.2055. PubMed: 11319194.
56. Cacciapaglia F, Navarini L, Menna P, Salvatorelli E, Minotti G, et al. (2011) Cardiovascular safety of anti-TNF-alpha therapies: facts and unsettled issues. Autoimmun Rev 10: 631-635. doi:10.1016/j.autrev.2011.04.014. PubMed: 21539939.
57. Gordon JW, Shaw JA, Kirshenbaum LA, (2011) Multiple facets of NF-kappaB in the heart: to be or not to NF-kappaB. Circ Res 108: 1122-1132. doi:10.1161/CIRCRESAHA.110.226928. PubMed: 21527742.
58. Lecour S, James RW, (2011) When are pro-inflammatory cytokines SAFE in heart failure? Eur Heart J 32: 680-685. doi:10.1093/eurheartj/ehq484. PubMed: 21303780.
59. Brasier AR, (2010) The nuclear factor-kappaB-interleukin-6 signalling pathway mediating vascular inflammation. Cardiovasc Res 86: 211-218. doi:10.1093/cvr/cvq076. PubMed: 20202975.
60. Chen D, Assad-Kottner C, Orrego C, Torre-Amione G, (2008) Cytokines and acute heart failure. Crit Care Med 36: S9-16. doi:10.1097/01.CCM.0000297160.48694.90. PubMed: 18158483.
61. Wu ML, Ho YC, Yet SF, (2011) A central role of heme oxygenase-1 in cardiovascular protection. Antioxid Redox 15: 1835-1846. doi:10.1089/ars.2010.3726.
62. Durante W, (2011) Protective role of heme oxygenase-1 against inflammation in atherosclerosis. Front Biosci 16: 2372-2388. doi:10.2741/3860. PubMed: 21622183.
63. Mougiakakos D, Jitschin R, Johansson CC, Okita R, Kiessling R, et al. (2011) The impact of inflammatory licensing on heme oxygenase-1-mediated induction of regulatory T cells by human mesenchymal stem cells. Blood. 117: 4826-4835. doi:10.1182/blood-2010-12-324038. PubMed: 21389316.
64. Sun L, Shi T, Qiao H, Jiang X, Jiang H, et al. (2011) Hepatic overexpression of heme oxygenase-1 improves liver allograft survival by expanding T regulatory cells. J Surg Res 166: e187-e194. doi:10.1016/j.jss.2010.11.917. PubMed: 21227452.
65. Orozco LD, Kapturczak MH, Barajas B, Wang X, Weinstein MM, et al. (2007) Heme oxygenase-1 expression in macrophages plays a beneficial role in atherosclerosis. Circ Res 100: 1703-1711. doi:10.1161/CIRCRESAHA.107.151720. PubMed: 17495224.
66. Wang G, Hamid T, Keith RJ, Zhou G, Partridge CR, et al. (2010) Cardioprotective and antiapoptotic effects of heme oxygenase-1 in the failing heart. Circulation 121: 1912-1925. doi:10.1161/CIRCULATIONAHA.109.905471. PubMed: 20404253.
67. Aki T, Yamaguchi K, Fujimiya T, Mizukami Y, (2003) Phosphoinositide 3-kinase accelerates autophagic cell death during glucose deprivation in the rat cardiomyocyte-derived cell line H9c2. Oncogene 22: 8529-8535. doi:10.1038/sj.onc.1207197. PubMed: 14627994.
68. Raphael J, Abedat S, Rivo J, Meir K, Beeri R, et al. (2006) Volatile anesthetic preconditioning attenuates myocardial apoptosis in rabbits after regional ischemia and reperfusion via Akt signaling and modulation of Bcl-2 family proteins. J Pharmacol Exp Ther 318: 186-194. doi:10.1124/jpet.105.100537. PubMed: 16551837.
69. Fukazawa R, Miller TA, Kuramochi Y, Frantz S, Kim YD, et al. (2003) Neuregulin-1 protects ventricular myocytes from anthracycline-induced apoptosis via erbB4-dependent activation of PI3-kinase/Akt. J Mol Cell Cardiol 35: 1473-1479. doi:10.1016/j.yjmcc.2003.09.012. PubMed: 14654373.
70. Hong F, Kwon SJ, Jhun BS, Kim SS, Ha J, et al. (2001) Insulin-like groWth factor-1 protects H9c2 cardiac myoblasts from oxidative stress-induced apoptosis via phosphatidylinositol 3-kinase and extracellular signal-regulated kinase pathways. Life Sci 68: 1095-1105. doi:10.1016/S0024-3205(00)01012-2. PubMed: 11228094.
71. Gnecchi M, He H, Liang OD, Melo LG, Morello F, et al. (2005) Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 11: 367-368. doi:10.1038/nm0405-367. PubMed: 15812508.
72. Martinet W, Knaapen MW, Kockx MM, De Meyer GR, (2007) Autophagy in cardiovascular disease. Trends Mol Med 13: 482-491. doi:10.1016/j.molmed.2007.08.004. PubMed: 18029229.
73. Carchman EH, Rao J, Loughran PA, Rosengart MR, Zuckerbraun BS, (2011) Heme oxygenase-1-mediated autophagy protects against hepatocyte cell death and hepatic injury from infection/sepsis in mice. Hepatology 53: 2053-2062. doi:10.1002/hep.24324. PubMed: 21437926.