Exogenous Hydrogen Sulfide Attenuates Cardiac Fibrosis Through Reactive Oxygen Species Signal Pathways in Experimental Diabetes Mellitus Models

Cellular Physiology and Biochemistry

Volumn 36, Issue 3, 2015, Pages 917-929

  Zheng, Dan ^a   Dong, Shiyun ^a   Li, Ting ^a   Yang, Fan ^a   Yu, Xiangjing ^a   Wu, Jichao ^a   Zhong, Xin ^a   Zhao, Yajun ^a   Wang, Lina ^a   Xu, Changqing ^a,b   Lu, Fanghao ^a   Zhang, Weihua ^a,b  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b Bio pharmaceutical Key Laboratory of Heilongjiang Province   (China)

Author keywords

Cardiac fibrosis; Diabetic cardiomyopathy; Hydrogen sulfide; NADPH oxidase 4; Reactive oxygen species

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 2; GELATINASE A; GELATINASE B; GLUCOSE; GYY 4137; HYDROGEN SULFIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OXIDIZING AGENT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; STREPTOZOCIN; UNCLASSIFIED DRUG; MORPHOLINE DERIVATIVE; NOX4 PROTEIN, RAT; PHOSPHOROTHIOIC ACID DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; SODIUM BISULFIDE; SULFIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; DISEASE COURSE; DRUG EFFECT; DRUG MECHANISM; ECHOCARDIOGRAPHY; EXPERIMENTAL DIABETES MELLITUS; FIBROBLAST; GLUCOSE BLOOD LEVEL; HEART CYCLE; HEART FIBROBLAST; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART MUSCLE FIBROSIS; HYPERGLYCEMIA; IMMUNOFLUORESCENCE; IN VIVO STUDY; MALE; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PRIMARY CULTURE; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; CYTOLOGY; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PRIMARY CELL CULTURE; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; DIABETES MELLITUS, EXPERIMENTAL; FIBROBLASTS; GENE EXPRESSION REGULATION; GLUCOSE; HYDROGEN SULFIDE; HYPERGLYCEMIA; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MORPHOLINES; NADPH OXIDASE; ORGANOTHIOPHOSPHORUS COMPOUNDS; PRIMARY CELL CULTURE; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STREPTOZOCIN; SULFIDES;

EID: 84931835242     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000430266     Document Type: Article

References (42)

1. Li CJ, Lv L, Li H, Yu DM: Cardiac fibrosis and dysfunction in experimental diabetic cardimyopathy are ameliorated by alpha-lipoic acid. Cardiovas Diabetol 2012;11:73-82.
2. Boudina S, Abel ED: Diabetic cardiomyopathy revisited. Circulation 2007;115:3212-3223.
3. Falcao-Pires I, Leite-Moreira AF: Diabetic cardiomyopathy: understanding the molecular and cellular basis to progress in diagnosis and treatment. Heart Fail Rev 2012;17:325-344.
4. Asbun J, Villarreal FJ: The pathogenesis of myocardial fibrosis in the setting of diabetic cardiomyopathy. J Am Coll Cardiol 2006;47:693-700.
5. Aragno M, Mastrocola R, Medana C, Catalano MG, Vercellinatto I, Danni O, Boccuzzi G: Oxidative Stress-Dependent Impairment of Cardiac-Specific Transcription Factors in Experimental Diabetes. Endocrinology 2006;147:5967-5974.
6. Zou P, Wu LL, Wu D, Fan D, Cui XB, Zhou Y, Wang C, Li L: High glucose increases periostin expression and the related signal pathway in adultrat cardiac fibroblasts. Acta Physiologica Sinica 2010;62:247-254.
7. Zhao W, Zhao T, Chen Y, Ahokas RA, Sun Y: Oxidative stress mediates cardiac fibrosis by enhancing transforming growth factor-betal in hypertensive rats. Mol Cell Biochem 2008;317:43-50.
8. Anejia A, Tang WH, Banisilal S, Garcia MJ, Farkouh ME: Diabetic cardiomyopathy: insights into pathogenesis, diagnostic challenges and thereputic option. Am J Med 2008;21:748-757.
9. Cail L, Wang Y, Zhou G, Chen T, Song Y, Li X, Kang YJ: Attenuation by metallothionein of early cardiac cell death via suppression of mitochondrial oxidative stress results in a prevention of diabetic cardiomyopathy. J Am Coll Cardiol 2006;48:1688-169.
10. Kuroda J, Ag T, Matsushima S, Zhai PY, Schneider M, Sadoshima J: NADPH oxidase (NOX4) is a major source of oxidative stress in the failing heart. Proc Acar Sci USA 2010;107:15565-15570.
11. Wen YD, Wang H, Kho SK, Rinkiko S, Sheng X, Shen HM, Zhu YZ: Hydrogen Sulfide Protects HUVECs against Hydrogen Peroxide Induced Mitochondrial Dysfunction and Oxidative Stress. Plos One 2013;8:53147-53156.
12. Yang CT, Zhao Y, Xian M, Li JH, Dong Q, Bai HB, Xu JD, Zhang MF: A novel controllable hydrogen sulfide-releasing molecule protects human skin keratinocytes against methylglyoxal-induced injury and dysfunction. Cell Physiol Biochem 2014;34:1304-1317.
13. Avanzato D, Merlino A, Porrera S, Wang R, Munaron L, Mancardi D: Role of calcium channels in the protective effect of hydrogen sulfide in rat cardiomyoblasts. Cell Physiol Biochem 2014;33:1205-1214.
14. Guo R, Wu K, Chen J, Mo L, Hua X, Zheng D, Chen P, Chen G, Xu W, Feng J: Exogenous hydrogen sulfide protects against doxorubicin-induced inflammation and cytotoxicity by inhibiting p38MAPK/NFKB pathway in H9c2 cardiac cells. Cell Physiol Bioche. 2013;32:1668-1680.
15. Wang R: Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 2012;92:791-896.
16. Ju YJ, Zhang WH, Pei YX Yang GD: H2S signaling in redox regulation of cellular functions .Can J Physiol Pharmacol 2013;91:1-7.
17. Pan LL, Liu XH, Shen YQ, Wang NZ, Xu J, Wu D, Xiong QH, Deng HY, Huang GY, Zhu YZ: Inhibition of NADPH oxidase 4-related signaling by sodium hydrosulfide attenuates myocardial fibrotic response. Int J Cardiol 2013;168:3770-3778.
18. Huang CR, Kan JT, Liu X, MaFF, Tran H, Zou YZ, Wang SJ, Zhu YZ: Cardioprotective Effects of a Novel Hydrogen Sulfide Agent-Controlled Realease Formulation of S-Propargyl-Cysteine on Heart Failure Rats and Molecular Mechanisms. PLoS One 2013;8:e669205.
19. Sheng JW, Shim W, Wei HM, Lim SY, Liew R, Lim TS, Ong BH, Chua YL, Wong P: Hydrogen sulphide suppresses human atrial fibroblast proliferation and transformation to myofibroblasts. J Cell Mol Med 2013;17:1345-1354.
20. Zhong X, Wang LH, Wang YW, Dong SY, Leng XN, Yang GD, Wu LY, Wang R, Lu FH, Zhang WH: Exogenous hydrogen sulfide attenuates diabetic myocardial injury through cardiac mitochondrial protection. Mol Cell Biochem 2012;371:187-198.
21. Lu FH, Fu SB, Leng XN, Zhang XY, Dong SY, Zhao YJ, Ren H, Li HL, Zhong X, Zhang WH: Role of the Calcium-Sensing Receptor in Cardiomyocyte Apoptosis via the Sarcoplasmic Reticulum and Mitochondrial Death Pathway in Cardiac Hypertrophy and Heart Failure. Cell Physiol Biochem 2013;31:728-743.
22. Zhang XY, Zhang TM, Wu JC, Yang F, Yu XJ, Xu CQ, Lu FH, Zhang WH: Calcium sensing receptor promoting cardiac fibroblats proliferation. Cell Physio Biochem 2014;33:414-423.
23. Taye A, Mekky M, Mohafe OM: Tempol ameliorates cardiac fibrosis in streptozotocin-induced diabetic rats: role of oxidative stress in diabetic cardiomyopathy. Naunyn-Schmiedeberg's Arch Pharmacol 2013;386:1071-1080.
24. Wang P, Li HW, Wang YP, Chen H, Zhang P: Effects of recombinant human relaxin upon proliferation of cardiac fibroblast and synthesis of collagen under high glucose condition. J Endocrinol Invest 2009;32:242-247.
25. Zhang M, Perino A, Ghigo A, Hirsch E, Shah AM: NADPH Oxidases in Heart Failure: Poachers or Gamekeepers? Antioxid Redox Signal 2013;18:1024-1032.
26. Bergman MR, Teerlink JR, Mahimkar R, Li L, Zhu BQ, Nguyen A, Dahi S, Karliner JS, Lovett DH: Cardiac matrix metalloproteinase-2 expression independently induces marked ventricular remodeling and systolic dysfunction. Am J Physiol Heart Circ Physiol 2007;292:H1847-H1860.
27. Fang ZY, Prins JB, Marwick TH: Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev 2004;25:543-567.
28. Haidara MA, Yassin HZ, Rateb M, Ammar H, Zorkani MA: Role of oxidative stress in development of cardiovascular complications in diabetes mellitus. Curr Vasc Pharmacol 2006;4:215-227.
29. Anilkumar N, Sirker A, Shah AM: Redox sensitive signaling pathways in cardiac remodeling, hypertrophy and failure. Front Biosci 2009;14:3168-3187.
30. Ide T, Tsutsui H, Kinugawa S, Suematsu N, Hayashidani S, Ichikawa K, Utsumi H, Machida Y, Egashira K, Takeshita A: Direct evidence for increased hydroxyl radicals originating from superoxide in the failing myocardium. Circ Res 2000;86:152-157.
31. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG: Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 2006;18:69-82.
32. Ushio-Fukai M: Localizing NADPH oxidase-derived ROS. Sci STKE 2006;re8.
33. Bedard K, Krause KH: The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology. Physiol Rev 2007;87:245-313.
34. Heymes C, Bendail JK, Ratajiczak P, Cave AC, Samuel JL, Hasenfuss G, Shah AM: Increased myocardial NADPH oxidase activity in human heart failure. J Am Coll Cardiol 2003;41:2164-2171.
35. Cucoranu I, Clempus R, Dikalova A, Phelan PJ, Arivan S, Dikalov S, Sorescu D: NAD(P)H oxidase 4 mediates transforming growth factorbeta1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ Res 2005;97:900-907.
36. Byrne JA, Grieve DJ, Bendall JK, Li JM, Gove C, Lambeth JD, Cave AC, Shah AM: Contrasting roles of NADPH oxidase isoforms in pressure overload versus angiotensin II-induced cardiac hypertrophy. Circ Res 2003;93:802-805.
37. Kabil O, Banerjee R: Redox biochemistry of hydrogen sulfide. J Biol Chem 2010;285:21903-21907.
38. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S, Snyder SH, Wang R: H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 2008;322:587-590.
39. Papapetropoulos A, Pyriochou A, Altaany Z, Yang G, Marazioti A, Zhou Z, Jeschke MG, Branski LK, Hemdon DN, Wang R, Szabo C: Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc. Natl. Acad. Sci USA 2009;106:21972-21977.
40. Calvert JW, Elston M, Nicholson CK, Gundewar S, Jha S, Elrod JW, Ramachandran A, Lefer DJ: Genetic and pharmacologic hydrogen sulfide therapy attenuates ischemia-induced heart failure in mice. Circulation 2010;122:11-19.
41. Snijder PM, Frenay AS, de Boer RA, Pasch A, Hille Branks J, Leuvenink HG, Van Goor H: Exogenous administration of thiosulfate, a donor of hydrogen sulfide, attenuates Aniotensin-induced hypertensive heart disease in rats. Br J Paharmacol DOI: 10.1111/bph.12825.
42. Han Y, Zeng F, Tan G, Yang C, Tang H, Luo Y, Feng J, Xiong H, Guo Q: Hydrogen sulfide inhibits abnormal proliferation of lymphocytes via AKT/GSK3p signal pathway in systemic lupus erythematosus patients. Cell Physiol Biochem 2013;31:795-804.