Effect of hydrogen sulfide in a porcine model of myocardial ischemia-reperfusion: Comparison of different administration regimens and characterization of the cellular mechanisms of protection

Journal of Cardiovascular Pharmacology

Volumn 54, Issue 4, 2009, Pages 287-297

  Osipov, Robert M ^a   Robich, Michael P ^a   Feng, Jun ^a   Liu, Yuhong ^a   Clements, Richard T ^a   Glazer, Hilary P ^a   Sodha, Neel R ^b   Szabo, Csaba ^a   Bianchi, Cesario ^a   Sellke, Frank W ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MALLINCKRODT PHARMACEUTICALS   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

Apoptosis; Cardiac function; Heart protection; Hydrogen sulfide; Microvascular reactivity; Myocardial ischemia "reperfusion injury

Indexed keywords

APOPTOSIS INDUCING FACTOR; BECLIN 1; CASPASE 3; DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; HYDROGEN SULFIDE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOGLYCOGEN SYNTHASE KINASE 3; PHOSPHOTRANSFERASE; PLACEBO; TRIPHENYLTETRAZOLIUM; TROPONIN I; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTERIAL GAS; ARTICLE; AUTOPHAGY; CELL COUNT; CELL DEATH; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; CORE TEMPERATURE; ENDOTHELIUM; HEART FUNCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE; HEART MUSCLE ISCHEMIA; HEMATOCRIT; HEMODYNAMICS; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MALE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION; STAINING; SWINE;

ANIMALS; APOPTOSIS; CARDIOTONIC AGENTS; CELL SURVIVAL; CORONARY CIRCULATION; DISEASE MODELS, ANIMAL; HYDROGEN SULFIDE; IN SITU NICK-END LABELING; INFUSIONS, INTRAVENOUS; INJECTIONS, INTRAVENOUS; MALE; MICROCIRCULATION; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; SWINE; TROPONIN I; VENTRICULAR FUNCTION, LEFT;

EID: 74949085029     PISSN: 01602446     EISSN: None     Source Type: Journal    
DOI: 10.1097/FJC.0b013e3181b2b72b     Document Type: Article

References (48)

1. Marzilli M, Orsini E, Marraccini P, et al. Beneficial effects of intracoronary adenosine as an adjunct to primary angioplasty in acute myocardial infarction. Circulation. 2000;101:2154-2159.
2. Sodha NR, Clements RT, Feng J, et al. The effects of therapeutic sulfide on myocardial apoptosis in response to ischemia-reperfusion injury. Eur J Cardiothorac Surg. 2008;33:906-913.
3. Quintana M, Kahan T, Hjemdahl P. Pharmacological prevention of reperfusion injury in acute myocardial infarction. A potential role for adenosine as a therapeutic agent. Am J Cardiovasc Drugs. 2004;4: 159-167.
4. Zhang Z, Huang H, Liu P, et al. Hydrogen sulfide contributes to cardioprotection during ischemia-reperfusion injury by opening K ATP channels. Can J Physiol Pharmacol. 2007;85:1248-1253.
5. Zhao G, Bou-Abdallah F, Yang X, et al. Is hydrogen peroxide produced during iron(II) oxidation in mammalian apoferritins? Biochemistry. 2001; 40:10832-10838.
6. Whiteman M, Armstrong JS, Chu SH, et al. The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'? J Neurochem. 2004;90:765-768.
7. Moore PK, Bhatia M, Moochhala S. Hydrogen sulfide: from the smell of the past to the mediator of the future? Trends Pharmacol Sci. 2003;24:609-611.
8. Wang R. The gasotransmitter role of hydrogen sulfide. Antioxid Redox Signal. 2003;5:493-501.
9. Bian JS, Yong QC, Pan TT, et al. Role of hydrogen sulfide in the cardioprotection caused by ischemic preconditioning in the rat heart and cardiac myocytes. J Pharmacol Exp Ther. 2006;316:670-678.
10. Johansen D, Ytrehus K, Baxter GF. Exogenous hydrogen sulfide (H2S) protects against regional myocardial ischemia-reperfusion injury-evidence for a role of K ATP channels. Basic Res Cardiol. 2006;101:53-60.
11. Elrod JW, Greer JJ, Lefer DJ. Sildenafil-mediated acute cardioprotection is independent of the NO/cGMP pathway. Am J Physiol Heart Circ Physiol. 2007;292:H342-H347.
12. Toyoda Y, Di Gregorio V, Parker RA, et al. Anti-stunning and anti-infarct effects of adenosine-enhanced ischemic preconditioning. Circulation. 2000;102:III326-III331.
13. Bengtsson A, Johnson JJ, Hill P, et al. Use of mono-bromo-bimane to derivatize sulfide in whole blood: comparison of blood sulfide levels during atmospheric hydrogen sulfide exposure and intravenous sulfide infusion. Presented at: Experimental Biology Meeting; 2008, April 5-9, San Diego, USA. Abstract 749.
14. Simon F, Giudici R, Duy CN, et al. Hemodynamic and metabolic effects of hydrogen sulfide during porcine ischemia/reperfusion injury. Shock. 2008;30:359-364.
15. Zhu JC, Shao JL, Ma H, et al. [Interaction between endogenous cystathionine synthase/hydrogen sulfide and heme oxygenase-1/carbon monoxide systems during myocardial ischemic-reperfusion: experiment with rats]. Zhonghua Yi Xue Za Zhi. 2008;88:3222-3225.
16. Pan TT, Feng ZN, Lee SW, et al. Endogenous hydrogen sulfide contributes to the cardioprotection by metabolic inhibition preconditioning in the rat ventricular myocytes. J Mol Cell Cardiol. 2006;40:119-130.
17. Sivarajah A, Collino M, Yasin M, et al. Antiapoptotic and antiinflammatory effects of hydrogen sulfide in a rat model of regional myocardial I/R. Shock. 2008;31:267-274.
18. Ji Y, Pang QF, Xu G, et al. Exogenous hydrogen sulfide postconditioning protects isolated rat hearts against ischemia-reperfusion injury. Eur J Pharmacol. 2008;587:1-7.
19. Elrod JW, Calvert JW, Morrison J, et al. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci U S A. 2007;104:15560-15565.
20. Zhong G, Chen F, Cheng Y, et al. The role of hydrogen sulfide generation in the pathogenesis of hypertension in rats induced by inhibition of nitric oxide synthase. J Hypertens. 2003;21:1879-1885.
21. Yanfei W, Lin S, Junbao D, et al. Impact of L-arginine on hydrogen sulfide/cystathionine-gamma-lyase pathway in rats with high blood flowinduced pulmonary hypertension. Biochem Biophys Res Commun. 2006; 345:851-857.
22. Kamoun P. Endogenous production of hydrogen sulfide in mammals. Amino Acids. 2004;26:243-254.
23. Komarnisky LA, Christopherson RJ, Basu TK. Sulfur: its clinical and toxicologic aspects. Nutrition. 2003;19:54-61.
24. Zakeri Z, Lockshin RA. Cell death: history and future. Adv Exp Med Biol. 2008;615:1-11.
25. Fujio Y, Nguyen T, Wencker D, et al. Akt promotes survival of cardiomyocytes in vitro and protects against ischemia-reperfusion injury in mouse heart. Circulation. 2000;101:660-667.
26. Yue TL, Wang C, Gu JL, et al. Inhibition of extracellular signal-regulated kinase enhances ischemia/reoxygenation-induced apoptosis in cultured cardiac myocytes and exaggerates reperfusion injury in isolated perfused heart. Circ Res. 2000;86:692-699.
27. Zhi L, Ang AD, Zhang H, et al. Hydrogen sulfide induces the synthesis of proinflammatory cytokines in human monocyte cell line U937 via the ERK-NF-kappaB pathway. J Leukoc Biol. 2007;81:1322-1332.
28. Kerkela R, Kockeritz L, Macaulay K, et al. Deletion of GSK-3beta in mice leads to hypertrophic cardiomyopathy secondary to cardiomyoblast hyperproliferation. J Clin Invest. 2008;118:3609-3618.
29. Hirotani S, Zhai P, Tomita H, et al. Inhibition of glycogen synthase kinase 3beta during heart failure is protective. Circ Res. 2007;101:1164-1174.
30. Lepore DA, Knight KR, Anderson RL, et al. Role of priming stresses and Hsp70 in protection from ischemia-reperfusion injury in cardiac and skeletal muscle. Cell Stress Chaperones. 2001;6:93-96.
31. Beere HM, Wolf BB, Cain K, et al. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol. 2000;2:469-475.
32. Okamura T, Miura T, Takemura G, et al. Effect of caspase inhibitors on myocardial infarct size and myocyte DNA fragmentation in the ischemiareperfused rat heart. Cardiovasc Res. 2000;45:642-650.
33. Gustafsson AB, Gottlieb RA. Bcl-2 family members and apoptosis, taken to heart. Am J Physiol Cell Physiol. 2007;292:C45-C51.
34. Volpato GP, Searles R, Yu B, et al. Inhaled hydrogen sulfide: a rapidly reversible inhibitor of cardiac and metabolic function in the mouse. Anesthesiology. 2008;108:659-668.
35. Du J, Hui Y, Cheung Y, et al. The possible role of hydrogen sulfide as a smooth muscle cell proliferation inhibitor in rat cultured cells. Heart Vessels. 2004;19:75-80.
36. Nicholls P. Inhibition of cytochrome c oxidase by sulphide. Biochem Soc Trans. 1975;3:316-319.
37. Baskar R, Li L, Moore PK. Hydrogen sulfide-induces DNA damage and changes in apoptotic gene expression in human lung fibroblast cells. FASEB J. 2007;21:247-255.
38. Cao Y, Adhikari S, Ang AD, et al. Mechanism of induction of pancreatic acinar cell apoptosis by hydrogen sulfide. Am J Physiol Cell Physiol. 2006;291:C503-C510. (Pubitemid 44343633)
39. Mazumder S, Plesca D, Almasan A. Caspase-3 activation is a critical determinant of genotoxic stress-induced apoptosis. Methods Mol Biol. 2008;414:13-21.
40. Baines CP, Molkentin JD. STRESS signaling pathways that modulate cardiac myocyte apoptosis. J Mol Cell Cardiol. 2005;38:47-62.
41. Yaoita H, Ogawa K, Maehara K, et al. Attenuation of ischemia/ reperfusion injury in rats by a caspase inhibitor. Circulation. 1998;97: 276-281.
42. Matsuda M, Matsumoto S, Noguchi M, et al. [Effects of intravenous anesthetics on acidosis induced apoptosis in primary brain cell culture]. Masui. 2007;56:911-919.
43. Gustafsson AB, Gottlieb RA. Autophagy in ischemic heart disease. Circ Res. 2009;104:150-158.
44. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science. 2000;290:1717-1721.
45. Reynolds THT, Bodine SC, Lawrence JC Jr. Control of Ser2448 phosphorylation in the mammalian target of rapamycin by insulin and skeletal muscle load. J Biol Chem. 2002;277:17657-17662.
46. Li HB, Yi X, Gao JM, et al. Magnolol-induced H460 cells death via autophagy but not apoptosis. Arch Pharm Res. 2007;30:1566-1574.
47. Hamacher-Brady A, Brady NR, Logue SE, et al. Response to myocardial ischemia/reperfusion injury involves BNip 3 and autophagy. Cell Death Differ. 2007;14:146-157.
48. Matsui Y, Takagi H, Qu X, et al. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res. 2007; 100:914-922.