Hydrogen sulfide attenuates hepatic ischemia-reperfusion injury: Role of antioxidant and antiapoptotic signaling

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 295, Issue 2, 2008, Pages

  Jha, Saurabh ^a   Calvert, John W ^b   Duranski, Mark R ^a   Ramachandran, Arun ^a   Lefer, David J ^b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Glutathione; Heat shock protein 90; Liver; Thioredoxin

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HEAT SHOCK PROTEIN 90; HYDROGEN SULFIDE; IK 1001; LIPID HYDROPEROXIDE; PROTEIN BCL 2; SODIUM SULFIDE; THIOREDOXIN 1; UNCLASSIFIED DRUG; ANTIOXIDANT; SULFIDE; THIOREDOXIN; TXN1 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; LIVER ISCHEMIA; LIVER PROTECTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; ANIMAL; BLOOD; C57BL MOUSE; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECT; LIPID PEROXIDATION; LIVER; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; SIGNAL TRANSDUCTION; VASCULARIZATION;

ALANINE TRANSAMINASE; ANIMALS; ANTIOXIDANTS; APOPTOSIS; ASPARTATE AMINOTRANSFERASES; CYTOPROTECTION; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTATHIONE; GLUTATHIONE DISULFIDE; HSP90 HEAT-SHOCK PROTEINS; HYDROGEN SULFIDE; LIPID PEROXIDATION; LIVER; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-BCL-2; REPERFUSION INJURY; SIGNAL TRANSDUCTION; SULFIDES; THIOREDOXINS;

EID: 52449104880     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00377.2008     Document Type: Article

References (48)

1. Bian JS, Yong QC, Pan TT, Feng ZN, Ali MY, Zhou S, Moore PK. Role of hydrogen sulfide in the cardioprotection caused by ischemic preconditioning in the rat heart and cardiac myocytes. J Pharmacol Exp Ther 316: 670-678, 2006.
2. Chakraborty A, Koldobskiy MA, Sixt KM, Juluri KR, Mustafa AK, Snowman AM, van Rossum DB, Patterson RL, Snyder SH. HSP90 regulates cell survival via inositol hexakisphosphate kinase-2. Proc Natl Acad Sci USA 105: 1134-1139, 2008.
3. Cheng Y, Ndisang JF, Tang G, Cao K, Wang R. Hydrogen sulfide-induced relaxation of resistance mesenteric artery beds of rats. Am J Physiol Heart Circ Physiol 287: H2316-H2323, 2004.
4. Dias S, Shmelkov SV, Lam G, Rafii S. VEGF(165) promotes survival of leukemic cells by Hsp90-mediated induction of Bcl-2 expression and apoptosis inhibition. Blood 99: 2532-2540, 2002.
5. Duranski MR, Elrod JW, Calvert JW, Bryan NS, Feelisch M, Lefer DJ. Genetic overexpression of eNOS attenuates hepatic ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 291: H2980-H2986, 2006.
6. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, Jiao X, Scalia R, Kiss L, Szabo C, Kimura H, Chow CW, Lefer DJ. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci USA 104: 15560-15565, 2007.
7. Esechie A, Kiss L, Olah G, Horvath EM, Hawkins HK, Szabo C, Traber DL. Protective effect of hydrogen sulfide in a murine model of combined burn and smoke inhalation-induced acute lung injury. Clin Sci (Lond), 2008.
8. Eto K, Ogasawara M, Umemura K, Nagai Y, Kimura H. Hydrogen sulfide is produced in response to neuronal excitation. J Neurosci 22: 3386-3391, 2002.
9. Exner R, Wessner B, Manhart N, Roth E. Therapeutic potential of glutathione. Wien Klin Wochenschr 112: 610-616, 2000.
10. Fan C, Zwacka RM, Engelhardt JF. Therapeutic approaches for ischemia/ reperfusion injury in the liver. J Mol Med 77: 577-592, 1999.
11. Fondevila C, Busuttil RW, Kupiec-Weglinski JW. Hepatic ischemia/ reperfusion injury - a fresh look. Exp Mol Pathol 74: 86-93, 2003.
12. Georgiev P, Dahm F, Graf R, Clavien PA. Blocking the path to death: anti-apoptotic molecules in ischemia/reperfusion injury of the liver. Curr Pharm Des 12: 2911-2921, 2006.
13. Girotti AW. Translocation as a means of disseminating lipid hydroperoxide-induced oxidative damage and effector action. Free Radic Biol Med 44: 956-968, 2008.
14. Glantzounis GK, Salacinski HJ, Yang W, Davidson BR, Seifalian AM. The contemporary role of antioxidant therapy in attenuating liver ischemia-reperfusion injury: a review. Liver Transpl 11: 1031-1047, 2005.
15. Gray CC, Amrani M, Yacoub MH. Heat stress proteins and myocardial protection: experimental model or potential clinical tool? Int J Biochem Cell Biol 31: 559-573, 1999.
16. Gundewar S, Calvert JW, Elrod JW, Lefer DJ. Cytoprotective effects of N,N,N-trimethylsphingosine during ischemia- reperfusion injury are lost in the setting of obesity and diabetes. Am J Physiol Heart Circ Physiol 293: H2462-H2471, 2007.
17. Hu Y, Chen X, Pan TT, Neo KL, Lee SW, Khin ES, Moore PK, Bian JS. Cardioprotection induced by hydrogen sulfide preconditioning involves activation of ERK and PI3K/Akt pathways. Pflügers Arch 455: 607-616, 2008.
18. Jaeschke H. Mechanisms of liver injury. II. Mechanisms of neutrophil-induced liver cell injury during hepatic ischemia-reperfusion and other acute inflammatory conditions. Am J Physiol Gastrointest Liver Physiol 290: G1083-G1088, 2006.
19. Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 284: G15-G26, 2003.
20. Jaeschke H, Lemasters JJ. Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology 125: 1246-1257, 2003.
21. Kang KJ. Mechanism of hepatic ischemia/reperfusion injury and protection against reperfusion injury. Transplant Proc 34: 2659-2661, 2002.
22. Kasuno K, Nakamura H, Ono T, Muso E, Yodoi J. Protective roles of thioredoxin, a redox-regulating protein, in renal ischemia/reperfusion injury. Kidney Int 64: 1273-1282, 2003.
23. Kimura Y, Dargusch R, Schubert D, Kimura H. Hydrogen sulfide protects HT22 neuronal cells from oxidative stress. Antioxid Redox Signal 8: 661-670, 2006.
24. Kimura Y, Kimura H. Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18: 1165-1167, 2004.
25. Koti RS, Seifalian AM, Davidson BR. Protection of the liver by ischemic preconditioning: a review of mechanisms and clinical applications. Dig Surg 20: 383-396, 2003.
26. Kupiec-Weglinski JW, Busuttil RW. Ischemia and reperfusion injury in liver transplantation. Transplant Proc 37: 1653-1656, 2005.
27. Leffler CW, Parfenova H, Jaggar JH, Wang R. Carbon monoxide and hydrogen sulfide: gaseous messengers in cerebrovascular circulation. J Appl Physiol 100: 1065-1076, 2006.
28. Lichtman SN, Lemasters JJ. Role of cytokines and cytokine-producing cells in reperfusion injury to the liver. Semin Liver Dis 19: 171-187, 1999.
29. Lowicka E, Beltowski J. Hydrogen sulfide (H2S)-the third gas of interest for pharmacologists. Pharmacol Rep 59: 4-24, 2007.
30. Moore PK, Bhatia M, Moochhala S. Hydrogen sulfide: from the smell of the past to the mediator of the future? Trends Pharmacol Sci 24: 609-611, 2003.
31. Plin C, Tillement JP, Berdeaux A, Morin D. Resveratrol protects against cold ischemia-warm reoxygenation-induced damages to mitochondria and cells in rat liver. Eur J Pharmacol 528: 162-168, 2005.
32. Rose P, Moore PK, Ming SH, Nam OC, Armstrong JS, Whiteman M. Hydrogen sulfide protects colon cancer cells from chemopreventative agent beta-phenylethyl isothiocyanate induced apoptosis. World J Gastroenterol 11: 3990-3997, 2005.
33. Scarabelli TM, Knight R, Stephanou A, Townsend P, Chen-Scarabelli C, Lawrence K, Gottlieb R, Latchman D, Narula J. Clinical implications of apoptosis in ischemic myocardium. Curr Probl Cardiol 31: 181-264, 2006.
34. Selzner M, Clavien PA. Fatty liver in liver transplantation and surgery. Semin Liver Dis 21: 105-113, 2001.
35. Sodha NR, Clements RT, Feng J, Liu Y, Bianchi C, Horvath EM, Szabo C, Sellke FW. The effects of therapeutic sulfide on myocardial apoptosis in response to ischemia-reperfusion injury. Eur J Cardiothorac Surg 33: 906-913, 2008.
36. Szabo C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6: 917-935, 2007.
37. Teague B, Asiedu S, Moore PK. The smooth muscle relaxant effect of hydrogen sulphide in vitro: evidence for a physiological role to control intestinal contractility. Br J Pharmacol 137: 139-145, 2002.
38. Teoh NC, Farrell GC. Hepatic ischemia reperfusion injury: pathogenic mechanisms and basis for hepatoprotection. J Gastroenterol Hepatol 18: 891-902, 2003.
39. Wang R. Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16: 1792-1798, 2002.
40. Whiteman M, Armstrong JS, Chu SH, Jia-Ling S, Wong BS, Cheung NS, Halliwell B, Moore PK. The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite "scavenger"? J Neurochem 90: 765-768, 2004.
41. World CJ, Yamawaki H, Berk BC. Thioredoxin in the cardiovascular system. J Mol Med 84: 997-1003, 2006.
42. Xu W, Neckers L. Targeting the molecular chaperone heat shock protein 90 provides a multifaceted effect on diverse cell signaling pathways of cancer cells. Clin Cancer Res 13: 1625-1629, 2007.
43. Yanada S, Saitoh Y, Kaneda Y, Miwa N. Cytoprotection by bcl-2 gene transfer against ischemic liver injuries together with repressed lipid peroxidation and increased ascorbic acid in livers and serum. J Cell Biochem 93: 857-870, 2004.
44. Yonezawa D, Sekiguchi F, Miyamoto M, Taniguchi E, Honjo M, Masuko T, Nishikawa H, Kawabata A. A protective role of hydrogen sulfide against oxidative stress in rat gastric mucosal epithelium. Toxicology 241: 11-18, 2007.
45. Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL. Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J 20: 2118-2120, 2006.
46. Zhang W, Wang M, Xie HY, Zhou L, Meng XQ, Shi J, Zheng S. Role of reactive oxygen species in mediating hepatic ischemia-reperfusion injury and its therapeutic applications in liver transplantation. Transplant Proc 39: 1332-1337, 2007.
47. Zhang Z, Huang H, Liu P, Tang C, Wang J. Hydrogen sulfide contributes to cardioprotection during ischemia-reperfusion injury by opening KATP channels. Can J Physiol Pharmacol 85: 1248-1253, 2007.
48. Zhao W, Zhang J, Lu Y, Wang R. The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener. EMBO J 20: 6008-6016, 2001.