Hydrogen sulfide augments survival signals in warm ischemia and reperfusion of the mouse liver

Surgery Today

Volumn 45, Issue 7, 2015, Pages 892-903

  Shimada, Shingo ^a   Fukai, Moto ^a   Wakayama, Kenji ^a   Ishikawa, Takahisa ^a   Kobayashi, Nozomi ^a   Kimura, Taichi ^a   Yamashita, Kenichiro ^a   Kamiyama, Toshiya ^a   Shimamura, Tsuyoshi ^b   Taketomi, Akinobu ^a   Todo, Satoru ^c  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b HOKKAIDO UNIVERSITY HOSPITAL   (Japan)

^c St Maria Hospital affiliated Laboratory   (Japan)

Author keywords

Hydrogen sulfide; Ischemia; Liver; Mouse; Reperfusion

Indexed keywords

ALANINE AMINOTRANSFERASE; CD40 LIGAND; GAMMA INTERFERON; HO 1 PROTEIN; HYDROGEN SULFIDE; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; PROTEIN; SODIUM CHLORIDE; SODIUM HYDROGEN SULFIDE; THIOREDOXIN 1; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; CYTOKINE; PROTECTIVE AGENT; SODIUM BISULFIDE; SULFIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; INFLAMMATION; LIPID PEROXIDATION; LIVER; LIVER ISCHEMIA; MALE; MOUSE; NONHUMAN; PHOSPHORYLATION; REPERFUSION INJURY; SCORING SYSTEM; SERUM; SURVIVAL; TISSUE INJURY; UPREGULATION; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; DRUG EFFECTS; EVALUATION STUDY; IMMUNOHISTOCHEMISTRY; METABOLISM; OXIDATIVE STRESS; REPERFUSION; VASCULARIZATION; WARM ISCHEMIA; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BIOMARKERS; BLOTTING, WESTERN; CYTOKINES; IMMUNOHISTOCHEMISTRY; LIVER; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; PROTECTIVE AGENTS; REPERFUSION; REPERFUSION INJURY; SULFIDES; WARM ISCHEMIA;

EID: 84930867465     PISSN: 09411291     EISSN: 14362813     Source Type: Journal    
DOI: 10.1007/s00595-014-1064-4     Document Type: Article

References (49)

1. Monbaliu D, Pirenne J, Talbot D. Liver transplantation using donation after cardiac death donors. J Hepatol. 2012;56:474–85.
2. Vollmar B, Menger MD. The hepatic microcirculation: mechanistic contributions and therapeutic targets in liver injury and repair. Physiol Rev. 2009;89:1269–339.
3. Zwacka RM, Zhou W, Zhang Y, Darby CJ, Dudus L, Halldorson J, et al. Redox gene therapy for ischemia/reperfusion injury of the liver reduces AP1 and NF-kappaB activation. Nat Med. 1998;4:698–704.
4. Abu-Amara M, Yang SY, Tapuria N, Fuller B, Davidson B, Seifalian A. Liver ischemia/reperfusion injury: processes in inflammatory networks—a review. Liver Transpl. 2010;16:1016–32.
5. Hu Y, Chen X, Pan TT, Neo KL, Lee SW, Khin ES, et al. Cardioprotection induced by hydrogen sulfide preconditioning involves activation of ERK and PI3 K/Akt pathways. Pflugers Arch. 2008;455:607–16.
6. Tsang A, Hausenloy DJ, Mocanu MM, Yellon DM. Postconditioning: a form of “modified reperfusion” protects the myocardium by activating the phosphatidylinositol 3-kinase-Akt pathway. Circ Res. 2004;95:230–2.
7. Noshita N, Lewen A, Sugawara T, Chan PH. Evidence of phosphorylation of Akt and neuronal survival after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab. 2001;21:1442–50.
8. King AL, Lefer DJ. Cytoprotective actions of hydrogen sulfide in ischaemia-reperfusion injury. Exp Physiol. 2011;96(9):840–6.
9. Calvert JW, Jha S, Gundewar S, Elrod JW, Ramachandran A, Pattillo CB, et al. Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res. 2009;105:365–74.
10. Hunter JP, Hosgood SA, Patel M, Rose R, Read K, Nicholson ML. Effects of hydrogen sulphide in an experimental model of renal ischaemia-reperfusion injury. Br J Surg. 2012;99:1665–71.
11. Fu Z, Liu X, Geng B, Fang L, Tang C. Hydrogen sulfide protects rat lung from ischemia-reperfusion injury. Life Sci. 2008;82:1196–202.
12. Henderson PW, Weinstein AL, Sohn AM, Jimenez N, Krijgh DD, Spector JA. Hydrogen sulfide attenuates intestinal ischemia-reperfusion injury when delivered in the post-ischemic period. J Gastroenterol Hepatol. 2010;25:1642–7.
13. Wang D, Ma Y, Li Z, Kang K, Sun X, Pan S, et al. The role of AKT1 and autophagy in the protective effect of hydrogen sulphide against hepatic ischemia/reperfusion injury in mice. Autophagy. 2012;8:954–62.
14. Jha S, Calvert JW, Duranski MR, Ramachandran A, Lefer DJ. Hydrogen sulfide attenuates hepatic ischemia-reperfusion injury: role of antioxidant and antiapoptotic signaling. Am J Physiol Heart Circ Physiol. 2008;295:H801–6.
15. Kang K, Zhao M, Jiang H, Tan G, Pan S, Sun X. Role of hydrogen sulfide in hepatic ischemia-reperfusion-induced injury in rats. Liver Transpl. 2009;15:1306–14.
16. Bos EM, Snijder PM, Jekel H, Weij M, Leemans JC, van Dijk MC, et al. Beneficial effects of gaseous hydrogen sulfide in hepatic ischemia/reperfusion injury. Transpl Int. 2012;25:897–908.
17. Kis A, Yellon DM, Baxter GF. Second window of protection following myocardial preconditioning: an essential role for PI3 kinase and p70S6 kinase. J Mol Cell Cardiol. 2003;35:1063–71.
18. Ban K, Kozar RA. Protective role of p70S6 K in intestinal ischemia/reperfusion injury in mice. PLoS One. 2012;7:e41584.
19. Lowicka E, Beltowski J. Hydrogen sulfide (H2S)—the third gas of interest for pharmacologists. Pharmacological reports. 2007;59:4–24.
20. Fukai M, Hayashi T, Yokota R, Shimamura T, Suzuki T, Taniguchi M, et al. Lipid peroxidation during ischemia depends on ischemia time in warm ischemia and reperfusion of rat liver. Free Radic Biol Med. 2005;38:1372–81.
21. Yadav SS, Gao W, Harland RC, Clavien PA. A new and simple technique of total hepatic ischemia in the mouse. Transplantation. 1998;65:1433–6.
22. Suzuki S, Nakamura S, Koizumi T, Sakaguchi S, Baba S, Muro H, et al. The beneficial effect of a prostaglandin I2 analog on ischemic rat liver. Transplantation. 1991;52:979–83.
23. Szabo C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov. 2007;6:917–35.
24. Nakamitsu A, Hiyama E, Imamura Y, Matsuura Y, Yokoyama T. Kupffer cell function in ischemic and nonischemic livers after hepatic partial ischemia/reperfusion. Surg Today. 2001;31:140–8.
25. Schlegel A, Graf R, Clavien PA, Dutkowski P. Hypothermic oxygenated perfusion (HOPE) protects from biliary injury in a rodent model of DCD liver transplantation. J Hepatol. 2013;59:984–91.
26. Chen Y, Wood KJ. Interleukin-23 and TH17 cells in transplantation immunity: does 23 + 17 equal rejection? Transplantation. 2007;84:1071–4.
27. Husted TL, Blanchard J, Schuster R, Shen H, Lentsch AB. Potential role for IL-23 in hepatic ischemia/reperfusion injury. Inflamm Res. 2006;55:177–8.
28. Bhogal RH, Weston CJ, Curbishley SM, Adams DH, Afford SC. Activation of CD40 with platelet derived CD154 promotes reactive oxygen species dependent death of human hepatocytes during hypoxia and reoxygenation. PLoS One. 2012;7:e30867.
29. Ke B, Shen XD, Ji H, Kamo N, Gao F, Freitas MC, et al. HO-1-STAT3 axis in mouse liver ischemia/reperfusion injury: regulation of TLR4 innate responses through PI3 K/PTEN signaling. J Hepatol. 2011;56:359–66.
30. Shen X, Wang Y, Gao F, Ren F, Busuttil RW, Kupiec-Weglinski JW, et al. CD4 T cells promote tissue inflammation via CD40 signaling without de novo activation in a murine model of liver ischemia/reperfusion injury. Hepatology. 2009;50:1537–46.
31. Yokota R, Fukai M, Shimamura T, Suzuki T, Watanabe Y, Nagashima K, et al. A novel hydroxyl radical scavenger, nicaraven, protects the liver from warm ischemia and reperfusion injury. Surgery. 2000;127:661–9.
32. Ota T, Hirai R, Urakami A, Soga H, Nawa S, Shimizu N. Endothelin-1 levels in portal venous blood in relation to hepatic tissue microcirculation disturbance and hepatic cell injury after ischemia/reperfusion. Surg Today. 1997;27:313–20.
33. 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.
34. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, et al. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci USA. 2007;104:15560–5.
35. Kimura Y, Goto Y, Kimura H. Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid Redox Signal. 2010;12:1–13.
36. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol. 2010;80:1895–903.
37. Kim YC, Yamaguchi Y, Kondo N, Masutani H, Yodoi J. Thioredoxin-dependent redox regulation of the antioxidant responsive element (ARE) in electrophile response. Oncogene. 2003;22:1860–5.
38. Akamatsu Y, Haga M, Tyagi S, Yamashita K, Graça-Souza AV, Ollinger R, et al. Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. Faseb J. 2004;18:771–2.
39. Wei Y, Chen P, de Bruyn M, Zhang W, Bremer E, Helfrich W. Carbon monoxide-releasing molecule-2 (CORM-2) attenuates acute hepatic ischemia reperfusion injury in rats. BMC Gastroenterol. 2010;10:42.
40. Watanabe R, Nakamura H, Masutani H, Yodoi J. Anti-oxidative, anti-cancer and anti-inflammatory actions by thioredoxin 1 and thioredoxin-binding protein-2. Pharmacol Ther. 2010;127:261–70.
41. 2S protects hippocampal neurons from anoxia-reoxygenation through cAMP-mediated PI3 K/Akt/p70S6 K cell-survival signaling pathways. J Mol Neurosci. 2011;43:453–60.
42. Si R, Tao L, Zhang HF, Yu QJ, Zhang R, Lv AL, et al. Survivin: a novel player in insulin cardioprotection against myocardial ischemia/reperfusion injury. J Mol Cell Cardiol. 2011;50:16–24.
43. Koh PO. Melatonin prevents hepatic injury-induced decrease in Akt downstream targets phosphorylations. J Pineal Res. 2011;51:214–9.
44. Debonera F, Wang G, Xie J, Que X, Gelman A, Leclair C, et al. Severe preservation injury induces Il-6/STAT3 activation with lack of cell cycle progression after partial liver graft transplantation. Am J Transplant. 2004;4:1964–71.
45. Taub R. Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol. 2004;5:836–47.
46. Zhang Q, Fu H, Zhang H, Xu F, Zou Z, Liu M, et al. Hydrogen sulfide preconditioning protects rat liver against ischemia/reperfusion injury by activating Akt-GSK-3β signaling and inhibiting mitochondrial permeability transition. PLoS One. 2013;8:e74422.
47. 2S administration in relation to its toxicity and effects on breathing. Am J Physiol Regul Integr Comp Physiol. 2013;305:R630–8.
48. Vitvitsky V, Kabil O, Banerjee R. High turnover rates for hydrogen sulfide allow for rapid regulation of its tissue concentrations. Antioxid Redox Signal. 2012;17:22–31.
49. Balaban CL, Rodriguez JV, Guibert EE. Delivery of the bioactive gas hydrogen sulfide during cold preservation of rat liver: effects on hepatic function in an ex vivo model. Artif Organs. 2011;35:508–15.