Journal of Surgical Research
Volume 157, Issue 1 , Pages e71-e78 , November 2009

Cytoprotective Effects of Human Interleukin-10 Gene Transfer Against Necrosis and Apoptosis Induced by Hepatic Cold Ischemia/Reperfusion Injury

Received 9 January 2009

References 

  1. Pirenne J, Gunson B, Khaleef H, et al. Influence of ischemia-reperfusion injury on rejection after liver transplantation. Transplant Proc. 1997;29:366
  2. Howard TK, Klintmalm GB, Cofer JB, et al. The influence of preservation injury on rejection in the hepatic transplant recipient. Transplantation. 1990;49:103
  3. Fondevila C, Busuttil RW, Kupiec-Weglinski JW. Hepatic ischemia/reperfusion injury—a fresh look. Exp Mol Pathol. 2003;74:86
  4. Jaeschke H, Lemasters JJ. Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology. 2003;125:1246
  5. El-Gibaly AM, Scheuer C, Menger MD, et al. Improvement of rat liver graft quality by pifithrin-alpha-mediated inhibition of hepatocyte necrapoptosis. Hepatology. 2004;39:1553
  6. Gao W, Bentley RC, Madden JF, et al. Apoptosis of sinusoidal endothelial cells is a critical mechanism of preservation injury in rat liver transplantation. Hepatology. 1998;27:1652
  7. Natori S, Selzner M, Valentino KL, et al. Apoptosis of sinusoidal endothelial cells occurs during liver preservation injury by a caspase-dependent mechanism. Transplantation. 1999;68:89
  8. Kohli V, Selzner M, Madden JF, et al. Endothelial cell and hepatocyte deaths occur by apoptosis after ischemia reperfusion injury in the rat liver. Transplantation. 1999;67:1099
  9. Huet PM, Nagaoka MR, Desbiens G, et al. Sinusoidal endothelial cell and hepatocyte death following cold ischemia-warm reperfusion of the rat liver. Hepatology. 2004;39:1110
  10. Zhu J, Wang S, Bie P, et al. Apoptosis and regeneration of sinusoidal endothelial cells after extended cold preservation and transplantation of rat liver. Transplantation. 2007;84:1483
  11. de Waal Malefyt R, Abrams J, Bennett B, et al. Interleukin-10 (IL-10) inhibits cytokine synthesis by human monocytes: An autoregulatory role of IL-10 produced by monocytes. J Exp Med. 1991;174:1209
  12. Ding L, Shevach EM. IL-10 inhibits mitogen-induced T cell proliferation by selectively inhibiting macrophage costimulatory function. J Immunol. 1992;148:3133
  13. Fiorentino DF, Zlotnik A, Mosmann TR, et al. IL-10 inhibits cytokine production of activated macrophage. J Immunol. 1991;147:3815
  14. Cassatella MA, Meda L, Bonora S, et al. Interleukin 10 (IL-10) inhibits the release of proinflammatory cytokines from human polymorphonuclear leukocytes. Evidence for an autocrine role of tumor necrosis factor and IL-1 beta in mediating the production of IL-8 triggered by lipopolysaccharide. J Exp Med. 1993;178:2207
  15. Yoshidome H, Kato A, Edwards MJ, et al. Interleukin-10 suppresses hepatic ischemia/reperfusion injury in mice: Implications of a central role for nuclear factor kappaB. Hepatology. 1999;30:203
  16. Lee TS, Chau LY. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med. 2002;8:240
  17. Pahan K, Khan M, Singh I. interleukin-10 and interleukin-13 inhibit proinflammatory cytokine-induced ceramide production through the activation of phosphatidylinositol 3-kinase. J Neurochem. 2000;75:576
  18. Ke B, Shen XD, Zhai Y, et al. Heme oxygenase 1 mediates the immunomodulatory and antiapoptotic effects of interleukin 13 gene therapy in vivo and in vitro. Hum Gene Ther. 2002;13:1845
  19. Ke B, Shen XD, Lassman CR, et al. Cytoprotective and antiapoptotic effects of IL-13 in hepatic cold ischemia/reperfusion injury are heme oxygenase-1 dependent. Am J Transplant. 2003;3:1076
  20. Wissing KM, Morelon E, Legendre C, et al. A pilot trial of recombinant human interleukin-10 in kidney transplant recipients receiving OKT3 induction therapy. Transplantation. 1997;64:999
  21. Donckier V, Loi P, Closset J, et al. Preconditioning of donors with interleukin-10 reduces hepatic ischemia-reperfusion injury after liver transplantation in pigs. Transplantation. 2003;75:902
  22. Blazar BR, Taylor PA, Smith S, et al. Interleukin-10 administration decreases survival in murine recipients of major histocompatibility complex disparate donor bone marrow grafts. Blood. 1995;85:842
  23. Kamada N, Calne RY. A surgical experience with 530 liver transplant in the rat. Surgery. 1983;93:64
  24. Suzuki S, Toledo-Pereyra LH, Rodriguez FJ, et al. Neutrophil infiltration as an important factor in liver ischemia and reperfusion injury. Modulating effects of FK506 and cyclosporine. Transplantation. 1993;55:1265
  25. Hai S, Takemura S, Minamiyama Y, et al. Mitochondrial K(ATP) channel opener prevents ischemia-reperfusion injury in rat liver. Transplant Proc. 2005;37:428
  26. Dinant S, Veteläinen RL, Florquin S, et al. IL-10 attenuates hepatic I/R injury and promotes hepatocyte proliferation. J Surg Res. 2007;141:176
  27. Ke B, Shen XD, Tsuchihashi S, et al. Viral interleukin-10 gene transfer prevents liver ischemia-reperfusion injury: Toll-like receptor-4 and heme oxygenase-1 signaling in innate and adaptive immunity. Hum Gene Ther. 2007;18:355
  28. Lichtman SN, Lemasters JJ. Role of cytokines and cytokine-producing cells in reperfusion injury to the liver. Semin Liver Dis. 1999;19:171
  29. Mochida S, Arai M, Ohno A, et al. Oxidative stress in hepatocytes and stimulatory state of Kupffer cells after reperfusion differ between warm and cold ischemia in rats. Liver. 1994;14:234
  30. Green DR. Apoptotic pathways: Paper wraps stone blunts scissors. Cell. 2000;102:1
  31. Selzner M, Rüdiger HA, Sindram D, et al. Mechanisms of ischemic injury are different in the steatotic and normal rat liver. Hepatology. 2000;32:1280
  32. Susin SA, Zamzami N, Castedo M, et al. The central executioner of apoptosis: Multiple connections between protease activation and mitochondria in Fas/APO-1/CD95- and ceramide-induced apoptosis. J Exp Med. 1997;186:25
  33. Marzo I, Brenner C, Zamzami N, et al. The permeability transition pore complex: A target for apoptosis regulation by caspases and bcl-2-related proteins. J Exp Med. 1998;187:1261
  34. Kluck RM, Bossy-Wetzel E, Green DR, et al. The release of cytochrome c from mitochondria: A primary site for Bcl-2 regulation of apoptosis. Science. 1997;275:1132
  35. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat Med. 2000;6:513
  36. Weiss JN, Korge P, Honda HM, et al. Role of the mitochondrial permeability transition in myocardial disease. Circ Res. 2003;93:292
  37. Kuznetsov AV, Schneeberger S, Seiler R, et al. Mitochondrial defects and heterogeneous cytochrome c release after cardiac cold ischemia and reperfusion. Am J Physiol Heart Circ Physiol. 2004;286:H1633
  38. Tatsumi T, Shiraishi J, Keira N, et al. Intracellular ATP is required for mitochondrial apoptotic pathways in isolated hypoxic rat cardiac myocytes. Cardiovasc Res. 2003;59:428
  39. Hoglen NC, Anselmo DM, Katori M, et al. A caspase inhibitor, IDN-6556, ameliorates early hepatic injury in an ex vivo rat model of warm and cold ischemia. Liver Transpl. 2007;13:361
  40. Rentsch M, Kienle K, Mueller T, et al. Adenoviral bcl-2 transfer improves survival and early graft function after ischemia and reperfusion in rat liver transplantation. Transplantation. 2005;80:1461
  41. Shiraishi J, Tatsumi T, Keira N, et al. Important role of energy-dependent mitochondrial pathways in cultured rat cardiac myocyte apoptosis. Am J Physiol Heart Circ Physiol. 2001;281:H1637
  42. Fang Y, Sharp GC, Braley-Mullen H. Interleukin-10 promotes resolution of granulomatous experimental autoimmune thyroiditis. Am J Pathol. 2008;172:1591
  43. Kokura S, Yoshida N, Ishikawa T, et al. Interleukin-10 plasmid DNA inhibits subcutaneous tumor growth of Colon 26 adenocarcinoma in mice. Cancer Lett. 2005;218:171
  44. Kirkby KA, Adin CA. Products of heme oxygenase and their potential therapeutic applications. Am J Physiol Renal Physiol. 2006;290:F563
  45. Otterbein LE, Soares MP, Yamashita K, et al. Heme oxygenase-1: Unleashing the protective properties of heme. Trends Immunol. 2003;24:449
  46. Blydt-Hansen TD, Katori M, Lassman C, et al. Gene transfer-induced local heme oxygenase-1 overexpression protects rat kidney transplants from ischemia/reperfusion injury. J Am Soc Nephrol. 2003;14:745
  47. Drechsler Y, Dolganiuc A, Norkina O, et al. Heme oxygenase-1 mediates the anti-inflammatory effects of acute alcohol on IL-10 induction involving p38 MAPK activation in monocytes. J Immunol. 2006;177:2592

PII: S0022-4804(09)00086-9

doi: 10.1016/j.jss.2009.03.004

Journal of Surgical Research
Volume 157, Issue 1 , Pages e71-e78 , November 2009

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