Heme Oxygenase-1 Overexpression Protects Rat Livers from Ischemia/Reperfusion Injury with Extended Cold Preservation

American Journal of Transplantation

Volumn 1, Issue 2, 2001, Pages 121-128

  Kato, Hirohisa ^a   Amersi, Farin ^a   Buelow, Roland ^b   Melinek, Judy ^a   Coito, Ana J ^a   Ke, Bibo ^a   Busuttil, Ronald W ^a   Kupiec Weglinski, Jerzy W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GENZYME CORPORATION   (United States)

Author keywords

Heme oxygenase; Ischemia reperfusion injury; Liver

Indexed keywords

HEME OXYGENASE; HEME OXYGENASE 1; PROTOPORPHYRIN; PROTOPORPHYRIN COPPER; PROTOPORPHYRIN ZINC;

ANIMAL; ARTICLE; COLD; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETICS; GRAFT SURVIVAL; ISOGRAFT; KINETICS; LIVER; LIVER TRANSPLANTATION; METHODOLOGY; ORGAN PRESERVATION; PHYSIOLOGY; RAT; REPERFUSION INJURY; TIME; VASCULARIZATION;

ANIMALS; COLD; GRAFT SURVIVAL; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; KINETICS; LIVER; LIVER TRANSPLANTATION; ORGAN PRESERVATION; PROTOPORPHYRINS; RATS; REPERFUSION INJURY; TIME FACTORS; TRANSPLANTATION, ISOGENEIC;

EID: 0035401243     PISSN: 16006135     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-6143.2001.10205.x     Document Type: Article

References (42)

1. NIH Consensus Development Conference Statement. Liver transplantation. Hepatology 1984; 4; 1075.
2. D'Allesandro AM, Kalayoglu M, Sollinger HW et al. The predictive value of donor liver biopsies for the development of primary nonfunction after orthotopic liver transplantation. Transplantation 1991; 51: 157-163.
3. Marino IR, Doyle HR, Aldrighetti L et al. Effect of donor age and sex on the outcome of liver transplantation. Hepatology 1995; 22: 1754-1762.
4. Figueras J, Busquets J, Grande L et al. The deleterious effect of donor high plasma sodium and extended preservation in liver transplantation: a multivariate analysis. Transplantation 1996; 61: 410-413.
5. Iu S, Harvey PRC, Makowka L et al. Markers of allograft viability in the rat. Transplantation 1987; 44: 562-569.
6. Howard T, Klintmalm GB, Coulter JB et al. The influence of preservation injury in the hepatic transplant recipient. Transplantation 1990; 49: 103-107.
7. Todo S, Nery J, Yunaga K et al. Extended preservation of human liver grafts with UW solution. JAMA 1989; 261: 711-715.
8. Ploeg RJ, D'Allesandro AM, Knechtle SJ et al. Risk factors for primary dysfunction after liver transplantation - a multivariate analysis. Transplantation 1993; 55: 807-813.
9. Greig PD, Woolf GM, Sinclair SB. Treatment of primary liver graft nonfunction with prostaglandin E1. Transplantation 1989; 48: 447-453.
10. Farmer DG, Amersi F, Kupiec-Weglinski JW, Busuttil RW. Current status of ischemia and reperfusion injury in the liver. Transplant Rev 2000; 14: 106-126.
11. Jaeschke H, Farhood A. Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol 1991; 260: G355-G362.
12. Shiratori Y, Kiriyama H, Fukushi Y et al. Modulation of ischemia-reperfusion induced hepatic injury by Kupffer cells. Dig Dis Sci 1994; 39: 1265-1272.
13. Attala SL, Toledo-Pereyra LH, Mackenzie GH et al. Influence of oxygen-derived free radicals on ischemic livers. Transplantation 1985; 40: 584-589.
14. Lemasters JJ, Thurman RG. Hypoxia and reperfusion injury to the liver. Prog Liver Dis 1994; 11: 85.
15. Lemasters JJ, Bunzendahl H, Thurman RG. Reperfusion injury to donor livers stored for transplantation. Liver Transpl Surg 1995; 1: 124-138.
16. Grace PA. Ischemia-reperfusion injury. Br J Surg 1994; 81: 637.
17. Maines MD. Heme Oxygenase: Clinical Applications and Functions. Boca Raton, FL: CRC Press; 1992.
18. Woo S, Iyer S, Cornejo MC et al. Stress protein-induced immunosuppression; inhibition of cellular immune effector function following overexpression of heme oxygenase (HSP 32). Transpl Immunol 1998; 6: 84-93.
19. Hancock WW, Buelow R, Sayegh MH, Turka LA. Antibody-induced transplant arteriosclerosis is prevented by graft expression of anti-oxidant and anti-apoptotic genes. Nat Med 1998; 4: 1392-1396.
20. Amersi F, Buelow R, Kato H et al. Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury. J Clin Invest 1999; 61: 1631-1639.
21. Kamada N, Calne Y. Orthotopic liver transplantation in the rat: technique using cuff for portal vein anastamosis and biliary drainage. Transplantation 1979; 28: 47-50.
22. International Banff Schema Consensus Worksheet. The Third Banff Congress on Allograft Pathology June 21-25, 1995.
23. Suzuki S, Teledo-Pereyra LH, Rodriguez FJ, Cejalvo O. Neutrophil infiltration as an important factor in liver ischemia and reperfusion injury. Transplantation 1993; 55: 1265-1272.
24. Coito AJ, Binder J, Brown LF et al. Anti-TNF-α antibody treatment downregulates the expression of fibronectin and decreases cellular infiltration of cardiac allografts in rats. J Immunol 1995; 154: 2949-2958.
25. Furukawa H, Todo S, Imventarazo O et al. Effects of cold ischemia time of the early outcome of human hepatic allografts preserved with University of Wisconsin solution. Transplantation 1991; 51: 1000-1004.
26. Nuno J, Cuervas V, Vicente E et al. Prolonged graft cold ischemia: a risk factor for early bacterial and fungal infections in liver transplant recipients. Transplant Proc 1993; 25: 3031-3032.
27. McKeown CMB, Edwards V, Phillips MJ et al. Sinusoidal lining cell damage: the critical injury in cold preservation of liver allografts in the rat. Transplantation 1988; 46: 178-191.
28. Squiers EC, Bruch D, Buelow R, Tice DG. Pretreatment of small bowel isograft donors with cobalt-protoporphyrin decreases preservation injury. Transplant Proc 1999; 311: 585-589.
29. DeBryne LA, Magee JC, Buelow R, Bromberg J. Gene transfer of immunomodulatory peptides correlates with heme oxygenase-1 induction and enhanced allograft survival. Transplantation 2000; 69: 120-128.
30. Soares MD, Lun Y, Anrather J et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med 1998; 4: 1073-1077.
31. Otterbein LE, Sylvester SL, Choi AMK. Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1. Am J Respir Cell Mol Biol 1995: 13: 595-602.
32. Haga Y, c MA, Kay D, Zetterman RK. Intracellular administration of unconjugated bilirubin inhibits phytohemagglutinin-induced proliferation and interleukin-1 production of human lymphocytes. Dig Dis Sci 1996; 41: 1468-1474.
33. Nagakami T, Toyumura K, Kinoshita T, Morisawa S. A beneficial role of bile pigments as an endogenous tissue protector. Anti-complement effects of biliverdin and conjugated bilirubin. Biochem Biophys Acta 1993; 1158: 189-193.
34. Haga Y, Tempero MA, Zetterman RK. Unconjugated bilirubin inhibits in vitro major histocompatibility complex-unrestricted cytotoxicity in human lymphocytes. Biochem Biophys Acta 1996; 1316: 29-34.
35. Brune B, Ulrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol Pharmacol 1987; 32: 492-504.
36. Otterbein LE, Bach FH, Alam J et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000; 6: 422-428.
37. Maines MD. The heme oxygenase system. A regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997; 37: 517-554.
38. Wang J, Rousseau DL, Abu-Soud HM, Stuehr DJ. Heme coordination of NO in NO synthase. Proc Natl Acad Sci USA 1994; 91: 10512-10516.
39. Rannen BH, Kohler N, Hole B, Bauer M, Clemens SG, Geiger KK. Protective role of endogenous carbon monoxide in hepatic microcirculatory dysfunction after hemorrhagic shock in rat. J Clin Invest 1998; 102: 1220-1228.
40. Stocker R, Yamamoto Y, McDonagh F et al. Bilirubin is an antioxidant of possible physiologic importance. Science 1987; 235: 1043-1046.
41. Nagakami T, Toyomura K, Kinoshita T, Morisawa S. A beneficial role of bile pigments as an endogenous tissue protector: anti-complement effects of biliverdin and conjugated bilirubin. Biochem Biophys Acta 1993; 1158: 189-193.
42. Neuzil J, Stocker R. Free and albumin bound bilirubin are efficient antioxidants for α-tocopherol inhibiting plasma and low density lipid peroxidation. J Biol Chem 1994; 269: 16712-16719.