Heme oxygenase-1 improves the survival of discordant cardiac xenograft through its anti-inflammatory and anti-apoptotic effects

Pediatric Transplantation

Volumn 11, Issue 8, 2007, Pages 850-859

  Zhen Wei, Xia ^a   Jian Le, Sun ^a   Qi, Qi ^a   Wen Wei, Zhong ^a   Xue Hong, Zhang ^a   Zi Li, Zhang ^b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Apoptosis; Cardiac xenotransplantation; Discordant; Heme oxygenase 1; Inflammation

Indexed keywords

CD40 LIGAND; COMPLEMENT COMPONENT C3; HEME OXYGENASE 1; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M ANTIBODY; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CELL SWELLING; CONCENTRATION RESPONSE; CONTROLLED STUDY; EDEMA; ENZYME INDUCTION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; GRAFT RECIPIENT; GRAFT SURVIVAL; HEART MUSCLE CELL; HEART TRANSPLANTATION; HUMAN; HUMAN CELL; INTERSTITIUM; LYMPHOCYTIC INFILTRATION; MALE; NONHUMAN; PROTEIN FUNCTION; RAT; SPLEEN; SURVIVAL TIME; THROMBOGENESIS; UPREGULATION; XENOGRAFT; XENOTRANSPLANTATION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CD40 LIGAND; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GRAFT REJECTION; GRAFT SURVIVAL; HEART TRANSPLANTATION; HEME OXYGENASE-1; IN SITU NICK-END LABELING; MALE; MYOCARDITIS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SPECTROPHOTOMETRY; TRANSCRIPTION, GENETIC; TRANSPLANTATION, HETEROLOGOUS;

EID: 35848961693     PISSN: 13973142     EISSN: 13993046     Source Type: Journal    
DOI: 10.1111/j.1399-3046.2007.00701.x     Document Type: Article

References (42)

1. Shiraishi F, Curtis LM, Truong L, et al. Heme oxygenase-1 gene ablation or expression modulates cisplatin-induced renal tubular apoptosis. Am J Physiol Renal Physiol 2000 : 278 : F726 736.
2. Choi AM. Heme oxygenase-1 protects the heart. Circ Res 2001 : 89 : 105 107.
3. Ryter SW, Choi AM. Heme oxygenase-1: Redox regulation of a stress protein in lung and cell culture models. Antioxid Redox Signal 2005 : 7 : 80 91.
4. Song R, Mahidhara RS, Liu F, Ning W, Otterbein LE, Choi AM. Carbon monoxide inhibits human airway smooth muscle cell proliferation via mitogen-activated protein kinase pathway. Am J Respir Cell Mol Biol 2002 : 27 : 603 610.
5. Almolki A, Taille C, Martin GF, et al. Heme oxygenase attenuates allergen-induced airway inflammation and hyperreactivity in guinea pigs. Am J Physiol Lung Cell Mol Physiol 2004 : 287 : L26 34.
6. Brenner P, Reichenspurner H, Schmoeckel M, et al. Prevention of hyperacute xenograft rejection in orthotopic xenotransplantation of pig hearts into baboons using immunoadsorption of antibodies and complement factors. Transpl Int 2000 : 13 : S508 517.
7. Holzknecht ZE, Kuypers KL, Plummer TB, et al. Apoptosis and cellular and activation in the pathogenesis of acute vascular rejection. Circ Res 2002 : 91 : 1135 1141.
8. Katori M, Busuttil RW, Kupiec-Weglinski JW. Heme oxygenase-1 system in organ transplantation. Transplantation 2002 : 74 : 905 912.
9. Dedja A, Dall'Olmo L, Cadrobbi R, et al. Heterotopic cardiac xenotransplantation in rodents: Report of a refined technique in a hamster-to-rat model. Microsurgery 2005 : 25 : 227 234.
10. Gock H, Salvaris E, Murray-Segal L, et al. Hyperacute rejection of vascularized heart transplants in BALB/c Gal knockout mice. Xenotransplantation 2000 : 7 : 237 246.
11. Suhr BD, Guzman-Paz M, Apasova EP, Matas AJ, Dalmasso AP. Induction of accommodation in the hamster-to-rat model requires inhibition of the membrane attack complex of complement. Transplant Proc 2000 : 32 : 976.
12. Lin Y, Soares MP, Sato K, et al. Rejection of cardiac xenografts by CD4+ or CD8+ T cells. J Immunol 1999 : 162 : 1206 1214.
13. Grosser N, Hemmerle A, Berndt G, et al. The antioxidant defense protein heme oxygenase 1 is a novel target for statins in endothelial cells. Free Radic Biol Med 2004 : 37 : 2064 2071.
14. Sato K, Balla J, Otterbein L, et al. Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants. J Immunol 2001 : 166 : 4185 4194.
15. Sakakibara N, Wolf P, Kriett J, Kapelanski DP, Jamieson SW. Cardiac xenotransplantation into complement 5-deficient mice. Transplant Proc 1996 : 28 : 689 690.
16. Triponez F, Oberholzer J, Morel P, et al. Xenogeneic islet re-transplantation in mice triggers an accelerated, species-specific rejection. Immunology 2000 : 101 : 548 554.
17. Souza AI, Felkin LE, Mccormack AM, et al. Sequential expression of three known protective genes in cardiac biopsies after transplantation. Transplantation 2005 : 79 : 584 590.
18. Xia ZW, Zhong WW, Xu LQ, et al. Heme oxygenase-1-mediated CD4+CD25high regulatory T cells suppress allergic airway inflammation. J Immunol 2006 : 177 : 5936 45.
19. Soares MP, Lin Y, Anrather J, et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med 1998 : 9 : 1073 1077.
20. Yamashita K, Ollinger R, Mcdaid J, et al. Heme oxygenase-1 is essential for and promotes tolerance to transplanted organs. FASEB J 2006 : 20 : 776 778.
21. Kushida T, Li Volti G, Quan S, Goodman A, Abraham NG. Role of human heme oxygenase-1 in attenuating TNF-a-mediated inflammation injury in endothelial cells. J Cell Biochem 2002 : 87 : 377 385.
22. Kushida T, Livolti G, Goodman AI, Abraham NG. TNF-a-mediated cell death is attenuated by retrovirus delivery of human heme oxygenase-1 gene into human microvessel endothelial cells. Transplant Proc 2002 : 34 : 2973 2978.
23. Tabata T, De Perrot M, Keshavjee S, Liu M, Downey GP, Waddell TK. Accommodation after lung enografting from hamster to rat. Transplantation 2003 : 75 : 607 612.
24. Ke B, Shen XD, Zhai Y, et al. Heme oxygenase-1 gene transfer prevents CD95/FasL-mediated apoptosis and improves liver allograft survival via carbon monoxide signaling pathway. Transplant Proc 2002 : 34 : 1465 1466.
25. Christl AR, Kazuhide F. Tumor necrosis factor-α, heme oxygenase-1 and manganese superoxide dismutase immunostaining of vessels and perivascular brain cells provides evidence for cyclic activation and inactivation of brain vessel segments. International Congress Series 2002 : 1235 : 493 500.
26. Abdel-Aziz MT, El-Asmar MF, El-Miligy D, et al. Retrovirus-mediated human heme oxygenase-1 (HO-1) gene transfer into rat endothelial cells: The effect of HO-1 inducers on the expression of cytokine. J Biochem Cell Biol 2003 : 35 : 324 332.
27. Fujita T, Toda K, Karimova A, et al. Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fibrinolysis. Nat Med 2001 : 7 : 598 604.
28. Baranano DE, Rao M, Ferris CD, Snyder SH. Biliverdin reductase: A major physiologic cytoprotectant. Proc Natl Acad Sci USA 2002 : 99 : 16093 16098.
29. Nakao A, Neto JS, Kanno S, et al. Protection against ischemia/reperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am J Transplant 2005 : 5 : 282 291.
30. Lederman S. The role of CD154 (CD40-ligand) in costimulation. Transplant Proc 2001 : 33 : 202 206.
31. Yamada A, Sayeghthe MH. CD154-CD40 costimulatory pathway in transplantion. Transplantation 2002 : 73 : S36 39.
32. Shen XD, KE B, Zhai Y, et al. CD154-CD40 T-cell costimulation pathway is required in the mechanism of hepatic ischemia/reperfusion injury, and its blockade facilitates and depends on heme oxygenase-1 mediated cytoprotection. Transplantation 2002 : 74 : 315 319.
33. Xu H, Arnaud F, Tadaki DK, Burkly LC, Harlan DM, Kirk AD. Human platelets activate porcine endothelial cells through a CD154-dependent pathway. Transplantation 2001 : 72 : 1858 1861.
34. Zheng XX, Schachter AD, Vasconcellos L, et al. Increased CD40 ligand gene expression during human renal and murine islet allograft rejection. Transplantation 1998 : 65 : 1512 1515.
35. Jones ND, Van Maurik A, Hara M, et al. CD40-CD40 ligand-independent activation of CD8+ T cells can trigger allograft rejection. J Immunol 2000 : 165 : 1111 1118.
36. Kirk AD, Burkly LC, Batty DS, et al. Treatment with humanized monoclonal antibody against CD154 prevents acute renal allograft rejection in nonhuman primates. Nat Med 1999 : 5 : 686 693.
37. Kenyon NS, Chatzipetrou M, Masetti M, et al. Long-term survival and function of intrahepatic islet allografts in rhesus monkeys treated with humanized anti-CD154. Proc Natl Acad Sci USA 1999 : 96 : 8132 8137.
38. Guillot C, Guillonneau C, Mathieu P, et al. Prolonged blockade of CD40-CD40 ligand interactions by gene transfer of CD40Ig results in long-term heart allograft survival and donor-specific hyporesponsiveness, but does not prevent chronic rejection. J Immunol 2002 : 168 : 1600 1609.
39. Wang N, Lee JM, Tobiasch E, et al. Induction of xenograft accommodation by modulation of elicited antibody responses. Transplantation 2002 : 74 : 334 345.
40. Lin Y, Soares MP, Sato K, et al. Long-term survival of hamster hearts in presensitized rats. J Immunol 2000 : 164 : 4883 4892.
41. Saadi S, Takahashi T, Holzknecht RA, Platt JL. Pathways to acute humoral rejection. Am J Pathol 2004 : 164 : 1073 1080.
42. Schuurman HJ, Pino-Chavez G, Phillips MJ, Thomas L, White DJG, Cozzi E. Incidence of hyperacute rejection in pig-to-primate transplantation using organs from hDAF-transgenic donors. Transplantation 2002 : 73 : 1146 1151.