Acute vascular rejection/delayed xenograft rejection and consumptive coagulopathy in xenotransplantation

Current Opinion in Organ Transplantation

Volumn 8, Issue 1, 2003, Pages 76-82

  Robson, Simon C ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 2942639459     PISSN: 10872418     EISSN: 15317013     Source Type: Journal    
DOI: 10.1097/00075200-200303000-00014     Document Type: Review

References (84)

1. Cooper DKC, Gollackner B, Sachs DH: Will the pig solve the transplantation backlog? [review]. Ann Rev Medicine 2002, 53:133-147.
2. Cooper DKC, Gollackner B, Knosalla C, et al.: Xenotransplantation - how far have we come? [review]. Transplant Immunol 2002, 9:251-256.
3. Dorling A: Clinical xenotransplantation: Pigs might fly [review]? Amer J Transpl 2002, 2:695-700.
4. Sachs DH, Sykes M, Robson SC, et al.: Xenotransplantation [review]. Adv Immunol 2001, 79:129-223.
5. Bach FH, Winkler H, Ferran C, et al.: Delayed xenograft rejection [review]. Immunol Today 1996, 17:379-384.
6. Bach FH, Robson SC, Ferran C, et al.: Endothelial cell activation and thromboregualtion during xenograft rejection [review]. Immunol Rev 1994, 141:5-30.
7. Platt JL, Lin SS, McGregor CGA: Acute vascular rejection [review]. Xenotransplantation 1998, 5:169-175.
8. Robson S, Schulte am Esch II J, et al.: Factors in xenograft rejection. Ann NY Acad Sciences 1999, 875:261-276.
9. Rosenberg JC, Broersma RJ, Bullemer G, et al.: relation of platelets, blood coagulation, and fibrinolysis to hyperacute rejection of renal xenografts. Transplantation 1969, 8:152-161.
10. Broersma RJ, Bullemer GD, Rosenberg JC, et al.: Coagulation changes in hyperacute rejection of renal xenografts. Thromb Diath Haemorrh Suppl 1969, 36:333-340.
11. Breimer ME, Bjorck S, Svalander CT, et al.: Extracorporeal (ex vivo) connection of pig kidneys to humans. Clinical data and studies of platelet destruction. Xenotransplantation 1996, 3:328-339.
12. Collins BH, Chari RS, Magee JC, et al.: Immunopathology of porcine livers perfused with blood of humans with fulminant hepatic failure. Transpl Proc 1995, 27:280-281.
13. Zaidi A, Schmoeckel M, Bhatti F, et al.: Life-supporting pig-to-primate renal xenotransplantation using genetically modified donors. Transplantation 1998, 65:1584-1590.
14. Schmoeckel M, Bhatti FNK, Zaidi A, et al.: Orthotopic heart transplantation in a transgenic pig-to-primate model. Transplantation 1998, 65:1570-1577.
15. Ierino FL, Kozlowski T, Siegel JB, et al.: Disseminated intravascular coagulation in association with the delayed rejection of pig-to-baboon renal xenografts. Transplantation 1998, 66:1439-1450.
16. Kozlowski T, Fuchimoto Y, Monroy R, et al.: Apheresis and column absorption for specific removal of Gal-alpha-1,3 Gal natural antibodies in a pig-tobaboon model. Transpl Proc 1997, 29.
17. Buhler L, Basker M, Alwayn I: Coagulation and thrombotic disorders associated with pig organ and hemopoietic cell transplantation in non-human primates. Transplantation 2000 70:1323-1331.
18. Cowan P, Aminian A, Barlow H, et al.: Renal xenografts from triple-transgenic pigs are not hyperacutely rejected but cause coagulopathy in nonimmunosuppressed baboons. Transplantation 2000 69:2504-2515.
19. Gaca JG, Lesher A, Aksoy O, et al.: Disseminated intravascular coagulation in association with pig-to-primate pulmonary xenotransplantation. Transplantation 2002, 73:1717-1723.
20. Tector AJ, Fridell JA, Elias N, et al.: Aberrations in hemostasis and coagulation in untreated discordant hepatic xenotransplantation: Studies in the dog-topig model. Liver Transpl 2002, 8:153-159.
21. Ramirez P, Chavez R, Majado M, et al.: Life-supporting human complement regulator decay accelerating factor transgenic pig liver xenograft maintains the metabolic function and coagulation in the nonhuman primate for up to 8 days. Transplantation 2000, 70:989-998.
22. Buhler L, Yamada K, Kitamura H, et al.: Pig kidney transplantation in baboons: Anti-Gal alpha 1-3Gal IgM alone is associated with acute humoral xenograft rejection and disseminated intravascular coagulation. Transplantation 2001, 72:1743-1752.
23. Starzl TE, Boehmig HJ, Amemiya H, et al.: Clotting changes, including disseminated intravascular coagulation, during rapid renal-homograft rejection. New Eng J Med 1970, 283:383-390
24. Starzl TE, Lerner RA, Dixon FJ, et al.: Shwartzman reaction after human renal homotransplantation. New Eng. J. Med. 1968, 278:642-648
25. Solvik UO, Haraldsen G, Fiane AE, et al.: Human serum-induced expression of E-selectin on porcine aortic endothelial cells in vitro is totally complement mediated. Transplantation 2002, 72:1967-1973.
26. Saadi S, Platt JL: Transient perturbation of endothelial integrity induced by natural antibodies and complement. J Exp Med 1995, 181:21-31.
27. Saadi S, Holzknecht RA, Patte CP, et al.: Complement-mediated regulation of tissue factor activity in endothelium. J Exp Med 1995, 182:1807-1814.
28. Palmetshofer A, Galili U, Dalmasso AP, et al.: Alpha-galactosyl epitopemediated activation of porcine aortic endothelial cells - type II activation. Transplantation 1998, 65:971-978.
29. Palmetshofer A, Galili U, Dalmasso AP, et al.: Alpha-galactosyl epitopemediated activation of porcine aortic endothelial cells - type I activation. Transplantation 1998, 65:844-853.
30. Palmetshofer A, Robson SC, Bach FH: Tyrosine phosphorylation following lectin mediated endothelial cell stimulation. Xenotransplantation 1998, 5:61-66.
31. Lin SS, Weidner BC, Byrne GW, et al.: The role of antibodies in acute vascular rejection of pig-to-baboon cardiac transplants. J Clin Invest 1998, 101:1745-1756.
32. Saadi S, Platt JL: Humoral rejection and endothelial cell activation, 2001. Xenotransplantation 2002, 9:239-241.
33. Saethre M, Solvik UO, Haraldsen G, et al.: Human serum-induced porcine endothelial cell E-selectin expression is associated with IgG3 and IgM anti- Gal antibodies. Xenotransplantation 2002, 9:350-358.
34. Bach FH, Hancock WW, Ferran C: Protective genes expressed in endothelial cells - a regulatory response to injury. Immunol Today 1997, 18:483-486.
35. Wang N, Lee JM, Tobiasch E, et al.: Induction of xenograft accommodation by modulation of elicited antibody responses. Transplantation 2002, 74:334-345.
36. Miyatake T, Koyamada N, Hancock WW, et al.: Survival of accommodated cardiac xenografts upon retransplantation into cyclosporine-treated recipients. Transplantation 1998, 65:1563-1569.
37. Dorling A, Jordan W, Brookes P, et al.: "Accommodated" pig endothelial cells promote nitric oxide-dependent Th-2 cytokine responses from human T cells. Transplantation 2002, 72:1597-1602.
38. Warrens AN, Simon AR, Theodore PR, et al.: Human-porcine receptor-ligand compatibility within the immune system: relevance for xenotransplantation [review]. Xenotransplantation 1999, 6:75-78.
39. Robson SC: Disordered regulation of coagulation and platelet activation in xenotransplantation. In: Platt J, ed. Xenotransplantation: Basic Science to Clinical Application. 2002 pp 215-246.
40. Robson SC, Candinas D, Hancock WW, et al.: Role of endothelial cells in transplantation [review]. Int Arch Allerg Immunol 1995, 106:305-322
41. Robson SC, Kaczmarek E, Siegel JB, et al.: Loss of ATP diphosphohydrolase activity with endothelial cell activation. J Exp Med 1997, 185:153-163.
42. Platt JL, Vercellotti GM, Lindman BJ, et al.: Release of heparan sulfate from endothelial cells. Implications for pathogenesis of hyperacute rejection. J Exp Med 1990, 171:1363-1368
43. Robson SC, Kopp C: Disordered thromboregulation in discordant xenograft rejection. Life Science 1996, 6:34-38.
44. Lawson JH, Platt JL: Molecular barriers to xenotransplantation. Transplantation 1996, 62:303-310.
45. Kopp CW, Robson SC, Siegel JB, et al.: Regulation of monocyte tissue factor activity by allogeneic and xenogeneic endothelial cells. Thromb Haemost 1998, 79:529-538.
46. Kopp CW, Siegel JB, Hancock WW, et al.: Effect of porcine endothelial tissue factor pathway inhibitor on human coagulation factors. Transplantation 1997, 63:749-758.
47. Siegel JB, Grey ST, Lesnikoski BA, et al.: Xenogeneic endothelial cells activate human prothrombin. Transplantation 1997, 64:888-896.
48. Robson SC, Young VK, Cook NS, et al.: Thrombin inhibition in an ex vivo model of porcine heart xenograft hyperacute rejection. Transplantation 1996, 61:862-868.
49. Esmon CT, Fukudome K: Cellular regulation of the protein C pathway. [Review]. Semin Cell Biol 1995, 6:259-268
50. Lawson JH, Daniels LJ, Platt JL: The evaluation of thrombomodulin activity in porcine to human xenotransplantation. Transpl Proc 1997, 29:884-885.
51. McGilvray ID, Lu Z, Wei AC, et al.: Murine hepatitis virus strain 3 induces the macrophage prothrombinase fgpl-2 through p38 mitogen-activated protein kinase activation. J Biol Chem 1998, 273:32222-32229.
52. Fay WP, Murphy JG, Owen WG: High concentrations of active plasminogen activator inhibitor-1 in porcine coronary artery thrombi. Arterioscl Thromb Vas Biol 1996, 16:1277-1284.
53. Kalady MF, Lawson JH, Sorrell RD, et al.: Decreased fibrinolytic activity in porcine-to-primate cardiac xenotransplantation. Molec Med 1998, 4:629-637.
54. Robson SC: Platelets and xenograft rejection. Xenotransplantation 1994 2:38-46.
55. Robson SC, Siegel JB, Lesnikoski BA, et al.: Aggregation of human platelets induced by porcine endothelial cells is dependent upon both activation of complement and thrombin generation. Xenotransplantation 1996, 3:24-34.
56. Peerschke EIB, Reid KBM, Ghebrehiwet B: Platelet activation by C1q results in the induction of αII/βIII integrins and the expression of P-selectin and procoagulant activity. J Exp Med 1993, 178:579-587.
57. Schulte am Esch J, Cruz MA, Siegel JB, et al.: Activation of human platelets by the membrane-expressed A1 domain of von-Willebrand-Factor. Blood 1997, 90:4425-4437.
58. Pareti FI, Mazzucato M, Bottini E, et al.: Interaction of porcine von Willebrand factor with the platelet glycoproteins Ib and IIb/IIIa complex. Brit J Haem 1992, 82:81-86
59. Xu H, Arnaud F, Tadaki DK, et al.: Human platelets activate porcine endothelial cells through a CD154-dependent pathway. Transplantation 2001, 72:1858-1861.
60. Kaczmarek E, Koziak K, Sevigny J, et al.: Identification and characterization of CD39 vascular ATP diphosphohydrolase. J Biol Chem 1996, 271:33116-33122.
61. Vandammieras M, Muller AD, Vanhinsbergh V, et al.: The procoagulant response of cytomegalovirus infected endothelial cells. Thromb Haemost 1992, 68:364-370.
62. Li C, Fung LS, Chung S, et al.: Monoclonal antiprothrombinase (3D4.3) prevents mortality from murine hepatitis virus (MHV-3) Iinfection. J Exp Med 1992, 176:689-697.
63. Altieri DC, Etingin OR, Fair DS, et al.: Structurally homologous ligand binding of integrin Mac-1 and viral glycoprotein-C receptors. Science 1991, 254:1200-1202.
64. Etingin OR, Silverstein RL, Hajjar DP: Von Willebrand factor mediates platelet adhesion to virally infected endothelial cells. Proc. Natl. Acad. Sci.(USA) 1993, 90:5153-5156.
65. Etingin OR, Silverstein RL, Hajjar DP: Identification of a monocyte receptor on herpesvirus-infected endothelial cells. Proc Natl Acad Sci USA 1991, 88:7200-7203.
66. Rother RP, Fodor WL, Springhorn JP, et al.: A novel mechanism of retrovirus inactivation in human serum mediated by anti-alpha-Galactosyl natural antibody. J Exp Med 1995, 182:1345-1355.
67. Thorley BR, Milland J, Christiansen D, et al.: Transgenic expression of a CD46 (membrane cofactor protein) minigene - studies of xenotransplantation and measles virus infection. Eur J Immunol 1997, 27:726-734.
68. Mazure G, Grundy JE, Nygard G, et al.: Measles virus induction of human endothelial cell tissue factor procoagulant activity in vitro. J Gen Virol 1994, 75:2863-2871.
69. Sutherland MR, Raynor CM, Leenknegt H, et al.: Coagulation initiated on herpesviruses. Proc Natl Acad Sci USA 1997, 94:13510-13514
70. Pryzdial EL, Wright JF: Prothrombinase assembly on an enveloped virus: evidence that the cytomegalovirus surface contains procoagulant phospholipid. Blood 1994, 84:3749-3757
71. Mueller NJ, Barth RN, Yamamoto S, et al.: Activation of cytomegalovirus in pig-to-primate organ xenotransplantation. J Virol 2002, 76:4734-4740.
72. Michaels MG: Infectious concerns of cross-species transplantation - xenozoonoses. World J Surg 1997, 21:968-974.
73. Chapman LE, Folks TM, Salomon DR, et al.: Xenotransplantation and xenogeneic infections. N Eng J Med 1995, 333:1498-1501.
74. Anrather D, Millan MT, Palmetshofer A, et al.: Thrombin activates Nuclear Factor-kappa-B and potentiates endothelial cell activation by TNF. J Immunol 1997, 159:5620-5628.
75. Chen DX, Riesbeck K, McVey JH, et al.: Human thrombin and FXa mediate porcine endothelial cell activation; modulation by expression of TFPI-CD4 and hirudin-CD4 fusion proteins. Xenotransplantation 2001, 8:258-265.
76. Cowan PJ, Aminian A, Barlow H, et al.: Protective effects of recombinant human antithrombin III in pig-to-primate renal xenotransplantation. Amer J Transpl 2002, 2:520-525.
77. Candinas D, Lesnikoski BA, Hancock WW, et al.: Inhibition of platelet integrin GPIIbIIIa prolongs survival of discordant cardiac xenografts. Transplantation 1996, 62:1-5.
78. Robson SC, Young VK, Cook NS, et al.: Inhibition of platelet GPIIbIIIa in an ex vivo model of hyperacute xenograft rejection does not prolong cardiac survival time. Xenotransplantation 1996, 3:43-52.
79. Makowka L, Chapman FA, Cramer DV, et al.: Platelet-activating factor and hyperacute rejection. The effect of a platelet-activating factor antagonist, SRI 63-441, on rejection of xenografts and allografts in sensitized hosts. Transplantation 1990, 50:359-365
80. Ohair DP, Roza AM, Komorowski R, et al.: Tulopafant, a PAF receptor antagonist, increases capillary patency and prolongs survival in discordant cardiac xenotransplants. J Lipid Mediat 1993, 7:79-84.
81. Coughlan AF, Berndt MC, Dunlop LC, et al.: In vivo studies of P-selectin and platelet activating factor during endotoxemia, accelerated allograft rejection, and discordant xenograft rejection. Transpl Proc 1993, 25:2930-2931
82. Koyamada N, Miyatake T, Candinas D, et al.: Apyrase administration prolongs discordant xenograft survival. Transplantation 1996, 62:1739-1743.
83. Meyer C, Wolf P, Romain N, et al.: Use of von Willebrand diseased kidney as donor in a pig-to-primate model of xenotransplantation. Transplantation 1999, 67:38-45.
84. Chen DX, Riesbeck K, McVey JH, et al.: Regulated inhibition of coagulation by porcine endothelial cells expressing: P-selectin-tagged hirudin and tissue factor pathway inhibitor fusion proteins. Transplantation 1999, 68:832-839.