Xenograft rejection: Molecular mechanisms and therapeutic prospects

Hematology and Cell Therapy

Volumn 38, Issue 4, 1996, Pages 331-343

  Azimzadeh, A ^a   Meyer, C ^a   Ravanat, C ^b   Cazenave, J P ^b   Wolf, P ^a  

^a Lab de Chir Experimentale   (France)

^b INSERM   (France)

Author keywords

complement; cross species transplantation; endothelial cells; hyperacute rejection; natural antibodies; xenoreactivity

Indexed keywords

CORTICOSTEROID; CYCLOPHOSPHAMIDE; CYCLOSPORIN A; IMMUNOSUPPRESSIVE AGENT; METHOTREXATE; PROSTAGLANDIN E1; TACROLIMUS;

ENDOTHELIUM CELL; GRAFT REJECTION; HUMAN; NONHUMAN; REVIEW; SWINE; XENOTRANSPLANTATION;

EID: 0029764435     PISSN: 14302772     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00282-996-0331-2     Document Type: Review

References (123)

1. Alexandre G, Heinle JS, Ibrahim S, et al (1989) Plasmapheresis and splenectomy in experimental renal xenotransplantation. In: Hardy MA (ed) Xenograft. Elsevier, New York, p 259
2. Auchincloss H (1988) Xenogeneic transplantation. Transplantation 46 : 1-20
3. Auchincloss H (1994) Cell-mediated xenoresponses: strong or weak? Clin Transplantation 8 : 155-159
4. Avrameas S (1991) Natural autoantibodies: from 'horror autotoxicus' to 'gnothi seauton'. Immunology Today 12 : 154-159
5. Azimzadeh A, Wolf P, Dalmasso AP, et al (1996) Assessment of hyperacute rejection in a rat-to-primate cardiac xenograft model. Transplantation 61 : 1305-1313
6. Bach FH, Auchincloss H and Robson SC (1995) Xenotransplantation. In: Bach FH (ed) Transplantation immunology. Wiley, New York, p 305-338
7. Bach FH, Blakely ML, van der Werf M, et al (1993) Discordant xenografting: a working model of problems and issues. Xeno 1 : 8-16
8. Bach FH, Robson SC, Ferran C, et al (1994) Endothelial cell activation and thromboregulation during xenograft rejection. Immunol Rev 141 : 5-30
9. Bach FH, Robson SC, Winkler H, et al (1995) Barriers to xenotransplantation. Nature Med 1 : 869-873
10. Bailey LL, Nehlsen-Cannarella SL, Concepcion W, et al (1985) Baboon-to-human cardiac xenotransplantation in a neonate. J Am Med Ass 254 : 3321-3324
11. Baldwin WM,III, Pruitt SK, Brauer RB, et al (1995) Complement in organ transplantation. Transplantation 59 : 797-808
12. Besse T, Duck L, Latinne D, et al (1994) Effect of plasmapheresis and splenectomy on parameters involved in vascular rejection of discordant xenografts in the swine to baboon model. Transplant Proc 26 : 1042-1044
13. Blakely ML, van der Werf WJ, Berndt MC, et al (1994) Activation of intragraft endothelial and mononuclear cells during discordant xenograft rejection. Transplantation 58 : 1059-1066
14. Borche L, Thibaudeau K, Navenot JM, et al (1994) Cytolytic effect of human anti-Gal IgM and complement on porcine endothelial cells: A kinetic analysis. Xenotransplantation 1 : 125-131
15. Chiche L, Adam R, Caillat-Zucman S, et al (1993) Xenotransplantation: baboons as potential liver donors? Transplantation 55 : 1418-1421
16. Calne RY (1970) Organ transplantation between widely disparate species. Transplant Proc 2 : 550
17. Casali P, Notkins AL (1989) CDS+ B Lymphocytes, polyreactive antibodies and the human B-cell repertoire. Immunol Today 10 : 364-368
18. Chari RS, Collins BH, Magee Jc et al (1994) Brief report treatment of hepatic failure with ex vivo pig-liver perfusion followed by liver transplantation. N Engl J Med 331 : 234-237
19. Collins BH, Cotterell AH, Mc Curry KR, et al (1995) Cardiac xenografts between primate species provide evidence for the importance of the α-Galactosyl determinant in hyperacute rejection. J Immunol 154 : 5500-5510
20. Collins BH, Parker W, Platt JL (1994) Characterization of porcine endothelial cell determinants recognized by human natural antibodies. Xenotransplantation 1 : 36-46
21. Cooper DKC (1991) Depletion of natural antibodies in non-human primates - A step towards successful discordant xenografting in humans. Clin Transplantation 6 : 178-183
22. Cooper DKC (1993) Xenografting: how great is the clinical need? Xeno 1 : 25-26
23. Cooper DKC, Koren E, Oriol R (1994) Oligosaccharides and discordant xenotransplantation. Immunol Rev 141 : 31-58
24. Cozzi E, White DJG (1995) The generation of transgenic pigs as potential organ donors for humans. Nature Med 1 : 964-966
25. Cramer DV (1995) The use of xenografts for acute hepatic failure. Transplant Proc 27 : 80-82
26. Cotterell AH, Collins BH, Parker W, et al (1995) The humoral immune response in humans following cross-perfusion of porcine organs. Transplantation 60 : 861-868
27. Czaplicki J, Blonska B, Zbigniew R (1992) The lack of hyperacute xenogeneic heart transplant rejection in a human. J Heart Lung Transplant 11 : 393-396
28. Dalmasso AP, Platt JL (1993) Prevention of complement-mediated activation of xenogeneic endothelial cells in an in vitro model of xenograft hyperacute rejection by C1 inhibitor. Transplantation 56 : 1171-1176
29. Dalmasso AP, Vercellotti GM, Fischel JR, et al (1992) Mechanism of complement activation in the hyperacute rejection of porcine organs transplanted into primate recipients. Am J Pathol 140 : 1157-1166
30. Dalmasso AP, Vercellotti GM, Platt JL, et al (1991) Inhibition of complement-mediated endothelial cell cytotoxicity by decay-accelerating factor. Transplantation 52 : 530-533
31. Dell RB, Kornfeld DS (1995) Guidelines for xenotransplantation. Science 268 : 349
32. Figueroa J, Fuad SA, Kunjummen BD, et al (1993) Suppression of synthesis of natural antibodies by mycophenolate mofetil (rs-61443). Transplantation 55 : 1371-1374
33. Fischel RJ, Matas AJ, Platt JL, et al (1992) Cardiac xenografting in the pig-to-rhesus monkey model: manipulation of antiendothelial antibody prolongs survival. J Heart Lung Transplant 11 : 965-974
34. Forty J, White DJG, Wallwork J (1993) Activation of the alternative pathway of complement in hyperacute xenograft rejection of rabbit hearts by human blood. J Heart Lung Transplant 12 : 283-287
35. Fujino Y, Kawamura T, Hullett DA, et al (1994) Evaluation of cyclosporine, mycophenolate mofetil,and brequinar sodium combination therapy on hamster-to-rat cardiac xenotransplantation. Transplantation 57 : 41-46
36. Furie B, Furie BC (1992) Molecular and cellular biology of blood coagulation. N Engl J Med 326 : 800-806
37. Galili U (1993) Interaction of the natural anti-Gal antibody with α-galactosyl epitopes: a major obstacle for xenotransplantation in humans. Immunol Today 14 : 480-482
38. Galili U (1994) Significance of the natural human anti-Gal antibody in xenotransplantation. Xeno 2 : 84-87
39. Galili U, Flechner I, Knyszynski A, et al (1986) The natural anti-α-galactosyl IgG on human normal senescent red blood cells. Br J Haematol 62 : 317-324
40. Gautreau C, Wolmant G, Grosse H, et al (1996) Human anti-B alloantibodies recognize xenoantigens on pig red blood cells and endothelial cells. Transplant Proc 28 : 668
41. Gewurz H, Clark DS, Cooper MD, et al (1967) Effect of cobra venom-induced inhibition of complement activity on allograft and xenograft rejection reactions. Transplantation 5 : 1296-1303
42. Good AH, Cooper DKC, Malcom AJ, et al (1992) Identification of carbohydrate structures that bind human antiporcine antibodies: Implications for discordant xenografting in humans. Transplant Proc 24 : 559-562
43. Groth CG, Korsgren O, Tibell J, et al (1994) Transplantation of porcine fetal pancreas to diabetic patients. Lancet 344 : 1402-1404
44. Gustafsson K, Straham K, Preece A (1994) α1,3Galactosyltransferase: A target for in vivo genetic manipulation in xenotransplantation. Immunol Rev 141 : 59-70
45. Hancock WW, Bach FH (1994) The immunopathology of discordant xenograft rejection. Xeno 2 : 68-74
46. Henry ML, Han LK, Davies EA, et al (1994) Antibody depletion prolongs xenograft survival. Surgery 115 : 355-361
47. Holzknecht ZE, Platt JL (1995) Identification of porcine endothelial cell membrane antigens recognized by human xenoreactive natural antibodies. J Immunol 154 : 4565-4575
48. Hunt BJ, Rosenberg RD (1993) The essential role of haemostasia in hyperacute rejection. Xeno 1 : 16-19
49. Inverardi L, Samaja M, Motterlini R, et al (1992) Early recognition of a discordant xenogeneic organ by human circulating lymphocytes.J Immunol 149 : 1416-1423
50. Jaboulay M (1906) Greffe de reins au plis du coude par soudures artérielles et veineuses. Lyon Med 107 : 575
51. Jalali-Araghi K, Macher BA (1994) Characterization of porcine kidney neutral glycosphingolipids: Identification of a carbohydrate antigen recognized by human natural antibodies. Glycoconjugate J 11 : 266-271
52. Johnston PS, Lim SML, Wang MW, et al (1991) Hyperacute rejection of xenografts in the complete absence of antibody. Transplant Proc 23 : 877-879
53. Jorgensen KA, Kemp E, Barfort P, et al (1983) The survival of pig to rabbit renal xenografts during inhibition of thromboxane synthesis. Thromb Res 32 : 585-591
54. Kemp E (1991) Experimental xenotransplantation between distantly related nonprimate species. In: Cooper DKC, Kemp E, Reemtsma K, White DJG (eds) Xeno-transplantation. The transplantation of organs and tissues between species. Springer, Berlin Heidelberg New York, p 377-388
55. Kemp E, Steinbrüchel D, Starklint H, et al (1987) Renal xenograft rejection: prolonging effect of captopril, ACE-inhibitors, prostacyclin and cobra venom factor. Transplant Proc 6 : 4471-4474
56. Kroshus TJ, Rollins SA, Dalmasso AP, et al (1995) Complement inhibition with an anti-C5 monoclonal antibody prevents acute cardiac tissue injury in an ex vivo model of pig to human xenotransplantation. Transplantation 60 : 1194-1202
57. Latinne D, Soares M, Havaux X, et al (1994) Depletion of IgM xenoreactive natural antibodies by injection of anti-μ monoclonal antibodies. Immunol Rev 141 : 95-126
58. Lesnikoski BA, Shaffer DA, van der Werf WJ, et al (1995) Endothelial and host mononuclear cell activation and cytokine expression during rejection of pig to baboon discordant xenografts. Transplant Proc 27 : 290-291
59. Leventhal JR, Dalmasso AP, Cromwell JW, et al (1993) Prolongation of cardiac xenograft survival by depletion of complement. Transplantation 55 : 857-866
60. Leventhal JR, Flores HC, Gruber SA, et al (1992) Evidence that 15-deoxyspergualin inhibits natural antibody production but fails to prevent hyperacute rejection in a discordant xenograft model. Transplantation 54 : 26-31
61. Leventhal JR, John R, Fryer JP, et al (1995) Removal of baboon and human antiporcine IgG and IgM natural antibodies by immunoadsorption. Transplantation 59 : 294-300
62. Lindhal KF, Bach FH (1976) Genetic and cellular aspects of xenogeneic mixed lymphocyte culture reaction. J Exp Med 144 : 305-318
63. Lucas PJ, Shearer GM, Neudorf S, et al (1990) The human antimurine xenogeneic cytotoxic response. 1. Dependance on responder antigen-presenting cells. J Immunol 144 : 4548-4554
64. Magee JC, Collins BH, Harland RC, et al (1995) Prevention of hyperacute xenograft rejection by intravenous immunoglobulin. Transplant Proc 27 : 271
65. Makowka L, Cramer DV, Hoffman A, et al (1995) The use of a pig liver xenograft for temporary support of a patient with fulminant hepatic failure. Transplantation 59 : 1654-1659
66. Makowka L, Miller C, Chapchap P, et al (1987) Prolongation of pig-to-dog renal xenograft survival by modification of the inflammatory mediator response. Ann Surg 206 : 482-495
67. Manning DD, Reed ND, Shaffer CF (1973) Maintenance of skin xenografts of widely divergent phylogenetic origin on congenitally athymic (nude) mice. J Exp Med 138 : 488-494
68. Mc Curry KR, Kooyman DL, Diamond LE, et al (1995) Transgenic expression of human complement regulatory proteins in mice results in diminished complement deposition during organ xenoperfusion. Transplantation 59 : 1177-1182
69. McCurry KR, Kooyman DL, Alvarado CG, et al (1995) Human complement regulatory proteins protect swine-to-primate cardiac xenografts from humoral injury. Nature Med 1 : 423-427
70. Meyer C, Azimzadeh A, Beller JP, et al (1996) Extracorporeal immunoadsorption of xenoreactive natural antibodies in the pig/rhesus model: comparison of three methods. Transplant Proc 28 : 799-800
71. Michaels MG, Mc Michael JP, Brasky K, et al (1994) Screening donors for xenotransplantation. Transplantation 57 : 1462-1465
72. Michaels MG, Simmons RL (1994) Xenotransplant-associated zoonoses. Transplantation 57 : 1-7
73. Miyagawa S, Hirose H, Shirakura R, et al (1988) The mechanism of discordant xenograft rejection. Transplantation 46 : 825-830
74. Morgan BP (1992) Effects of the membrane attack complex of complement on nucleated cells. Curr Top Microbiol Immunol 178 : 115-140
75. Moses RD, Winn HJ, Auchincloss Jr H (1992) Evidence that multiple defects in cell-surface molecule interactions across species differences are responsible for diminished xenogeneic T cell responses. Transplantation 53 : 203-209
76. Murray AG, Khodadoust MM, Pober JS, et al (1994) Porcine aortic endothelial cells activate human T cells: direct presentation of MHC antigens and costimulation by ligands for human CD2 and CD28. Immunity 1 : 57-63
77. Oriol R, Barthod F, Bergemer AM, et al (1994) Monomorphic and polymorphic carbohydrate antigens on pig tissues: implications for organ xenotransplantation in the pig-to-human model. Transplant Int 7 : 405-413
78. Parker W, Bruno D, Holzknecht ZE, et al (1994) Characterization and affinity isolation of xenoreactive human natural antibodies. J Immunol 153 : 3791-3803
79. Perper RJ, Najarian JS (1966) Experimental renal heterotransplantation. I. In widely divergent species. Transplantation 4 : 377
80. Perper RJ, Najarian JS (1967) Experimental renal heterotransplantation. III. Passive transfer of transplantation immunity. Transplantation 5 : 514-533
81. Platt JL (1992) Mechanisms of tissue injury in hyperacute xenograft rejection. ASAIO J 38 : 8-16
82. Platt JL, Bach FH (1991) The barrier to xenotransplantation. Transplantation 52 : 937-947
83. Platt JL, Fischel RJ, Matas AJ, et al (1991) Immunopathology of hyperacute xenograft rejection in a swine-to-primate model. Transplantation 52 : 214-220
84. Platt JL, Holzknecht ZE (1994) Porcine platelet antigens recognized by human xenoreactive natural antibodies. Transplantation 57 : 327-335
85. Platt JL, Lindman BJ, Chen H, et al (1990) Endothelial cell antigens recognized by xenoreactive human natural antibodies. Transplantation 50 : 817-822
86. Platt JL, Turman MA, Noreen HJ, et al (1989) An ELISA assay for xenoreactive natural antibodies. Transplantation 49 : 1000-1001
87. Platt JL, Vercellotti GM, Dalmasso AP, et al (1990) Transplantation of discordant xenografts: a review of progress. Immunol Today 11 : 450-458
88. Pober JS, Cotran RS (1990) Cytokines and endothelial cell biology. Physiol Rev 70 : 427-451
89. Pruitt SK, Kirk AD, Bollinger RR, et al (1994) The effect of soluble complement receptor type 1 on hyperacute rejection of porcine xenografts. Transplantation 57 : 363-370
90. Ross JR, Kirk AD, Ibrahim SE, et al (1993) Characterization of human anti-porcine "natural antibodies" recovered from ex vivo perfused hearts-Predominance of IgM and IgG2. Transplantation 55 : 1144-1150
91. Reemtsma K (1991) Xenotransplantation - a brief history of clinical experiences: 1900-1965. In: Cooper D, Kemp E, Reemtsma E (eds) Xenotransplantation: the transplantation of organs and tissues between species. Springer, Berlin Heidelberg New York, p 9-22
92. Rieben R, Von Allmen E, Korchagina EY, et al (1995) Detection, immunoabsorption and inhibition of cytotoxic activity of anti-αGal antibodies using newly developed substances with synthetic Gal α-3Gal disaccharide epitopes. Xeno 2 : 98-106
93. Rollins SA, Kennedy SP, Chodera AJ, et al (1994) Evidence that activation of human T cells by procine endothelium involves direct recognition of porcine SLA and costimulation by porcine ligands for LFA-1 and CD2. Transplantation 57 : 1709-1716
94. Rosengard AM, Cary NRB, Langford GA, et al (1995) Tissue expression of human complement inhibitor, decay-accelerating factor, in transgenic pigs. Transplantation 59 : 1325-1333
95. Rozga J, Podesta E, LePage A, et al (1993) Control of cerebral oedema by total hepatectomy and extracorporeal liver support in fulminant hepatic failure. Lancet 342 : 898-899
96. Ryan US (1995) Complement inhibitory therapeutics and xenotransplantation. Nature Med 1 : 967-968
97. Satake M, Kumagai-Braesch M, Korsgren O, et al (1993) Characterization of humoral human anti-porcine xenoreactivity. Clin Transplantation 7 : 281-288
98. Saadi S, Platt JL (1995) Transient perturbation of endothelial integrity induced by natural antibodies and complement. J Exp Med 181 : 21-31
99. Sablinski T, Lorf T, Monroy R, et al (1995) Absorption of preformed primate anti swine antibodies by extracorporeal perfusion through galα(1,3)gal columns. The Third International Congress for Xenotransplantation Abstracts Po-33 : 18
100. Sachs DH, Sykes E, Greenstein JL, et al (1995) Tolerance and xenograft survival. Nature Med 1 : 969
101. Samuelsson BE, Rydberg L, Breimer ME, et al (1994) Natural antibodies and human Xenotransplantation. Immunol Rev 141 : 151-168
102. Sandrin MS, Fodor WL, Mouhtouris E, et al (1995) Enzymatic remodelling of the carbohydrate surface of a xenogenic cell substantially reduces human antibody binding and complement-mediated cytolysis. Nature Med 1 : 1261-1267
103. Sandrin MS, Vaughan HA, Dabkowski PL, et al (1993) Anti-pig-IgM antibodies in human serum react predominantly with Galα(1-3)Gal epitopes. Proc Natl Acad Sci 90 : 11391-11395
104. Schaapherder AFM, Daha MR, Bulte M-TJW, et al (1994) Antibody-dependent cell-mediated cytotoxicity against porcine endothelium induced by a majority of human sera. Transplantation 57 : 1376-1382
105. Schaapherder AFM, Gooszen HG, Te Bulte M-TJW, et al (1995) Human complement activation via the alternative pathway on porcine endothelium initiated by IgA antibodies. Transplantation 60 : 287-291
106. Slapak M, Greenbaum M, Bardawil W, et al (1971) Effect of heparin, arvin, liver perfusion and heterologous antiplatelet serum on rejection of pig kidney by dog. Transplant Proc 3 : 558
107. Soares M, van Beneden R, Havaux X, et al (1994) Characterization of xenoreactive natural antibodies secreting cells in rats. Xenotransplantation 1 : 118-124
108. Starzl TE, Fung J, Tzakis A, Todo S, et al (1993) Baboon-to-human liver transplantation. Lancet 341 : 65-71
109. Strahan KM, Preece AF, Xu Y, et al (1995) Antisense inhibition of pig α1,3 galactosyl-transferase leads to a reduction in expression of the major target for human natural antibodies on pig vascular endothelial cells. Xeno 2 : 143-147
110. Sykes M, Lee LA, Sachs DH (1994) Xenograft tolerance. Immunol Rev 141 : 245-276
111. Tearle RG, Tange MJ, Zannettino ZL, et al (1996) The α-1,3-Galactosyltransferase knockout mouse. Transplantation 61 : 13-19
112. Thompson C (1995) Humanised pigs hearts boots xenotransplantation. Lancet 346 : 766
113. Tuso PJ, Cramer DV, Middleton YD, et al (1993) Pig aortic endothelial cell antigens recognized by human IgM natural antibodies. Transplantation 56 : 651-655
114. Vanhove B, Bach FH (1993) Human xenoreactive natural antibodies-avidity and targets on porcine endothelial cells. Transplantation 56 : 1251-1253
115. Vanhove B, R de Martin J, Lipp J, et al (1994) Human xenoreactive natural antibodies of the IgM isotype activate pig endothelial cells. Xeno 1 : 17-23
116. Vaughan HA, Mc Kenzie IFC, Sandrin MS (1995) Biochemical studies of pig xenoantigens detected by naturally occurring human antibodies and the Galα(1,3)Gal reactive lectin. Transplantation 59 : 102-109
117. Weill Bf, Régimbeau JM, Calmus Y, et al (1994) The alternative complement pathway in hyperacute xenograft rejection. Xeno 2 : 92-94
118. Wiener AS (1951) Origin of naturally-occurring hemagglutinins and hemolysins: a review. J Immunol 66 : 287
119. Winkler H, Ferran C, Bach FH (1995) Accommodation of xenografts : a concept revisited. Xeno 2 : 53-56
120. Wrighton CJ, Kopp CW, Mc Shea A, et al (1995) High-level expression of functional human thombomodulin in cultured porcine aortic endothelial cells. Transplant Proc 27 : 288-289
121. Xu H, Edwards NM, Chen JM, et al (1995) Newborn baboon serum lacks natural anti-pig xenoantibody. Transplantation 59 : 1189-1194
122. Ye Y, Cooper DKC (1991) Experimental xenotransplantation in nonhuman primates using distantly related donor species. In : Cooper DKC, Kemp E, Reemtsma K, White DJG (ed) Xeno-transplantation. The transplantation of organs and tissues between species. Springer, Berlin Heidelberg New York, p 389-393
123. Zhao Z, Termignon JL, Cardoso J, et al (1994) Hyperacute xenograft rejection in the swine to human donor recipient combination. Transplantation 57 : 245-249