Prospects for xenotransplantation of the liver

Journal of Hepatology

Volumn 25, Issue 2, 1996, Pages 248-258

  Harland, Robert C ^a   Platt, Jeffrey L ^a,b  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRAFT REJECTION; HUMAN; LIVER DISEASE; LIVER TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SWINE; XENOTRANSPLANTATION;

EID: 0030220904     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-8278(96)80082-1     Document Type: Article

References (98)

1. Evans RW, Orians CE, Ascher NL. The potential supply of organ donors: an assessment of the efficiency of organ procurement efforts in the United States. JAMA. 267:1992;239-246.
2. Evans RW. Executive summary. The National Cooperative Transplantation Study. 1991;BHARC, Seattle, WA, USA.
3. Transplantation statistics. 11:1995;10-11. UNOS Update.
4. Platt JL. Hyperacute Xenograft Rejection. 1995;R.G. Landes Company, Austin.
5. Parker W, Saadi S, Lin SS, Holzknecth ZE, Bustos M, Platt JL. Transplantation of discordant xenografts: a challenge revisited. ImmunolToday. 1996;. in press.
6. Starzl TE, Kaupp HA, Brock DR, Lazarus RE, Johnson RV. Reconstructive problems in canine liver homotransplantation with special reference to the postoperative role of hepatic venous flow. Surg Gynecol Obstet. 111:1960;733-743.
7. Moore FD, Wheeler HB, Demissianos HV, Smith LL, Balankura O. Experimental whole-organ transplantation of the liver and of the spleen. Ann Surg. 152:1960;374-387.
8. Calne RY, White HJO, Herbertson BM, Millard PR, Davis DR, Salaman JR, Samuel JR. Pig-to-baboon liver xenografts. Lancet. i:1968;1176-1178.
9. Calne RY, Davis DR, Pena JR, Balner H, De Vries M, Herbertson BM, Joysey VC, Millard PR, Seaman MJ, Samuel JR, Stibbe J, Westbroek DL. Hepatic allografts and xenografts in primates. Lancet. i:1970;103-106.
10. Starzl TE. Experience in Hepatic Transplantation. 1969;415-419 Saunders, Philadelphia.
11. Giles GR, Boehmig HJ, Amemiya H, Halgrimson CG, Starzl TE. Clinical heterotransplantation of the liver. Transpl Proc. 2:1970;506-512.
12. Makowka L, Wu GD, Hoffman A, Podesta L, Sher L, Tuso PJ, Chapman FA, Consenza C, Yasunaga C, Cramer DV. Immunohistopathologic lesions associated with the rejection of a pig-to-human liver xenograft. Transpl Proc. 26:1994;1074-1075.
13. Makowka L, Cramer DV, Hoffman A. Pig liver xenografts as a temporary bridge for human allografting. Xeno. 1:1993;27-29.
14. Starzl TE, Fung J, Tzakis A, Todo S, Demetris AJ, Marino IR, Doyle H, Zeevi A, Warty V, Michaels M, Kusne S, Rudert WA, Trucco M. Baboon-to-human liver transplantation. Lancet. 341:1993;65-71.
15. Eiseman B, Liem S, Raffucci F. Heterologous liver perfusion in treatment of hepatic failure. Ann Surg. 162:1965;329-345.
16. Harland RC, Bollinger RR. Extracorporeal hepatic perfusion in the treatment of patients with acute hepatic failure. Transplant Rev. 8:1994;73-79.
17. Chari RS, Collins BH, Magee JC, Kirk AD, Harland RC, McCann Rl, Platt JL, Meyers WC. Treatment of hepatic failure with ex-vivo pig liver perfusion followed by liver transplantation. New Engl J Med. 331:1994;234-237.
18. Rozga J, Podesta L, LePage E, Hoffman a, Morsiani E, Sher L, Woolf GM, Makowka L, Demetriou AA. Control of cerebral oedema by total hepatectomy and extracorporeal liver support in fulminant hepatic failure. Lancet. 342:1993;898-899.
19. Michaels MG, d Simmons RL. Xenotransplant-associated zoonoses. Transplantation. 57:1994;1-7.
20. Ye Y, Niekrasz M, Kosanke S, Welsh R, Jordan HE, Fox JC, Edwards WC, Maxwell C, Cooper DKC. The pig as a potential organ donor for man. Transplantation. 57:1994;694-703.
21. Logan JS, Martin MJ. Transgenic swine as a recombinant production system for human hemoglobin. Methods Enzymol. 231:1994;435-5.
22. Perper RJ, Najarian JS. Experimental renal heterotransplantation. I. In widely divergent species. Transplantation. 4:1966;377-388.
23. Auchincloss H Jr. Xenogeneic transplantation. Transplantation. 46:1988;1-20.
24. Platt JL, Vercelloti GM, Dalmasso AP, Matas AJ, Bolman RM, Najarian JS, Bach FH. Transplantation of discordant xenografts: a review of progress. Immunol Today. 11:1990;450-456.
25. Calne RY. Organ transplantation between widely disparate species. Transpl Proc. 2:1970;550-556.
26. Platt JL. Antibodies in graft rejection. Bach FH, Auchincloss H. Transplantation Immunology. 1995;113-129 Wiley-Liss, Inc. New York City, NY.
27. Platt JL. Xenotransplantation. Fogarty P. Handbook of Transplant Immunology. 1995;259-299 Medical & Scientific Productions, Bucks, UK.
28. Platt PL, Fischel RJ, Matas AJ, Reif SA, Bolman RM, Bach FH. Immunopathology of hyperacute xenograft rejection in a swine-to-primate model. Transplantation. 52:1991;214-220.
29. Boyden SV. Natural antibodies and the immune response. Adv Immunol. 5:1964;1-28.
30. Dalmasso AP, Vercellotti GM, Fischel RJ, Bolman RM, Bach FH, Platt JL. Mechanism of complement activation in the hyperacute rejection of porcine organs transplanted into primate recipients. Am J Pathol. 140:1992;1157-1166.
31. Cooper DKC, Human PA, Lexer G, Rose AG, Rees J, Keraan M, Du Toit E. Effects of cyclosporine and antibody adsorption on pig cardiac xenograft survival in the baboon. J Heart Transpl. 7:1988;238-6.
32. Kaplon RJ, Michler RE, Xu H, Kwiatkowski PA, Edwards NM, Platt JL. Absence of hyperacute rejection in newborn pig-to-baboon cardiac xenografts. Transplantation. 59:1994;1-6.
33. Miyagawa S, Hirose H, Shirakura R, Naka Y, Nakata S, Kawashima Y, Seya T, Matsumoto M, Uenaka A, Kitamura H. The mechanisn of discordant xenograft rejection. Transplantation. 46:1988;825-830.
34. Leventhal JR, Matas AJ, Sun LH, Reif S, Bolman RM III, Dalmasso AP, Platt JL. The immunopathology of cardiac xenograft rejection in the guinea pig to rat model. Transplantation. 56:1993;1-8.
35. Johnston PS, Wang M-W, Lim SML, Wright LJ, White DJG. Discordant xenograft rejection in an antibody-free model. Transplantation. 54:1992;573-576.
36. Platt JL, Vercellotti GM, Lindman BJ, Oegema TR Jr, Bach FH, Dalmasso AP. Release of heparan sulfate from endothelial cells: implications for pathogenesis of hyperacute rejection. J Exp Med. 171:1990;1363-1368.
37. Edwards J. Complement activation by xenogeneic red blood cells. Transplantation. 31:1981;226-227.
38. Hourcade D, Holers VM, Atkinson JP. The regulators of complement activation (RCA) gene clusters. Adv Immunol. 45:1989;381-416.
39. McCurry KR, Kooyman DL, Alvarado CG, Cotterell AH, Martin MJ, Logan JS, Platt JL. Human complement regulatory proteins protect swine-to-primate cardiac xenografts from humoral injury. Nature Med. 1:1995;4237.
40. Byrne GW, McCurry KR, Martin MJ, McClellan SM, Platt JL, Logan JS. Expression of human CD59 and DAF in transgenic pigs: intrinsic regulation of complement activity.
41. Saadi S, Ihrcke NS, Platt JL. Endothelial cell shape and hyperacute rejection. Transpl Proc. 26:1994;1149.
42. Platt JL, Dalmasso AP, Lindman BJ, Ihrcke NS, Bach FH. The role of C5a and antibody in the release of heparan sulfate from endothelial cells. Eur J Immunol. 21:1991;2887-2890.
43. Vercellotti GM, Platt JL, Bach FH, Dalmasso AP. Neutrophil adhesion to xenogeneic endothelium via c3bio-ic3b. J Immunol. 146:1991;730-734.
44. Collins BH, Chari RS, Magee JC, Harland RC, Lindman BJ, Logan JS, Bollinger RR, Meyers WC, Platt JL. Mechanisms of injury in porcine livers perfused with blood of humans with fulminant hepatic failure. Transplantation. 58:1994;1162-1171.
45. Gordon RD, Iwatsuki S, Esquivel CO, Tzakis A, Todo S, Starzl TE. Liver transplantation across ABO blood groups. Surgery. 100:1986;342-348.
46. Gordon RD, Fung JJ, Markus B, Fox I, Iwatsuki S, Esquivel CO, Tzakis A, Todo S, Starzl TE. The antibody crossmatch in liver transplantation. Surgery. 100:1986;705-715.
47. Knechtle SJ, Kolbeck PC, Tsuchimoto S, Coundouriotis A, Sanfilippo F, Bollinger RR. Hepatic transplantation into sentisized recipients: demonstration of hyperacute rejection. Transplantation. 43:1987;8-12.
48. Merion RM, Colletti LM. Hyperacute rejection in porcine liver transplantation: I. Clinical characteristics, histopathology, disappearance of donor-specific lymphocytotoxic antibody from serum. Transplantation. 49:1990;861-868.
49. Saadi S, Ihrcke NS, Platt JL. Pathophysiology of xenograft rejection. Lieberman R, Morris R. Principles of immunomodulatory drug development in transplantation and autoimmunity. 1996;Raven Press, New York, NY. in press.
50. Saadi S, Platt JL. Transient perturbation of endothelial integrity induced by antibodies and complement. J Exp Med. 181:1995;21-31.
51. Cotterell AH, Collins BH, Parke W, Harland RC, Platt JL. The humoral immune response in humans following cross-perfusion of porcine organs. Transplantation. 60:1995;861-868.
52. Chopek MW, Simmons RL, Platt JL. ABO incompatible renal transplantation: initial immunopathologic evaluation. Transpl. Proc. 19:1987;4553-4557.
53. Alexandre GPJ, Squifflet JP, De Bruyere M, Latinne D, Reding R, Gianello P, Carlier M, Pirson V. Present experiences in a series of 26 ABO-incompatible living donor renal allografts. Transpl Proc. 19:1987;4538-4542.
54. Alexandre GPJ, Gianello P, Latinne D, Carlier M, Dewaele A, Van Obbergh L, Moriau M, Marbaix E, Lambotte JL, Lambotte L, Squifflet JP. Plasmapheresis, splenectomy in experimental renal xenotransplantation. Hardy MA. Xenograft 25. 259-266:1989;Elsevier Science Publishers, New York, NY.
55. Fischel RJ, Matas AJ, Platt JL, Perry E, Noreen H, Shumway SJ, Bolman RM. Cardiac xenografting in the pig to rhesus model; manipulation of anti-endothelial antibody prolongs survival. J Heart Lung Transplant. 11:1992;965-974.
56. Busso N, Huet S, Nicodeme E, Hiernaux J, Hyafil F. Refractory period phenomenon in the induction of tissue factor expression on endothelial cells. Blood. 78:1991;2027-2035.
57. Colman RB, Habal M, Hollenberg NK, Birtch AG, Busch GJ. Hyperacute renal allograft rejection in the primate. Am J Pathol. 82:1976;25-42.
58. Forbes RDC, Guttmann RD, Kuramochi T, Klassen J, Knaack J. Nonessential role of neutrophils as mediators of hyperacute cardiac allograft rejection in the rat. Lab Inv. 34:1976;229-234.
59. Zehr KJ, Herskowitz A, Lee PC, Kumar P, Gillinov AM, Baumgartner WA. Neutrophil adhesion and complement inhibition prolongs survival of cardiac xenografts in discordant species. Transplantation. 57:1994;900-906.
60. Inverardi L, Samaja M, Motterlini R, Mangili F, Bender JR, Pardi R. Early recognition of a discordant xenogeneic organ by human circulating lymphocytes. J Immunol. 149:1992;1416-1423.
61. Blakely ML, Van Der Werf WJ, Berndt MC, Dalmasso AP, Bach FH, Hancock WW. Activation of intragraft endothelial and mononuclear cells during discordant xenograft rejection. Transplantation. 58:1994;1059-1066.
62. Geller RL, Turman MA, Dalmasso AP, Platt JL. The natural immune barrier to xenotransplantation. JASN. 3:1993;1189-1200.
63. Murray AG, Khodadoust MM, Pober JS, Bothwell ALM. Porcine aortic endothelial cells activate human T cells: direct presentation of MHC antigens and costimulation by ligands for human CD2 and CD28. Immunity. 1:1994;57-63.
64. Ihrcke NS, Wrenshall LE, Lindman BJ, Platt JL. Role of heparan sulfate in immune system-blood vessel interactions. Immunol Today. 14:1993;500-505.
65. Platt JL. A perspective on xenograft rejection and accommodation. Immunol Rev. 141:1994;127-149.
66. Platt JL, Parker W. Another step toward clinical xenotransplantation. Nature Med. 1:1995;1248-1250.
67. Galili U, Rachmilewitz EA, Peleg A, Flechner I. A unique natural human IgG antibody with anti-a-galactosyl specificity. J Exp Med. 160:1984;1519-1531.
68. Galili U. Interaction of the natural anti-Gal antibody with α-galactosyl epitopes: a major obstacle for xenotransplantation in humans. Immunol Today. 14:1993;480-482.
69. Collins BH, Parker WR, Platt JL. Characterization of porcine endothelial cell determinants recognized by human natural antibodies. Xenotransplantation. 1:1994;36-46.
70. Galili U, Clark MR, Shohet SB, Buehler J, Macher BA. Evolutionary relationship between the natural anti-Gal antibody and the Gal α-3Gal epitope in primates. Proc Natl Acad Sci USA. 84:1987;1369-1373.
71. Good AH, Cooper DKC, Malcolm AJ, Ippolito RM, Koren E, Neethling FA, Ye Y, Zuhdi N, Lamontagne LR. Identification of carbohydrate structures that bind human antiporcine antibodies: implications for discordant xenografting in humans. Transpl Proc. 24:1992;559-562.
72. Neethling FA, Koren E, Ye Y, Richards SV, Kujundzic M, Oriol R, Cooper DKC. Protection of pig kidney (PK15) cells from the cytotoxic effect of anti-pig antibodies by a-galactosyl oligosaccharides. Transplantation. 57:1994;959-963.
73. Sandrin MS, Vaughan HA, Dabkowski PL, McKenzie IFC. Anti-pig IgM antibodies in human serum react predominantly with Galα(1,3)Gal epitopes. Proc Natl Acad Sci USA. 90:1993;11391-11395.
74. Collins BH, Cotterell AH, McCurry KR, Alvarado CG, Magee JC, Parker WR, Platt JL. Hyperacute rejection of cardiac xenografts between primate species: evidence to support the significance of the α-Galactosyl determinant. J Immunol. 154:1995;5500-5510.
75. Bannett AD, McAlack RF, Raja R, Baquero A, Morris M. Experiences with known ABO-mismatched renal transplants. Transpl Proc. 19:1987;4543-4546.
76. Cooper DKC, Ye Y, Niekrasz M, Kehoe M, Martin M, Neethling FA, Kosanke S, DeBault LE, Worsley G, Zudhi N, Oriol R, Romano E. Specific intravenous carbohydrate therapy: a new concept in inhibition antibody-mediated rejection - experience with ABO-incompatible cardiac allografting in the baboon. Transplantation. 56:1993;769-777.
77. Parker WR, Bruno D, Holzknecht ZE, Platt JL. Xenoreactive natural antibodies: isolation and initial characterization. J Immunol. 153:1994;3791-3803.
78. Geller RL, Rubinstein P, Platt JL. Variation in experience of porcine xenogeneic antigens. Transplantation. 58:1994;272-277.
79. Cotterell AH, Alvarado CG, Logan JS, Platt JL. Variation in expression of porcine antigens recognized by human xenoreactive natural antibodies. Transpl Proc. 27:1995;278-279.
80. Strahan K, Gu F, Andersson L, Gustafsson K. Pig a 1,3 galactosyltransferase: sequence of a full length cDNA clone and chromosomal localisation of the corresponding gene. Transpl Proc. 27:1995;245-248.
81. Sandrin MS, Fodor WL, Mouhtouris E, Osman N, Cohney S, Rollins SA, Guilmette ER, Setter E, Squinto SP, McKenzie I. Enzymatic remodelling of the carbohydrate surface of a xenogeneic cell substantially reduces human antibody binding and complement-mediated cytolysis. Nature Med. 1:1995;1261-1267.
82. Sharma A, Okabe JF, Birch P, Platt JL, Logan JS. Reduction in the level of Gal(α1,3)Gal in transgenic mice and pigs by the expression of α(1,2) fucosyltransferase. Proc Natl Acad Sci USA. 1996;. in press.
83. Gewurz H, Clark DS, Cooper MD, Varco RL, Good RA. Effect of cobra venom-induced inhibition of complement activity on allograft and xenograft rejection reactions. Transplantation. 5:1967;1296-1303.
84. Leventhal JR, Dalmasso AP, Cromwell JW, Platt JL, Manivel CJ, Bolman RM, Matas AJ. Prolongation of cardiac xenograft survival by depletion of complement. Transplantation. 55:1993;857-866.
85. Pruitt SK, Kirk AD, Bollinger RR, Marsh HC Jr, Collins BH, Levin JL, Mault RJ, Heinle JS, Ibrahim S, Rudolph AR, Baldwin WM III, Sanfilippo F. The effect of soluble complement receptor type on 1 hyperacute rejection of porcine xenografts. Transplantation. 57:1994;363-370.
86. Weisman HF, Bartow T, Leppo MK, Marsh H.C. Jr, Carson GR, Concino MF, Boyle MP, Roux KH, Weisfeldt ML, Fearon DT. Soluble human complement receptor type 1: in vivo inhibitor of complement suppressing post-ischemic myocardial inflammation and necrosis. Science. 249:1990;146-151.
87. Leventhal JR, Sakiyalak P, Witson J, Simone P, Matas AJ, Bolman RM, Dalmasso AP. The synergistic effect of combined antibody and complement depletion on discordant cardiac xenograft survival in nonhuman primates. Transplantation. 57:1994;974-978.
88. Dalmasso AP, Platt JL. Prevention of complement-mediated activation of xenogeneic endothelial cells in an in vitro model of xenograft hyperacute rejection by C1 inhibitor. Transplantation. 56:1993;1171-1176.
89. Magee JC, Collins BH, Harland RC, Bollinger RR, Frank MM, Platt JL, Lindman BJ. Immunoglobulin prevents complement mediated hyperacute rejection in swine-to-primate xenotransplantation. J Clin Invest. 96:1995;2404-2412.
90. Frank MM, Basta M, Fries LF. The effects of intravenous immune globulin on complement-dependent immune damage of cells and tissues. Clin Immunol Immunopathol. 62:1992;s82-s86.
91. Dalmasso AP, Vercellotti GM, Platt JL, Bach FH. Inhibition of complement-mediated endothelial cell cytotoxicity by decay accelerating factor: Potential for prevention of xenograft hyperacute rejection. Transplantation. 52:1991;530-533.
92. McClellan S, Kagan DT, Byrne GW, Platt JL, Logan JS, Kooyman D. Demonstration of intermembrane transfer of CD59 during coculture of human erythrocytes with porcine and bovine aortic endothelial cells. Transpl Proc. 26:1994;1240.
93. Cary N, Moody J, Yannoutsos N, Wallwork J, White D. Tissue expression of human decay accelerating factor, a regulator of complement activation expressed in mice: a potential approach to inhibition of hyperacute xenograft rejection. Transpl Proc. 25:1993;400-401.
94. Kooyman D, Byrne GW, McClellan S, Nielsen DL, Kagan DT, Coffman T, Masahide T, Waldmann H, Platt JL, Logan JS. Erythroid-specific expression of human CD59 and transfer to vascular endothelial cells. Transpl Proc. 26:1994;1241.
95. Diamond LE, Oldham ER, Platt JL, Waslman H, Tone M, Walsh LA, Logan JS. Cell and tissue specific expression of a human CD59 minigene in transgenic mice. Transpl Proc. 26:1994;1239.
96. Kagan DT, Platt JL, Logan JS, Byrne GW. Expression of complement regulatory factors using heterologous promoters in transgenic mice. Transpl Proc. 26:1994;1242.
97. McCurry KR, Kooyman DL, Diamond LE, Byrne GW, Logan JS, Platt JL. Human complement regulatory proteins in transgenic animals regulate complement activation in xenoperfused organs. Transpl Proc. 27:1995;317-318.
98. Thompson C. Humanised pigs hearts boost xenotransplantation. Lancet. 346:1995;766.