Transfusion and Apheresis Science
Volume 35, Issue 1 , Pages 45-58 , August 2006

Xenotransplantation and ABO incompatible transplantation: The similarities they share

Received 13 March 2006 ,Accepted 19 May 2006.

References 

  1. Alexandre GP, Squifflet JP, DeBruyere BM, et al. Present experiences in a series of 26 ABO-incompatible living donor renal allografts. Transplant Proc. 1987;19:4538–4542
  2. Bannett AD, McAlack RF, Raja R, et al. Experience with known ABO-mismatched renal transplants. Transplant Proc. 1987;19:4543–4546
  3. Slapak M, Digard N, Ahmed M, et al. Renal transplantation across the ABO barrier-A 9-year experience. Transplant Proc. 1990;22:1425–1428
  4. Mendez R, Sakhrani L, Aswad S, et al. Successful living-related ABO incompatible renal transplant using the BIOSYNSORB. Immunoadsorption Column Transplant Proc. 1992;24:1738–1746
  5. Yamashita M, Aikawa A, Ohara T, et al. Local immune states in ABO-incompatible renal allografts. Transplant Proc. 1993;25:274–276
  6. Tanabe K, Takahashi K, Sonda K, et al. Long-term results of ABO-incompatible living kidney transplantation: a single-center experience. Transplantation. 1998;65:224–228
  7. Karakayali H, Moray G, Demirag A, et al. Long-term follow-up of ABO-incompatible renal transplant recipients. Transplant Proc. 1999;31:256–257
  8. Kobayashi T, Yokoyama I, Nagasaka T, et al. Comparative study of antibody removal before pig-to-baboon and human ABO-incompatible renal transplantation. Transplant Proc. 2000;32:1097
  9. Takahashi K. ABO incompatible kidney transplantation. Amsterdam: Elsevier Science; 2001;
  10. Shishido S, Asanuma H, Tajima E, et al. ABO-incompatible living-donor kidney transplantation in children. Transplantation. 2001;72:1037–1042
  11. Rydberg L. ABO incompatibility in solid organ transplantation. Transfusion Med. 2001;11:325–342
  12. Wu A, Buhler LH, Cooper DK. ABO-incompatible organ and bone marrow transplantation: current status. Transplant Int. 2003;16:291–299
  13. Starzl TE. Renal homografts in patients with major donor recipient blood group incompatibilities. Surgery. 1964;55:195–200
  14. Wilbrandt R, Tung KS, Deodhar SD, et al. ABO blood group incompatibility in human renal homotransplantation. Am J Clin Pathol. 1969;51:15–23
  15. Cooper DK. Clinical survey of heart transplantation between ABO blood group-incompatible recipients and donors. J Heart Transplant. 1990;9:376–381
  16. Chopek MW, Simmons RL, Platt JL. ABO-incompatible kidney transplantation: initial immunopathologic evaluation. Transplant Proc. 1987;19:4553–4557
  17. Ishida H, Koyama I, Sawada T, et al. Anti-AB titer changes in patients with ABO incompatibility after living related kidney transplantations: survey of 101 cases to determine whether splenectomies are necessary for successful transplantation. Transplantation. 2000;70:681–685
  18. Latinne D, Squifflet JP, De Bruyere M, et al. Subclasses of ABO isoagglutinins in ABO-incompatible kidney transplantation. Transplant Proc. 1989;21:641–642
  19. Park WD, Grande JP, Ninova D, Nath KA, Platt JL, Gloor JM, et al. Accommodation in ABO-incompatible kidney allografts, a novel mechanism of self-protection against antibody-mediated injury. Am J Transplant. 2003;3:952–960
  20. Galili U, Ishida H, Toma K, Tanabe H. Anti-Gal A/B, a novel anti-blood group antibody identified in recipients of ABO incompatible kidney allografts. Transplantation. 2003;74:1574–1580
  21. Platt JL, Bach FH. The barrier to xenotransplantation. Transplantation. 1991;52:937–947
  22. Bach FH, Ferran C, Soares M, et al. Modification of vascular responses in xenotransplantation: inflammation and apoptosis. Nat Med. 1997;3:944–948
  23. Soares MP, Lin Y, Sato K, et al. Accommodation. Immunol Today. 1999;20:434–437
  24. Bach FH, Turman MA, Vercellotti GM, Platt JL, Dalmasso AP. Accommodation: a working paradigm for progressing toward clinical discordant xenografting. Transplant Proc. 1991;23:205–207
  25. Yuzawa Y, Brett J, Fukatsu A, et al. Interaction of antibody with Forssman antigen in guinea pigs. A mechanism of adaptation to antibody- and complement-mediated injury. Am J Pathol. 1995;146:1260–1272
  26. Ulfvin A, Backer AE, Clausen H, Hakomori S, Rydberg L, Samuelsson BE, et al. Expression of glycolipid blood group antigens in single human kidneys: change in antigen expression of rejected ABO incompatible kidney grafts. Kidney Int. 1993;44:1289–1297
  27. Mohiuddin MM, Ogawa H, Yin DP, Shen J, Galili U. Antibody-mediated accommodation of heart grafts expressing an incompatible carbohydrate antigen. Transplantation. 2003;75:258–262
  28. West LJ, Pollock-Barziv SM, Dipchand AI, et al. ABO-incompatible heart transplantation in infants. New Engl J Med. 2001;344:793–800
  29. Galili U, Buehler J, Shohet SB, Macher BA. The human natural anti-Gal IgG. III. The subtlety of immune tolerance in man as demonstrated by crossreactivity between natural anti-Gal and anti-B antibodies. J Exp Med. 1987;165:693–704
  30. Galili U, Clark MR, Shohet SB, Buehler J, Macher BA. Evolutionary relationship between the anti-Gal antibody and the Galα1→3Gal epitope in primates. Proc Natl Acad Sci USA. 1987;84:1369–1373
  31. Galili U, Shohet SB, Kobrin E, Stults CLM, Macher BA. Man, apes, and Old World monkeys differ from other mammals in the expression of α-galactosyl epitopes on nucleated cells. J Biol Chem. 1988;263:17755–17762
  32. Thall A, Etienne-Decerf J, Winand R, Galili U. The α-galactosyl epitope on mammalian thyroid cells. Acta Endocrinol. 1991;124:692–699
  33. Basu M, Basu S. Enzymatic synthesis of blood group related pentaglycosyl ceramide by an α-galactosyltransferase. J Biol Chem. 1973;248:1700–1706
  34. Betteridge A, Watkins WM. Two α-3-d galactosyltransferases in rabbit stomach mucosa with different acceptor substrate specificities. Eur J Biochem. 1983;132:29–35
  35. Blake DD, Goldstein IJ. An α-d-galactosyltransferase in Ehrlich ascites tumor cells: Biosynthesis and characterization of a trisaccharide (α-d-galacto(1-3)-N-acetyllactosamine). J Biol Chem. 1981;256:5387–5393
  36. Blanken WM, van den Eijnden DH. Biosynthesis of terminal Gal α1-3Galß1-4GlcNAc-R oligosaccharide sequence on glycoconjugates: purification and acceptor specificity of a UDP-Gal: N-acetyllactosamine α1,3galactosyltransferase. J Biol Chem. 1985;260:12927–12934
  37. Joziasse DH, Shaper JH, Van den Eijnden DH, Van Tunen AH, Shaper NL. Bovine α1-3galactosyltransferase: isolation and characterization of a cDNA clone. Identification of homologous sequences in human genomic DNA. J Biol Chem. 1989;264:14290–14297
  38. Larsen RD, Rajan VP, Ruff M, Kukowska-Latallo J, Cummings RD, Lowe JB. Isolation of a cDNA encoding murine UDP galactose: ßd-galactosyl-1,4-N-acetyl-d-glucosaminide α1,3-galactosyltransferase: Expression cloning by gene transfer. Proc Natl Acad Sci USA. 1989;86:8227–8231
  39. Larsen RD, Rivera-Marrero CA, Ernst LK, Cummings RD, Lowe JB. Frameshift and nonsense mutations in a human genomic sequence homologous to a murine UDP-Galβ-d-Gal(1,4)-d-GlcNAc α(1,3) galactosyltransferase cDNA. J. Biol. Chem. 1990;265:7055–7062
  40. Galili U, Swanson K. Gene sequences suggest inactivation of α1,3 galactosyltransferase in catarrhines after the divergence of apes from monkeys. Proc Natl Acad Sci USA. 1991;88:7401–7404
  41. Joziasse DH, Shaper JH, Jabs EW, Shaper NL. Characterization of an α1-3-galactosyltransferase homologue on human chromosome 12 that is organized as a processed pseudogene. J Biol Chem. 1991;266:6991–6998
  42. Koike C, Fung JJ, Geller DA, et al. Molecular basis of evolutionary loss of the α1,3-galactosyltransferase gene in higher primates. J Biol Chem. 2002;277:10114–10120
  43. Lanteri M, Giordanengo V, Vidal F, Gaudray P, Lefebvre JC. A complete α1,3-galactosyltransferase gene is present in the human genome and partially transcribed. Glycobiology. 2002;12:785–792
  44. Galili U, Rachmilewitz EA, Peleg A, Flechner I. A unique natural human IgG antibody with anti-α-galactosyl specificity. J Exp Med. 1984;160:1519–1531
  45. Galili U, Macher BA, Buehler J, Shohet SB. Human natural anti-α-galactosyl IgG. II. The specific recognition of α(1→3)-linked galactose residues. J Exp Med. 1985;162:573–582
  46. Galili U, Buehler J, Shohet SB, Macher BA. The human natural anti-Gal IgG. III. The subtlety of immune tolerance in man as demonstrated by crossreactivity between natural anti-Gal and anti-B antibodies. J Exp Med. 1987;165:693–704
  47. Towbin H, Rosenfelder G, Wieslander J, et al. Circulating antibodies to mouse laminin in Chagas disease, American cutaneous leishmaniasis, and normal individuals recognize terminal galactosyl(α1-3)-galactose epitopes. J Exp Med. 1987;66:419–432
  48. Galili U. Evolution and pathophysiology of the human natural anti-Gal antibody. Springer Sem Immunopathol. 1993;15:155–171
  49. Hamadeh RM, Galili U, Zhou P, Griffiss JM. Anti-α-galactosyl immunoglobulin A (IgA), IgG, and IgM in human secretions. Clin Diagn Lab Immunol. 1995;2:125–131
  50. Springer GF, Horton RE. Blood group isoantibody stimulation in man by feeding blood group-active bacteria. J Clin Invest. 1969;48:1280–1291
  51. Galili U, Mandrell RE, Hamadeh RM, Shohet SB, Griffis JM. Interaction between human natural anti-α-galactosyl immunoglobulin G and bacteria of the human flora. Infect Immun. 1988;56:1730–1737
  52. Galili U, Anaraki F, Thall A, Hill-Black C, Radic M. One percent of human circulating B lymphocytes are capable of producing the natural anti-Gal antibody. Blood. 1993;82:2485–2493
  53. Galili U, LaTemple DC, Radic MZ. A sensitive assay for measuring α-gal epitope expression on cells by a monoclonal anti-Gal antibody. Transplantation. 1998;65:1129–1132
  54. Galili U. Interaction of the natural anti-Gal antibody with α-galactosyl epitopes: a major obstacle for xenotranplantation in humans. Immunol Today. 1993;14:480–482
  55. Good AH, Cooper DCK, Malcolm AJ, et al. Identification of carbohydrate structures which bind human anti-porcine antibodies: implication for discordant xenografting in man. Transplant Proc. 1992;24:559–562
  56. Sandrin M, Vaughan HA, Dabkowski PL, McKenzie IFC. Anti-pig IgM antibodies in human serum react predominantly with Galα1-3Gal epitopes. Proc Natl Acad Sci USA. 1993;90:11391–11395
  57. Collins BH, Cotterell AH, McCurry KR, et al. Cardiac xenografts between primate species provide evidence of the α-galactosyl determinant in hyperacute rejection. J Immunol. 1994;154:5500–5510
  58. Platt JL. A perspective on xenograft rejection and accommodation. Immunol Rev. 1994;141:127–149
  59. Simon PM, Neethling FA, Taniguchi S, et al. Intravenous infusion of Galα1-3Gal oligosaccharides in baboons delays hyperacute rejection of porcine heart xenografts. Transplantation. 1998;65:346–353
  60. Watier H, Guillaumin J-M, Vallee I, et al. Human NK cell-mediated direct and IgG dependent cytotoxicity against xenogeneic porcine endothelial cells. Transplant Immunol. 1996;4:293–299
  61. McMorrow IM, Comrack CA, Nazarey PP, Sachs DH, DerSimonian H. Relationship between ABO blood group and levels of Galα3Galactose-reactive human immunoglobulin G. Transplantation. 1997;64:546–549
  62. Galili U, Tibell A, Samuelsson B, Rydberg B, Groth CG. Increased anti-Gal activity in diabetic patients transplanted with fetal porcine islet cell clusters. Transplantation. 1995;59:1549–1556
  63. Galili U, LaTemple DC, Walgenbach AW, Stone KR. Porcine and bovine cartilage transplants in cynomolgus monkey: II. Changes in anti-Gal response during chronic rejection. Transplantation. 1997;63:646–651
  64. Stone KR, Ayala G, Goldstein J, Hurst R, Walgenbach A, Galili U. Porcine cartilage transplants in cynomolgus monkey: III. Transplantation of α-galactosidase treated porcine cartilage. Transplantation. 1998;65:1577–1583
  65. Thall AD, Maly P, Lowe JB. Oocyte Galα1-3Gal epitopes implicated in sperm adhesion to the zona pellucide glycoprotein ZP3 are not required for fertilization in the mouse. J Biol Chem. 1995;270:21437–21440
  66. Tearle RG, Tange MJ, Zannettino ZL, et al. The α-1,3-galactosyltransferase knockout mouse. Implications for xenotransplantation. Transplantation. 1996;61:13–19
  67. Tanemura M, Yin D, Chong AS, Galili U. : Differential immune responses to α-gal epitopes on xenografts and allografts: implications for accommodation in xenotransplantation. J Clin Invest. 2000;105:301–310
  68. LaTemple DC, Abrams JT, Zhang SU, Galili U. Increased immunogenicity of tumor vaccines complexed with anti-Gal: Studies in knock out mice for α1,3galactosyltranferase. Cancer Res. 1999;59:3417–3423
  69. Pearse MJ, Witort E, Mottram P, et al. Anti-Gal antibody-mediated allograft rejection in α1,3-galactosyltransferase gene knockout mice: a model of delayed xenograft rejection. Transplantation. 1998;66:748–754
  70. Fan X, Ang A, Pollock-Barziv SM, Dipchand AI, Ruiz P, Wilson G, et al. Donor-specific B-cell tolerance after ABO-incompatible infant heart transplantation. Nat Med. 2004;10:1165–1166
  71. Speir JA, Abdel-Motal UM, Jondal M, Wilson IA. Crystal structure of an MHC class I presented glycopeptide that generates carbohydrate-specific CTL. Immunity. 1999;10:51–61
  72. Bensinger WI, Baker DA, Buckner CD, Clift RA, Thomas ED. Immunoadsorption for removal of A and B blood-group antibodies. New Engl J Med. 1981;304:160–162
  73. Rieben R, Korchagina EY, von Allmen E, et al. In vitro evaluation of the efficacy and biocompatibility of new, synthetic ABO immunoabsorbents. Transplantation. 1995;60:425–430
  74. Cretin N, Bracy J, Hanson K, Iacomini J. The role of T cell help in the production of antibodies specific for Galα1-3Gal. J Immunol. 2002;168:1479–1483
  75. Ogawa H, Mohiuddin MM, Yin DP, Shen J, Chong AS, Galili U. Mouse-heart grafts expressing an incompatible carbohydrate antigen. II. Transition from accommodation to tolerance. Transplantation. 2004;77:366–373
  76. Galili U. Immune response, accommodation and tolerance to transplantation carbohydrate antigens. Transplantation. 2004;78:1093–1098
  77. Groth CG, Korsgren O, Tibell A, Tollemar J, Moller E, Bolinder J, et al. Transplantation of porcine fetal pancreas to diabetic patients. Lancet. 1994;344:1402–1404
  78. Ohdan H, Yang YG, Shimizu A, Swenson KG, Sykes M. Mixed chimerism induced without lethal conditioning prevents T cell- and anti-Galα1,3Gal-mediated graft rejection. J Clin Invest. 1999;104:281–290
  79. Yang YG, deGoma E, Ohdan H, et al. Tolerization of anti-Galα1-3Gal natural antibody-forming B cells by induction of mixed chimerism. J Exp Med. 1998;187:1335–1342
  80. Bracy JL, Sachs DH, Iacomini J. Inhibition of xenoreactive natural antibody production by retroviral gene therapy. Science. 1998;281:845–847
  81. Bracy JL, Iacomini J. Induction of B-cell tolerance by retroviral gene therapy. Blood. 2000;96:3008–3015
  82. Ogawa H, Yin DP, Shen J, Galili U. Tolerance induction to a mammalian blood group-like carbohydrate antigen by syngeneic lymphocytes expressing the antigen. Blood. 2003;101:2318–2320
  83. Mohiuddin M, Ogawa H, Yin DP, Galili U. Tolerance induction to a mammalian blood group like carbohydrate antigen by syngeneic lymphocytes expressing the antigen: II. Tolerance induction on memory B cells. Blood. 2003;102:229–236
  84. Deriy L, Chen ZC, Gao GP, Galili U. Expression of α-gal epitopes on HeLa cells transduced with adenovirus containing α1,3galactosyltransferase cDNA. Glycobiology. 2002;12:135–144
  85. Ogawa H, Yin DP, Galili U. Induction of immune tolerance to a transplantation carbohydrate antigen by gene therapy with autologous lymphocytes transduced with adenovirus containing the corresponding glycosyltransferase gene. Gene Ther. 2004;11:292–301
  86. Yamamoto F, Clausen H, White T, Marken J, Hakomori S. Molecular genetic basis of the histo-blood group ABO system. Nature. 1990;345:229–233

PII: S1473-0502(06)00090-5

doi: 10.1016/j.transci.2006.05.007

Transfusion and Apheresis Science
Volume 35, Issue 1 , Pages 45-58 , August 2006

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