Spectrum of the early xenograft response: From hyperacute rejection to delayed xenograft injury

Critical Reviews in Immunology

Volumn 27, Issue 2, 2007, Pages 153-166

  Ierino, Francesco L ^a   Sandrin, Mauro S ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Antibody mediated rejection; Carbohydrate antigens; Coagulation; Vascular rejection

Indexed keywords

CARBOHYDRATE ANTIGEN; COMPLEMENT; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN M ANTIBODY;

ANTIBODY RESPONSE; ANTIGEN BINDING; BLOOD CLOTTING; DNA MODIFICATION; GRAFT SURVIVAL; HYPERACUTE GRAFT REJECTION; INFLAMMATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; THROMBOTIC THROMBOCYTOPENIC PURPURA; XENOGRAFT; XENOTRANSPLANTATION;

EID: 34347360550     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: 10.1615/critrevimmunol.v27.i2.30     Document Type: Review

References (113)

1. Calne RY. Organ transplantation between widely disparate species. Transplant Proc. 1970;2(4):550-6.
2. Murray JE, Merrill JP, Dammin GJ, Dealy JB Jr, Walter CW, Brooke MS, Wilson RE. Study on transplantation immunity after total body irradiation: clinical and experimental investigation. Surgery. 1960;48:272-84.
3. Starzl TE, Marchioro TL, Holmes JH, Hermann G, Brittain RS, Stonington OH, Talmage DW, Waddell WR. Renal Homografts in Patients with Major Donor-Recipient Blood Group Incompatibilities. Surgery. 1964;55:195-200.
4. Hume DM, Merrill JP, Miller BF, Thorn GW. Experiences with renal homotransplantation in the human: report of nine cases. J Clin Invest. 1955;34(2):327-82.
5. Milland J, Sandrin MS. ABO blood group and related antigens, natural antibodies and transplantation. Tissue Antigens. 2006;68(6):459-66.
6. Good AH, Cooper DK, 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. Transplant Proc. 1992;24(2):559-62.
7. Oriol R, Ye Y, Koren E, Cooper DK. Carbohydrate antigens of pig tissues reacting with human natural antibodies as potential targets for hyperacute vascular rejection in pig-to-man organ xenotransplantation. Transplantation. 1993;56(6):1433-42.
8. Sandrin MS, Vaughan HA, Dabkowski PL, McKenzie IF. Anti-pig IgM antibodies in human serum react predominantly with Gal(alpha 1-3)Gal epitopes. Proc Natl Acad Sci U S A. 1993;90(23):11391-5.
9. Sandrin MS, McKenzie IF. Gal alpha (1,3)Gal, the major xenoantigen(s) recognised in pigs by human natural antibodies. Immunol Rev. 1994;141:169-90.
10. Vaughan HA, Loveland BE, Sandrin MS. Gal alpha(1,3)Gal is the major xenoepitope expressed on pig endothelial cells recognized by naturally occurring cytotoxic human antibodies. Transplantation. 1994;58(8):879-82.
11. Milland J, Christiansen D, Lazarus BD, Taylor SG, Xing PX, Sandrin MS. The molecular basis for galalpha(1,3)gal expression in animals with a deletion of the alpha1,3galactosyltransferase gene. J Immunol. 2006;176(4):2448-54.
12. Sharma A, Naziruddin B, Cui C, Martin MJ, Xu H, Wan H, Lei Y, Harrison C, Yin J, Okabe J, Mathews C, Stark A, Adams CS, Houtz J, Wiseman BS, Byrne GW, Logan JS. Pig cells that lack the gene for alpha1-3 galactosyltransferase express low levels of the gal antigen. Transplantation. 2003;75(4):430-6.
13. Chen G, Sun H, Yang H, Kubelik D, Garcia B, Luo Y, Xiang Y, Qian A, Copeman L, Liu W, Cardella CJ, Wang W, Xiong Y, Wall W, White DJ, Zhong R. The role of anti-non-Gal antibodies in the development of acute humoral xenograft rejection of hDAF transgenic porcine kidneys in baboons receiving anti-Gal antibody neutralization therapy. Transplantation. 2006;81(2):273-83.
14. Tseng YL, Moran K, Dor FJ, Sanderson TM, Li W, Lancos CJ, Schuurman HJ, Sachs DH, Cooper DK. Elicited antibodies in baboons exposed to tissues from alpha1,3-galactosyltransferase gene-knockout pigs. Transplantation. 2006;81(7):1058-62.
15. Buhler L, Xu Y, Li W, Zhu A, Cooper DK. An investigation of the specificity of induced anti-pig antibodies in baboons. Xenotransplantation. 2003;10(1):88-93.
16. Gollackner B, Goh SK, Qawi I, Buhler L, Knosalla C, Daniel S, Kaczmarek E, Awwad M, Cooper DK, Robson SC. Acute vascular rejection of xenografts: roles of natural and elicited xenoreactive antibodies in activation of vascular endothelial cells and induction of procoagulant activity. Transplantation. 2004;77(11):1735-41.
17. Chen G, Qian H, Starzl T, Sun H, Garcia B, Wang X, Wise Y, Liu Y, Xiang Y, Copeman L, Liu W, Jevnikar A, Wall W, Cooper DK, Murase N, Dai Y, Wang W, Xiong Y, White DJ, Zhong R. Acute rejection is associated with antibodies to non-Gal antigens in baboons using Gal-knockout pig kidneys. Nat Med. 2005;11(12):1295-8.
18. Dehoux JP, de la Parra B, Latinne D, Bazin H, Gianello P. Characterization of baboon anti-porcine IgG antibodies during acute vascular rejection of porcine kidney xenograft. Xenotransplantation. 2002;9(5):338-49.
19. McCurry KR, Parker W, Cotterell AH, Weidner BC, Lin SS, Daniels LJ, Holzknecht ZE, Byrne GW, Diamond LE, Logan JS, Platt JL. Humoral responses to pig-to-baboon cardiac transplantation: implications for the pathogenesis and treatment of acute vascular rejection and for accommodation. Hum Immunol. 1997;58(2):91-105.
20. Platt JL, Bach FH. The barrier to xenotransplantation. Transplantation. 1991;52(6):937-47.
21. Platt JL, Fischel RJ, Matas AJ, Reif SA, Bolman RM, Bach FH. Immunopathology of hyperacute xenograft rejection in a swine-to-primate model. Transplantation. 1991;52(2):214-20.
22. Chen RH, Naficy S, Logan JS, Diamond LE, Adams DH. Hearts from transgenic pigs constructed with CD59/DAF genomic clones demonstrate improved survival in primates. Xenotransplantation. 1999;6(3):194-200.
23. 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. Nat Med. 1995;1(5):423-7.
24. Schuurman HJ, Pino-Chavez G, Phillips MJ, Thomas L, White DJ, Cozzi E. Incidence of hyperacute rejection in pig-to-primate transplantation using organs from hDAF-transgenic donors. Transplantation. 2002;73(7):1146-51.
25. Kroshus TJ, Bolman RM, III, Dalmasso AP, Rollins SA, Guilmette ER, Williams BL, Squinto SP, Fodor WL. Expression of human CD59 in transgenic pig organs enhances organ survival in an ex vivo xenogeneic perfusion model. Transplantation. 1996;61(10):1513-21.
26. Diamond LE, McCurry KR, Martin MJ, McClellan SB, Oldham ER, Platt JL, Logan JS. Characterization of transgenic pigs expressing functionally active human CD59 on cardiac endothelium. Transplantation. 1996;61(8):1241-9.
27. van Denderen BJ, Pearse MJ, Katerelos M, Nottle MB, Du ZT, Aminian A, Adam WR, Shenoy-Scaria A, Lublin DM, Shinkel TA, d'Apice AJ. Expression of functional decay-accelerating factor (CD55) in transgenic mice protects against human complement-mediated attack. Transplantation. 1996;61(4):582-8.
28. Byrne GW, McCurry KR, Martin MJ, McClellan SM, Platt JL, Logan JS. Transgenic pigs expressing human CD59 and decay-accelerating factor produce an intrinsic barrier to complement-mediated damage. Transplantation. 1997;63(1):149-55.
29. Storck M, Abendroth D, Prestel R, Pino-Chavez G, Muller-Hoker J, White DJ, Hammer C. Morphology of hDAF (CD55) transgenic pig kidneys following ex-vivo hemoperfusion with human blood. Transplantation. 1997;63(2):304-10.
30. Schmoeckel M, Nollert G, Shahmohammadi M, Young VK, Chavez G, Kasper-Konig W, White DJ, Muller-Hocker J, Arendt RM, Wilbert-Lampen U, Hammer C, Reichart B. Prevention of hyperacute rejection by human decay accelerating factor in xenogeneic perfused working hearts. Transplantation. 1996;62(6):729-34.
31. Pruitt SK, Bollinger RR, Collins BH, Marsh HC Jr, Levin JL, Rudolph AR, Baldwin WM, 3rd, Sanfilippo F. Effect of continuous complement inhibition using soluble complement receptor type 1 on survival of pig-to-primate cardiac xenografts. Transplantation. 1997 Mar 27;63(6):900-2.
32. Davis EA, Pruitt SK, Greene PS, Ibrahim S, Lam TT, Levin JL, Baldwin WM, 3rd, Sanfilippo F. Inhibition of complement, evoked antibody, and cellular response prevents rejection of pig-to-primate cardiac xenografts. Transplantation. 1996;62(7):1018-23.
33. 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. 1991;52(3):530-3.
34. Loveland BE, Milland J, Kyriakou P, Thorley BR, Christiansen D, Lanteri MB, Regensburg M, Duffield M, French AJ, Williams L, Baker L, Brandon MR, Xing PX, Kahn D, McKenzie IF. Characterization of a CD46 transgenic pig and protection of transgenic kidneys against hyperacute rejection in non-immunosuppressed baboons. Xenotransplantation. 2004;11(2):171-83.
35. Cowan PJ, Aminian A, Barlow H, Brown AA, Chen CG, Fisicaro N, Francis DM, Goodman DJ, Han W, Kurek M, Nottle MB, Pearse MJ, Salvaris E, Shinkel TA, Stainsby GV, Stewart AB, d'Apice AJ. Renal xenografts from triple-transgenic pigs are not hyperacutely rejected but cause coagulopathy in non-immunosuppressed baboons. Transplantation. 2000;69(12):2504-15.
36. Ierino FL, Kozlowski T, Siegel JB, Shimizu A, Colvin RB, Banerjee PT, Cooper DK, Cosimi AB, Bach FH, Sachs DH, SC. R. Disseminated intravascular coagulation in association with the delayed rejection of pig-to-baboon renal xenografts. Transplantation. 1998;66(11):1439-50.
37. Robson SC, Cooper DK, d'Apice AJ. Disordered regulation of coagulation and platelet activation in xenotransplantation. Xenotransplantation. 2000;7(3):166-76.
38. Gaca JG, Lesher A, Aksoy O, Gonzalez-Stawinski GV, Platt JL, Lawson JH, Parker W, Davis RD. Disseminated intravascular coagulation in association with pig-to-primate pulmonary xenotransplantation. Transplantation. 2002;73(11):1717-23.
39. Kozlowski T, Shimizu A, Lambrigts D, Yamada K, Fuchimoto Y, Glaser R, Monroy R, Xu Y, Awwad M, Colvin RB, Cosimi AB, Robson SC, Fishman J, Spitzer TR, Cooper DK, Sachs DH. Porcine kidney and heart transplantation in baboons undergoing a tolerance induction regimen and antibody adsorption. Transplantation. 1999;67(1):18-30.
40. Buhler L, Basker M, Alwayn IP, Goepfert C, Kitamura H, Kawai T, Gojo S, Kozlowski T, Ierino FL, Awwad M, Sachs DH, Sackstein R, Robson SC, Cooper DK. Coagulation and thrombotic disorders associated with pig organ and hematopoietic cell transplantation in nonhuman primates. Transplantation. 2000;70(9):1323-31.
41. Alwayn IP, Buhler L, Basker M, Goepfert C, Kawai T, Kozlowski T, Ierino F, Sachs DH, Sackstein R, Robson SC, Cooper DK. Coagulation/thrombotic disorders associated with organ and cell xenotransplantation. Transplant Proc. 2000;32(5):1099.
42. Ikeda K, Nagasawa K, Horiuchi T, Tsuru T, Nishizaka H, Niho Y. C5a induces tissue factor activity on endothelial cells. Thromb Haemost. 1997;77(2):394-8.
43. 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. 1990;171(4):1363-8.
44. Smolenski R, Kochan Z, Karbowska J, Slominska E, Forni M, Kalsi K, Bacci ML, Lavitrano M, Yacoub MH. Low expression of ecto-5′-nucleotidase in the pig heart - a potential barrier to xenotransplantation. J Heart Lung Transplant. 2001;20(2):214-5.
45. Robson SC, Kaczmarek E, Siegel JB, Candinas D, Koziak K, Millan M, Hancock WW, Bach FH. Loss of ATP diphosphohydrolase activity with endothelial cell activation. J Exp Med. 1997;185(1):153-63.
46. Kopp CW, Siegel JB, Hancock WW, Anrather J, Winkler H, Geczy CL, Kaczmarek E, Bach FH, Robson SC. Effect of porcine endothelial tissue factor pathway inhibitor on human coagulation factors. Transplantation. 1997 Mar 15;63(5):749-58.
47. Siegel JB, Grey ST, Lesnikoski BA, Kopp CW, Soares M, Schulte am Esch J, 2nd, Bach FH, Robson SC. Xenogeneic endothelial cells activate human prothrombin. Transplantation. 1997;64(6):888-96.
48. Lawson JH, Platt JL. Molecular barriers to xenotransplantation. Transplantation. 1996;62(3):303-10.
49. Schulte Am Esch J, 2nd, Robson SC, Knoefel WT, Hosch SB, Rogiers X. O-linked glycosylation and functional incompatibility of porcine von Willebrand factor for human platelet GPIb receptors. Xenotransplantation. 2005;12(1):30-7.
50. Schulte am Esch J, 2nd, Cruz MA, Siegel JB, Anrather J, Robson SC. Activation of human platelets by the membrane-expressed A1 domain of von Willebrand factor. Blood. 1997;90(11):4425-37.
51. Pareti FI, Mazzucato M, Bottini E, Mannucci PM. Interaction of porcine von Willebrand factor with the platelet glycoproteins Ib and IIb/IIIa complex. Br J Haematol. 1992;82(1):81-6.
52. Mazzucato M, De Marco L, Pradella P, Masotti A, Pareti FI. Porcine von Willebrand factor binding to human platelet GPIb induces transmembrane calcium influx. Thromb Haemost. 1996;75(4):655-60.
53. 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-Gal:beta-D-Gal(1,4)-D-GlcNAc alpha(1,3)-galactosyltransferase cDNA. J Biol Chem. 1990;265(12):7055-61.
54. Joziasse DH, Shaper JH, Jabs EW, Shaper NL. Characterization of an alpha 1 - 3-galactosyltransferase homologue on human chromosome 12 that is organized as a processed pseudogene. J Biol Chem. 1991;266(11):6991-8.
55. Galili U, Swanson K. Gene sequences suggest inactivation of alpha-1,3-galactosyltransferase in catarrhines after the divergence of apes from monkeys. Proc Natl Acad Sci U S A. 1991;88(16):7401-4.
56. Minanov OP, Itescu S, Neethling FA, Morgenthau AS, Kwiatkowski P, Cooper DK, Michler RE. Anti-GaL IgG antibodies in sera of newborn humans and baboons and its significance in pig xenotransplantation. Transplantation. 1997;63(2):182-6.
57. Xu H, Edwards NM, Chen JM, Dong X, Michler RE. Natural antipig xenoantibody is absent in neonatal human serum. J Heart Lung Transplant. 1995;14(4):749-54.
58. Kaplon RJ, Michler RE, Xu H, Kwiatkowski PA, Edwards NM, Platt JL. Absence of hyperacute rejection in newborn pig-to-baboon cardiac xenografts. Transplantation. 1995;59(1):1-6.
59. Parker W, Bruno D, Holzknecht ZE, Platt JL. Characterization and affinity isolation of xenoreactive human natural antibodies. J Immunol. 1994;153(8):3791-803.
60. Winn HJ, Baldamus CA, Jooste SV, Russell PS. Acute destruction by humoral antibody of rat skin grafted to mice. J Exp Med. 1973;137(4):893-910.
61. Koch CA, Khalpey ZI, Platt JL. Accommodation: preventing injury in transplantation and disease. J Immunol. 2004;172(9):5143-8.
62. Johnsson C, Andersson A, Bersztel A, Karlsson-Parra A, Gannedahl G, Tufveson G. Successful retransplantation of mouse-to-rat cardiac xenografts under immunosuppressive monotherapy with cyclosporine. Transplantation. 1997;63(5):652-6.
63. Dalmasso AP, Benson BA, Johnson JS, Lancto C, Abrahamsen MS. Resistance against the membrane attack complex of complement induced in porcine endothelial cells with a Gal alpha(1-3)Gal binding lectin: up-regulation of CD59 expression. J Immunol. 2000;164(7):3764-73.
64. Shibata T, Cosio FG, Birmingham DJ. Complement activation induces the expression of decay-accelerating factor on human mesangial cells. J Immunol. 1991;147(11):3901-8.
65. Bach FH, Ferran C, Candinas D, Miyatake T, Koyamada N, Mark W, Hechenleitner P, Hancock WW. Accommodation of xenografts: expression of "protective genes" in endothelial and smooth muscle cells. Transplant Proc. 1997;29(1-2):56-8.
66. Bach FH, Ferran C, Hechenleitner P, Mark W, Koyamada N, Miyatake T, Winkler H, Badrichani A, Candinas D, Hancock WW. Accommodation of vascularized xenografts: expression of "protective genes" by donor endothelial cells in a host Th2 cytokine environment. Nat Med. 1997;3(2):196-204.
67. Bach FH, Hancock WW, Ferran C. Protective genes expressed in endothelial cells: a regulatory response to injury. Immunol Today. 1997;18(10):483-6.
68. Williams JM, Holzknecht ZE, Plummer TB, Lin SS, Brunn GJ, Platt JL. Acute vascular rejection and accommodation: divergent outcomes of the humoral response to organ transplantation. Transplantation. 2004;78(10):1471-8.
69. Bannett AD, McAlack RF, Morris M, Chopek MW, Platt JL. ABO incompatible renal transplantation: a qualitative analysis of native endothelial tissue ABO antigens after transplantation. Transplant Proc. 1989;21(1 Pt 1):783-5.
70. Park WD, Grande JP, Ninova D, Nath KA, Platt JL, Gloor JM, Stegall MD. Accommodation in ABO-incompatible kidney allografts, a novel mechanism of self-protection against antibody-mediated injury. Am J Transplant. 2003;3(8):952-60.
71. King KE, Warren DS, Samaniego-Picota M, Campbell-Lee S, Montgomery RA, Baldwin WM, 3rd. Antibody, complement and accommodation in ABO-incompatible transplants. Curr Opin Immunol. 2004;16(5):545-9.
72. Brenner P, Hinz M, Huber H, Schmoeckel M, Reichenspurner H, Meiser B, Hammer C, Reichart B. The influence of antibody and complement removal with a Ig-Therasorb column in a xenogeneic working heart model. Eur J Cardiothorac Surg. 1999;15(5):672-9.
73. Kozlowski T, Ierino FL, Lambrigts D, Foley A, Andrews D, Awwad M, Monroy R, Cosimi AB, Cooper DK, Sachs DH. Depletion of anti-Gal(alpha)1-3Gal antibody in baboons by specific alpha-Gal immunoaffinity columns. Xenotransplantation. 1998;5(2):122-31.
74. Taniguchi S, Neethling FA, Korchagina EY, Bovin N, Ye Y, Kobayashi T, Niekrasz M, Li S, Koren E, Oriol R, Cooper DK. In vivo immunoadsorption of antipig antibodies in baboons using a specific Gal(alpha)1-3Gal column. Transplantation. 1996;62(10):1379-84.
75. Simon PM, Neethling FA, Taniguchi S, Goode PL, Zopf D, Hancock WW, Cooper DK. Intravenous infusion of Galalpha1-3Gal oligosaccharides in baboons delays hyperacute rejection of porcine heart xenografts. Transplantation. 1998;65(3):346-53.
76. McCurry KR, Kooyman DL, Diamond LE, Byrne GW, Martin MJ, Logan JS, Platt JL. Human complement regulatory proteins in transgenic animals regulate complement activation in xenoperfused organs. Transplant Proc. 1995;27(1):317-8.
77. Phelps CJ, Koike C, Vaught TD, Boone J, Wells KD, Chen SH, Ball S, Specht SM, Polejaeva IA, Monahan JA, Jobst PM, Sharma SB, Lamborn AE, Garst AS, Moore M, Demetris AJ, Rudert WA, Bottino R, Bertera S, Trucco M, Starzl TE, Dai Y, Ayares DL. Production of alpha 1,3-galactosyltransferase-deficient pigs. Science. 2003;299(5605):411-4.
78. Kolber-Simonds D, Lai L, Watt SR, Denaro M, Arn S, Augenstein ML, Betthauser J, Carter DB, Greenstein JL, Hao Y, Im GS, Liu Z, Mell GD, Murphy CN, Park KW, Rieke A, Ryan DJ, Sachs DH, Forsberg EJ, Prather RS, Hawley RJ. Production of alpha-1,3-galactosyltransferase null pigs by means of nuclear transfer with fibroblasts bearing loss of heterozygosity mutations. Proc Natl Acad Sci U S A. 2004;101(19):7335-40.
79. Lai L, Kolber-Simonds D, Park KW, Cheong HT, Greenstein JL, Im GS, Samuel M, Bonk A, Rieke A, Day BN, Murphy CN, Carter DB, Hawley RJ, Prather RS. Production of alpha-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning. Science. 2002;295(5557):1089-92.
80. Dai Y, Vaught TD, Boone J, Chen SH, Phelps CJ, Ball S, Monahan JA, Jobst PM, McCreath KJ, Lamborn AE, Cowell-Lucero JL, Wells KD, Colman A, Polejaeva IA, Ayares DL. Targeted disruption of the alpha1,3-galactosyltransferase gene in cloned pigs. Nat Biotechnol. 2002 Mar;20(3):251-5.
81. Kuwaki K, Tseng YL, Dor FJ, Shimizu A, Houser SL, Sanderson TM, Lancos CJ, Prabharasuth DD, Cheng J, Moran K, Hisashi Y, Mueller N, Yamada K, Greenstein JL, Hawley RJ, Patience C, Awwad M, Fishman JA, Robson SC, Schuurman HJ, Sachs DH, Cooper DK. Heart transplantation in baboons using alpha1,3-galactosyltransferase gene-knockout pigs as donors: initial experience. Nat Med. 2005;11(1):29-31.
82. Yamada K, Yazawa K, Shimizu A, Iwanaga T, Hisashi Y, Nuhn M, O'Malley P, Nobori S, Vagefi PA, Patience C, Fishman J, Cooper DK, Hawley RJ, Greenstein J, Schuurman HJ, Awwad M, Sykes M, Sachs DH. Marked prolongation of porcine renal xenograft survival in baboons through the use of alpha1,3-galactosyltransferase gene-knockout donors and the cotransplantation of vascularized thymic tissue. Nat Med. 2005;11(1):32-4.
83. McGregor CG, Tazelaar HD, Rao VP, Ricci D, Miyagi N, Gazi M, Whelan S, Edgerton S, Byrne GW. Gene-knockout (GT-KO) heterotopic cardiac xenotransplantation: are GT-KO pigs essential for successful clinical xenotransplantation? Xenotransplantation. 2007;14(2):181-2.
84. Keusch JJ, Manzella SM, Nyame KA, Cummings RD, Baenziger JU. Expression cloning of a new member of the ABO blood group glycosyltransferases, iGb3 synthase, that directs the synthesis of isoglobo-glycosphingolipids. J Biol Chem. 2000;275(33):25308-14.
85. Taylor SG, McKenzie IF, Sandrin MS. Characterization of the rat alpha(1,3)galactosyltransferase: evidence for two independent genes encoding glycosyltransferases that synthesize Galalpha(1,3)Gal by two separate glycosylation pathways. Glycobiology. 2003;13(5):327-37.
86. Kojima Y, Fukumoto S, Furukawa K, Okajima T, Wiels J, Yokoyama K, Suzuki Y, Urano T, Ohta M, Furukawa K. Molecular cloning of globotriaosylceramide/CD77 synthase, a glycosyltransferase that initiates the synthesis of globo series glycosphingolipids. J Biol Chem. 2000;275(20):15152-6.
87. Zhou D, Mattner J, Cantu C, 3rd, Schrantz N, Yin N, Gao Y, Sagiv Y, Hudspeth K, Wu YP, Yamashita T, Teneberg S, Wang D, Proia RL, Levery SB, Savage PB, Teyton L, Bendelac A. Lysosomal glycosphingo-lipid recognition by NKT cells. Science. 2004;306(5702):1786-9.
88. Kroshus TJ, Salerno CT, Yeh CG, Higgins PJ, Bolman RM III, Dalmasso AP. A recombinant soluble chimeric complement inhibitor composed of human CD46 and CD55 reduces acute cardiac tissue injury in models of pig-to-human heart transplantation. Transplantation. 2000;69(11):2282-9.
89. Lau CL, Daggett WC, Yeatman MF, Chai P, Lin SS, Lodge AJ, Chen EP, Diamond LE, Byrne GW, Logan JS, Parker W, Platt JL, Davis RD. The role of antibodies in dysfunction of pig-to-baboon pulmonary transplants. J Thorac Cardiovasc Surg. 2000;120(1):29-38.
90. McKenzie IF, Patton K, Smit JA, Mouhtouris E, Xing P, Myburgh JA, Sandrin MS. Definition and characterization of chicken Gal alpha(1,3)Gal antibodies. Transplantation. 1999 Mar 27;67(6):864-70.
91. Crikis S, Cowan PJ, d'Apice AJ. Intravascular thrombosis in discordant xenotransplantation. Transplantation. 2006;82(9):1119-23.
92. Shimizu A, Yamada K, Yamamoto S, Lavelle JM, Barth RN, Robson SC, Sachs DH, Colvin RB. Thrombotic microangiopathic glomerulopathy in human decay accelerating factor-transgenic swine-to-baboon kidney xenografts. J Am Soc Nephrol. 2005;16(9):2732-45.
93. Fryer JP, Leventhal JR, Dalmasso AP, Chen S, Simone PA, Goswitz JJ, Reinsmoen NL, Matas AJ. Beyond hyperacute rejection. Accelerated rejection in a discordant xenograft model by adoptive transfer of specific cell subsets. Transplantation. 1995;59(2):171-6.
94. Fryer JP, Chen S, Johnson EM, Simone P, Matas AJ. The role of macrophages in endothelial cell injury - a possible mechanism for delayed xenograft rejection. Transplant Proc. 1996;28(2):626.
95. Millan MT, Geczy C, Stuhlmeier KM, Goodman DJ, Ferran C, Bach FH. Human monocytes activate porcine endothelial cells, resulting in increased E-selectin, interleukin-8, monocyte chemotactic protein-1, and plasminogen activator inhibitor-type-1 expression. Transplantation. 1997;63(3):421-9.
96. Malyguine AM, Saadi S, Platt JL, Dawson JR. Human natural killer cells induce morphologic changes in porcine endothelial cell monolayers. Transplantation. 1996;61(1):161-4.
97. Goodman DJ, Von Albertini M, Willson A, Millan MT, Bach FH. Direct activation of porcine endothelial cells by human natural killer cells. Transplantation. 1996;61(5):763-71.
98. Schaapherder AF, Daha MR, te Bulte MT, van der Woude FJ, Gooszen HG. Antibody-dependent cell-mediated cytotoxicity against porcine endothelium induced by a majority of human sera. Transplantation. 1994;57(9):1376-82.
99. Watier H, Guillaumin JM, Vallee I, Thibault G, Gruel Y, Lebranchu Y, Bardos P. Human NK cell-mediated direct and IgG-dependent cytotoxicity against xenogeneic porcine endothelial cells. Transpl Immunol. 1996;4(4):293-9.
100. Leventhal JR, Dalmasso AP, Cromwell JW, Platt JL, Manivel CJ, Bolman RM, 3rd, Matas AJ. Prolongation of cardiac xenograft survival by depletion of complement. Transplantation. 1993;55(4):857-65; discussion 65-6.
101. Leventhal JR, Matas AJ, Sun LH, Reif S, Bolman RM, 3rd, Dalmasso AP, Platt JL. The immunopathology of cardiac xenograft rejection in the guinea pig-to-rat model. Transplantation. 1993;56(1):1-8.
102. Xia G, Ji P, Rutgeerts O, Waer M. Natural killer cell- and macrophage mediated discordant guinea pig→ rat xenograft rejection in the absence of complement, xenoantibody and T cell immunity. Transplantation. 2000;70(1):86-93.
103. Minanov OP, Artrip JH, Szabolcs M, Kwiatkowski PA, Galili U, Itescu S, Michler RE. Triple immunosuppression reduces mononuclear cell infiltration and prolongs graft life in pig-to-newborn baboon cardiac xenotransplantation. J Thorac Cardiovasc Surg. 1998;115(5):998-1006.
104. Shimizu A, Meehan SM, Kozlowski T, Sablinski T, Ierino FL, Cooper DK, Sachs DH, Colvin RB. Acute humoral xenograft rejection: destruction of the microvascular capillary endothelium in pig-to-nonhuman primate renal grafts. Lab Invest. 2000;80(6):815-30.
105. Rieben R, Seebach JD. Xenograft rejection: IgG1, complement and NK cells team up to activate and destroy the endothelium. Trends Immunol. 2005;26(1):2-5.
106. Bennet W, Sundberg B, Lundgren T, Tibell A, Groth CG, Richards A, White DJ, Elgue G, Larsson R, Nilsson B, Korsgren O. Damage to porcine islets of Langerhans after exposure to human blood in vitro, or after intraportal transplantation to cynomologus monkeys: protective effects of sCR1 and heparin. Transplantation. 2000;69(5):711-9.
107. Hering BJ, Wijkstrom M, Graham ML, Hardstedt M, Aasheim TC, Jie T, Ansite JD, Nakano M, Cheng J, Li W, Moran K, Christians U, Finnegan C, Mills CD, Sutherland DE, Bansal-Pakala P, Murtaugh MP, Kirchhof N, Schuurman HJ. Prolonged diabetes reversal after intraportal xenotransplantation of wild-type porcine islets in immunosuppressed nonhuman primates. Nat Med. 2006;12(3):301-3.
108. Buhler L, Goepfert C, Kitamura H, Basker M, Gojo S, Alwayn IP, Chang Q, Down JD, Tsai H, Wise R, Sachs DH, Cooper DK, Robson SC, Sackstein R. Porcine hematopoietic cell xenotransplantation in nonhuman primates is complicated by thrombotic microangiopathy. Bone Marrow Transplant. 2001;27(12):1227-36.
109. Alwayn IP, Buhler L, Appel JZ, 3rd, Goepfert C, Csizmadia E, Correa L, Harper D, Kitamura H, Down J, Awwad M, Sackstein R, Cooper DK, Robson SC. Mechanisms of thrombotic microangiopathy following xenogeneic hematopoietic progenitor cell transplantation. Transplantation. 2001;71(11):1601-9.
110. Appel JZ, 3rd, Newman D, Awwad M, Kruger Gray HS, Down J, Cooper DK, Robson SC. Activation of human endothelial cells by mobilized porcine leukocytes in vitro: implications for mixed chimerism in xenotransplantation. Transplantation. 2002;73(8):1302-9.
111. Knosalla C, Giovino MA, Harper D, Kaczmarek E, Gollackner B, Cooper DK, Robson SC. Relative effects of GAL+ and GALlow/- porcine hematopoietic cells on primate platelet aggregation and endothelial cell activation: implications for the induction of mixed hematopoietic chimerism in the pig-to-primate model. Xenotransplantation. 2004;11(1):72-7.
112. Tseng YL, Dor FJ, Kuwaki K, Ryan D, Wood J, Denaro M, Giovino M, Yamada K, Hawley R, Patience C, Schuurman HJ, Awwad M, Sachs DH, Cooper DK. Bone marrow transplantation from alpha1,3-galactosyltransferase gene-knockout pigs in baboons. Xenotransplantation. 2004;11(4):361-70.
113. Tseng YL, Sachs DH, Cooper DK. Porcine hematopoietic progenitor cell transplantation in nonhuman primates: a review of progress. Transplantation. 2005;79(1):1-9.