Xenotransplantation as a model of integrated, multidisciplinary research

Organogenesis

Volumn 5, Issue 1, 2009, Pages 14-22

  Cozzi, Emanuele ^a,b,c   Bosio, Erika ^b   Seveso, Michela ^c   Rubello, Domenico ^d   Ancona, Ermanno ^a,b,c  

^a UNIVERSITY HOSPITAL OF PADOVA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c CORIT   (Italy)

^d S MARIA DELLA MISERICORDIA HOSPITAL   (Italy)

Author keywords

Clinical trials; Ethics; Pig; Primate; Xenotransplantation

Indexed keywords

BELATACEPT; EVEROLIMUS; FINGOLIMOD; LEFLUNOMIDE; RAPAMYCIN;

CELL SURVIVAL; CLINICAL RESEARCH; ETHICS; GRAFT REJECTION; GRAFT SURVIVAL; IMMUNOLOGY; INTERVENTION STUDY; MODEL; NONHUMAN; ORGAN; PHYSIOLOGY; PRIMATE; REVIEW; RISK BENEFIT ANALYSIS; SAFETY; SWINE; XENOGRAFT; XENOTRANSPLANTATION;

ANIMALIA; PRIMATES; SUIDAE; SUS;

EID: 65949084500     PISSN: 15476278     EISSN: 15558592     Source Type: Journal    
DOI: 10.4161/org.7578     Document Type: Review

References (93)

1. Cooper DK, Ye Y, Rolf JLL, Zuhdi N. The pig as potential organ donor for man in Cooper DK, Kemp E, Reemtsma K and White DJ, eds. Xeno-transplantation. The transplantation of organs and tissues between species. 1st Springer-Verlag 1991; 481-500.
2. Abboud O, Abbud-Filho M, Abdramanov K, Abdulla S, Abraham G, Abueva A, et al. The Declaration of Istanbul on organ trafficking and transplant tourism. Kidney international 2008; 74:854-859
3. Hammer C. Physiological obstacles after xenotransplantation. Annals of the New York Academy of Sciences 1998; 862:19-27. (Pubitemid 29044008)
4. Hammer C. Xenotransplantation: facts and fiction. Annales chirurgiae et gynaecologiae 1997; 86:195-201.
5. Iverson WO, Talbot T. Definition of a production specification for xenotransplantation. A European perspective. Annals of the New York Academy of Sciences 1998; 862:121-124
6. Baldan N, Rigotti P, Calabrese F, Cadrobbi R, Dedja A, Iacopetti I, et al. Ureteral stenosis in HDAF pig-to-primate renal xenotransplantation: a phenomenon related to immunological events? Am J Transplant 2004; 4:475-481
7. Byrne GW, Davies WR, Oi K, Rao VP, Teotia SS, Ricci D, et al. Increased immunosuppression, not anticoagulation, extends cardiac xenograft survival. Transplantation 2006; 82:1787-1791
8. Barth RN, Yamamoto S, LaMattina JC, Kumagai N, Kitamura H, Vagefi PA, et al. Xenogeneic thymokidney and thymic tissue transplantation in a pig-to-baboon model: I. Evidence for pig-specific T-cell unresponsiveness. Transplantation 2003; 75:1615-1624
9. Lan P, Wang L, Diouf B, Eguchi H, Su H, Bronson R, et al. Induction of human T-cell tolerance to porcine xenoantigens through mixed hematopoietic chimerism. Blood 2004; 103:3964-3969
10. Sykes M, Shimizu I, Kawahara T. Mixed hematopoietic chimerism for the simultaneous induction of T and B cell tolerance. Transplantation 2005; 79:28-29 (Pubitemid 40293570)
11. Koch CA, Khalpey ZI, Platt JL. Accommodation: preventing injury in transplantation and disease. J Immunol 2004; 172:5143-5148
12. Gianello P, Dufrane D. Encapsulation of pig islets by alginate matrix to correct streptozotocin-induced diabetes in primates without immunosuppression. Presented at the Joint meeting of the International Xenotransplantation Association (IXA), the International Pancreas and Islet Transplant Association (IPITA), and the Cell Transplant Society (CTS). Minneapolis, MN, USA. Xenotransplantation 2007; 14:441.
13. Cozzi E, White DJ. The generation of transgenic pigs as potential organ donors for humans. Nature medicine 1995; 1:964-966
14. Platt JL, Lin SS, McGregor CG. Acute vascular rejection. Xenotransplantation 1998; 5:169-175 (Pubitemid 28444962)
15. Bach FH, Winkler H, Ferran C, Hancock WW, Robson SC. Delayed xenograft rejection. Immunol Today 1996; 17:379-384 (Pubitemid 26247798)
16. Pino-Chavez G. Differentiating acute humoral from acute cellular rejection histopathologically. Graft 2001; 4:60-62
17. 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; 52:214-220
18. Good AH, Cooper DK, Malcolm AJ, Ippolito RM, Koren E, Neethling FA, et al. Identification of carbohydrate structures that bind human antiporcine antibodies: implications for discordant xenografting in humans. Transplantation proceedings 1992; 24:559-562
19. 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 USA 1993; 90:11391-11395 (Pubitemid 23354435)
20. McCurry KR, Kooyman DL, Alvarado CG, Cotterell AH, Martin MJ, Logan JS, et al. Human complement regulatory proteins protect swine-to-primate cardiac xenografts from humoral injury. Nature medicine 1995; 1:423-427
21. Adams A, Pearson T, Larsen C. Conventional immunosuppression and co-stimulation blockade. Philos Trans R Soc Lond, B, Biol Sci 2001; 356:703-705
22. Diamond LE, McCurry KR, Martin MJ, McClellan SB, Oldham ER, Platt JL, et al. Characterization of transgenic pigs expressing functionally active human CD59 on cardiac endothelium. Transplantation 1996; 61:1241-1249
23. 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; 73:1146-1151 (Pubitemid 34415451)
24. 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; 6:194-200. (Pubitemid 29439065)
25. Shimizu A, Hisashi Y, Kuwaki K, Tseng YL, Dor FJ, Houser SL, et al. Thrombotic microangiopathy associated with humoral rejection of cardiac xenografts from alpha1,3-galactosyltransferase gene-knockout pigs in baboons. The American journal of pathology 2008; 172:1471-1481
26. Lam TT, Hausen B, Hook L, Lau M, Higgins J, Christians U, et al. The effect of soluble complement receptor type 1 on acute humoral xenograft rejection in hDAF-transgenic pig-to-primate life-supporting kidney xenografts. Xenotransplantation 2005; 12:20-29
27. Sharma A, Naziruddin B, Cui C, Martin MJ, Xu H, Wan H, et al. Pig cells that lack the gene for alpha1-3 galactosyltransferase express low levels of the gal antigen. Transplantation 2003; 75:430-436
28. Chen G, Qian H, Starzl T, Sun H, Garcia B, Wang X, Wet al. Acute rejection is associated with antibodies to non-Gal antigens in baboons using Gal-knockout pig kidneys. Nat Med 2005; 11:1295-1298
29. Robson SC, Cooper DK, d'Apice AJ. Disordered regulation of coagulation and platelet activation in xenotransplantation. Xenotransplantation 2000; 7:166-176
30. Buhler LH, Cooper DK. How strong is the T cell response in the pig-to-primate model? Xenotransplantation 2005; 12:85-87
31. Sebille F, Guillet M, Brouard S, Gagne K, Petzold T, Blancho G, et al. T-cell-mediated rejection of vascularized xenografts in the absence of induced anti-donor antibody response. Am J Transplant 2001; 1:21-28
32. Kuwaki K, Tseng YL, Dor FJ, Shimizu A, Houser SL, Sanderson TM, et al. Heart transplantation in baboons using alpha1,3-galactosyltransferase gene-knockout pigs as donors: initial experience. Nat Med 2005; 11:29-31. (Pubitemid 40215833)
33. Rayat GR, Rajotte RV, Hering BJ, Binette TM, Korbutt GS. In vitro and in vivo expression of Galalpha-(1,3)Gal on porcine islet cells is age dependent. J Endocrinol 2003; 177:127-135
34. Bennet W, Sundberg B, Lundgren T, Tibell A, Groth CG, Richards A, et al. 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; 69:711-719
35. Goto M, Johansson H, Maeda A, Elgue G, Korsgren O, Nilsson B. Low-molecular weight dextran sulfate abrogates the instant blood-mediated inflammatory reaction induced by adult porcine islets both in vitro and in vivo. Transplant Proc 2004; 36:1186-1187 (Pubitemid 38766317)
36. Cabric S, Sanchez J, Lundgren T, Foss A, Felldin M, Kallen R, et al. Islet Surface Heparinization Prevents the Instant Blood-Mediated Inflammatory Reaction in Islet Transplantation. Diabetes 2007.
37. Soderlund J, Wennberg L, Castanos-Velez E, Biberfeld P, Zhu S, Tibell A, et al. Fetal porcine islet-like cell clusters transplanted to cynomolgus monkeys: an immunohistochemical study. Transplantation 1999; 67:784-791
38. Kirchhof N, Shibata S, Wijkstrom M, Kulick DM, Salerno CT, Clemmings SM, et al. Reversal of diabetes in non-immunosuppressed rhesus macaques by intraportal porcine islet xenografts precedes acute cellular rejection. Xenotransplantation 2004; 11:396-407.
39. Solomon MF, Kuziel WA, Mann DA, Simeonovic CJ. The role of chemokines and their receptors in the rejection of pig islet tissue xenografts. Xenotransplantation 2003; 10:164-177 (Pubitemid 36903786)
40. Hering BJ, Wijkstrom M, Graham ML, Hardstedt M, Aasheim TC, Jie T, et al. Prolonged diabetes reversal after intraportal xenotransplantation of wild-type porcine islets in immunosuppressed nonhuman primates. Nat Med 2006; 12:301-303
41. Cardona K, Korbutt GS, Milas Z, Lyon J, Cano J, Jiang W, et al. Long-term survival of neonatal porcine islets in nonhuman primates by targeting costimulation pathways. Nat Med 2006; 12:304-306
42. Dufrane D, Goebbels RM, Saliez A, Guiot Y, Gianello P. Six-month survival of microencapsulated pig islets and alginate biocompatibility in primates: proof of concept. Transplantation 2006; 81:1345-1353 (Pubitemid 43804557)
43. Cardona K, Milas Z, Strobert E, Cano J, Jiang W, Safley SA, et al. Engraftment of adult porcine islet xenografts in diabetic nonhuman primates through targeting of costimulation pathways. Am J Transplant 2007; 7:2260-2268
44. Koyama I, Kawai T, Andrews D, Boskovic S, Nadazdin O, Wee SL, et al. Thrombophilia associated with anti-CD154 monoclonal antibody treatment and its prophylaxis in nonhuman primates. Transplantation 2004; 78:1238-1239
45. Sun Y, Ma X, Zhou D, Vacek I, Sun AM. Normalization of diabetes in spontaneously diabetic cynomologus monkeys by xenografts of microencapsulated porcine islets without immunosuppression. J Clin Invest 1996; 98:1417-1422 (Pubitemid 26322067)
46. Dwyer KM, Mysore TB, Crikis S, Robson SC, Nandurkar H, Cowan PJ, D'Apice AJ. The transgenic expression of human CD39 on murine islets inhibits clotting of human blood. Transplantation 2006; 82:428-432 (Pubitemid 44223045)
47. Klose R, Kemter E, Bedke T, Bittmann I, Kelsser B, Endres R, Pfeffer K, Schwinzer R, Wolf E. Expression of biologically active human TRAIL in transgenic pigs. Transplantation 2005; 80:222-230 (Pubitemid 41061679)
48. Tseng YL, Dor FJ, Kuwaki K, Ryan D, Wood J, Denaro M, et al. Bone marrow transplantation from alpha1,3-galactosyltransferase gene-knockout pigs in baboons. Xenotransplantation 2004; 11:361-370
49. Cosimi AB, Sachs DH. Mixed chimerism and transplantation tolerance. Transplantation 2004; 77:943-946 (Pubitemid 38436841)
50. Wood K. Is B cell tolerance essential for transplantation tolerance? Transplantation 2005; 79:40-42
51. Kawahara T, Shimizu I, Ohdan H, Zhao G, Sykes M. Differing mechanisms of early and late B cell hyporesponsiveness induced by mixed chimerism. Am J Transplant 2005; 5:2821-2829 (Pubitemid 43923942)
52. Yang YG, Sykes M. Xenotransplantation: current status and a perspective on the future. Nature reviews 2007; 7:519-531
53. Yamada K, Yazawa K, Shimizu A, Iwanaga T, Hisashi Y, Nuhn M, et al. 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; 11:32-34
54. Lee LA, Gritsch HA, Sergio JJ, Arn JS, Glaser RM, et al. Specific tolerance across a discordant xenogeneic transplantation barrier. Proceedings of the National Academy of Sciences of the United States of America 1994; 91:10864-10867
55. Nikolic B, Gardner JP, Scadden DT, Arn JS, Sachs DH, Sykes M. Normal development in porcine thymus grafts and specific tolerance of human T cells to porcine donor MHC. J Immunol 1999; 162:3402-3407 (Pubitemid 29313590)
56. Zhao Y, Swenson K, Sergio JJ, Arn JS, Sachs DH, Sykes M. Skin graft tolerance across a discordant xenogeneic barrier. Nature medicine 1996; 2:1211-1216 (Pubitemid 26375404)
57. Chen AM, Zhou Y, Swenson K, Sachs DH, Sykes M, Yang YG. Porcine stem cell engraftment and seeding of murine thymus with class II+ cells in mice expressing porcine cytokines: toward tolerance induction across discordant xenogeneic barriers. Transplantation 2000; 69:2484-2490 (Pubitemid 30482012)
58. + cell transplantation. Blood 2006; 108:487-492
59. Sykes M. Mixed chimerism and transplant tolerance. Immunity 2001; 14:417-424 (Pubitemid 32441594)
60. Mollnes TE, Fiane AE. Perspectives on complement in xenotransplantation. Mol Immunol 2003; 40:135-143 (Pubitemid 36959822)
61. Soin B, Smith KG, Zaidi A, Cozzi E, Bradley JR, Ostlie DJ, et al. Physiological aspects of pig-to-primate renal xenotransplantation. Kidney international 2001; 60:1592-1597
62. 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; 12:30-37
63. Robson SC, Young VK, Cook NS, Metternich R, Kasper-Konig W, Lesnikoski BA, et al. Thrombin inhibition in an ex vivo model of porcine heart xenograft hyperacute rejection. Transplantation 1996; 61:862-868
64. 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; 64:888-896
65. Kopp CW, Grey ST, Siegel JB, McShea A, Vetr H, Wrighton CJ, Set al. Expression of human thrombomodulin cofactor activity in porcine endothelial cells. Transplantation 1998; 66:244-251
66. Osborne FN, Kalsi KK, Lawson C, Lavitrano M, Yacoub MH, Rose ML, et al. Expression of human ecto-5′-nucleotidase in pig endothelium increases adenosine production and protects from NK cell-mediated lysis. Am J Transplant 2005; 5:1248-1255
67. Dwyer KM, Robson SC, Nandurkar HH, Campbell DJ, Gock H, Murray-Segal LJ,et al. Thromboregulatory manifestations in human CD39 transgenic mice and the implications for thrombotic disease and transplantation. The Journal of clinical investigation 2004; 113:1440-1446 (Pubitemid 39071699)
68. Chen D, Weber M, McVey JH, Kemball-Cook G, Tuddenham EG, Lechler RI, et al. Complete inhibition of acute humoral rejection using regulated expression of membrane-tethered anticoagulants on xenograft endothelium. Am J Transplant 2004; 4:1958-1963.
69. Toomey JR, Kratzer KE, Lasky NM, Broze GJ Jr. Effect of tissue factor deficiency on mouse and tumor development. Proceedings of the National Academy of Sciences of the United States of America 1997; 94:6922-6926 (Pubitemid 27281966)
70. Weiss EJ, Hamilton JR, Lease KE, Coughlin SR. Protection against thrombosis in mice lacking PAR3. Blood 2002; 100:3240-3244 (Pubitemid 35217073)
71. Mendicino M, Liu M, Ghanekar A, He W, Koscik C, Shalev I, Javadi M, et al. Targeted deletion of Fgl-2/fibroleukin in the donor modulates immunologic response and acute vascular rejection in cardiac xenografts. Circulation 2005; 112:248-256
72. McGregor CG, Davies WR, Oi K, Teotia SS, Schirmer JM, Risdahl JM, et al. Cardiac xenotransplantation: recent preclinical progress with 3-month median survival. The Journal of thoracic and cardiovascular surgery 2005; 130:844-851 (Pubitemid 41265729)
73. Palacios G, Druce J, Du L, Tran T, Birch C, Briese T, et al. A new arenavirus in a cluster of fatal transplant-associated diseases. The New England journal of medicine 2008; 358:991-998
74. Fishman JA, Patience C. Xenotransplantation: infectious risk revisited. Am J Transplant 2004; 4:1383-1390
75. Paradis K, Langford G, Long Z, Heneine W, Sandstrom P, Switzer WM, et al. Search for cross-species transmission of porcine endogenous retrovirus in patients treated with living pig tissue. The XEN 111 Study Group. Science (New York, NY) 1999; 285:1236-1241 (Pubitemid 29398604)
76. Wilhelm M, Fishman JA, Pontikis R, Aubertin AM, Wilhelm FX. Susceptibility of recombinant porcine endogenous retrovirus reverse transcriptase to nucleoside and non-nucleoside inhibitors. Cell Mol Life Sci 2002; 59:2184-2190 (Pubitemid 36140291)
77. Oldmixon BA, Wood JC, Ericsson TA, Wilson CA, White-Scharf ME, Andersson G, et al. Porcine endogenous retrovirus transmission characteristics of an inbred herd of miniature swine. Journal of virology 2002; 76:3045-3048 (Pubitemid 34184890)
78. Scobie L, Taylor S, Wood JC, Suling KM, Quinn G, Meikle S, et al. Absence of replication-competent human-tropic porcine endogenous retroviruses in the germ line DNA of inbred miniature Swine. Journal of virology 2004; 78:2502-2509 (Pubitemid 38228944)
79. Fiebig U, Stephan O, Kurth R, Denner J. Neutralizing antibodies against conserved domains of p15E of porcine endogenous retroviruses: basis for a vaccine for xenotransplantation? Virology 2003; 307:406-413
80. Komoda H, Miyagawa S, Omori T, Takahagi Y, Murakami H, Shigehisa T, et al. Survival of adult islet grafts from transgenic pigs with N-acetylglucosaminyltransferase-III (GnT-III) in cynomolgus monkeys. Xenotransplantation 2005; 12:209-216
81. Dieckhoff B, Petersen B, Kues WA, Kurth R, Niemann H, Denner J. Knockdown of porcine endogenous retrovirus (PERV) expression by PERV-specific shRNA in transgenic pigs. Xenotransplantation 2008; 15:36-45.
82. Wang D, Coscoy L, Zylberberg M, Avila PC, Boushey HA, Ganem D, et al. Microarray-based detection and genotyping of viral pathogens. Proceedings of the National Academy of Sciences of the United States of America 2002; 99:15687-15692
83. U.S. Public Health Service. PHS Guideline on Infectious Disease Issues in Xenotransplantation 2001; www4.od.nih.gov/oba/sacx/xenoguide01.pdf.
84. U.S. Department of Health and Human Services, Food and Drug Administration, Center for Biologics Evaluation and Research (CBER). Guidance for Industry-Source Animal, Product, Preclinical and Clinical Issues Concerning the Use of Xenotransplantation Products in Humans April 2003; http://www.fda.gov/cber/guidelines.htm.
85. COUNCIL OF EUROPE COMMITTEE OF MINISTERS. Recommendation Rec(2003)10 of the Committee of Ministers to Member States on Xenotransplantation 2003; http://www.legaltext.ee/text/en/K90038.htm.
86. World Health Organisation. Statement from the xenotransplantation advisory consultation. Geneva April 18-20 2005; http://www.who.int/ transplantation/xeno/en/.
87. Sykes M, d'Apice A, Sandrin M. Position paper of the Ethics Committee of the International Xenotransplantation Association. Xenotransplantation 2003; 10:194-203.
88. Sykes M, Sandrin M, D'Apice A. Guidelines for xenotransplantation. The New England journal of medicine 2003; 349:1294-1295 (Pubitemid 37152046)
89. Sykes M, Sandrin M, Cozzi E, Rees MA. World Health Organization resolution on xenotransplantation. Xenotransplantation 2004; 11:224-225 (Pubitemid 38623055)
90. d'Apice AJ, Cowan PJ. Gene-modified pigs. Xenotransplantation 2008; 15:87-90.
91. Nottle MB, Beebe LF, Harrison SJ, McIlfatrick SM, Ashman RJ, O'Connell PJ, et al. Production of homozygous alpha-1,3-galactosyltransferase knockout pigs by breeding and somatic cell nuclear transfer. Xenotransplantation 2007; 14:339-344
92. Lavitrano M, Busnelli M, Cerrito MG, Giovannoni R, Manzini S, Vargiolu A. Sperm-mediated gene transfer. Reproduction, fertility and development 2006; 18:19-23.
93. Martin C, Plat M, Nerriere-Daguin V, Coulon F, Uzbekova S, Venturi E, et al. Transgenic expression of CTLA4-Ig by fetal pig neurons for xenotransplantation. Transgenic research 2005; 14:373-384