Development of a consensus protocol to quantify primate anti-non-Gal xenoreactive antibodies using pig aortic endothelial cells

Xenotransplantation

Volumn 21, Issue 6, 2014, Pages 555-566

  Azimzadeh, Agnes M ^a   Byrne, Guerard W ^b,c   Ezzelarab, Mohamed ^d   Welty, Emily ^a   Braileanu, Gheorghe ^a   Cheng, Xiangfei ^a   Robson, Simon C ^e   McGregor, Christopher G A ^b,c   Cooper, David K C ^d   Pierson, Richard N ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b MAYO CLINIC   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF PITTSBURGH   (United States)

^e BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

antibody; cell line; galactosyl transferase; non Gal antibody; xenoreactive assay; xenotransplantation

Indexed keywords

ALPHA 1,3 GALACTOSYLTRANSFERASE; EPITOPE; ANTIBODY; IMMUNOGLOBULIN;

ANIMAL CELL; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; CELL CULTURE; CELL MEMBRANE; CLINICAL PROTOCOL; ENDOTHELIUM CELL; FLOW CYTOMETRY; NONHUMAN; PHENOTYPE; SWINE; XENOTRANSPLANTATION; ANIMAL; AORTA; BABOON; CONSENSUS; GRAFT REJECTION; IMMUNOLOGY; METABOLISM; PIG; PROCEDURES; XENOGRAFT;

ANIMALS; ANTIBODIES; AORTA; CONSENSUS; ENDOTHELIAL CELLS; GRAFT REJECTION; IMMUNOGLOBULINS; PAPIO; SWINE; TRANSPLANTATION, HETEROLOGOUS;

EID: 84916196448     PISSN: 0908665X     EISSN: 13993089     Source Type: Journal    
DOI: 10.1111/xen.12125     Document Type: Article

References (58)

1. Ekser B, Ezzelarab M, Hara H, et al. Clinical xenotransplantation: the next medical revolution? Lancet 2012; 379: 672-683.
2. Pierson RN III, Dorling A, Ayares D, et al. Current status of xenotransplantation and prospects for clinical application. Xenotransplantation 2009; 16: 263-280.
3. Allan JS,. Understanding xenotransplantation risks from nonhuman primate retroviruses. Curr Top Microbiol Immunol 2003; 278: 101-123.
4. Issa NC, Wilkinson RA, Griesemer A, et al. Absence of replication of porcine endogenous retrovirus and porcine lymphotropic herpesvirus type 1 with prolonged pig cell microchimerism after pig-to-baboon xenotransplantation. J Virol 2008; 82: 12441-12448.
5. Scobie L, Padler-Karavani V, Le Bas-Bernardet S, et al. Long-term IgG response to porcine Neu5Gc antigens without transmission of PERV in burn patients treated with porcine skin xenografts. J Immunol 2013; 191: 2907-2915.
6. Platt JL,. Mechanisms of tissue injury in hyperacute xenograft rejection. ASAIO J 1992; 38: 8-16.
7. Good AH, Cooper DKC, Malcom AJ, et al. Identification of carbohydrate structures that bind human antiporcine antibodies: implications for discordant xenografting in humans. Transplant Proc 1992; 24: 559-562.
8. Oriol R, Ye Y, Koren E, Cooper DKC,. 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: 1433-1442.
9. Sandrin MS, McKenzie IFC,. Galα(1,3)gal, the major xenoantigen(s) recognised in pigs by human natural antibodies. Immunol Rev 1994; 141: 169-190.
10. Rieben R, Bovin NV, Korchagina EY, et al. Xenotransplantation: in vitro analysis of synthetic alpha-galactosyl inhibitors of human anti-Galalpha1->3Gal IgM and IgG antibodies. Glycobiology 2000; 10: 141-148.
11. Byrne GW, Schwarz A, Fesi JR, et al. Evaluation of different alpha-Galactosyl glycoconjugates for use in xenotransplantation. Bioconjug Chem 2002; 13: 571-581.
12. Dean PG, Cohen AJ, Dalla VH, et al. The effect of anti-alphaGal antibody removal with immunoabsorption and splenectomy on CD46 transgenic kidney xenograft survival. Transplant Proc 2001; 33: 721-722.
13. Wu G, Pfeiffer S, Schroder C, et al. Coagulation cascade activation triggers early failure of pig hearts expressing human complement regulatory genes. Xenotransplantation 2007; 14: 34-47.
14. Phelps CJ, Koike C, Vaught TD, et al. Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 2003; 299: 411-414.
15. Dai Y, Vaught TD, Boone J, et al. Targeted disruption of the alpha1,3-galactosyltransferase gene in cloned pigs. Nat Biotechnol 2002; 20: 251-255.
16. Kolber-Simonds D, Lai L, Watt SR, et al. Production of alpha-1,3-galactosyltransferase null pigs by means of nuclear transfer with fibroblasts bearing loss of heterozygosity mutations. Proc Natl Acad Sci USA 2004; 101: 7335-7340.
17. Lutz AJ, Li P, Estrada JL, et al. Double knockout pigs deficient in N-glycolylneuraminic acid and Galactose alpha-1,3-Galactose reduce the humoral barrier to xenotransplantation. Xenotransplantation 2013; 20: 27-35.
18. Cozzi E, Tucker AW, Langford GA, et al. Characterization of pigs transgenic for human decay- accelerating factor. Transplantation 1997; 64: 1383-1392.
19. McGregor CG, Ricci D, Miyagi N, et al. Human CD55 expression blocks hyperacute rejection and restricts complement activation in Gal knockout cardiac xenografts. Transplantation 2012; 93: 686-692.
20. Cooper DK, Ekser B, Burlak C, et al. Clinical lung xenotransplantation-what donor genetic modifications may be necessary? Xenotransplantation 2012; 19: 144-158.
21. Kuwaki K, Tseng YL, Dor FJ, et al. Heart transplantation in baboons using alpha1,3-galactosyltransferase gene-knockout pigs as donors: initial experience. Nat Med 2005; 11: 29-31.
22. Yamada K, Yazawa K, Shimizu A, 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.
23. Azimzadeh AM, Kelishadi SS, Stoddard T, et al. Role of complement regulatory protein expression and CD154 blockade in Gal-independent xenograft rejection. Xenotransplantation 2010; 17: 117.
24. Ezzelarab MB, Ekser B, Echeverri G, et al. Costimulation blockade in pig artery patch xenotransplantation-a simple model to monitor the adaptive immune response in nonhuman primates. Xenotransplantation 2012; 19: 221-232.
25. Byrne GW, Davies WR, Oi K, et al. Increased immunosuppression, not anticoagulation, extends cardiac xenograft survival. Transplantation 2006; 82: 1787-1791.
26. Mohiuddin MM, Corcoran PC, Singh AK, et al. B-cell depletion extends the survival of GTKO.hCD46Tg pig heart xenografts in baboons for up to 8 months. Am J Transplant 2012; 12: 763-771.
27. Brouard S, Gagne K, Blancho G, Soulillou JP,. T cell response in xenorecognition and xenografts: a review. Hum Immunol 1999; 60: 455-468.
28. Thompson P, Badell IR, Lowe M, et al. Alternative immunomodulatory strategies for xenotransplantation: CD40/154 pathway-sparing regimens promote xenograft survival. Am J Transplant 2012; 12: 1765-1775.
29. Ezzelarab M, Hara H, Busch J, et al. Antibodies directed to pig non-Gal antigens in naive and sensitized baboons. Xenotransplantation 2006; 13: 400-407.
30. Saethre M, Baumann BC, Fung M, Seebach JD, Mollnes TE,. Characterization of natural human anti-non-gal antibodies and their effect on activation of porcine gal-deficient endothelial cells. Transplantation 2007; 84: 244-250.
31. Wu G, Pfeiffer S, Schroder C, et al. Co-stimulation blockade targeting CD154 and CD28/B7 modulates the induced antibody response after a pig-to-baboon cardiac xenograft. Xenotransplantation 2005; 12: 197-208.
32. Azimzadeh A, Wolf P, Thibaudeau K, et al. Comparative study of target antigens for primate xenoreactive natural antibodies in pig and rat endothelial cells. Transplantation 1997; 64: 1166-1174.
33. Byrne GW, Stalboerger PG, Davila E, et al. Proteomic identification of non-Gal antibody targets after pig-to-primate cardiac xenotransplantation. Xenotransplantation 2008; 15: 268-276.
34. Ezzelarab M, Garcia B, Azimzadeh A, et al. The innate immune response and activation of coagulation in alpha1,3-galactosyltransferase gene-knockout xenograft recipients. Transplantation 2009; 87: 805-812.
35. Davila E, Byrne GW, Labreche PT, et al. T-cell responses during pig-to-primate xenotransplantation. Xenotransplantation 2006; 13: 31-40.
36. Byrne GW, Stalboerger PG, Du Z, Davis TR, McGregor CG,. Identification of new carbohydrate and membrane protein antigens in cardiac xenotransplantation. Transplantation 2011; 91: 287-292.
37. Weinstock C, Schnaidt M,. The complement-mediated prozone effect in the Luminex single-antigen bead assay and its impact on HLA antibody determination in patient sera. Int J Immunogenet 2013; 40: 171-177.
38. Chen G, Sun H, Yang H, et al. 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: 273-283.
39. Burlak C, Wang ZY, Chihara RK, et al. Identification of human preformed antibody targets in GTKO pigs. Xenotransplantation 2012; 19: 92-101.
40. Samuelsson BE, Rydberg L, Breimer ME, et al. Natural antibodies and human xenotransplantation. Immunol Rev 1994; 141: 151-168.
41. Christiansen D, Mouhtouris E, Ramsland PA, Sandrin MS,. Studies on carbohydrate xenoantigens. Methods Mol Biol 2012; 885: 47-56.
42. Ezzelarab M, Ayares D, Cooper DK,. Carbohydrates in xenotransplantation. Immunol Cell Biol 2005; 83: 396-404.
43. Diswall M, Angstrom J, Karlsson H, et al. Structural characterization of alpha1,3-galactosyltransferase knockout pig heart and kidney glycolipids and their reactivity with human and baboon antibodies. Xenotransplantation 2010; 17: 48-60.
44. Breimer ME,. Gal/non-Gal antigens in pig tissues and human non-Gal antibodies in the GalT-KO era. Xenotransplantation 2011; 18: 215-228.
45. Padler-Karavani V, Varki A,. Potential impact of the non-human sialic acid N-glycolylneuraminic acid on transplant rejection risk. Xenotransplantation 2011; 18: 1-5.
46. Baumann BC, Stussi G, Huggel K, Rieben R, Seebach JD,. Reactivity of human natural antibodies to endothelial cells from Galalpha(1,3)Gal-deficient pigs. Transplantation 2007; 83: 193-201.
47. Nguyen BN, Azimzadeh AM, Schroeder C, et al. Absence of Gal epitope prolongs survival of swine lungs in an ex vivo model of hyperacute rejection. Xenotransplantation 2011; 18: 94-107.
48. Tseng YL, Moran K, Dor FJ, et al. Elicited antibodies in baboons exposed to tissues from alpha1,3-galactosyltransferase gene-knockout pigs. Transplantation 2006; 81: 1058-1062.
49. 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: 88-93.
50. Platt JL, Turman MA, Noreen HJ, et al. An ELISA assay for xenoreactive natural antibodies. Transplantation 1989; 49: 1000-1001.
51. Azimzadeh A, Meyer C, Watier H, et al. Removal of primate xenoreactive natural antibodies by extracorporeal perfusion of pig kidneys and livers. Transpl Immunol 1998; 6: 13-22.
52. Linhardt RJ, Bazin H,. Properties of carbohydrates. In:, Fraser-Reid B, Tatsuka K, Thiem J, eds. Glycoscience: Chemistry and Chemical Biology. Heidelberg: Springer-Verlag, 2001: 53-61.
53. Zenger VE, Vogt R, Mandy F, Schwartz A, Marti GE,. Quantitative flow cytometry: inter-laboratory variation. Cytometry 1998; 33: 138-145.
54. Krishnan NS, Fleetwood P, Higgins RM, et al. Application of flow cytometry to monitor antibody levels in ABO incompatible kidney transplantation. Transplantation 2008; 86: 474-477.
55. Perfetto SP, Ambrozak D, Nguyen R, Chattopadhyay PK, Roederer M,. Quality assurance for polychromatic flow cytometry using a suite of calibration beads. Nat Protoc 2012; 7: 2067-2079.
56. Miwa Y, Kobayashi T, Nagasaka T, et al. Are N-glycolylneuraminic acid (Hanganutziu-Deicher) antigens important in pig-to-human xenotransplantation? Xenotransplantation 2004; 11: 247-253.
57. Padler-Karavani V, Tremoulet AH, Yu H, et al. A simple method for assessment of human anti-Neu5Gc antibodies applied to Kawasaki disease. PLoS ONE 2013; 8: e58443.
58. Chihara RK, Lutz AJ, Paris LL, et al. Fibronectin from alpha 1,3-galactosyltransferase knockout pigs is a xenoantigen. J Surg Res 2013; 184: 1123-1133.