Relative efficiency of porcine and human cytotoxic T-lymphocyte antigen 4 immunoglobulin in inhibiting human CD4 + T-cell responses co-stimulated by porcine and human B7 molecules

Immunology

Volumn 134, Issue 4, 2011, Pages 386-397

  Koshika, Tadatsura ^a   Phelps, Carol ^b   Fang, Jason ^a   Lee, Seung Eun ^a   Fujita, Minoru ^a   Ayares, David ^b   Cooper, David K C ^a   Hara, Hidetaka ^a  

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

^b REVIVICOR INC   (United States)

Author keywords

Co stimulatory molecules; Human CD4+ T cells; Porcine CTLA4 Ig; Xenotransplantation

Indexed keywords

B7 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 IMMUNOGLOBULIN; IMMUNOGLOBULIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOPLASM; DRUG EFFECT; DRUG EFFICACY; ENDOTHELIUM CELL; GRAFT REJECTION; HUMAN; HUMAN CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; TRANSGENIC PIG; XENOTRANSPLANTATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, CD4; B7 ANTIGENS; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; CTLA-4 ANTIGEN; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; IMMUNOSUPPRESSION; SWINE; T-LYMPHOCYTES, CYTOTOXIC; TRANSPLANTATION IMMUNOLOGY; TRANSPLANTATION, HETEROLOGOUS; TRANSPLANTATION, HOMOLOGOUS;

EID: 80355140497     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2011.03496.x     Document Type: Article

References (54)

1. Phelps CJ, Koike C, Vaught TD et al. Production of α1, 3-galactosyltransferase-deficient pigs. Science 2003; 299:411-4.
2. Cooper DK, Dorling A, Pierson RN, III rd, et al. α1, 3-galactosyltransferase gene-knockout pigs for xenotransplantation: where do we go from here? Transplantation 2007; 84:1-7.
3. Pierson RN, III rd, Dorling A, Ayares D, Rees MA, Seebach JD, Fishman JA, Hering BJ, Cooper DK. Current status of xenotransplantation and prospects for clinical application. Xenotransplantation 2009; 16:263-80.
4. Le Bas-Bernardet S, Blancho G. Current cellular immunological hurdles in pig-to-primate xenotransplantation. Transpl Immunol 2009; 21:60-4.
5. Brouard S, Gagne K, Blancho G, Soulillou JP. T cell response in xenorecognition and xenografts: a review. Hum Immunol 1999; 60:455-68.
6. Davila E, Byrne GW, LaBreche PT et al. T-cell responses during pig-to-primate xenotransplantation. Xenotransplantation 2006; 13:31-40.
7. Lenschow DJ, Zeng Y, Thistlethwaite JR, Montag A, Brady W, Gibson MG, Linsley PS, Bluestone JA. Long-term survival of xenogeneic pancreatic islet grafts induced by CTLA4Ig. Science 1992; 257:789-92.
8. Larsen CP, Morris PJ, Austyn JM. Migration of dendritic leukocytes from cardiac allografts into host spleens. A novel pathway for initiation of rejection. J Exp Med 1990; 171:307-14.
9. Faustman DL, Steinman RM, Gebel HM, Hauptfeld V, Davie JM, Lacy PE. Prevention of rejection of murine islet allografts by pretreatment with anti-dendritic cell antibody. Proc Natl Acad Sci USA 1984; 81:3864-8.
10. Mirenda V, Le Mauff B, Boeffard F, Cassard A, Jugeau N, Soulillou JP, Anegon I. Intact pancreatic islet function despite humoral xenorecognition in the pig-to-monkey combination. Transplantation 1998; 66:1485-95.
11. Rogers NJ, Mirenda V, Jackson I, Dorling A, Lechler RI. Costimulatory blockade by the induction of an endogenous xenospecific antibody response. Nat Immunol 2000; 1:163-8.
12. Mirenda V, Golshayan D, Read J, Berton I, Warrens AN, Dorling A, Lechler RI. Achieving permanent survival of islet xenografts by independent manipulation of direct and indirect T-cell responses. Diabetes 2005; 54:1048-55.
13. Murray AG, Khodadoust MM, Pober JS, Bothwell AL. Porcine aortic endothelial cells activate human T cells: direct presentation of MHC antigens and costimulation by ligands for human CD2 and CD28. Immunity 1994; 1:57-63.
14. Maher SE, Karmann K, Min W, Hughes CC, Pober JS, Bothwell AL. Porcine endothelial CD86 is a major costimulator of xenogeneic human T cells: cloning, sequencing, and functional expression in human endothelial cells. J Immunol 1996; 157:3838-44.
15. Rogers NJ, Jackson IM, Jordan WJ, Hawadle MA, Dorling A, Lechler RI. Cross-species costimulation: relative contributions of CD80, CD86, and CD40. Transplantation 2003; 75:2068-76.
16. Wada M, Amae S, Sasaki H, Ishii T, Sano N, Nio M, Hayashi Y, Ohi R. The functional roles of porcine CD80 molecule and its ability to stimulate and regulate human anti-pig cellular response. Transplantation 2003; 75:1887-94.
17. Choi I, Kim SD, Cho B et al. Xenogeneic interaction between human CD40L and porcine CD40 activates porcine endothelial cells through NF-kappaB signaling. Mol Immunol 2008; 45:575-80.
18. Yamada K, Sachs DH, DerSimonian H. Human anti-porcine xenogeneic T cell response. Evidence for allelic specificity of mixed leukocyte reaction and for both direct and indirect pathways of recognition. J Immunol 1995; 155:5249-56.
19. Lin YJ, Hara H, Tai HC et al. Suppressive efficacy and proliferative capacity of human regulatory T cells in allogeneic and xenogeneic responses. Transplantation 2008; 86:1452-62.
20. + T cell responses costimulated by pig but not human B7. J Immunol 2000; 165:3175-81.
21. Peach RJ, Bajorath J, Brady W, Leytze G, Greene J, Naemura J, Linsley PS. Complementarity determining region 1 (CDR1)- and CDR3-analogous regions in CTLA-4 and CD28 determine the binding to B7-1. J Exp Med 1994; 180:2049-58.
22. Morton PA, Fu XT, Stewart JA et al. Differential effects of CTLA-4 substitutions on the binding of human CD80 (B7-1) and CD86 (B7-2). J Immunol 1996; 156:1047-54.
23. Metzler WJ, Bajorath J, Fenderson W et al. Solution structure of human CTLA-4 and delineation of a CD80/CD86 binding site conserved in CD28. Nat Struct Biol 1997; 4:527-31.
24. Phelps CJ, Ball SF, Vaught TD et al. Production and characterization of transgenic pigs expressing porcine CTLA4-Ig. Xenotransplantation 2009; 16:477-85.
25. Hara H, Long C, Lin YJ, Tai HC, Ezzelarab M, Ayares D, Cooper DK. In vitro investigation of pig cells for resistance to human antibody-mediated rejection. Transpl Int 2008; 21:1163-74.
26. Long C, Hara H, Pawlikowski Z et al. Genetically engineered pig red blood cells for clinical transfusion: initial in vitro studies. Transfusion 2009; 49:2418-29.
27. Hara H, Koike N, Long C et al. Initial in vitro investigation of the human immune response to corneal cells from genetically-engineered pigs. Invest Ophthalmol Vis Sci 2011; 52:5278-86.
28. Ezzelarab M, Welchons D, Torres C, Hara H, Long C, Yeh P, Ayares D, Cooper DK. Atorvastatin down-regulates the primate cellular response to porcine aortic endothelial cells in vitro. Transplantation 2008; 86:733-7.
29. Salomon B, Bluestone JA. Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation. Annu Rev Immunol 2001; 19:225-52.
30. Fife BT, Bluestone JA. Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways. Immunol Rev 2008; 224:166-82.
31. Durrbach A, Francois H, Jacquet A, Beaudreuil S, Charpentier B. Co-signals in organ transplantation. Curr Opin Organ Transplant 2010; 15:474-80.
32. Turka LA, Linsley PS, Lin H et al. T-cell activation by the CD28 ligand B7 is required for cardiac allograft rejection in vivo. Proc Natl Acad Sci USA 1992; 89:11102-5.
33. Lin H, Bolling SF, Linsley PS, Wei RQ, Gordon D, Thompson CB, Turka LA. Long-term acceptance of major histocompatibility complex mismatched cardiac allografts induced by CTLA4Ig plus donor-specific transfusion. J Exp Med 1993; 178:1801-6.
34. Levisetti MG, Padrid PA, Szot GL et al. Immunosuppressive effects of human CTLA4Ig in a non-human primate model of allogeneic pancreatic islet transplantation. J Immunol 1997; 159:5187-91.
35. Kirk AD, Harlan DM, Armstrong NN et al. CTLA4-Ig and anti-CD40 ligand prevent renal allograft rejection in primates. Proc Natl Acad Sci USA 1997; 94:8789-94.
36. Larsen CP, Pearson TC, Adams AB et al. Rational development of LEA29Y (belatacept), a high-affinity variant of CTLA4-Ig with potent immunosuppressive properties. Am J Transplant 2005; 5:443-53.
37. Linsley PS, Wallace PM, Johnson J, Gibson MG, Greene JL, Ledbetter JA, Singh C, Tepper MA. Immunosuppression in vivo by a soluble form of the CTLA-4 T cell activation molecule. Science 1992; 257:792-5.
38. + T cells. J Exp Med 1994; 179:819-30.
39. Genovese MC, Becker JC, Schiff M et al. Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N Engl J Med 2005; 353:1114-23.
40. Korhonen R, Moilanen E. Abatacept, a novel CD80/86-CD28 T cell co-stimulation modulator, in the treatment of rheumatoid arthritis. Basic Clin Pharmacol Toxicol 2009; 104:276-84.
41. Nogid A, Pham DQ. Role of abatacept in the management of rheumatoid arthritis. Clin Ther 2006; 28:1764-78.
42. Ma Y, Lin BR, Lin B et al. Pharmacokinetics of CTLA4Ig fusion protein in healthy volunteers and patients with rheumatoid arthritis. Acta Pharmacol Sin 2009; 30:364-71.
43. Durrbach A, Pestana JM, Pearson T et al. A phase III study of belatacept versus cyclosporine in kidney transplants from extended criteria donors (BENEFIT-EXT study). Am J Transplant 2010; 10:547-57.
44. Vincenti F, Charpentier B, Vanrenterghem Y et al. A phase III study of belatacept-based immunosuppression regimens versus cyclosporine in renal transplant recipients (BENEFIT study). Am J Transplant 2010; 10:535-46.
45. Emamaullee JA, Merani S, Larsen CP, Shapiro AM. Belatacept and basiliximab diminish human antiporcine xenoreactivity and synergize to inhibit alloimmunity. Transplantation 2008; 85:118-24.
46. Lau HT, Yu M, Fontana A, Stoeckert CJ, Jr. Prevention of islet allograft rejection with engineered myoblasts expressing FasL in mice. Science 1996; 273:109-12.
47. Gainer AL, Korbutt GS, Rajotte RV, Warnock GL, Elliott JF. Expression of CTLA4-Ig by biolistically transfected mouse islets promotes islet allograft survival. Transplantation 1997; 63:1017-121.
48. Olthoff KM, Judge TA, Gelman AE, da Shen X, Hancock WW, Turka LA, Shaked A. Adenovirus-mediated gene transfer into cold-preserved liver allografts: survival pattern and unresponsiveness following transduction with CTLA4Ig. Nat Med 1998; 4:194-200.
49. Takeda Y, Gotoh M, Dono K et al. Protection of islet allografts transplanted together with Fas ligand expressing testicular allografts. Diabetologia 1998; 41:315-21.
50. Martin C, Plat M, Nerriere-Daguin V et al. Transgenic expression of CTLA4-Ig by fetal pig neurons for xenotransplantation. Transgenic Res 2005; 14:373-84.
51. Badin R, Padoan A, Vadori M et al. Porcine embryonic xenografts transgenic for CTLA4-Ig enable longterm recovery in Parkinsonian macaques. Am J Transplant 2010; 10 (S4):208.(Abstract LB01).
52. Hara H, Cooper DK. Xenotransplantation - the future of corneal transplantation? Cornea 2010; 30:371-8.
53. Hara H, Cooper DK. The immunology of corneal xenotransplantation: a review of the literature. Xenotransplantation 2010; 17:338-49.
54. Phelps CJ, Vaught TD, Ball SF et al. Multi-transgenic pigs designed for xenoislet transplants. Xenotransplantation 2009; 16:374.