Blockade of CD40-CD154 costimulatory pathway promotes long-term survival of full-thickness porcine corneal grafts in nonhuman primates: Clinically applicable xenocorneal transplantation

American Journal of Transplantation

Volumn 15, Issue 3, 2015, Pages 628-641

  Choi, H J ^a,b,c,d   Lee, J J ^e   Kim, D H ^b,c,d   Kim, Mee Kum ^b,c,d   Lee, H J ^c   Ko, A Y ^c   Kang, H J ^f   Park, C ^b,d   Wee, W R ^b,c,d  

^a Seoul National University Hospital Healthcare System Gangnam Center   (South Korea)

^b Seoul National University College of Medicine   (South Korea)

^c Seoul National University College of Medicine   (South Korea)

^d Seoul National University Hospital   (South Korea)

^e Chungnam National University College of Medicine   (South Korea)

^f Hallym University College of Medicine   (South Korea)

Author keywords

Basic (laboratory) research science; corneal transplantation ophthalmology; fusion proteins and monoclonal antibodies: costimulation molecule specific; graft survival; immunosuppressant; immunosuppression immune modulation; rejection; translational research science; xenoantibody; xenoantigen; xenotransplantation

Indexed keywords

CD40 ANTIGEN; CD40 LIGAND; COMPLEMENT COMPONENT C3A; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; MONOCYTE CHEMOTACTIC PROTEIN 1; POD 318; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CORNEA TRANSPLANTATION; FEMALE; GRAFT SURVIVAL; IMMUNOSUPPRESSIVE TREATMENT; LONG TERM SURVIVAL; MACROPHAGE; MALE; MEMORY T LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL TIME; XENOCORNEAL TRANSPLANTATION; ANIMAL; ANTAGONISTS AND INHIBITORS; IMMUNOLOGY; PIG; PRIMATE; XENOGRAFT;

ANIMALS; ANTIGENS, CD40; CD40 LIGAND; CORNEAL TRANSPLANTATION; FEMALE; HETEROGRAFTS; MALE; PRIMATES; SWINE;

EID: 84924018182     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.13057     Document Type: Article

References (54)

1. Whitcher JP, Srinivasan M, Upadhyay MP., Corneal blindness: A global perspective. Bull World Health Organ 2001; 79: 214-221.
2. Pascolini D, Mariotti SP., Global estimates of visual impairment: 2010. Br J Ophthalmol 2012; 96: 614-618.
3. Hara H, Cooper DK., Xenotransplantation-The future of corneal transplantation ? Cornea 2011; 30: 371-378.
4. Zeng Y, Yang J, Huang K, Lee Z, Lee X., A comparison of biomechanical properties between human and porcine cornea. J Biomech 2001; 34: 533-537.
5. Amano S, Shimomura N, Kaji Y, Ishii K, Yamagami S, Araie M., Antigenicity of porcine cornea as xenograft. Curr Eye Res 2003; 26: 313-318.
6. Lee HI, Kim MK, Oh JY, et al. Gal alpha(1-3)Gal expression of the cornea in vitro, in vivo and in xenotransplantation. Xenotransplantation 2007; 14: 612-618.
7. Cooper DK., Clinical xenotransplantion-How close are we ? Lancet 2003; 362: 557-559.
8. Cozzi E, Gianello P, Soulillou JP., A new start for xenotransplantation research in the European Union. Xenotransplantation 2007; 14: 196-197.
9. Sprangers B, Waer M, Billiau AD., Xenotransplantation: Where are we in 2008 ? Kidney Int 2008; 74: 14-21.
10. Pierson RN III, Dorling A, Ayares D, et al. Current status of xenotransplantation and prospects for clinical application. Xenotransplantation 2009; 16: 263-280.
11. Cooper DK, Casu A., The International Xenotransplantation Association consensus statement on conditions for undertaking clinical trials of porcine islet products in type 1 diabetes-Chapter 4: Pre-clinical efficacy and complication data required to justify a clinical trial. Xenotransplantation 2009; 16: 229-238.
12. Hering BJ, Cooper DK, Cozzi E, et al. The International Xenotransplantation Association consensus statement on conditions for undertaking clinical trials of porcine islet products in type 1 diabetes-Executive summary. Xenotransplantation 2009; 16: 196-202.
13. Zhiqiang P, Cun S, Ying J, Ningli W, Li W., WZS-pig is a potential donor alternative in corneal xenotransplantation. Xenotransplantation 2007; 14: 603-611.
14. Choi HJ, Kim MK, Lee HJ, et al. Efficacy of pig-to-rhesus lamellar corneal xenotransplantation. Invest Ophthalmol Vis Sci 2011; 52: 6643-6650.
15. Li A, Pan Z, Jie Y, Sun Y, Luo F, Wang L., Comparison of immunogenicity and porcine-to-rhesus lamellar corneal xenografts survival between fresh preserved and dehydrated porcine corneas. Xenotransplantation 2011; 18: 46-55.
16. Jie Y, Liu L, Pan Z, Wang L., Survival of pig-to-rhesus corneal xenografts prolonged by prior donor bone marrow transplantation. Mol Med Rep 2013; 7: 869-874.
17. Choi HJ, Kim MK, Lee HJ, et al. Effect of alphaGal on corneal xenotransplantation in a mouse model. Xenotransplantation 2011; 18: 176-182.
18. Qian Y, Dana MR., Molecular mechanisms of immunity in corneal allotransplantation and xenotransplantation. Expert Rev Mol Med 2001; 3: 1-21.
19. Hara H, Cooper DK., The immunology of corneal xenotransplantation: A review of the literature. Xenotransplantation 2010; 17: 338-349.
20. Kim MK, Wee WR, Park CG, Kim SJ., Xenocorneal transplantation. Curr Opin Organ Transplant 2011; 16: 231-236.
21. Ross JR, Howell DN, Sanfilippo FP., Characteristics of corneal xenograft rejection in a discordant species combination. Invest Ophthalmol Vis Sci 1993; 34: 2469-2476.
22. Tanaka K, Yamada J, Streilein JW., Xenoreactive CD4+ T cells and acute rejection of orthotopic guinea pig corneas in mice. Invest Ophthalmol Vis Sci 2000; 41: 1827-1832.
23. Tanaka K, Sonoda K, Streilein JW., Acute rejection of orthotopic corneal xenografts in mice depends on CD4(+) T cells and self-antigen-presenting cells. Invest Ophthalmol Vis Sci 2001; 42: 2878-2884.
24. Oh JY, Kim MK, Ko JH, et al. Acute cell-mediated rejection in orthotopic pig-to-mouse corneal xenotransplantation. Xenotransplantation 2009; 16: 74-82.
25. Hering BJ, Wijkstrom M, Graham ML, et al. Prolonged diabetes reversal after intraportal xenotransplantation of wild-type porcine islets in immunosuppressed nonhuman primates. Nat Med 2006; 12: 301-303.
26. Cardona K, Korbutt GS, Milas Z, et al. Long-term survival of neonatal porcine islets in nonhuman primates by targeting costimulation pathways. Nat Med 2006; 12: 304-306.
27. Cardona K, Milas Z, Strobert E, et al. Engraftment of adult porcine islet xenografts in diabetic nonhuman primates through targeting of costimulation pathways. Am J Transplant 2007; 7: 2260-2268.
28. Higuchi R, Streilein JW., CD8+ T cell-mediated delayed rejection of orthotopic guinea pig cornea grafts in mice deficient in CD4+ T cells. Invest Ophthalmol Vis Sci 2003; 44: 175-182.
29. Jones ND, Van Maurik A, Hara M, et al. CD40-CD40 ligand-independent activation of CD8+ T cells can trigger allograft rejection. J Immunol 2000; 165: 1111-1118.
30. Li S, Waer M, Billiau AD., Xenotransplantation: Role of natural immunity. Transpl Immunol 2009; 21: 70-74.
31. Cadili A, Kneteman N., The role of macrophages in xenograft rejection. Transplant Proc 2008; 40: 3289-3293.
32. Phelps CJ, Koike C, Vaught TD, et al. Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 2003; 299: 411-414.
33. Cozzi E, White DJ., The generation of transgenic pigs as potential organ donors for humans. Nat Med 1995; 1: 964-966.
34. Diamond LE, Quinn CM, Martin MJ, Lawson J, Platt JL, Logan JS., A human CD46 transgenic pig model system for the study of discordant xenotransplantation. Transplantation 2001; 71: 132-142.
35. Hara H, Long C, Lin YJ, et al. In vitro investigation of pig cells for resistance to human antibody-mediated rejection. Transpl Int 2008; 21: 1163-1174.
36. Phelps CJ, Ball SF, Vaught TD, et al. Production and characterization of transgenic pigs expressing porcine CTLA4-Ig. Xenotransplantation 2009; 16: 477-485.
37. Takano T, Williams KA., Mechanism of corneal endothelial destruction in rejecting rat corneal allografts and xenografts: A role for CD4+ cells. Transplant Proc 1995; 27: 260-261.
38. Hargrave SL, Mayhew E, Hegde S, Niederkorn J., Are corneal cells susceptible to antibody-mediated killing in corneal allograft rejection ? Transpl Immunol 2003; 11: 79-89.
39. Grewal IS, Flavell RA., A central role of CD40 ligand in the regulation of CD4+ T-cell responses. Immunol Today 1996; 17: 410-414.
40. Bühler L, Awwad M, Basker M, et al. High-dose porcine hematopoietic cell transplantation combined with CD40 ligand blockade in baboons prevents an induced anti-pig humoral response. Transplantation 2000; 69: 2296-2304.
41. 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.
42. Tseng YL, Kuwaki K, Dor FJ, et al. alpha1,3-Galactosyltransferase gene-knockout pig heart transplantation in baboons with survival approaching 6 months. Transplantation 2005; 80: 1493-1500.
43. Hisashi Y, Yamada K, Kuwaki K, et al. Rejection of cardiac xenografts transplanted from alpha1,3-galactosyltransferase gene-knockout (GalT-KO) pigs to baboons. Am J Transplant 2008; 8: 2516-2526.
44. van der Windt DJ, Bottino R, Casu A, et al. Long-term controlled normoglycemia in diabetic non-human primates after transplantation with hCD46 transgenic porcine islets. Am J Transplant 2009; 9: 2716-2726.
45. Magee JC, Collins BH, Harland RC, et al. Immunoglobulin prevents complement-mediated hyperacute rejection in swine-to-primate xenotransplantation. J Clin Invest 1995; 96: 2404-2412.
46. Latremouille C, Genevaz D, Hu MC, et al. Normal human immunoglobulins for intravenous use (IVIg) delay hyperacute xenograft rejection through F(ab')2-mediated anti-complement activity. Clin Exp Immunol 1997; 110: 122-126.
47. Bayry J, Lacroix-Desmazes S, Kazatchkine MD, Kaveri SV., Monoclonal antibody and intravenous immunoglobulin therapy for rheumatic diseases: Rationale and mechanisms of action. Nat Clin Pract Rheumatol 2007; 3: 262-272.
48. Kawai T, Andrews D, Colvin RB, Sachs DH, Cosimi AB., Thromboembolic complications after treatment with monoclonal antibody against CD40 ligand. Nat Med 2000; 6: 114.
49. Knosalla C, Gollackner B, Cooper DK., Anti-CD154 monoclonal antibody and thromboembolism revisited. Transplantation 2002; 74: 416-417.
50. Koyama I, Kawai T, Andrews D, et al. Thrombophilia associated with anti-CD154 monoclonal antibody treatment and its prophylaxis in nonhuman primates. Transplantation 2004; 77: 460-462.
51. Boumpas DT, Furie R, Manzi S, et al. A short course of BG9588 (anti-CD40 ligand antibody) improves serologic activity and decreases hematuria in patients with proliferative lupus glomerulonephritis. Arthritis Rheum 2003; 48: 719-727.
52. Thompson P, Cardona K, Russell M, et al. CD40-specific costimulation blockade enhances neonatal porcine islet survival in nonhuman primates. Am J Transplant 2011; 11: 947-957.
53. Qian Y, Dana MR., Effect of locally administered anti-CD154 (CD40 ligand) monoclonal antibody on survival of allogeneic corneal transplants. Cornea 2002; 21: 592-597.
54. 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.