Alternative Immunomodulatory Strategies for Xenotransplantation: CD80/CD86-CTLA4 Pathway-Modified Immature Dendritic Cells Promote Xenograft Survival

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Tian, Min ^a   Lv, Yi ^a   Zhai, Chao ^a   Zhu, Haitao ^a   Yu, Liang ^a   Wang, Bo ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD86 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; HYBRID PROTEIN; IMMUNOGLOBULIN G4; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL STRUCTURE; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; GRAFT REJECTION; GRAFT SURVIVAL; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE SUBPOPULATION; MALE; MIXED LYMPHOCYTE REACTION; MONOCYTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; REGULATORY T LYMPHOCYTE; SPLEEN; SURVIVAL TIME; T LYMPHOCYTE ACTIVATION; XENOTRANSPLANTATION;

ANIMALS; ANTIGENS, CD80; ANTIGENS, CD86; CELLS, CULTURED; CTLA-4 ANTIGEN; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; GRAFT SURVIVAL; IMMUNOGLOBULIN G; LYMPHOCYTE CULTURE TEST, MIXED; MALE; MICE; SWINE; TRANSPLANTATION, HETEROLOGOUS;

EID: 84880778138     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069640     Document Type: Article

References (50)

1. Cardona K, Korbutt GS, Milas Z, Lyon J, Cano J, et al. (2006) Long-term survival of neonatal porcine islets in nonhuman primates by targeting costimulation pathways. Nat Med 12: 304-306.
2. Hering BJ, Wijkstrom M, Graham ML, Harstedt M, Aasheim TC, et al. (2006) Prolonged diabetes reversal after intraportal xenotransplantation of wild-type porcine islets in immunosuppressed nonhuman primates. Nat Med 12: 301-303.
3. Tonomura N, Shimizu A, Wang S, Yamada K, Tchipashvili V, et al. (2008) Pig islet xenograft rejection in a mouse model with an established human immune system. Xenotransplantation 15: 129-135.
4. Pierson RN, Dorling A, Ayares D, Rees MA, Seebach JD, et al. (2009) Current status of xenotransplantation and prospects for clinical application. Xenotransplantation 16: 263-280.
5. Phelps CJ, Koike C, Vaught TD, Boone J, Wells KD, et al. (2003) Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 299: 411-414.
6. Ekser B, Rigotti P, Gridelli B, Cooper DK, (2009) Xenotransplantation of solid organs in the pig-to-primate model. Transpl Immunol 21: 87-92.
7. Rayat GR, Rajotte RV, Hering BJ, Binette TM, Korbutt GS, (2003) In vitro and in vivo expression of Gal-(1,3) Gal on porcine islet cells is age dependent. J Endocrinol 177: 127-135.
8. Koulmanda M, Laufer TM, Auchincloss H, Smith RN, (2004) Prolonged survival of fetal pig islet xenografts in mice lacking the capacity for an indirect response. Xenotransplantation 11: 525-530.
9. Mirenda V, Golshayan D, Read J, Berton I, Warrens AN, et al. (2005) Achieving permanent survival of islet xenografts by independent manipulation of direct and indirect T-cell responses. Diabetes 54: 1048-1055.
10. Morelli AE, Thomson AW, (2007) Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 7: 610-621.
11. Ezzelarab M, Thomson AW, (2011) Tolerogenic dendritic cells and their role in transplantation. Semin Immunol 23: 252-263.
12. Lutz MB, Kurts C, (2009) Induction of peripheral CD4(+) T-cell tolerance and CD8(+) T-cell cross-tolerance by dendritic cells. Eur J Immunol 39: 2325-2330.
13. Probst HC, McCoy K, Okazaki T, Honjo T, van den Broek M, (2005) Resting dendritic cells induce peripheral CD8(+) T cell tolerance through PD-1 and CTLA-4. Nat Immunol 6: 280-286.
14. Menges M, Rossner S, Voigtlander C, Schindler H, Kukutsch NA, et al. (2002) Repetitive injections of dendritic cells matured with tumor necrosis factor alpha induce antigen-specific protection of mice from autoimmunity. J Exp Med 195: 15-21.
15. Jiang A, Bloom O, Ono S, Cui W, Unternaehrer J, et al. (2007) Disruption of E-cadherin-mediated adhesion induces a functionally distinct pathway of dendritic cell maturation. Immunity 27: 610-624.
16. Jung ID, Lee JS, Lee CM, Noh KT, Jeong YI, et al. (2010) Induction of indoleamine 2,3-dioxygenase expression via heme oxygenase-1-dependant pathway during murine dendritic cell maturation. Biochem Pharmacol 80: 491-505.
17. Nasreen M, Waldie TM, Dixon CM, Steptoe RJ, (2010) Steady-state antigen-expressing dendritic cells terminate CD4(+) memory T-cell responses. Eur J Immunol 40: 2016-2025.
18. Xia J, Chen J, Shao W, Lan T, Wang Y, et al. (2010) Suppressing memory T cell activation induces islet allograft tolerance in alloantigen-primed mice.Transpl Int. 23: 1154-1163.
19. Wood KJ, Sakaguchi S, (2003) Regulatory T cells in transplantation tolerance. Nat Rev Immunol 3: 199-210.
20. Stockis J, Colau D, Coulie PG, Lucas S, (2009) Membrane protein GARP is a receptor for latent TGF-beta on the surface of activated human Treg. Eur J Immunol 39: 3315-3322.
21. Hubert P, Jacobs N, Caberg JH, Boniver J, Delvenne P, (2007) The cross-talk between dendritic and regulatory T cells: good or evil? J Leukoc Biol 82: 781-794.
22. Sucher R, Fischler N, Oberhuber R, Schneeberger S, Fuchs D, et al. (2009) Indoleamine 2,3-dioxygenase (IDO) and T-regulatory cells are key players in CTLA4-Ig-mediated tolerance induction. J Am Coll Surg 209: S56-S56.
23. Vaughan AN, Malde P, Rogers NJ, Jackson IM, Lechler RI, et al. (2000) Porcine CTLA4-Ig lacks a MYPPPY motif, binds inefficiently to human B7 and specifically suppresses human CD4(+) T cell responses costimulated by pig but not human B7. J Immunol 165: 3175-3181.
24. Tian M, Lu Y, Zhai C, Zhu HT, Wang B, et al. (2010) pCTLA4-Ig gene-modified porcine immature dendritic cells inhibit the proliferation of xenogeneic spleen cells. Chinese journal of cellular and molecular immunology 26: 434-437.
25. Summerfield A, McCullough KC, (2009) The porcine dendritic cell family. Dev Comp Immunol 33: 299-309.
26. Kim HI, Lee SY, Jin SM, Kim KS, Yu JE, et al. (2009) Parameters for successful pig islet isolation as determined using 68 specific-pathogen-free miniature pigs. Xenotransplantation 16: 11-18.
27. Noguchi H, Ikemoto T, Naziruddin B, Jackson A, Shimoda M, et al. (2009) Iodixanol-Controlled Density Gradient During Islet Purification Improves Recovery Rate in Human Islet Isolation. Transplantation 87: 1629-1635.
28. Yonekawa Y, Matsumoto S, Okitsu T, Arata T, Iwanaga Y, et al. (2005) Effective islet isolation method with extremely high islet yields from adult pigs. Cell Transplant 14: 757-762.
29. Tian M, Lv Y, Zhai C, Zhu HT, Wu W, et al. (2010) Superiority of Visipaque (lodixanol)-Controlled Density Gradient Over Ficoll-400 in Adult Porcine Islet Purification. Transplant Proc 42: 1825-1828.
30. Maestri M, Rademacher J, Gaspari A, Lenti LM, Crespi S, et al. (2008) Short-Term Cyclosporine Therapy and Cotransplantation of Donor Splenocytes: Effects on Graft Rejection and Survival Rates in Pigs Subjected to Renal Transplantation. J Surg Res 150: 100-109.
31. Zhai C, Yu L, Zhu HT, Tian M, Zhang XG, et al. (2011) Porcine CTLA4-Ig prolong islet xenografts in rats by downregulating the direct pathway of T-cell activation. Xenotransplantation 18: 40-45.
32. Tesar BM, Chalasani G, Smith DL, Baddoura FK, Lakkis FG, et al. (2004) Direct antigen presentation by a xenograft induces immunity independently of secondary lymphoid organs. J Immunol 173: 4377-4386.
33. Rossini AA, Greiner DL, Mordes JP, (1999) Induction of Immunologic Tolerance for Transplantation. Physiol Rev 79: 99-141.
34. Koulmanda M, Laufer TM, Auchincloss H, Smith RN, (2004) Prolonged survival of fetal pig islet xenografts in mice lacking the capacity for an indirect response. Xenotransplantation 11: 525-530.
35. Moses RD, Pierson RN, Winn HJ, Auchincloss H, (1990) Xenogeneic proliferation and lymphokine production are dependent on CD4+ helper T cells and self antigenpresenting cells in the mouse. J Exp Med 172: 567-575.
36. Olack BJ, Jaramillo A, Zhang L, Swanson C, Rayan K, et al. (2001) The role of indirect antigen recognition in islet xenograft rejection. Transplant Proc 33: 784-785.
37. Singh NP, Guo L, Que X, Shirwan H, (2004) Blockade of indirect recognition mediated by CD4+ T cells leads to prolonged cardiac xenograft survival. Xenotransplantation 11: 33-42.
38. Graves SS, Stone D, Loretz C, Peterson L, McCune JS, et al. (2009) Establishment of long-term tolerance to SRBC in dogs by recombinant canine CTLA4-Ig. Transplantation 88: 317-322.
39. Yang DF, Qiu WH, Zhu HF, Lei P, Wen X, et al. (2008) CTLA4-Ig-modified dendritic cells inhibit lymphocyte-mediated alloimmune responses and prolong the islet graft survival in mice. Transpl Immunol 19: 197-201.
40. Rudd CE, Taylor A, Schneider H, (2009) CD28 and CTLA-4 coreceptor expression and signal transduction. Immunol Rev 229: 12-26.
41. Schneider H, Downey J, Smith A, Zinselmeyer BH, Rush C, et al. (2006) Reversal of the TCR stop signal by CTLA-4. Science 313: 1972-1975.
42. Ellis JH, Burden MN, Vinogradov DV, Linge C, Crowe JS, (1996) Interactions of CD80 and CD86 with CD28 and CTLA4. J Immunol 156: 2700-2709.
43. Thomson AW, (2010) Tolerogenic Dendritic Cells: All Present and Correct? Am J Transplant 10: 214-219.
44. Lob S, Konigsrainer A, (2009) Role of IDO in Organ Transplantation: Promises and Difficulties. Int Rev Immunol 28: 185-206.
45. Lin YJ, Hara H, Tai HC, Long C, Tokita D, et al. (2008) Suppressive efficacy and proliferative capacity of human regulatory T cells in allogeneic and xenogeneic responses. Transplantation 86: 1452-1462.
46. Nishimura T, Onda M, Takao S, (2010) CD4+ CD25+ regulatory T cells suppressed the indirect xenogeneic immune response mediated by porcine epithelial cell pulsed dendritic cells. Xenotransplantation 17: 313-323.
47. Grohmann U, Orabona C, Fallarino F, Vacca C, Calcinaro F, et al. (2002) CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat Immunol 3: 1097-1101.
48. Dejean AS, Beisner DR, Chen IL, KerdilesYM, Babour A, et al. (2009) Transcription factor Foxo3 controls the magnitude of T cell immune responses by modulating the function of dendritic cells. Nat Immunol 10: 504-513.
49. Robert S, Klaus F, Rupert OR, Irmgard K, Christian M, et al. (2012) Robert IDO and Regulatory T Cell Support Are Critical for Cytotoxic T Lymphocyte-Associated Ag-4 Ig-Mediated Long-Term Solid Organ Allograft Survival. J Immunol 188: 37-46.
50. Robert OL, Johann P, (2010) Role of heme oxygenase-1 in transplantation. Transpl Int 23: 1071-1081.