Abnormal regulatory and effector T cell function predispose to autoimmunity following xenogeneic thymic transplantation

Journal of Immunology

Volumn 181, Issue 11, 2009, Pages 7649-7659

  Fudaba, Yasuhiro ^a,b   Onoe, Takashi ^a   Chittenden, Meredith ^a   Shimizu, Akira ^a   Shaffer, Juanita M ^a   Bronson, Roderick ^a   Sykes, Megan ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HIROSHIMA UNIV SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; TRANSCRIPTION FACTOR FOXP3;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; BAGG ALBINO MOUSE; CD25+ T LYMPHOCYTE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL COUNT; CELL EXPANSION; CELL FUNCTION; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; EFFECTOR CELL; EPITHELIUM CELL; FEMALE; FETUS; GRAFT RECIPIENT; HOST; INJECTION; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; NUDE MOUSE; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPLEEN CELL; SWINE; THYMOCYTE; THYMUS GRAFT; THYMUS TRANSPLANTATION; XENOGRAFT;

EID: 71849094573     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.11.7649     Document Type: Article

References (49)

1. Lee, L. A., H. A. Gritsch, J. J. Sergio, J. S. Arn, R. M. Glaser, T. Sablinski, D. H. Sachs, and M. Sykes. 1994. Specific tolerance across a discordant xenogeneic transplantation barrier. Proc. Natl. Acad. Sci. USA 91: 10864-10867.
2. Zhao, Y., K. Swenson, J. J. Sergio, J. S. Arn, D. H. Sachs, and M. Sykes. 1996. Skin graft tolerance across a discordant xenogeneic barrier. Nat. Med. 2: 1211-1216. (Pubitemid 26375404)
3. Zhao, Y., J. A. Fishman, J. J. Sergio, J. L. Oliveros, D. A. Pearson, G. L. Szot, R. A. Wilkinson, J. S. Arn, D. H. Sachs, and M. Sykes. 1997. Immune restoration by fetal pig thymus grafts in T cell-depleted, thymectomized mice. J. Immunol. 158: 1641-1649. (Pubitemid 127469518)
4. Zhao, Y., J. I. Rodriguez-Barbosa, A. Shimizu, K. Swenson, D. H. Sachs, and M. Sykes. 2002. Despite efficient intrathymic negative selection of host-reactive T cells, autoimmune disease may develop in porcine thymus-grafted athymic mice: evidence for failure of regulatory mechanisms suppressing autoimmunity. Transplantation 75: 1832-1840. (Pubitemid 36734639)
5. Zhao, Y., J. I. Rodriguez-Barbosa, G. Zhao, J. Shaffer, J. S. Arn, and M. Sykes. 2000. Maturation and function of mouse T cells with a transgeneic TCR positively selected by highly disparate xenogeneic porcine MHC. Cell. Mol. Biol. 47: 217-228.
6. + T cells with a mouse MHC-restricted TCR in pig thymus grafts. J. Immunol. 161: 1320-1326.
7. Sachs, D. H. 1994. The pig as a potential xenograft donor. Vet. Immunol. Immunopathol. 43: 185-191.
8. Zhao, Y., J. I. Rodriguez-Barbosa, K. Swenson, G. Zhao, J. S. Arn, D. H. Sachs, and M. Sykes. 2001. Highly disparate xenogeneic skin graft tolerance induction by fetal pig thymus in thymectomized mice: conditioning requirements and the role of co-implantation of fetal pig liver. Transplantation 72: 1608-1615.
9. Yan, Y., T. Devos, L. Yu, G. Xia, O. Rutgeerts, J. Goebels, C. Segers, Y. Lin, M. Vandeputte, and M. Waer. 2003. Pathogenesis of autoimmunity after xenogeneic thymus transplantation. J. Immunol. 170: 5936-5946. (Pubitemid 36682573)
10. Barthlott, T., G. Kassiotis, and B. Stockinger. 2003. T cell regulation as a side effect of homeostasis and competition. J. Exp. Med. 197: 451-460. (Pubitemid 36278601)
11. + T cells: evidence from a lymphopenic T cell model. Immunity 17: 425-436.
12. Nikolic, B., J. P. Gardner, D. T. Scadden, J. S. Arn, D. H. Sachs, and M. Sykes. 1999. Normal development in porcine thymus grafts and specific tolerance of human T cells to porcine donor MHC. J. Immunol. 162: 3402-3407. (Pubitemid 29313590)
13. Yamada, K., K. Yazawa, A. Shimizu, T. Iwanaga, Y. Hisashi, M. Nuhn, P. O'malley, S. Nobori, P. A. Vagefi, C. Patience, et al. 2005. Marked prolongation of porcine renal xenograft survival in baboons through the use of α1,3-galactosyltransferase gene-knockout donors and the cotransplantation of vascularized thymic tissue. Nat. Med. 11: 32-34.
14. Baldwin, T. A., K. A. Hogquist, and S. C. Jameson. 2004. The fourth way? Harnessing aggressive tendencies in the thymus. J. Immunol. 173: 6515-6520.
15. Zheng, Y., S. Z. Josefowicz, A. Kas, T. T. Chu, M. A. Gavin, and A. Y. Rudensky. 2007. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 445: 936-940. (Pubitemid 46309837)
16. + T cells in mice. Transplantation 85: 1167-1174.
17. Ernst, B., D.-S. Lee, J. M. Chang, J. Sprent, and C. D. Surh. 1999. The peptide ligands mediating positive selection in the thymus control T cell survival and homeostatic proliferation in the periphery. Immunity 11: 173-181. (Pubitemid 29428810)
18. Rodriguez-Barbosa, J. I., Y. Zhao, A. Ezquerra, G. Zhao, D. H. Sachs, and M. Sykes. 2002. Murine CD4 T cells selected in a highly disparate xenogeneic porcine thymus graft do not show rapid decay in the absence of selecting MHC in the periphery. J. Immunol. 169: 6697-6710.
19. + regulatory T cells induced by an agonist self-peptide. Nat. Immunol. 2: 301-306.
20. Apostolou, I., A. Sarukhan, L. Klein, and H. Von Boehmer. 2002. Origin of regulatory T cells with known specificity for antigen. Nat. Immunol. 3: 756-763. (Pubitemid 34884832)
21. + regulatory T cells in vivo. J. Exp. Med. 198: 249-258.
22. Shrivastava, S., J. H. McVey, and A. Dorling. 2007. The interface between coagulation and immunity. Am. J. Transplant. 7: 499-506.
23. Devos, T., B. Sprangers, Y. Lin, S. Li, Y. Yan, W. Landuyt, C. Lenaerts, O. Rutgeerts, J. Goebels, D. Bullens, et al. 2008. Occurrence of autoimmunity after xenothymus transplantation in T-cell-deficient mice depends on the thymus transplant technique. Transplantation 85: 640-644.
24. + regulatory T cells. J. Immunol. 171: 5678-5682.
25. Rodriguez-Barbosa, J. I., Y. Zhao, R. Barth, G. Zhao, J. S. Arn, D. H. Sachs, and M. Sykes. 2001. Enhanced CD4 reconstitution by grafting neonatal porcine tissue in alternative locations is associated with donor-specific tolerance and suppression of pre-existing xenoreactive T cells. Transplantation 72: 1223-1231.
26. +T cells in xenogeneic neonatal porcine thymus-grafted athymic mice. Am. J. Transplant. 6: 2841-2850.
27. + regulatory T cells in mice. Transplantation 82: 1484-1492.
28. + regulatory T cells protects from lethal acute GVHD. Blood 105: 2220-2226.
29. Powrie, F., J. Carlino, M. W. Leach, S. Mauze, and R. L. Coffman. 1996. A critical role for transforming growth factor-β but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RBlow CD4+ T cells. J. Exp. Med. 183: 2669-2674. (Pubitemid 26192376)
30. + T cells: a population of T cells with immune regulatory activities in vitro. Eur. J. Immunol. 28: 3435-3447.
31. Lasarte, J. J., F. J. Corrales, N. Casares, A. López-Díaz de Cerio, C. Qian, X. Xie, F. Borras-Cuesta, and J. Prieto. 1999. Different doses of adenoviral vector expressing IL-12 enhance or depress the immune response to a coadministered antigen: the role of nitric oxide. J. Immunol. 162: 5270-5277.
32. Blume, K. G. 2001. The E. Donnall Thomas Lecture 2001: improve the outcome of autologous hematopoietic cell transplantation. Biol. Blood Marrow Transplant. 7: 363-367.
33. Anderson, M. S., E. S. Venanzi, L. Klein, Z. Chen, S. P. Berzins, S. J. Turley, H. Von Boehmer, R. Bronson, A. Dierich, C. Benoist, and D. Mathis. 2002. Projection of an immunological self shadow within the thymus by the aire protein. Science 298: 1395-1401.
34. Xia, G., J. Goebels, O. Rutgeerts, M. Vandeputte, and M. Waer. 2001. Transplantation tolerance and autoimmunity after xenogeneic thymus transplantation. J. Immunol. 166: 1843-1854. (Pubitemid 32114670)
35. Taguchi, O., T. Takahashi, M. Seto, R. Namikawa, M. Matsuyama, and Y. Nishizuka. 1986. Development of multiple organ-localized autoimmune diseases in nude mice after reconstitution of T cell function by rat fetal thymus graft. J. Exp. Med. 164: 60-71. (Pubitemid 16069222)
36. Nishigaki-Maki, K., T. Takahashi, K. Ohno, T. Morimoto, H. Ikeda, M. Takeuchi, M. Ueda, and O. Taguchi. 1999. Autoimmune diseases developed in athymic nude mice grafted with embryonic thymus of xenogeneic origin. Eur. J. Immunol. 29: 3350-3359. (Pubitemid 29484226)
37. Iwasaki, A., Y. Yoshikai, M. Sakumoto, K. Himeno, H. Yuuki, M. Kumamoto, K. Sueishi, and K. Nomoto. 1990. Sequential appearance of host-derived T cell subsets during differentiation in nude mice grafted with rat fetal thymus. J. Immunol. 145: 28-35. (Pubitemid 20217379)
38. + T regulatory cells that can suppress ongoing experimental autoimmune encephalomyelitis. J. Immunol. 172: 1991-1995.
39. Xystrakis, E., A. S. Dejean, I. Bernard, P. Druet, R. Liblau, D. Gonzalez-Dunia, and A. Saoudi. 2004. Identification of a novel natural regulatory CD8 T-cell subset and analysis of its mechanism of regulation. Blood 104: 3294-3301. (Pubitemid 39507148)
40. Hu, D., K. Ikizawa, L. Lu, M. E. Sanchirico, M. L. Shinohara, and H. Cantor. 2004. Analysis of regulatory CD8 T cells in Qa-1-deficient mice. Nat. Immunol. 5: 516-523. (Pubitemid 38660464)
41. + T cells. J. Immunol. 177: 7645-7655.
42. + T cells develop in porcine thymus grafts in mice. Xenotransplantation 5: 99-104.
43. Hongo, D., S. Hadidi, S. Damrauer, V. Garrigue, D. Kraft, D. H. Sachs, B. Nikolic, and M. Sykes. 2007. Porcine thymic grafts protect human thymocytes from HIV-1-induced destruction. J. Infect. Dis. 196: 900-910. (Pubitemid 47378941)
44. Min, B., H. Yamane, J. Hu-Li, and W. E. Paul. 2005. Spontaneous and homeostatic proliferation of CD4 T cells are regulated by different mechanisms. J. Immunol. 174: 6039-6044. (Pubitemid 40663791)
45. + T cells in lymphopenic hosts. Immunity 11: 183-190.
46. Kieper, W. C., and S. C. Jameson. 1999. Homeostatic expansion and phenotypic conversion of naive T cells in response to self peptide/MHC ligands. Proc. Natl. Acad. Sci. USA 96: 13306-13311.
47. + T cells perceive a positively selecting class II MHC/peptide complex in the periphery. J. Immunol. 164: 3087-3094.
48. Zhao, Y., J. J. Sergio, K. A. Swenson, J. S. Arn, D. H. Sachs, and M. Sykes. 1997. Positive and negative selection of functional mouse CD4 cells by porcine MHC in pig thymus grafts. J. Immunol. 159: 2100-2107. (Pubitemid 127680997)
49. Shimizu, I., Y. Fudaba, A. Shimizu, Y. G. Yang, and M. Sykes. 2008. Comparison of human T cell repertoire generated in xenogeneic porcine and human thymus grafts. Transplantation 86: 601-610.