Constraints in antigen presentation severely restrict T cell recognition of the allogeneic fetus

Journal of Clinical Investigation

Volumn 117, Issue 5, 2007, Pages 1399-1411

  Erlebacher, Adrian ^a   Vencato, Daniela ^a   Price, Kelly A ^b   Zhang, Dorothy ^b   Glimcher, Laurie H ^b,c  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; FETAL ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OVALBUMIN;

ALLOGENEIC RESTRICTION; ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; FETUS OUTCOME; GRAFT REJECTION; IMMUNE RESPONSE; IMMUNITY; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTOTOXICITY; MAJOR HISTOCOMPATIBILITY COMPLEX; MOTHER FETUS RELATIONSHIP; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; SURVIVAL; TROPHOBLAST;

ANIMALS; ANTIGEN PRESENTATION; EGG PROTEINS; FEMALE; FETUS; H-2 ANTIGENS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, KNOCKOUT; MICE, TRANSGENIC; OVALBUMIN; PREGNANCY; T-LYMPHOCYTES;

EID: 34248214561     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI28214     Document Type: Article

References (49)

1. Game, D.S., and Lechler, R.I. 2002. Pathways of allorecognition: implications for transplantation tolerance. Transpl. Immunol. 10:101-108.
2. Benichou, G., Valujskikh, A., and Heeger, P.S. 1999. Contributions of direct and indirect T cell alloreactivity during allograft rejection in mice. J. Immunol. 162:352-358.
3. Suchin, E.J., et al. 2001. Quantifying the frequency of alloreactive T cells in vivo: new answers to an old question. J. Immunol. 166:973-981.
4. Campos, L., et al. 1995. Survival of MHC-deficient mouse heterotopic cardiac allografts. Transplantation. 59:187-191.
5. Chen, Y., Demir, Y., Valujskikh, A., and Heeger, P.S. 2003. The male minor transplantation antigen preferentially activates recipient CD4+ T cells through the indirect presentation pathway in vivo. J. Immunol. 171:6510-6518.
6. Pietra, B.A., Wiseman, A., Bolwerk, A., Rizeq, M., and Gill, R.G. 2000. CD4 T cell-mediated cardiac allograft rejection requires donor but not host MHC class II. J. Clin. Invest. 106:1003-1010.
7. Valujskikh, A., Lantz, O., Celli, S., Matzinger, P., and Heeger, P.S. 2002. Cross-primed CD8(+) T cells mediate graft rejection via a distinct effector pathway. Nat. Immunol. 3:844-851.
8. Grazia, T.J., et al. 2004. A two-step model of acute CD4 T-cell mediated cardiac allograft rejection. J. Immunol. 172:7451-7458.
9. Moffett, A., and Loke, C. 2006. Immunology of placentation in eutherian mammals. Nat. Rev. Immunol. 6:584-594.
10. Trowsdale, J., and Betz, A.G. 2006. Mother's little helpers: mechanisms of maternal-fetal tolerance. Nat. Immunol. 7:241-246.
11. Tafuri, A., Alferink, J., Moller, P., Hammerling, G.J., and Arnold, B. 1995. T cell awareness of paternal alloantigens during pregnancy. Science. 270:630-633.
12. Jaffe, L., Jeannotte, L., Bikoff, E.K., and Robertson, E.J. 1990. Analysis of beta 2-microglobulin gene expression in the developing mouse embryo and placenta. J. Immunol. 145:3474-3482.
13. Jaffe, L., Robertson, E.J., and Bikoff, E.K. 1991. Distinct patterns of expression of MHC class I and beta 2-microglobulin transcripts at early stages of mouse development. J. Immunol. 147:2740-2749.
14. Mattsson, R., Mattsson, A., Holmdahl, R., Scheynius, A., and Van der Meide, P.H. 1992. In vivo treatment with interferon-gamma during early pregnancy in mice induces strong expression of major histocompatibility complex class I and II molecules in uterus and decidua but not in extra-embryonic tissues. Biol. Reprod. 46:1176-1186.
15. Rogers, A.M., Boime, I., Connolly, J., Cook, J.R., and Russell, J.H. 1998. Maternal-fetal tolerance is maintained despite transgene-driven trophoblast expression of MHC class I, and defects in Fas and its ligand. Eur. J. Immunol. 28:3479-3487.
16. Zhou, M., and Mellor, A.L. 1998. Expanded cohorts of maternal CD8+ T-cells specific for paternal MHC class I accumulate during pregnancy. J. Reprod. Immunol. 40:47-62.
17. Vacchio, M.S., and Hodes, R.J. 2003. CD28 costimulation is required for in vivo induction of peripheral tolerance in CD8 T cells. J. Exp. Med. 197:19-26.
18. Kearney, E.R., Pape, K.A., Loh, D.Y., and Jenkins, M.K. 1994. Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity. 1:327-339.
19. Seavey, M.M., and Mosmann, T.R. 2006. Paternal antigen-bearing cells transferred during insemination do not stimulate anti-paternal CD8+ T cells: role of estradiol in locally inhibiting CD8+ T cell responses. J. Immunol. 177:7567-7578.
20. Munn, D.H., et al. 1998. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science. 281:1191-1193.
21. Aluvihare, V.R., Kallikourdis, M., and Betz, A.G. 2004. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 5:266-271.
22. Guleria, I., et al. 2005. A critical role for the programmed death ligand 1 in fetomaternal tolerance. J. Exp. Med. 202:231-237.
23. Duclos, A.J., Pomerantz, D.K., and Baines, M.G. 1994. Relationship between decidual leukocyte infiltration and spontaneous abortion in a murine model of early fetal resorption. Cell. Immunol. 159:184-193.
24. Ehst, B.D., Ingulli, E., and Jenkins, M.K. 2003. Development of a novel transgenic mouse for the study of interactions between CD4 and CD8 T cells during graft rejection. Am. J. Transplant. 3:1355-1362.
25. Barnden, M.J., Allison, J., Heath, W.R., and Carbone, F.R. 1998. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76:34-40.
26. Erlebacher, A., Zhang, D., Parlow, A.F., and Glimcher, L.H. 2004. Ovarian insufficiency and early pregnancy loss induced by activation of the innate immune system. J. Clin. Invest. 114:39-48. doi:10.1172/ JCI200420645.
27. Kurts, C., Kosaka, H., Carbone, F.R., Miller, J.F., and Heath, W.R. 1997. Class I-restricted cross-presentation of exogenous self-antigens leads to deletion of autoreactive CD8(+) T cells. J. Exp. Med. 186:239-245.
28. Jiang, S., Herrera, O., and Lechler, R.I. 2004. New spectrum of allorecognition pathways: implications for graft rejection and transplantation tolerance. Curr. Opin. Immunol. 16:550-557.
29. Nikolic-Zugic, J., and Bevan, M.J. 1990. Role of self-peptides in positively selecting the T-cell repertoire. Nature. 344:65-67.
30. Sponaas, A.M., et al. 1994. Induction of tolerance to self MHC class I molecules expressed under the control of milk protein or beta-globin gene promoters. Int. Immunol. 6:277-287.
31. Hernandez, J., Aung, S., Redmond, W.L., and Sherman, L.A. 2001. Phenotypic and functional analysis of CD8(+) T cells undergoing peripheral deletion in response to cross-presentation of self-antigen. J. Exp. Med. 194:707-717.
32. Quezada, S.A., et al. 2005. Analysis of the underlying cellular mechanisms of anti-CD154-induced graft tolerance: the interplay of clonal anergy and immune regulation. J. Immunol. 175:771-779.
33. Reinhardt, R.L., Khoruts, A., Merica, R., Zell, T., and Jenkins, M.K. 2001. Visualizing the generation of memory CD4 T cells in the whole body. Nature. 410:101-105.
34. Bonifaz, L., et al. 2002. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J. Exp. Med. 196:1627-1638.
35. Ahonen, C.L., et al. 2004. Combined TLR and CD40 triggering induces potent CD8+ T cell expansion with variable dependence on type I IFN. J. Exp. Med. 199:775-784.
36. Bonney, E.A., and Matzinger, P. 1997. The maternal immune system's interaction with circulating fetal cells. J. Immunol. 158:40-47.
37. Huppertz, B., and Herrler, A. 2005. Regulation of proliferation and apoptosis during development of the preimplantation embryo and the placenta. Birth Defects Res. C Embryo Today. 75:249-261.
38. Tew, J.G., et al. 1997. Follicular dendritic cells and presentation of antigen and costimulatory signals to B cells. Immunol. Rev. 156:39-52.
39. Auphan, N., et al. 1994. The degree of CD8 dependence of cytolytic T cell precursors is determined by the nature of the T cell receptor (TCR) and influences negative selection in TCR-transgenic mice. Eur. J. Immunol. 24:1572-1577.
40. Baratin, M., Bonin, K., and Daniel, C. 2004. Frontline: peripheral priming of alloreactive T cells by the direct pathway of allorecognition. Eur. J. Immunol. 34:3305-3314.
41. Braun, M.Y., et al. 2001. Acute rejection in the absence of cognate recognition of allograft by T cells. J. Immunol. 166:4879-4883.
42. He, C., and Heeger, P.S. 2004. CD8 T cells can reject major histocompatibility complex class I-deficient skin allografts. Am. J. Transplant. 4:698-704.
43. Sandner, S.E., et al. 2003. New TCR transgenic model for tracking allospecific CD4 T-cell activation and tolerance in vivo. Am. J. Transplant. 3:1242-1250.
44. Valujskikh, A., Zhang, Q., and Heeger, P.S. 2006. CD8 T cells specific for a donor-derived, self-restricted transplant antigen are nonpathogenic bystanders after vascularized heart transplantation in mice. J. Immunol. 176:2190-2196.
45. -/- mice. Nat. Med. 7:557-562.
46. Lanier, L.L. 2005. NK cell recognition. Annu. Rev. Immunol. 23:225-274.
47. Hanna, J., et al. 2006. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat. Med. 12:1065-1074.
48. Uehara, S., et al. 2005. NK cells can trigger allograft vasculopathy: the role of hybrid resistance in solid organ allografts. J. Immunol. 175:3424-3430.
49. Ouyang, W., et al. 1998. Inhibition of Th1 development mediated by GATA-3 through an IL-4-independent mechanism. Immunity. 9:745-755.