Pathogenic effector T cell enrichment overcomes regulatory T cell control and generates autoimmune gastritis

Journal of Immunology

Volumn 181, Issue 9, 2008, Pages 5895-5903

  Monteiro, João P ^a,b   Farache, Julia ^a,b   Mercadante, Ana Carolina ^a   Mignaco, Julio A ^b   Bonamino, Martin ^a   Bonomo, Adriana ^a,b  

^a INSTITUTO NACIONAL DE CÂNCER   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNE DISEASE; CLONE; CONTROLLED STUDY; DISEASE PREDISPOSITION; EFFECTOR CELL; GASTRITIS; HUMAN; LYMPHOCYTOPENIA; MOUSE; NEWBORN; NEWBORN PERIOD; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; THYMECTOMY; THYMUS; A J MOUSE; ANIMAL; BAGG ALBINO MOUSE; C3H MOUSE; C57BL MOUSE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CYTOLOGY; DBA MOUSE; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; MOUSE MUTANT; NUDE MOUSE; PATHOLOGY;

ANIMALS; ANIMALS, NEWBORN; AUTOIMMUNE DISEASES; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; GASTRITIS; GENETIC PREDISPOSITION TO DISEASE; IMMUNITY, INNATE; LYMPHOPENIA; MICE; MICE, INBRED A; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, NUDE; MICE, SCID; T-LYMPHOCYTES, REGULATORY;

EID: 58749102616     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.9.5895     Document Type: Article

References (46)

1. + regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22: 531-562.
2. + regulatory T cells. Nat. Immunol. 4: 330-336.
3. + T regulatory cells. Nat. Immunol. 4: 337-342.
4. Torgerson, T. R., and H. D. Ochs. 2007. Immune dysregulation, polyendocrinopathy, enteropathy, X-linked: forkhead box protein 3 mutations and lack of regulatory T cells. J. Allergy Clin. Immunol. 120: 744-750; quiz 751-1742
5. Asano, M., M. Toda, N. Sakaguchi, and S. Sakaguchi. 1996. Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J. Exp. Med. 184: 387-396. (Pubitemid 26324092)
6. Gleeson, P. A., B. H. Toh, and I. R. van Driel. 1996. Organ-specific autoimmunity induced by lymphopenia. Immunol. Rev. 149: 97-125.
7. Shevach, E. M. 2000. Regulatory T cells in autoimmmunity. Annu. Rev. Immunol. 18: 423-449.
8. Sakaguchi, S., T. Takahashi, and Y. Nishizuka. 1982. Study on cellular events in postthymectomy autoimmune oophoritis in mice: I. Requirement of Lyt-1 effector cells for oocytes damage after adoptive transfer. J. Exp. Med. 156: 1565-1576. (Pubitemid 13167405)
9. Suri-Payer, E., P. J. Kehn, A. W. Cheever, and E. M. Shevach. 1996. Pathogenesis of post-thymectomy autoimmune gastritis: identification of anti-H/K adenosine triphosphatase-reactive T cells. J. Immunol. 157: 1799-1805. (Pubitemid 126449125)
10. Kim, J. M., J. P. Rasmussen, and A. Y. Rudensky. 2007. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 8: 191-197.
11. Kojima, A., and R. T. Prehn. 1981. Genetic susceptibility to post-thymectomy autoimmune diseases in mice. Immunogenetics 14: 15-27. (Pubitemid 12246051)
12. Mori, Y., M. Hosono, K. Murakami, H. Katoh, Y. Yoshikawa, K. Kuribayashi, R. Kannagi, M. Sakai, M. Okuma, and T. Masuda. 1991. Genetic studies on experimental autoimmune gastritis induced by neonatal thymectomy using recombinant inbred strains between a high-incidence strain, BALB/c, and a low-incidence strain, DBA/2. Clin. Exp. Immunol. 84: 145-152.
13. Alderuccio, F., B. H. Toh, S. S. Tan, P. A. Gleeson, and I. R. van Driel. 1993. An autoimmune disease with multiple molecular targets abrogated by the transgenic expression of a single autoantigen in the thymus. J. Exp. Med. 178: 419-426. (Pubitemid 23218190)
14. Taguchi, O., Y. Nishizuka, T. Sakakura, and A. Kojima. 1980. Autoimmune oophoritis in thymectomized mice: detection of circulating antibodies against oocytes. Clin. Exp. Immunol. 40: 540-553. (Pubitemid 10070085)
15. Bonomo, A., P. J. Kehn, and E. M. Shevach. 1994. Premature escape of double-positive thymocytes to the periphery of young mice: possible role in autoimmunity. J. Immunol. 152: 1509-1514. (Pubitemid 24075680)
16. Morgan, D. J., C. Kurts, H. T. Kreuwel, K. L. Holst, W. R. Heath, and L. A. Sherman. 1999. Ontogeny of T cell tolerance to peripherally expressed antigens. Proc. Natl. Acad. Sci. USA 96: 3854-3858. (Pubitemid 29169000)
17. Smith, H., I. M. Chen, R. Kubo, and K. S. Tung. 1989. Neonatal thymectomy results in a repertoire enriched in T cells deleted in adult thymus. Science 245: 749-752. (Pubitemid 19214009)
18. Bonomo, A., P. J. Kehn, E. Payer, L. Rizzo, A. W. Cheever, and E. M. Shevach. 1995. Pathogenesis of post-thymectomy autoimmunity: role of syngeneic MLR-reactive T cells. J. Immunol. 154: 6602-6611.
19. Le Campion, A., C. Bourgeois, F. Lambolez, B. Martin, S. Leaument, N. Dautigny, C. Tanchot, C. Penit, and B. Lucas. 2002. Naive T cells proliferate strongly in neonatal mice in response to self-peptide/self-MHC complexes. Proc. Natl. Acad. Sci. USA 99: 4538-4543. (Pubitemid 34286020)
20. Rocha, B., C. Penit, C. Baron, F. Vasseur, N. Dautigny, and A. A. Freitas. 1990. Accumulation of bromodeoxyuridine-labeled cells in central and peripheral lymphoid organs: minimal estimates of production and turnover rates of mature lymphocytes. Eur. J. Immunol. 20: 1697-1708. (Pubitemid 20290902)
21. + T cells. Proc. Natl. Acad. Sci. USA 101: 14473-14478.
22. Jones, C. M., J. M. Callaghan, P. A. Gleeson, Y. Mori, T. Masuda, and B. H. Toh. 1991. The parietal cell autoantigens recognized in neonatal thymectomy-induced murine gastritis are the α and β subunits of the gastric proton pump. Gastroenterology 101: 287-294.
23. Suri-Payer, E., A. Z. Amar, R. McHugh, K. Natarajan, D. H. Margulies, and E. M. Shevach. 1999. Post-thymectomy autoimmune gastritis: fine specificity and pathogenicity of anti-H/K ATPase-reactive T cells. Eur. J. Immunol. 29: 669-677. (Pubitemid 29078529)
24. + T cells prevent the development of organ-specific autoimmune disease by inhibiting the differentiation of autoreactive effector T cells. J. Immunol. 175: 7135-7142.
25. Scheinecker, C., R. McHugh, E. M. Shevach, and R. N. Germain. 2002. Constitutive presentation of a natural tissue autoantigen exclusively by dendritic cells in the draining lymph node. J. Exp. Med. 196: 1079-1090. (Pubitemid 35231766)
26. Min, B., R. McHugh, G. D. Sempowski, C. Mackall, G. Foucras, and W. E. Paul. 2003. Neonates support lymphopenia-induced proliferation. Immunity 18: 131-140.
27. + medullary thymic epithelial cells. Nat. Immunol. 8: 351-358.
28. Fontenot, J. D., J. L. Dooley, A. G. Farr, and A. Y. Rudensky. 2005. Developmental regulation of Foxp3 expression during ontogeny. J. Exp. Med. 202: 901-906. (Pubitemid 41396890)
29. Sakaguchi, S., N. Sakaguchi, M. Asano, M. Itoh, and M. Toda. 1995. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25): breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155: 1151-1164.
30. La Gruta, N. L., I. R. Driel, and P. A. Gleeson. 2000. Peripheral T cell expansion in lymphopenic mice results in a restricted T cell repertoire. Eur. J. Immunol. 30: 3380-3386.
31. + regulatory T cells is indexed to the number of IL-2-producing cells. J. Immunol. 177: 192-200.
32. Fontenot, J. D., J. P. Rasmussen, L. M. Williams, J. L. Dooley, A. G. Farr, and A. Y. Rudensky. 2005. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22: 329-341. (Pubitemid 40387475)
33. + T regulatory cell development during the neonatal period. J. Exp. Med. 201: 769-777.
34. Samy E. T., K. M. Wheeler, R. J. Roper, C. Teuscher, and K. S. Tung. 2008. Cutting edge: autoimmune disease in day 3 thymectomized mice is actively controlled by endogenous disease-specific regulatory T cells. J. Immunol. 180: 4366-4370.
35. Kyewski, B., and J. Derbinski. 2004. Self-representation in the thymus: an extended view. Nat. Rev. Immunol. 4: 688-698.
36. 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.
37. Liston, A., S. Lesage, J. Wilson, L. Peltonen, and C. C. Goodnow. 2003. Aire regulates negative selection of organ-specific T cells. Nat. Immunol. 4: 350-354. (Pubitemid 36432317)
38. DeVoss, J., Y. Hou, K. Johannes, W. Lu, G. I. Liou, J. Rinn, H. Chang, R. R. Caspi, L. Fong, and M. S. Anderson. 2006. Spontaneous autoimmunity prevented by thymic expression of a single self-antigen. J. Exp. Med. 203: 2727-2735. (Pubitemid 44833348)
39. Klein, L., M. Klugmann, K. A. Nave, V. K. Tuohy, and B. Kyewski. 2000. Shaping of the autoreactive T-cell repertoire by a splice variant of self protein expressed in thymic epithelial cells. Nat. Med. 6: 56-61. (Pubitemid 30048526)
40. De Silva, H. D., P. A. Gleeson, B. H. Toh, I. R. Van Driel, and F. R. Carbone. 1999. Identification of a gastritogenic epitope of the H/K ATPase β-subunit. Immunology 96: 145-151.
41. Allen, S., S. Read, R. DiPaolo, R. S. McHugh, E. M. Shevach, P. A. Gleeson, and I. R. van Driel. 2005. Promiscuous thymic expression of an autoantigen gene does not result in negative selection of pathogenic T cells. J. Immunol. 175: 5759-5764. (Pubitemid 41508059)
42. Alderuccio, F., P. A. Gleeson, S. P. Berzins, M. Martin, I. R. Van Driel, and B. H. Toh. 1997. Expression of the gastric H/K-ATPase α-subunit in the thymus may explain the dominant role of the β-subunit in the pathogenesis of autoimmune gastritis. Autoimmunity 25: 167-175. (Pubitemid 27384766)
43. Canto, E., S. Vidal, and J. L. Rodriguez-Sanchez. 2003. HK-ATPase expression in the susceptible BALB/c and the resistant DBA/2 strains of mice to autoimmune gastritis. Autoimmunity 36: 275-283. (Pubitemid 36992448)
44. Taubert, R., J. Schwendemann, and B. Kyewski. 2007. Highly variable expression of tissue-restricted self-antigens in human thymus: implications for self-tolerance and autoimmunity. Eur. J. Immunol. 37: 838-848. (Pubitemid 46916950)
45. Laurie, K. L., I. R. Van Driel, T. D. Zwar, S. P. Barrett, and P. A. Gleeson. 2002. Endogenous H/K ATPase β-subunit promotes T cell tolerance to the immunodominant gastritogenic determinant. J. Immunol. 169: 2361-2367.
46. + regulatory T cells inhibit the antigen-dependent expansion of self-reactive T cells in vivo. J. Immunol. 176: 1609-1617.