How specificity for self-peptides shapes the development and function of regulatory T cells

Journal of Leukocyte Biology

Volumn 88, Issue 6, 2010, Pages 1099-1107

  Simons, Donald M ^a   Cozzo Picca, Cristina ^a   Oh, Soyoung ^a   Perng, Olivia A ^a   Aitken, Malinda ^a   Erikson, Jan ^a   Caton, Andrew J ^a  

^a WISTAR INSTITUTE   (United States)

Author keywords

Foxp3; Immune regulation; Selection; T cell receptor; Thymocyte

Indexed keywords

PEPTIDE; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ANTIGEN RECOGNITION; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL MATURATION; CELLULAR IMMUNITY; HUMAN; LYMPHOCYTE FUNCTION; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; THYMOCYTE; THYMUS; TRANSGENIC ANIMAL;

ANIMALS; AUTOANTIGENS; AUTOIMMUNE DISEASES; HUMANS; MICE; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND;

MUS;

EID: 78649722883     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0310183     Document Type: Review

References (59)

1. Marrack, P., Kappler, J. (1994) Subversion of the immune system by pathogens. Cell 76, 323-332.
2. Nossal, G. J. (1994) Negative selection of lymphocytes. Cell 76, 229-239.
3. Sprent, J., Kishimoto, H. (2002) The thymus and negative selection. Immunol. Rev. 185, 126-135.
4. Schwartz, R. H. (1997) T cell clonal anergy. Curr. Opin. Immunol. 9, 351-357.
5. Sakaguchi, S. (2000) Regulatory T cells: key controllers of immunologic self-tolerance. Cell 101, 455-458.
6. Shevach, E. M. (2000) Regulatory T cells in autoimmmunity. Annu. Rev. Immunol. 18, 423-449.
7. Sakaguchi, S. (2004) Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22, 531-562.
8. Zheng, Y., Rudensky, A. Y. (2007) Foxp3 in control of the regulatory T cell lineage. Nat. Immunol. 8, 457-462.
9. Starr, T. K., Jameson, S. C., Hogquist, K. A. (2003) Positive and negative selection of T cells. Annu. Rev. Immunol. 21, 139-176.
10. Hogquist, K. A., Jameson, S. C., Heath, W. R., Howard, J. L., Bevan, M. J., Carbone, F. R. (1994) T cell receptor antagonist peptides induce positive selection. Cell 76, 17-27.
11. Jameson, S. C., Hogquist, K. A., Bevan, M. J. (1994) Specificity and flexibility in thymic selection. Nature 369, 750-752.
12. Ashton-Rickardt, P. G., Bandeira, A., Delaney, J. R., Van Kaer, L., Pircher, H. P., Zinkernagel, R. M., Tonegawa, S. (1994) Evidence for a differential avidity model of T cell selection in the thymus. Cell 76, 651-663.
13. Sakaguchi, S., Takahashi, T., Nishizuka, Y. (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.
14. Sakaguchi, S., Takahashi, T., Nishizuka, Y. (1982) Study on cellular events in post-thymectomy autoimmune oophoritis in mice. II. Requirement of Lyt-1 cells in normal female mice for the prevention of oophoritis. J. Exp. Med. 156, 1577-1586. (Pubitemid 13167406)
15. Le Douarin, N., Corbel, C., Bandeira, A., Thomas-Vaslin, V., Modigliani, Y., Coutinho, A., Salaün, J. (1996) Evidence for a thymus-dependent form of tolerance that is not based on elimination or anergy of reactive T cells. Immunol. Rev. 149, 35-53. (Pubitemid 26096977)
16. Seddon, B., Mason, D. (2000) The third function of the thymus. Immunol. Today 21, 95-99.
17. Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M., Toda, M. (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.
18. Asano, M., Toda, M., Sakaguchi, N., Sakaguchi, S. (1996) Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J. Exp. Med. 184, 387-396.
19. Itoh, M., Takahashi, T., Sakaguchi, N., Kuniyasu, Y., Shimizu, J., Otsuka, F., Sakaguchi, S. (1999) Thymus and autoimmunity: production of CD25+ CD4+ naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J. Immunol. 162, 5317-5326. (Pubitemid 29307138)
20. Hori, S., Nomura, T., Sakaguchi, S. (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057-1061.
21. Fontenot, J. D., Gavin, M. A., Rudensky, A. Y. (2003) Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4, 330-336.
22. Fontenot, J. D., Dooley, J. L., Farr, A. G., Rudensky, A. Y. (2005) Developmental regulation of Foxp3 expression during ontogeny. J. Exp. Med. 202, 901-906.
23. Olivares-Villagomez, D., Wang, Y., Lafaille, J. J. (1998) Regulatory CD4(+) T cells expressing endogenous T cell receptor chains protect myelin basic protein-specific transgenic mice from spontaneous autoimmune encephalomyelitis. J. Exp. Med. 188, 1883-1894.
24. Van de Keere, F., Tonegawa, S. (1998) CD4(+) T cells prevent spontaneous experimental autoimmune encephalomyelitis in anti-myelin basic protein T cell receptor transgenic mice. J. Exp. Med. 188, 1875-1882.
25. Hori, S., Haury, M., Coutinho, A., Demengeot, J. (2002) Specificity requirements for selection and effector functions of CD25+4+ regulatory T cells in anti-myelin basic protein T cell receptor transgenic mice. Proc. Natl. Acad. Sci. USA 99, 8213-8218. (Pubitemid 34651032)
26. Jordan, M. S., Boesteanu, A., Reed, A. J., Petrone, A. L., Holenbeck, A. E., Lerman, M. A., Naji, A., Caton, A. J. (2001) Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat. Immunol. 2, 301-306.
27. Kawahata, K., Misaki, Y., Yamauchi, M., Tsunekawa, S., Setoguchi, K., Miyazaki, J., Yamamoto, K. (2002) Generation of CD4(+)CD25(+) regulatory T cells from autoreactive T cells simultaneously with their negative selection in the thymus and from nonautoreactive T cells by endogenous TCR expression. J. Immunol. 168, 4399-4405.
28. Larkin III, J., Rankin, A. L., Picca, C. C., Riley, M. P., Jenks, S. A., Sant, A. J., Caton, A. J. (2008) CD4+CD25+ regulatory T cell repertoire formation shaped by differential presentation of peptides from a self-antigen. J. Immunol. 180, 2149-2157.
29. Bautista, J. L., Lio, C-W. J., Lathrop, S. K., Forbush, K., Liang, Y., Luo, J., Rudensky, A. Y., Hsieh, C-S. (2009) Intraclonal competition limits the fate determination of regulatory T cells in the thymus. Nat. Immunol. 10, 610-617.
30. Leung, M. W., Shen, S., Lafaille, J. J. (2009) TCR-dependent differentiation of thymic Foxp3+ cells is limited to small clonal sizes. J. Exp. Med. 206, 2121-2130.
31. DiPaolo, R. J., Shevach, E. M. (2009) CD4+ T-cell development in a mouse expressing a transgenic TCR derived from a Treg. Eur. J. Immunol. 39, 234-240.
32. Jordan, M. S., Riley, M. P., von Boehmer, H., Caton, A. J. (2000) Anergy and suppression regulate CD4(+) T cell responses to a self peptide. Eur. J. Immunol. 30, 136-144.
33. Kirberg, J., Baron, A., Jakob, S., Rolink, A., Karjalainen, K., von Boehmer, H. (1994) Thymic selection of CD8+ single positive cells with a class II major histocompatibility complex-restricted receptor. J. Exp. Med. 180, 25-34.
34. Apostolou, I., Sarukhan, A., Klein, L., von Boehmer, H. (2002) Origin of regulatory T cells with known specificity for antigen. Nat. Immunol. 3, 756-763.
35. Lerman, M. A., Larkin III, J., Cozzo, C., Jordan, M. S., Caton, A. J. (2004) CD4+ CD25+ regulatory T cell repertoire formation in response to varying expression of a neo-self-antigen. J. Immunol. 173, 236-244.
36. Aschenbrenner, K., D'Cruz, L. M., Vollmann, E. H., Hinterberger, M., Emmerich, J., Swee, L. K., Rolink, A., Klein, L. (2007) Selection of Foxp3+ regulatory T cells specific for self antigen expressed and presented by Aire+ medullary thymic epithelial cells. Nat. Immunol. 8, 351-358.
37. Walker, L. S., Chodos, A., Eggena, M., Dooms, H., Abbas, A. K. (2003) Antigen-dependent proliferation of CD4+ CD25+ regulatory T cells in vivo. J. Exp. Med. 198, 249-258.
38. Van Santen, H. M., Benoist, C., Mathis, D. (2004) Number of Treg cells that differentiate does not increase upon encounter of agonist ligand on thymic epithelial cells. J. Exp. Med. 200, 1221-1230. (Pubitemid 39552564)
39. Kersh, G. J., Allen, P. M. (1996) Essential flexibility in the T-cell recognition of antigen. Nature 380, 495-498.
40. Picca, C. C., Oh, S., Panarey, L., Aitken, M., Basehoar, A., Caton, A. J. (2009) Thymocyte deletion can bias Treg formation toward low-abundance self-peptide. Eur. J. Immunol. 39, 3301-3306.
41. Mathis, D., Benoist, C. (2007) A decade of AIRE. Nat. Rev. Immunol. 7, 645-650.
42. Pacholczyk, R., Kern, J., Singh, N., Iwashima, M., Kraj, P., Ignatowicz, L. (2007) Nonself-antigens are the cognate specificities of Foxp3+ regulatory T cells. Immunity 27, 493-504.
43. Lio, C-W. J., Hsieh, C-S. (2008) A two-step process for thymic regulatory T cell development. Immunity 28, 100-111.
44. Hsieh, C. S., Zheng, Y., Liang, Y., Fontenot, J. D., Rudensky, A. Y. (2006) An intersection between the self-reactive regulatory and nonregulatory T cell receptor repertoires. Nat. Immunol. 7, 401-410.
45. Thornton, A. M., Shevach, E. M. (2000) Suppressor effector function of CD4+CD25+ immunoregulatory T cells is antigen nonspecific. J. Immunol. 164, 183-190.
46. Larkin III, J., Picca, C. C., Caton, A. J. (2007) Activation of CD4+ CD25+ regulatory T cell suppressor function by analogs of the selecting peptide. Eur. J. Immunol. 37, 139-146.
47. Seddon, B., Mason, D. (1999) Peripheral autoantigen induces regulatory T cells that prevent autoimmunity. J. Exp. Med. 189, 877-882.
48. Setiady, Y. Y., Ohno, K., Samy, E. T., Bagavant, H., Qiao, H., Sharp, C., She, J. X., Tung, K. S. (2006) Physiologic self antigens rapidly capacitate autoimmune disease-specific polyclonal CD4+ CD25+ regulatory T cells. Blood 107, 1056-1062.
49. Samy, E. T., Setiady, Y. Y., Ohno, K., Pramoonjago, P., Sharp, C., Tung, K. S. (2006) The role of physiological self-antigen in the acquisition and maintenance of regulatory T-cell function. Immunol. Rev. 212, 170-184.
50. Wheeler, K. M., Samy, E. T., Tung, K. S. K. (2009) Cutting edge: normal regional lymph node enrichment of antigen-specific regulatory T cells with autoimmune disease-suppressive capacity. J. Immunol. 183, 7635-7638.
51. Rankin, A. L., Reed, A. J., Oh, S., Cozzo Picca, C., Guay, H. M., Larkin III, J., Panarey, L., Aitken, M. K., Koeberlein, B., Lipsky, P. E., Tomaszewski, J. E., Naji, A., Caton, A. J. (2008) CD4+ T cells recognizing a single self-peptide expressed by APCs induce spontaneous autoimmune arthritis. J. Immunol. 180, 833-841.
52. Seo, S. J., Fields, M. L., Buckler, J. L., Reed, A. J., Mandik-Nayak, L., Nish, S. A., Noelle, R. J., Turka, L. A., Finkelman, F. D., Caton, A. J., Erikson, J. (2002) The impact of T helper and T regulatory cells on the regulation of anti-double-stranded DNA B cells. Immunity 16, 535-546.
53. Kanagawa, O., Militech, A., Vaupel, B. A. (2002) Regulation of diabetes development by regulatory T cells in pancreatic islet antigen-specific TCR transgenic nonobese diabetic mice. J. Immunol. 168, 6159-6164.
54. Tarbell, K. V., Yamazaki, S., Olson, K., Toy, P., Steinman, R. M. (2004) CD25+ CD4+ T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes. J. Exp. Med. 199, 1467-1477.
55. Tang, Q., Henriksen, K. J., Bi, M., Finger, E. B., Szot, G., Ye, J., Masteller, E. L., McDevitt, H., Bonyhadi, M., Bluestone, J. A. (2004) In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J. Exp. Med. 199, 1455-1465.
56. McHugh, R. S., Shevach, E. M., Margulies, D. H., Natarajan, K. (2001) A T cell receptor transgenic model of severe, spontaneous organ-specific autoimmunity. Eur. J. Immunol. 31, 2094-2103.
57. Datta, S., Sarvetnick, N. (2009) Lymphocyte proliferation in immune-mediated diseases. Trends Immunol. 30, 430-438.
58. Stummvoll, G. H., DiPaolo, R. J., Huter, E. N., Davidson, T. S., Glass, D., Ward, J. M., Shevach, E. M. (2008) Th1, Th2, and Th17 effector T cell-induced autoimmune gastritis differs in pathological pattern and in susceptibility to suppression by regulatory T cells. J. Immunol. 181, 1908-1916.
59. Oh, S., Rankin, A. L., Caton, A. J. (2010) CD4+CD25+ regulatory T cells in autoimmune arthritis. Immunol. Rev. 233, 97-111.