The origin of thymic CD4+CD25+ regulatory T cells and their co-stimulatory requirements are determined after elimination of recirculating peripheral CD4+ cells

International Immunology

Volumn 19, Issue 4, 2007, Pages 455-463

  Zhan, Yifan ^a   Bourges, Dorothee ^a   Dromey, James A ^a   Harrison, Leonard C ^a   Lew, Andrew M ^a  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; FLOW CYTOMETRY; HOMEOSTASIS; LYMPHOCYTE DEPLETION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; THYMOCYTE; THYMUS; TRANSGENIC MOUSE; WILD TYPE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD28; ANTIGENS, CD4; CD4-POSITIVE T-LYMPHOCYTES; CD40 LIGAND; CELL COUNT; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; COCULTURE TECHNIQUES; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOCONJUGATES; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, NERVE GROWTH FACTOR; RECEPTORS, TUMOR NECROSIS FACTOR; SPLEEN; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND;

EID: 34047100896     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxm010     Document Type: Article

References (49)

1. Fehervari, Z. and Sakaguchi, S. 2004. Development and function of CD25+CD4+ regulatory T cells. Curr. Opin. Immunol. 16:203.
2. Shevach, E. M. 2002. CD4+ CD25+ suppressor T cells: More questions than answers. Nat. Rev. Immunol. 2:389.
3. Itoh, M., Takahashi, T., Sakaguchi, N. et al. 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.
4. McHugh, R. S., Whitters, M. J., Piccirillo, C. A. et al. 2002. CD4(+)CD25(+) immunoregulatory T cells: Gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 16:311.
5. Hori, S., Nomura, T. and Sakaguchi, S. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057.
6. Fontenot, J. D., Gavin, M. A. and Rudensky, A. Y. 2003. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4:330.
7. Fontenot, J. D., Dooley, J. L., Farr, A. G. and Rudensky, A. Y. 2005. Developmental regulation of Foxp3 expression during ontogeny. J. Exp. Med. 202:901.
8. Fontenot, J. D., Rasmussen, J. P., Williams, L. M., Dooley, J. L., Farr, A. G. and Rudensky, A. Y. 2005. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22:329.
9. Fontenot, J. D., Rasmussen, J. P., Gavin, M. A. and Rudensky, A. Y. 2005. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6:1142.
10. Knoechel, B., Lohr, J., Kahn, E., Bluestone, J. A. and Abbas, A. K. 2005. Sequential development of interleukin 2-dependent effector and regulatory T cells in response to endogenous systemic antigen. J. Exp. Med. 202:1375.
11. Liang, S., Alard, P., Zhao, Y., Parnell, S., Clark, S. L. and Kosiewicz, M. M. 2005. Conversion of CD4+ CD25- cells into CD4+ CD25+ regulatory T cells in vivo requires B7 costimulation, but not the thymus. J. Exp. Med. 201:127.
12. Naparstek, Y., Holoshitz, J., Eisenstein, S. et al. 1982. Effector T lymphocyte line cells migrate to the thymus and persist there. Nature 300:262.
13. Michie, S. A. and Rouse, R. V. 1989. Traffic of mature lymphocytes into the mouse thymus. Thymus 13:141.
14. Agus, D. B., Surh, C. D. and Sprent, J. 1991. Reentry of T cells to the adult thymus is restricted to activated T cells. J. Exp. Med. 173:1039.
15. Westermann, J., Smith, T., Peters, U. et al. 1996. Both activated and nonactivated leukocytes from the periphery continuously enter the thymic medulla of adult rats: Phenotypes, sources and magnitude of traffic. Eur. J. Immunol. 26:1866.
16. Tian, C., Bagley, J., Forman, D. and Iacomini, J. 2004. Induction of central tolerance by mature T cells. J. Immunol. 173:7217.
17. Gopinathan, R., DePaz, H. A., Oluwole, O. O. et al. 2001. Role of reentry of in vivo alloMHC peptide-activated T cells into the adult thymus in acquired systemic tolerance. Transplantation 72:1533.
18. Chau, L. A., Rohekar, S., Wang, J. J. et al. 2002. Thymic re-entry of mature activated T cells and increased negative selection in vascularized allograft recipients. Clin. Exp. Immunol. 127:43.
19. Emmanouilidis, N., Guo, Z., Dong, Y. et al. 2006. Immunosuppressive and trafficking properties of donor splenic and bone marrow dendritic cells. Transplantation 81:455.
20. Salomon, B., Lenschow, D. J., Rhee, L. et al. 2000. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 12:431.
21. Tang, Q., Henriksen, K. J., Boden, E. K. et al. 2003. Cutting edge: CD28 controls peripheral homeostasis of CD4+CD25+ regulatory T cells. J. Immunol. 171:3348.
22. Tai, X., Cowan, M., Feigenbaum, L. and Singer, A. 2005. CD28 costimulation of developing thymocytes induces Foxp3 expression and regulatory T cell differentiation independently of interleukin 2. Nat. Immunol. 6:152.
23. Tang, Q., Henriksen, K. J., Bi, M. et al. 2004. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J. Exp. Med. 199:1455.
24. Kumanogoh, A., Wang, X., Lee, I. et al. 2001. Increased T cell autoreactivity in the absence of CD40-CD40 ligand interactions: A role of CD40 in regulatory T cell development. J. Immunol. 166:353.
25. Guiducci, C., Valzasina, B., Dislich, H. and Colombo, M. P. 2005. CD40/ CD40L interaction regulates CD4+CD25+ Treg homeostasis through dendritic cell-produced IL-2. Eur. J. Immunol. 35:557.
26. Bour-Jordan, H., Salomon, B. L., Thompson, H. L., Szot, G. L., Bernhard, M. R. and Bluestone, J. A. 2004. Costimulation controls diabetes by altering the balance of pathogenic and regulatory T cells. J. Clin. Invest. 114:979.
27. Zhan, Y., Purton, J. F., Godfrey, D. I., Cole, T. J., Heath, W. R. and Lew, A. M. 2003. Without peripheral interference, thymic deletion is mediated in a cohort of double-positive cells without classical activation. Proc. Natl Acad. Sci. USA 100:1197.
28. Zhan, Y., Brown, L. E., Deliyannis, G. et al. 2004. Responses against complex antigens in various models of CD4 T-cell deficiency: Surprises from an anti-CD4 antibody transgenic mouse. Immunol. Res. 30:1.
29. Sutherland, R. M., Brady, J. L., Georgiou, H. M., Thomas, H. E. and Lew, A. M. 2000. Protective effect of CTLA4Ig secreted by transgenic fetal pancreas allografts. Transplantation 69:1806.
30. Zhan, Y., Brady, J. L., Sutherland, R. M. and Lew, A. M. 2001. Without CD4 help, CD8 rejection of pig xenografts requires CD28 costimulation but not perforin killing. J. Immunol. 167:6279.
31. Xu, J., Foy, T. M., Laman, J. D. et al. 1994. Mice deficient for the CD40 ligand. Immunity 1:423.
32. Sakaguchi, S. 2003. The origin of FOXP3-expressing CD4+ regulatory T cells: Thymus or periphery. J. Clin. Invest. 112:1310.
33. Apostolou, I., Sarukhan, A., Klein, L. and von Boehmer, H. 2002. Origin of regulatory T cells with known specificity for antigen. Nat. Immunol. 3:756.
34. Watanabe, N., Wang, Y. H., Lee, H. K., Ito, T., Cao, W. and Liu, Y. J. 2005. Hassall's corpuscles instruct dendritic cells to induce CD4+CD25+ regulatory Tcells in human thymus. Nature 436:1181.
35. Michie, S. A., Kirkpatrick, E. A. and Rouse, R. V. 1988. Rare peripheral T cells migrate to and persist in normal mouse thymus. J. Exp. Med. 168:1929.
36. Wei, S., Kryczek, I. and Zou, W. 2006. Regulatory T-cell compartmentalization and trafficking. Blood 108:426.
37. Bell, E. B., Sparshott, S. M. and Ager, A. 1995. Migration pathways of CD4 T cell subsets in vivo: The CD45RC- subset enters the thymus via alpha 4 integrin-VCAM-1 interaction. Int. Immunol. 7:1861.
38. McCarthy, S. A., Kruisbeek, A. M., Uppenkamp, I. K., Sharrow, S. O. and Singer, A. 1988. Engagement of the CD4 molecule influences cell surface expression of the T-cell receptor on thymocytes. Nature 336:76.
39. Jordan, M. S., Boesteanu, A., Reed, A. J. et al. 2001. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat. Immunol. 2:301.
40. Lohr, J., Knoechel, B., Kahn, E. C. and Abbas, A. K. 2004. Role of B7 in T cell tolerance. J. Immunol. 173:5028.
41. Sansom, D. M. and Walker, L. S. 2006. The role of CD28 and cytotoxic T-lymphocyte antigen-4 (CTLA-4) in regulatory T-cell biology. Immunol. Rev. 212:131.
42. Foy, T. M., Page, D. M., Waldschmidt, T. J. et al. 1995. An essential role for gp39, the ligand for CD40, in thymic selection. J. Exp. Med. 182:1377.
43. Li, R. and Page, D. M. 2001. Requirement for a complex array of costimulators in the negative selection of autoreactive thymocytes in vivo. J. Immunol. 166:6050.
44. Linsley, P. S., Greene, J. L., Brady, W., Bajorath, J., Ledbetter, J. A. and Peach, R. 1994. Human B7-1 (CD80) and B7-2 (CD86) bind with similar avidities but distinct kinetics to CD28 and CTLA-4 receptors. Immunity 1:793.
45. Pentcheva-Hoang, T., Egen, J. G., Wojnoonski, K. and Allison, J. P. 2004. B7-1 and B7-2 selectively recruit CTLA-4 and CD28 to the immunological synapse. Immunity 21:401.
46. Montagnoli, C., Bacci, A., Bozza, S. et al. 2002. B7/CD28-dependent CD4+CD25+ regulatory T cells are essential components of the memory-protective immunity to Candida albicans. J. Immunol. 169:6298.
47. Chen, W., Jin, W., Hardegen, N. et al. 2003. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198:1875.
48. Kretschmer, K., Apostolou, I., Hawiger, D., Khazaie, K., Nussenzweig, M. C. and von Boehmer, H. 2005. Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 6:1219.
49. Fehr, T., Takeuchi, Y., Kurtz, J., Wekerle, T. and Sykes, M. 2005. Early regulation of CD8 T cell alloreactivity by CD4+CD25- T cells in recipients of anti-CD154 antibody and allogeneic BMT is followed by rapid peripheral deletion of donor-reactive CD8+ T cells, precluding a role for sustained regulation. Eur. J. Immunol. 35:2679.