Autoimmunity during thymectomy-induced lymphopenia: Role of thymus ablation and initial effector T cell activation timing in nonobese diabetic mice

Journal of Immunology

Volumn 183, Issue 8, 2009, Pages 4913-4920

  Gagnerault, Marie Claude ^a   Lanvin, Olivia ^b   Pasquier, Virginie ^b   Garcia, Corinne ^c   Damotte, Diane ^d   Lucas, Bruno ^c,e   Lepault, Françoise ^c,e  

^a INSERM   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^e Cochin Hospital ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CONTROLLED STUDY; DIABETES MELLITUS; EFFECTOR CELL; FEMALE; GASTRITIS; INCIDENCE; LYMPHOCYTE COUNT; LYMPHOCYTOPENIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THYMECTOMY;

ADOPTIVE TRANSFER; ANIMALS; AUTOIMMUNITY; B-LYMPHOCYTE SUBSETS; DIABETES MELLITUS, TYPE 1; FEMALE; GASTRITIS; LYMPHOPENIA; MALE; MICE; MICE, INBRED NOD; T-LYMPHOCYTES, REGULATORY; THYMECTOMY; THYMUS GLAND;

EID: 77954104659     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901954     Document Type: Article

References (52)

1. Baccala, R., and A. N. Theofilopoulos. 2005. The new paradigm of T-cell homeostatic proliferation-induced autoimmunity. Trends Immunol. 26: 5-8.
2. Krupica, T., Jr., T. J. Fry, and C. L. Mackall. 2006. Autoimmunity during lymphopenia: a two-hit model. Clin. Immunol. 120: 121-128.
3. Kojima, A., and R. T. Prehn. 1981. Genetic susceptibility to post-thymectomy autoimmune diseases in mice. Immunogenetics 14: 15-27. (Pubitemid 12246051)
4. 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)
5. 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.
6. 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.
7. + T cells. Proc. Natl. Acad. Sci. USA 100: 6021-6026.
8. 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.
9. + T-cell pool in a nonlymphopenic environment. Blood 108: 270-277.
10. Surh, C. D., and J. Sprent. 2008. Homeostasis of naive and memory T cells. Immunity 29: 848-862.
11. + T cells. Proc. Natl. Acad. Sci. USA 101: 14473-14478.
12. Jackson, R., N. Rassi, T. Crump, B. Haynes, and G. S. Eisenbarth. 1981. The BB diabetic rat: profound T-cell lymphocytopenia. Diabetes 30: 887-889. (Pubitemid 11020067)
13. King, C., A. Ilic, K. Koelsch, and N. Sarvetnick. 2004. Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell 117: 265-277.
14. Berzins, S. P., E. S. Venanzi, C. Benoist, and D. Mathis. 2003. T-cell compartments of prediabetic NOD mice. Diabetes 52: 327-334.
15. Dardenne, M., F. Lepault, A. Bendelac, and J. F. Bach. 1989. Acceleration of the onset of diabetes in NOD mice by thymectomy at weaning. Eur. J. Immunol. 19: 889-895.
16. Bourgeois, C., Z. Hao, K. Rajewsky, A. J. Potocnik, and B. Stockinger. 2008. Ablation of thymic export causes accelerated decay of naive CD4 T cells in the periphery because of activation by environmental antigen. Proc. Natl. Acad. Sci. USA 105: 8691-8696.
17. + T lymphocytes induces diabetes in resistant biobreeding/Worcester (BB/W) rats. J. Exp. Med. 166: 461-475.
18. Gregori, S., N. Giarratana, S. Smiroldo, and L. Adorini. 2003. Dynamics of pathogenic and suppressor T cells in autoimmune diabetes development. J. Immunol. 171: 4040-4047.
19. + regulatory T-cells contributes to the onset of autoimmune diabetes. Diabetes 57: 113-123.
20. + regulatory T cells. Immunology 121: 15-28.
21. D'Alise, A. M., V. Auyeung, M. Feuerer, J. Nishio, J. Fontenot, C. Benoist, and D. Mathis. 2008. The defect in T-cell regulation in NOD mice is an effect on the T-cell effectors. Proc. Natl. Acad. Sci. USA 105: 19857-19862.
22. Lepault, F., M. C. Gagnerault, C. Faveeuw, H. Bazin, and C. Boitard. 1995. Lack of L-selectin expression by cells transferring diabetes in NOD mice: insights into the mechanisms involved in diabetes prevention by Mel-14 antibody treatment. Eur. J. Immunol. 25: 1502-1507.
23. East, J., M. A. De Sousa, D. M. Parrott, and H. Jaquet. 1967. Consequences of neonatal thymectomy in New Zealand Black mice. Clin. Exp. Immunol. 2: 203-215.
24. + regulatory T cells. J. Exp. Med. 199: 303-313.
25. Billiard, F., E. Litvinova, D. Saadoun, F. Djelti, D. Klatzmann, J. L. Cohen, G. Marodon, and B. L. Salomon. 2006. Regulatory and effector T cell activation levels are prime determinants of in vivo immune regulation. J. Immunol. 177: 2167-2174.
26. + regulatory T cells controls wasting disease, IL-10 secretion and T cell homeostasis. Eur. J. Immunol. 33: 2419-2428.
27. + regulatory T cells originate from both naive T cells and naturally occurring naive-like regulatory T cells. J. Immunol. 180: 146-155.
28. Tang, Q., and J. A. Bluestone. 2006. Regulatory T-cell physiology and application to treat autoimmunity. Immunol. Rev. 212: 217-237.
29. Le Campion, A., M. C. Gagnerault, C. Auffray, C. Becourt, M. Poitrasson-Riviere, E. Lallemand, B. Bienvenu, B. Martin, F. Lepault, and B. Lucas. 2009. Lymphopenia- induced spontaneous T-cell proliferation as a cofactor for autoimmune disease development. Blood DOI 10.1182.
30. + T cells in lymphopenic hosts. Immunity 11: 183-190.
31. 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.
32. Kieper, W. C., A. Troy, J. T. Burghardt, C. Ramsey, J. Y. Lee, H. Q. Jiang, W. Dummer, H. Shen, J. J. Cebra, and C. D. Surh. 2005. Recent immune status determines the source of antigens that drive homeostatic T cell expansion. J. Immunol. 174: 3158-3163.
33. 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)
34. 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.
35. Mackall, C. L., C. V. Bare, L. A. Granger, S. O. Sharrow, J. A. Titus, and R. E. Gress. 1996. Thymic-independent T cell regeneration occurs via antigendriven expansion of peripheral T cells resulting in a repertoire that is limited in diversity and prone to skewing. J. Immunol. 156: 4609-4616.
36. 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)
37. Garza, K. M., S. S. Agersborg, E. Baker, and K. S. Tung. 2000. Persistence of physiological self antigen is required for the regulation of self tolerance. J. Immunol. 164: 3982-3989.
38. Tung, K. S., S. Smith, C. Teuscher, C. Cook, and R. E. Anderson. 1987. Murine autoimmune oophoritis, epididymoorchitis, and gastritis induced by day 3 thymectomy. Immunopathology. Am. J. Pathol. 126: 293-302. (Pubitemid 17033854)
39. Hoglund, P., J. Mintern, C. Waltzinger, W. Heath, C. Benoist, and D. Mathis. 1999. Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes. J. Exp. Med. 189: 331-339.
40. Gagnerault, M. C., J. J. Luan, C. Lotton, and F. Lepault. 2002. Pancreatic lymph nodes are required for priming of β cell reactive T cells in NOD mice. J. Exp. Med. 196: 369-377.
41. + Treg cells impinge on autoimmune diabetes. J. Exp. Med. 202: 1387-1397.
42. Tang, Q., J. Y. Adams, A. J. Tooley, M. Bi, B. T. Fife, P. Serra, P. Santamaria, R. M. Locksley, M. F. Krummel, and J. A. Bluestone. 2006. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat. Immunol. 7: 83-92.
43. + regulatory T cell: a jack of all trades, master of regulation. Nat. Immunol. 9: 239-244.
44. Monteiro, J. P., J. Farache, A. C. Mercadante, J. A. Mignaco, M. Bonamino, and A. Bonomo. 2008. Pathogenic effector T cell enrichment overcomes regulatory T cell control and generates autoimmune gastritis. J. Immunol. 181: 5895-5903.
45. Turley, S., L. Poirot, M. Hattori, C. Benoist, and D. Mathis. 2003. Physiological β cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model. J. Exp. Med. 198: 1527-1537.
46. Trudeau, J. D., J. P. Dutz, E. Arany, D. J. Hill, W. E. Fieldus, and D. T. Finegood. 2000. Neonatal β-cell apoptosis: a trigger for autoimmune diabetes? Diabetes 49: 1-7.
47. Kurrer, M. O., S. V. Pakala, H. L. Hanson, and J. D. Katz. 1997. Beta cell apoptosis in T cell-mediated autoimmune diabetes. Proc. Natl. Acad. Sci. USA 94: 213-218.
48. Mintern, J. D., R. M. Sutherland, A. M. Lew, K. Shortman, F. R. Carbone, and W. R. Heath. 2002. Constitutive, but not inflammatory, cross-presentation is disabled in the pancreas of young mice. Eur. J. Immunol. 32: 1044-1051.
49. + regulatory T cells. J. Immunol. 181: 7350-7355.
50. Clough, L. E., C. J. Wang, E. M. Schmidt, G. Booth, T. Z. Hou, G. A. Ryan, and L. S. Walker. 2008. Release from regulatory T cell-mediated suppression during the onset of tissue-specific autoimmunity is associated with elevated IL-21. J. Immunol. 180: 5393-5401.
51. Spolski, R., M. Kashyap, C. Robinson, Z. Yu, and W. J. Leonard. 2008. IL-21 signaling is critical for the development of type I diabetes in the NOD mouse. Proc. Natl. Acad. Sci. USA 105: 14028-14033.
52. Andre, I., A. Gonzalez, B. Wang, J. Katz, C. Benoist, and D. Mathis. 1996. Checkpoints in the progression of autoimmune disease: lessons from diabetes models. Proc. Natl. Acad. Sci. USA 93: 2260-2263.