Diversification and senescence of Foxp3+ regulatory T cells during experimental autoimmune encephalomyelitis

European Journal of Immunology

Volumn 43, Issue 5, 2013, Pages 1195-1207

  Tauro, Sharyn ^a   Nguyen, Phuong ^a   Li, Bofeng ^a   Geiger, Terrence L ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Autoimmunity; EAE; Foxp3; KLRG1; Regulatory T (Treg) cell; T cell senescence

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR; NATURAL KILLER CELL LECTIN LIKE RECEPTOR G2; PROTEIN BCL 2; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CELL AGING; CELL DEATH; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; FLOW CYTOMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SPLEEN; SPLEEN CELL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; THYMOCYTE;

ADOPTIVE TRANSFER; ANIMALS; APOPTOSIS; AUTOIMMUNITY; CELL AGING; CELL DIFFERENTIATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; IMMUNOPHENOTYPING; INTERLEUKIN-10; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MICE; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTES, REGULATORY; UP-REGULATION;

EID: 84876864132     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242881     Document Type: Article

References (48)

1. Geiger, T. L. and Tauro, S., Nature and nurture in Foxp3(+) regulatory T cell development, stability, and function. Hum. Immunol. 2012. 73: 232-239.
2. Josefowicz, S. Z., Lu, L. F. and Rudensky, A. Y., Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 2012. 30: 531-564.
3. Miyara, M., Gorochov, G., Ehrenstein, M., Musset, L., Sakaguchi, S. and Amoura, Z., Human FoxP3+ regulatory T cells in systemic autoimmune diseases. Autoimmun. Rev. 2011. 10: 744-755.
4. O'connor, R. A., Malpass, K. H. and Anderton, S. M., The inflamed central nervous system drives the activation and rapid proliferation of foxp3+ regulatory T cells. J. Immunol. 2007. 179: 958-966.
5. Liu, X., Alli, R., Steeves, M., Nguyen, P., Vogel, P. and Geiger, T. L., The T cell response to IL-10 alters cellular dynamics and paradoxically promotes central nervous system autoimmunity. J. Immunol. 2012. 189: 669-678.
6. Selvaraj, R. K. and Geiger, T. L., Mitigation of experimental allergic encephalomyelitis by TGF-{beta} induced Foxp3 +regulatory T lymphocytes through the induction of anergy and infectious tolerance. J. Immunol. 2008. 180: 2830-2838.
7. Mekala, D. J., Alli, R. S. and Geiger, T. L., IL-10-dependent infectious tolerance after the treatment of experimental allergic encephalomyelitis with redirected CD4+CD25+ T lymphocytes. Proc. Natl. Acad. Sci. USA 2005. 102: 11817-11822.
8. Zhang, X., Koldzic, D. N., Izikson, L., Reddy, J., Nazareno, R. F., Sakaguchi, S., Kuchroo, V. K. et al., IL-10 is involved in the suppression of experimental autoimmune encephalomyelitis by CD25(+)CD4(+) regulatory T cells. Int. Immunol. 2004. 16: 249-256.
9. Kohm, A. P., Carpentier, P. A., Anger, H. A. and Miller, S. D., Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J. Immunol. 2002. 169: 4712-4716.
10. Li, Y., Hofmann, M., Wang, Q., Teng, L., Chlewicki, L. K., Pircher, H. and Mariuzza, R. A., Structure of natural killer cell receptor KLRG1 bound to E-cadherin reveals basis for MHC-independent missing self recognition. Immunity 2009. 31: 35-46.
11. Reiley, W. W., Shafiani, S., Wittmer, S. T., Tucker-Heard, G., Moon, J. J., Jenkins, M. K., Urdahl, K. B. et al., Distinct functions of antigen-specific CD4 T cells during murine Mycobacterium tuberculosis infection. Proc. Natl. Acad. Sci. USA 2010. 107: 19408-19413.
12. Sarkar, S., Kalia, V., Haining, W. N., Konieczny, B. T., Subramaniam, S. and Ahmed, R., Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J. Exp. Med. 2008. 205: 625-640.
13. Voehringer, D., Blaser, C., Brawand, P., Raulet, D. H., Hanke, T. and Pircher, H., Viral infections induce abundant numbers of senescent CD8 T cells. J. Immunol. 2001. 167: 4838-4843.
14. Wiesel, M., Crouse, J., Bedenikovic, G., Sutherland, A., Joller, N. and Oxenius, A., Type-I IFN drives the differentiation of short-lived effector CD8+ T cells in vivo. Eur. J. Immunol. 2012. 42: 320-329.
15. Jung, Y. W., Rutishauser, R. L., Joshi, N. S., Haberman, A. M. and Kaech, S. M., Differential localization of effector and memory CD8 T cell subsets in lymphoid organs during acute viral infection. J. Immunol. 2010. 185: 5315-5325.
16. Grundemann, C., Schwartzkopff, S., Koschella, M., Schweier, O., Peters, C., Voehringer, D. and Pircher, H., The NK receptor KLRG1 is dispensable for virus-induced NK and CD8+ T-cell differentiation and function in vivo. Eur. J. Immunol. 2010. 40: 1303-1314.
17. Prlic, M., Sacks, J. A. and Bevan, M. J., Dissociating markers of senescence and protective ability in memory T cells. PLoS. One. 2012. 7: e32576.
18. Beyersdorf, N., Ding, X., Tietze, J. K. and Hanke, T., Characterization of mouse CD4 T cell subsets defined by expression of KLRG1. Eur. J. Immunol. 2007. 37: 3445-3454.
19. Stephens, G. L., Andersson, J. and Shevach, E. M., Distinct subsets of FoxP3+ regulatory T cells participate in the control of immune responses. J. Immunol. 2007. 178: 6901-6911.
20. Rosenblum, M. D., Gratz, I. K., Paw, J. S., Lee, K., Marshak-Rothstein, A. and Abbas, A. K., Response to self antigen imprints regulatory memory in tissues. Nature 2011. 480: 538-542.
21. Layland, L. E., Mages, J., Loddenkemper, C., Hoerauf, A., Wagner, H., Lang, R. and da Costa, C. U., Pronounced phenotype in activated regulatory T cells during a chronic helminth infection. J. Immunol. 2010. 184: 713-724.
22. Feuerer, M., Hill, J. A., Kretschmer, K., von, B. H., Mathis, D. and Benoist, C., Genomic definition of multiple ex vivo regulatory T cell subphenotypes. Proc. Natl. Acad. Sci. USA 2010. 107: 5919-5924.
23. Chauhan, S. K., Saban, D. R., Lee, H. K. and Dana, R., Levels of Foxp3 in regulatory T cells reflect their functional status in transplantation. J. Immunol. 2009. 182: 148-153.
24. Kuczma, M., Pawlikowska, I., Kopij, M., Podolsky, R., Rempala, G. A. and Kraj, P., TCR repertoire and Foxp3 expression define functionally distinct subsets of CD4+ regulatory T cells. J. Immunol. 2009. 183: 3118-3129.
25. Coleman, M. M., Finlay, C. M., Moran, B., Keane, J., Dunne, P. J. and Mills, K. H., The immunoregulatory role of CD4(+) FoxP3(+) CD25(-) regulatory T cells in lungs of mice infected with Bordetella pertussis. FEMS Immunol. Med. Microbiol. 2012. 64: 413-424.
26. Nishioka, T., Shimizu, J., Iida, R., Yamazaki, S. and Sakaguchi, S., CD4+CD25+Foxp3+ T cells and CD4+CD25-Foxp3 +T cells in aged mice. J. Immunol. 2006. 176: 6586-6593.
27. Bonelli, M., Savitskaya, A., Steiner, C. W., Rath, E., Smolen, J. S. and Scheinecker, C., Phenotypic and functional analysis of CD4+. J. Immunol. 2009. 182: 1689-1695.
28. Huan, J., Culbertson, N., Spencer, L., Bartholomew, R., Burrows, G. G., Chou, Y. K., Bourdette, D. et al., Decreased FOXP3 levels in multiple sclerosis patients. J. Neurosci. Res. 2005. 81: 45-52.
29. Zabransky, D. J., Nirschl, C. J., Durham, N. M., Park, B. V., Ceccato, C. M., Bruno, T. C., Tam, A. J. et al., Phenotypic and functional properties of Helios+ regulatory T cells. PLoS. One 2012. 7: e34547.
30. Akimova, T., Beier, U. H., Wang, L., Levine, M. H. and Hancock, W. W., Helios expression is a marker of T cell activation and proliferation. PLoS. One 2011. 6: e24226.
31. Nguyen, P., Liu, W., Ma, J., Manirarora, J. N., Liu, X., Cheng, C. and Geiger, T. L., Discrete TCR repertoires and CDR3 features distinguish effector and Foxp3+ regulatory T lymphocytes in myelin oligodendrocyte glycoprotein-induced experimental allergic encephalomyelitis. J. Immunol. 2010. 185: 3895-3904.
32. Liu, X., Nguyen, P., Liu, W., Cheng, C., Steeves, M., Obenauer, J. C., Ma, J. et al., T cell receptor CDR3 sequence but not recognition characteristics distinguish autoreactive effector and Foxp3(+) regulatory T cells. Immunity 2009. 31: 909-920.
33. Selvaraj, R. K. and Geiger, T. L., A kinetic and dynamic analysis of Foxp3 induced in T cells by TGF-beta. J. Immunol. 2007. 178: 7667-7677.
34. Floess, S., Freyer, J., Siewert, C., Baron, U., Olek, S., Polansky, J., Schlawe, K. et al., Epigenetic control of the foxp3 locus in regulatory T cells. PLoS. Biol. 2007. 5: e38.
35. Mann, M. K., Maresz, K., Shriver, L. P., Tan, Y. and Dittel, B. N., B cell regulation of CD4+CD25+ T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J. Immunol. 2007. 178: 3447-3456.
36. Ferber, I. A., Brocke, S., Taylor-Edwards, C., Ridgway, W., Dinisco, C., Steinman, L., Dalton, D. et al., Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 1996. 156: 5-7.
37. Chu, C. Q., Wittmer, S. and Dalton, D. K., Failure to suppress the expansion of the activated CD4 T cell population in interferon gamma-deficient mice leads to exacerbation of experimental autoimmune encephalomyelitis. J. Exp. Med. 2000. 192: 123-128.
38. McGeachy, M. J., Stephens, L. A. and Anderton, S. M., Natural recovery and protection from autoimmune encephalomyelitis: contribution of CD4+CD25+ regulatory cells within the central nervous system. J. Immunol. 2005. 175: 3025-3032.
39. Gupta, S., Thornley, T. B., Gao, W., Larocca, R., Turka, L. A., Kuchroo, V. K. and Strom, T. B., Allograft rejection is restrained by short-lived TIM-3+PD-1+Foxp3+ Tregs. J. Clin. Invest 2012. 122: 2395-2404.
40. Huang, C. T., Workman, C. J., Flies, D., Pan, X., Marson, A. L., Zhou, G., Hipkiss, E. L. et al., Role of LAG-3 in regulatory T cells. Immunity 2004. 21: 503-513.
41. Chang, L. Y., Lin, Y. C., Kang, C. W., Hsu, C. Y., Chu, Y. Y., Huang, C. T., Day, Y. J. et al., The indispensable role of CCR5 for in vivo suppressor function of tumor-derived CD103 +effector/memory regulatory T cells. J. Immunol. 2012. 189: 567-574.
42. O'connor, R. A. and Anderton, S. M., Foxp3+ regulatory T cells in the control of experimental CNS autoimmune disease. J. Neuroimmunol. 2008. 193: 1-11.
43. Apostolou, I. and von, B. H., In vivo instruction of suppressor commitment in naive T cells. J. Exp. Med. 2004. 199: 1401-1408.
44. Weiner, H. L., da Cunha, A. P., Quintana, F. and Wu, H., Oral tolerance. Immunol. Rev. 2011. 241: 241-259.
45. Joshi, N. S., Cui, W., Chandele, A., Lee, H. K., Urso, D. R., Hagman, J., Gapin, L. and Kaech, S. M., Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 2007. 27: 281-295.
46. Cheng, G., Yuan, X., Tsai, M. S., Podack, E. R., Yu, A. and Malek, T. R., IL-2 receptor signaling is essential for the development of Klrg1+ terminally differentiated T regulatory cells. J. Immunol. 2012. 189: 1780-1791.
47. Ferber, I. A., Brocke, S., Taylor-Edwards, C., Ridgway, W., Dinisco, C., Steinman, L., Dalton, D. et al., Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 1996. 156: 5-7.
48. Komiyama, Y., Nakae, S., Matsuki, T., Nambu, A., Ishigame, H., Kakuta, S., Sudo, K. et al., IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2006. 177: 566-573.