ICER/CREM-mediated transcriptional attenuation of IL-2 and its role in suppression by regulatory T cells

European Journal of Immunology

Volumn 37, Issue 4, 2007, Pages 884-895

  Bodor, Josef ^a   Fehervari, Zoltan ^b   Diamond, Betty ^a   Sakaguchi, Shimon ^b  

^a College of Physicians and Surgeons ^*  (United States)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

CD+CD25+ T cells; Cytotoxic T lymphocyte associated antigen 4; GITR; ICER CREM; IL 2

Indexed keywords

B7 ANTIGEN; CYCLIC AMP RESPONSIVE ELEMENT MODULATOR; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INDUCIBLE CYCLIC AMP EARLY REPRESSOR; INTERLEUKIN 2; PROTEIN; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; CREM PROTEIN, MOUSE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; INTERLEUKIN 2 RECEPTOR ALPHA; REPRESSOR PROTEIN;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; LYMPHOCYTE COUNT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY T LYMPHOCYTE; RNA INTERFERENCE; TRANSCRIPTION REGULATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; DOWN REGULATION; DRUG ANTAGONISM; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT MODULATOR; DOWN-REGULATION; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOSUPPRESSION; INTERLEUKIN-2; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; REPRESSOR PROTEINS; T-LYMPHOCYTES, REGULATORY; TRANSCRIPTION, GENETIC;

EID: 34249701932     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200636510     Document Type: Article

References (53)

1. Hori, S., Nomura, T. and Sakaguchi, S., Control of regulatory T cell development by the transcription factor Foxp3. Science 2003. 299: 1057-1061.
2. Williams, L. M. and Rudensky, A. Y., Maintenance of the Foxp3-dependent developmental program in mature regulatory T cells requires continued expression of Foxp3. Nat. Immunol. 2007. 8: 277-284.
3. Wan, Y. Y. and Flavell, R. A., Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature 2007. 445: 766-770.
4. Schubert, L. A., Jeffery, E., Zhang, Y., Ramsdell, F. and Ziegler, S. F., Scurfin (FOXP3) acts as a repressor of transcription and regulates T cell activation. J. Biol. Chem. 2001. 276: 37672-37679.
5. Bodor, J., Fehervari, Z., Diamond, B. and Sakaguchi, S., Regulatory T cell-mediated suppression: potential role of ICER. J. Leukoc. Biol. 2007. 81: 161-167.
6. + T lymphocytes. J. Immunol. 2002. 169: 6231-6235.
7. Schneider, H., Downey, J., Smith, A., Zinselmeyer, B. H., Rush, C., Brewer, J. M., Wei, B. et al., Reversal of the TCR stop signal by CTLA-4. Science 2006. 313: 1972-1975.
8. Gonzalez-Rey, E., Chorny, A. and Delgado, M., Regulation of immune tolerance by anti-inflammatory neuropeptides. Nat. Rev. Immunol. 2007. 7: 52-63.
9. + regulatory T cells in vivo. J. Immunol. 2006. 177: 209-215.
10. + natural regulatory T cells revealed by DNA microarray analysis. Int. Immunol. 2006. 18: 1197-1209.
11. + T cells. J. Immunol. 2005. 175: 1483-1490.
12. + adaptive regulatory T cells express cyclooxygenase-2 and suppress effector T cells by a prostaglandin E2-dependent mechanism. J. Immunol. 2006. 177: 246-254.
13. Bodor, J., Spetz, A. L., Strominger, J. L. and Habener, J. F., cAMP inducibility of transcriptional repressor ICER in developing and mature human T lymphocytes. Proc. Natl. Acad. Sci. USA 1996. 93: 3536-3541.
14. Bodor, J. and Habener, J. F., Role of transcriptional repressor ICER in cyclic AMP-mediated attenutation of cytokine gene expression in human thymocytes. J. Biol. Chem. 1998. 273: 9544-9551.
15. Bodor, J., Bodorova, J., Bare, C., Hodge, D. L., Young, H. A. and Gress, R. E., Differential inducibility of the transcriptional repressor ICER and its role in modulation of Fas ligand expression in T and NK lymphocytes. Eur. J. Immunol. 2002. 32: 203-212.
16. Bodor, J., Feigenbaum, L., Bodorova, J., Bare, C., Reitz, M. S., Jr. and Gress, R. E., Suppression of T-cell responsiveness by inducible cAMP early repressor (ICER). J. Leukoc. Biol. 2001. 69: 1053-1059.
17. Barton, K., Muthusamy, N., Chanyangam, M., Fischer, C., Clendenin, C. and Leiden, J. M., Defective thymocyte proliferation and IL-2 production in transgenic mice expressing a dominant-negative form of CREB. Nature 1996. 379: 81-85.
18. Molina, C. A., Foulkes, N. S., Lalli, E. and Sassone-Corsi, P., Inducibility and negative autoregulation of CREM: an alternative promoter directs the expression of ICER, an early response repressor. Cell 1993. 75: 875-886.
19. Powell, J. D., Lerner, C. G., Ewoldt, G. R. and Schwartz, R. H., The -180 site of the IL-2 promoter is the target of CREB/CREM binding in T cell anergy. J. Immunol. 1999. 163: 6631-6639.
20. Tenbrock, K., Juang, Y. T., Gourley, M. F., Nambiar, M. P. and Tsokos, G. C., Antisense cyclic adenosine 5′-monophosphate response element modulator up-regulates IL-2 in T cells from patients with systemic lupus erythematosus. J. Immunol. 2002. 169: 4147-4152.
21. Gavin, M. A., Clarke, S. R., Negrou, E., Gallegos, A. and Rudensky, A., Homeostasis and anergy of CD4(+)CD25(+) suppressor T cells in vivo. Nat. Immunol. 2002. 3: 33-41.
22. Greenwald, R. J., Freeman, G. J. and Sharpe, A. H., The B7 family revisited. Annu. Rev. Immunol. 2005. 23: 515-548.
23. Fallarino, F., Grohmann, U., Hwang, K. W., Orabona, C., Vacca, C., Bianchi, R., Belladonna, M. L. et al., Modulation of tryptophan catabolism by regulatory T cells. Nat. Immunol. 2003. 4: 1206-1212.
24. + regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 2004. 22: 531-562.
25. Taylor, P. A., Lees, C. J., Fournier, S., Allison, J. P., Sharpe, A. H. and Blazar, B. R., B7 expression on T cells down-regulates immune responses through CTLA-4 ligation via T-T interactions. J. Immunol. 2004. 172: 34-39.
26. Paust, S., Lu, L., McCarty, N. and Cantor, H., Engagement of B7 on effector T cells by regulatory T cells prevents autoimmune disease. Proc. Natl. Acad. Sci. USA 2004. 101: 10398-10403.
27. Tarbell, K. V., Yamazaki, S. and Steinman, R. M., The interactions of dendritic cells with antigen-specific, regulatory T cells that suppress autoimmunity. Semin. Immunol. 2006. 18: 93-102.
28. Paust, S. and Cantor, H., Regulatory T cells and autoimmune disease. Immunol. Rev. 2005. 204: 195-207.
29. Peggs, K. S., Quezada, S. A., Korman, A. J. and Allison, J. P., Principles and use of anti-CTLA4 antibody in human cancer immunotherapy. Curr. Opin. Immunol. 2006. 18: 206-213.
30. + T cell suppressor function. J. Immunol. 2004. 172: 6519-6523.
31. + regulatory T cell activity. J. Immunol. 2005. 175: 7274-7280.
32. Macian, F., NFAT proteins: key regulators of T-cell development and function. Nat. Rev. Immunol. 2005. 5: 472-484.
33. Takahashi, T., Tagami, T., Yamazaki, S., Uede, T., Shimizu, J., Sakaguchi, N., Mak, T. W. and Sakaguchi, S., Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J. Exp. Med. 2000. 192: 303-310.
34. + T cells. J. Immunol. 2004. 173: 5008-5020.
35. + regulatory cell activation and function by dendritic cells. Int. Immunol. 2004. 16: 1769-1780.
36. + regulatory T cells by antigen-processing dendritic cells. J. Exp. Med. 2003. 198: 235-247.
37. Zheng, Y., Manzotti, C. N., Liu, M., Burke, F., Mead, K. I. and Sansom, D. M., CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells. J. Immunol. 2004. 172: 2778-2784.
38. Sansom, D. M. and Walker, L. S., The role of CD28 and cytotoxic T-lymphocyte antigen-4 (CTLA-4) in regulatory T-cell biology. Immunol. Rev. 2006. 212: 131-148.
39. + T cells in rats. Int. Immunol. 2004. 16: 365-375.
40. Serfling, E., Chuvpilo, S., Liu, J., Hofer, T. and Palmetshofer, A., NFATc1 autoregulation: a crucial step for cell-fate determination. Trends Immunol. 2006. 27: 461-469.
41. Wu, Y., Borde, M., Heissmeyer, V., Feuerer, M., Lapan, A. D., Stroud, J. C., Bates, D. L. et al., FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 2006. 126: 375-387.
42. Setoguchi, R., Hori, S., Takahashi, T. and Sakaguchi, S., Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J. Exp. Med. 2005. 201: 723-735.
43. Fehervari, Z., Yamaguchi, T. and Sakaguchi, S., The dichotomous role of IL-2: tolerance versus immunity. Trends Immunol. 2006. 27: 109-111.
44. Antony, P. A., Paulos, C. M., Abmadzadeh, M., Akpinarli, A., Palmer, D. C., Sato, N., Kaiser, A. et al., Interleukin-2-dependent mechanisms of tolerance and immunity in vivo. J. Immunol. 2006. 176: 5255-5266.
45. Schneider, H., Mandelbrot, D. A., Greenwald, R. J., Ng, F., Lechler, R., Sharpe, A. H. and Rudd, C. E., Cutting edge: CTLA-4 (CD152) differentially regulates mitogen-activated protein kinases (extracellular signal-regulated kinase and c-Jun N-terminal kinase) in CD4+ T cells from receptor/ligand-deficient mice. J. Immunol. 2002. 169: 3475-3479.
46. Yehia, G., Schlotter, F., Razavi, R., Alessandrini, A. and Molina, C. A., Mitogen-activated protein kinase phosphorylates and targets inducible cAMP early repressor to ubiquitin-mediated destruction. J. Biol. Chem. 2001. 276: 35272-35279.
47. Nimmerjahn, F. and Ravetch, J. V., Fcgamma receptors: old friends and new family members. Immunity 2006. 24: 19-28.
48. Cohen, A. D., Diab, A., Perales, M. A., Wolchok, J. D., Rizzuto, G., Merghoub, T., Huggins, D. et al., Agonist anti-GITR antibody enhances vaccine-induced CD8 (+) T-cell responses and tumor immunity. Cancer Res. 2006. 66: 4904-4912.
49. D'Adamio, F., Zollo, O., Moraca, R., Ayroldi, E., Bruscoli, S., Bartoli, A., Cannarile, L. et al., A new dexamethasone-induced gene of the leucine zipper family protects T lymphocytes from TCR/CD3-activated cell death. Immunity 1997. 7: 803-812.
50. Riccardi, C., Cifone, M. G. and Mighorati, G., Glucocorticoid hormone-induced modulation of gene expression and regulation of T-cell death: role of GITR and GILZ, two dexamethasone-induced genes. Cell Death Differ. 1999. 6: 1182-1189.
51. Delfino, D. V., Agostini, M., Spinicelli, S., Vacca, C. and Riccardi, C., Inhibited cell death, NF-kappaB activity and increased IL-10 in TCR-triggered thymocytes of transgenic mice overexpressing the glucocorticoid-induced protein GILZ. Int. Immunopharmacol. 2006. 6: 1126-1134.
52. Berrebi, D., Bruscoli, S., Cohen, N., Foussat, A., Migliorati, G., Bouchet-Delbos, L., Maillot, M. C. et al., Synthesis of glucocorticoid-incluced leucine zipper (GILZ) by macrophages: an anti-inflammatory and immunosuppressive mechanism shared by glucocorticoids and IL-10. Blood 2003. 101: 729-738.
53. Morita, S., Kojima, T. and Kitamura, T., Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 2000. 7: 1063-1066.