Loss of T regulatory cell suppression following signaling through glucocorticoid-induced tumor necrosis receptor (GITR) is dependent on c-Jun N-terminal kinase activation

Journal of Biological Chemistry

Volumn 287, Issue 21, 2012, Pages 17100-17108

  Joetham, Anthony ^a   Ohnishi, Hiroshi ^a   Okamoto, Masakazu ^a   Takeda, Katsuyuki ^a   Schedel, Michaela ^a   Domenico, Joanne ^a   Dakhama, Azzeddine ^a   Gelfand, Erwin W ^a  

^a DEPARTMENT OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGIC RESPONSE; AUTOIMMUNE DISEASE; C-JUN N-TERMINAL KINASE; CELL FUNCTIONS; CELL SUPPRESSION; EXTRACELLULAR SIGNAL-REGULATED PROTEIN KINASE; IMMUNOPRECIPITATES; IN-VITRO; IN-VIVO; MITOGEN-ACTIVATED PROTEIN KINASE KINASE; NATURALLY OCCURRING; P38 MAPK; T CELLS; TUMOR NECROSIS; WILD TYPES;

BIOLOGICAL ORGANS; CHEMICAL ACTIVATION; CYTOLOGY; DISEASES; ENZYME ACTIVITY; PHOSPHORYLATION; TRANSCRIPTION FACTORS; TUMORS;

CELLS;

GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTHRACENES; ASTHMA; AUTOIMMUNE DISEASES; CELL PROLIFERATION; ENZYME ACTIVATION; FEMALE; GLUCOCORTICOID-INDUCED TNFR-RELATED PROTEIN; IMMUNE TOLERANCE; LUNG; MAP KINASE KINASE 4; MAP KINASE KINASE 7; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; T-LYMPHOCYTES, REGULATORY;

MUS;

EID: 84861215296     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.316943     Document Type: Article

References (40)

1. Nocentini, G., Giunchi, L., Ronchetti, S., Krausz, L. T., Bartoli, A., Moraca, R., Migliorati, G., and Riccardi, C. (1997) A new member of the tumor necrosis factor/nerve growth factor receptor family inhibits T cell-receptor- induced apoptosis. Proc. Natl. Acad. Sci. U.S.A. 94, 6216-6221 (Pubitemid 27270664)
2. Kwon, B., Yu, K. Y., Ni, J., Yu, G. L., Jang, I. K., Kim, Y. J., Xing, L., Liu, D., Wang, S. X., and Kwon, B. S. (1999) Identification of a novel activation-inducible protein of the tumor necrosis factor receptor superfamily and its ligand. J. Biol. Chem. 274, 6056-6061 (Pubitemid 29111009)
3. Watts, T. H. (2005) TNF/TNFR family members in costimulation of T cell responses. Annu. Rev. Immunol. 23, 23-68
4. Cuzzocrea, S., Nocentini, G., Di Paola, R., Agostini, M., Mazzon, E., Ronchetti, S., Crisafulli, C., Esposito, E., Caputi, A. P., and Riccardi, C. (2006) Proinflammatory role of glucocorticoid-induced TNF receptor-related gene in acute lung inflammation. J. Immunol. 177, 631-641 (Pubitemid 43939177)
5. Motta, A. C., Vissers, J. L., Gras, R., Van Esch, B. C., Van Oosterhout, A. J., and Nawijn, M. C. (2009) GITR signaling potentiates airway hyper-responsiveness by enhancing Th2 cell activity in a mouse model of asthma. Respir. Res. 10, 93
6. + regulatory T cells through GITR breaks immunological self-tolerance. Nat. Immunol. 3, 135-142
7. + immunoregulatory T cells. Gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 16, 311-323
8. Joetham, A., Matsubara, S., Okamoto, M., Takeda, K., Miyahara, N., Dakhama, A., and Gelfand, E. W. (2008) Plasticity of regulatory T cells. Subversion of suppressive function and conversion to enhancement of lung allergic responses. J. Immunol. 180, 7117-7124
9. Ji, H. B., Liao, G., Faubion, W. A., Abadía-Molina, A. C., Cozzo, C., Laroux, F. S., Caton, A., and Terhorst, C. (2004) Cutting Edge. The natural ligand for glucocorticoid-induced TNF receptor-related protein abrogates regulatory T cell suppression. J. Immunol. 172, 5823-5827 (Pubitemid 38621178)
10. Stephens, G. L., McHugh, R. S., Whitters, M. J., Young, D. A., Luxenberg, D., Carreno, B. M., Collins, M., and Shevach, E. M. (2004) Engagement of glucocorticoid-induced TNFR family-related receptor on effector T cells by its ligand mediates resistance to suppression by CD4+CD25+ T cells. J. Immunol. 173, 5008-5020 (Pubitemid 39387783)
11. Cardona, I. D., Goleva, E., Ou, L. S., and Leung, D. Y. (2006) Staphylococcal enterotoxin B inhibits regulatory T cells by inducing glucocorticoid-induced TNF receptor-related protein ligand on monocytes. J. Allergy Clin. Immunol. 117, 688-695 (Pubitemid 43340237)
12. + T-cell regulation of airway allergic responses depends on IL-10 induction of TGF-β. J. Immunol. 178, 1433-1442
13. + regulatory cells on lung allergic responses requires CD8 and MHC I interaction. Proc. Natl. Acad. Sci. 104, 15057-15062
14. Akbari, O., Freeman, G. J., Meyer, E. H., Greenfield, E. A., Chang, T. T., Sharpe, A. H., Berry, G., DeKruyff, R. H., and Umetsu, D. T. (2002) Antigen- specific regulatory T cells develop via the ICOS-ICOSSL pathway and inhibit allergen-induced airway hyper-reactivity. Nat. Med. 8, 1024-1032 (Pubitemid 35033708)
15. Joetham, A., Takeda, K., Okamoto, M., Taube, C., Matsuda, H., Dakhama, A., and Gelfand, E. W. (2009) Antigen specificity is not required for modulation of lung allergic responses by naturally occurring regulatory T cells. J. Immunol. 183, 1821-1827
16. 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, 329-341 (Pubitemid 40387475)
17. Clark, L. B., Appleby, M. W., Brunkow, M. E., Wilkinson, J. E., Ziegler, S. F., and Ramsdell, F. (1999) Cellular and molecular characterization of the scurfy mouse mutant. J. Immunol. 162, 2546-2554 (Pubitemid 29309272)
18. Bennett, C. L., Christie, J., Ramsdell, F., Brunkow, M. E., Ferguson, P. J., Whitesell, L., Kelly, T. E., Saulsbury, F. T., Chance, P. F., and Ochs, H. D. (2001) The immune dysregulation, polyendocrinopathy, enteropathy, and X-linked syndrome are caused by mutations of Foxp3. Nat. Genet. 27, 20-21 (Pubitemid 32044513)
19. Joetham, A., Okamoto, M., Takeda, K., Schedel, M., Ohnishi, H., Dakhama, A., and Gelfand, E. W. (2011) CD8 regulates the endogenous production of IL-6 in naturally occurring T regulatory cells and maintains their suppressive phenotype in allergic lung disease. J. Immunol. 186, 113-120
20. Wan, Y. Y., and Flavell, R. A. (2007) Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature 445, 766-770 (Pubitemid 46279706)
21. Zhou, X., Bailey-Bucktrout, S. L., Jeker, L. T., Penaranda, C., Martínez- Llordella, M., Ashby, M., Nakayama, M., Rosenthal, W., and Bluestone, J. A. (2009) Instability of the transcription factor Foxp3 leads to generation of pathogenic memory T cells in vivo. Nat. Immunol. 10, 1000-1007
22. Esparza, E. M., and Arch, R. H. (2005) Glucocorticoid-induced TNF receptor, a costimulatory receptor on naive and activated T cells, uses TNF receptor-associated factor 2 in a novel fashion as an inhibitor of NF-κB activation. J. Immunol. 174, 7875-7882 (Pubitemid 40806297)
23. + T cells. J. Immunol. 172, 7306-7314
24. + T cells. J. Immunol. 179, 5916-5926
25. Bae, E. M., Kim, W. J., Suk, K., Kang, Y. M., Park, J. E., Kim, W. Y., Choi, E. M., Choi, B. K., Kwon, B. S., and Lee, W. H. (2008) Reverse signaling initiated from GITRL induces NF-κB activation through ERK in the inflammatory activation of macrophages. Mol. Immunol. 45, 523-533 (Pubitemid 47332628)
26. Dong, C., Davis, R. J., and Flavell, R. A. (2002) MAPKs in the immune response. Annu. Rev. Immunol. 20, 55-72
27. Adler, H. S., Kubsch, S., Graulich, E., Ludwig S., Knop, J., and Steinbrink, K. (2007) Activation of MAPkinase p38 is critical for the cell cycle-controlled suppressor function of regulatory T cells. Blood 109, 4351-4359 (Pubitemid 46743403)
28. Luo, X., Zhang, Q., Liu, V., Xia, Z., Pothoven, K. L., and Lee, C. (2008) Cutting Edge. TGF-b-induced expression of Foxp3 in T cells is mediated through inactivation of ERK. J. Immunol. 180, 2757-2761
29. Sato, S., Sanjo, H., Tsujimura, T., Ninomiya-Tsuji, J., Yamamoto, M., Kawai, T., Takeuchi, O., and Akira, S. (2006) TAK1 is indispensable for development of T cells and prevention of colitis by the generation of regulatory T cells. Int. Immunol. 18, 1405-1411 (Pubitemid 44446818)
30. Dérijard, B., Hibi, M., Wu, I. H., Barrett, T., Su, B., Deng, T., Karin, M., and Davis, R. J. (1994) JNK1. A protein kinase stimulated by UV light and Ha-ras that binds and phosphorylates the c-Jun activation domain. Cell 76, 1025-1037 (Pubitemid 24106383)
31. Bennett, B. L., Sasaki, D. T., Murray, B. W., O'Leary, E. C., Sakata, S. T., Xu, W., Leisten, J. C., Motiwala, A., Pierce, S., Satoh, Y., Bhagwat, S. S., Manning, A. M., and Anderson, D. W. (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. U.S.A. 98, 13681-13686 (Pubitemid 33115958)
32. Chialda, L., Zhang, M., Brune, K., and Pahl, A. (2005) Inhibitors of mitogen- activated protein kinases differentially regulate costimulated T cells cytokine production and mouse airway eosinophilia. Respir. Res. 6, 36
33. Tournier, C., Whitmarsh, A. J., Cavanagh, J., Barrett, T., and Davis, R. J. (1997) Mitogen-activated protein kinase kinase 7 is an activator of the c-Jun N-terminal kinase. Proc. Natl. Acad. Sci. U.S.A. 94, 7337-7342 (Pubitemid 27345316)
34. Sánchez, I., Hughes, R. T., Mayer, B. J., Yee, K., Woodgett, J. R., Avruch, J., Kyriakis, J. M., and Zon, L. I. (1994) Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature 372, 794-798
35. Whitmarsh, A. J., and Davis, R. J. (1996) Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J. Mol. Med. 17, 2360-2371
36. + regulatory T cell function. Science 322, 271-275
37. Sakaguchi, S., Yamaguchi, T., Nomura, T., and Ono, M. (2008) Regulatory T cells and immune tolerance. Cell 133, 775-787 (Pubitemid 351707693)
38. Lin, A., Minden, A., Martinetto, H., Claret, F. X., Lange-Carter, C., Mercurio, F., Johnson, G. L., and Karin, M. (1995) Identification of a dual specificity kinase that activates the Jun kinases and p38-Mpk2. Science 268, 286-290
39. Presser, K., Schwinge, D., Wegmann, M., Huber, S., Schmitt, S., Quaas, A., Maxeiner, J. H., Finotto, S., Lohse, A. W., Blessing, M., and Schramm, C. (2008) Coexpression of TGF-β1 and IL-10 enables regulatory T cells to completely suppress airway hyper-reactivity. J. Immunol. 181, 7751-7758
40. + Foxp3 regulatory cells. Int. Immunol. 22, 259-270