Histone deacetylase sirtuin 1 deacetylates IRF1 protein and programs dendritic cells to control Th17 protein differentiation during autoimmune inflammation

Journal of Biological Chemistry

Volumn 288, Issue 52, 2013, Pages 37256-37266

  Yang, Heeyoung ^a   Lee, Sang Myeong ^a   Gao, Beixue ^a   Zhang, Jinping ^b   Fang, Deyu ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b SOOCHOW UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DC FUNCTIONS; DENDRITIC CELLS; HISTONE DEACETYLASES; INFLAMMATORY DISEASE; SIRTUIN;

PATHOLOGY; PROTEINS;

CELLS;

BETA ACTIN; BETA INTERFERON; HISTONE DEACETYLASE; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 27; SIRTUIN 1;

ACETYLATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELLULAR IMMUNITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEACETYLATION; DENDRITIC CELL; ENZYME ASSAY; FLUORESCENCE MICROSCOPY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH17 CELL;

EID: 84891450164     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.527531     Document Type: Article

References (48)

1. Shore, D., Squire, M., and Nasmyth, K. A. (1984) Characterization of two genes required for the position-effect control of yeast mating-type genes. EMBO J. 3, 2817-2823
2. Michishita, E., Park, J. Y., Burneskis, J. M., Barrett, J. C., and Horikawa, I. (2005) Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol. Biol. Cell 16, 4623-4635
3. Haigis, M. C., and Sinclair, D. A. (2010) Mammalian sirtuins: biological insights and disease relevance. Annu. Rev. Pathol. 5, 253-295
4. Gillum, M. P., Erion, D. M., and Shulman, G. I. (2010) Sirtuin-1 regulation of mammalian metabolism. Trends Mol. Med. 17, 8-13, 22
5. Schug, T. T., Xu, Q., Gao, H., Peres-da-Silva, A., Draper, D. W., Fessler, M. B., Purushotham, A., and Li, X. (2010) Myeloid deletion of SIRT1 induces inflammatory signaling in response to environmental stress. Mol. Cell. Biol. 30, 4712-4721
6. Zhang, J., Lee, S. M., Shannon, S., Gao, B., Chen, W., Chen, A., Divekar, R., McBurney, M. W., Braley-Mullen, H., Zaghouani, H., and Fang, D. (2009) The type III histone deacetylase Sirt1 is essential for maintenance of T cell tolerance in mice. J. Clin. Invest. 119, 3048-3058
7. Kong, S., Kim, S. J., Sandal, B., Lee, S. M., Gao, B., Zhang, D. D., and Fang, D. (2011) The type III histone deacetylase Sirt1 protein suppresses p300- mediated histone H3 lysine 56 acetylation at Bclaf1 promoter to inhibit T cell activation. J. Biol. Chem. 286, 16967-16975
8. Gao, B., Kong, Q., Kemp, K., Zhao, Y. S., and Fang, D. (2012) Analysis of sirtuin 1 expression reveals a molecular explanation of IL-2-mediated reversal of T-cell tolerance. Proc. Natl. Acad. Sci. U.S.A. 109, 899-904
9. Sequeira, J., Boily, G., Bazinet, S., Saliba, S., He, X., Jardine, K., Kennedy, C., Staines, W., Rousseaux, C., Mueller, R., and McBurney, M. W. (2008) Sirt1-null mice develop an autoimmune-like condition. Exp. Cell Res. 314, 3069-3074
10. +T cells. Immunity 16, 779-790
11. Pirhonen, J., Sirén, J., Julkunen, I., and Matikainen, S. (2007) IFN-α regulates Toll-like receptor-mediated IL-27 gene expression in human macrophages. J. Leukocyte Biol. 82, 1185-1192
12. Remoli, M. E., Gafa, V., Giacomini, E., Severa, M., Lande, R., and Coccia, E. M. (2007) IFN-α modulates the response to TLR stimulation in human DC: involvement of IFN regulatory factor-1 (IRF-1) in IL-27 gene expression. Eur. J. Immunol. 37, 3499-3508
13. Schuetze, N., Schoeneberger, S., Mueller, U., Freudenberg, M. A., Alber, G., and Straubinger, R. K. (2005) IL-12 family members: differential kinetics of their TLR4-mediated induction by Salmonella enteritidis and the impact of IL-10 in bone marrow-derived macrophages. Int. Immunol. 17, 649-659
14. Matsuyama, T., Kimura, T., Kitagawa, M., Pfeffer, K., Kawakami, T., Watanabe, N., Kündig, T. M., Amakawa, R., Kishihara, K., and Wakeham, A. (1993) Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development. Cell 75, 83-97
15. Stranges, P. B., Watson, J., Cooper, C. J., Choisy-Rossi, C. M., Stonebraker, A. C., Beighton, R. A., Hartig, H., Sundberg, J. P., Servick, S., Kaufmann, G., Fink, P. J., and Chervonsky, A. V. (2007) Elimination of antigen-presenting cells and autoreactive T cells by Fas contributes to prevention of autoimmunity. Immunity 26, 629-641
16. Chen, A., Gao, B., Zhang, J., McEwen, T., Ye, S. Q., Zhang, D., and Fang, D. (2009) The HECT-type E3 ubiquitin ligase AIP2 inhibits activation-induced T-cell death by catalyzing EGR2 ubiquitination. Mol. Cell. Biol. 29, 5348-5356
17. Gao, B., Calhoun, K., and Fang, D. (2006) The proinflammatory cytokines IL-1′ and TNF-α induce the expression of Synoviolin, an E3 ubiquitin ligase, in mouse synovial fibroblasts via the Erk1/2-ETS1 pathway. Arthritis Res. Ther. 8, R172
18. Lin, Z., Yang, H., Kong, Q., Li, J., Lee, S. M., Gao, B., Dong, H., Wei, J., Song, J., Zhang, D. D., and Fang, D. (2012) USP22 antagonizes p53 transcriptional activation by deubiquitinating Sirt1 to suppress cell apoptosis and is required for mouse embryonic development. Mol. Cell 46, 484-494
19. Lee, S. M., Gao, B., and Fang, D. (2008) FoxP3 maintains Treg unresponsiveness by selectively inhibiting the promoter DNA-binding activity of AP-1. Blood 111, 3599-3606
20. +T-cell differentiation and allergic lung inflammation. Mol. Cell. Biol. 31, 3445-3456
21. Qiu, Q., Zheng, Z., Chang, L., Zhao, Y. S., Tan, C., Dandekar, A., Zhang, Z., Lin, Z., Gui, M., Li, X., Zhang, T., Kong, Q., Li, H., Chen, S., Chen, A., Kaufman, R. J., Yang, W. L., Lin, H. K., Zhang, D., Perlman, H., Thorp, E., Zhang, K., and Fang, D. (2013) Toll-like receptor-mediated IRE1α activation as a therapeutic target for inflammatory arthritis. EMBO J. 32, 2477-2490
22. Kemp, K. L., Li, Z., Zhao, F., Gao, B., Song, J., Zhang, K., and Fang, D. (2013) The serine-threonine kinase inositol-requiring enzyme 1α (IRE1α) promotes IL-4 production in T helper cells. J. Biol. Chem. 288, 33272-33282
23. Cox, J. H., Kljavin, N. M., Ramamoorthi, N., Diehl, L., Batten, M., and Ghilardi, N. (2011) IL-27 promotes T cell-dependent colitis through multiple mechanisms. J. Exp. Med. 208, 115-123
24. Apetoh, L., Quintana, F. J., Pot, C., Joller, N., Xiao, S., Kumar, D., Burns, E. J., Sherr, D. H., Weiner, H. L., and Kuchroo, V. K. (2010) The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat. Immunol. 11, 854-861
25. +T cells. J. Immunol. 183, 2435-2443
26. Pot, C., Jin, H., Awasthi, A., Liu, S. M., Lai, C. Y., Madan, R., Sharpe, A. H., Karp, C. L., Miaw, S. C., Ho, I. C., and Kuchroo, V. K. (2009) Cutting edge: IL-27 induces the transcription factor c-Maf, cytokine IL-21, and the costimulatory receptor ICOS that coordinately act together to promote differentiation of IL-10-producing Tr1 cells. J. Immunol. 183, 797-801
27. Awasthi, A., Carrier, Y., Peron, J. P., Bettelli, E., Kamanaka, M., Flavell, R. A., Kuchroo, V. K., Oukka, M., and Weiner, H. L. (2007) A dominant function for interleukin 27 in generating interleukin 10-producing antiinflammatory T cells. Nat. Immunol. 8, 1380-1389
28. Fraternale, A., Crinelli, R., Casabianca, A., Paoletti, M. F., Orlandi, C., Carloni, E., Smietana, M., Palamara, A. T., and Magnani, M. (2013) Molecules altering the intracellular thiol content modulate NF-κB and STAT- 1/IRF-1 signalling pathways and IL-12 p40 and IL-27 p28 production in murine macrophages. PLoS One 8, e57866
29. Mattei, F., Schiavoni, G., Sestili, P., Spadaro, F., Fragale, A., Sistigu, A., Lucarini, V., Spada, M., Sanchez, M., Scala, S., Battistini, A., Belardelli, F., and Gabriele, L. (2012) IRF-8 controls melanoma progression by regulating the cross-talk between cancer and immune cells within the tumor microenvironment. Neoplasia 14, 1223-1235
30. Molle, C., Nguyen, M., Flamand, V., Renneson, J., Trottein, F., De Wit, D., Willems, F., Goldman, M., and Goriely, S. (2007) IL-27 synthesis induced by TLR ligation critically depends on IFN regulatory factor 3. J. Immunol. 178, 7607-7615
31. Zhang, J., Qian, X., Ning, H., Yang, J., Xiong, H., and Liu, J. (2010) Activation of IL-27 p28 gene transcription by interferon regulatory factor 8 in cooperation with interferon regulatory factor 1. J. Biol. Chem. 285, 21269-21281
32. Kim, H. S., Go, H., Akira, S., and Chung, D. H. (2011) TLR2-mediated production of IL-27 and chemokines by respiratory epithelial cells promotes bleomycin-induced pulmonary fibrosis in mice. J. Immunol. 187, 4007-4017
33. Génin, P., Morin, P., and Civas, A. (2003) Impairment of interferon-induced IRF-7 gene expression due to inhibition of ISGF3 formation by trichostatin A. J. Virol. 77, 7113-7119
34. Masumi, A., Wang, I. M., Lefebvre, B., Yang, X. J., Nakatani, Y., and Ozato, K. (1999) The histone acetylase PCAF is a phorbol-ester-inducible coactivator of the IRF family that confers enhanced interferon responsiveness. Mol. Cell. Biol. 19, 1810-1820
35. Molle, C., Goldman, M., and Goriely, S. (2010) Critical role of the IFNstimulated gene factor 3 complex in TLR-mediated IL-27p28 gene expression revealing a two-step activation process. J. Immunol. 184, 1784-1792
36. Lock, C., Hermans, G., Pedotti, R., Brendolan, A., Schadt, E., Garren, H., Langer-Gould, A., Strober, S., Cannella, B., Allard, J., Klonowski, P., Austin, A., Lad, N., Kaminski, N., Galli, S. J., Oksenberg, J. R., Raine, C. S., Heller, R., and Steinman, L. (2002) Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 8, 500-508
37. Yang, X. O., Pappu, B. P., Nurieva, R., Akimzhanov, A., Kang, H. S., Chung, Y., Ma, L., Shah, B., Panopoulos, A. D., Schluns, K. S., Watowich, S. S., Tian, Q., Jetten, A. M., and Dong, C. (2008) T helper 17 lineage differentiation is programmed by orphan nuclear receptors RORα and RORα. Immunity 28, 29-39
38. Korn, T., Oukka, M., Kuchroo, V., and Bettelli, E. (2007) Th17 cells: effector T cells with inflammatory properties. Semin. Immunol. 19, 362-371
39. Kryczek, I., Wei, S., Vatan, L., Escara-Wilke, J., Szeliga, W., Keller, E. T., and Zou, W. (2007) Cutting edge: opposite effects of IL-1 and IL-2 on the regulation of IL-17+T cell pool IL-1 subverts IL-2-mediated suppression. J. Immunol. 179, 1423-1426
40. Annunziato, F., Cosmi, L., Santarlasci, V., Maggi, L., Liotta, F., Mazzinghi, B., Parente, E., Filì, L., Ferri, S., Frosali, F., Giudici, F., Romagnani, P., Parronchi, P., Tonelli, F., Maggi, E., and Romagnani, S. (2007) Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204, 1849-1861
41. Nurieva, R., Yang, X. O., Martinez, G., Zhang, Y., Panopoulos, A. D., Ma, L., Schluns, K., Tian, Q., Watowich, S. S., Jetten, A. M., and Dong, C. (2007) Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448, 480-483
42. Hirahara, K., Ghoreschi, K., Yang, X. P., Takahashi, H., Laurence, A., Vahedi, G., Sciumè, G., Hall, A. O., Dupont, C. D., Francisco, L. M., Chen, Q., Tanaka, M., Kanno, Y., Sun, H. W., Sharpe, A. H., Hunter, C. A., and O'Shea, J. J. (2012) Interleukin-27 priming of T cells controls IL-17 production in trans via induction of the ligand PD-L1. Immunity 36, 1017-1030
43. Zou, T., Yang, Y., Xia, F., Huang, A., Gao, X., Fang, D., Xiong, S., and Zhang, J. (2013) Resveratrol inhibits CD4+ T cell activation by enhancing the expression and activity of Sirt1. PLoS One 8, e75139
44. Kuroda, S., Yamazaki, M., Abe, M., Sakimura, K., Takayanagi, H., and Iwai, Y. (2011) Basic leucine zipper transcription factor, ATF-like (BATF) regulates epigenetically and energetically effector CD8 T-cell differentiation via Sirt1 expression. Proc. Natl. Acad. Sci. U.S.A. 108, 14885-14889
45. Feng, D., Sangster-Guity, N., Stone, R., Korczeniewska, J., Mancl, M. E., Fitzgerald-Bocarsly, P., and Barnes, B. J. (2010) Differential requirement of histone acetylase and deacetylase activities for IRF5-mediated proinflammatory cytokine expression. J. Immunol. 185, 6003-6012
46. Masumi, A., Yamakawa, Y., Fukazawa, H., Ozato, K., and Komuro, K. (2003) Interferon regulatory factor-2 regulates cell growth through its acetylation. J. Biol. Chem. 278, 25401-25407
47. Caillaud, A., Prakash, A., Smith, E., Masumi, A., Hovanessian, A. G., Levy, D. E., and Marié, I. (2002) Acetylation of interferon regulatory factor-7 by p300/CREB-binding protein (CBP)-associated factor (PCAF) impairs its DNA binding. J. Biol. Chem. 277, 49417-49421
48. Huang, G., Wang, Y., Vogel, P., Kanneganti, T. D., Otsu, K., and Chi, H. (2012) Signaling via the kinase p38′ programs dendritic cells to drive TH17 differentiation and autoimmune inflammation. Nat. Immunol. 13, 152-161