The DNA-binding inhibitor Id3 regulates IL-9 production in CD4 + T cells

Nature Immunology

Volumn 16, Issue 10, 2015, Pages 1077-1084

  Nakatsukasa, Hiroko ^a   Zhang, Dunfang ^a,b   Maruyama, Takashi ^a   Chen, Hua ^a   Cui, Kairong ^c   Ishikawa, Masaki ^a   Deng, Lisa ^a   Zanvit, Peter ^a   Tu, Eric ^a   Jin, Wenwen ^a   Abbatiello, Brittany ^a   Goldberg, Nathan ^a   Chen, Qianming ^b   Sun, Lingyun ^d   Zhao, Keji ^c   Chen, Wanjun ^a  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^b SICHUAN UNIVERSITY   (China)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^d THE AFFILIATED DRUM TOWER HOSPITAL OF NANJING UNIVERSITY MEDICAL SCHOOL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INHIBITOR OF DIFFERENTIATION 3; INTERLEUKIN 4; INTERLEUKIN 9; TRANSCRIPTION FACTOR E2A; TRANSCRIPTION FACTOR GATA 3; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TRANSFORMING GROWTH FACTOR BETA1; ID3 PROTEIN, HUMAN; INHIBITOR OF DIFFERENTIATION PROTEIN; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TH9 CELL; TUMOR IMMUNITY; WILD TYPE; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL DIFFERENTIATION; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; POLYMERASE CHAIN REACTION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; FLOW CYTOMETRY; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEINS; INTERLEUKIN-9; MICE; NEOPLASM PROTEINS; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84941996879     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3252     Document Type: Article

References (35)

1. Schmitt, E. et al. IL-9 production of naive CD4+ T cells depends on IL-2, is synergistically enhanced by a combination of TGF-β and IL-4, and is inhibited by IFN-γ. J. Immunol. 153, 3989-3996 (1994).
2. Veldhoen, M. et al. Transforming growth factor-β 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat. Immunol. 9, 1341-1346 (2008).
3. Dardalhon, V. et al. IL-4 inhibits TGF-β-induced Foxp3+ T cells and, together with TGF-β, generates IL-9+IL-10+Foxp3- effector T cells. Nat. Immunol. 9, 1347-1355 (2008).
4. Nicolaides, N.C. et al. Interleukin 9: a candidate gene for asthma. Proc. Natl. Acad. Sci. USA 94, 13175-13180 (1997).
5. Cheng, G. et al. Anti-interleukin-9 antibody treatment inhibits airway inflammation and hyperreactivity in mouse asthma model. Am. J. Respir. Crit. Care Med. 166, 409-416 (2002).
6. Staudt, V. et al. Interferon-regulatory factor 4 is essential for the developmental program of T helper 9 cells. Immunity 33, 192-202 (2010).
7. Jäger, A., Dardalhon, V., Sobel, R.A., Bettelli, E. & Kuchroo, V.K. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J. Immunol. 183, 7169-7177 (2009).
8. Singh, T.P. et al. Involvement of IL-9 in Th17-associated inflammation and angiogenesis of psoriasis. PLoS ONE 8, e51752 (2013).
9. Purwar, R. et al. Robust tumor immunity to melanoma mediated by interleukin-9-producing T cells. Nat. Med. 18, 1248-1253 (2012).
10. Lu, Y. et al. Th9 cells promote antitumor immune responses in vivo. J. Clin. Invest. 122, 4160-4171 (2012).
11. Goswami, R. et al. STAT6-dependent regulation of Th9 development. J. Immunol. 188, 968-975 (2012).
12. Chang, H.C. et al. The transcription factor PU.1 is required for the development of IL-9-producing T cells and allergic inflammation. Nat. Immunol. 11, 527-534 (2010).
13. Chen, W. et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886 (2003).
14. Ivanov, I.I. et al. The orphan nuclear receptor RORγt directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126, 1121-1133 (2006).
15. Bettelli, E. et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235-238 (2006).
16. Maruyama, T. et al. Control of the differentiation of regulatory T cells and TH17 cells by the DNA-binding inhibitor Id3. Nat. Immunol. 12, 86-95 (2011).
17. Li, H., Dai, M. & Zhuang, Y.A. T cell intrinsic role of Id3 in a mouse model for primary Sjogren's syndrome. Immunity 21, 551-560 (2004).
18. Jones-Mason, M.E. et al. E protein transcription factors are required for the development of CD4+ lineage T cells. Immunity 36, 348-361 (2012).
19. Liu, Y. et al. A critical function for TGF-β signaling in the development of natural CD4+CD25+Foxp3+ regulatory T cells. Nat. Immunol. 9, 632-640 (2008).
20. Derynck, R. & Zhang, Y.E. Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 425, 577-584 (2003).
21. Mu, Y., Gudey, S.K. & Landstrom, M. Non-Smad signaling pathways. Cell Tissue Res. 347, 11-20 (2012).
22. Choi, M.E., Ding, Y. & Kim, S.I. TGF-β signaling via TAK1 pathway: role in kidney fibrosis. Semin. Nephrol. 32, 244-252 (2012).
23. Tanaka, K. et al. Loss of suppressor of cytokine signaling 1 in helper T cells leads to defective Th17 differentiation by enhancing antagonistic effects of IFN-γ on STAT3 and Smads. J. Immunol. 180, 3746-3756 (2008).
24. Tamiya, T. et al. Smad2/3 and IRF4 play a cooperative role in IL-9-producing T cell induction. J. Immunol. 191, 2360-2371 (2013).
25. Wang, A. et al. Cutting edge: Smad2 and Smad4 regulate TGF-β-mediated Il9 gene expression via EZH2 displacement. J. Immunol. 191, 4908-4912 (2013).
26. Yamashita, M. et al. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-β. Mol. Cell 31, 918-924 (2008).
27. Xiao, X. et al. OX40 signaling favors the induction of TH9 cells and airway inflammation. Nat. Immunol. 13, 981-990 (2012).
28. Murre, C. Helix-loop-helix proteins and lymphocyte development. Nat. Immunol. 6, 1079-1086 (2005).
29. Murre, C. et al. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58, 537-544 (1989).
30. Wilhelm, C. et al. An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat. Immunol. 12, 1071-1077 (2011).
31. Jash, A. et al. Nuclear factor of activated T cells 1 (NFAT1)-induced permissive chromatin modification facilitates nuclear factor-κB (NF-κB)-mediated interleukin-9 (IL-9) transactivation. J. Biol. Chem. 287, 15445-15457 (2012).
32. Tan, C. et al. Antigen-specific Th9 cells exhibit uniqueness in their kinetics of cytokine production and short retention at the inflammatory site. J. Immunol. 185, 6795-6801 (2010).
33. Yang, X. et al. Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-β. EMBO J. 18, 1280-1291 (1999).
34. Konkel, J.E. et al. Control of the development of CD8αα+ intestinal intraepithelial lymphocytes by TGF-β. Nat. Immunol. 12, 312-319 (2011).
35. Wei, G., Hu, G., Cui, K. & Zhao, K. Genome-wide mapping of nucleosome occupancy, histone modifications, and gene expression using next-generation sequencing technology. Methods Enzymol. 513, 297-313 (2012).