The transcription factor musculin promotes the unidirectional development of peripheral T reg cells by suppressing the T H 2 transcriptional program

Nature Immunology

Volumn 18, Issue 3, 2017, Pages 344-353

  Wu, Chuan ^a,c   Chen, Zuojia ^a   Dardalhon, Valerie ^a,d   Xiao, Sheng ^a   Thalhamer, Theresa ^a   Liao, Mengyang ^a   Madi, Asaf ^a   Franca, Rafael F ^a,e   Han, Timothy ^a   Oukka, Mohammed ^b   Kuchroo, Vijay ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 27; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR MUSCULIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; GATA3 PROTEIN, MOUSE; MSC PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CELL MATURATION; CHROMATIN IMMUNOPRECIPITATION; EMBRYO TRANSFER; ENTERITIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; HISTONE MODIFICATION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PNEUMONIA; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE SUBPOPULATION; TH2 CELL; ANIMAL; C57BL MOUSE; CELL CULTURE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; INFLAMMATION; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; FORKHEAD TRANSCRIPTION FACTORS; GATA3 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; INFLAMMATION; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PNEUMONIA; T-LYMPHOCYTES, REGULATORY; TH2 CELLS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 85010857684     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3667     Document Type: Article

References (50)

1. Murphy, K. M. & Stockinger, B. Effector T cell plasticity: flexibility in the face of changing circumstances. Nat. Immunol. 11, 674-680 (2010).
2. Josefowicz, S. Z., Lu, L. F. & Rudensky, A. Y. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30, 531-564 (2012).
3. Sakaguchi, S., Miyara, M., Costantino, C. M. & Hafler, D. A. FOXP3+ regulatory T cells in the human immune system. Nat. Rev. Immunol. 10, 490-500 (2010).
4. Brunkow, M. E. et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27, 68-73 (2001).
5. Zheng, Y. & Rudensky, A. Y. Foxp3 in control of the regulatory T cell lineage. Nat. Immunol. 8, 457-462 (2007).
6. Bluestone, J. A. & Abbas, A. K. Natural versus adaptive regulatory T cells. Nat. Rev. Immunol. 3, 253-257 (2003).
7. Fontenot, J. D., Gavin, M. A. & Rudensky, A. Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4, 330-336 (2003).
8. Marie, J. C., Letterio, J. J., Gavin, M. & Rudensky, A. Y. TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J. Exp. Med. 201, 1061-1067 (2005).
9. Davidson, T. S., DiPaolo, R. J., Andersson, J. & Shevach, E. M. Cutting Edge: IL-2 is essential for TGF-mediated induction of Foxp3+ T regulatory cells. J. Immunol. 178, 4022-4026 (2007).
10. Wahl, S. M. et al. Transforming growth factor- is a potent immunosuppressive agent that inhibits IL-1-dependent lymphocyte proliferation. J. Immunol. 140, 3026-3032 (1988).
11. Ruegemer, J. J. et al. Regulatory effects of transforming growth factor- on IL-2-and IL-4-dependent T cell-cycle progression. J. Immunol. 144, 1767-1776 (1990).
12. Mathas, S. et al. Intrinsic inhibition of transcription factor E2A by HLH proteins ABF-1 and Id2 mediates reprogramming of neoplastic B cells in Hodgkin lymphoma. Nat. Immunol. 7, 207-215 (2006).
13. Lu, J. R. et al. Control of facial muscle development by MyoR and capsulin. Science 298, 2378-2381 (2002).
14. Debuisson, D., Mari, N., Denanglaire, S., Leo, O. & Andris, F. Myor/ABF-1 mRNA expression marks follicular helper T cells but is dispensable for Tfh cell differentiation and function in vivo. PLoS One 8, e84415 (2013).
15. Hall, A. O. et al. The cytokines interleukin 27 and interferon- promote distinct Treg cell populations required to limit infection-induced pathology. Immunity 37, 511-523 (2012).
16. Ciofani, M. et al. A validated regulatory network for Th17 cell specification. Cell 151, 289-303 (2012).
17. Tussiwand, R. et al. Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature 490, 502-507 (2012).
18. Weiss, J. M. et al. Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3+ T reg cells. J. Exp. Med. 209, 1723-1742 (2012).
19. Yadav, M. et al. Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J. Exp. Med. 209, 1713-1722 (2012).
20. Takimoto, T. et al. Smad2 and Smad3 are redundantly essential for the TGF-mediated regulation of regulatory T plasticity and Th1 development. J. Immunol. 185, 842-855 (2010).
21. Xu, L. et al. Positive and negative transcriptional regulation of the Foxp3 gene is mediated by access and binding of the Smad3 protein to enhancer I. Immunity 33, 313-325 (2010).
22. Siddiqui, K. R. & Powrie, F. CD103+ GALT DCs promote Foxp3+ regulatory T cells. Mucosal Immunol. 1 (Suppl. 1), S34-S38 (2008).
23. Coombes, J. L. et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF- And retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757-1764 (2007).
24. Lu, J., Webb, R., Richardson, J. A. & Olson, E. N. MyoR: a muscle-restricted basic helix-loop-helix transcription factor that antagonizes the actions of MyoD. Proc. Natl. Acad. Sci. USA 96, 552-557 (1999).
25. Dardalhon, V. et al. IL-4 inhibits TGF-induced Foxp3+ T cells and, together with TGF-, generates IL-9+IL-10+Foxp3 effector T cells. Nat. Immunol. 9, 1347-1355 (2008).
26. Beal, A. M., Ramos-Hernández, N., Riling, C. R., Nowelsky, E. A. & Oliver, P. M. TGF- induces the expression of the adaptor Ndfip1 to silence IL-4 production during iTreg cell differentiation. Nat. Immunol. 13, 77-85 (2011).
27. Rice, J. C. et al. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol. Cell 12, 1591-1598 (2003).
28. Tao, X. et al. Neutralization of IL-4 and IFN- facilitates inducing TGF-induced CD4+Foxp3+ regulatory cells. Int. J. Biomed. Sci. 4, 52-57 (2008).
29. Zheng, W. & Flavell, R. A. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89, 587-596 (1997).
30. Massari, M. E. et al. Characterization of ABF-1, a novel basic helix-loop-helix transcription factor expressed in activated B lymphocytes. Mol. Cell. Biol. 18, 3130-3139 (1998).
31. Kishikawa, H., Sun, J., Choi, A., Miaw, S. C. & Ho, I. C. The cell type-specific expression of the murine IL-13 gene is regulated by GATA-3. J. Immunol. 167, 4414-4420 (2001).
32. Tanaka, S. et al. The enhancer HS2 critically regulates GATA-3-mediated Il4 transcription in TH2 cells. Nat. Immunol. 12, 77-85 (2011).
33. Spilianakis, C. G. & Flavell, R. A. Long-range intrachromosomal interactions in the T helper type 2 cytokine locus. Nat. Immunol. 5, 1017-1027 (2004).
34. Sanyal, A., Lajoie, B. R., Jain, G. & Dekker, J. The long-range interaction landscape of gene promoters. Nature 489, 109-113 (2012).
35. Ribeiro de Almeida, C. et al. Critical role for the transcription regulator CCCTC-binding factor in the control of Th2 cytokine expression. J. Immunol. 182, 999-1010 (2009).
36. Joller, N. et al. Treg cells expressing the coinhibitory molecule TIGIT selectively inhibit proinflammatory Th1 and Th17 cell responses. Immunity 40, 569-581 (2014).
37. Chen, W. et al. Conversion of peripheral CD4+CD25 naive T cells to CD4+CD25+ regulatory T cells by TGF- induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886 (2003).
38. Wei, G. et al. Genome-wide analyses of transcription factor GATA-3-mediated gene regulation in distinct T cell types. Immunity 35, 299-311 (2011).
39. Xu, W. et al. Adoptive transfer of induced-Treg cells effectively attenuates murine airway allergic inflammation. PLoS One 7, e40314 (2012).
40. Belkaid, Y. Regulatory T cells and infection: a dangerous necessity. Nat. Rev. Immunol. 7, 875-888 (2007).
41. Flavell, R. A., Sanjabi, S., Wrzesinski, S. H. & Licona-Limón, P. The polarization of immune cells in the tumour environment by TGF. Nat. Rev. Immunol. 10, 554-567 (2010).
42. Zheng, Y. et al. Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 463, 808-812 (2010).
43. Josefowicz, S. Z. et al. Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature 482, 395-399 (2012).
44. 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).
45. Jones, S. An overview of the basic helix-loop-helix proteins. Genome Biol. 5, 226 (2004).
46. Oestreich, K. J. & Weinmann, A. S. Master regulators or lineage-specifying Changing views on CD4+ T cell transcription factors. Nat. Rev. Immunol. 12, 799-804 (2012).
47. Pillemer, B. B. et al. STAT6 activation confers upon T helper cells resistance to suppression by regulatory T cells. J. Immunol. 183, 155-163 (2009).
48. Wohlfert, E. A. et al. GATA-3 controls Foxp3 regulatory T cell fate during inflammation in mice. J. Clin. Invest. 121, 4503-4515 (2011).
49. Datto, M. B. et al. Targeted disruption of Smad3 reveals an essential role in transforming growth factor -mediated signal transduction. Mol. Cell. Biol. 19, 2495-2504 (1999).
50. Sánchez-Fueyo, A. et al. Tim-3 inhibits T helper type 1-mediated auto-and alloimmune responses and promotes immunological tolerance. Nat. Immunol. 4, 1093-1101 (2003).