Id2 and Id3 maintain the regulatory T cell pool to suppress inflammatory disease

Nature Immunology

Volumn 15, Issue 8, 2014, Pages 767-776

  Miyazaki, Masaki ^a   Miyazaki, Kazuko ^a   Chen, Shuwen ^a   Itoi, Manami ^b   Miller, Marina ^b   Lu, Li Fan ^a   Varki, Nissi ^d   Chang, Aaron N ^a   Broide, David H ^c   Murre, Cornelis ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MEIJI UNIVERSITY OF INTEGRATIVE MEDICINE   (Japan)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR5; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN M; INDUCIBLE T CELL COSTIMULATOR; INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION 3; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; L SELECTIN; NEUROPILIN 1; OSTEOGENIC PROTEIN 1; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN MYB; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR E2F2; TRANSCRIPTION FACTOR FOXP3;

ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CELL ACTIVATION; CELL CYCLE CHECKPOINT; CELL DEATH; CELL DIFFERENTIATION; CELL FUNCTION; CELL POPULATION; CELL SPECIFICITY; CELLULAR DISTRIBUTION; CONTROL; DERMATITIS; ENHANCER REGION; FEMALE; GENETIC TRANSCRIPTION; IMMUNOGLOBULIN BLOOD LEVEL; INFLAMMATORY DISEASE; INFLAMMATORY INFILTRATE; LYMPH NODE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION;

ANIMALS; BASE SEQUENCE; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; INFLAMMATION; INHIBITOR OF DIFFERENTIATION PROTEIN 2; INHIBITOR OF DIFFERENTIATION PROTEINS; INTERLEUKIN-10; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, CXCR5; SEQUENCE ANALYSIS, RNA; T-LYMPHOCYTES, REGULATORY;

EID: 84904727902     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2928     Document Type: Article

References (53)

1. Josefowicz, S.Z., Lu, L.F. & Rudensky, A.Y. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30, 531-564 (2012).
2. Sakaguchi, S., Yamaguchi, T., Nomura, T. & Ono, M. Regulatory T cells and immune tolerance. Cell 133, 775-787 (2008).
3. Vignali, D.A.A., Collison, L.W. & Workman, C.J. How regulatory T cells work. Nat. Rev. Immunol. 8, 523-532 (2008).
4. Locksley, R.M. Asthma and allergic inflammation. Cell 140, 777-783 (2010).
5. Rothenberg, M.E. & Hogan, S.P. The eosinophil. Annu. Rev. Immunol. 24, 147-174 (2006).
6. Sakaguchi, S. et al. Immunologic self-tolerance maintained by activated T cells expressing Il2-receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155, 1151-1164 (1995).
7. Bennett, C.L. et al. The immune dysregulation, polyendocrinopahty, X-linked syndrome (IPEX) is caused by mutations of Foxp3. Nat. Genet. 27, 20-21 (2001).
8. Wildin, R.S. et al. X-linked neonatal diabetes, emteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat. Genet. 27, 18-20 (2001).
9. Hori, S., Nomura, T. & Sakaguchi, S. Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057-1061 (2003).
10. 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).
11. Khattri, R., Cox, T., Yasayko, S.A. & Ramsdell, F. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat. Immunol. 4, 337-342 (2003).
12. Josefowicz, S.Z. et al. Extratymically generated regulatory T cells control mucosal Th2 inflammation. Nature 482, 395-399 (2012).
13. Wing, J.B. & Sakaguchi, S. Foxp3+ Treg cells in humoral immunity. Int. Immunol. 26, 61-69 (2014).
14. Chung, Y. et al. Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat. Med. 17, 983-988 (2011).
15. Linterman, M.A. et al. Foxp3 follicular regulatory T cells control the germinal center response. Nat. Med. 17, 975-982 (2011).
16. Sage, P.T., Francisco, L.M., Carman, C.V. & Sharpe, A.H. The receptor PD-1 controls follicular regulatory T cells in the lymph nodes and blood. Nat. Immunol. 14, 152-161 (2013).
17. Murre, C. Helix-loop-helix proteins and lymphocyte development. Nat. Immunol. 6, 1079-1086 (2005).
18. Murre, C., McCaw, P.S. & Baltimore, D. A new DNA binding and dimerization motif. Cell 56, 777-783 (1989).
19. Benezra, R., Davis, R.L., Lockshon, D., Turner, D.L. & Weintraub, H. The protein Id: A negative regulator of helix-loop-helix DNA binding proteins. Cell 61, 49-59 (1990).
20. Yokota, Y. et al. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix protein Id2. Nature 397, 702-706 (1999).
21. Rivera, R.R., Johns, C.P., Quan, J., Johnson, R.S. & Murre, C. Thymocyte selection is regulated by the helix-loop-helix inhibitor protein, Id3. Immunity 12, 17-26 (2000).
22. Verykokakis, M., Boos, M.D., Bendelac, A. & Kee, B.L. SAP protein-dependent natural killer T-like cells regulate the development of CD8(+) T cells with innate lymphocyte characteristics. Immunity 33, 203-215 (2010).
23. 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).
24. 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).
25. 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).
26. Miyazaki, M. et al. The opposing roles of the transcription factor E2A and its antagonist Id3 that orchestrate and enforce the naive fate of T cells. Nat. Immunol. 12, 992-1001 (2011).
27. Yang, C.Y. et al. The transcriptional regulators Id2 and Id3 control the formation of distinct memory CD8+ T cell subsets. Nat. Immunol. 12, 1221-1229 (2011).
28. Niola, F. et al. Id proteins synchronize stemness and anchorage to the niche of neural stem cells. Nat. Cell Biol. 14, 477-487 (2012).
29. Rubtsov, Y.P. et al. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28, 546-558 (2008).
30. Liston, A., Lu, L.F., O'Carroll, D., Tarakhovsky, A. & Rudensky, A.Y. Dicer-dependent microRNA pathway safeguards regulatory T cell function. J. Exp. Med. 205, 1993-2004 (2008).
31. Nussbaum, J.C. et al. Type 2 Innate lymphoid cells control eosinophil homeostasis. Nature 502, 245-248 (2013).
32. Monticelli, L.A., Sonnenberg, G.F. & Artis, D. Innate lymphoid cells: critical regulators of allergic inflammation and tissue repair in the lung. Curr. Opin. Immunol. 24, 284-289 (2012).
33. Chang, Y.J. et al. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat. Immunol. 12, 631-638 (2011).
34. Cretney, E., Kallies, A. & Nutt, S.L. Differentiation and function of Foxp3+ effector regulatory T cells. Trends Immunol. 34, 74-80 (2013).
35. Cretney, E. et al. The transcription factors, Blimp-1 and IRF4 jointly control the differentiation and function of effector regulatory T cells. Nat. Immunol. 12, 304-311 (2011).
36. Smigiel, K.S. et al. CCR7 provides localized access to IL-2 and defines homeostatically distinct regulatory T cell subsets. J. Exp. Med. 211, 121-136 (2014).
37. Thornton, A.M. et al. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J. Immunol. 184, 3433-3441 (2010).
38. Weiss, J.M. et al. Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3+ Treg cells. J. Exp. Med. 209, 1723-1742 (2012).
39. Delgoffe, G.M. et al. Stability of regulatory T cells is maintained by a neuropilin-1-semaphorin-4a axis. Nature 501, 252-256 (2013).
40. Lin, Y.C. et al. A global network of transcription factors, involving E2A, EBF1, and Foxo1, that orchestrates B cell fate. Nat. Immunol. 11, 635-643 (2010).
41. Xu, H. et al. Follicular T-helper cell recruitment governed by bystanding B cells and ICOS-driven motility. Nature 496, 523-527 (2013).
42. Choi, Y.S. et al. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 34, 932-946 (2011).
43. Liu, X. et al. Transcription factor achaete-scute homologue 2 initiates follicular T-helper-cell development. Nature 507, 513-518 (2014).
44. 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).
45. Bain, G. et al. Thymocyte maturation is regulated by the activity of the helix-loop-helix protein, E47. J. Exp. Med. 190, 1605-1616 (1999).
46. Engel, I., Johns, C., Bain, G., Rivera, R.R. & Murre, C. Early thymocyte development is regulated by modulation of E2A protein activity. J. Exp. Med. 194, 733-745 (2001).
47. Quong, M. et al. Receptor editing and marginal zone B cell development are regulated by the helix-loop-helix protein, E2A. J. Exp. Med. 199, 1101-1112 (2004).
48. Masson, F. et al. Id2-mediated inhibition of E2A represses memory CD8+ T cell differentiation. J. Immunol. 190, 4585-4594 (2013).
49. Knell, J. et al. Id2 influences differentiation of killer cell lectin-like receptor G1(hi) short-lived CD8+ effector T cells. J. Immunol. 190, 1501-1509 (2013).
50. Burich, A. et al. Helicobacter-induced inflammatory bowel disease in IL-10- and T cell-deficient mice. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G764-G778 (2001).
51. Suzukawa, M. et al. Sialyltransferase ST3Gal-III regulates SiglecF ligand formation and eosinophilic lung inflammation in mice. J. Immunol. 190, 5939-5948 (2013).
52. Smith, K.G.C. et al. bcl-2 transgene expression Inhibits apoptosis in the germinal center and reveals differences in the selection of memory B cells and bone marrow antibody-forming cells. J. Exp. Med. 191, 475-484 (2000).
53. Miyazaki, K. et al. The role of the basic helix-loop-helix transcription factor Dec1 in the regulatory T cells. J. Immunol. 185, 7330-7339 (2010).