Id2 reinforces TH 1 differentiation and inhibits E2A to repress TFH differentiation

Nature Immunology

Volumn 17, Issue 7, 2016, Pages 834-843

  Shaw, Laura A ^a   Bélanger, Simon ^b   Omilusik, Kyla D ^a   Cho, Sunglim ^a   Scott Browne, James P ^b   Nance, J Philip ^b   Goulding, John ^a   Lasorella, Anna ^c   Lu, Li Fan ^a   Crotty, Shane ^b,d   Goldrath, Ananda W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^c NewYork Presbyterian Hospital   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR5; INHIBITOR OF DIFFERENTIATION 2; INHIBITOR OF DIFFERENTIATION 3; PROTEIN BCL 6; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR E2A; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BCL6 PROTEIN, MOUSE; IDB2 PROTEIN, MOUSE; PROTEIN BINDING; SMALL INTERFERING RNA; TCF3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; GENE EXPRESSION REGULATION; GENE LOCUS; GENE REPRESSION; HELPER CELL; LYMPHOCYTE DIFFERENTIATION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; T CELL DEPLETION; T FOLLICULAR HELPER CELL; TH1 CELL; TOXOPLASMA GONDII; TOXOPLASMOSIS; ANIMAL; ARENAVIRUS INFECTION; C57BL MOUSE; CBA MOUSE; CELL CULTURE; CELL DIFFERENTIATION; GENETICS; GERMINAL CENTER; IMMUNOLOGY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; METABOLISM; PARASITOLOGY; PHYSIOLOGY; TOXOPLASMA; TRANSGENIC MOUSE; VIROLOGY;

ANIMALS; ARENAVIRIDAE INFECTIONS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; GERMINAL CENTER; INHIBITOR OF DIFFERENTIATION PROTEIN 2; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, TRANSGENIC; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-BCL-6; RNA, SMALL INTERFERING; TH1 CELLS; TOXOPLASMA; TOXOPLASMOSIS;

EID: 84969795465     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3461     Document Type: Article

References (54)

1. Zhu, J., Yamane, H. & Paul, W. E. Differentiation of effector CD4 T cell populations. Annu. Rev. Immunol. 28, 445-489 (2010).
2. Crotty, S. T follicular helper cell differentiation, function, and roles in disease. Immunity 41, 529-542 (2014).
3. Vahedi, G. et al. Helper T-cell identity and evolution of differential transcriptomes and epigenomes. Immunol. Rev. 252, 24-40 (2013).
4. Nurieva, R. I. et al. Bcl6 mediates the development of T follicular helper cells. Science 325, 1001-1005 (2009).
5. Yu, D. et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 31, 457-468 (2009).
6. Nakayamada, S. et al. Early Th1 cell differentiation is marked by a Tfh cell-like transition. Immunity 35, 919-931 (2011).
7. Oestreich, K. J., Mohn, S. E. & Weinmann, A. S. Molecular mechanisms that control the expression and activity of Bcl-6 in TH1 cells to regulate flexibility with a TFH-like gene profile. Nat. Immunol. 13, 405-411 (2012).
8. Johnston, R. J. et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 325, 1006-1010 (2009).
9. Cannarile, M. A. et al. Transcriptional regulator Id2 mediates CD8+ T cell immunity. Nat. Immunol. 7, 1317-1325 (2006).
10. de Pooter, R. F. & Kee, B. L. E proteins and the regulation of early lymphocyte development. Immunol. Rev. 238, 93-109 (2010).
11. D'Cruz, L. M., Stradner, M. H., Yang, C. Y. & Goldrath, A. W. E and Id proteins influence invariant NKT cell sublineage differentiation and proliferation. J. Immunol. 192, 2227-2236 (2014).
12. 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).
13. Eberl, G., Colonna, M., Di Santo, J. P. & McKenzie, A. N. Innate lymphoid cells. Innate lymphoid cells: a new paradigm in immunology. Science 348, aaa6566 (2015).
14. 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).
15. D'Cruz, L. M., Lind, K. C., Wu, B. B., Fujimoto, J. K. & Goldrath, A. W. Loss of E protein transcription factors E2A and HEB delays memory-precursor formation during the CD8+ T-cell immune response. Eur. J. Immunol. 42, 2031-2041 (2012).
16. Masson, F. et al. Id2-mediated inhibition of E2A represses memory CD8+ T cell differentiation. J. Immunol. 190, 4585-4594 (2013).
17. Ji, Y. et al. Repression of the DNA-binding inhibitor Id3 by Blimp-1 limits the formation of memory CD8+ T cells. Nat. Immunol. 12, 1230-1237 (2011).
18. Gao, P. et al. Dynamic changes in E-protein activity regulate T reg cell development. J. Exp. Med. 211, 2651-2668 (2014).
19. 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).
20. Miyazaki, M. et al. Id2 and Id3 maintain the regulatory T cell pool to suppress inflammatory disease. Nat. Immunol. 15, 767-776 (2014).
21. Lin, Y. Y. et al. Transcriptional regulator Id2 is required for the CD4 T cell immune response in the development of experimental autoimmune encephalomyelitis. J. Immunol. 189, 1400-1405 (2012).
22. Liu, X. et al. Transcription factor achaete-scute homologue 2 initiates follicular T-helper-cell development. Nature 507, 513-518 (2014).
23. Choi, Y. S. et al. Bcl6 expressing follicular helper CD4 T cells are fate committed early and have the capacity to form memory. J. Immunol. 190, 4014-4026 (2013).
24. 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).
25. 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).
26. Choi, Y. S. et al. LEF-1 and TCF-1 orchestrate TFH differentiation by regulating differentiation circuits upstream of the transcriptional repressor Bcl6. Nat. Immunol. 16, 980-990 (2015).
27. Nance, J. P. et al. Bcl6 middle domain repressor function is required for T follicular helper cell differentiation and utilizes the corepressor MTA3. Proc. Natl. Acad. Sci. USA 112, 13324-13329 (2015).
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. Johnston, R. J., Choi, Y. S., Diamond, J. A., Yang, J. A. & Crotty, S. STAT5 is a potent negative regulator of TFH cell differentiation. J. Exp. Med. 209, 243-250 (2012).
30. Poholek, A. C. et al. In vivo regulation of Bcl6 and T follicular helper cell development. J. Immunol. 185, 313-326 (2010).
31. Ray, J. P. et al. The interleukin-2-mTORc1 kinase axis defines the signaling, differentiation, and metabolism of T helper 1 and follicular B helper T cells. Immunity 43, 690-702 (2015).
32. Amir, A. D. et al. viSNE enables visualization of high dimensional single-cell data and reveals phenotypic heterogeneity of leukemia. Nat. Biotechnol. 31, 545-552 (2013).
33. Sher, A. et al. Induction and regulation of IL-12-dependent host resistance to Toxoplasma gondii. Immunol. Res. 27, 521-528 (2003).
34. Guo, Z. et al. Modeling Sjögren's syndrome with Id3 conditional knockout mice. Immunol. Lett. 135, 34-42 (2011).
35. Nance, J. P., Bélanger, S., Johnston, R. J., Takemori, T. & Crotty, S. Cutting edge: T follicular helper cell differentiation is defective in the absence of Bcl6 BTB repressor domain function. J. Immunol. 194, 5599-5603 (2015).
36. Pepper, M., Pagán, A. J., Igyártó, B. Z., Taylor, J. J. & Jenkins, M. K. Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 35, 583-595 (2011).
37. Hatzi, K. et al. BCL6 orchestrates Tfh cell differentiation via multiple distinct mechanisms. J. Exp. Med. 212, 539-553 (2015).
38. Xiao, R. et al. Identification and characterization of a cathepsin D homologue from lampreys (Lampetra japonica). Dev. Comp. Immunol. 49, 149-156 (2015).
39. Stone, E. L. et al. ICOS coreceptor signaling inactivates the transcription factor FOXO1 to promote Tfh cell differentiation. Immunity 42, 239-251 (2015).
40. Miyazaki, M. et al. The E-Id protein axis modulates the activities of the PI3K-AKT-mTORC1-Hif1a and c-myc/p19Arf pathways to suppress innate variant TFH cell development, thymocyte expansion, and lymphomagenesis. Genes Dev. 29, 409-425 (2015).
41. Kitano, M. et al. Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity 34, 961-972 (2011).
42. Hale, J. S. et al. Distinct memory CD4+ T cells with commitment to T follicular helper-and T helper 1-cell lineages are generated after acute viral infection. Immunity 38, 805-817 (2013).
43. Yusuf, I. et al. Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150). J. Immunol. 185, 190-202 (2010).
44. 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).
45. Wu, T. et al. TCF1 is required for the T follicular helper cell response to viral infection. Cell Rep. 12, 2099-2110 (2015).
46. Xu, L. et al. The transcription factor TCF-1 initiates the differentiation of TFH cells during acute viral infection. Nat. Immunol. 16, 991-999 (2015).
47. Kroenke, M. A. et al. Bcl6 and Maf cooperate to instruct human follicular helper CD4 T cell differentiation. J. Immunol. 188, 3734-3744 (2012).
48. Choi, Y. S., Eto, D., Yang, J. A., Lao, C. & Crotty, S. Cutting edge: STAT1 is required for IL-6-mediated Bcl6 induction for early follicular helper cell differentiation. J. Immunol. 190, 3049-3053 (2013).
49. Baumjohann, D., Okada, T. & Ansel, K. M. Cutting Edge: distinct waves of BCL6 expression during T follicular helper cell development. J. Immunol. 187, 2089-2092 (2011).
50. Oxenius, A., Bachmann, M. F., Zinkernagel, R. M. & Hengartner, H. Virus-specific MHC-class II-restricted TCR-transgenic mice: effects on humoral and cellular immune responses after viral infection. Eur. J. Immunol. 28, 390-400 (1998).
51. Kaji, T. et al. Distinct cellular pathways select germline-encoded and somatically mutated antibodies into immunological memory. J. Exp. Med. 209, 2079-2097 (2012).
52. Chen, R. et al. In vivo RNA interference screens identify regulators of antiviral CD4+ and CD8+ T cell differentiation. Immunity 41, 325-338 (2014).
53. Doedens, A. L. et al. Hypoxia-inducible factors enhance the effector responses of CD8+ T cells to persistent antigen. Nat. Immunol. 14, 1173-1182 (2013).
54. Ebert, A. et al. The distal VH gene cluster of the Igh locus contains distinct regulatory elements with Pax5 transcription factor-dependent activity in pro-B cells. Immunity 34, 175-187 (2011).