Ikaros sets the potential for Th17 lineage gene expression through effects on chromatin state in early T Cell Development

Journal of Biological Chemistry

Volumn 288, Issue 49, 2013, Pages 35170-35179

  Wong, Larry Y ^a   Hatfield, Julianne K ^a   Brown, Melissa A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEVELOPMENT; CELL DIFFERENTIATION; CELL FATES; ESSENTIAL GENE; HEMATOPOIETIC CELL DIFFERENTIATION;

CHEMICAL ACTIVATION; CHROMOSOMES; GENE EXPRESSION;

T-CELLS;

CD4 ANTIGEN; GAMMA INTERFERON; HERMES ANTIGEN; IKAROS TRANSCRIPTION FACTOR; INTERLEUKIN 17 ANTIBODY; INTERLEUKIN 22; INTERLEUKIN 23 RECEPTOR; RETINOID RELATED ORPHAN RECEPTOR GAMMA; T LYMPHOCYTE RECEPTOR BETA CHAIN; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR T BET;

AHR GENE; ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL MATURATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; EPIGENETICS; GENE; GENE EXPRESSION; GENE LOCUS; GENE REPRESSION; HELPER CELL; IL17A GENE; IL22 GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MODIFICATION; RORC GENE; RUNX1 GENE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TH17 CELL; THYMUS;

GENE REGULATION; IMMUNOLOGY; T CELL; TRANSCRIPTION FACTORS; TRANSCRIPTION REGULATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DEATH; CELL LINEAGE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CORE BINDING FACTOR ALPHA 2 SUBUNIT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMATOPOIESIS; HISTONES; IKAROS TRANSCRIPTION FACTOR; INTERLEUKIN-17; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, ARYL HYDROCARBON; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; TRANSCRIPTION FACTORS;

EID: 84890284061     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.481440     Document Type: Article

References (68)

1. Kanno, Y., Vahedi, G., Hirahara, K., Singleton, K., and O'Shea, J. J. (2012) Transcriptional and epigenetic control of T helper cell specification. Molecular mechanisms underlying commitment and plasticity. Annu. Rev. Immunol. 30, 707-731
2. Zhu, J., and Paul, W. E. (2010) Peripheral CD4- T-cell differentiation regulated by networks of cytokines and transcription factors. Immunol. Rev. 238, 247-262
3. Mosmann, T. R., Cherwinski, H., Bond, M. W., Giedlin, M. A., and Coffman, R. L. (1986) Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 136, 2348-2357
4. Harrington, L. E., Mangan, P. R., and Weaver, C. T. (2006) Expanding the effector CD4 T-cell repertoire. The Th17 lineage. Curr. Opin. Immunol. 18, 349-356
5. McGeachy, M. J., and McSorley, S. J. (2012) Microbial-induced Th17. Superhero or supervillain J. Immunol. 189, 3285-3291
6. Bettelli, E., Oukka, M., and Kuchroo, V. K. (2007) T(H)-17 cells in the circle of immunity and autoimmunity. Nat. Immunol. 8, 345-350
7. Langowski, J. L., Zhang, X., Wu, L., Mattson, J. D., Chen, T., Smith, K., Basham, B., McClanahan, T., Kastelein, R. A., and Oft, M. (2006) IL-23 promotes tumour incidence and growth. Nature 442, 461-465
8. Zygmunt, B., and Veldhoen, M. (2011) T helper cell differentiation more than just cytokines. Adv. Immunol. 109, 159-196
9. Kimura, A., Naka, T., and Kishimoto, T. (2007) IL-6-dependent and -independent pathways in the development of interleukin 17-producing T helper cells. Proc. Natl. Acad. Sci. U.S.A. 104, 12099-12104
10. Oukka, M. (2007) Interplay between pathogenic Th17 and regulatory T cells. Ann. Rheum. Dis. 66, (SUPPL. 3) iii87-90
11. Weaver, C. T., Harrington, L. E., Mangan, P. R., Gavrieli, M., and Murphy, K. M. (2006) Th17. An effector CD4 cell lineage with regulatory T cell ties. Immunity 24, 677-688
12. Ivanov, I. I., McKenzie, B. S., Zhou, L., Tadokoro, C. E., Lepelley, A., Lafaille, J. J., Cua, D. J., and Littman, D. R. (2006) The orphan nuclear receptor ROR-t directs the differentiation program of proinflammatory IL-17- T helper cells. Cell 126, 1121-1133
13. 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 ROR- and ROR-. Immunity 28, 29-39
14. Brüstle, A., Heink, S., Huber, M., Rosenplänter, C., Stadelmann, C., Yu, P., Arpaia, E., Mak, T. W., Kamradt, T., and Lohoff, M. (2007) The development of inflammatory T(H)-17 cells requires interferon-regulatory factor Nat. Immunol. 8, 958-966
15. Zhang, F., Meng, G., and Strober, W. (2008) Interactions among the transcription factors Runx1, ROR-t and Foxp3 regulate the differentiation of interleukin 17-producing T cells. Nat. Immunol. 9, 1297-1306
16. Yang, X. O., Panopoulos, A. D., Nurieva, R., Chang, S. H., Wang, D., Watowich, S. S., and Dong, C. (2007) STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. 282, 9358-9363
17. Mudter, J., Yu, J., Zufferey, C., Brüstle, A., Wirtz, S., Weigmann, B., Hoffman, A., Schenk, M., Galle, P. R., Lehr, H. A., Mueller, C., Lohoff, M., and Neurath, M. F. (2011) IRF4 regulates IL-17A promoter activity and controls ROR-t-dependent Th17 colitis in vivo. Inflamm. Bowel Dis. 17, 1343-1358
18. Ito, Y., and Miyazono, K. (2003) RUNX transcription factors as key targets of TGF- superfamily signaling. Curr. Opin. Genet. Dev. 13, 43-47
19. Quintana, F. J., Basso, A. S., Iglesias, A. H., Korn, T., Farez, M. F., Bettelli, E., Caccamo, M., Oukka, M., and Weiner, H. L. (2008) Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 453, 65-71
20. Veldhoen, M., Hirota, K., Westendorf, A. M., Buer, J., Dumoutier, L., Renauld, J. C., and Stockinger, B. (2008) The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453, 106-109
21. Zhou, L., Ivanov, I. I., Spolski, R., Min, R., Shenderov, K., Egawa, T., Levy, D. E., Leonard, W. J., and Littman, D. R. (2007) IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 8, 967-974
22. Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., Sedgwick, J. D., McClanahan, T., Kastelein, R. A., and Cua, D. J. (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201, 233-240
23. Zhou, L., Lopes, J. E., Chong, M. M., Ivanov, I. I., Min, R., Victora, G. D., Shen, Y., Du, J., Rubtsov, Y. P., Rudensky, A. Y., Ziegler, S. F., and Littman, D. R. (2008) TGF-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing ROR-t function. Nature 453, 236-240
24. Nichogiannopoulou, A., Trevisan, M., Friedrich, C., and Georgopoulos, K. (1998) Ikaros in hemopoietic lineage determination and homeostasis. Semin. Immunol. 10, 119-125
25. Koipally, J., Renold, A., Kim, J., and Georgopoulos, K. (1999) Repression by Ikaros and Aiolos is mediated through histone deacetylase complexes. EMBO J. 18, 3090-3100
26. Koipally, J., Kim, J., Jones, B., Jackson, A., Avitahl, N., Winandy, S., Trevisan, M., Nichogiannopoulou, A., Kelley, C., and Georgopoulos, K. (1999) Ikaros chromatin remodeling complexes in the control of differentiation of the hemo-lymphoid system. Cold Spring Harb. Symp. Quant. Biol. 64, 79-86
27. Koipally, J., Heller, E. J., Seavitt, J. R., and Georgopoulos, K. (2002) Unconventional potentiation of gene expression by Ikaros. J. Biol. Chem. 277, 13007-13015
28. Koipally, J., and Georgopoulos, K. (2002) Ikaros-CtIP interactions do not require C-terminal binding protein and participate in a deacetylase-independent mode of repression. J. Biol. Chem. 277, 23143-23149
29. Koipally, J., and Georgopoulos, K. (2002) A molecular dissection of the repression circuitry of Ikaros. J. Biol. Chem. 277, 27697-27705
30. Koipally, J., and Georgopoulos, K. (2000) Ikaros interactions with CtBP reveal a repression mechanism that is independent of histone deacetylase activity. J. Biol. Chem. 275, 19594-19602
31. Winandy, S., Wu, P., and Georgopoulos, K. (1995) A dominant mutation in the Ikaros gene leads to rapid development of leukemia and lymphoma. Cell 83, 289-299
32. Quirion, M. R., Gregory, G. D., Umetsu, S. E., Winandy, S., and Brown, M. A. (2009) Cutting edge. Ikaros is a regulator of Th2 cell differentiation. J. Immunol. 182, 741-745
33. Umetsu, S. E., and Winandy, S. (2009) Ikaros is a regulator of Il10 expression in CD4- T cells. J. Immunol. 183, 5518-5525
34. Thomas, R. M., Chen, C., Chunder, N., Ma, L., Taylor, J., Pearce, E. J., and Wells, A. D. (2010) Ikaros silences T-bet expression and interferon- production during T helper 2 differentiation. J. Biol. Chem. 285, 2545-2553
35. Thomas, R. M., Chunder, N., Chen, C., Umetsu, S. E., Winandy, S., and Wells, A. D. (2007) Ikaros enforces the costimulatory requirement for IL2 gene expression and is required for anergy induction in CD4-T lymphocytes. J. Immunol. 179, 7305-7315
36. Wang, J. H., Nichogiannopoulou, A., Wu, L., Sun, L., Sharpe, A. H., Bigby, M., and Georgopoulos, K. (1996) Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity 5, 537-549
37. Kathrein, K. L., Lorenz, R., Innes, A. M., Griffiths, E., and Winandy, S. (2005) Ikaros induces quiescence and T-cell differentiation in a leukemia cell line. Mol. Cell. Biol. 25, 1645-1654
38. Cortes, M., Wong, E., Koipally, J., and Georgopoulos, K. (1999) Control of lymphocyte development by the Ikaros gene family. Curr. Opin. Immunol. 11, 167-171
39. Urban, J. A., and Winandy, S. (2004) Ikaros null mice display defects in T cell selection and CD4 versus CD8 lineage decisions. J. Immunol. 173, 4470-4478
40. Szabo, S. J., Kim, S. T., Costa, G. L., Zhang, X., Fathman, C. G., and Glimcher, L. H. (2000) A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100, 655-669
41. Lazarevic, V., Chen, X., Shim, J. H., Hwang, E. S., Jang, E., Bolm, A. N., Oukka, M., Kuchroo, V. K., and Glimcher, L. H. (2011) T-bet represses T(H)17 differentiation by preventing Runx1-mediated activation of the gene encoding ROR-t. Nat. Immunol. 12, 96-104
42. Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T. B., Oukka, M., Weiner, H. L., and Kuchroo, V. K. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235-238
43. Fontenot, J. D., Gavin, M. A., and Rudensky, A. Y. (2003) Foxp3 programs the development and function of CD4-CD25- regulatory T cells. Nat. Immunol. 4, 330-336
44. Vermeulen, M., and Timmers, H. T. (2010) Grasping trimethylation of histone H3 at lysine 4. Epigenomics 2, 395-406
45. Ruthenburg, A. J., Allis, C. D., and Wysocka, J. (2007) Methylation of lysine 4 on histone H3. Intricacy of writing and reading a single epigenetic mark. Mol. Cell 25, 15-30
46. Marks, B. R., Nowyhed, H. N., Choi, J. Y., Poholek, A. C., Odegard, J. M., Flavell, R. A., and Craft, J. (2009) Thymic self-reactivity selects natural interleukin 17-producing T cells that can regulate peripheral inflammation. Nat. Immunol. 10, 1125-1132
47. Kim, J. S., Smith-Garvin, J. E., Koretzky, G. A., and Jordan, M. S. (2011) The requirements for natural Th17 cell development are distinct from those of conventional Th17 cells. J. Exp. Med. 208, 2201-2207
48. Wang, Z., Zang, C., Rosenfeld, J. A., Schones, D. E., Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Peng, W., Zhang, M. Q., and Zhao, K. (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40, 897-903
49. Akimzhanov, A. M., Yang, X. O., and Dong, C. (2007) Chromatin remodeling of interleukin-17 (IL-17)-IL-17F cytokine gene locus during inflammatory helper T cell differentiation. J. Biol. Chem. 282, 5969-5972
50. Mukasa, R., Balasubramani, A., Lee, Y. K., Whitley, S. K., Weaver, B. T., Shibata, Y., Crawford, G. E., Hatton, R. D., and Weaver, C. T. (2010) Epigenetic instability of cytokine and transcription factor gene loci underlies plasticity of the T helper 17 cell lineage. Immunity 32, 616-627
51. Zhou, L., and Littman, D. R. (2009) Transcriptional regulatory networks in Th17 cell differentiation. Curr. Opin. Immunol. 21, 146-152
52. Kimura, A., Naka, T., Nohara, K., Fujii-Kuriyama, Y., and Kishimoto, T. (2008) Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc. Natl. Acad. Sci. U.S.A. 105, 9721-9726
53. Quintana, F. J., Jin, H., Burns, E. J., Nadeau, M., Yeste, A., Kumar, D., Rangachari, M., Zhu, C., Xiao, S., Seavitt, J., Georgopoulos, K., and Kuchroo, V. K. (2012) Aiolos promotes TH17 differentiation by directly silencing Il2 expression. Nat. Immunol. 13, 770-777
54. Zúñiga, L. A., Jain, R., Haines, C., and Cua, D. J. (2013) Th17 cell development. From the cradle to the grave. Immunol. Rev. 252, 78-88
55. Kim, J. S., Sklarz, T., Banks, L. B., Gohil, M., Waickman, A. T., Skuli, N., Krock, B. L., Luo, C. T., Hu, W., Pollizzi, K. N., Li, M. O., Rathmell, J. C., Birnbaum, M. J., Powell, J. D., Jordan, M. S., and Koretzky, G. A. (2013) Natural and inducible TH17 cells are regulated differently by Akt and mTOR pathways. Nat. Immunol. 14, 611-618
56. Thornton, A. M., Korty, P. E., Tran, D. Q., Wohlfert, E. A., Murray, P. E., Belkaid, Y., and Shevach, E. M. (2010) Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3- T regulatory cells. J. Immunol. 184, 3433-3441
57. Veldhoen, M., and Duarte, J. H. (2010) The aryl hydrocarbon receptor. Fine-tuning the immune-response. Curr. Opin. Immunol. 22, 747-752
58. Brembilla, N. C., Ramirez, J. M., Chicheportiche, R., Sorg, O., Saurat, J. H., and Chizzolini, C. (2011) In vivo dioxin favors interleukin-22 production by human CD4- T cells in an aryl hydrocarbon receptor (AhR)-dependent manner. PLoS One 6, e18741
59. Ramirez, J. M., Brembilla, N. C., Sorg, O., Chicheportiche, R., Matthes, T., Dayer, J. M., Saurat, J. H., Roosnek, E., and Chizzolini, C. (2010) Activation of the aryl hydrocarbon receptor reveals distinct requirements for IL-22 and IL-17 production by human T helper cells. Eur. J. Immunol. 40, 2450-2459
60. Nakahama, T., Kimura, A., Nguyen, N. T., Chinen, I., Hanieh, H., Nohara, K., Fujii-Kuriyama, Y., and Kishimoto, T. (2011) Aryl hydrocarbon receptor deficiency in T cells suppresses the development of collagen-induced arthritis. Proc. Natl. Acad. Sci. U.S.A. 108, 14222-14227
61. Ono, M., Yaguchi, H., Ohkura, N., Kitabayashi, I., Nagamura, Y., Nomura, T., Miyachi, Y., Tsukada, T., and Sakaguchi, S. (2007) Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 446, 685-689
62. Djuretic, I. M., Levanon, D., Negreanu, V., Groner, Y., Rao, A., and Ansel, K. M. (2007) Transcription factors T-bet and Runx3 cooperate to activate Ifng and silence Il4 in T helper type 1 cells. Nat. Immunol. 8, 145-153
63. Ichiyama, K., Yoshida, H., Wakabayashi, Y., Chinen, T., Saeki, K., Nakaya, M., Takaesu, G., Hori, S., Yoshimura, A., and Kobayashi, T. (2008) Foxp3 inhibits ROR-t-mediated IL-17A mRNA transcription through direct interaction with ROR-t. J. Biol. Chem. 283, 17003-17008
64. Funatake, C. J., Marshall, N. B., Steppan, L. B., Mourich, D. V., and Kerkvliet, N. I. (2005) Cutting edge. Activation of the aryl hydrocarbon receptor by 2,3,7,8-tetrachlorodibenzo-p-dioxin generates a population of CD4- CD25- cells with characteristics of regulatory T cells. J. Immunol. 175, 4184-4188
65. Gandhi, R., Kumar, D., Burns, E. J., Nadeau, M., Dake, B., Laroni, A., Kozoriz, D., Weiner, H. L., and Quintana, F. J. (2010) Activation of the aryl hydrocarbon receptor induces human type 1 regulatory T cell-like and Foxp3- regulatory T cells. Nat. Immunol. 11, 846-853
66. Liao, W., Lin, J. X., Wang, L., Li, P., and Leonard, W. J. (2011) Modulation of cytokine receptors by IL-2 broadly regulates differentiation into helper T cell lineages. Nat. Immunol. 12, 551-559
67. Yang, X. P., Ghoreschi, K., Steward-Tharp, S. M., Rodriguez-Canales, J., Zhu, J., Grainger, J. R., Hirahara, K., Sun, H. W., Wei, L., Vahedi, G., Kanno, Y., O'Shea, J. J., and Laurence, A. (2011) Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat. Immunol. 12, 247-254
68. Laurence, A., Tato, C. M., Davidson, T. S., Kanno, Y., Chen, Z., Yao, Z., Blank, R. B., Meylan, F., Siegel, R., Hennighausen, L., Shevach, E. M., and O'Shea, J. J. (2007) Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26, 371-381