Opposing roles of STAT4 and Dnmt3a in Th1 gene regulation

Journal of Immunology

Volumn 191, Issue 2, 2013, Pages 902-911

  Pham, Duy ^a   Yu, Qing ^a   Walline, Crystal C ^a   Muthukrishnan, Rajarajeswari ^a   Blum, Janice S ^a   Kaplan, Mark H ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 3A; GAMMA INTERFERON; HISTONE H3; STAT4 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HLX1; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL FATE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE LOCUS; GENE LOSS; GENE REPRESSION; GENE TARGETING; GENETIC SUSCEPTIBILITY; GENETIC TRANSCRIPTION; HISTONE METHYLATION; IFNG GENE; JMJD3 GENE; LYMPH NODE CELL; MALE; MOUSE; NONHUMAN; PARALYSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; SPLEEN CELL; T LYMPHOCYTE; TH1 GENE; TRANSACTIVATION;

ANIMALS; CHROMATIN; CORE BINDING FACTOR ALPHA 3 SUBUNIT; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENE EXPRESSION REGULATION; HISTONES; HOMEODOMAIN PROTEINS; INTERFERON-GAMMA; INTERLEUKIN-12; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; METHYLATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, INTERFERON; RNA INTERFERENCE; RNA, SMALL INTERFERING; STAT4 TRANSCRIPTION FACTOR; T-BOX DOMAIN PROTEINS; TH1 CELLS; TRANSCRIPTION FACTORS;

EID: 84880086292     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203229     Document Type: Article

References (52)

1. Kaplan, M. H. 2005. STAT4: a critical regulator of inflammation in vivo. Immunol. Res. 31: 231-242.
2. Watford, W. T., B. D. Hissong, J. H. Bream, Y. Kanno, L. Muul, and J. J. O'Shea. 2004. Signaling by IL-12 and IL-23 and the immunoregulatory roles of STAT4. Immunol. Rev. 202: 139-156. (Pubitemid 39576910)
3. Hsieh, C.-S., S. E. Macatonia, C. S. Tripp, S. F. Wolf, A. O'Garra, and K. M. Murphy. 1993. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science 260: 547-549. (Pubitemid 23161621)
4. Afkarian, M., J. R. Sedy, J. Yang, N. G. Jacobson, N. Cereb, S. Y. Yang, T. L. Murphy, and K. M. Murphy. 2002. T-bet is a STAT1-induced regulator of IL-12R expression in naïve CD4+ T cells. Nat. Immunol. 3: 549-557. (Pubitemid 34662307)
5. Wenner, C. A., M. L. Güler, S. E. Macatonia, A. O'Garra, and K. M. Murphy. 1996. Roles of IFN-γ and IFN-α in IL-12-induced T helper cell-1 development. J. Immunol. 156: 1442-1447.
6. Kaplan, M. H., Y.-L. Sun, T. Hoey, and M. J. Grusby. 1996. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature 382: 174-177. (Pubitemid 26242885)
7. Thierfelder, W. E., J. M. van Deursen, K. Yamamoto, R. A. Tripp, S. R. Sarawar, R. T. Carson, M. Y. Sangster, D. A. A. Vignali, P. C. Doherty, G. C. Grosveld, and J. N. Ihle. 1996. Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cells. Nature 382: 171-174. (Pubitemid 26242884)
8. Yang, Y., J. C. Ochando, J. S. Bromberg, and Y. Ding. 2007. Identification of a distant T-bet enhancer responsive to IL-12/Stat4 and IFNgamma/Stat1 signals. Blood 110: 2494-2500. (Pubitemid 47523171)
9. Lighvani, A. A., D. M. Frucht, D. Jankovic, H. Yamane, J. Aliberti, B. D. Hissong, B. V. Nguyen, M. Gadina, A. Sher, W. E. Paul, and J. J. O'Shea. 2001. T-bet is rapidly induced by interferon-gamma in lymphoid and myeloid cells. Proc. Natl. Acad. Sci. USA 98: 15137-15142. (Pubitemid 34013982)
10. Schulz, E. G., L. Mariani, A. Radbruch, and T. Höfer. 2009. Sequential polarization and imprinting of type 1 T helper lymphocytes by interferon-gamma and interleukin-12. Immunity 30: 673-683.
11. Thieu, V. T., Q. Yu, H. C. Chang, N. Yeh, E. T. Nguyen, S. Sehra, and M. H. Kaplan. 2008. Signal transducer and activator of transcription 4 is required for the transcription factor T-bet to promote T helper 1 cell-fate determination. Immunity 29: 679-690.
12. Djuretic, I. M., D. Levanon, V. Negreanu, Y. Groner, A. Rao, and K. M. Ansel. 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. (Pubitemid 46152645)
13. Mullen, A. C., A. S. Hutchins, F. A. High, H. W. Lee, K. J. Sykes, L. A. Chodosh, and S. L. Reiner. 2002. Hlx is induced by and genetically interacts with T-bet to promote heritable T(H)1 gene induction. Nat. Immunol. 3: 652-658. (Pubitemid 34752474)
14. Yu, Q., V. T. Thieu, and M. H. Kaplan. 2007. Stat4 limits DNA methyltransferase recruitment and DNA methylation of the IL-18Ralpha gene during Th1 differentiation. EMBO J. 26: 2052-2060. (Pubitemid 46625788)
15. Yu, Q., B. Zhou, Y. Zhang, E. T. Nguyen, J. Du, N. L. Glosson, and M. H. Kaplan. 2012. DNA methyltransferase 3a limits the expression of interleukin-13 in T helper 2 cells and allergic airway inflammation. Proc. Natl. Acad. Sci. USA 109: 541-546.
16. Pekowska, A., T. Benoukraf, J. Zacarias-Cabeza, M. Belhocine, F. Koch, H. Holota, J. Imbert, J. C. Andrau, P. Ferrier, and S. Spicuglia. 2011. H3K4 trimethylation provides an epigenetic signature of active enhancers. EMBO J. 30: 4198-4210.
17. Kouzarides, T. 2007. SnapShot: histone-modifying enzymes. Cell 131: 822.
18. Allis, C. D., S. L. Berger, J. Cote, S. Dent, T. Jenuwien, T. Kouzarides, L. Pillus, D. Reinberg, Y. Shi, R. Shiekhattar, et al. 2007. New nomenclature for chromatin-modifying enzymes. Cell 131: 633-636. (Pubitemid 350089969)
19. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128: 693-705. (Pubitemid 46273577)
20. Shahbazian, M. D., and M. Grunstein. 2007. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76: 75-100.
21. Good, S. R., V. T. Thieu, A. N. Mathur, Q. Yu, G. L. Stritesky, N. Yeh, J. T. O'Malley, N. B. Perumal, and M. H. Kaplan. 2009. Temporal induction pattern of STAT4 target genes defines potential for Th1 lineage-specific programming. J. Immunol. 183: 3839-3847.
22. Wei, L., G. Vahedi, H. W. Sun, W. T. Watford, H. Takatori, H. L. Ramos, H. Takahashi, J. Liang, G. Gutierrez-Cruz, C. Zang, et al. 2010. Discrete roles of STAT4 and STAT6 transcription factors in tuning epigenetic modifications and transcription during T helper cell differentiation. Immunity 32: 840-851.
23. O'Sullivan, A., H. C. Chang, Q. Yu, and M. H. Kaplan. 2004. STAT4 is required for interleukin-12-induced chromatin remodeling of the CD25 locus. J. Biol. Chem. 279: 7339-7345. (Pubitemid 38248884)
24. Yu, Q., H. C. Chang, A. N. Ahyi, and M. H. Kaplan. 2008. Transcription factor-dependent chromatin remodeling of Il18r1 during Th1 and Th2 differentiation. J. Immunol. 181: 3346-3352.
25. Letimier, F. A., N. Passini, S. Gasparian, E. Bianchi, and L. Rogge. 2007. Chromatin remodeling by the SWI/SNF-like BAF complex and STAT4 activation synergistically induce IL-12Rbeta2 expression during human Th1 cell differentiation. EMBO J. 26: 1292-1302. (Pubitemid 46398709)
26. Zhang, F., and M. Boothby. 2006. T helper type 1-specific Brg1 recruitment and remodeling of nucleosomes positioned at the IFN-gamma promoter are Stat4 dependent. J. Exp. Med. 203: 1493-1505. (Pubitemid 43877611)
27. Vahedi, G., H. Takahashi, S. Nakayamada, H. W. Sun, V. Sartorelli, Y. Kanno, and J. J. O'Shea. 2012. STATs shape the active enhancer landscape of T cell populations. Cell 151: 981-993.
28. Gamper, C. J., A. T. Agoston, W. G. Nelson, and J. D. Powell. 2009. Identification of DNA methyltransferase 3a as a T cell receptor-induced regulator of Th1 and Th2 differentiation. J. Immunol. 183: 2267-2276.
29. Thomas, R. M., C. J. Gamper, B. H. Ladle, J. D. Powell, and A. D. Wells. 2012. De novo DNA methylation is required to restrict T helper lineage plasticity. J. Biol. Chem. 287: 22900-22909.
30. Mo, C., W. Chearwae, J. T. O'Malley, S. M. Adams, S. Kanakasabai, C. C. Walline, G. L. Stritesky, S. R. Good, N. B. Perumal, M. H. Kaplan, and J. J. Bright. 2008. Stat4 isoforms differentially regulate inflammation and demyelination in experimental allergic encephalomyelitis. J. Immunol. 181: 5681-5690.
31. Chang, H. C., S. Zhang, V. T. Thieu, R. B. Slee, H. A. Bruns, R. N. Laribee, M. J. Klemsz, and M. H. Kaplan. 2005. PU.1 expression delineates heterogeneity in primary Th2 cells. Immunity 22: 693-703. (Pubitemid 40814500)
32. Mathur, A. N., H. C. Chang, D. G. Zisoulis, R. Kapur, M. L. Belladonna, G. S. Kansas, and M. H. Kaplan. 2006. T-bet is a critical determinant in the instability of the IL-17-secreting T-helper phenotype. Blood 108: 1595-1601. (Pubitemid 44316127)
33. Pham, D., J. W. Vincentz, A. B. Firulli, and M. H. Kaplan. 2012. Twist1 regulates Ifng expression in Th1 cells by interfering with Runx3 function. J. Immunol. 189: 832-840.
34. Chang, S., and T. M. Aune. 2007. Dynamic changes in histone-methylation 'marks' across the locus encoding interferon-gamma during the differentiation of T helper type 2 cells. Nat. Immunol. 8: 723-731. (Pubitemid 46965348)
35. Schoenborn, J. R., M. O. Dorschner, M. Sekimata, D. M. Santer, M. Shnyreva, D. R. Fitzpatrick, J. A. Stamatoyannopoulos, and C. B. Wilson. 2007. Comprehensive epigenetic profiling identifies multiple distal regulatory elements directing transcription of the gene encoding interferon-gamma. [Published erratum appears in 2007 Nat. Immunol. 8: 893 and 2008 Nat. Immunol. 9: 105.] Nat. Immunol. 8: 732-742. (Pubitemid 46965349)
36. Wei, G., L. Wei, J. Zhu, C. Zang, J. Hu-Li, Z. Yao, K. Cui, Y. Kanno, T. Y. Roh, W. T. Watford, et al. 2009. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30: 155-167.
37. Li, J. Y., M. T. Pu, R. Hirasawa, B. Z. Li, Y. N. Huang, R. Zeng, N. H. Jing, T. Chen, E. Li, H. Sasaki, and G. L. Xu. 2007. Synergistic function of DNA methyltransferases Dnmt3a and Dnmt3b in the methylation of Oct4 and Nanog. Mol. Cell. Biol. 27: 8748-8759.
38. Otani, J., T. Nankumo, K. Arita, S. Inamoto, M. Ariyoshi, and M. Shirakawa. 2009. Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep. 10: 1235-1241.
39. Chen, S., J. Ma, F. Wu, L. J. Xiong, H. Ma, W. Xu, R. Lv, X. Li, J. Villen, S. P. Gygi, et al. 2012. The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation. Genes Dev. 26: 1364-1375.
40. Zhang, Y., R. Jurkowska, S. Soeroes, A. Rajavelu, A. Dhayalan, I. Bock, P. Rathert, O. Brandt, R. Reinhardt, W. Fischle, and A. Jeltsch. 2010. Chromatin methylation activity of Dnmt3a and Dnmt3a/3L is guided by interaction of the ADD domain with the histone H3 tail. Nucleic Acids Res. 38: 4246-4253.
41. Chitnis, T., N. Najafian, C. Benou, A. D. Salama, M. J. Grusby, M. H. Sayegh, and S. J. Khoury. 2001. Effect of targeted disruption of STAT4 and STAT6 on the induction of experimental autoimmune encephalomyelitis. J. Clin. Invest. 108: 739-747. (Pubitemid 32906203)
42. Miller, S. A., S. E. Mohn, and A. S. Weinmann. 2010. Jmjd3 and UTX play a demethylase-independent role in chromatin remodeling to regulate T-box family member-dependent gene expression. Mol. Cell 40: 594-605.
43. Pierson, E., S. B. Simmons, L. Castelli, and J. M. Goverman. 2012. Mechanisms regulating regional localization of inflammation during CNS autoimmunity. Immunol. Rev. 248: 205-215.
44. Lal, G., N. Zhang, W. van der Touw, Y. Ding, W. Ju, E. P. Bottinger, S. P. Reid, D. E. Levy, and J. S. Bromberg. 2009. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J. Immunol. 182: 259-273.
45. O'Malley, J. T., S. Sehra, V. T. Thieu, Q. Yu, H. C. Chang, G. L. Stritesky, E. T. Nguyen, A. N. Mathur, D. E. Levy, and M. H. Kaplan. 2009. Signal transducer and activator of transcription 4 limits the development of adaptive regulatory T cells. Immunology 127: 587-595.
46. Bacon, C. M., E. F. Petricoin, III, J. R. Ortaldo, R. C. Rees, A. C. Larner, J. A. Johnston, and J. J. O'Shea. 1995. Interleukin 12 induces tyrosine phosphorylation and activation of STAT4 in human lymphocytes. Proc. Natl. Acad. Sci. USA 92: 7307-7311.
47. Jacobson, N. G., S. J. Szabo, R. M. Weber-Nordt, Z. Zhong, R. D. Schreiber, J. E. Darnell, Jr., and K. M. Murphy. 1995. Interleukin 12 signaling in T helper type 1 (Th1) cells involves tyrosine phosphorylation of signal transducer and activator of transcription (Stat)3 and Stat4. J. Exp. Med. 181: 1755-1762.
48. Nakahira, M., H. J. Ahn, W. R. Park, P. Gao, M. Tomura, C. S. Park, T. Hamaoka, T. Ohta, M. Kurimoto, and H. Fujiwara. 2002. Synergy of IL-12 and IL-18 for IFN-gamma gene expression: IL-12-induced STAT4 contributes to IFN-gamma promoter activation by up-regulating the binding activity of IL-18-induced activator protein 1. J. Immunol. 168: 1146-1153. (Pubitemid 34094479)
49. Tanaka, T., M. A. Soriano, and M. J. Grusby. 2005. SLIM is a nuclear ubiquitin E3 ligase that negatively regulates STAT signaling. Immunity 22: 729-736. (Pubitemid 40814503)
50. Nakahira, M., T. Tanaka, B. E. Robson, J. P. Mizgerd, and M. J. Grusby. 2007. Regulation of signal transducer and activator of transcription signaling by the tyrosine phosphatase PTP-BL. Immunity 26: 163-176. (Pubitemid 46329438)
51. Niesner, U., I. Albrecht, M. Janke, C. Doebis, C. Loddenkemper, M. H. Lexberg, K. Eulenburg, S. Kreher, J. Koeck, R. Baumgrass, et al. 2008. Autoregulation of Th1-mediated inflammation by twist1. J. Exp. Med. 205: 1889-1901.
52. Miller, S. A., A. C. Huang, M. M. Miazgowicz, M. M. Brassil, and A. S. Weinmann. 2008. Coordinated but physically separable interaction with H3K27-demethylase and H3K4-methyltransferase activities are required for T-box protein-mediated activation of developmental gene expression. Genes Dev. 22: 2980-2993.