Epigenetic regulation of cytokine gene expression in T lymphocytes

Yonsei Medical Journal

Volumn 50, Issue 3, 2009, Pages 322-330

  Lee, Choong Gu ^a   Sahoo, Anupama ^a   Im, Sin Hyeog ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

Author keywords

Cytokine; Epigenetics; Gene regulation; T lymphocytes

Indexed keywords

CYTOKINE; DNA METHYLTRANSFERASE; GAMMA INTERFERON; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE METHYLTRANSFERASE; IMMUNOGLOBULIN E; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; LYMPHOTOXIN; STAT3 PROTEIN; STAT4 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR ROR GAMMA T; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ACETYLATION; ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL LINEAGE; CELL MATURATION; CELLULAR IMMUNITY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CPG ISLAND; CYTOKINE PRODUCTION; DNA METHYLATION; DNA MODIFICATION; EFFECTOR CELL; EPIGENETICS; GENE EXPRESSION REGULATION; GENE LOCUS; HELPER CELL; HOMEOSTASIS; HUMAN; HUMORAL IMMUNITY; LYMPHOCYTE DIFFERENTIATION; MACROPHAGE ACTIVATION; NONHUMAN; PHENOTYPE; PROMOTER REGION; PROTEIN METHYLATION; PROTEIN PROCESSING; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; TH2 CELL; TRANSCRIPTION REGULATION;

ANIMALS; CYTOKINES; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HUMANS; T-LYMPHOCYTES;

EID: 67651152840     PISSN: 05135796     EISSN: None     Source Type: Journal    
DOI: 10.3349/ymj.2009.50.3.322     Document Type: Review

References (100)

1. Ansel KM, Lee DU, Rao A. An epigenetic view of helper T cell differentiation. Nat Immunol 2003;4:616-23.
2. Hsieh CS, Macatonia SE, Tripp CS, Wolf SF, O'Garra A, Murphy KM. Development of TH1 CD4 + T cells through IL-12 produced by Listeria-induced macrophages. Science 1993;260:547-9.
3. Kaplan MH, Sun YL, Hoey T, Grusby MJ. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature 1996;382:174-7.
4. Thierfelder WE, van Deursen JM, Yamamoto K, Tripp RA, Sarawar SR, Carson RT, et al. Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cells. Nature 1996;382:171-4.
5. Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 2000;100:655-69.
6. Szabo SJ, Sullivan BM, Stemmann C, Satoskar AR, Sleckman BP, Glimcher LH. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 2002;295:338-42.
7. Afkarian M, Sedy JR, Yang J, Jacobson NG, Cereb N, Yang SY, et al. T-bet is a STAT1-induced regulator of IL-12R expression in naïve CD4+ T cells. Nat Immunol 2002;3:549-57.
8. Lighvani AA, Frucht DM, Jankovic D, Yamane H, Aliberti J, Hissong BD, et al. T-bet is rapidly induced by interferon-gamma in lymphoid and myeloid cells. Proc Natl Acad Sci U S A 2001;98: 15137-42.
9. Shi M, Lin TH, Appell KC, Berg LJ. Janus-kinase-3-dependent signals induce chromatin remodeling at the lfng locus during T helper 1 cell differentiation. Immunity 2008;28:763-73.
10. Abbas AK, Murphy KM, Sher A. Functional diversity of helper T lymphocytes. Nature 1996;383:787-93.
11. Paul WE, Seder RA. Lymphocyte responses and cytokines. Cell 1994;76:241-51.
12. Romagnani S. Lymphokine production by human T cells in disease states. Annu Rev Immunol 1994;12:227-57.
13. Sher A, Coffman RL. Regulation of immunity to parasites by T cells and T cell-derived cytokines. Annu Rev Immunol 1992;10: 385-409.
14. Swain SL, Weinberg AD, English M, Huston G. IL-4 directs the development of Th2-like helper effectors. J Immunol 1990;145: 3796-806.
15. Kaplan MH, Schindler U, Smiley ST, Grusby MJ. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 1996;4:313-9.
16. Kurata H, Lee HJ, O'Garra A, Arai N. Ectopic expression of activated Stat6 induces the expression of Th2-specific cytokines and transcription factors in developing Th1 cells. Immunity 1999; 11:677-88.
17. Lee HJ, Takemoto N, Kurata H, Kamogawa Y, Miyatake S, O'Garra A, et al. GATA-3 induces T helper cell type 2 (Th2) cytokine expression and chromatin remodeling in committed Th1 cells. J Exp Med 2000;192:105-15.
18. Shimoda K, van Deursen J, Sangster MY, Sarawar SR, Carson RT, Tripp RA, et al. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 1996; 380:630-3.
19. Takeda K, Tanaka T, Shi W, Matsumoto M, Minami M, Kashiwamura S, et al. Essential role of Stat6 in IL-4 signalling. Nature 1996;380:627-30.
20. Kim JI, Ho IC, Grusby MJ, Glimcher LH. The transcription factor c-Maf controls the production of interleukin-4 but not other Th2 cytokines. Immunity 1999;10:745-51.
21. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005;201:233-40.
22. Ivanov, II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006;126:1121-33.
23. Yang XO, Panopoulos AD, Nurieva R, Chang SH, Wang D, Watowich SS, et al. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem 2007;282:9358-63.
24. Yang XO, Pappu BP, Nurieva R, Akimzhanov A, Kang HS, Chung Y, et al. T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma. Immunity 2008;28:29-39.
25. Ouyang W, Kolls JK, Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008; 28:454-67.
26. Sakaguchi S; Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995;155:1151-64.
27. Sakaguchi S. Regulatory T cells: key controllers of immunologic self-tolerance. Cell 2000;101:455-8.
28. Fontenot JD, Rudensky AY. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 2005;6:331-7.
29. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003;299: 1057-61.
30. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA, et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 2001;27:68-73.
31. Gambineri E, Torgerson TR, Ochs HD. Immune dysregulation, polyendocrinopathy, enteropathy, and X-linked inheritance (IPEX), a syndrome of systemic autoimmunity caused by mutations of FOXP3, a critical regulator of T-cell homeostasis. Curr Opin Rheumatol 2003;15:430-5.
32. Roncarolo MG, Bacchetta R, Bordignon C, Narula S, Levings MK. Type 1 T regulatory cells. Immunol Rev 2001;182:68-79.
33. Roncarolo MG, Gregori S, Battaglia M, Bacchetta R, Fleischhauer K, Levings MK. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006;212:28-50.
34. Weiner HL. Oral tolerance: immune mechanisms and the generation of Th3-type TGF-beta-secreting regulatory cells. Microbes Infect 2001;3:947-54.
35. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002;16:6-21.
36. Illingworth R, Kerr A, Desousa D, Jorgensen H, Ellis P, Stalker J, et al. A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol 2008;6:e22.
37. Miranda TB, Jones PA. DNA methylation: the nuts and bolts of repression. J Cell Physiol 2007;213:384-90.
38. Delcuve GP, Rastegar M, Davie JR. Epigenetic control. J Cell Physiol 2009;219:243-50.
39. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 2002;3:662-73.
40. Feng Q, Zhang Y. The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev 2001;15:827-32.
41. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 1998;19:187-91.
42. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998;393:386-8.
43. Ng HH, Zhang Y, Hendrich B, Johnson CA, Turner BM, Erdjument-Bromage H, et al. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat Genet 1999;23:58-61.
44. Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, Bird A, Reinberg D. Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev 1999;13:1924-35.
45. Bruniquel D, Schwartz RH. Selective, stable demethylation of the interleukin-2 gene enhances transcription by an active process. Nat Immunol 2003;4:235-40.
46. Ooi SK, Bestor TH. The colorful history of active DNA demethylation. Cell 2008;133:1145-8.
47. Kouzarides T. Chromatin modifications and their function. Cell 2007;128:693-705.
48. Munshi A, Shafi G, Aliya N, Jyothy A. Histone modifications dictate specific biological readouts. J Genet Genomics 2009;36:75-88.
49. Min-Hao Kuo CDA. Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays 1998;20:615-26.
50. Roth SY, Denu JM, Allis CD. Histone acetyltransferases. Annu Rev Biochem 2001;70:81-120.
51. Robinson PJ, An W, Routh A, Martino F, Chapman L, Roeder RG, et al. 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction. J Mol Biol 2008; 381:816-25.
52. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007;447:407-12.
53. Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293:1074-80.
54. Jenuwein T. Re-SET-ting heterochromatin by histone methyltransferases. Trends Cell Biol 2001;11:266-73.
55. Cosgrove MS, Boeke JD, Wolberger C. Regulated nucleosome mobility and the histone code. Nat Struct Mol Biol 2004;11:1037-43.
56. Cosgrove MS, Wolberger C. How does the histone code work? Biochem Cell Biol 2005;83:468-76.
57. Peterson CL, Laniel MA. Histones and histone modifications. Curr Biol 2004;14:R546-51.
58. Sims RJ 3rd, Reinberg D. Histone H3 Lys 4 methylation: caught in a bind? Genes Dev 2006;20:2779-86.
59. Strähle U, Rastegar S. Conserved non-coding sequences and transcriptional regulation. Brain Res Bull 2008;75:225-30.
60. Janson PC, Winerdal ME, Winqvist O. At the crossroads of T helper lineage commitment-Epigenetics points the way. Biochim Biophys Acta 2008 Dec 30. [Epub ahead of print].
61. Kadonaga JT. Regulation of RNA polymerase II transcription by sequence-specific DNA binding factors. Cell 2004;116:247-57.
62. Hardison RC. Conserved noncoding sequences are reliable guides to regulatory elements. Trends Genet 2000;16:369-72.
63. Lee GR, Fields PE, Griffin TJ, Flavell RA. Regulation of the Th2 cytokine locus by a locus control region. Immunity 2003;19:145-53.
64. West AG, Fraser P. Remote control of gene transcription. Hum Mol Genet 2005;14:R101-11.
65. Grogan JL, Mohrs M, Harmon B, Lacy DA, Sedat JW, Locksley RM. Early transcription and silencing of cytokine genes underlie polarization of T helper cell subsets. Immunity 2001;14:205-15.
66. Avni O, Lee D, Macian F, Szabo SJ, Glimcher LH, Rao A. T (H) cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes. Nat Immunol 2002;3:643-51.
67. Murphy KM, Reiner SL. The lineage decisions of helper T cells. Nat Rev Immunol 2002;2:933-44.
68. Schoenborn JR, Dorschner MO, Sekimata M, Santer DM, Shnyreva M, Fitzpatrick DR, et al. Comprehensive epigenetic profiling identifies multiple distal regulatory elements directing transcription of the gene encoding interferon-gamma. Nat Immunol 2007;8: 732-42.
69. Jones B, Chen J. Inhibition of IFN-gamma transcription by site-specific methylation during T helper cell development. EMBO J 2006;25:2443-52.
70. Agarwal S, Rao A. Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 1998;9:765-75.
71. Lee DU, Avni O, Chen L, Rao A. A distal enhancer in the interferon-gamma (IFN-gamma) locus revealed by genome sequence comparison. J Biol Chem 2004;279:4802-10.
72. Shnyreva M, Weaver WM, Blanchette M, Taylor SL, Tompa M, Fitzpatrick DR, et al. Evolutionarily conserved sequence elements that positively regulate IFN-gamma expression in T cells. Proc Natl Acad Sci U S A 2004;101:12622-7.
73. Chang S, Aune TM. Dynamic changes in histone-methylation 'marks' across the locus encoding interferon-gamma during the differentiation of T helper type 2 cells. Nat Immunol 2007;8:723-31.
74. Zhang F, Boothby M. T helper type 1-specific Brg1 recruitment and remodeling of nucleosomes positioned at the IFN-gamma promoter are Stat4 dependent. J Exp Med 2006;203:1493-505.
75. Fields PE, Kim ST, Flavell RA. Cutting edge: changes in histone acetylation at the IL-4 and IFN-gamma loci accompany Th1/Th2 differentiation. J Immunol 2002;169:647-50.
76. Mullen AC, High FA, Hutchins AS, Lee HW, Villarino AV, Livingston DM, et al. Role of T-bet in commitment of TH1 cells before IL-12-dependent selection. Science 2001;292:1907-10.
77. Tong Y, Aune T, Boothby M. T-bet antagonizes mSin3a recruitment and transactivates a fully methylated IFN-gamma promoter via a conserved T-box half-site. Proc Natl Acad Sci U S A 2005;102: 2034-9.
78. Miller SA, Huang AC, Miazgowicz MM, Brassil MM, Weinmann AS. 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 2008;22:2980-93.
79. Lee GR, Kim ST, Spilianakis CG, Fields PE, Flavell RA. T helper cell differentiation: regulation by cis elements and epigenetics. Immunity 2006;24:369-79.
80. Bird JJ, Brown DR, Mullen AC, Moskowitz NH, Mahowald MA, Sider JR, et al. Helper T cell differentiation is controlled by the cell cycle. Immunity 1998;9:229-37.
81. Hutchins AS, Mullen AC, Lee HW, Sykes KJ, High FA, Hendrich BD, et al. Gene silencing quantitatively controls the function of a developmental trans-activator. Mol Cell 2002;10:81-91.
82. Fields PE, Lee GR, Kim ST, Bartsevich VV, Flavell RA. Th2-specific chromatin remodeling and enhancer activity in the Th2 cytokine locus control region. Immunity 2004;21:865-76.
83. Lee DU, Rao A. Molecular analysis of a locus control region in the T helper 2 cytokine gene cluster: a target for STAT6 but not GATA3. Proc Natl Acad Sci U S A 2004;101:16010-5.
84. Baguet A, Bix M. Chromatin landscape dynamics of the Il4-Il13 locus during T helper 1 and 2 development. Proc Natl Acad Sci U S A 2004;101:11410-5.
85. Koyanagi M, Baguet A, Martens J, Margueron R, Jenuwein T, Bix M. EZH2 and histone 3 trimethyl lysine 27 associated with Il4 and Il13 gene silencing in Th1 cells. J Biol Chem 2005;280:31470-7.
86. Wilson CB, Rowell E, Sekimata M. Epigenetic control of T-helper-cell differentiation. Nat Rev Immunol 2009;9:91-105.
87. Jones EA, Flavell RA. Distal enhancer elements transcribe intergenic RNA in the IL-10 family gene cluster. J Immunol 2005;175:7437-46.
88. Lee CG, Kang KH, So JS, Kwon HK, Son JS, Song MK, et al. A distal cis-regulatory element, CNS-9, controls NFAT1 and IRF4-mediated IL-10 gene activation in T helper cells. Mol Immunol 2008;46:613-21
89. Im SH, Hueber A, Monticelli S, Kang KH, Rao A. Chromatin-level regulation of the IL 10 gene in T cells. J Biol Chem 2004; 279:46818-25.
90. Wang ZY, Sato H, Kusam S, Sehra S, Toney LM, Dent AL. Regulation of IL-10 gene expression in Th2 Cells by Jun proteins. J Immunol 2005;174:2098-105.
91. Chang HD, Helbig C, Tykocinski L, Kreher S, Koeck J, Niesner U, et al. Expression of IL-10 in Th memory lymphocytes is conditional on IL-12 or IL-4, unless the IL-10 gene is imprinted by GATA-3. Eur J Immunol 2007;37:807-17.
92. Shoemaker J, Saraiva M, O'Garra A. GATA-3 directly remodels the IL-10 locus independently of IL-4 in CD4+ T cells. J Immunol 2006;176:3470-9.
93. Ivanov, II, Zhou L, Littman DR. Transcriptional regulation of Th17 cell differentiation. Semin Immunol 2007;19:409-17.
94. Akimzhanov AM, Yang XO, Dong C. Chromatin remodeling of interleukin-17 (IL-17)-IL-17F cytokine gene locus during inflammatory helper T cell differentiation. J Biol Chem 2007;282:5969-72.
95. Wei L, Laurence A, Elias KM, O'Shea JJ. IL-21 is produced by Th17 cells and drives IL-17 production in a STAT3-dependent manner. J Biol Chem 2007;282:34605-10.
96. Floess S, Freyer J, Siewert C, Baron U, Olek S, Polansky J, et al. Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol 2007;5:e38.
97. Kim HP, Leonard WJ. CREB/ATF-dependent T cell receptor-induced FoxP3 gene expression: a role for DNA methylation. J Exp Med 2007;204:1543-51.
98. Polansky JK, Kretschmer K, Freyer J, Floess S, Garbe A, Baron U, et al. DNA methylation controls Foxp3 gene expression. Eur J Immunol 2008;38:1654-63.
99. Lal G, Zhang N, van der Touw W, Ding Y, Ju W, Bottinger EP, et al. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J Immunol 2009;182:259-73.
100. Tone Y, Furuuchi K, Kojima Y, Tykocinski ML, Greene MI, Tone M. Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nat Immunol 2007;9:194-202.