Deciphering the epigenetic code of T lymphocytes

Immunological Reviews

Volumn 261, Issue 1, 2014, Pages 50-61

  Allan, Rhys S ^a,b   Nutt, Stephen L ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Epigenetic; Gene expression; Histone modification; T cell

Indexed keywords

TRANSCRIPTION FACTOR;

ARTICLE; CELL COMPARTMENTALIZATION; CELL DIVISION; CELL LINEAGE; CHROMATIN; EPIGENETICS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HERITABILITY; HISTONE MODIFICATION; HUMAN; IMMUNOMODULATION; IMMUNOPATHOLOGY; INFLAMMATORY DISEASE; LYMPHOCYTE DIFFERENTIATION; LYMPHOMA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE; THYMUS; ANIMAL; BIOLOGICAL THERAPY; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETIC EPIGENESIS; GENETICS; HISTONE CODE; IMMUNE SYSTEM DISEASES; IMMUNOLOGY; PHYSIOLOGY; TRENDS;

ANIMALS; BIOLOGICAL THERAPY; CELL DIFFERENTIATION; CELL LINEAGE; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HISTONE CODE; HUMANS; IMMUNE SYSTEM DISEASES; LYMPHOMA; T-LYMPHOCYTES;

EID: 84905984340     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12207     Document Type: Article

References (148)

1. Ptashne M. On the use of the word 'epigenetic'. Curr Biol 2007;17:R233-R236.
2. Bird JJ, et al. Helper T cell differentiation is controlled by the cell cycle. Immunity 1998;9:229-237.
3. 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;14:205-215.
4. Richter A, Lohning M, Radbruch A. Instruction for cytokine expression in T helper lymphocytes in relation to proliferation and cell cycle progression. J Exp Med 1999;190:1439-1450.
5. Murphy KM, Stockinger B. Effector T cell plasticity: flexibility in the face of changing circumstances. Nat Immunol 2010;11:674-680.
6. O'Shea JJ, Paul WE. Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science 2010;327:1098-1102.
7. Smale ST. The establishment and maintenance of lymphocyte identity through gene silencing. Nat Immunol 2003;4:607-615.
8. Wilson CB, Rowell E, Sekimata M. Epigenetic control of T-helper-cell differentiation. Nat Rev Immunol 2009;9:91-105.
9. Han M, Grunstein M. Nucleosome loss activates yeast downstream promoters in vivo. Cell 1988;55:1137-1145.
10. Jenuwein T, Allis CD. Translating the histone code. Science 2001;293:1074-1080.
11. Suganuma T, Workman JL. Crosstalk among histone modifications. Cell 2008;135:604-607.
12. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000;403:41-45.
13. Barski A, et al. High-resolution profiling of histone methylations in the human genome. Cell 2007;129:823-837.
14. Wang Z, et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 2008;40:897-903.
15. Cairns BR. The logic of chromatin architecture and remodelling at promoters. Nature 2009;461:193-198.
16. Schones DE, Zhao K. Genome-wide approaches to studying chromatin modifications. Nat Rev Genet 2008;9:179-191.
17. Valouev A, Johnson SM, Boyd SD, Smith CL, Fire AZ, Sidow A. Determinants of nucleosome organization in primary human cells. Nature 2011;474:516-520.
18. Soboleva TA, Nekrasov M, Ryan DP, Tremethick DJ. Histone variants at the transcription start-site. Trends Genet 2014;30:199-209.
19. Talbert PB, Henikoff S. Histone variants-ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 2010;11:264-275.
20. Agarwal S, Rao A. Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 1998;9:765-775.
21. Boyle AP, et al. High-resolution mapping and characterization of open chromatin across the genome. Cell 2008;132:311-322.
22. Allfrey VG, Faulkner R, Mirsky AE. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci USA 1964;51:786-794.
23. Ren Q, Gorovsky MA. Histone H2A.Z acetylation modulates an essential charge patch. Mol Cell 2001;7:1329-1335.
24. Marmorstein R, Berger SL. Structure and function of bromodomains in chromatin-regulating complexes. Gene 2001;272:1-9.
25. 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;3:643-651.
26. Araki Y, Fann M, Wersto R, Weng NP. Histone acetylation facilitates rapid and robust memory CD8 T cell response through differential expression of effector molecules (eomesodermin and its targets: perforin and granzyme B). J Immunol 2008;180:8102-8108.
27. Dispirito JR, Shen H. Histone acetylation at the single-cell level: a marker of memory CD8+ T cell differentiation and functionality. J Immunol 2010;184:4631-4636.
28. Fann M, et al. Histone acetylation is associated with differential gene expression in the rapid and robust memory CD8(+) T-cell response. Blood 2006;108:3363-3370.
29. Northrop JK, Wells AD, Shen H. Cutting edge: chromatin remodeling as a molecular basis for the enhanced functionality of memory CD8 T cells. J Immunol 2008;181:865-868.
30. Northrop JK, Thomas RM, Wells AD, Shen H. Epigenetic remodeling of the IL-2 and IFN-gamma loci in memory CD8 T cells is influenced by CD4 T cells. J Immunol 2006;177:1062-1069.
31. Denton AE, Russ BE, Doherty PC, Rao S, Turner SJ. Differentiation-dependent functional and epigenetic landscapes for cytokine genes in virus-specific CD8+ T cells. Proc Natl Acad Sci USA 2011;108:15306-15311.
32. Roh TY, Cuddapah S, Zhao K. Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev 2005;19:542-552.
33. Roth SY, Denu JM, Allis CD. Histone acetyltransferases. Annu Rev Biochem 2001;70:81-120.
34. Heintzman ND, et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 2007;39:311-318.
35. Visel A, et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009;457:854-858.
36. Wang Z, et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009;138:1019-1031.
37. Agalioti T, Chen G, Thanos D. Deciphering the transcriptional histone acetylation code for a human gene. Cell 2002;111:381-392.
38. Cho H, et al. A human RNA polymerase II complex containing factors that modify chromatin structure. Mol Cell Biol 1998;18:5355-5363.
39. Iizuka M, Stillman B. Histone acetyltransferase HBO1 interacts with the ORC1 subunit of the human initiator protein. J Biol Chem 1999;274:23027-23034.
40. Taunton J, Hassig CA, Schreiber SL. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 1996;272:408-411.
41. Nan X, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998;393:386-389.
42. Zhang Y, LeRoy G, Seelig HP, Lane WS, Reinberg D. The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 1998;95:279-289.
43. Tong JK, Hassig CA, Schnitzler GR, Kingston RE, Schreiber SL. Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 1998;395:917-921.
44. Vaute O, Nicolas E, Vandel L, Trouche D. Functional and physical interaction between the histone methyl transferase Suv39H1 and histone deacetylases. Nucleic Acids Res 2002;30:475-481.
45. Pinheiro I, et al. Prdm3 and Prdm16 are H3K9me1 methyltransferases required for mammalian heterochromatin integrity. Cell 2012;150:948-960.
46. Ferrari KJ, et al. Polycomb-dependent H3K27me1 and H3K27me2 regulate active transcription and enhancer fidelity. Mol Cell 2014;53:49-62.
47. Heintzman ND, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009;459:108-112.
48. Milne TA, et al. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol Cell 2002;10:1107-1117.
49. Lee JH, Tate CM, You JS, Skalnik DG. Identification and characterization of the human Set1B histone H3-Lys4 methyltransferase complex. J Biol Chem 2007;282:13419-13428.
50. Hayashi K, Yoshida K, Matsui Y. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 2005;438:374-378.
51. Vermeulen M, et al. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 2007;131:58-69.
52. Krogan NJ, et al. The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol Cell 2003;11:721-729.
53. Ng HH, Robert F, Young RA, Struhl K. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 2003;11:709-719.
54. Li H, et al. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 2006;442:91-95.
55. Wysocka J, et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 2006;442:86-90.
56. Landry JW, Banerjee S, Taylor B, Aplan PD, Singer A, Wu C. Chromatin remodeling complex NURF regulates thymocyte maturation. Genes Dev 2011;25:275-286.
57. Sims RJ 3rd, et al. Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol Cell 2007;28:665-676.
58. Wei G, et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 2009;30:155-167.
59. Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, Ahringer J. Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 2009;41:376-381.
60. Guttman M, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009;458:223-227.
61. Kooistra SM, Helin K. Molecular mechanisms and potential functions of histone demethylases. Nat Rev Mol Cell Biol 2012;13:297-311.
62. Bernstein BE, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006;125:315-326.
63. Roh TY, Cuddapah S, Cui K, Zhao K. The genomic landscape of histone modifications in human T cells. Proc Natl Acad Sci USA 2006;103:15782-15787.
64. Hawkins RD, et al. Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 2010;6:479-491.
65. Guelen L, et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 2008;453:948-951.
66. 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;8:723-731.
67. Tumes DJ, et al. The polycomb protein Ezh2 regulates differentiation and plasticity of CD4(+) T helper type 1 and type 2 cells. Immunity 2013;39:819-832.
68. Araki Y, et al. Genome-wide analysis of histone methylation reveals chromatin state-based regulation of gene transcription and function of memory CD8+ T cells. Immunity 2009;30:912-925.
69. 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;280:31470-31477.
70. Margueron R, Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011;469:343-349.
71. Son J, Shen SS, Margueron R, Reinberg D. Nucleosome-binding activities within JARID2 and EZH1 regulate the function of PRC2 on chromatin. Genes Dev 2013;27:2663-2677.
72. Margueron R, et al. Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol Cell 2008;32:503-518.
73. Shen X, et al. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol Cell 2008;32:491-502.
74. Xie H, et al. Polycomb repressive complex 2 regulates normal hematopoietic stem cell function in a developmental-stage-specific manner. Cell Stem Cell 2013;14:68-80.
75. Zhou W, et al. Histone H2A monoubiquitination represses transcription by inhibiting RNA polymerase II transcriptional elongation. Mol Cell 2008;29:69-80.
76. Cao R, Tsukada Y, Zhang Y. Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell 2005;20:845-854.
77. Eskeland R, et al. Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination. Mol Cell 2010;38:452-464.
78. Schmitges FW, et al. Histone methylation by PRC2 is inhibited by active chromatin marks. Mol Cell 2011;42:330-341.
79. Wen B, Wu H, Shinkai Y, Irizarry RA, Feinberg AP. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat Genet 2009;41:246-250.
80. Rice JC, et al. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell 2003;12:1591-1598.
81. Peters AH, et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 2003;12:1577-1589.
82. Chaturvedi CP, et al. Maintenance of gene silencing by the coordinate action of the H3K9 methyltransferase G9a/KMT1C and the H3K4 demethylase Jarid1a/KDM5A. Proc Natl Acad Sci USA 2012;109:18845-18850.
83. Mozzetta C, et al. The histone H3 lysine 9 methyltransferases G9a and GLP regulate polycomb repressive complex 2-mediated gene silencing. Mol Cell 2014;53:277-289.
84. Rea S, et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 2000;406:593-599.
85. Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ 3rd. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 2002;16:919-932.
86. Bannister AJ, et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001;410:120-124.
87. Elgin SC, Grewal SI. Heterochromatin: silence is golden. Curr Biol 2003;13:R895-R898.
88. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001;410:116-120.
89. Fritsch L, et al. A subset of the histone H3 lysine 9 methyltransferases Suv39h1, G9a, GLP, and SETDB1 participate in a multimeric complex. Mol Cell 2010;37:46-56.
90. Maison C, Almouzni G. HP1 and the dynamics of heterochromatin maintenance. Nat Rev Mol Cell Biol 2004;5:296-304.
91. Maison C, et al. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet 2002;30:329-334.
92. Taddei A, Maison C, Roche D, Almouzni G. Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat Cell Biol 2001;3:114-120.
93. Allen HF, Wade PA, Kutateladze TG. The NuRD architecture. Cell Mol Life Sci 2013;70:3513-3524.
94. Allan RS, et al. An epigenetic silencing pathway controlling T helper 2 cell lineage commitment. Nature 2012;487:249-253.
95. Lehnertz B, et al. Activating and inhibitory functions for the histone lysine methyltransferase G9a in T helper cell differentiation and function. J Exp Med 2010;207:915-922.
96. Zaret KS, Carroll JS. Pioneer transcription factors: establishing competence for gene expression. Genes Dev 2011;25:2227-2241.
97. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676.
98. Heinz S, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010;38:576-589.
99. Miller SA, Mohn SE, Weinmann AS. Jmjd3 and UTX play a demethylase-independent role in chromatin remodeling to regulate T-box family member-dependent gene expression. Mol Cell 2010;40:594-605.
100. Hosokawa H, et al. Functionally distinct Gata3/Chd4 complexes coordinately establish T helper 2 (Th2) cell identity. Proc Natl Acad Sci USA 2013;110:4691-4696.
101. Radman-Livaja M, et al. Patterns and mechanisms of ancestral histone protein inheritance in budding yeast. PLoS Biol 2011;9:e1001075.
102. Moazed D. Mechanisms for the inheritance of chromatin states. Cell 2011;146:510-518.
103. Hansen KH, et al. A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol 2008;10:1291-1300.
104. Hathaway NA, Bell O, Hodges C, Miller EL, Neel DS, Crabtree GR. Dynamics and memory of heterochromatin in living cells. Cell 2012;149:1447-1460.
105. Cavalli G, Paro R. Epigenetic inheritance of active chromatin after removal of the main transactivator. Science 1999;286:955-958.
106. Chong MM, Simpson N, Ciofani M, Chen G, Collins A, Littman DR. Epigenetic propagation of CD4 expression is established by the Cd4 proximal enhancer in helper T cells. Genes Dev 2010;24:659-669.
107. Mullen AC, et al. Hlx is induced by and genetically interacts with T-bet to promote heritable T(H)1 gene induction. Nat Immunol 2002;3:652-658.
108. Zhu J, et al. Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat Immunol 2004;5:1157-1165.
109. Pai SY, Truitt ML, Ho IC. GATA-3 deficiency abrogates the development and maintenance of T helper type 2 cells. Proc Natl Acad Sci USA 2004;101:1993-1998.
110. Martins GA, Hutchins AS, Reiner SL. Transcriptional activators of helper T cell fate are required for establishment but not maintenance of signature cytokine expression. J Immunol 2005;175:5981-5985.
111. Orkin SH, Hochedlinger K. Chromatin connections to pluripotency and cellular reprogramming. Cell 2011;145:835-850.
112. Onder TT, et al. Chromatin-modifying enzymes as modulators of reprogramming. Nature 2012;483:598-602.
113. Hegazy AN, et al. Interferons direct Th2 cell reprogramming to generate a stable GATA-3(+)T-bet(+) cell subset with combined Th2 and Th1 cell functions. Immunity 2010;32:116-128.
114. Henikoff S, Shilatifard A. Histone modification: cause or cog? Trends Genet 2011;27:389-396.
115. Pengelly AR, Copur O, Jackle H, Herzig A, Muller J. A histone mutant reproduces the phenotype caused by loss of histone-modifying factor Polycomb. Science 2013;339:698-699.
116. Kasper LH, et al. Conditional knockout mice reveal distinct functions for the global transcriptional coactivators CBP and p300 in T-cell development. Mol Cell Biol 2006;26:789-809.
117. Weinreich MA, Odumade OA, Jameson SC, Hogquist KA. T cells expressing the transcription factor PLZF regulate the development of memory-like CD8+ T cells. Nat Immunol 2010;11:709-716.
118. Fukuyama T, Kasper LH, Boussouar F, Jeevan T, van Deursen J, Brindle PK. Histone acetyltransferase CBP is vital to demarcate conventional and innate CD8+ T-cell development. Mol Cell Biol 2009;29:3894-3904.
119. Juelich T, et al. Interplay between chromatin remodeling and epigenetic changes during lineage-specific commitment to granzyme B expression. J Immunol 2009;183:7063-7072.
120. Liu Y, et al. Inhibition of p300 impairs Foxp3(+) T regulatory cell function and promotes antitumor immunity. Nat Med 2013;19:1173-1177.
121. Smith PM, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013;341:569-573.
122. Arpaia N, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013;504:451-455.
123. Furusawa Y, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013;504:446-450.
124. Grausenburger R, et al. Conditional deletion of histone deacetylase 1 in T cells leads to enhanced airway inflammation and increased Th2 cytokine production. J Immunol 2010;185:3489-3497.
125. Boucheron N, et al. CD4(+) T cell lineage integrity is controlled by the histone deacetylases HDAC1 and HDAC2. Nat Immunol 2014;15:439-448.
126. Onodera A, et al. STAT6-mediated displacement of polycomb by trithorax complex establishes long-term maintenance of GATA3 expression in T helper type 2 cells. J Exp Med 2010;207:2493-2506.
127. Yamashita M, et al. Crucial role of MLL for the maintenance of memory T helper type 2 cell responses. Immunity 2006;24:611-622.
128. Suzuki A, et al. Polycomb group gene product Ring1B regulates Th2-driven airway inflammation through the inhibition of Bim-mediated apoptosis of effector Th2 cells in the lung. J Immunol 2010;184:4510-4520.
129. Yamashita M, et al. Bmi1 regulates memory CD4 T cell survival via repression of the Noxa gene. J Exp Med 2008;205:1109-1120.
130. Kimura M, et al. Regulation of Th2 cell differentiation by mel-18, a mammalian polycomb group gene. Immunity 2001;15:275-287.
131. Hosokawa H, et al. Regulation of Th2 cell development by Polycomb group gene bmi-1 through the stabilization of GATA3. J Immunol 2006;177:7656-7664.
132. He S, et al. The histone methyltransferase Ezh2 is a crucial epigenetic regulator of allogeneic T-cell responses mediating graft-versus-host disease. Blood 2013;122:4119-4128.
133. Jacob E, Hod-Dvorai R, Schif-Zuck S, Avni O. Unconventional association of the polycomb group proteins with cytokine genes in differentiated T helper cells. J Biol Chem 2008;283:13471-13481.
134. Su IH, et al. Polycomb group protein ezh2 controls actin polymerization and cell signaling. Cell 2005;121:425-436.
135. Bardot ES, et al. Polycomb subunits Ezh1 and Ezh2 regulate the Merkel cell differentiation program in skin stem cells. EMBO J 2013;32:1990-2000.
136. Antignano F, et al. Methyltransferase G9A regulates T cell differentiation during murine intestinal inflammation. J Clin Invest 2014;124:1945-1955.
137. Shin HM, Kapoor VN, Guan T, Kaech SM, Welsh RM, Berg LJ. Epigenetic modifications induced by Blimp-1 Regulate CD8(+) T cell memory progression during acute virus infection. Immunity 2013;39:661-675.
138. Nielsen AL, et al. Interaction with members of the heterochromatin protein 1 (HP1) family and histone deacetylation are differentially involved in transcriptional silencing by members of the TIF1 family. EMBO J 1999;18:6385-6395.
139. Chikuma S, Suita N, Okazaki IM, Shibayama S, Honjo T. TRIM28 prevents autoinflammatory T cell development in vivo. Nat Immunol 2012;13:596-603.
140. Santoni de Sio FR, et al. KAP1 regulates gene networks controlling T-cell development and responsiveness. FASEB J 2012;26:4561-4575.
141. Kelly TK, De Carvalho DD, Jones PA. Epigenetic modifications as therapeutic targets. Nat Biotechnol 2010;28:1069-1078.
142. Helin K, Dhanak D. Chromatin proteins and modifications as drug targets. Nature 2013;502:480-488.
143. Arrowsmith CH, Bountra C, Fish PV, Lee K, Schapira M. Epigenetic protein families: a new frontier for drug discovery. Nat Rev Drug Discov 2012;11:384-400.
144. Wang L, Tao R, Hancock WW. Using histone deacetylase inhibitors to enhance Foxp3(+) regulatory T-cell function and induce allograft tolerance. Immunol Cell Biol 2009;87:195-202.
145. Beier UH, et al. Sirtuin-1 targeting promotes Foxp3+ T-regulatory cell function and prolongs allograft survival. Mol Cell Biol 2011;31:1022-1029.
146. Nicodeme E, et al. Suppression of inflammation by a synthetic histone mimic. Nature 2010;468:1119-1123.
147. McCabe MT, et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature 2012;492:108-112.
148. Qi W, et al. Selective inhibition of Ezh2 by a small molecule inhibitor blocks tumor cells proliferation. Proc Natl Acad Sci USA 2012;109:21360-21365.