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Annual Review of Immunology

Volume 32, 2014

Chromatin Contributions to the Regulation of Innate Immunity

Abstract

A fundamental property of cells of the innate immune system is their ability to elicit a transcriptional response to a microbial stimulus or danger signal with a high degree of cell type and stimulus specificity. The selective response activates effector pathways to control the insult and plays a central role in regulating adaptive immunity through the differential regulation of cytokine genes. Selectivity is dictated by signaling pathways and their transcription factor targets. However, a growing body of evidence supports models in which different subsets of genes exhibit distinct chromatin features that play active roles in shaping the response. Chromatin also participates in innate memory mechanisms that can promote tolerance to a stimulus or prime cells for a more robust response. These findings have generated interest in the capacity to modulate chromatin regulators with small-molecule compounds for the treatment of diseases associated with innate or adaptive immunity.

Keyword(s): chromatin, epigenetics, innate immunity, macrophages, transcription
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2014-03-21
2024-04-18
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Literature Cited

  1. Medzhitov R, Janeway CA Jr. 1.  1997. Innate immunity: impact on the adaptive immune system. Curr. Opin. Immunol. 9:4–9 [Google Scholar]
  2. Medzhitov R, Janeway CA Jr. 2.  1997. Innate immunity: the virtues of a nonclonal system of recognition. Cell 91:295–98 [Google Scholar]
  3. Schenten D, Medzhitov R. 3.  2011. The control of adaptive immune responses by the innate immune system. Adv. Immunol. 109:87–124 [Google Scholar]
  4. Janeway CA Jr. 4.  1989. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54:Pt. 11–13 [Google Scholar]
  5. Lamaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA. 5.  1996. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973–83 [Google Scholar]
  6. Medzhitov R, Preston-Hurlburt P, Janeway CA Jr. 6.  1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394–97 [Google Scholar]
  7. Takeuchi O, Akira S. 7.  2010. Pattern recognition receptors and inflammation. Cell 140:805–20 [Google Scholar]
  8. Kumar H, Kawai T, Akira S. 8.  2011. Pathogen recognition by the innate immune system. Int. Rev. Immunol. 30:16–34 [Google Scholar]
  9. Medzhitov R, Horng T. 9.  2009. Transcriptional control of the inflammatory response. Nat. Rev. Immunol. 9:692–703 [Google Scholar]
  10. Smale ST. 10.  2010. Selective transcription in response to an inflammatory stimulus. Cell 140:833–44 [Google Scholar]
  11. Natoli G. 11.  2010. Maintaining cell identity through global control of genomic organization. Immunity 33:12–24 [Google Scholar]
  12. Natoli G, Ghisletti S, Barozzi I. 12.  2011. The genomic landscapes of inflammation. Genes Dev. 25:101–6 [Google Scholar]
  13. Smale ST. 13.  2012. Transcriptional regulation in the innate immune system. Curr. Opin. Immunol. 24:51–57 [Google Scholar]
  14. Biswas SK, Lopez-Collazo E. 14.  2009. Endotoxin tolerance: new mechanisms, molecules, and clinical significance. Trends Immunol. 30:475–87 [Google Scholar]
  15. Monticelli S, Natoli G. 15.  2013. Short-term memory of danger signals and environmental stimuli in immune cells. Nat. Immunol. 14:777–84 [Google Scholar]
  16. Lyakh L, Trinchieri G, Provezza L, Carra G, Gerosa F. 16.  2008. Regulation of interleukin-12/interleukin-23 production and the T-helper 17 response in humans. Immunol. Rev. 226:112–31 [Google Scholar]
  17. Gilmore TD, Gerondakis S. 17.  2011. The c-Rel transcription factor in development and disease. Genes Cancer 2:695–711 [Google Scholar]
  18. Smale ST. 18.  2012. Dimer-specific regulatory mechanisms within the NF-κB family of transcription factors. Immunol. Rev. 246:193–204 [Google Scholar]
  19. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW. 19.  et al. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39:311–18 [Google Scholar]
  20. Jeong KW, Kim K, Situ AJ, Ullmer TS, An W, Stallcup MR. 20.  2011. Recognition of enhancer element-specific histone methylation by TIP60 in transcriptional activation. Nat. Struct. Mol. Biol. 18:1358–65 [Google Scholar]
  21. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW. 21.  et al. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. USA 107:21931–36 [Google Scholar]
  22. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 22.  2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470:279–83 [Google Scholar]
  23. Otsuni R, Piccolo V, Barozzi I, Polletti S, Termanini A. 23.  et al. 2013. Latent enhancers activated by stimulation in differentiated cells. Cell 152:157–71 [Google Scholar]
  24. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A. 24.  et al. 2009. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:108–12 [Google Scholar]
  25. Chen J, Li Q. 25.  2011. Life and death of transcriptional co-activator p300. Epigenetics 6:957–61 [Google Scholar]
  26. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA. 26.  et al. 2009. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457:854–58 [Google Scholar]
  27. Ghisletti S, Barozzi I, Mietton F, Polletti S, De Santa F. 27.  et al. 2010. Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity 32:317–28 [Google Scholar]
  28. Scott EW, Simon MC, Anastasi J, Singh H. 28.  1994. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265:1573–77 [Google Scholar]
  29. Heinz S, Benner C, Spann N, Bertolino E, Lin YC. 29.  et al. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38:576–89 [Google Scholar]
  30. DeKoter RP, Singh H. 30.  2000. Regulation of B lymphocyte and macrophage development by graded expression of PU.1. Science 288:1439–41 [Google Scholar]
  31. Gualdi R, Bossard P, Zheng M, Hamada Y, Coleman JR, Zaret KS. 31.  1996. Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes Dev. 10:1670–82 [Google Scholar]
  32. Smale ST. 32.  2010. Pioneer factors in embryonic stem cells and differentiation. Curr. Opin. Genet. Dev. 20:519–26 [Google Scholar]
  33. Zaret KS, Carroll JS. 33.  2011. Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25:2227–41 [Google Scholar]
  34. Xu J, Pope SD, Jazirehi AR, Attema JL, Papathanasiou P. 34.  et al. 2007. Pioneer factor interactions and unmethylated CpG dinucleotides mark silent tissue-specific enhancers in embryonic stem cells. Proc. Natl. Acad. Sci. USA 104:12377–82 [Google Scholar]
  35. Xu J, Watts JA, Pope SD, Gadue P, Kamps M. 35.  et al. 2009. Transcriptional competence and the active marking of tissue-specific enhancers by defined transcription factors in embryonic stem and induced pluripotent stem cells. Genes Dev. 23:2824–38 [Google Scholar]
  36. de Wit E, de Laat W. 36.  2012. A decade of 3C technologies: insights into nuclear organization. Genes Dev. 26:11–24 [Google Scholar]
  37. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM. 37.  et al. 2010. Widespread transcription at neuronal activity-regulated enhancers. Nature 465:182–87 [Google Scholar]
  38. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S. 38.  et al. 2010. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol. 8:e1000384 [Google Scholar]
  39. Koch F, Fenouil R, Gut M, Cauchy P, Albert TK. 39.  et al. 2011. Transcription initiation platforms and GTF recruitment at tissue-specific enhancers and promoters. Nat. Struct. Mol. Biol. 18:956–63 [Google Scholar]
  40. Natoli G, Andrau JC. 40.  2012. Noncoding transcription at enhancers: general principles and functional models. Annu. Rev. Genet. 46:1–19 [Google Scholar]
  41. Lam MT, Cho H, Lesch HP, Gosselin D, Heinz S. 41.  et al. 2013. Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 498:511–15 [Google Scholar]
  42. Yamamoto KR, Alberts BM. 42.  1976. Steroid receptors: elements for modulation of eukaryotic transcription. Annu. Rev. Biochem. 45:721–46 [Google Scholar]
  43. Herschman HR. 43.  1991. Primary response genes induced by growth factors and tumor promoters. Annu. Rev. Biochem. 60:281–319 [Google Scholar]
  44. Fowler T, Ren R, Roy AL. 44.  2011. Regulation of primary response genes. Mol. Cell 44:348–60 [Google Scholar]
  45. Sen R, Baltimore D. 45.  1986. Inducibility of kappa immunoglobulin enhancer-binding protein NF-κB by a posttranslational mechanism. Cell 47:921–28 [Google Scholar]
  46. Hayden MS, Ghosh S. 46.  2012. NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 26:203–34 [Google Scholar]
  47. Price MA, Hill C, Treisman R. 47.  1996. Integration of growth factor signals at the c-fos serum response element. Philos. Trans. R. Soc. B 351:551–59 [Google Scholar]
  48. Posem G, Treisman R. 48.  2006. Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol. 16:588–96 [Google Scholar]
  49. Almer A, Horz W. 49.  1986. Nuclease hypersensitive regions with adjacent positioned nucleosomes mark the gene boundaries of the PHO5/PHO3 locus in yeast. EMBO J. 5:2681–87 [Google Scholar]
  50. Almer A, Rudolph H, Hinnen A, Horz W. 50.  1986. Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activation DNA elements. EMBO J. 5:2689–96 [Google Scholar]
  51. McAndrew PC, Svaren J, Martin SR, Horz W, Goding CR. 51.  1998. Requirements for chromatin modulation and transcription activation by the Pho4 acidic activation domain. Mol. Cell. Biol. 18:5818–27 [Google Scholar]
  52. Verdin E, Paras P, Van Lint C. 52.  1993. Chromatin disruption in the promoter of human immunodeficiency virus type 1 during transcriptional activation. EMBO J. 12:3249–59 [Google Scholar]
  53. Richard-Foy H, Hager GL. 53.  1987. Sequence-specific positioning of nucleosomes over the steroid-inducible MMTV promoter. EMBO J. 6:2321–28 [Google Scholar]
  54. Fragaso G, John S, Roberts MS, Hager GL. 54.  1995. Nucleosome positioning on the MMTV LTR result from the frequency-biased occupancy of multiple frames. Genes Dev. 9:1933–47 [Google Scholar]
  55. Siebenlist U, Durand DB, Bressler P, Holbrook NJ, Norris CA. 55.  et al. 1986. Promoter region of interleukin-2 gene undergoes chromatin structure changes and confers inducibility on chloramphenicol acetyltransferase gene during activation of T cells. Mol. Cell. Biol. 6:3042–49 [Google Scholar]
  56. Ward SB, Hernandez-Hoyas G, Chen F, Waterman M, Reeves R, Rothenberg EV. 56.  1998. Chromatin remodeling of the interleukin-2 gene: distinct alterations in the proximal versus distal enhancer regions. Nucleic Acids Res. 26:2923–34 [Google Scholar]
  57. Agarwal S, Rao A. 57.  1998. Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 9:765–75 [Google Scholar]
  58. Weinmann AS, Plevy SE, Smale ST. 58.  1999. Rapid and selective remodeling of a positioned nucleosome during the induction of IL-12 p40 transcription. Immunity 11:665–75 [Google Scholar]
  59. Agalioti T, Lomvardas S, Parekh B, Yie J, Maniatis T, Thanos D. 59.  2000. Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter. Cell 103:667–78 [Google Scholar]
  60. Parekh BS, Maniatis T. 60.  1999. Virus infection leads to localized hyperacetylation of histones H3 and H4 at the IFN-β promoter. Mol. Cell 3:125–29 [Google Scholar]
  61. Peterson CL, Workman JL. 61.  2000. Promoter targeting and chromatin remodeling by the SWI/SNF complex. Curr. Opin. Genet. Dev. 10:187–92 [Google Scholar]
  62. Li B, Carey M, Workman JL. 62.  2007. The role of chromatin during transcription. Cell 128:707–19 [Google Scholar]
  63. Carey M, Peterson CL, Smale ST. 63.  2009. Transcriptional Regulation in Eukaryotes: Concepts, Strategies, and Techniques New York: Cold Spring Harbor Lab, 2nd ed..
  64. Natoli G. 64.  2009. Control of NF-κB-dependent transcriptional responses by chromatin organization. Cold Spring Harb. Perspect. Biol. 1:a000224 [Google Scholar]
  65. Sen R, Smale ST. 65.  2010. Selectivity of the NF-κB response. Cold Spring Harb. Perspect. Biol. 2:a000257 [Google Scholar]
  66. Smale ST. 66.  2011. Hierarchies of NF-κB target-gene regulation. Nat. Immunol. 12:689–94 [Google Scholar]
  67. Saccani S, Pantano S, Natoli G. 67.  2001. Two waves of nuclear factor κB recruitment to target promoters. J. Exp. Med. 193:1351–59 [Google Scholar]
  68. Ramirez-Carrozzi VR, Nazarian AA, Li CC, Gore SL, Sridharan R. 68.  et al. 2006. Selective and antagonistic functions of SWI/SNF and Mi-2β nucleosome remodeling complexes during an inflammatory response. Genes Dev. 20:282–96 [Google Scholar]
  69. Ramirez-Carrozzi VR, Braas D, Bhatt DM, Cheng CS, Hong C. 69.  et al. 2009. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 138:114–28 [Google Scholar]
  70. Wang W, Cote J, Xue J, Zhou S, Khavari PA. 70.  et al. 1996. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J. 15:5370–82 [Google Scholar]
  71. Hargreaves DC, Horng T, Medzhitov R. 71.  2009. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 138:129–45 [Google Scholar]
  72. Drew HR, Travers AA. 72.  1985. DNA bending and its relation to nucleosome positioning. J. Mol. Biol. 196:261–82 [Google Scholar]
  73. Satchwell SC, Drew HR, Travers AA. 73.  1986. Sequence periodicities in chicken nucleosome core DNA. J. Mol. Biol. 191:659–75 [Google Scholar]
  74. Lowary PT, Widom J. 74.  1998. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276:19–42 [Google Scholar]
  75. Fenouil R, Cauchy P, Koch F, Descostes N, Cabeza JZ. 75.  et al. 2012. CpG islands and GC content dictate nucleosome depletion in a transcription-independent manner at mammalian promoters. Genome Res. 22:2399–408 [Google Scholar]
  76. Lone IN, Shukla MS, Charles Richard JL, Peshev ZY, Dimitrov S, Angelov D. 76.  2013. Binding of NF-κB to nucleosomes: effect of translational positioning, nucleosome remodeling, and linker histone H1. PLoS Genet. 9:e1003830 [Google Scholar]
  77. Weinmann AS, Mitchell DM, Sanjabi S, Bradley MN, Hoffmann A. 77.  et al. 2001. Nucleosome remodeling at the IL-12 p40 promoter is a TLR-dependent, Rel-independent event. Nat. Immunol. 2:51–57 [Google Scholar]
  78. Kishimoto T. 78.  2010. IL-6: from its discovery to clinical applications. Int. Immunol. 22:347–52 [Google Scholar]
  79. Kimura A, Kishimoto T. 79.  2010. IL-6: regulator of Treg/Th17 balance. Eur. J. Immunol. 40:1830–35 [Google Scholar]
  80. Bhatt DM, Pandya-Jones A, Tong AJ, Barozzi I, Lissner MM. 80.  et al. 2012. Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions. Cell 150:279–90 [Google Scholar]
  81. De Santa F, Narang V, Yap ZH, Tusi BK, Burgold T. 81.  et al. 2009. Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J. 28:3341–52 [Google Scholar]
  82. Simon JA, Kingston RE. 82.  2013. Occupying chromatin: polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol. Cell 49:808–24 [Google Scholar]
  83. Perkins ND. 83.  2006. Post-translational modifications regulating the activity and function of the nuclear factor κB pathway. Oncogene 25:6717–30 [Google Scholar]
  84. Zhong H, Voll RE, Ghosh S. 84.  1998. Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the co-activator CBP/p300. Mol. Cell 1:661–71 [Google Scholar]
  85. Chen LF, Fischle W, Verdin E, Greene WC. 85.  2001. Duration of nuclear NF-κB action regulated by reversible acetylation. Science 293:1653–57 [Google Scholar]
  86. Zhong H, May MJ, Jimi E, Ghosh S. 86.  2002. Phosphorylation of nuclear NF-κB governs its association with either HDAC-1 or CBP/p300: a mechanism for regulating the transcriptional activity of NF-κB. Mol. Cell 9:625–36 [Google Scholar]
  87. Duran A, Diaz-Meco MT, Moscat J. 87.  2003. Essential role of RelA Ser311 phosphorylation by ζPKC in NF-κB transcriptional activation. EMBO J. 22:3910–18 [Google Scholar]
  88. Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR. 88.  et al. 2004. Modulation of NF-κB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 23:2369–80 [Google Scholar]
  89. Dong J, Jimi E, Zhong H, Hayden MS, Ghosh S. 89.  2008. Epigenetic regulation of NF-κB dependent gene expression. Genes Dev. 22:1159–73 [Google Scholar]
  90. Ea CK, Baltimore D. 90.  2009. Regulation of NF-κB activity through lysine monomethylation of p65. Proc. Natl. Acad. Sci. USA 106:18972–77 [Google Scholar]
  91. Yang XD, Yuang B, Li M, Lamb A, Kelleher NL, Chen LF. 91.  2009. Negative regulation of NF-κB action by Set9-mediated lysine methylation of the RelA subunit. EMBO J. 28:1055–66 [Google Scholar]
  92. Huang B, Yang XD, Zhou MM, Ozato K, Chen LF. 92.  2009. Brd4 coactivates transcriptional activation of NF-κB via specific binding to acetylated RelA. Mol. Cell. Biol. 29:1375–87 [Google Scholar]
  93. Yang XD, Tajkhorshid E, Chen LF. 93.  2010. Functional interplay between acetylation and methylation of the RelA subunit of NF-κB. Mol. Cell. Biol. 30:2170–80 [Google Scholar]
  94. Levy D, Kuo AJ, Chang Y, Schaefer U, Kitson C. 94.  et al. 2011. Lysine methylation of the NF-κB subunit RelA by SETD6 couples activity of the histone methyltransferase GLP at chromatin to tonic repression of NF-κB signaling. Nat. Immunol. 12:29–36 [Google Scholar]
  95. Allison DF, Wamsley JJ, Kumar M, Li D, Gray LG. 95.  et al. 2012. Modification of RelA by O-linked N-acetylglucosamine links glucose metabolism to NF-κB acetylation and transcription. Proc. Natl. Acad. Sci. USA 109:16888–93 [Google Scholar]
  96. Liu Y, Mayo MW, Nagji AS, Smith PW, Ramsey CS. 96.  et al. 2012. Phosphorylation of RelA/p65 promotes DNMT-1 recruitment to chromatin and represses transcription of the tumor metastasis suppressor gene BRMS1. Oncogene 31:1143–54 [Google Scholar]
  97. Lu T, Yang M, Huang DB, Wei H, Ozer GH. 97.  et al. 2013. Role of lysine methylation of NF-κB in differential gene regulation. Proc. Natl. Acad. Sci. USA 110:13510–15 [Google Scholar]
  98. Wei H, Wang B, Miyagi M, She Y, Gopalan B. 98.  et al. 2013. PRMT5 dimethylates P30 of the p65 subunit to activate NF-κB. Proc. Natl. Acad. Sci. USA 110:13516–21 [Google Scholar]
  99. Ramakrishnan P, Clark PM, Mason DE, Peters EC, Hsieh-Wilson LC, Baltimore D. 99.  2013. Activation of the transcriptional function of the NF-κB protein c-Rel by O-GlcNAc glycosylation. Sci. Signal. 6:ra75 [Google Scholar]
  100. Covic M, Hassa PO, Saccani S, Buerki C, Meier NI. 100.  et al. 2005. Arginine methyltransferase CARM1 is a promoter-specific regulator of NF-κB-dependent gene expression. EMBO J. 24:85–96 [Google Scholar]
  101. Hassa PO, Covic M, Bedford MT, Hottiger MO. 101.  2008. Protein arginine methyltransferase 1 coactivates NF-κB-dependent gene expression synergistically with CARM1 and PARP1. J. Mol. Biol. 377:668–78 [Google Scholar]
  102. Wan F, Anderson DE, Barnitz RA, Snow A, Bidere N. 102.  et al. 2007. Ribosomal protein S3: a KH domain subunit in NF-κB complexes that mediates selective gene regulation. Cell 131:927–39 [Google Scholar]
  103. Yamamoto M, Takeda K. 103.  2008. Role of nuclear IκB proteins in the regulation of host immune responses. J. Infect. Chemother. 14:265–69 [Google Scholar]
  104. van Essen D, Engist B, Natoli G, Saccani S. 104.  2009. Two modes of transcriptional activation at native promoters by NF-κB p65. PLoS Biol. 7:e73 [Google Scholar]
  105. Ea CK, Hao S, Yeo KS, Baltimore D. 105.  2012. EHMT1 protein binds to nuclear factor-κB p50 and represses gene expression. J. Biol. Chem. 287:31207–17 [Google Scholar]
  106. Mukherjee SP, Behar M, Birnbaum HA, Hoffmann A, Wright PE, Ghosh G. 106.  2013. Analysis of the RelA:CBP/p300 interaction reveals its involvement in NF-κB-driven transcription. PLoS Biol. 11:e1001647 [Google Scholar]
  107. Zou YR, Sunshine MJ, Taniuchi I, Hatam F, Killeen N, Littman DR. 107.  2001. Epigenetic silencing of CD4 in T cells committed to the cytotoxic lineage. Nat. Genet. 29:332–36 [Google Scholar]
  108. Gialitakis M, Sellars M, Littman DR. 108.  2012. The epigenetic landscape of lineage choice: lessons from the heritability of CD4 and CD8 expression. Curr. Top. Microbiol. Immunol. 356:165–88 [Google Scholar]
  109. Ptashne M. 109.  2013. Epigenetics: core misconcept. Proc. Natl. Acad. Sci. USA 110:7101–13 [Google Scholar]
  110. Ivashkiv LB. 110.  2011. Inflammatory signaling in macrophages: transitions from acute to tolerant and alternative activation states. Eur. J. Immunol. 41:2477–81 [Google Scholar]
  111. Ivashkiv LB. 111.  2013. Epigenetic regulation of macrophage polarization and function. Trends Immunol. 34:216–23 [Google Scholar]
  112. Foster SL, Hargreaves DC, Medzhitov R. 112.  2007. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447:972–78 [Google Scholar]
  113. Yan Q, Carmody RJ, Qu Z, Ruan Q, Jager J. 113.  et al. 2012. Nuclear factor-κB binding motifs specify Toll-like receptor-induced gene repression through an inducible repressosome. Proc. Natl. Acad. Sci. USA 109:14140–45 [Google Scholar]
  114. Gasparini C, Feldmann M. 114.  2012. NF-κB as a target for modulating inflammatory responses. Curr. Pharm. Des. 18:5735–45 [Google Scholar]
  115. Zeng L, Zhou MM. 115.  2002. Bromodomain: an acetyl-lysine binding domain. FEBS Lett. 513:124–28 [Google Scholar]
  116. Mujtaba S, Zeng L, Zhou MM. 116.  2007. Structure and acetyl-lysine recognition of the bromodomain. Oncogene 26:5521–27 [Google Scholar]
  117. Zippo A, Serafini R, Rocchigiani M, Pennacchini S, Krepelova A, Oliviero S. 117.  2009. Histone crosstalk between H3S10ph and K4K16ac generates a histone code that mediates transcription elongation. Cell 138:1122–36 [Google Scholar]
  118. Filippakopoulos P, Knapp S. 118.  2012. The bromodomain interaction module. FEBS Lett. 586:2692–704 [Google Scholar]
  119. Filippakopoulos P, Picaud S, Mangos M, Keates T, Lambert JP. 119.  et al. 2012. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 149:214–31 [Google Scholar]
  120. Dey A, Chitsaz F, Abbasi A, Misteli T, Ozato K. 120.  2003. The double bromodomain protein Brd4 binds to acetylated chromatin during interphase and mitosis. Proc. Natl. Acad. Sci. USA 100:8758–63 [Google Scholar]
  121. McBride AA, McPhillips MG, Oliveira JG. 121.  2004. Brd4: tethering, segregation and beyond. Trends Microbiol. 12:527–29 [Google Scholar]
  122. Rahman S, Sowa ME, Ottinger M, Smith JA, Shi Y. 122.  et al. 2011. The Brd4 extraterminal domain confers transcription activation independent of pTEFb by recruiting multiple proteins, including NSD3. Mol. Cell. Biol. 31:2641–52 [Google Scholar]
  123. Schröder S, Cho S, Zeng L, Zhang Q, Kaehlcke K. 123.  et al. 2012. Two-pronged binding with bromodomain-containing protein 4 liberates positive transcription elongation factor b from inactive ribonucleoprotein complexes. J. Biol. Chem. 287:1090–99 [Google Scholar]
  124. Peterlin BM, Price DH. 124.  2006. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23:297–305 [Google Scholar]
  125. Zhou Q, Li T, Price DH. 125.  2012. RNA polymerase II elongation control. Annu. Rev. Biochem. 81:119–43 [Google Scholar]
  126. Dawson MA, Prinjha RK, Dittmann A, Giotopoulos G, Bantscheff M. 126.  et al. 2011. Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature 478:529–33 [Google Scholar]
  127. Belkina AC, Denis GV. 127.  2012. BET domain co-regulators in obesity, inflammation and cancer. Nat. Rev. Cancer 12:465–77 [Google Scholar]
  128. Salter-Cid L, Flajnik MF. 128.  1995. Evolution and developmental regulation of the major histocompatibility complex. Crit. Rev. Immunol. 15:31–75 [Google Scholar]
  129. Belkina AC, Nikolajczyk BS, Denis GV. 129.  2013. BET protein function is required for inflammation: Brd2 genetic disruption and BET inhibitor JQ1 impair mouse macrophage inflammatory responses. J. Immunol. 190:3670–78 [Google Scholar]
  130. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ. 130.  2007. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 14:1025–40 [Google Scholar]
  131. Filippakopoulos P, Qi J, Picaud S, Shen Y, Smith WB, Fedorov O. 131.  et al. 2010. Selective inhibition of BET bromodomains. Nature 468:1067–73 [Google Scholar]
  132. Nicodeme E, Jeffrey KL, Schaefer U, Beinke S, Dewell S. 132.  et al. 2010. Suppression of inflammation by a synthetic histone mimic. Nature 468:1119–23 [Google Scholar]
  133. Bierne H, Cossart P. 133.  2012. When bacteria target the nucleus: the emerging family of nucleomodulins. Cell. Microbiol. 14:622–33 [Google Scholar]
  134. Bierne H, Hamon M, Cossart P. 134.  2012. Epigenetics and bacterial infections. Cold Spring Harb. Perspect. Med. 2:a010272 [Google Scholar]
  135. Fonseca GJ, Thillainadesan G, Yousef AF, Ablack JN, Mossman KL. 135.  et al. 2012. Adenovirus evasion of interferon-mediated innate immunity by direct antagonism of a cellular histone posttranslational modification. Cell Host Microbe 11:597–606 [Google Scholar]
  136. Mueller CL, Jaehning JA. 136.  2002. Ctr9, Rtf1, and Leo1 are components of the PAF1/RNA polymerase II complex. Mol. Cell. Biol. 22:1971–80 [Google Scholar]
  137. Jaehning JA. 137.  2010. The Paf1 complex: platform or player in RNA polymerase II transcription?. Biochim. Biophys. Acta 1799:379–88 [Google Scholar]
  138. Kim J, Roeder RG. 138.  2009. Direct Bre1-Paf1 complex interactions and RING finger-independent Bre1-Rad6 interactions mediate histone H2B ubiquitylation in yeast. J. Biol. Chem. 284:20582–92 [Google Scholar]
  139. Kim J, Guermah M, McGinty RK, Lee JS, Tang Z. 139.  et al. 2009. RAD6-mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 137:459–71 [Google Scholar]
  140. Lee JS, Shukla A, Schneider J, Swanson SK, Washburn MP. 140.  et al. 2007. Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131:1084–96 [Google Scholar]
  141. Xiao T, Kao CF, Krogan NJ, Sun ZW, Greenblatt JF. 141.  2005. Histone H2B ubiquitylation is associated with elongating RNA polymerase II. Mol. Cell. Biol. 25:637–51 [Google Scholar]
  142. Luo Z, Lin C, Shilatifard A. 142.  2012. The super elongation complex (SEC) family in transcriptional control. Nat. Rev. Mol. Cell Biol. 13:543–47 [Google Scholar]
  143. Haye K, Burmakina S, Moran T, Garcia-Sastre A, Fernandez-Sesma A. 143.  2009. The NS1 protein of a human influenza virus inhibits type 1 interferon production and the induction of antiviral responses in primary human dendritic and respiratory epithelial cells. J. Virol. 83:6849–62 [Google Scholar]
  144. Hale BG, Randall RE, Ortin J, Jackson D. 144.  2008. The multifunctional NS1 protein of influenza A viruses. J. Gen. Virol. 89:2359–76 [Google Scholar]
  145. Kochs G, Garcia-Sastre A, Martinez-Sobrido L. 145.  2007. Multiple anti-interferon actions of the influenza A virus NS1 protein. J. Virol. 81:7011–21 [Google Scholar]
  146. Marazzi I, Ho JS, Kim J, Manicassamy B, Dewell S. 146.  et al. 2012. Suppression of the antiviral response by an influenza histone mimic. Nature 483:428–33 [Google Scholar]
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Chromatin Contributions to the Regulation of Innate Immunity
Annual Review of Immunology 32, 489 (2014); https://doi.org/10.1146/annurev-immunol-031210-101303
/content/journals/10.1146/annurev-immunol-031210-101303
/content/journals/10.1146/annurev-immunol-031210-101303
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