Recruitment of histone deacetylase 3 to the interferon-A gene promoters attenuates interferon expression

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Génin, Pierre ^a   Lin, Rongtuan ^b   Hiscott, John ^b,c   Civas, Ahmet ^a  

^a CNRS   (France)

^b MCGILL UNIVERSITY   (Canada)

^c Vaccine and Gene Therapy Institute of Florida   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE 3; HISTONE H3; INTERFERON; INTERFERON A; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; LYSINE; SMALL INTERFERING RNA; TATA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CONTROLLED STUDY; DEACETYLATION; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; LYMPHOID CELL LINE; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; SENDAI VIRUS INFECTION;

ACETYLATION; BURKITT LYMPHOMA; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEK293 CELLS; HISTONE DEACETYLASES; HISTONES; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOBLOTTING; INTERFERON REGULATORY FACTOR-3; INTERFERON REGULATORY FACTOR-7; INTERFERON-ALPHA; LYSINE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN ISOFORMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SENDAI VIRUS; TATA-BOX BINDING PROTEIN;

EID: 84862017441     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038336     Document Type: Article

References (77)

1. Lee MS, Kim YJ, (2007) Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu. Rev. Biochem. 76: 447-480.
2. Kumar H, Kawai T, Akira S, (2011) Pathogen recognition by the innate immune system. Int. Rev. Immunol. 30: 16-34.
3. Nakhaei P, Genin P, Civas A, Hiscott J, (2009) RIG-I-like receptors: sensing and responding to RNA virus infection. Semin. Immunol. 21: 215-222.
4. Palm NW, Medzhitov R, (2009) Pattern recognition receptors and control of adaptive immunity. Immunol. Rev. 227: 221-233.
5. Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, et al. (2000) Distinct and Essential Roles of Transcription Factors IRF-3 and IRF-7 in Response to Viruses for IFN-alpha/beta Gene Induction. Immunity 13: 539-548.
6. Honda K, Taniguchi T, (2006) IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 6: 644-658.
7. Honda K, Takaoka A, Taniguchi T, (2006) Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349-360.
8. Yoneyama M, Fujita T, (2009) RNA recognition and signal transduction by RIG-I-like receptors. Immunol. Rev. 227: 54-65.
9. Savitsky D, Tamura T, Yanai H, Taniguchi T, (2010) Regulation of immunity and oncogenesis by the IRF transcription factor family. Cancer Immunol. Immunother. 59: 489-510.
10. Kawai T, Sato S, Ishii KJ, Coban C, Hemmi H, et al. (2004) Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 5: 1061-1068.
11. Honda K, Yanai H, Mizutani T, Negishi H, Shimada N, et al. (2004) Role of a transductional-transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling. Proc. Natl. Acad. Sci. 101: 15416-15421.
12. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, et al. (2005) IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434: 772-777.
13. Kawai T, Akira S, (2008) Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 1143: 1-20.
14. Panne D, Maniatis T, Harrison SC, (2007) An atomic model of the interferon-beta enhanceosome. Cell 129: 1111-1123.
15. Apostolou E, Thanos D, (2008) Virus Infection Induces NF-kappaB-dependent interchromosomal associations mediating monoallelic IFN-beta gene expression. Cell 134: 85-96.
16. Uze G, Schreiber G, Piehler J, Pellegrini S, (2007) The receptor of the type I interferon family. Curr. Top. Microbiol. Immunol. 316: 71-95.
17. Borden EC, Sen GC, Uze G, Silverman RH, Ransohoff RM, et al. (2007) Interferons at age 50: past, current and future impact on biomedicine. Nat. Rev. Drug Discov. 6: 975-990.
18. Theofilopoulos AN, Baccala R, Beutler B, Kono DH, (2005) Type I interferons (alpha/beta) in immunity and autoimmunity. Annu. Rev. Immunol. 23: 307-335.
19. Baccala R, Hoebe K, Kono DH, Beutler B, Theofilopoulos AN, (2007) TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat. Med. 13: 543-551.
20. Fitzgerald-Bocarsly P, Dai J, Singh S, (2008) Plasmacytoid dendritic cells and type I IFN: 50 years of convergent history. Cytokine Growth Factor Rev. 19: 3-19.
21. Heinig M, Petretto E, Wallace C, Bottolo L, Rotival M, et al. (2010) A trans-acting locus regulates an anti-viral expression network and type 1 diabetes risk. Nature 467: 460-464.
22. Whittemore LA, Maniatis T, (1990) Postinduction repression of the beta-interferon gene is mediated through two positive regulatory domains. Proc. Natl. Acad. Sci. 87: 7799-7803.
23. Palombella VJ, Maniatis T, (1992) Inducible processing of interferon regulatory factor-2. Mol. Cell. Biol. 12: 3325-3336.
24. Ren B, Chee KJ, Kim TH, Maniatis T, (1999) PRDI-BF1/Blimp-1 repression is mediated by corepressors of the Groucho family of proteins. Genes Dev. 13: 125-137.
25. Gyory I, Wu J, Fejer G, Seto E, Wright KL, (2004) PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat. Immunol. 5: 299-308.
26. Senger K, Merika M, Agalioti T, Yie J, Escalante CR, et al. (2000) Gene repression by coactivator repulsion. Mol. Cell 6: 931-937.
27. Higgs R, Jefferies CA, (2008) Targeting IRFs by ubiquitination: regulating antiviral responses. Biochem. Soc. Trans. 36: 453-458.
28. Higgs R, Lazzari E, Wynne C, Ni Gabhann J, Espinosa A, et al. (2010) Self protection from anti-viral responses-Ro52 promotes degradation of the transcription factor IRF7 downstream of the viral Toll-Like receptors. PLoS One 5: e11776.
29. Yu Y, Hayward GS, (2010) The ubiquitin E3 ligase RAUL negatively regulates type i interferon through ubiquitination of the transcription factors IRF7 and IRF3. Immunity 33: 863-877.
30. Kubota T, Matsuoka M, Chang TH, Tailor P, Sasaki T, et al. (2008) Virus infection triggers SUMOylation of IRF3 and IRF7, leading to the negative regulation of type I interferon gene expression. J. Biol. Chem. 283: 25660-25670.
31. Liang Q, Deng H, Sun CW, Townes TM, Zhu F, (2011) Negative regulation of IRF7 activation by activating transcription factor 4 suggests a cross-regulation between the IFN responses and the cellular integrated stress responses. J. Immunol. 186: 1001-1010.
32. Liang Q, Deng H, Li X, Wu X, Tang Q, et al. (2011) Tripartite motif-containing protein 28 is a small ubiquitin-related modifier E3 ligase and negative regulator of IFN regulatory factor 7. J. Immunol. 187: 4754-4763.
33. Ye J, Maniatis T, (2011) Negative Regulation of Interferon-beta Gene Expression during Acute and Persistent Virus Infections. PLoS One 6: e20681.
34. Genin P, Lin R, Hiscott J, Civas A, (2009) Differential regulation of human interferon A gene expression by interferon regulatory factors 3 and 7. Mol. Cell. Biol. 29: 3435-3450.
35. Lin CH, Hare BJ, Wagner G, Harrison SC, Maniatis T, et al. (2001) A small domain of CBP/p300 binds diverse proteins: solution structure and functional studies. Mol. Cell 8: 581-590.
36. Caillaud A, Prakash A, Smith E, Masumi A, Hovanessian AG, et al. (2002) Acetylation of interferon regulatory factor-7 by p300/CREB-binding protein (CBP)-associated factor (PCAF) impairs its DNA binding. J. Biol. Chem. 277: 49417-49421.
37. Yang H, Lin CH, Ma G, Baffi MO, Wathelet MG, (2003) Interferon Regulatory Factor-7 Synergizes with Other Transcription Factors through Multiple Interactions with p300/CBP Coactivators. J. Biol. Chem. 278: 15495-15504.
38. Seto E, (2006) The Biology of HDAC3. In: Verdin E, editors. Histone Deacetylases Totowa Humana Press pp. 61-86.
39. Villagra A, Sotomayor EM, Seto E, (2010) Histone deacetylases and the immunological network: implications in cancer and inflammation. Oncogene 29: 157-173.
40. Ramirez-Carrozzi VR, Nazarian AA, Li CC, Gore SL, Sridharan R, et al. (2006) Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response. Genes Dev. 20: 282-296.
41. Medzhitov R, Horng T, (2009) Transcriptional control of the inflammatory response. Nat. Rev. Immunol. 9: 692-703.
42. Civas A, Genin P, Morin P, Lin R, Hiscott J, (2006) Promoter organization of the interferon-A genes differentially affects virus-induced expression and responsiveness to TBK1 and IKKepsilon. J. Biol. Chem. 281: 4856-4866.
43. Chen L, Fischle W, Verdin E, Greene WC, (2001) Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 293: 1653-1657.
44. Van den Wyngaert I, de Vries W, Kremer A, Neefs J, Verhasselt P, et al. (2000) Cloning and characterization of human histone deacetylase 8. FEBS Lett. 478: 77-83.
45. Fischer DD, Cai R, Bhatia U, Asselbergs FA, Song C, et al. (2002) Isolation and characterization of a novel class II histone deacetylase, HDAC10. J. Biol. Chem. 277: 6656-6666.
46. Makkonen KM, Malinen M, Ropponen A, Vaisanen S, Carlberg C, (2009) Cell cycle regulatory effects of retinoic Acid and forskolin are mediated by the cyclin C gene. J. Mol. Biol. 393: 261-271.
47. Suka N, Suka Y, Carmen AA, Wu J, Grunstein M, (2001) Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol. Cell 8: 473-479.
48. Fuchs SM, Krajewski K, Baker RW, Miller VL, Strahl BD, (2011) Influence of combinatorial histone modifications on antibody and effector protein recognition. Curr. Biol. 21: 53-58.
49. O'Donnell A, Yang SH, Sharrocks AD, (2008) MAP kinase-mediated c-fos regulation relies on a histone acetylation relay switch. Mol. Cell 29: 780-785.
50. Koutroubas G, Merika M, Thanos D, (2008) Bypassing the requirements for epigenetic modifications in gene transcription by increasing enhancer strength. Mol. Cell. Biol. 28: 926-938.
51. Perissi V, Scafoglio C, Zhang J, Ohgi KA, Rose DW, et al. (2008) TBL1 and TBLR1 phosphorylation on regulated gene promoters overcomes dual CtBP and NCoR/SMRT transcriptional repression checkpoints. Mol. Cell 29: 755-766.
52. Aguilera C, Nakagawa K, Sancho R, Chakraborty A, Hendrich B, et al. (2011) c-Jun N-terminal phosphorylation antagonises recruitment of the Mbd3/NuRD repressor complex. Nature 469: 231-235.
53. Chen J, Baig E, Fish EN, (2004) Diversity and relatedness among the type I interferons. J. Interferon Cytokine Res. 24: 687-698.
54. Genin P, Vaccaro A, Civas A, (2009) The role of differential expression of human interferon-a genes in antiviral immunity. Cytokine Growth Factor Rev 20: 283-295.
55. Kurdistani SK, Tavazoie S, Grunstein M, (2004) Mapping global histone acetylation patterns to gene expression. Cell 117: 721-733.
56. Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, et al. (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517-527.
57. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA, (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77-88.
58. Marmorstein R, (2001) Structure and function of histone acetyltransferases. Cell. Mol. Life Sci. 58: 693-703.
59. Campos EI, Reinberg D, (2009) Histones: annotating chromatin. Annu. Rev. Genet. 43: 559-599.
60. Agalioti T, Chen G, Thanos D, (2002) Deciphering the transcriptional histone acetylation code for a human gene. Cell 111: 381-392.
61. Ford E, Thanos D, (2010) The transcriptional code of human IFN-beta gene expression. Biochim Biophys Acta 1799: 328-336.
62. Katan-Khaykovich Y, Struhl K, (2002) Dynamics of global histone acetylation and deacetylation in vivo: rapid restoration of normal histone acetylation status upon removal of activators and repressors. Genes Dev. 16: 743-752.
63. Clayton AL, Hazzalin CA, Mahadevan LC, (2006) Enhanced histone acetylation and transcription: a dynamic perspective. Mol. Cell 23: 289-296.
64. Nusinzon I, Horvath CM, (2006) Positive and negative regulation of the innate antiviral response and beta interferon gene expression by deacetylation. Mol. Cell. Biol. 26: 3106-3113.
65. Rehwinkel J, Tan CP, Goubau D, Schulz O, Pichlmair A, et al. (2010) RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 140: 397-408.
66. Gitlin L, Benoit L, Song C, Cella M, Gilfillan S, et al. (2010) Melanoma differentiation-associated gene 5 (MDA5) is involved in the innate immune response to Paramyxoviridae infection in vivo. PLoS Pathog. 6: e1000734.
67. Woelk CH, Frost SD, Richman DD, Higley PE, Kosakovsky Pond SL, (2007) Evolution of the interferon alpha gene family in eutherian mammals. Gene 397: 38-50.
68. Au WC, Pitha PM, (2001) Recruitment of multiple interferon regulatory factors and histone acetyltransferase to the transcriptionally active interferon a promoters. J. Biol. Chem. 276: 41629-41637.
69. Lin R, Genin P, Mamane Y, Hiscott J, (2000) Selective DNA binding and association with the CREB binding protein coactivator contribute to differential activation of alpha/beta interferon genes by interferon regulatory factors 3 and 7. Mol. Cell. Biol. 20: 6342-6353.
70. Agalioti T, Lomvardas S, Parekh B, Yie J, Maniatis T, et al. (2000) Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter. Cell 103: 667-678.
71. Topalidou I, Papamichos-Chronakis M, Thireos G, (2003) Post-TATA binding protein recruitment clearance of Gcn5-dependent histone acetylation within promoter nucleosomes. Mol. Cell. Biol. 23: 7809-7817.
72. Barth TK, Imhof A, (2010) Fast signals and slow marks: the dynamics of histone modifications. Trends Biochem. Sci. 35: 618-626.
73. Weiss C, Schneider S, Wagner EF, Zhang X, Seto E, et al. (2003) JNK phosphorylation relieves HDAC3-dependent suppression of the transcriptional activity of c-Jun. EMBO J. 22: 3686-3695.
74. Chen LF, Greene WC, (2003) Regulation of distinct biological activities of the NF-kappaB transcription factor complex by acetylation. J. Mol. Med. 81: 549-557.
75. Karagianni P, Wong J, (2007) HDAC3: taking the SMRT-N-CoRrect road to repression. Oncogene 26: 5439-5449.
76. Sankar N, Baluchamy S, Kadeppagari RK, Singhal G, Weitzman S, et al. (2008) p300 provides a corepressor function by cooperating with YY1 and HDAC3 to repress c-Myc. Oncogene 27: 5717-5728.
77. Luebben WR, Sharma N, Nyborg JK, (2010) Nucleosome eviction and activated transcription require p300 acetylation of histone H3 lysine 14. Proc. Natl. Acad. Sci. 107: 19254-19259.