The transcriptional code of human IFN-β gene expression

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1799, Issue 3-4, 2010, Pages 328-336

  Ford, Ethan ^a   Thanos, Dimitris ^a  

^a BIOMEDICAL RESEARCH FOUNDATION   (Greece)

Author keywords

Chromatin; Enhanceosome; Interferon ; IRF 3; NF B; Transcription

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; BETA INTERFERON; CHOLECYSTOKININ OCTAPEPTIDE[28,31 N METHYLNORLEUCINE]; ENHANCEOSOME; HIGH MOBILITY GROUP A1A PROTEIN; HISTONE; HISTONE ACETYLTRANSFERASE GCN5; HISTONE ACETYLTRANSFERASE PCAF; HOLOENZYME; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR; INTERFERON REGULATORY FACTOR 3; PROTEIN C JUN; PROTEIN SWI; RNA POLYMERASE II; STRESS ACTIVATED PROTEIN KINASE;

ACETYLATION; ALU SEQUENCE; CHROMOSOME REARRANGEMENT; CONFORMATIONAL TRANSITION; DOWN REGULATION; ENZYME BINDING; EUKARYOTE; EUKARYOTIC CELL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENETIC CODE; HUMAN; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; STOCHASTIC MODEL; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; VIRUS INDUCTION; VIRUS INFECTION; VIRUS INHIBITION;

ANIMALS; GENE EXPRESSION REGULATION; HUMANS; INTERFERON-BETA; REGULATORY SEQUENCES, NUCLEIC ACID; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 77749242510     PISSN: 18749399     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2010.01.010     Document Type: Review

References (93)

1. Ptashne M. Regulation of transcription: from lambda to eukaryotes. Trends Biochem. Sci. 30 (2005) 275-279
2. Gilmore T.D. Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 25 (2006) 6680-6684
3. Naamane N., van Helden J., and Eizirik D.L. In silico identification of NF-kappaB-regulated genes in pancreatic beta-cells. BMC Bioinformatics 8 (2007) 55
4. Babu M.M., Janga S.C., de Santiago I., and Pombo A. Eukaryotic gene regulation in three dimensions and its impact on genome evolution. Curr. Opin. Genet. Dev. 18 (2008) 571-582
5. Osborne C.S., Chakalova L., Brown K.E., Carter D., Horton A., Debrand E., Goyenechea B., Mitchell J.A., Lopes S., Reik W., and Fraser P. Active genes dynamically colocalize to shared sites of ongoing transcription. Nat. Genet. 36 (2004) 1065-1071
6. Kouzarides T. Chromatin modifications and their function. Cell 128 (2007) 693-705
7. Kamakaka R.T., and Biggins S. Histone variants: deviants?. Genes Dev. 19 (2005) 295-310
8. Schones D.E., Cui K., Cuddapah S., Roh T.Y., Barski A., Wang Z., Wei G., and Zhao K. Dynamic regulation of nucleosome positioning in the human genome. Cell 132 (2008) 887-898
9. Jiang C., and Pugh B.F. Nucleosome positioning and gene regulation: advances through genomics. Nat. Rev. Genet. 10 (2009) 161-172
10. Takaoka A., and Yanai H. Interferon signalling network in innate defence. Cell Microbiol. 8 (2006) 907-922
11. Horvath C.M. Weapons of STAT destruction. Interferon evasion by paramyxovirus V protein. Eur. J. Biochem. 271 (2004) 4621-4628
12. Honda K., Yanai H., Takaoka A., and Taniguchi T. Regulation of the type I IFN induction: a current view. Int. Immunol. 17 (2005) 1367-1378
13. Malmgaard L. Dendritic cells, toll-like receptors, and T-cell responses: lessons from viral infections in vivo. Viral Immunol. 18 (2005) 584-594
14. Chinenov Y., and Kerppola T.K. Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 20 (2001) 2438-2452
15. Prinarakis E., Chantzoura E., Thanos D., and Spyrou G. S-glutathionylation of IRF3 regulates IRF3-CBP interaction and activation of the IFN beta pathway. EMBO J. 27 (2008) 865-875
16. Munshi N., Yie Y., Merika M., Senger K., Lomvardas S., Agalioti T., and Thanos D. The IFN-beta enhancer: a paradigm for understanding activation and repression of inducible gene expression. Cold Spring Harb. Symp. Quant. Biol. 64 (1999) 149-159
17. Fujita T., Kimura Y., Miyamoto M., Barsoumian E.L., and Taniguchi T. Induction of endogenous IFN-alpha and IFN-beta genes by a regulatory transcription factor, IRF-1. Nature 337 (1989) 270-272
18. Hiscott J., Alper D., Cohen L., Leblanc J.F., Sportza L., Wong A., and Xanthoudakis S. Induction of human interferon gene expression is associated with a nuclear factor that interacts with the NF-kappa B site of the human immunodeficiency virus enhancer. J. Virol. 63 (1989) 2557-2566
19. Lenardo M.J., Fan C.M., Maniatis T., and Baltimore D. The involvement of NF-kappa B in beta-interferon gene regulation reveals its role as widely inducible mediator of signal transduction. Cell 57 (1989) 287-294
20. Visvanathan K.V., and Goodbourn S. Double-stranded RNA activates binding of NF-kappa B to an inducible element in the human beta-interferon promoter. EMBO J. 8 (1989) 1129-1138
21. Hiscott J., Pitha P., Genin P., Nguyen H., Heylbroeck C., Mamane Y., Algarte M., and Lin R. Triggering the interferon response: the role of IRF-3 transcription factor. J. Interferon Cytokine Res. 19 (1999) 1-13
22. Sato M., Suemori H., Hata N., Asagiri M., Ogasawara K., Nakao K., Nakaya T., Katsuki M., Noguchi S., Tanaka N., and Taniguchi T. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13 (2000) 539-548
23. Sato M., Tanaka N., Hata N., Oda E., and Taniguchi T. Involvement of the IRF family transcription factor IRF-3 in virus-induced activation of the IFN-beta gene. FEBS Lett. 425 (1998) 112-116
24. Wathelet M.G., Lin C.H., Parekh B.S., Ronco L.V., Howley P.M., and Maniatis T. Virus infection induces the assembly of coordinately activated transcription factors on the IFN-beta enhancer in vivo. Mol. Cell 1 (1998) 507-518
25. Du W., and Maniatis T. An ATF/CREB binding site is required for virus induction of the human interferon beta gene [corrected]. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 2150-2154
26. Du W., and Maniatis T. The high mobility group protein HMG I(Y) can stimulate or inhibit DNA binding of distinct transcription factor ATF-2 isoforms. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 11318-11322
27. Thanos D., and Maniatis T. The high mobility group protein HMG I(Y) is required for NF-kappa B-dependent virus induction of the human IFN-beta gene. Cell 71 (1992) 777-789
28. Yie J., Merika M., Munshi N., Chen G., and Thanos D. The role of HMG I(Y) in the assembly and function of the IFN-beta enhanceosome. EMBO J. 18 (1999) 3074-3089
29. Thanos D., and Maniatis T. Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome. Cell 83 (1995) 1091-1100
30. Falvo J.V., Thanos D., and Maniatis T. Reversal of intrinsic DNA bends in the IFN beta gene enhancer by transcription factors and the architectural protein HMG I(Y). Cell 83 (1995) 1101-1111
31. Reeves R., and Beckerbauer L. HMGI/Y proteins: flexible regulators of transcription and chromatin structure. Biochim. Biophys. Acta 1519 (2001) 13-29
32. Falvo J.V., Parekh B.S., Lin C.H., Fraenkel E., and Maniatis T. Assembly of a functional beta interferon enhanceosome is dependent on ATF-2-c-jun heterodimer orientation. Mol. Cell. Biol. 20 (2000) 4814-4825
33. Panne D., Maniatis T., and Harrison S.C. Crystal structure of ATF-2/c-Jun and IRF-3 bound to the interferon-beta enhancer. EMBO J. 23 (2004) 4384-4393
34. Miyamoto M., Fujita T., Kimura Y., Maruyama M., Harada H., Sudo Y., Miyata T., and Taniguchi T. Regulated expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-beta gene regulatory elements. Cell 54 (1988) 903-913
35. Matsuyama T., Kimura T., Kitagawa M., Pfeffer K., Kawakami T., Watanabe N., Kundig T.M., Amakawa R., Kishihara K., Wakeham A., et al. Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development. Cell 75 (1993) 83-97
36. Reis L.F., Ruffner H., Stark G., Aguet M., and Weissmann C. Mice devoid of interferon regulatory factor 1 (IRF-1) show normal expression of type I interferon genes. EMBO J. 13 (1994) 4798-4806
37. Honda K., Yanai H., Negishi H., Asagiri M., Sato M., Mizutani T., Shimada N., Ohba Y., Takaoka A., Yoshida N., and Taniguchi T. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434 (2005) 772-777
38. Lin R., Heylbroeck C., Pitha P.M., and Hiscott J. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell. Biol. 18 (1998) 2986-2996
39. Panne D., McWhirter S.M., Maniatis T., and Harrison S.C. Interferon regulatory factor 3 is regulated by a dual phosphorylation-dependent switch. J. Biol. Chem. 282 (2007) 22816-22822
40. Berkowitz B., Huang D.B., Chen-Park F.E., Sigler P.B., and Ghosh G. The X-ray crystal structure of the NF-kappa B p50.p65 heterodimer bound to the interferon beta-kappa B site. J. Biol. Chem. 277 (2002) 24694-24700
41. Escalante C.R., Yie J., Thanos D., and Aggarwal A.K. Structure of IRF-1 with bound DNA reveals determinants of interferon regulation. Nature 391 (1998) 103-106
42. Qin B.Y., Liu C., Srinath H., Lam S.S., Correia J.J., Derynck R., and Lin K. Crystal structure of IRF-3 in complex with CBP. Structure 13 (2005) 1269-1277
43. Panne D., Maniatis T., and Harrison S.C. An atomic model of the interferon-beta enhanceosome. Cell 129 (2007) 1111-1123
44. Thanos D., and Maniatis T. Identification of the rel family members required for virus induction of the human beta interferon gene. Mol. Cell. Biol. 15 (1995) 152-164
45. Klemm J.D., and Pabo C.O. Oct-1 POU domain-DNA interactions: cooperative binding of isolated subdomains and effects of covalent linkage. Genes Dev. 10 (1996) 27-36
46. Passner J.M., Ryoo H.D., Shen L., Mann R.S., and Aggarwal A.K. Structure of a DNA-bound Ultrabithorax-Extradenticle homeodomain complex. Nature 397 (1999) 714-719
47. Escalante C.R., Brass A.L., Pongubala J.M., Shatova E., Shen L., Singh H., and Aggarwal A.K. Crystal structure of PU.1/IRF-4/DNA ternary complex. Mol. Cell 10 (2002) 1097-1105
48. Kim T.K., Kim T.H., and Maniatis T. Efficient recruitment of TFIIB and CBP-RNA polymerase II holoenzyme by an interferon-beta enhanceosome in vitro. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 12191-12196
49. Kim T.K., and Maniatis T. The mechanism of transcriptional synergy of an in vitro assembled interferon-beta enhanceosome. Mol. Cell 1 (1997) 119-129
50. Merika M., Williams A.J., Chen G., Collins T., and Thanos D. Recruitment of CBP/p300 by the IFN beta enhanceosome is required for synergistic activation of transcription. Mol. Cell 1 (1998) 277-287
51. Escalante C.R., Nistal-Villan E., Shen L., Garcia-Sastre A., and Aggarwal A.K. Structure of IRF-3 bound to the PRDIII-I regulatory element of the human interferon-beta enhancer. Mol. Cell 26 (2007) 703-716
52. Huth J.R., Bewley C.A., Nissen M.S., Evans J.N., Reeves R., Gronenborn A.M., and Clore G.M. The solution structure of an HMG-I(Y)-DNA complex defines a new architectural minor groove binding motif. Nat. Struct. Biol. 4 (1997) 657-665
53. Yie J., Liang S., Merika M., and Thanos D. Intra- and intermolecular cooperative binding of high-mobility-group protein I(Y) to the beta-interferon promoter. Mol. Cell. Biol. 17 (1997) 3649-3662
54. Thomas J.O., and Travers A.A. HMG1 and 2, and related 'architectural' DNA-binding proteins. Trends Biochem. Sci. 26 (2001) 167-174
55. Munshi N., Agalioti T., Lomvardas S., Merika M., Chen G., and Thanos D. Coordination of a transcriptional switch by HMGI(Y) acetylation. Science 293 (2001) 1133-1136
56. Dragan A.I., Carrillo R., Gerasimova T.I., and Privalov P.L. Assembling the human IFN-beta enhanceosome in solution. J. Mol. Biol. 384 (2008) 335-348
57. Agalioti T., Lomvardas S., Parekh B., Yie J., Maniatis T., and Thanos D. Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter. Cell 103 (2000) 667-678
58. Agalioti T., Chen G., and Thanos D. Deciphering the transcriptional histone acetylation code for a human gene. Cell 111 (2002) 381-392
59. Perissi V., Dasen J.S., Kurokawa R., Wang Z., Korzus E., Rose D.W., Glass C.K., and Rosenfeld M.G. Factor-specific modulation of CREB-binding protein acetyltransferase activity. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 3652-3657
60. Suka N., Suka Y., Carmen A.A., Wu J., and Grunstein M. Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol. Cell 8 (2001) 473-479
61. Taatjes D.J., Naar A.M., Andel III F., Nogales E., and Tjian R. Structure, function, and activator-induced conformations of the CRSP coactivator. Science 295 (2002) 1058-1062
62. Jenuwein T., and Allis C.D. Translating the histone code. Science 293 (2001) 1074-1080
63. Roychoudhury M., Sitlani A., Lapham J., and Crothers D.M. Global structure and mechanical properties of a 10-bp nucleosome positioning motif. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 13608-13613
64. Imbalzano A.N., Kwon H., Green M.R., and Kingston R.E. Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature 370 (1994) 481-485
65. de la Cruz X., Lois S., Sanchez-Molina S., and Martinez-Balbas M.A. Do protein motifs read the histone code?. Bioessays 27 (2005) 164-175
66. Kim J.L., Nikolov D.B., and Burley S.K. Co-crystal structure of TBP recognizing the minor groove of a TATA element. Nature 365 (1993) 520-527
67. Lomvardas S., and Thanos D. Nucleosome sliding via TBP DNA binding in vivo. Cell 106 (2001) 685-696
68. Hamiche A., Kang J.G., Dennis C., Xiao H., and Wu C. Histone tails modulate nucleosome mobility and regulate ATP-dependent nucleosome sliding by NURF. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 14316-14321
69. Lomvardas S., and Thanos D. Modifying gene expression programs by altering core promoter chromatin architecture. Cell 110 (2002) 261-271
70. Shrader T.E., and Crothers D.M. Artificial nucleosome positioning sequences. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 7418-7422
71. Koutroubas G., Merika M., and Thanos D. Bypassing the requirements for epigenetic modifications in gene transcription by increasing enhancer strength. Mol. Cell. Biol. 28 (2008) 926-938
72. Du W., Thanos D., and Maniatis T. Mechanisms of transcriptional synergism between distinct virus-inducible enhancer elements. Cell 74 (1993) 887-898
73. Munshi N., Merika M., Yie J., Senger K., Chen G., and Thanos D. Acetylation of HMG I(Y) by CBP turns off IFN beta expression by disrupting the enhanceosome. Mol. Cell 2 (1998) 457-467
74. Senger K., Merika M., Agalioti T., Yie J., Escalante C.R., Chen G., Aggarwal A.K., and Thanos D. Gene repression by coactivator repulsion. Mol. Cell 6 (2000) 931-937
75. Zawatzky R., De Maeyer E., and De Maeyer-Guignard J. Identification of individual interferon-producing cells by in situ hybridization. Proc. Natl. Acad. Sci. U. S. A. 82 (1985) 1136-1140
76. Hu J., Sealfon S.C., Hayot F., Jayaprakash C., Kumar M., Pendleton A.C., Ganee A., Fernandez-Sesma A., Moran T.M., and Wetmur J.G. Chromosome-specific and noisy IFNB1 transcription in individual virus-infected human primary dendritic cells. Nucleic Acids Res. 35 (2007) 5232-5241
77. Hottiger M.O., Felzien L.K., and Nabel G.J. Modulation of cytokine-induced HIV gene expression by competitive binding of transcription factors to the coactivator p300. EMBO J. 17 (1998) 3124-3134
78. Lipniacki T., Paszek P., Brasier A.R., Luxon B.A., and Kimmel M. Stochastic regulation in early immune response. Biophys. J. 90 (2006) 725-742
79. Apostolou E., and Thanos D. Virus infection induces NF-kappaB-dependent interchromosomal associations mediating monoallelic IFN-beta gene expression. Cell 134 (2008) 85-96
80. Agelopoulos M., and Thanos D. Epigenetic determination of a cell-specific gene expression program by ATF-2 and the histone variant macroH2A. EMBO J. 25 (2006) 4843-4853
81. Mukaida N., Okamoto S., Ishikawa Y., and Matsushima K. Molecular mechanism of interleukin-8 gene expression. J. Leukoc. Biol. 56 (1994) 554-558
82. Hoffmann E., Dittrich-Breiholz O., Holtmann H., and Kracht M. Multiple control of interleukin-8 gene expression. J. Leukoc. Biol. 72 (2002) 847-855
83. Allen M.D., Buckle A.M., Cordell S.C., Lowe J., and Bycroft M. The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macroH2A. J. Mol. Biol. 330 (2003) 503-511
84. Kustatscher G., Hothorn M., Pugieux C., Scheffzek K., and Ladurner A.G. Splicing regulates NAD metabolite binding to histone macroH2A. Nat. Struct. Mol. Biol. 12 (2005) 624-625
85. Changolkar L.N., and Pehrson J.R. macroH2A1 histone variants are depleted on active genes but concentrated on the inactive X chromosome. Mol. Cell. Biol. 26 (2006) 4410-4420
86. Chang E.Y., Ferreira H., Somers J., Nusinow D.A., Owen-Hughes T., and Narlikar G.J. MacroH2A allows ATP-dependent chromatin remodeling by SWI/SNF and ACF complexes but specifically reduces recruitment of SWI/SNF. Biochemistry 47 (2008) 13726-13732
87. de Laat W., and Grosveld F. Inter-chromosomal gene regulation in the mammalian cell nucleus. Curr. Opin. Genet. Dev. 17 (2007) 456-464
88. Sexton T., Bantignies F., and Cavalli G. Genomic interactions: chromatin loops and gene meeting points in transcriptional regulation. Semin. Cell Dev. Biol. (2009)
89. Osborne C.S., Chakalova L., Mitchell J.A., Horton A., Wood A.L., Bolland D.J., Corcoran A.E., and Fraser P. Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol. 5 (2007) e192
90. Schoenfelder S., Sexton T., Chakalova L., Cope N.F., Horton A., Andrews S., Kurukuti S., Mitchell J.A., Umlauf D., Dimitrova D.S., Eskiw C.H., Luo Y., Wei C.L., Ruan Y., Bieker J.J., and Fraser P. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat. Genet. 42 (2010) 53-61
91. Kimura H., Sugaya K., and Cook P.R. The transcription cycle of RNA polymerase II in living cells. J. Cell Biol. 159 (2002) 777-782
92. Metivier R., Penot G., Hubner M.R., Reid G., Brand H., Kos M., and Gannon F. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115 (2003) 751-763
93. Wang X., Hussain S., Wang E.J., Li M.O., Garcia-Sastre A., and Beg A.A. Lack of essential role of NF-kappa B p50, RelA, and cRel subunits in virus-induced type 1 IFN expression. J. Immunol. 178 (2007) 6770-6776