Logic of the inflammation-associated transcriptional response

Advances in Immunology

Volumn 119, Issue , 2013, Pages 107-133

  Tarakhovsky, Alexander ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Bromodomain inhibitor; Chromatin; Epigenetics; Gene expression; Histone; Immune response; Inflammation; Pathogen

Indexed keywords

HISTONE; PROTEIN BRD4; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; GENE CONTROL; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; HUMAN; INFLAMMATION; INNATE IMMUNITY; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA SPLICING; RNA TRANSLATION; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

EID: 84880433569     PISSN: 00652776     EISSN: 15578445     Source Type: Book Series    
DOI: 10.1016/B978-0-12-407707-2.00004-7     Document Type: Chapter

References (138)

1. Adelman K., Kennedy M.A., Nechaev S., Gilchrist D.A., Muse G.W., Chinenov Y., et al. Immediate mediators of the inflammatory response are poised for gene activation through RNA polymerase II stalling. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:18207-18212.
2. Adelman K., Lis J.T. Promoter-proximal pausing of RNA polymerase II: Emerging roles in metazoans. Nature Reviews. Genetics 2012, 13:720-731.
3. Alon U. Network motifs: Theory and experimental approaches. Nature Reviews. Genetics 2007, 8:450-461.
4. Amit I., Citri A., Shay T., Lu Y., Katz M., Zhang F., et al. A module of negative feedback regulators defines growth factor signaling. Nature Genetics 2007, 39:503-512.
5. Amit I., Regev A., Hacohen N. Strategies to discover regulatory circuits of the mammalian immune system. Nature Reviews. Immunology 2011, 11:873-880.
6. Ashida H., Kim M., Schmidt-Supprian M., Ma A., Ogawa M., Sasakawa C. A bacterial E3 ubiquitin ligase IpaH9.8 targets NEMO/IKKgamma to dampen the host NF-kappaB-mediated inflammatory response. Nature Cell Biology 2010, 12:66-73. sup pp. 61-69.
7. Bak P. Self-organized criticality. Physical Review A 1988, 38:364-374.
8. Bak P., Tang C., Wiesenfeld K. Self-organized criticality: An explanation of the 1/f noise. Physical Review Letters 1987, 59:381-384.
9. Balazsi G., van Oudenaarden A., Collins J.J. Cellular decision making and biological noise: From microbes to mammals. Cell 2011, 144:910-925.
10. Bardwell A.J., Abdollahi M., Bardwell L. Anthrax lethal factor-cleavage products of MAPK (mitogen-activated protein kinase) kinases exhibit reduced binding to their cognate MAPKs. The Biochemical Journal 2004, 378:569-577.
11. Bar-Even A., Paulsson J., Maheshri N., Carmi M., O'Shea E., Pilpel Y., et al. Noise in protein expression scales with natural protein abundance. Nature Genetics 2006, 38:636-643.
12. Barkai N., Shilo B.Z. Variability and robustness in biomolecular systems. Molecular Cell 2007, 28:755-760.
13. Belkina A.C., Denis G.V. BET domain co-regulators in obesity, inflammation and cancer. Nature Reviews. Cancer 2012, 12:465-477.
14. Belkina A.C., Nikolajczyk B.S., Denis G.V. BET protein function is required for inflammation: Brd2 genetic disruption and BET inhibitor JQ1 impair mouse macrophage inflammatory responses. Journal of Immunology 2013, 190(7):3670-3678.
15. Bhatt D.M., Pandya-Jones A., Tong A.J., Barozzi I., Lissner M.M., Natoli G., et al. Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions. Cell 2012, 150:279-290.
16. Bierne H., Cossart P. When bacteria target the nucleus: The emerging family of nucleomodulins. Cellular Microbiology 2012, 14:622-633.
17. Bierne H., Hamon M., Cossart P. Epigenetics and bacterial infections. Cold Spring Harbor Perspectives in Medicine 2012, 2:a010272.
18. Biswas S.K., Lopez-Collazo E. Endotoxin tolerance: New mechanisms, molecules and clinical significance. Trends in Immunology 2009, 30:475-487.
19. Blake W.J., Kaem M., Cantor C.R., Collins J.J. Noise in eukaryotic gene expression. Nature 2003, 422:633-637.
20. Brennan D.F., Barford D. Eliminylation: A post-translational modification catalyzed by phosphothreonine lyases. Trends in Biochemical Sciences 2009, 34:108-114.
21. Brent M.M., Marmorstein R. Ankyrin for methylated lysines. Nature Structural & Molecular Biology 2008, 15:221-222.
22. Cai L., Dalal C.K., Elowitz M.B. Frequency-modulated nuclear localization bursts coordinate gene regulation. Nature 2008, 455:485-490.
23. Cairns B.R. Chromatin remodeling: Insights and intrigue from single-molecule studies. Nature Structural & Molecular Biology 2007, 14:989-996.
24. Cairns B.R. The logic of chromatin architecture and remodelling at promoters. Nature 2009, 461:193-198.
25. Calado D.P., Paixao T., Holmberg D., Haury M. Stochastic monoallelic expression of IL-10 in T cells. Journal of Immunology 2006, 177:5358-5364.
26. Carlson J.M., Swindle G.H. Self-organized criticality: Sandpiles, singularities, and scaling. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:6712-6719.
27. Cheong R., Rhee A., Wang C.J., Nemenman I., Levchenko A. Information transduction capacity of noisy biochemical signaling networks. Science 2011, 334:354-358.
28. Chubb J.R., Liverpool T.B. Bursts and pulses: Insights from single cell studies into transcriptional mechanisms. Current Opinion in Genetics & Development 2010, 20:478-484.
29. Collins R.E., Northrop J.P., Horton J.R., Lee D.Y., Zhang X., Stallcup M.R., et al. The ankyrin repeats of G9a and GLP histone methyltransferases are mono- and dimethyllysine binding modules. Nature Structural & Molecular Biology 2008, 15:245-250.
30. Covert M.W., Leung T.H., Gaston J.E., Baltimore D. Achieving stability of lipopolysaccharide-induced NF-kappaB activation. Science 2005, 309:1854-1857.
31. Davuluri R.V., Grosse I., Zhang M.Q. Computational identification of promoters and first exons in the human genome. Nature Genetics 2001, 29:412-417.
32. Dawson M.A., Prinjha R.K., Dittmann A., Giotopoulos G., Bantscheff M., Chan W.I., et al. Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature 2011, 478:529-533.
33. Denis G.V., Green M.R. A novel, mitogen-activated nuclear kinase is related to a Drosophila developmental regulator. Genes & Development 1996, 10:261-271.
34. Dey A., Chitsaz F., Abbasi A., Misteli T., Ozato K. The double bromodomain protein Brd4 binds to acetylated chromatin during interphase and mitosis. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:8758-8763.
35. Diribarne G., Bensaude O. 7SK RNA, a non-coding RNA regulating P-TEFb, a general transcription factor. RNA Biology 2009, 6:122-128.
36. Dover G.A. The Origins of Order-Self-Organization and Selection in Evolution-Kauffman, Sa. Nature 1993, 365:704-706.
37. Elowitz M.B., Levine A.J., Siggia E.D., Swain P.S. Stochastic gene expression in a single cell. Science 2002, 297:1183-1186.
38. Fang T.C., Schaefer U., Mecklenbrauker I., Stienen A., Dewell S., Chen M.S., et al. Histone H3 lysine 9 di-methylation as an epigenetic signature of the interferon response. The Journal of Experimental Medicine 2012, 209:661-669.
39. Filippakopoulos P., Knapp S. The bromodomain interaction module. FEBS Letters 2012, 586:2692-2704.
40. Filippakopoulos P., Picaud S., Mangos M., Keates T., Lambert J.P., Barsyte-Lovejoy D., et al. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 2012, 149:214-231.
41. Filippakopoulos P., Qi J., Picaud S., Shen Y., Smith W.B., Fedorov O., et al. Selective inhibition of BET bromodomains. Nature 2010, 468:1067-1073.
42. Fonseca G.J., Thillainadesan G., Yousef A.F., Ablack J.N., Mossman K.L., Torchia J., et al. Adenovirus evasion of interferon-mediated innate immunity by direct antagonism of a cellular histone posttranslational modification. Cell Host & Microbe 2012, 11:597-606.
43. Ford E., Thanos D. The transcriptional code of human IFN-beta gene expression. Biochimica et Biophysica Acta 2010, 1799:328-336.
44. Foster S.L., Hargreaves D.C., Medzhitov R. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 2007, 447:972-978.
45. Foster S.L., Medzhitov R. Gene-specific control of the TLR-induced inflammatory response. Clinical Immunology 2009, 130:7-15.
46. Garcia-Garcia J.C., Rennoll-Bankert K.E., Pelly S., Milstone A.M., Dumler J.S. Silencing of host cell CYBB gene expression by the nuclear effector AnkA of the intracellular pathogen Anaplasma phagocytophilum. Infection and Immunity 2009, 77:2385-2391.
47. Ghisletti S., Barozzi I., Mietton F., Polletti S., De Santa F., Venturini E., et al. Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity 2010, 32:317-328.
48. Guo L., Hu-Li J., Paul W.E. Probabilistic regulation of IL-4 production in Th2 cells: Accessibility at the Il4 locus. Immunity 2004, 20:193-203.
49. Gutschow M.V., Hughey J.J., Ruggero N.A., Bajar B.T., Valle S.D., Covert M.W. Single-cell and population NF-kappaB dynamic responses depend on lipopolysaccharide preparation. PloS One 2013, 8:e53222.
50. Hager G.L., McNally J.G., Misteli T. Transcription dynamics. Molecular Cell 2009, 35:741-753.
51. Hale B.G., Randall R.E., Ortin J., Jackson D. The multifunctional NS1 protein of influenza A viruses. The Journal of General Virology 2008, 89:2359-2376.
52. Hargreaves D.C., Horng T., Medzhitov R. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 2009, 138:129-145.
53. Haye K., Burmakina S., Moran T., Garcia-Sastre A., Fernandez-Sesma A. The NS1 protein of a human influenza virus inhibits type I interferon production and the induction of antiviral responses in primary human dendritic and respiratory epithelial cells. Journal of Virology 2009, 83:6849-6862.
54. Hollander G.A. On the stochastic regulation of interleukin-2 transcription. Seminars in Immunology 1999, 11:357-367.
55. Ivaldi M.S., Karam C.S., Corces V.G. Phosphorylation of histone H3 at Ser10 facilitates RNA polymerase II release from promoter-proximal pausing in Drosophila. Genes & Development 2007, 21:2818-2831.
56. Jaehning J.A. The Paf1 complex: Platform or player in RNA polymerase II transcription?. Biochimica et Biophysica Acta 2010, 1799:379-388.
57. Kaplan N., Moore I.K., Fondufe-Mittendorf Y., Gossett A.J., Tillo D., Field Y., et al. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 2009, 458:362-366.
58. Karn J. A new BET on the control of HIV latency. Cell Cycle 2013, 12:545-546.
59. Kim J., Guermah M., McGinty R.K., Lee J.S., Tang Z., Milne T.A., et al. RAD6-mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 2009, 137:459-471.
60. Kim J., Roeder R.G. Direct Bre1-Paf1 complex interactions and RING finger-independent Bre1-Rad6 interactions mediate histone H2B ubiquitylation in yeast. The Journal of Biological Chemistry 2009, 284:20582-20592.
61. Kochs G., Garcia-Sastre A., Martinez-Sobrido L. Multiple anti-interferon actions of the influenza A virus NS1 protein. Journal of Virology 2007, 81:7011-7021.
62. Kondo Y., Issa J.P. Enrichment for histone H3 lysine 9 methylation at Alu repeats in human cells. The Journal of Biological Chemistry 2003, 278:27658-27662.
63. Kornberg R.D., Lorch Y. Chromatin structure and transcription. Annual Review of Cell Biology 1992, 8:563-587.
64. Larson D.R. What do expression dynamics tell us about the mechanism of transcription?. Current Opinion in Genetics & Development 2011, 21:591-599.
65. Lee T.K., Covert M.W. High-throughput, single-cell NF-kappaB dynamics. Current Opinion in Genetics & Development 2010, 20:677-683.
66. Lee J.M., Lee J.S., Kim H., Kim K., Park H., Kim J.Y., et al. EZH2 generates a methyl degron that is recognized by the DCAF1/DDB1/CUL4 E3 ubiquitin ligase complex. Molecular Cell 2012, 48:572-586.
67. Lee J.S., Shukla A., Schneider J., Swanson S.K., Washburn M.P., Florens L., et al. Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 2007, 131:1084-1096.
68. Lionnet T., Singer R.H. Transcription goes digital. EMBO Reports 2012, 13:313-321.
69. Litvak V., Ramsey S.A., Rust A.G., Zak D.E., Kennedy K.A., Lampano A.E., et al. Function of C/EBPdelta in a regulatory circuit that discriminates between transient and persistent TLR4-induced signals. Nature Immunology 2009, 10:437-443.
70. Locke J.C., Young J.W., Fontes M., Hernandez Jimenez M.J., Elowitz M.B. Stochastic pulse regulation in bacterial stress response. Science 2011, 334:366-369.
71. Luo Z., Lin C., Shilatifard A. The super elongation complex (SEC) family in transcriptional control. Nature Reviews. Molecular Cell Biology 2012, 13:543-547.
72. Marazzi I., Ho J.S., Kim J., Manicassamy B., Dewell S., Albrecht R.A., et al. Suppression of the antiviral response by an influenza histone mimic. Nature 2012, 483:428-433.
73. McBride A.A., McPhillips M.G., Oliveira J.G. Brd4: Tethering, segregation and beyond. Trends in Microbiology 2004, 12:527-529.
74. Medzhitov R. TLR-mediated innate immune recognition. Seminars in Immunology 2007, 19:1-2.
75. Medzhitov R. Origin and physiological roles of inflammation. Nature 2008, 454:428-435.
76. Medzhitov R., Horng T. Transcriptional control of the inflammatory response. Nature Reviews. Immunology 2009, 9:692-703.
77. Medzhitov R., Schneider D.S., Soares M.P. Disease tolerance as a defense strategy. Science 2012, 335:936-941.
78. Mujtaba S., Zeng L., Zhou M.M. Structure and acetyl-lysine recognition of the bromodomain. Oncogene 2007, 26:5521-5527.
79. Murphy K.M. Fate vs choice: The immune system reloaded. Immunologic Research 2005, 32:193-200.
80. Nagler J., Hauert C., Schuster H.G. Self-organized criticality in a nutshell. Physical Review. E, Statistical Physics, Plasmas, Fluids, and Related Interdisciplinary Topics 1999, 60:2706-2709.
81. Natoli G. Specialized chromatin patterns in the control of inflammatory gene expression. Current Topics in Microbiology and Immunology 2011, 349:61-72.
82. Natoli G., Ghisletti S., Barozzi I. The genomic landscapes of inflammation. Genes & Development 2011, 25:101-106.
83. Nechaev S., Adelman K. Promoter-proximal Pol II: When stalling speeds things up. Cell Cycle 2008, 7:1539-1544.
84. Nicodeme E., Jeffrey K.L., Schaefer U., Beinke S., Dewell S., Chung C.W., et al. Suppression of inflammation by a synthetic histone mimic. Nature 2010, 468:1119-1123.
85. Novershtern N., Subramanian A., Lawton L.N., Mak R.H., Haining W.N., McConkey M.E., et al. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell 2011, 144:296-309.
86. Ozbudak E.M., Thattai M., Kurtser I., Grossman A.D., van Oudenaarden A. Regulation of noise in the expression of a single gene. Nature Genetics 2002, 31:69-73.
87. Park J., Kim K.J., Choi K.S., Grab D.J., Dumler J.S. Anaplasma phagocytophilum AnkA binds to granulocyte DNA and nuclear proteins. Cellular Microbiology 2004, 6:743-751.
88. Paulsson J. Summing up the noise in gene networks. Nature 2004, 427:415-418.
89. Pedraza J.M., Paulsson J. Effects of molecular memory and bursting on fluctuations in gene expression. Science 2008, 319:339-343.
90. Peterlin B.M., Price D.H. Controlling the elongation phase of transcription with P-TEFb. Molecular Cell 2006, 23:297-305.
91. Petesch S.J., Lis J.T. Overcoming the nucleosome barrier during transcript elongation. Trends in Genetics 2012, 28:285-294.
92. Price D.H. P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase II. Molecular and Cellular Biology 2000, 20:2629-2634.
93. Rahman S., Sowa M.E., Ottinger M., Smith J.A., Shi Y., Harper J.W., et al. The Brd4 extraterminal domain confers transcription activation independent of pTEFb by recruiting multiple proteins, including NSD3. Molecular and Cellular Biology 2011, 31:2641-2652.
94. Raj A., van Oudenaarden A. Single-molecule approaches to stochastic gene expression. Annual Review of Biophysics 2009, 38:255-270.
95. Rall S.C., Okinaka R.T., Strniste G.F. Histone composition of nucleosomes isolated from cultured Chinese hamster cells. Biochemistry 1977, 16:4940-4944.
96. Ramirez-Carrozzi V.R., Braas D., Bhatt D.M., Cheng C.S., Hong C., Doty K.R., et al. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 2009, 138:114-128.
97. Ramsey S.A., Klemm S.L., Zak D.E., Kennedy K.A., Thorsson V., Li B., et al. Uncovering a macrophage transcriptional program by integrating evidence from motif scanning and expression dynamics. PLoS Computational Biology 2008, 4:e1000021.
98. Raser J.M., O'Shea E.K. Noise in gene expression: Origins, consequences, and control. Science 2005, 309:2010-2013.
99. Raymond B., Batsche E., Boutillon F., Wu Y.Z., Leduc D., Balloy V., et al. Anthrax lethal toxin impairs IL-8 expression in epithelial cells through inhibition of histone H3 modification. PLoS Pathogens 2009, 5:e1000359.
100. Rice A.P. P-TEFb as a target to reactivate latent HIV: Two Brds are now in hand. Cell Cycle 2013, 12:392-393.
101. Roach J.C., Smith K.D., Strobe K.L., Nissen S.M., Haudenschild C.D., Zhou D., et al. Transcription factor expression in lipopolysaccharide-activated peripheral-blood-derived mononuclear cells. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:16245-16250.
102. Robinson P.A. Scaling properties of self-organized criticality. Physical Review. E, Statistical Physics, Plasmas, Fluids, and Related Interdisciplinary Topics 1994, 49:3919-3926.
103. Rohde J.R., Breitkreutz A., Chenal A., Sansonetti P.J., Parsot C. Type III secretion effectors of the IpaH family are E3 ubiquitin ligases. Cell Host & Microbe 2007, 1:77-83.
104. Rosenfeld S. Global consensus theorem and self-organized criticality: Unifying principles for understanding self-organization, swarm intelligence and mechanisms of carcinogenesis. Gene Regulation and Systems Biology 2013, 7:23-39.
105. Rosenfeld N., Elowitz M.B., Alon U. Negative autoregulation speeds the response times of transcription networks. Journal of Molecular Biology 2002, 323:785-793.
106. Saccani S., Natoli G. Dynamic changes in histone H3 Lys 9 methylation occurring at tightly regulated inducible inflammatory genes. Genes & Development 2002, 16:2219-2224.
107. Salter-Cid L., Du Pasquier L., Flajnik M. RING3 is linked to the Xenopus major histocompatibility complex. Immunogenetics 1996, 44:397-399.
108. Sampath S.C., Marazzi I., Yap K.L., Sampath S.C., Krutchinsky A.N., Mecklenbrauker I., et al. Methylation of a histone mimic within the histone methyltransferase G9a regulates protein complex assembly. Molecular Cell 2007, 27:596-608.
109. Saxonov S., Berg P., Brutlag D.L. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:1412-1417.
110. Schroder S., Cho S., Zeng L., Zhang Q., Kaehlcke K., Mak L., et al. Two-pronged binding with bromodomain-containing protein 4 liberates positive transcription elongation factor b from inactive ribonucleoprotein complexes. The Journal of Biological Chemistry 2012, 287:1090-1099.
111. Segal E., Widom J. From DNA sequence to transcriptional behaviour: A quantitative approach. Nature Reviews. Genetics 2009, 10:443-456.
112. Segal E., Widom J. Poly(dA:dT) tracts: Major determinants of nucleosome organization. Current Opinion in Structural Biology 2009, 19:65-71.
113. Shay T., Jojic V., Zuk O., Rothamel K., Puyraimond-Zemmour D., Feng T., et al. Conservation and divergence in the transcriptional programs of the human and mouse immune systems. Proceedings of the National Academy of Sciences of the United States of America 2013, 110:2946-2951.
114. Smale S.T. Selective transcription in response to an inflammatory stimulus. Cell 2010, 140:833-844.
115. Smith J.A., White E.A., Sowa M.E., Powell M.L., Ottinger M., Harper J.W., et al. Genome-wide siRNA screen identifies SMCX, EP400, and Brd4 as E2-dependent regulators of human papillomavirus oncogene expression. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:3752-3757.
116. Sobhian B., Laguette N., Yatim A., Nakamura M., Levy Y., Kiernan R., et al. HIV-1 Tat assembles a multifunctional transcription elongation complex and stably associates with the 7SK snRNP. Molecular Cell 2010, 38:439-451.
117. Stevense M., Muramoto T., Muller I., Chubb J.R. Digital nature of the immediate-early transcriptional response. Development 2010, 137:579-584.
118. Suganuma T., Workman J.L. Signals and combinatorial functions of histone modifications. Annual Review of Biochemistry 2011, 80:473-499.
119. Suganuma T., Workman J.L. MAP kinases and histone modification. Journal of Molecular Cell Biology 2012, 4:348-350.
120. Tan R.Z., van Oudenaarden A. Transcript counting in single cells reveals dynamics of rDNA transcription. Molecular Systems Biology 2010, 6:358.
121. Taniguchi Y., Matsuzaka Y., Fujimoto H., Miyado K., Kohda A., Okumura K., et al. Nucleotide sequence of the ring3 gene in the class II region of the mouse MHC and its abundant expression in testicular germ cells. Genomics 1998, 51:114-123.
122. Taverna S.D., Li H., Ruthenburg A.J., Allis C.D., Patel D.J. How chromatin-binding modules interpret histone modifications: Lessons from professional pocket pickers. Nature Structural & Molecular Biology 2007, 14:1025-1040.
123. Tay S., Hughey J.J., Lee T.K., Lipniacki T., Quake S.R., Covert M.W. Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature 2010, 466:267-271.
124. Thorpe K.L., Abdulla S., Kaufman J., Trowsdale J., Beck S. Phylogeny and structure of the RING3 gene. Immunogenetics 1996, 44:391-396.
125. Wagner G.P. The Origins of Order-Self-Organization and Selection in Evolution-Kauffman, Sa. Science 1993, 260:1531-1533.
126. Weake V.M., Workman J.L. Inducible gene expression: Diverse regulatory mechanisms. Nature Reviews. Genetics 2010, 11:426-437.
127. Wen B., Wu H., Loh Y.H., Briem E., Daley G.Q., Feinberg A.P. Euchromatin islands in large heterochromatin domains are enriched for CTCF binding and differentially DNA-methylated regions. BMC Genomics 2012, 13:566.
128. Wen B., Wu H., Shinkai Y., Irizarry R.A., Feinberg A.P. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nature Genetics 2009, 41:246-250.
129. Xiao T., Kao C.F., Krogan N.J., Sun Z.W., Greenblatt J.F., Osley M.A., et al. Histone H2B ubiquitylation is associated with elongating RNA polymerase II. Molecular and Cellular Biology 2005, 25:637-651.
130. You J., Croyle J.L., Nishimura A., Ozato K., Howley P.M. Interaction of the bovine papillomavirus E2 protein with Brd4 tethers the viral DNA to host mitotic chromosomes. Cell 2004, 117:349-360.
131. Zak D.E., Aderem A. Systems biology of innate immunity. Immunological Reviews 2009, 227:264-282.
132. Zeng L., Zhou M.M. Bromodomain: An acetyl-lysine binding domain. FEBS Letters 2002, 513:124-128.
133. Zhao M., Zhang J., Phatnani H., Scheu S., Maniatis T. Stochastic expression of the interferon-beta gene. PLoS Biology 2012, 10:e1001249.
134. Zhou Q., Li T., Price D.H. RNA polymerase II elongation control. Annual Review of Biochemistry 2012, 81:119-143.
135. Zhu Y., Li H., Long C., Hu L., Xu H., Liu L., et al. Structural insights into the enzymatic mechanism of the pathogenic MAPK phosphothreonine lyase. Molecular Cell 2007, 28:899-913.
136. Zhu B., Nethery K.A., Kuriakose J.A., Wakeel A., Zhang X., McBride J.W. Nuclear translocated Ehrlichia chaffeensis ankyrin protein interacts with a specific adenine-rich motif of host promoter and intronic Alu elements. Infection and Immunity 2009, 77:4243-4255.
137. Zippo A., De Robertis A., Serafini R., Oliviero S. PIM1-dependent phosphorylation of histone H3 at serine 10 is required for MYC-dependent transcriptional activation and oncogenic transformation. Nature Cell Biology 2007, 9:932-944.
138. Zippo A., Serafini R., Rocchigiani M., Pennacchini S., Krepelova A., Oliviero S. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 2009, 138:1122-1136.