Cells adapt to the epigenomic disruption caused by histone deacetylase inhibitors through a coordinated, chromatin-mediated transcriptional response

Epigenetics and Chromatin

Volumn 8, Issue 1, 2015, Pages

  Halsall, John A ^a   Turan, Nil ^a   Wiersma, Maaike ^a   Turner, Bryan M ^a  

^a NONE

Author keywords

Chromatin; Gene expression; Histone deacetylase inhibitors; Histone modification; Polycomb complex; Suberoylanilide hydroxamic acid; Valproic acid

Indexed keywords

HISTONE DEACETYLASE INHIBITOR; HISTONE H3; METHYLTRANSFERASE; TRANSCRIPTION FACTOR EZH1; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; VALPROIC ACID;

ACETYLATION; ARTICLE; CELL FUNCTION; CHROMATIN; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; EPIGENETICS; GENE CLUSTER; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; PHENOTYPE; PRIORITY JOURNAL; TRANSCRIPTION INITIATION SITE; UPREGULATION;

EID: 84941884474     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/s13072-015-0021-9     Document Type: Article

References (89)

1. Johnsson A, Durand-Dubief M, Xue-Franzén Y, Rönnerblad M, Ekwall K, Wright A. HAT-HDAC interplay modulates global histone H3K14 acetylation in gene-coding regions during stress. EMBO Rep. 2009;10:1009-14.
2. Marmorstein R, Trievel RC. Histone modifying enzymes: structures, mechanisms, and specificities. Biochim Biophys Acta. 2009;1789:58-68.
3. Covault J, Chalkley R. The identification of distinct populations of acetylated histone. J Biol Chem. 1980;255:9110-6.
4. Nightingale KP, Gendreizig S, White DA, Bradbury C, Hollfelder F, Turner BM. Cross-talk between histone modifications in response to histone deacetylase inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation. J Biol Chem. 2007;282:4408-16.
5. Ekwall K. Genome-wide analysis of HDAC function. Trends Genet. 2005;21:608-15.
6. Kasper LH, Qu C, Obenauer JC, McGoldrick DJ, Brindle PK. Genome-wide and single-cell analyses reveal a context dependent relationship between CBP recruitment and gene expression. Nucleic Acids Res. 2014;42:11363-82.
7. Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell. 2009;138:1019-31.
8. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125:315-26.
9. Weake VM, Dyer JO, Seidel C, Box A, Swanson SK, Peak A, et al. Post-transcription initiation function of the ubiquitous SAGA complex in tissue-specific gene activation. Genes Dev. 2011;25:1499-509.
10. Fan J, Krautkramer KA, Feldman JL, Denu JM. Metabolic regulation of histone post-translational modifications. ACS Chem Biol. 2015;10:95-108.
11. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693-705.
12. Nightingale KP, O'Neill LP, Turner BM. Histone modifications: signalling receptors and potential elements of a heritable epigenetic code. Curr Opin Genet Dev. 2006;16:125-36.
13. Oliver SS, Denu JM. Dynamic interplay between histone H3 modifications and protein interpreters: emerging evidence for a "histone language". ChemBioChem. 2011;12:299-307.
14. Turner BM. Defining an epigenetic code. Nat Cell Biol. 2007;9:2-6.
15. Turner BM. The adjustable nucleosome: an epigenetic signaling module. Trends Genet. 2012;28:436-44.
16. Allegra P, Sterner R, Clayton DF, Allfrey VG. Affinity chromatographic purification of nucleosomes containing transcriptionally active DNA sequences. J Mol Biol. 1987;196:379-88.
17. Covault J, Perry M, Chalkley R. Effects of histone hyperacetylation and hypoacetylation on RNA synthesis in HTC cells. J Biol Chem. 1982;257:13433-40.
18. Johnson EM, Sterner R, Allfrey VG. Altered nucleosomes of active nucleolar chromatin contain accessible histone H3 in its hyperacetylated forms. J Biol Chem. 1987;262:6943-6.
19. Kurdistani SK, Tavazoie S, Grunstein M. Mapping global histone acetylation patterns to gene expression. Cell. 2004;117:721-33.
20. Kellis M, Wold B, Snyder MP, Bernstein BE, Kundaje A, Marinov GK, et al. Defining functional DNA elements in the human genome. Proc Natl Acad Sci USA. 2014;111:6131-8.
21. Schübeler D, MacAlpine DM, Scalzo D, Wirbelauer C, Kooperberg C, van Leeuwen F, et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 2004;18:1263-71.
22. Roh T-Y, Cuddapah S, Zhao K. Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev. 2005;19:542-52.
23. Roh T, Wei G, Farrell CM, Zhao K. Genome-wide prediction of conserved and nonconserved enhancers by histone acetylation patterns. Genome Res. 2006;17:74-81.
24. Verdin E, Ott M. 50 years of protein acetylation: from gene regulation to epigenetics, metabolism and beyond. Nat Rev Mol Cell Biol. 2014;16:258-64.
25. Gelbart ME, Larschan E, Peng S, Park PJ, Kuroda MI. Drosophila MSL complex globally acetylates H4K16 on the male X chromosome for dosage compensation. Nat Struct Mol Biol. 2009;16:825-32.
26. Turner BM, Birley AJ, Lavender J. Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell. 1992;69:375-84.
27. Taylor GCA, Eskeland R, Hekimoglu-Balkan B, Pradeepa MM, Bickmore WA. H4K16 acetylation marks active genes and enhancers of embryonic stem cells, but does not alter chromatin compaction. Genome Res. 2013;23:2053-65.
28. Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F, et al. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57-74.
29. Jin Q, Yu L-R, Wang L, Zhang Z, Kasper LH, Lee J-E, et al. Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J. 2011;30:249-62.
30. Pasini D, Malatesta M, Jung HR, Walfridsson J, Willer A, Olsson L, et al. Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of Polycomb group target genes. Nucleic Acids Res. 2010;38:4958-69.
31. Schmitges FW, Prusty AB, Faty M, Stützer A, Lingaraju GM, Aiwazian J, et al. Histone methylation by PRC2 is inhibited by active chromatin marks. Mol Cell. 2011;42:330-41.
32. Boudadi E, Stower H, Halsall JA, Rutledge CE, Leeb M, Wutz A, et al. The histone deacetylase inhibitor sodium valproate causes limited transcriptional change in mouse embryonic stem cells but selectively overrides Polycomb-mediated Hoxb silencing. Epigenetics Chromatin. 2013;6:11.
33. Hezroni H, Sailaja BS, Meshorer E. Pluripotency-related, valproic acid (VPA)-induced genome-wide histone H3 lysine 9 (H3K9) acetylation patterns in embryonic stem cells. J Biol Chem. 2011;286:35977-88.
34. Evason K, Collins JJ, Huang C, Hughes S, Kornfeld K. Valproic acid extends Caenorhabditis elegans lifespan. Aging Cell. 2008;7:305-17.
35. Forthun RB, Sengupta T, Skjeldam HK, Lindvall JM, McCormack E, Gjertsen BT, et al. Cross-species functional genomic analysis identifies resistance genes of the histone deacetylase inhibitor valproic acid. PLoS One. 2012;7:e48992.
36. Gerstner T, Bell N, König S. Oral valproic acid for epilepsy-long-term experience in therapy and side effects. Expert Opin Pharmacother. 2008;9:285-92.
37. Duenas-Gonzalez A, Candelaria M, Perez-Plascencia C, Perez-Cardenas E, de la Cruz-Hernandez E, Herrera LA. Valproic acid as epigenetic cancer drug: preclinical, clinical and transcriptional effects on solid tumors. Cancer Treat Rev. 2008;34:206-22.
38. Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L. The role of short-chain fatty acids in health and disease. Adv Immunol. 2014;121:91-119.
39. West AC, Johnstone RW. New and emerging HDAC inhibitors for cancer treatment. J Clin Invest. 2014;124:30-9.
40. Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene. 2007;26:5541-52.
41. Halsall J, Gupta V, O'Neill LP, Turner BM, Nightingale KP. Genes are often sheltered from the global histone hyperacetylation induced by HDAC inhibitors. PLoS One. 2012;7:e33453.
42. Rada-Iglesias A, Enroth S, Ameur A, Koch CM, Clelland GK, Respuela-Alonso P, et al. Butyrate mediates decrease of histone acetylation centered on transcription start sites and down-regulation of associated genes. Genome Res. 2007;17:708-19.
43. Peart MJ, Smyth GK, van Laar RK, Bowtell DD, Richon VM, Marks PA, et al. Identification and functional significance of genes regulated by structurally different histone deacetylase inhibitors. Proc Natl Acad Sci USA. 2005;102:3697-702.
44. Van Lint C, Emiliani S, Verdin E. The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation. Gene Expr. 1996;5:245-53.
45. Smith CL. A shifting paradigm: histone deacetylases and transcriptional activation. BioEssays. 2008;30:15-24.
46. Yang X-J, Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol. 2008;9:206-18.
47. Kelly RDW, Cowley SM. The physiological roles of histone deacetylase (HDAC) 1 and 2: complex co-stars with multiple leading parts. Biochem Soc Trans. 2013;41:741-9.
48. Jamaladdin S, Kelly RDW, O'Regan L, Dovey OM, Hodson GE, Millard CJ, et al. Histone deacetylase (HDAC) 1 and 2 are essential for accurate cell division and the pluripotency of embryonic stem cells. Proc Natl Acad Sci USA. 2014;111:9840-5.
49. Seto E, Yoshida M. Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb Perspect Biol. 2014;6:a018713.
50. Lombardi PM, Cole KE, Dowling DP, Christianson DW. Structure, mechanism, and inhibition of histone deacetylases and related metalloenzymes. Curr Opin Struct Biol. 2011;21:735-43.
51. Fu M, Liu M, Sauve AA, Jiao X, Zhang X, Wu X, et al. Hormonal control of androgen receptor function through SIRT1. Mol Cell Biol. 2006;26:8122-35.
52. Welsbie DS, Xu J, Chen Y, Borsu L, Scher HI, Rosen N, et al. Histone deacetylases are required for androgen receptor function in hormone-sensitive and castrate-resistant prostate cancer. Cancer Res. 2009;69:958-66.
53. Downey M, Johnson JR, Davey NE, Newton BW, Johnson TL, Galaang S, et al. Acetylome profiling reveals overlap in the regulation of diverse processes by sirtuins, gcn5, and esa1. Mol Cell Proteom. 2015;14:162-76.
54. Jack J, Rotroff D, Motsinger-Reif A. Lymphoblastoid cell lines models of drug response: successes and lessons from this pharmacogenomic model. Curr Mol Med. 2014;14:833-40.
55. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.
56. Huang Q, Cheung AP, Zhang Y, Huang H-F, Auersperg N, Leung PCK. Effects of growth differentiation factor 9 on cell cycle regulators and ERK42/44 in human granulosa cell proliferation. Am J Physiol Endocrinol Metab. 2009;296:E1344-53.
57. Omtzigt JG, Nau H, Los FJ, Pijpers L, Lindhout D. The disposition of valproate and its metabolites in the late first trimester and early second trimester of pregnancy in maternal serum, urine, and amniotic fluid: effect of dose, co-medication, and the presence of spina bifida. Eur J Clin Pharmacol. 1992;43:381-8.
58. Bantscheff M, Hopf C, Savitski MM, Dittmann A, Grandi P, Michon A-M, et al. Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes. Nat Biotechnol. 2011;29:255-65.
59. Di Croce L, Helin K. Transcriptional regulation by Polycomb group proteins. Nat Struct Mol Biol. 2013;20:1147-55.
60. Konze KD, Ma A, Li F, Barsyte-Lovejoy D, Parton T, Macnevin CJ, et al. An orally bioavailable chemical probe of the Lysine Methyltransferases EZH2 and EZH1. ACS Chem Biol. 2013;8:1324-34.
61. Xu B, On DM, Ma A, Parton T, Konze KD, Pattenden SG, et al. Selective inhibition of EZH2 and EZH1 enzymatic activity by a small molecule suppresses MLL-rearranged leukemia. Blood. 2015;125:346-57.
62. Leeb M, Pasini D, Novatchkova M, Jaritz M, Helin K, Wutz A. Polycomb complexes act redundantly to repress genomic repeats and genes. Genes Dev. 2010;24:265-76.
63. Saunders N, Dicker A, Popa C, Jones S, Dahler A. Histone deacetylase inhibitors as potential anti-skin cancer agents. Cancer Res. 1999;59:399-404.
64. Yoshida M, Beppu T. Reversible arrest of proliferation of rat 3Y1 fibroblasts in both the G1 and G2 phases by trichostatin A. Exp Cell Res. 1988;177:122-31.
65. Kim B, Park H, Salvador LA, Serrano PE, Kwan JC, Zeller SL, et al. Evaluation of class I HDAC isoform selectivity of largazole analogues. Bioorg Med Chem Lett. 2014;24:3728-31.
66. Newkirk TL, Bowers AA, Williams RM. Discovery, biological activity, synthesis and potential therapeutic utility of naturally occurring histone deacetylase inhibitors. Nat Prod Rep. 2009;26:1293-320.
67. Sauer J, Richter KK, Pool-Zobel BL. Physiological concentrations of butyrate favorably modulate genes of oxidative and metabolic stress in primary human colon cells. J Nutr Biochem. 2007;18:736-45.
68. Yadav H, Lee J-H, Lloyd J, Walter P, Rane SG. Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion. J Biol Chem. 2013;288:25088-97.
69. Yoshida M, Nomura S, Beppu T. Effects of trichostatins on differentiation of murine erythroleukemia cells. Cancer Res. 1987;47:3688-91.
70. Johnke J, Cohen Y, de Leeuw M, Kushmaro A, Jurkevitch E, Chatzinotas A. Multiple micro-predators controlling bacterial communities in the environment. Curr Opin Biotechnol. 2014;27:185-90.
71. Fujioka M, Sun G, Jaynes JB. The Drosophila eve insulator Homie promotes eve expression and protects the adjacent gene from repression by polycomb spreading. PLoS Genet. 2013;9:e1003883.
72. Schwartz YB, Pirrotta V. Ruled by ubiquitylation: a new order for polycomb recruitment. Cell Rep. 2014;8:321-5.
73. Gil J, O'Loghlen A. PRC1 complex diversity: where is it taking us? Trends Cell Biol. 2014;24:632-41.
74. Hansen KH, Bracken AP, Pasini D, Dietrich N, Gehani SS, Monrad A, et al. A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol. 2008;10:1291-300.
75. Voigt P, Leroy G, Drury WJ, Zee BM, Son J, Beck DB, et al. Asymmetrically modified nucleosomes. Cell. 2012;151:181-93.
76. Gehani SS, Agrawal-Singh S, Dietrich N, Christophersen NS, Helin K, Hansen K. Polycomb group protein displacement and gene activation through MSK-dependent H3K27me3S28 phosphorylation. Mol Cell. 2010;39:886-900.
77. Lau PNI, Cheung P. Histone code pathway involving H3 S28 phosphorylation and K27 acetylation activates transcription and antagonizes polycomb silencing. Proc Natl Acad Sci USA. 2011;108:2801-6.
78. Sawicka A, Hartl D, Goiser M, Pusch O, Stocsits RR, Tamir IM, et al. H3S28 phosphorylation is a hallmark of the transcriptional response to cellular stress. Genome Res. 2014;24:1808-20.
79. Bock I, Dhayalan A, Kudithipudi S, Brandt O, Rathert P, Jeltsch A. Detailed specificity analysis of antibodies binding to modified histone tails with peptide arrays. Epigenetics. 2011;6:256-63.
80. Alder O, Lavial F, Helness A, Brookes E, Pinho S, Chandrashekran A, et al. Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment. Development. 2010;137:2483-92.
81. Azuara V, Perry P, Sauer S, Spivakov M, Jørgensen HF, John RM, et al. Chromatin signatures of pluripotent cell lines. Nat Cell Biol. 2006;8:532-8.
82. Stock JK, Giadrossi S, Casanova M, Brookes E, Vidal M, Koseki H, et al. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat Cell Biol. 2007;9:1428-35.
83. Landeira D, Sauer S, Poot R, Dvorkina M, Mazzarella L, Jørgensen HF, et al. Jarid2 is a PRC2 component in embryonic stem cells required for multi-lineage differentiation and recruitment of PRC1 and RNA polymerase II to developmental regulators. Nat Cell Biol. 2010;12:618-24.
84. Rowe M, Young LS, Crocker J, Stokes H, Henderson S, Rickinson AB. Epstein-Barr virus (EBV)-associated lymphoproliferative disease in the SCID mouse model: implications for the pathogenesis of EBV-positive lymphomas in man. J Exp Med. 1991;173:147-58.
85. White DA, Belyaev ND, Turner BM. Preparation of site-specific antibodies to acetylated histones. Methods. 1999;19:417-24.
86. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques. 2003;34:374-8.
87. O'Neill LP, Turner BM. Immunoprecipitation of native chromatin: NChIP. Methods. 2003;31:76-82.
88. Quail MA, Swerdlow H, Turner DJ. Improved protocols for the illumina genome analyzer sequencing system. Curr Protoc Hum Genet. 2009;18:18.2.
89. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357-9.