Chromatin signatures at Notch-regulated enhancers reveal large-scale changes in H3K56ac upon activation

EMBO Journal

Volumn 34, Issue 14, 2015, Pages 1889-1904

  Skalska, Lenka ^a   Stojnic, Robert ^a,b   Li, Jinghua ^a   Fischer, Bettina ^a,b   Cerda Moya, Gustavo ^a   Sakai, Hiroshi ^c   Tajbakhsh, Shahragim ^c   Russell, Steven ^a,b   Adryan, Boris ^a,b   Bray, Sarah J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c INSTITUT PASTEUR   (France)

Author keywords

CBP Nejire; chromatin state; CSL; H3K56ac; Notch

Indexed keywords

ECDYSONE; HISTONE; HISTONE ACETYLTRANSFERASE; NOTCH RECEPTOR; TRANSCRIPTION FACTOR RUNX; CELL CYCLE PROTEIN; CHROMATIN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; HEY1 PROTEIN, MOUSE; HISTONE ACETYLTRANSFERASE PCAF; LOZENGE PROTEIN, DROSOPHILA; NEJIRE PROTEIN, DROSOPHILA; NOTCH PROTEIN, DROSOPHILA; REPRESSOR PROTEIN; SPACER DNA; SUPPRESSOR OF HAIRLESS PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR;

ACETYLATION; ANIMAL CELL; ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DROSOPHILA; ENHANCER REGION; GENETIC TRANSCRIPTION; HISTONE MODIFICATION; MAMMAL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; CHROMATIN; CYTOLOGY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

ACETYLATION; ANIMALS; CELL CYCLE PROTEINS; CHROMATIN; DNA, INTERGENIC; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ECDYSONE; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; HISTONE ACETYLTRANSFERASES; HISTONES; P300-CBP TRANSCRIPTION FACTORS; RECEPTORS, NOTCH; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

EID: 84948564302     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201489923     Document Type: Article

References (65)

1. Borggrefe T, Oswald F, (2009) The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell Mol Life Sci 66: 1631-1646
2. Bowers EM, Yan G, Mukherjee C, Orry A, Wang L, Holbert MA, Crump NT, Hazzalin CA, Liszczak G, Yuan H, Larocca C, Saldanha SA, Abagyan R, Sun Y, Meyers DJ, Marmorstein R, Mahadevan LC, Alani RM, Cole PA, (2010) Virtual ligand screening of the p300/CBP histone acetyltransferase: identification of a selective small molecule inhibitor. Chem Biol 17: 471-482
3. Bray SJ, (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7: 678-689
4. Bray S, Bernard F, (2010) Notch targets and their regulation. Curr Top Dev Biol 92: 253-275
5. Calo E, Wysocka J, (2013) Modification of enhancer chromatin: what, how, and why? Mol Cell 49: 825-837
6. Castel D, Mourikis P, Bartels SJ, Brinkman AB, Tajbakhsh S, Stunnenberg HG, (2013) Dynamic binding of RBPJ is determined by Notch signaling status. Genes Dev 27: 1059-1071
7. Chanut-Delalande H, Hashimoto Y, Pelissier-Monier A, Spokony R, Dib A, Kondo T, Bohere J, Niimi K, Latapie Y, Inagaki S, Dubois L, Valenti P, Polesello C, Kobayashi S, Moussian B, White KP, Plaza S, Kageyama Y, Payre F, (2014) Pri peptides are mediators of ecdysone for the temporal control of development. Nat Cell Biol 16: 1035-1044
8. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, Boyer LA, Young RA, Jaenisch R, (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A 107: 21931-21936
9. Das C, Lucia MS, Hansen KC, Tyler JK, (2009) CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459: 113-117
10. Das C, Roy S, Namjoshi S, Malarkey CS, Jones DN, Kutateladze TG, Churchill ME, Tyler JK, (2014) Binding of the histone chaperone ASF1 to the CBP bromodomain promotes histone acetylation. Proc Natl Acad Sci U S A 111: E1072-E1081
11. Ferjoux G, Auge B, Boyer K, Haenlin M, Waltzer L, (2007) A GATA/RUNX cis-regulatory module couples Drosophila blood cell commitment and differentiation into crystal cells. Dev Biol 305: 726-734
12. Filippakopoulos P, Knapp S, (2014) Targeting bromodomains: epigenetic readers of lysine acetylation. Nat Rev Drug Discov 13: 337-356
13. Fryer CJ, Lamar E, Turbachova I, Kintner C, Jones KA, (2002) Mastermind mediates chromatin-specific transcription and turnover of the Notch enhancer complex. Genes Dev 16: 1397-1411
14. Gallenkamp D, Gelato KA, Haendler B, Weinmann H, (2014) Bromodomains and their pharmacological inhibitors. ChemMedChem 9: 438-464
15. Gauhar Z, Sun LV, Hua S, Mason CE, Fuchs F, Li TR, Boutros M, White KP, (2009) Genomic mapping of binding regions for the Ecdysone receptor protein complex. Genome Res 19: 1006-1013
16. Guan X, Rastogi N, Parthun MR, Freitas MA, (2013) Discovery of histone modification crosstalk networks by stable isotope labeling of amino acids in cell culture mass spectrometry (SILAC MS). Mol Cell Proteomics 12: 2048-2059
17. Gupta-Rossi N, Le Bail O, Gonen H, Brou C, Logeat F, Six E, Ciechanover A, Israel A, (2001) Functional interaction between SEL-10, an F-box protein, and the nuclear form of activated Notch1 receptor. J Biol Chem 276: 34371-34378
18. Hay DA, Fedorov O, Martin S, Singleton DC, Tallant C, Wells C, Picaud S, Philpott M, Monteiro OP, Rogers CM, Conway SJ, Rooney TP, Tumber A, Yapp C, Filippakopoulos P, Bunnage ME, Muller S, Knapp S, Schofield CJ, Brennan PE, (2014) Discovery and optimization of small-molecule ligands for the CBP/p300 bromodomains. J Am Chem Soc 136: 9308-9319
19. Helin K, Dhanak D, (2013) Chromatin proteins and modifications as drug targets. Nature 502: 480-488
20. Ho JW, Jung YL, Liu T, Alver BH, Lee S, Ikegami K, Sohn KA, Minoda A, Tolstorukov MY, Appert A, Parker SC, Gu T, Kundaje A, Riddle NC, Bishop E, Egelhofer TA, Hu SS, Alekseyenko AA, Rechtsteiner A, Asker D, et al, (2014) Comparative analysis of metazoan chromatin organization. Nature 512: 449-452
21. Housden BE, Fu AQ, Krejcí A, Bernard F, Fischer B, Tavare S, Russell S, Bray SJ, (2013) Transcriptional dynamics elicited by a short pulse of notch activation involves feed-forward regulation by E(spl)/Hes genes. PLoS Genet 9: e1003162
22. Ilagan MX, Lim S, Fulbright M, Piwnica-Worms D, Kopan R, (2011) Real-time imaging of notch activation with a luciferase complementation-based reporter. Sci Signal 4: rs7
23. Jin S, Mutvei AP, Chivukula IV, Andersson ER, Ramskold D, Sandberg R, Lee KL, Kronqvist P, Mamaeva V, Ostling P, Mpindi JP, Kallioniemi O, Screpanti I, Poellinger L, Sahlgren C, Lendahl U, (2013) Non-canonical Notch signaling activates IL-6/JAK/STAT signaling in breast tumor cells and is controlled by p53 and IKKalpha/IKKbeta. Oncogene 32: 4892-4902
24. Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, Ernst J, Sabo PJ, Larschan E, Gorchakov AA, Gu T, Linder-Basso D, Plachetka A, Shanower G, Tolstorukov MY, Luquette LJ, Xi R, Jung YL, Park RW, Bishop EP, Canfield TK, et al, (2011) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471: 480-485
25. Kopan R, Ilagan MX, (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137: 216-233
26. Kouzarides T, (2007) Chromatin modifications and their function. Cell 128: 693-705
27. Kovall RA, Blacklow SC, (2010) Mechanistic insights into Notch receptor signaling from structural and biochemical studies. Curr Top Dev Biol 92: 31-71
28. Krejcí A, Bray S, (2007) Notch activation stimulates transient and selective binding of Su(H)/CSL to target enhancers. Genes Dev 21: 1322-1327
29. Krejcí A, Bernard F, Housden BE, Collins S, Bray SJ, (2009) Direct response to Notch activation: signaling crosstalk and incoherent logic. Sci Signal 2: ra1
30. Lake RJ, Tsai PF, Choi I, Won KJ, Fan HY, (2014) RBPJ, the major transcriptional effector of Notch signaling, remains associated with chromatin throughout mitosis, suggesting a role in mitotic bookmarking. PLoS Genet 10: e1004204
31. Lalonde ME, Cheng X, Cote J, (2014) Histone target selection within chromatin: an exemplary case of teamwork. Genes Dev 28: 1029-1041
32. Louvi A, Artavanis-Tsakonas S, (2012) Notch and disease: a growing field. Semin Cell Dev Biol 23: 473-480
33. Marquardt S, Escalante-Chong R, Pho N, Wang J, Churchman LS, Springer M, Buratowski S, (2014) A chromatin-based mechanism for limiting divergent noncoding transcription. Cell 157: 1712-1723
34. Marshall NF, Price DH, (1995) Purification of P-TEFb, a transcription factor required for the transition into productive elongation. J Biol Chem 270: 12335-12338
35. Miele L, Golde T, Osborne B, (2006) Notch signaling in cancer. Curr Mol Med 6: 905-918
36. Neumann H, Hancock SM, Buning R, Routh A, Chapman L, Somers J, Owen-Hughes T, van Noort J, Rhodes D, Chin JW, (2009) A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol Cell 36: 153-163
37. North JA, Shimko JC, Javaid S, Mooney AM, Shoffner MA, Rose SD, Bundschuh R, Fishel R, Ottesen JJ, Poirier MG, (2012) Regulation of the nucleosome unwrapping rate controls DNA accessibility. Nucleic Acids Res 40: 10215-10227
38. Ntziachristos P, Lim JS, Sage J, Aifantis I, (2014) From fly wings to targeted cancer therapies: a centennial for notch signaling. Cancer Cell 25: 318-334
39. Oswald F, Tauber B, Dobner T, Bourteele S, Kostezka U, Adler G, Liptay S, Schmid RM, (2001) p300 acts as a transcriptional coactivator for mammalian Notch-1. Mol Cell Biol 21: 7761-7774
40. Radtke F, Raj K, (2003) The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nat Rev Cancer 3: 756-767
41. Roy M, Pear WS, Aster JC, (2007) The multifaceted role of Notch in cancer. Curr Opin Genet Dev 17: 52-59
42. Sekiya T, Muthurajan UM, Luger K, Tulin AV, Zaret KS, (2009) Nucleosome-binding affinity as a primary determinant of the nuclear mobility of the pioneer transcription factor FoxA. Genes Dev 23: 804-809
43. Shimko JC, North JA, Bruns AN, Poirier MG, Ottesen JJ, (2011) Preparation of fully synthetic histone H3 reveals that acetyl-lysine 56 facilitates protein binding within nucleosomes. J Mol Biol 408: 187-204
44. Shlyueva D, Stelzer C, Gerlach D, Yanez-Cuna JO, Rath M, Boryn LM, Arnold CD, Stark A, (2014) Hormone-responsive enhancer-activity maps reveal predictive motifs, indirect repression, and targeting of closed chromatin. Mol Cell 54: 180-192
45. Simon M, North JA, Shimko JC, Forties RA, Ferdinand MB, Manohar M, Zhang M, Fishel R, Ottesen JJ, Poirier MG, (2011) Histone fold modifications control nucleosome unwrapping and disassembly. Proc Natl Acad Sci U S A 108: 12711-12716
46. Smith E, Shilatifard A, (2014) Enhancer biology and enhanceropathies. Nat Struct Mol Biol 21: 210-219
47. Swygert SG, Peterson CL, (2014) Chromatin dynamics: interplay between remodeling enzymes and histone modifications. Biochim Biophys Acta 1839: 728-736
48. Tan Y, Xue Y, Song C, Grunstein M, (2013) Acetylated histone H3K56 interacts with Oct4 to promote mouse embryonic stem cell pluripotency. Proc Natl Acad Sci U S A 110: 11493-11498
49. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ, (2007) How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 14: 1025-1040
50. Terriente-Felix A, Li J, Collins S, Mulligan A, Reekie I, Bernard F, Krejcí A, Bray S, (2013) Notch cooperates with Lozenge/Runx to lock haemocytes into a differentiation programme. Development 140: 926-937
51. Thummel CS, (1995) From embryogenesis to metamorphosis: the regulation and function of Drosophila nuclear receptor superfamily members. Cell 83: 871-877
52. Toedling J, Skylar O, Krueger T, Fischer JJ, Sperling S, Huber W, (2007) Ringo-an R/Bioconductor package for analyzing ChIP-chip readouts. BMC Bioinformatics 8: 221
53. Tsai CC, Kao HY, Yao TP, McKeown M, Evans RM, (1999) SMRTER, a Drosophila nuclear receptor coregulator, reveals that EcR-mediated repression is critical for development. Mol Cell 4: 175-186
54. Wallberg AE, Pedersen K, Lendahl U, Roeder RG, (2002) p300 and PCAF act cooperatively to mediate transcriptional activation from chromatin templates by Notch intracellular domains in vitro. Mol Cell Biol 22: 7812-7819
55. Wang H, Zou J, Zhao B, Johannsen E, Ashworth T, Wong H, Pear WS, Schug J, Blacklow SC, Arnett KL, Bernstein BE, Kieff E, Aster JC, (2012) Genome-wide analysis reveals conserved and divergent features of Notch1/RBPJ binding in human and murine T-lymphoblastic leukemia cells. Proc Natl Acad Sci U S A 108: 14908-14913
56. Wang H, Zang C, Taing L, Arnett KL, Wong YJ, Pear WS, Blacklow SC, Liu XS, Aster JC, (2014) NOTCH1-RBPJ complexes drive target gene expression through dynamic interactions with superenhancers. Proc Natl Acad Sci U S A 111: 705-710
57. Watanabe S, Radman-Livaja M, Rando OJ, Peterson CL, (2014) A histone acetylation switch regulates H2A.Z deposition by the SWR-C remodeling enzyme. Science 340: 195-199
58. Williams SK, Truong D, Tyler JK, (2008) Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc Natl Acad Sci U S A 105: 9000-9005
59. de Wit E, van Steensel B, (2009) Chromatin domains in higher eukaryotes: insights from genome-wide mapping studies. Chromosoma 118: 25-36
60. Xie W, Song C, Young NL, Sperling AS, Xu F, Sridharan R, Conway AE, Garcia BA, Plath K, Clark AT, Grunstein M, (2009) Histone H3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells. Mol Cell 33: 417-427
61. Xu F, Zhang K, Grunstein M, (2005) Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121: 375-385
62. Yanez-Cuna JO, Arnold CD, Stampfel G, Boryn LM, Gerlach D, Rath M, Stark A, (2014) Dissection of thousands of cell type-specific enhancers identifies dinucleotide repeat motifs as general enhancer features. Genome Res 24: 1147-1156
63. Yu Z, Wu H, Chen H, Wang R, Liang X, Liu J, Li C, Deng WM, Jiao R, (2013) CAF-1 promotes Notch signaling through epigenetic control of target gene expression during Drosophila development. Development 140: 3635-3644
64. Zaret KS, Carroll JS, (2011) Pioneer transcription factors: establishing competence for gene expression. Genes Dev 25: 2227-2241
65. Zhang Z, Yang Q, Sun G, Chen S, He Q, Li S, Liu Y, (2014) Histone H3K56 acetylation is required for quelling-induced small RNA production through its role in homologous recombination. J Biol Chem 289: 9365-9371