Acetylation of histone H3 at lysine 64 regulates nucleosome dynamics and facilitates transcription

eLife

Volumn 2014, Issue 3, 2014, Pages

  Di Cerbo, Vincenzo ^a,b   Mohn, Fabio ^c   Ryan, Daniel P ^d,l   Montellier, Emilie ^e,f   Kacem, Salim ^g   Tropberger, Philipp ^a,b   Kallis, Eleni ^h   Holzner, Monika ^h   Hoerner, Leslie ⁱ   Feldmann, Angelika ⁱ   Richter, Florian Martin ^b   Bannister, Andrew J ^j,k   Mittler, Gerhard ^b   Michaelis, Jens ^h   Khochbin, Saadi ^e,f   Feil, Robert ^g   Schuebeler, Dirk ⁱ   Owen Hughes, Tom ^d   Daujat, Sylvain ^a   Schneider, Robert ^a  

^a CNRS   (France)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^c INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

^e INSERM   (France)

^f INSTITUT ALBERT BONNIOT   (France)

^g INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^h UNIVERSITY OF ULM   (Germany)

ⁱ FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^j UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^k UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^l Australian National University   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIBODY; HISTONE H3; SMALL INTERFERING RNA; HISTONE; HISTONE ACETYLTRANSFERASE PCAF; LYSINE; NUCLEOSOME; XENOPUS PROTEIN;

ACETYLATION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA TRANSCRIPTION; DYNAMICS; EUCHROMATIN; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION; GENE INDUCTION; GENE MUTATION; GENOTYPE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEOSOME; POLYMERASE CHAIN REACTION; WESTERN BLOTTING; 3T3 CELL LINE; ANIMAL; CHEMISTRY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONFORMATION; EMBRYONIC STEM CELL; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; KINETICS; MALE; METABOLISM; METHYLATION; NEURAL STEM CELL; PROTEIN CONFORMATION; PROTEIN PROCESSING; PROTEIN STABILITY; TRANSCRIPTION INITIATION; XENOPUS LAEVIS;

ACETYLATION; ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; EMBRYONIC STEM CELLS; HISTONES; HUMANS; KINETICS; LYSINE; MALE; METHYLATION; MICE; NEURAL STEM CELLS; NIH 3T3 CELLS; NUCLEIC ACID CONFORMATION; NUCLEOSOMES; P300-CBP TRANSCRIPTION FACTORS; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84898765622     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01632     Document Type: Article

References (60)

1. Antonik M, Felekyan S, Gaiduk A, Seidel CAM. 2006. Separating structural heterogeneities from stochastic variations in fluorescence resonance energy transfer distributions via photon distribution analysis. The Journal of Physical Chemistry B 110:6970-6978. doi: 10.1021/jp057257+.
2. Bibel M, Richter J, Lacroix E, Barde Y-A. 2007. Generation of a defined and uniform population of CNS progenitors and neurons from mouse embryonic stem cells. Nature Protocols 2:1034-1043. doi: 10.1038/nprot.2007.147.
3. Bönisch C, Schneider K, Pünzeler S, Wiedemann SM, Bielmeier C, Bocola M, Eberl HC, Kuegel W, Neumann J, Kremmer E, Leonhardt H, Mann M, Michaelis J, Schermelleh L, Hake SB. 2012. H2A.Z.2.2 is an alternatively spliced H2A. Z variant that causes severe nucleosome destabilization. Nucleic Acids Research 40:5951-5964. doi: 10.1093/nar/gks267.
4. Clapier CR, Cairns BR. 2009. The biology of chromatin remodeling complexes. Annual Review of Biochemistry 78:273-304. doi: 10.1146/annurev.biochem.77.062706.153223.
5. Cosgrove MS, Boeke JD, Wolberger C. 2004. Regulated nucleosome mobility and the histone code. Nature Structure Molecular Biology 11:1037-1043. doi: 10.1038/nsmb851.
6. Cosgrove MS. 2007. Histone proteomics and the epigenetic regulation of nucleosome mobility. Expert Review of Proteomics 4:465-478. doi: 10.1586/14789450.4.4.465.
7. 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. Proceedings of the National Academy of Sciences of the United States of America 107:21931-21936. doi: 10.1073/pnas.1016071107.
8. Cuthbert GL, Daujat S, Snowden AW, Erdjument-Bromage H, Hagiwara T, Yamada M, Schneider R, Gregory PD, Tempst P, Bannister AJ, Kouzarides T. 2004. Histone deimination antagonizes arginine methylation. Cell 118:545-553. doi: 10.1016/j.cell.2004.08.020.
9. Daujat S, Bauer UM, Shah V, Turner B, Berger S, Kouzarides T. 2002. Crosstalk between CARM1 methylation and CBP acetylation on histone H3. Current Biology 12:2090-2097. doi: 10.1016/S0960-9822(02)01387-8.
10. Daujat S, Weiss T, Mohn F, Lange UC, Ziegler-Birling C, Zeissler U, Lappe M, Schubeler D, Torres-Padilla ME, Schneider R. 2009. H3K64 trimethylation marks heterochromatin and is dynamically remodeled during developmental reprogramming. Nature Structure Molecular Biology 16:777-781. doi: 10.1038/nsmb.1629.
11. Davey CA, Richmond TJ. 2002. DNA-dependent divalent cation binding in the nucleosome core particle. Proceedings of the National Academy of Sciences of the United States of America 99:11169-11174. doi: 10.1073/pnas.172271399.
12. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ. 2002. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. Journal of Molecular Biology 319:1097-1113. doi: 10.1016/S0022-2836(02)00386-8.
13. Dedon PC, Soults JA, Allis CD, Gorovsky MA. 1991. A simplified formaldehyde fixation and immunoprecipitation technique for studying protein-DNA interactions. Analytical Biochemistry 197:83-90. doi: 10.1016/0003-2697(91)90359-2.
14. Edgar R, Domrachev M, Lash AE. 2002. Gene expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acid Research 30:207-210. doi: 10.1093/nar/30.1.207.
15. Ferreira H, Flaus A, Owen-Hughes T. 2007. Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms. Journal of Molecular Biology 374:563-579. doi: 10.1016/j.jmb.2007.09.059.
16. Flaus A, Martin DMA, Barton GJ, Owen-Hughes T. 2006. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Research 34:2887-2905. doi: 10.1093/nar/gkl295.
17. Flaus A, Owen-Hughes T. 2003. Dynamic properties of nucleosomes during thermal and ATP-driven mobilization. Molecular and Cellular Biology 23:7767-7779. doi: 10.1128/MCB.23.21.7767-7779.2003.
18. Flaus A, Richmond TJ. 1998. Positioning and stability of nucleosomes on MMTV 3'LTR sequences. Journal of Molecular Biology 275:427-441. doi: 10.1006/jmbi.1997.1464.
19. Gansen A, Hieb AR, Böhm V, Tóth K, Langowski J. 2013. Closing the gap between single molecule and bulk FRET analysis of nucleosomes. PLOS ONE 8:e57018. doi: 10.1371/journal.pone.0057018.
20. Garcia BA. 2009. Mass spectrometric analysis of histone variants and Post-translational modifications. Frontiers in Bioscience (Scholar Edition) 1:142-153. doi: 10.2741/s14.
21. Gaucher J, Boussouar F, Montellier E, Curtet S, Buchou T, Bertrand S, Hery P, Jounier S, Depaux A, Vitte AL, Guardiola P, Pernet K, Debernardi A, Lopez F, Holota H, Imbert J, Wolgemuth DJ, Gerard M, Rousseaux S, Khochbin S. 2012. Bromodomain-dependent stage-specific male genome programming by Brdt. The EMBO Journal 31:3809-3820. doi: 10.1038/emboj.2012.233.
22. Gaucher J, Reynoird N, Montellier E, Boussouar F, Rousseaux S, Khochbin S. 2010. From meiosis to postmeiotic events: the secrets of histone disappearance. The FEBS Journal 277:599-604. doi: 10.1111/j.1742-4658.2009.07504.x.
23. Gregory RI, Feil R. 1999. Analysis of chromatin in limited numbers of cells: a PCR-SSCP based assay of allele-specific nuclease sensitivity. Nucleic Acids Research 27:e32.
24. Gutierrez JL, Chandy M, Carrozza MJ, Workman JL. 2007. Activation domains drive nucleosome eviction by SWI/SNF. The EMBO Journal 26:730-740. doi: 10.1038/sj.emboj.7601524.
25. Hake SB, Garcia BA, Duncan EM, Kauer M, Dellaire G, Shabanowitz J, Bazett-Jones DP, Allis CD, Hunt DF. 2006. Expression patterns and post-translational modifications associated with mammalian histone H3 variants. The Journal of Biological Chemistry 281:559-568. doi: 10.1074/jbc.M509266200.
26. Ito T, Ikehara T, Nakagawa T, Kraus WL, Muramatsu M. 2000. p300-mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone. Genes & Development 14:1899-1907.
27. Kotaja N, Kimmins S, Brancorsini S, Hentsch D, Vonesch JL, Davidson I, Parvinen M, Sassone-Corsi P. 2004. Preparation, isolation and characterization of stage-specific spermatogenic cells for cellular and molecular analysis. Nature Methods 1:249-254. doi: 10.1038/nmeth1204-249.
28. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128:693-705. doi: 10.1016/j.cell.2007.02.005.
29. Kraus WL, Kadonaga JT. 1998. p300 and estrogen receptor cooperatively activate transcription via differential enhancement of initiation and reinitiation. Genes & Development 12:331-342. doi: 10.1101/gad.12.3.331.
30. Lange UC, Siebert S, Wossidlo M, Weiss T, Ziegler-Birling C, Walter J, Torres-Padilla ME, Daujat S, Schneider R. 2013. Dissecting the role of H3K64me3 in mouse pericentromeric heterochromatin. Nature Communications 4:2233. doi: 10.1038/ncomms3233.
31. Lienert F, Mohn F, Tiwari VK, Baubec T, Roloff TC, Gaidatzis D, Stadler MB, Schübeler D. 2011. Genomic prevalence of heterochromatic H3K9me2 and transcription do not discriminate pluripotent from terminally differentiated cells. PLOS Genetics 7:e1002090. doi: 10.1371/journal.pgen.1002090.
32. Manohar M, Mooney AM, North JA, Nakkula RJ, Picking JW, Edon A, Fishel R, Poirier MG, Ottesen JJ. 2009. Acetylation of histone H3 at the nucleosome dyad alters DNA-histone binding. The Journal of Biological Chemistry 284:23312-23321. doi: 10.1074/jbc.M109.003202.
33. Mersfelder EL, Parthun MR. 2006. The tale beyond the tail: histone core domain modifications and the regulation of chromatin structure. Nucleic Acids Research 34:2653-2662. doi: 10.1093/nar/gkl338.
34. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553-560. doi: 10.1038/nature06008.
35. Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB, Bibel M, Schubeler D. 2008. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Molecular Cell 30:755-766. doi: 10.1016/j.molcel.2008.05.007.
36. Mortensen P, Gouw JW, Olsen JV, Ong SE, Rigbolt KT, Bunkenborg J, Cox J, Foster LJ, Heck AJ, Blagoev B, Andersen JS, Mann M. 2010. MSQuant, an open source platform for mass spectrometry-based quantitative proteomics. Journal of Proteome Research 9:393-403. doi: 10.1021/pr900721e.
37. 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. Molecular Cell 36:153-163. doi: 10.1016/j.molcel.2009.07.027.
38. Nir E, Michalet X, Hamadani KM, Laurence TA, Neuhauser D, Kovchegov Y, Weiss S. 2006. Short-noise limited single-molecule FRET histograms: comparison between theory and experiments. The Journal of Physical Chemistry B 110:22103-22124. doi: 10.1021/jp063483n.
39. Orlando V, Strutt H, Paro R. 1997. Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods 11:205-214. doi: 10.1006/meth.1996.0407.
40. Pannetier M, Julien E, Schotta G, Tardat M, Sardet C, Jenuwein T, Feil R. 2008. PR-SET7 and SUV4-20H regulate H4 lysine-20 methylation at imprinting control regions in the mouse. EMBO Reports 9:998-1005. doi: 10.1038/embor.2008.147.
41. Park YJ, Dyer PN, Tremethick DJ, Luger K. 2004. A new fluorescence resonance energy transfer approach demonstrates that the histone variant H2AZ stabilizes the histone octamer within the nucleosome. The Journal of Biological Chemistry 279:24274-24282. doi: 10.1074/jbc.M313152200.
42. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470:279-283. doi: 10.1038/nature09692.
43. Rappsilber J, Mann M, Ishihama Y. 2007. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nature Protocols 2:1896-1906. doi: 10.1038/nprot.2007.261.
44. Russel LD, Ettlin RA, Sinha Hikim AP, Clegg ED. 1990. Histological and histopathological evaluation of the testis. Clearwater, USA:Cache River Press.
45. Ryan DP, Sundaramoorthy R, Martin D, Singh V, Owen-Hughes T. 2011. The DNA-binding domain of the Chd1 chromatin-remodelling enzyme contains SANT and SLIDE domains. The EMBO Journal 30:2596-2609. doi: 10.1038/emboj.2011.166.
46. Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, Moore IK, Wang JP, Widom J. 2006. A genomic code for nucleosome positioning. Nature 442:772-778. doi: 10.1038/nature04979.
47. Sharma N, Nyborg JK. 2008. The coactivators CBP/p300 and the histone chaperone NAP1 promote transcription-independent nucleosome eviction at the HTLV-1 promoter. Proceedings of the National Academy of Sciences of the United States of America 105:7959-7963. doi: 10.1073/pnas.0800534105.
48. Singh P, Han L, Rivas GE, Lee D-H, Nicholson TB, Larson GP, Chen T, Szabó PE. 2010. Allele-specific H3K79 Di-versus trimethylation distinguishes opposite parental alleles at imprinted regions. Molecular and Cellular Biology 30:2693-2707. doi: 10.1128/MCB.01537-09.
49. Smyth GK. 2004. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology 3, article 3:doi: 10.2202/1544-6115.1027.
50. Smyth GK, Speed T. 2003. Normalization of cDNA microarray data. Methods 31:265-273. doi: 10.1016/S1046-2023(03)00155-5.
51. Somers J, Owen-Hughes T. 2009. Mutations to the histone H3 alpha N region selectively alter the outcome of ATP-dependent nucleosome-remodelling reactions. Nucleic Acids Research 37:2504-2513. doi: 10.1093/nar/gkp114.
52. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Schöler A, Van Nimwegen E, Wirbelauer C, Oakeley EJ, Gaidatzis D, Tiwari VK, Schübeler D. 2011. DNA-binding factors shape the shape the mouse methylome at distal regulatory regions. Nature 480:490-495.
53. Tan M, Luo H, Lee S, Jin F, Yang JS, Montellier E, Buchou T, Cheng Z, Rousseaux S, Rajagopal N, Lu Z, Ye Z, Zhu Q, Wysocka J, Ye Y, Khochbin S, Ren B, Zhao Y. 2011. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146:1016-1028. doi: 10.1016/j.cell.2011.08.008.
54. Thåström A, Lowary PT, Widom J. 2004. Measurement of histone-DNA interaction free energy in nucleosomes. Methods 33:33-44. doi: 10.1016/j.ymeth.2003.10.018.
55. Trelle MB, Jensen ON. 2008. Utility of immonium ions for assignment of epsilon-N-acetyllysine-containing peptides by tandem mass spectrometry. Analytical Chemistry 80:3422-3430. doi: 10.1021/ac800005n.
56. Tropberger P, Pott S, Keller C, Kamieniarz-Gdula K, Caron M, Richter F, Li G, Mittler G, Liu ET, Buhler M, Margueron R, Schneider R. 2013. Regulation of transcription through acetylation of H3K122 on the lateral surface of the histone octamer. Cell 152:859-872. doi: 10.1016/j.cell.2013.01.032.
57. Tropberger P, Schneider R. 2010. Going global: novel histone modifications in the globular domain of H3. Epigenetics 5:112-117. doi: 10.4161/epi.5.2.11075.
58. Tropberger P, Schneider R. 2013. Scratching the (lateral) surface of chromatin regulation by histone modifications. Nature Structure Molecular Biology 20:657-661. doi: 10.1038/nsmb.2581.
59. Umlauf D, Goto Y, Cao R, Cerqueira F, Wagschal A, Zhang Y, Feil R. 2004. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nature Genetics 36:1296-1300. doi: 10.1038/ng1467.
60. Waldmann T, Izzo A, Kamieniarz K, Richter F, Vogler C, Sarg B, Lindner H, Young NL, Mittler G, Garcia BA, Schneider R. 2011. Methylation of H2AR29 is a novel repressive PRMT6 target. Epigenetics & Chromatin 4:11. doi: 10.1186/1756-8935-4-11.