Acetyl-methyllysine marks chromatin at active transcription start sites.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
Oct 2023
Historique:
received: 19 08 2021
accepted: 23 08 2023
medline: 23 10 2023
pubmed: 21 9 2023
entrez: 21 9 2023
Statut: ppublish

Résumé

Lysine residues in histones and other proteins can be modified by post-translational modifications that encode regulatory information

Identifiants

pubmed: 37731000
doi: 10.1038/s41586-023-06565-9
pii: 10.1038/s41586-023-06565-9
doi:

Substances chimiques

Chromatin 0
Histones 0
Lysine K3Z4F929H6
Peptides 0
Histone Deacetylases EC 3.5.1.98
BRD2 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

173-179

Subventions

Organisme : NICHD NIH HHS
ID : DP2 HD083992
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM137117
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM141313
Pays : United States

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Wang, Z. A. & Cole, P. A. The chemical biology of reversible lysine post-translational modifications. Cell Chem. Biol. 27, 953–969 (2020).
pubmed: 32698016 pmcid: 7487139 doi: 10.1016/j.chembiol.2020.07.002
Allfrey, V. G., Faulkner, R. & Mirsky, A. E. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc. Natl Acad. Sci. USA 51, 786–794 (1964).
pubmed: 14172992 pmcid: 300163 doi: 10.1073/pnas.51.5.786
Allis, C. D. & Jenuwein, T. The molecular hallmarks of epigenetic control. Nat. Rev. Genet. 17, 487–500 (2016).
pubmed: 27346641 doi: 10.1038/nrg.2016.59
Muller, M. M. & Muir, T. W. Histones: at the crossroads of peptide and protein chemistry. Chem. Rev. 115, 2296–2349 (2015).
pubmed: 25330018 doi: 10.1021/cr5003529
Fuhs, S. R. et al. Monoclonal 1- and 3-phosphohistidine antibodies: new tools to study histidine phosphorylation. Cell 162, 198–210 (2015).
pubmed: 26140597 pmcid: 4491144 doi: 10.1016/j.cell.2015.05.046
Hori, T. et al. Histone H4 Lys 20 monomethylation of the CENP-A nucleosome is essential for kinetochore assembly. Dev. Cell 29, 740–749 (2014).
pubmed: 24960696 pmcid: 4081567 doi: 10.1016/j.devcel.2014.05.001
Jorgensen, S., Schotta, G. & Sorensen, C. S. Histone H4 lysine 20 methylation: key player in epigenetic regulation of genomic integrity. Nucleic Acids Res. 41, 2797–2806 (2013).
pubmed: 23345616 pmcid: 3597678 doi: 10.1093/nar/gkt012
Chen, Y. et al. Lysine propionylation and butyrylation are novel post-translational modifications in histones. Mol. Cell. Proteomics 6, 812–819 (2007).
pubmed: 17267393 doi: 10.1074/mcp.M700021-MCP200
Garcia, B. A. et al. Chemical derivatization of histones for facilitated analysis by mass spectrometry. Nat. Protoc. 2, 933–938 (2007).
pubmed: 17446892 pmcid: 4627699 doi: 10.1038/nprot.2007.106
Hseiky, A., Crespo, M., Kieffer-Jaquinod, S., Fenaille, F. & Pflieger, D. Small mass but strong information: diagnostic ions provide crucial clues to correctly identify histone lysine modifications. Proteomes 9, 18 (2021).
pubmed: 33922761 pmcid: 8167651 doi: 10.3390/proteomes9020018
Muroski, J. M., Fu, J. Y., Nguyen, H. H., Ogorzalek Loo, R. R. & Loo, J. A. Leveraging immonium ions for targeting acyl-lysine modifications in proteomic datasets. Proteomics 21, e2000111 (2021).
pubmed: 32896103 doi: 10.1002/pmic.202000111
Wan, N. et al. Cyclic immonium ion of lactyllysine reveals widespread lactylation in the human proteome. Nat. Methods 19, 854–864 (2022).
pubmed: 35761067 doi: 10.1038/s41592-022-01523-1
Green, E. M., Mas, G., Young, N. L., Garcia, B. A. & Gozani, O. Methylation of H4 lysines 5, 8 and 12 by yeast Set5 calibrates chromatin stress responses. Nat. Struct. Mol. Biol. 19, 361–363 (2012).
pubmed: 22343720 pmcid: 3334815 doi: 10.1038/nsmb.2252
Mahat, D. B., Salamanca, H. H., Duarte, F. M., Danko, C. G. & Lis, J. T. Mammalian heat shock response and mechanisms underlying its genome-wide transcriptional regulation. Mol. Cell 62, 63–78 (2016).
pubmed: 27052732 pmcid: 4826300 doi: 10.1016/j.molcel.2016.02.025
Schofield, J. A., Duffy, E. E., Kiefer, L., Sullivan, M. C. & Simon, M. D. TimeLapse-seq: adding a temporal dimension to RNA sequencing through nucleoside recoding. Nat. Methods 15, 221–225 (2018).
pubmed: 29355846 pmcid: 5831505 doi: 10.1038/nmeth.4582
Zimmer, J. T., Rosa-Mercado, N. A., Canzio, D., Steitz, J. A. & Simon, M. D. STL-seq reveals pause-release and termination kinetics for promoter-proximal paused RNA polymerase II transcripts. Mol. Cell 81, 4398–4412 (2021).
pubmed: 34520723 pmcid: 9020433 doi: 10.1016/j.molcel.2021.08.019
Lasko, L. M. et al. Discovery of a selective catalytic p300/CBP inhibitor that targets lineage-specific tumours. Nature 550, 128–132 (2017).
pubmed: 28953875 pmcid: 6050590 doi: 10.1038/nature24028
Lu, X. et al. The effect of H3K79 dimethylation and H4K20 trimethylation on nucleosome and chromatin structure. Nat. Struct. Mol. Biol. 15, 1122–1124 (2008).
pubmed: 18794842 pmcid: 2648974 doi: 10.1038/nsmb.1489
Shogren-Knaak, M. et al. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311, 844–847 (2006).
pubmed: 16469925 doi: 10.1126/science.1124000
Beaver, J. E. & Waters, M. L. Molecular recognition of Lys and Arg methylation. ACS Chem. Biol. 11, 643–653 (2016).
pubmed: 26759915 doi: 10.1021/acschembio.5b00996
McCullough, C. E. & Marmorstein, R. Molecular basis for histone acetyltransferase regulation by binding partners, associated domains, and autoacetylation. ACS Chem. Biol. 11, 632–642 (2016).
pubmed: 26555232 doi: 10.1021/acschembio.5b00841
Filippakopoulos, P. & Knapp, S. The bromodomain interaction module. FEBS Lett. 586, 2692–2704 (2012).
pubmed: 22710155 doi: 10.1016/j.febslet.2012.04.045
Zaware, N. & Zhou, M. M. Bromodomain biology and drug discovery. Nat. Struct. Mol. Biol. 26, 870–879 (2019).
pubmed: 31582847 pmcid: 6984398 doi: 10.1038/s41594-019-0309-8
Brand, M. et al. Small molecule inhibitors of bromodomain-acetyl-lysine interactions. ACS Chem. Biol. 10, 22–39 (2015).
pubmed: 25549280 doi: 10.1021/cb500996u
Filippakopoulos, P. et al. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 149, 214–231 (2012).
pubmed: 22464331 pmcid: 3326523 doi: 10.1016/j.cell.2012.02.013
LeRoy, G., Rickards, B. & Flint, S. J. The double bromodomain proteins Brd2 and Brd3 couple histone acetylation to transcription. Mol. Cell 30, 51–60 (2008).
pubmed: 18406326 pmcid: 2387119 doi: 10.1016/j.molcel.2008.01.018
Umehara, T. et al. Structural basis for acetylated histone H4 recognition by the human BRD2 bromodomain. J. Biol. Chem. 285, 7610–7618 (2010).
pubmed: 20048151 pmcid: 2844208 doi: 10.1074/jbc.M109.062422
Umehara, T. et al. Structural implications for K5/K12-di-acetylated histone H4 recognition by the second bromodomain of BRD2. FEBS Lett. 584, 3901–3908 (2010).
pubmed: 20709061 pmcid: 4158924 doi: 10.1016/j.febslet.2010.08.013
Kent, L. N. & Leone, G. The broken cycle: E2F dysfunction in cancer. Nat. Rev. Cancer 19, 326–338 (2019).
pubmed: 31053804 doi: 10.1038/s41568-019-0143-7
Brehm, A. et al. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 391, 597–601 (1998).
pubmed: 9468139 doi: 10.1038/35404
Luo, R. X., Postigo, A. A. & Dean, D. C. Rb interacts with histone deacetylase to repress transcription. Cell 92, 463–473 (1998).
pubmed: 9491888 doi: 10.1016/S0092-8674(00)80940-X
Magnaghi-Jaulin, L. et al. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 391, 601–605 (1998).
pubmed: 9468140 doi: 10.1038/35410
Nicolas, E., Ait-Si-Ali, S. & Trouche, D. The histone deacetylase HDAC3 targets RbAp48 to the retinoblastoma protein. Nucleic Acids Res. 29, 3131–3136 (2001).
pubmed: 11470869 pmcid: 55834 doi: 10.1093/nar/29.15.3131
Coffey, K. et al. Characterisation of a Tip60 specific inhibitor, NU9056, in prostate cancer. PLoS ONE 7, e45539 (2012).
pubmed: 23056207 pmcid: 3466219 doi: 10.1371/journal.pone.0045539
Nguyen, D. P., Garcia Alai, M. M., Kapadnis, P. B., Neumann, H. & Chin, J. W. Genetically encoding N
pubmed: 19772323 doi: 10.1021/ja906603s
Nikolovska-Coleska, Z. et al. Design and characterization of bivalent Smac-based peptides as antagonists of XIAP and development and validation of a fluorescence polarization assay for XIAP containing both BIR2 and BIR3 domains. Anal. Biochem. 374, 87–98 (2008).
pubmed: 18023397 doi: 10.1016/j.ab.2007.10.032
Amblard, M., Fehrentz, J. A., Martinez, J. & Subra, G. Methods and protocols of modern solid phase peptide synthesis. Mol. Biotechnol. 33, 239–254 (2006).
pubmed: 16946453 doi: 10.1385/MB:33:3:239
Pinilla, C., Appel, J. R., Judkowski, V. & Houghten, R. A. Identification of B cell and T cell epitopes using synthetic peptide combinatorial libraries. Curr. Protoc. Immunol. Chapter 9, 9.5.1–9.5.16 (2012).
Peptide Competition Assay (PCA) (Abcam) (accessed March 2019); http://docs.abcam.com/pdf/protocols/peptide_competition_assay_protocol.pdf .
Sidoli, S., Bhanu, N. V., Karch, K. R., Wang, X. & Garcia, B. A. Complete workflow for analysis of histone post-translational modifications using bottom-up mass spectrometry: from histone extraction to data analysis. J. Vis. Exp. 17, 54112 (2016).
Hentges, P., Van Driessche, B., Tafforeau, L., Vandenhaute, J. & Carr, A. M. Three novel antibiotic marker cassettes for gene disruption and marker switching in Schizosaccharomyces pombe. Yeast 22, 1013–1019 (2005).
pubmed: 16200533 doi: 10.1002/yea.1291
Kao, L. R. & Megraw, T. L. RNAi in cultured Drosophila cells. Methods Mol. Biol. 247, 443–457 (2004).
pubmed: 14707365 pmcid: 2493298
Machyna, M., Kiefer, L. & Simon, M. D. Enhanced nucleotide chemistry and toehold nanotechnology reveals lncRNA spreading on chromatin. Nat. Struct. Mol. Biol. 27, 297–304 (2020).
pubmed: 32157249 doi: 10.1038/s41594-020-0390-z
Bowman, S. K. et al. Multiplexed Illumina sequencing libraries from picogram quantities of DNA. BMC Genom. 14, 466 (2013).
doi: 10.1186/1471-2164-14-466
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet 17, 10–12 (2011).
doi: 10.14806/ej.17.1.200
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286 pmcid: 3322381 doi: 10.1038/nmeth.1923
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943 pmcid: 2723002 doi: 10.1093/bioinformatics/btp352
Zhang, Y. et al. Model-based analysis of ChIP-seq (MACS). Genome Biol. 9, R137 (2008).
pubmed: 18798982 pmcid: 2592715 doi: 10.1186/gb-2008-9-9-r137
Ramirez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160–W165 (2016).
pubmed: 27079975 pmcid: 4987876 doi: 10.1093/nar/gkw257
Quinlan, A. R. BEDTools: the Swiss-Army tool for genome feature analysis. Curr. Protoc. Bioinform. 47, 11.12.11–11.12.34 (2014).
doi: 10.1002/0471250953.bi1112s47
Simovski, B. et al. Coloc-stats: a unified web interface to perform colocalization analysis of genomic features. Nucleic Acids Res. 46, W186–W193 (2018).
pubmed: 29873782 pmcid: 6030976 doi: 10.1093/nar/gky474
Welch, R. P. et al. ChIP-Enrich: gene set enrichment testing for ChIP-seq data. Nucleic Acids Res. 42, e105 (2014).
pubmed: 24878920 pmcid: 4117744 doi: 10.1093/nar/gku463
Zou, Z., Ohta, T., Miura, F. & Oki, S. ChIP-Atlas 2021 update: a data-mining suite for exploring epigenomic landscapes by fully integrating ChIP-seq, ATAC-seq and Bisulfite-seq data. Nucleic Acids Res. 50, W175–W182 (2022).
pubmed: 35325188 pmcid: 9252733 doi: 10.1093/nar/gkac199
Stark, R. B. G. DiffBind: differential binding analysis of ChIP-seq peak data (2013); http://bioconductor.org/packages/release/bioc/vignettes/DiffBind/inst/doc/DiffBind.pdf .
Lawrence, M. et al. Software for computing and annotating genomic ranges. PLoS Comput. Biol. 9, e1003118 (2013).
pubmed: 23950696 pmcid: 3738458 doi: 10.1371/journal.pcbi.1003118
Kuleshov, M. V. et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 44, W90–W97 (2016).
pubmed: 27141961 pmcid: 4987924 doi: 10.1093/nar/gkw377
Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).
pubmed: 20513432 pmcid: 2898526 doi: 10.1016/j.molcel.2010.05.004
Vock, I. W. & Simon, M. D. bakR: uncovering differential RNA synthesis and degradation kinetics transcriptome-wide with Bayesian hierarchical modeling. RNA 29, 958–976 (2023).
pubmed: 37028916 pmcid: 10275263 doi: 10.1261/rna.079451.122
Duffy, E. E. et al. Tracking distinct RNA populations using efficient and reversible covalent chemistry. Mol. Cell 59, 858–866 (2015).
pubmed: 26340425 pmcid: 4560836 doi: 10.1016/j.molcel.2015.07.023
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281 pmcid: 4302049 doi: 10.1186/s13059-014-0550-8
Abmayr, S. M., Yao, T., Parmely, T. & Workman, J. L. Preparation of nuclear and cytoplasmic extracts from mammalian cells. Curr. Protoc. Mol. Biol. Chapter 12, 12.1.1–12.1.10 (2006).
Wysocka, J. Identifying novel proteins recognizing histone modifications using peptide pull-down assay. Methods 40, 339–343 (2006).
pubmed: 17101446 pmcid: 4491501 doi: 10.1016/j.ymeth.2006.05.028
Kabsch, W. Xds. Acta Crystallogr. D 66, 125–132 (2010).
pubmed: 20124692 pmcid: 2815665 doi: 10.1107/S0907444909047337
Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235–242 (2011).
pubmed: 21460441 pmcid: 3069738 doi: 10.1107/S0907444910045749
Faivre, E. J. et al. Selective inhibition of the BD2 bromodomain of BET proteins in prostate cancer. Nature 578, 306–310 (2020).
pubmed: 31969702 doi: 10.1038/s41586-020-1930-8
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).
pubmed: 20124702 pmcid: 2815670 doi: 10.1107/S0907444909052925
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010).
pubmed: 20057044 doi: 10.1107/S0907444909042073
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
pubmed: 20383002 pmcid: 2852313 doi: 10.1107/S0907444910007493
Turnbull, W. B. & Daranas, A. H. On the value of c: can low affinity systems be studied by isothermal titration calorimetry? J. Am. Chem. Soc. 125, 14859–14866 (2003).
pubmed: 14640663 doi: 10.1021/ja036166s

Auteurs

William J Lu-Culligan (WJ)

Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT, USA.
Institute of Biomolecular Design & Discovery, Yale University, West Haven, CT, USA.

Leah J Connor (LJ)

Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT, USA.
Institute of Biomolecular Design & Discovery, Yale University, West Haven, CT, USA.

Yixuan Xie (Y)

Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St Louis, MO, USA.

Babatunde E Ekundayo (BE)

Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT, USA.

Brendan T Rose (BT)

Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT, USA.
Institute of Biomolecular Design & Discovery, Yale University, West Haven, CT, USA.

Martin Machyna (M)

Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT, USA.
Institute of Biomolecular Design & Discovery, Yale University, West Haven, CT, USA.

Andreas P Pintado-Urbanc (AP)

Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT, USA.
Institute of Biomolecular Design & Discovery, Yale University, West Haven, CT, USA.

Joshua T Zimmer (JT)

Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT, USA.
Institute of Biomolecular Design & Discovery, Yale University, West Haven, CT, USA.

Isaac W Vock (IW)

Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT, USA.
Institute of Biomolecular Design & Discovery, Yale University, West Haven, CT, USA.

Natarajan V Bhanu (NV)

Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St Louis, MO, USA.

Megan C King (MC)

Department of Cell Biology, Yale School of Medicine, New Haven, CT, USA.

Benjamin A Garcia (BA)

Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St Louis, MO, USA.

Franziska Bleichert (F)

Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT, USA.

Matthew D Simon (MD)

Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT, USA. matthew.simon@yale.edu.
Institute of Biomolecular Design & Discovery, Yale University, West Haven, CT, USA. matthew.simon@yale.edu.

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