Histone post-translational modifications - cause and consequence of genome function.
Journal
Nature reviews. Genetics
ISSN: 1471-0064
Titre abrégé: Nat Rev Genet
Pays: England
ID NLM: 100962779
Informations de publication
Date de publication:
09 2022
09 2022
Historique:
accepted:
28
02
2022
pubmed:
27
3
2022
medline:
20
8
2022
entrez:
26
3
2022
Statut:
ppublish
Résumé
Much has been learned since the early 1960s about histone post-translational modifications (PTMs) and how they affect DNA-templated processes at the molecular level. This understanding has been bolstered in the past decade by the identification of new types of histone PTM, the advent of new genome-wide mapping approaches and methods to deposit or remove PTMs in a locally and temporally controlled manner. Now, with the availability of vast amounts of data across various biological systems, the functional role of PTMs in important processes (such as transcription, recombination, replication, DNA repair and the modulation of genomic architecture) is slowly emerging. This Review explores the contribution of histone PTMs to the regulation of genome function by discussing when these modifications play a causative (or instructive) role in DNA-templated processes and when they are deposited as a consequence of such processes, to reinforce and record the event. Important advances in the field showing that histone PTMs can exert both direct and indirect effects on genome function are also presented.
Identifiants
pubmed: 35338361
doi: 10.1038/s41576-022-00468-7
pii: 10.1038/s41576-022-00468-7
doi:
Substances chimiques
Histones
0
DNA
9007-49-2
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
563-580Subventions
Organisme : Cancer Research UK
ID : RG96894
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C6946/A24843
Pays : United Kingdom
Organisme : Wellcome Trust
ID : WT203144
Pays : United Kingdom
Informations de copyright
© 2022. Springer Nature Limited.
Références
Luger, K., Dechassa, M. L. & Tremethick, D. J. New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Nat. Rev. Mol. Cell Biol. 13, 436–447 (2012).
pubmed: 22722606
pmcid: 3408961
doi: 10.1038/nrm3382
Lai, W. K. M. & Pugh, B. F. Understanding nucleosome dynamics and their links to gene expression and DNA replication. Nat. Rev. Mol. Cell Biol. 18, 548–562 (2017).
pubmed: 28537572
pmcid: 5831138
doi: 10.1038/nrm.2017.47
Turner, B. M. Decoding the nucleosome. Cell 75, 5–8 (1993). This review article introduces the concept of epigenetic code via histone PTMs.
pubmed: 8402900
doi: 10.1016/S0092-8674(05)80078-9
Dai, Z., Ramesh, V. & Locasale, J. W. The evolving metabolic landscape of chromatin biology and epigenetics. Nat. Rev. Genet. 21, 737–753 (2020).
pubmed: 32908249
pmcid: 8059378
doi: 10.1038/s41576-020-0270-8
Wiese, M. & Bannister, A. J. Two genomes, one cell: mitochondrial–nuclear coordination via epigenetic pathways. Mol. Metab. 38, 100942 (2020).
pubmed: 32217072
pmcid: 7300384
doi: 10.1016/j.molmet.2020.01.006
Martire, S. & Banaszynski, L. A. The roles of histone variants in fine-tuning chromatin organization and function. Nat. Rev. Mol. Cell Biol. 21, 522–541 (2020).
pubmed: 32665685
pmcid: 8245300
doi: 10.1038/s41580-020-0262-8
Nacev, B. A. et al. The expanding landscape of ‘oncohistone’ mutations in human cancers. Nature 567, 473–478 (2019). This article highlights the prevalence of mutations in histone modification sites in cancer.
pubmed: 30894748
pmcid: 6512987
doi: 10.1038/s41586-019-1038-1
Byvoet, P., Shepherd, G. R., Hardin, J. M. & Noland, B. J. The distribution and turnover of labeled methyl groups in histone fractions of cultured mammalian cells. Arch. Biochem. Biophys. 148, 558–567 (1972).
pubmed: 5063076
doi: 10.1016/0003-9861(72)90174-9
Xhemalce B., Dawson M. A. & Bannister A. J. In Epigenetic Regulation and Epigenomics (ed. Meyers, R. A.) 657–703 (Wiley–Blackwell, 2012).
Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289–293 (2009).
pubmed: 19815776
pmcid: 2858594
doi: 10.1126/science.1181369
Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376–380 (2012).
pubmed: 22495300
pmcid: 3356448
doi: 10.1038/nature11082
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
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
Cosgrove, M. S., Boeke, J. D. & Wolberger, C. Regulated nucleosome mobility and the histone code. Nat. Struct. Mol. Biol. 11, 1037–1043 (2004).
pubmed: 15523479
doi: 10.1038/nsmb851
Neumann, H. et al. A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol. Cell 36, 153–163 (2009). Describes an elegant method for the production of recombinant histones with site-specific acetylations and reveals effects of H3K56ac on DNA breathing.
pubmed: 19818718
pmcid: 2856916
doi: 10.1016/j.molcel.2009.07.027
Verdin, E. & Ott, M. 50 years of protein acetylation: from gene regulation to epigenetics, metabolism and beyond. Nat. Rev. Mol. Cell Biol. 16, 258–264 (2015).
pubmed: 25549891
doi: 10.1038/nrm3931
Durrin, L. K., Mann, R. K., Kayne, P. S. & Grunstein, M. Yeast histone H4 N-terminal sequence is required for promoter activation in vivo. Cell 65, 1023–1031 (1991).
pubmed: 2044150
doi: 10.1016/0092-8674(91)90554-C
Protacio, R. U., Li, G., Lowary, P. T. & Widom, J. Effects of histone tail domains on the rate of transcriptional elongation through a nucleosome. Mol. Cell Biol. 20, 8866–8878 (2000).
pubmed: 11073987
pmcid: 86542
doi: 10.1128/MCB.20.23.8866-8878.2000
Zhang, W., Bone, J. R., Edmondson, D. G., Turner, B. M. & Roth, S. Y. Essential and redundant functions of histone acetylation revealed by mutation of target lysines and loss of the Gcn5p acetyltransferase. EMBO J. 17, 3155–3167 (1998).
pubmed: 9606197
pmcid: 1170654
doi: 10.1093/emboj/17.11.3155
Nitsch, S., Zorro Shahidian, L. & Schneider, R. Histone acylations and chromatin dynamics: concepts, challenges, and links to metabolism. EMBO Rep. 22, e52774 (2021).
pubmed: 34159701
pmcid: 8406397
doi: 10.15252/embr.202152774
Tan, M. et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146, 1016–1028 (2011).
pubmed: 21925322
pmcid: 3176443
doi: 10.1016/j.cell.2011.08.008
Sabari, B. R. et al. Intracellular crotonyl-CoA stimulates transcription through p300-catalyzed histone crotonylation. Mol. Cell 58, 203–215 (2015).
pubmed: 25818647
pmcid: 4501262
doi: 10.1016/j.molcel.2015.02.029
Gowans, G. J. et al. Recognition of histone crotonylation by TAF14 links metabolic state to gene expression. Mol. Cell 76, 909–921.e903 (2019).
pubmed: 31676231
pmcid: 6931132
doi: 10.1016/j.molcel.2019.09.029
Tidwell, T., Allfrey, V. G. & Mirsky, A. E. The methylation of histones during regeneration of the liver. J. Biol. Chem. 243, 707–715 (1968).
pubmed: 5638586
doi: 10.1016/S0021-9258(19)81723-4
Bannister, A. J., Schneider, R. & Kouzarides, T. Histone methylation: dynamic or static? Cell 109, 801–806 (2002).
pubmed: 12110177
doi: 10.1016/S0092-8674(02)00798-5
Henikoff, S. & Shilatifard, A. Histone modification: cause or cog? Trends Genet. 27, 389–396 (2011).
pubmed: 21764166
doi: 10.1016/j.tig.2011.06.006
Talbert, P. B., Meers, M. P. & Henikoff, S. Old cogs, new tricks: the evolution of gene expression in a chromatin context. Nat. Rev. Genet. 20, 283–297 (2019).
pubmed: 30886348
doi: 10.1038/s41576-019-0105-7
Chen, K. et al. Broad H3K4me3 is associated with increased transcription elongation and enhancer activity at tumor-suppressor genes. Nat. Genet. 47, 1149–1157 (2015).
pubmed: 26301496
pmcid: 4780747
doi: 10.1038/ng.3385
Benayoun, B. A. et al. H3K4me3 breadth is linked to cell identity and transcriptional consistency. Cell 158, 673–688 (2014).
pubmed: 25083876
pmcid: 4137894
doi: 10.1016/j.cell.2014.06.027
Vermeulen, M. et al. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131, 58–69 (2007).
pubmed: 17884155
doi: 10.1016/j.cell.2007.08.016
Lauberth, S. M. et al. H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 152, 1021–1036 (2013).
pubmed: 23452851
pmcid: 3588593
doi: 10.1016/j.cell.2013.01.052
Cano-Rodriguez, D. et al. Writing of H3K4Me3 overcomes epigenetic silencing in a sustained but context-dependent manner. Nat. Commun. 7, 12284 (2016).
pubmed: 27506838
pmcid: 4987519
doi: 10.1038/ncomms12284
Newman, J. R. et al. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441, 840–846 (2006).
pubmed: 16699522
doi: 10.1038/nature04785
Dahl, J. A. et al. Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nature 537, 548–552 (2016).
pubmed: 27626377
pmcid: 6283663
doi: 10.1038/nature19360
Zhang, B. et al. Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature 537, 553–557 (2016). The preceding two studies reveal the atypical distribution of H3K4me3 during early mammalian development.
pubmed: 27626382
doi: 10.1038/nature19361
Erkek, S. et al. Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa. Nat. Struct. Mol. Biol. 20, 868–875 (2013).
pubmed: 23770822
doi: 10.1038/nsmb.2599
Ng, H. H., Robert, F., Young, R. A. & Struhl, K. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 11, 709–719 (2003).
pubmed: 12667453
doi: 10.1016/S1097-2765(03)00092-3
Petruk, S. et al. Trithorax and dCBP acting in a complex to maintain expression of a homeotic gene. Science 294, 1331–1334 (2001).
pubmed: 11701926
doi: 10.1126/science.1065683
Hormanseder, E. et al. H3K4 methylation-dependent memory of somatic cell identity inhibits reprogramming and development of nuclear transfer embryos. Cell Stem Cell 21, 135–143.e136 (2017).
pubmed: 28366589
pmcid: 5505866
doi: 10.1016/j.stem.2017.03.003
Siklenka, K. et al. Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science 350, aab2006 (2015).
pubmed: 26449473
doi: 10.1126/science.aab2006
Lismer, A. et al. Histone H3 lysine 4 trimethylation in sperm is transmitted to the embryo and associated with diet-induced phenotypes in the offspring. Dev. Cell 56, 671–686.e6 (2021).
pubmed: 33596408
doi: 10.1016/j.devcel.2021.01.014
Heintzman, N. D. et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459, 108–112 (2009).
pubmed: 19295514
pmcid: 2910248
doi: 10.1038/nature07829
Creyghton, M. P. et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl Acad. Sci. USA 107, 21931–21936 (2010).
pubmed: 21106759
pmcid: 3003124
doi: 10.1073/pnas.1016071107
Dorighi, K. M. et al. Mll3 and Mll4 facilitate enhancer RNA synthesis and transcription from promoters independently of H3K4 monomethylation. Mol. Cell 66, 568–576.e4 (2017).
pubmed: 28483418
pmcid: 5662137
doi: 10.1016/j.molcel.2017.04.018
Rickels, R. et al. Histone H3K4 monomethylation catalyzed by TRR and mammalian COMPASS-like proteins at enhancers is dispensable for development and viability. Nat. Genet. 49, 1647–1653 (2017).
pubmed: 28967912
pmcid: 5663216
doi: 10.1038/ng.3965
Zhang, T., Zhang, Z., Dong, Q., Xiong, J. & Zhu, B. Histone H3K27 acetylation is dispensable for enhancer activity in mouse embryonic stem cells. Genome Biol. 21, 45 (2020).
pubmed: 32085783
pmcid: 7035716
doi: 10.1186/s13059-020-01957-w
Bleckwehl, T. et al. Enhancer-associated H3K4 methylation safeguards in vitro germline competence. Nat. Commun. 12, 5771 (2021).
pubmed: 34599190
pmcid: 8486853
doi: 10.1038/s41467-021-26065-6
Hughes, A. L., Kelley, J. R. & Klose, R. J. Understanding the interplay between CpG island-associated gene promoters and H3K4 methylation. Biochim. Biophys. Acta Gene Regul. Mech. 1863, 194567 (2020).
pubmed: 32360393
pmcid: 7294231
doi: 10.1016/j.bbagrm.2020.194567
Hontelez, S. et al. Embryonic transcription is controlled by maternally defined chromatin state. Nat. Commun. 6, 10148 (2015).
pubmed: 26679111
doi: 10.1038/ncomms10148
Murphy, P. J., Wu, S. F., James, C. R., Wike, C. L. & Cairns, B. R. Placeholder nucleosomes underlie germline-to-embryo DNA methylation reprogramming. Cell 172, 993–1006.e13 (2018).
pubmed: 29456083
doi: 10.1016/j.cell.2018.01.022
Liu, X. et al. Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537, 558–562 (2016).
pubmed: 27626379
doi: 10.1038/nature19362
Hanna, C. W. et al. MLL2 conveys transcription-independent H3K4 trimethylation in oocytes. Nat. Struct. Mol. Biol. 25, 73–82 (2018).
pubmed: 29323282
doi: 10.1038/s41594-017-0013-5
Ooi, S. K. T. et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714–717 (2007).
pubmed: 17687327
pmcid: 2650820
doi: 10.1038/nature05987
Bannister, A. J. et al. Spatial distribution of di- and tri-methyl lysine 36 of histone H3 at active genes. J. Biol. Chem. 280, 17732–17736 (2005).
pubmed: 15760899
doi: 10.1074/jbc.M500796200
Vakoc, C. R., Sachdeva, M. M., Wang, H. X. & Blobel, G. A. Profile of histone lysine methylation across transcribed mammalian chromatin. Mol. Cell Biol. 26, 9185–9195 (2006).
pubmed: 17030614
pmcid: 1698537
doi: 10.1128/MCB.01529-06
Kizer, K. O. et al. A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3K36 methylation with transcript elongation. Mol. Cell Biol. 25, 3305–3316 (2005).
pubmed: 15798214
pmcid: 1069628
doi: 10.1128/MCB.25.8.3305-3316.2005
Carrozza, M. J. et al. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123, 581–592 (2005).
pubmed: 16286007
doi: 10.1016/j.cell.2005.10.023
Luco, R. F. et al. Regulation of alternative splicing by histone modifications. Science 327, 996–1000 (2010).
pubmed: 20133523
pmcid: 2913848
doi: 10.1126/science.1184208
Huang, H. L. et al. Histone H3 trimethylation at lysine 36 guides m
pubmed: 30867593
pmcid: 6438714
doi: 10.1038/s41586-019-1016-7
Meers, M. P. et al. Histone gene replacement reveals a post-transcriptional role for H3K36 in maintaining metazoan transcriptome fidelity. eLife 6, e23249 (2017).
pubmed: 28346137
pmcid: 5404926
doi: 10.7554/eLife.23249
Van Rechem, C. et al. Collective regulation of chromatin modifications predicts replication timing during cell cycle. Cell Rep. 37, 109799 (2021).
pubmed: 34610305
pmcid: 8530517
doi: 10.1016/j.celrep.2021.109799
Weinberg, D. N. et al. The histone mark H3K36me2 recruits DNMT3A and shapes the intergenic DNA methylation landscape. Nature 573, 281–286 (2019).
pubmed: 31485078
pmcid: 6742567
doi: 10.1038/s41586-019-1534-3
Dawson, M. A. et al. Three distinct patterns of histone H3Y41 phosphorylation mark active genes. Cell Rep. 2, 470–477 (2012).
pubmed: 22999934
pmcid: 3607218
doi: 10.1016/j.celrep.2012.08.016
Brehove, M. et al. Histone core phosphorylation regulates DNA accessibility. J. Biol. Chem. 290, 22612–22621 (2015).
pubmed: 26175159
pmcid: 4566235
doi: 10.1074/jbc.M115.661363
Lo, W. S. et al. Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol. Cell 5, 917–926 (2000).
pubmed: 10911986
doi: 10.1016/S1097-2765(00)80257-9
Zippo, A. et al. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138, 1122–1136 (2009).
pubmed: 19766566
doi: 10.1016/j.cell.2009.07.031
Hake, S. B. et al. Serine 31 phosphorylation of histone variant H3.3 is specific to regions bordering centromeres in metaphase chromosomes. Proc. Natl Acad. Sci. USA 102, 6344–6349 (2005).
pubmed: 15851689
pmcid: 1088391
doi: 10.1073/pnas.0502413102
Martire, S. et al. Phosphorylation of histone H3.3 at serine 31 promotes p300 activity and enhancer acetylation. Nat. Genet. 51, 941–946 (2019).
pubmed: 31152160
pmcid: 6598431
doi: 10.1038/s41588-019-0428-5
Armache, A. et al. Histone H3.3 phosphorylation amplifies stimulation-induced transcription. Nature 583, 852–857 (2020).
pubmed: 32699416
pmcid: 7517595
doi: 10.1038/s41586-020-2533-0
Sitbon, D., Boyarchuk, E., Dingli, F., Loew, D. & Almouzni, G. Histone variant H3.3 residue S31 is essential for Xenopus gastrulation regardless of the deposition pathway. Nat. Commun. 11, 1256 (2020). The above three articles identify and demonstrate a functional role for modification of a histone variant-specific residue.
pubmed: 32152320
pmcid: 7062693
doi: 10.1038/s41467-020-15084-4
Macdonald, N. et al. Molecular basis for the recognition of phosphorylated and phosphoacetylated histone H3 by 14-3-3. Mol. Cell 20, 199–211 (2005).
pubmed: 16246723
doi: 10.1016/j.molcel.2005.08.032
Schneider, R., Bannister, A. J., Weise, C. & Kouzarides, T. Direct binding of INHAT to H3 tails disrupted by modifications. J. Biol. Chem. 279, 23859–23862 (2004).
pubmed: 15100215
doi: 10.1074/jbc.C400151200
Gehani, S. S. et al. Polycomb group protein displacement and gene activation through MSK-dependent H3K27me3S28 phosphorylation. Mol. Cell 39, 886–900 (2010).
pubmed: 20864036
doi: 10.1016/j.molcel.2010.08.020
Fischle, W. et al. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438, 1116–1122 (2005).
pubmed: 16222246
doi: 10.1038/nature04219
Schuettengruber, B. & Cavalli, G. Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 136, 3531–3542 (2009).
pubmed: 19820181
doi: 10.1242/dev.033902
Simon, J. A. & Kingston, R. E. Mechanisms of polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 10, 697–708 (2009).
pubmed: 19738629
doi: 10.1038/nrm2763
Aranda, S., Mas, G. & Di Croce, L. Regulation of gene transcription by Polycomb proteins. Sci. Adv. 1, e1500737 (2015).
pubmed: 26665172
pmcid: 4672759
doi: 10.1126/sciadv.1500737
Pengelly, A. R., Copur, O., Jackle, H., Herzig, A. & Muller, J. A histone mutant reproduces the phenotype caused by loss of histone-modifying factor Polycomb. Science 339, 698–699 (2013).
pubmed: 23393264
doi: 10.1126/science.1231382
Pengelly, A. R., Kalb, R., Finkl, K. & Muller, J. Transcriptional repression by PRC1 in the absence of H2A monoubiquitylation. Genes Dev. 29, 1487–1492 (2015).
pubmed: 26178786
pmcid: 4526733
doi: 10.1101/gad.265439.115
Blackledge, N. P. et al. PRC1 catalytic activity is central to Polycomb system function. Mol. Cell 77, 857–874.e9 (2020).
pubmed: 31883950
pmcid: 7033600
doi: 10.1016/j.molcel.2019.12.001
Tamburri, S. et al. Histone H2AK119 mono-ubiquitination is essential for Polycomb-mediated transcriptional repression. Mol. Cell 77, 840–856.e845 (2020).
pubmed: 31883952
pmcid: 7033561
doi: 10.1016/j.molcel.2019.11.021
Francis, N. J., Kingston, R. E. & Woodcock, C. L. Chromatin compaction by a Polycomb group protein complex. Science 306, 1574–1577 (2004).
pubmed: 15567868
doi: 10.1126/science.1100576
Eskeland, R. et al. Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination. Mol. Cell 38, 452–464 (2010).
pubmed: 20471950
pmcid: 3132514
doi: 10.1016/j.molcel.2010.02.032
Plys, A. J. et al. Phase separation of Polycomb-repressive complex 1 is governed by a charged disordered region of CBX2. Genes Dev. 33, 799–813 (2019).
pubmed: 31171700
pmcid: 6601514
doi: 10.1101/gad.326488.119
Tatavosian, R. et al. Nuclear condensates of the Polycomb protein chromobox 2 (CBX2) assemble through phase separation. J. Biol. Chem. 294, 1451–1463 (2019).
pubmed: 30514760
doi: 10.1074/jbc.RA118.006620
Mei, H. et al. H2AK119ub1 guides maternal inheritance and zygotic deposition of H3K27me3 in mouse embryos. Nat. Genet. 53, 539–550 (2021).
pubmed: 33821003
doi: 10.1038/s41588-021-00820-3
Chen, Z., Djekidel, M. N. & Zhang, Y. Distinct dynamics and functions of H2AK119ub1 and H3K27me3 in mouse preimplantation embryos. Nat. Genet. 53, 551–563 (2021).
pubmed: 33821005
pmcid: 8092361
doi: 10.1038/s41588-021-00821-2
Inoue, A., Jiang, L., Lu, F., Suzuki, T. & Zhang, Y. Maternal H3K27me3 controls DNA methylation-independent imprinting. Nature 547, 419–424 (2017). This article demonstrates a role for H3K27me3 in non-canonical imprinting.
pubmed: 28723896
doi: 10.1038/nature23262
Zenk, F. et al. Germ line-inherited H3K27me3 restricts enhancer function during maternal-to-zygotic transition. Science 357, 212–216 (2017).
pubmed: 28706074
doi: 10.1126/science.aam5339
Coleman, R. T. & Struhl, G. Causal role for inheritance of H3K27me3 in maintaining the OFF state of a Drosophila HOX gene. Science 356, eaai8236 (2017).
pubmed: 28302795
pmcid: 5595140
doi: 10.1126/science.aai8236
Escobar, T. M. et al. Active and repressed chromatin domains exhibit distinct nucleosome segregation during DNA replication. Cell 179, 953–963.e11 (2019).
pubmed: 31675501
pmcid: 6917041
doi: 10.1016/j.cell.2019.10.009
Riising, E. M. et al. Gene silencing triggers polycomb repressive complex 2 recruitment to CpG islands genome wide. Mol. Cell 55, 347–360 (2014).
pubmed: 24999238
doi: 10.1016/j.molcel.2014.06.005
Allshire, R. C. & Madhani, H. D. Ten principles of heterochromatin formation and function. Nat. Rev. Mol. Cell Biol. 19, 229–244 (2018).
pubmed: 29235574
doi: 10.1038/nrm.2017.119
Nicetto, D. & Zaret, K. S. Role of H3K9me3 heterochromatin in cell identity establishment and maintenance. Curr. Opin. Genet. Dev. 55, 1–10 (2019).
pubmed: 31103921
pmcid: 6759373
doi: 10.1016/j.gde.2019.04.013
Bannister, A. J. et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120–124 (2001).
pubmed: 11242054
doi: 10.1038/35065138
Lachner, M., O’Carroll, D., Rea, S., Mechtler, K. & Jenuwein, T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116–120 (2001).
pubmed: 11242053
doi: 10.1038/35065132
Canzio, D. et al. Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly. Mol. Cell 41, 67–81 (2011).
pubmed: 21211724
pmcid: 3752404
doi: 10.1016/j.molcel.2010.12.016
Jack, A. P. et al. H3K56me3 is a novel, conserved heterochromatic mark that largely but not completely overlaps with H3K9me3 in both regulation and localization. PLoS One 8, e51765 (2013).
pubmed: 23451023
pmcid: 3579866
doi: 10.1371/journal.pone.0051765
Schotta, G. et al. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18, 1251–1262 (2004).
pubmed: 15145825
pmcid: 420351
doi: 10.1101/gad.300704
Daujat, S. et al. H3K64 trimethylation marks heterochromatin and is dynamically remodeled during developmental reprogramming. Nat. Struct. Mol. Biol. 16, 777–781 (2009).
pubmed: 19561610
doi: 10.1038/nsmb.1629
Soufi, A., Donahue, G. & Zaret, K. S. Facilitators and impediments of the pluripotency reprogramming factors’ initial engagement with the genome. Cell 151, 994–1004 (2012).
pubmed: 23159369
pmcid: 3508134
doi: 10.1016/j.cell.2012.09.045
Ninova, M., Fejes Toth, K. & Aravin, A. A. The control of gene expression and cell identity by H3K9 trimethylation. Development 146, dev181180 (2019).
pubmed: 31540910
pmcid: 6803365
doi: 10.1242/dev.181180
Nicetto, D. et al. H3K9me3-heterochromatin loss at protein-coding genes enables developmental lineage specification. Science 363, 294–297 (2019). This article demonstrates a function for H3K9me3 in regulating tissue-specific gene expression in vivo.
pubmed: 30606806
pmcid: 6664818
doi: 10.1126/science.aau0583
McCarthy, R. L. et al. Diverse heterochromatin-associated proteins repress distinct classes of genes and repetitive elements. Nat. Cell Biol. 23, 905–914 (2021).
pubmed: 34354237
pmcid: 9248069
doi: 10.1038/s41556-021-00725-7
Burton, A. et al. Heterochromatin establishment during early mammalian development is regulated by pericentromeric RNA and characterized by non-repressive H3K9me3. Nat. Cell Biol. 22, 767–778 (2020).
pubmed: 32601371
pmcid: 7610380
doi: 10.1038/s41556-020-0536-6
Zhang, D. et al. Metabolic regulation of gene expression by histone lactylation. Nature 574, 575–580 (2019). This article reveals the widespread occurrence of a new histone PTM.
pubmed: 31645732
pmcid: 6818755
doi: 10.1038/s41586-019-1678-1
Farrelly, L. A. et al. Histone serotonylation is a permissive modification that enhances TFIID binding to H3K4me3. Nature 567, 535–539 (2019). This study uncovers monoaminylation as a new class of histone PTM.
pubmed: 30867594
pmcid: 6557285
doi: 10.1038/s41586-019-1024-7
Lepack, A. E. et al. Dopaminylation of histone H3 in ventral tegmental area regulates cocaine seeking. Science 368, 197–201 (2020). This work demonstrates a physiological role for a new type of histone monoaminylation.
pubmed: 32273471
pmcid: 7228137
doi: 10.1126/science.aaw8806
Gehre, M. et al. Lysine 4 of histone H3.3 is required for embryonic stem cell differentiation, histone enrichment at regulatory regions and transcription accuracy. Nat. Genet. 52, 273–282 (2020).
pubmed: 32139906
doi: 10.1038/s41588-020-0586-5
Li, G., Levitus, M., Bustamante, C. & Widom, J. Rapid spontaneous accessibility of nucleosomal DNA. Nat. Struct. Mol. Biol. 12, 46–53 (2005).
pubmed: 15580276
doi: 10.1038/nsmb869
Shimko, J. C., North, J. A., Bruns, A. N., Poirier, M. G. & Ottesen, J. J. Preparation of fully synthetic histone H3 reveals that acetyl-lysine 56 facilitates protein binding within nucleosomes. J. Mol. Biol. 408, 187–204 (2011).
pubmed: 21310161
doi: 10.1016/j.jmb.2011.01.003
North, J. A. et al. Regulation of the nucleosome unwrapping rate controls DNA accessibility. Nucleic Acids Res. 40, 10215–10227 (2012).
pubmed: 22965129
pmcid: 3488218
doi: 10.1093/nar/gks747
Di Cerbo, V. et al. Acetylation of histone H3 at lysine 64 regulates nucleosome dynamics and facilitates transcription. eLife 3, e01632 (2014).
pubmed: 24668167
pmcid: 3965291
doi: 10.7554/eLife.01632
Lange, U. C. et al. Dissecting the role of H3K64me3 in mouse pericentromeric heterochromatin. Nat. Commun. 4, 2233 (2013).
pubmed: 23903902
doi: 10.1038/ncomms3233
North, J. A. et al. Phosphorylation of histone H3(T118) alters nucleosome dynamics and remodeling. Nucleic Acids Res. 39, 6465–6474 (2011).
pubmed: 21576235
pmcid: 3159469
doi: 10.1093/nar/gkr304
Tropberger, P. et al. Regulation of transcription through acetylation of H3K122 on the lateral surface of the histone octamer. Cell 152, 859–872 (2013).
pubmed: 23415232
doi: 10.1016/j.cell.2013.01.032
Zorro Shahidian, L. et al. Succinylation of H3K122 destabilizes nucleosomes and enhances transcription. EMBO Rep. 22, e51009 (2021).
pubmed: 33512761
pmcid: 7926236
doi: 10.15252/embr.202051009
Bao, X. et al. Glutarylation of histone H4 lysine 91 regulates chromatin dynamics. Mol. Cell 76, 660–675.e9 (2019).
pubmed: 31542297
doi: 10.1016/j.molcel.2019.08.018
Tessarz, P. et al. Glutamine methylation in histone H2A is an RNA-polymerase-I-dedicated modification. Nature 505, 564–568 (2014).
pubmed: 24352239
doi: 10.1038/nature12819
Mawer, J. S. P. et al. Nhp2 is a reader of H2AQ105me and part of a network integrating metabolism with rRNA synthesis. EMBO Rep. 22, e52435 (2021).
pubmed: 34409714
pmcid: 8490984
doi: 10.15252/embr.202152435
van Leeuwen, F., Gafken, P. R. & Gottschling, D. E. Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 109, 745–756 (2002).
pubmed: 12086673
doi: 10.1016/S0092-8674(02)00759-6
Lawrence, M., Daujat, S. & Schneider, R. Lateral thinking: how histone modifications regulate gene expression. Trends Genet. 32, 42–56 (2016).
pubmed: 26704082
doi: 10.1016/j.tig.2015.10.007
Schubeler, D. et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18, 1263–1271 (2004).
pubmed: 15175259
pmcid: 420352
doi: 10.1101/gad.1198204
Godfrey, L. et al. DOT1L inhibition reveals a distinct subset of enhancers dependent on H3K79 methylation. Nat. Commun. 10, 2803 (2019).
pubmed: 31243293
pmcid: 6594956
doi: 10.1038/s41467-019-10844-3
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
Spruce, C. et al. HELLS and PRDM9 form a pioneer complex to open chromatin at meiotic recombination hot spots. Genes Dev. 34, 398–412 (2020).
pubmed: 32001511
pmcid: 7050486
doi: 10.1101/gad.333542.119
Mihola, O. et al. Rat PRDM9 shapes recombination landscapes, duration of meiosis, gametogenesis, and age of fertility. BMC Biol. 19, 86 (2021).
pubmed: 33910563
pmcid: 8082845
doi: 10.1186/s12915-021-01017-0
Kaiser, V. B. & Semple, C. A. Chromatin loop anchors are associated with genome instability in cancer and recombination hotspots in the germline. Genome Biol. 19, 101 (2018).
pubmed: 30060743
pmcid: 6066925
doi: 10.1186/s13059-018-1483-4
Grey, C. et al. In vivo binding of PRDM9 reveals interactions with noncanonical genomic sites. Genome Res. 27, 580–590 (2017).
pubmed: 28336543
pmcid: 5378176
doi: 10.1101/gr.217240.116
Liu, C., Zhang, Y., Liu, C. C. & Schatz, D. G. Structural insights into the evolution of the RAG recombinase. Nat. Rev. Immunol. https://doi.org/10.1038/s41577-021-00628-6 (2021).
doi: 10.1038/s41577-021-00628-6
pubmed: 34675378
pmcid: 8283745
Hanahan, D. & Weinberg, R. A. The hallmarks of cancer. Cell 100, 57–70 (2000).
pubmed: 10647931
doi: 10.1016/S0092-8674(00)81683-9
Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S. & Bonner, W. M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858–5868 (1998).
pubmed: 9488723
doi: 10.1074/jbc.273.10.5858
Clouaire, T. & Legube, G. A snapshot on the cis chromatin response to DNA double-strand breaks. Trends Genet. 35, 330–345 (2019).
pubmed: 30898334
doi: 10.1016/j.tig.2019.02.003
Arnould, C. et al. Loop extrusion as a mechanism for formation of DNA damage repair foci. Nature 590, 660–665 (2021). This study demonstrates a dependence of γH2A.X-containing repair foci on loop extrusion and genome topology.
pubmed: 33597753
pmcid: 7116834
doi: 10.1038/s41586-021-03193-z
Thorslund, T. et al. Histone H1 couples initiation and amplification of ubiquitin signalling after DNA damage. Nature 527, 389–393 (2015).
pubmed: 26503038
doi: 10.1038/nature15401
Mattiroli, F. et al. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150, 1182–1195 (2012).
pubmed: 22980979
doi: 10.1016/j.cell.2012.08.005
Pesavento, J. J., Yang, H., Kelleher, N. L. & Mizzen, C. A. Certain and progressive methylation of histone H4 at lysine 20 during the cell cycle. Mol. Cell Biol. 28, 468–486 (2008).
pubmed: 17967882
doi: 10.1128/MCB.01517-07
Botuyan, M. V. et al. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127, 1361–1373 (2006).
pubmed: 17190600
pmcid: 1804291
doi: 10.1016/j.cell.2006.10.043
Fradet-Turcotte, A. et al. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 499, 50–54 (2013).
pubmed: 23760478
pmcid: 3955401
doi: 10.1038/nature12318
Nakamura, K. et al. H4K20me0 recognition by BRCA1–BARD1 directs homologous recombination to sister chromatids. Nat. Cell Biol. 21, 311–318 (2019).
pubmed: 30804502
pmcid: 6420097
doi: 10.1038/s41556-019-0282-9
Becker, J. R. et al. BARD1 reads H2A lysine 15 ubiquitination to direct homologous recombination. Nature 596, 433–437 (2021).
pubmed: 34321663
doi: 10.1038/s41586-021-03776-w
Pfister, S. X. et al. SETD2-dependent histone H3K36 trimethylation is required for homologous recombination repair and genome stability. Cell Rep. 7, 2006–2018 (2014).
pubmed: 24931610
pmcid: 4074340
doi: 10.1016/j.celrep.2014.05.026
Gong, F., Clouaire, T., Aguirrebengoa, M., Legube, G. & Miller, K. M. Histone demethylase KDM5A regulates the ZMYND8-NuRD chromatin remodeler to promote DNA repair. J. Cell Biol. 216, 1959–1974 (2017).
pubmed: 28572115
pmcid: 5496618
doi: 10.1083/jcb.201611135
Li, X. et al. Histone demethylase KDM5B is a key regulator of genome stability. Proc. Natl Acad. Sci. USA 111, 7096–7101 (2014).
pubmed: 24778210
pmcid: 4024858
doi: 10.1073/pnas.1324036111
Ayrapetov, M. K., Gursoy-Yuzugullu, O., Xu, C., Xu, Y. & Price, B. D. DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin. Proc. Natl Acad. Sci. USA 111, 9169–9174 (2014).
pubmed: 24927542
pmcid: 4078803
doi: 10.1073/pnas.1403565111
Alagoz, M. et al. SETDB1, HP1 and SUV39 promote repositioning of 53BP1 to extend resection during homologous recombination in G2 cells. Nucleic Acids Res. 43, 7931–7944 (2015).
pubmed: 26206670
pmcid: 4652757
doi: 10.1093/nar/gkv722
Qin, B. et al. UFL1 promotes histone H4 ufmylation and ATM activation. Nat. Commun. 10, 1242 (2019). This study demonstrates a role for a new histone PTM in DNA repair.
pubmed: 30886146
pmcid: 6423285
doi: 10.1038/s41467-019-09175-0
Miotto, B. & Struhl, K. HBO1 histone acetylase activity is essential for DNA replication licensing and inhibited by Geminin. Mol. Cell 37, 57–66 (2010).
pubmed: 20129055
pmcid: 2818871
doi: 10.1016/j.molcel.2009.12.012
Sansam, C. G. et al. A mechanism for epigenetic control of DNA replication. Genes Dev. 32, 224–229 (2018).
pubmed: 29483155
pmcid: 5859964
doi: 10.1101/gad.306464.117
Kuo, A. J. et al. The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier–Gorlin syndrome. Nature 484, 115–119 (2012).
pubmed: 22398447
pmcid: 3321094
doi: 10.1038/nature10956
Beck, D. B. et al. The role of PR-Set7 in replication licensing depends on Suv4-20h. Genes Dev. 26, 2580–2589 (2012).
pubmed: 23152447
pmcid: 3521623
doi: 10.1101/gad.195636.112
Tardat, M. et al. The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat. Cell Biol. 12, 1086–1093 (2010).
pubmed: 20953199
doi: 10.1038/ncb2113
Lim, H. J. et al. The G2/M regulator histone demethylase PHF8 is targeted for degradation by the anaphase-promoting complex containing CDC20. Mol. Cell Biol. 33, 4166–4180 (2013).
pubmed: 23979597
pmcid: 3811896
doi: 10.1128/MCB.00689-13
Long, H. et al. H2A.Z facilitates licensing and activation of early replication origins. Nature 577, 576–581 (2020).
pubmed: 31875854
doi: 10.1038/s41586-019-1877-9
Rondinelli, B. et al. H3K4me3 demethylation by the histone demethylase KDM5C/JARID1C promotes DNA replication origin firing. Nucleic Acids Res. 43, 2560–2574 (2015).
pubmed: 25712104
pmcid: 4357704
doi: 10.1093/nar/gkv090
Wu, R., Wang, Z., Zhang, H., Gan, H. & Zhang, Z. H3K9me3 demethylase Kdm4d facilitates the formation of pre-initiative complex and regulates DNA replication. Nucleic Acids Res. 45, 169–180 (2017).
pubmed: 27679476
doi: 10.1093/nar/gkw848
Mishra, S. et al. Cross-talk between lysine-modifying enzymes controls site-specific DNA amplifications. Cell 175, 1716 (2018).
pubmed: 30500540
pmcid: 6373865
doi: 10.1016/j.cell.2018.11.018
Black, J. C. et al. KDM4A lysine demethylase induces site-specific copy gain and rereplication of regions amplified in tumors. Cell 154, 541–555 (2013).
pubmed: 23871696
doi: 10.1016/j.cell.2013.06.051
Klein, K. N. et al. Replication timing maintains the global epigenetic state in human cells. Science 372, 371–378 (2021).
pubmed: 33888635
pmcid: 8173839
doi: 10.1126/science.aba5545
Pope, B. D. et al. Topologically associating domains are stable units of replication-timing regulation. Nature 515, 402–405 (2014).
pubmed: 25409831
pmcid: 4251741
doi: 10.1038/nature13986
Rowley, M. J. & Corces, V. G. Organizational principles of 3D genome architecture. Nat. Rev. Genet. 19, 789–800 (2018).
pubmed: 30367165
doi: 10.1038/s41576-018-0060-8
Falk, M. et al. Heterochromatin drives compartmentalization of inverted and conventional nuclei. Nature 570, 395–399 (2019).
pubmed: 31168090
pmcid: 7206897
doi: 10.1038/s41586-019-1275-3
Feng, Y. et al. Simultaneous epigenetic perturbation and genome imaging reveal distinct roles of H3K9me3 in chromatin architecture and transcription. Genome Biol. 21, 296 (2020).
pubmed: 33292531
pmcid: 7722448
doi: 10.1186/s13059-020-02201-1
Bian, Q., Anderson, E. C., Yang, Q. & Meyer, B. J. Histone H3K9 methylation promotes formation of genome compartments in Caenorhabditis elegans via chromosome compaction and perinuclear anchoring. Proc. Natl Acad. Sci. USA 117, 11459–11470 (2020).
pubmed: 32385148
pmcid: 7261013
doi: 10.1073/pnas.2002068117
Montavon, T. et al. Complete loss of H3K9 methylation dissolves mouse heterochromatin organization. Nat. Commun. 12, 4359 (2021).
pubmed: 34272378
pmcid: 8285382
doi: 10.1038/s41467-021-24532-8
van Steensel, B. & Belmont, A. S. Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression. Cell 169, 780–791 (2017).
pubmed: 28525751
pmcid: 5532494
doi: 10.1016/j.cell.2017.04.022
Towbin, B. D. et al. Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150, 934–947 (2012).
pubmed: 22939621
doi: 10.1016/j.cell.2012.06.051
Kind, J. et al. Single-cell dynamics of genome-nuclear lamina interactions. Cell 153, 178–192 (2013).
pubmed: 23523135
doi: 10.1016/j.cell.2013.02.028
Poleshko, A. et al. H3K9me2 orchestrates inheritance of spatial positioning of peripheral heterochromatin through mitosis. eLife 8, e49278 (2019).
pubmed: 31573510
pmcid: 6795522
doi: 10.7554/eLife.49278
Boettiger, A. N. et al. Super-resolution imaging reveals distinct chromatin folding for different epigenetic states. Nature 529, 418–422 (2016).
pubmed: 26760202
pmcid: 4905822
doi: 10.1038/nature16496
Kundu, S. et al. Polycomb repressive complex 1 generates discrete compacted domains that change during differentiation. Mol. Cell 65, 432–446.e5 (2017).
pubmed: 28157505
pmcid: 5421375
doi: 10.1016/j.molcel.2017.01.009
Du, Z. et al. Polycomb group proteins regulate chromatin architecture in mouse oocytes and early embryos. Mol. Cell 77, 825–839.e7 (2020).
pubmed: 31837995
doi: 10.1016/j.molcel.2019.11.011
Rhodes, J. D. P. et al. Cohesin disrupts polycomb-dependent chromosome interactions in embryonic stem cells. Cell Rep. 30, 820–835.e10 (2020).
pubmed: 31968256
pmcid: 6988126
doi: 10.1016/j.celrep.2019.12.057
Mas, G. et al. Promoter bivalency favors an open chromatin architecture in embryonic stem cells. Nat. Genet. 50, 1452–1462 (2018).
pubmed: 30224650
doi: 10.1038/s41588-018-0218-5
Huang, Y. et al. Polycomb-dependent differential chromatin compartmentalization determines gene coregulation in Arabidopsis. Genome Res. 31, 1230–1244 (2021).
pmcid: 8256866
doi: 10.1101/gr.273771.120
Crane, E. et al. Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature 523, 240–244 (2015).
pubmed: 26030525
pmcid: 4498965
doi: 10.1038/nature14450
Anderson, E. C. et al. X chromosome domain architecture regulates Caenorhabditis elegans lifespan but not dosage compensation. Dev. Cell 51, 192–207.e6 (2019).
pubmed: 31495695
pmcid: 6810858
doi: 10.1016/j.devcel.2019.08.004
Brejc, K. et al. Dynamic control of X chromosome conformation and repression by a histone H4K20 demethylase. Cell 171, 85–102.e23 (2017).
pubmed: 28867287
pmcid: 5678999
doi: 10.1016/j.cell.2017.07.041
Flavahan, W. A. et al. Altered chromosomal topology drives oncogenic programs in SDH-deficient GISTs. Nature 575, 229–233 (2019).
pubmed: 31666694
pmcid: 6913936
doi: 10.1038/s41586-019-1668-3
Faulkner, S., Maksimovic, I. & David, Y. A chemical field guide to histone nonenzymatic modifications. Curr. Opin. Chem. Biol. 63, 180–187 (2021).
pubmed: 34157651
pmcid: 9063854
doi: 10.1016/j.cbpa.2021.05.002
Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823–837 (2007).
pubmed: 17512414
doi: 10.1016/j.cell.2007.05.009
Hebbes, T. R., Thorne, A. W. & Crane-Robinson, C. A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J. 7, 1395–1402 (1988).
pubmed: 3409869
pmcid: 458389
doi: 10.1002/j.1460-2075.1988.tb02956.x
Brind’Amour, J. et al. An ultra-low-input native ChIP-seq protocol for genome-wide profiling of rare cell populations. Nat. Commun. 6, 6033 (2015).
pubmed: 25607992
doi: 10.1038/ncomms7033
Skene, P. J. & Henikoff, S. An efficient targeted nuclease strategy for high-resolution mapping of DNA binding sites. eLife 6, e21856 (2017). Describes mapping of protein–DNA interactions by CUT&RUN as an attractive alternative to ChIP–seq.
pubmed: 28079019
pmcid: 5310842
doi: 10.7554/eLife.21856
Hainer, S. J. & Fazzio, T. G. High-resolution chromatin profiling using CUT&RUN. Curr. Protoc. Mol. Biol. 126, e85 (2019).
pubmed: 30688406
pmcid: 6422702
doi: 10.1002/cpmb.85
Brahma, S. & Henikoff, S. RSC-associated subnucleosomes define MNase-sensitive promoters in yeast. Mol. Cell 73, 238–249.e3 (2019).
pubmed: 30554944
doi: 10.1016/j.molcel.2018.10.046
Kaya-Okur, H. S. et al. CUT&Tag for efficient epigenomic profiling of small samples and single cells. Nat. Commun. 10, 1930 (2019).
pubmed: 31036827
pmcid: 6488672
doi: 10.1038/s41467-019-09982-5
Meers, M. P., Janssens, D. H. & Henikoff, S. Multifactorial chromatin regulatory landscapes at single cell resolution. Preprint at bioRxiv https://doi.org/10.1101/2021.07.08.451691v1.full (2021).
doi: 10.1101/2021.07.08.451691v1.full
Gopalan, S., Wang, Y., Harper, N. W., Garber, M. & Fazzio, T. G. Simultaneous profiling of multiple chromatin proteins in the same cells. Mol. Cell 81, 4736–4746.e5 (2021).
pubmed: 34637755
doi: 10.1016/j.molcel.2021.09.019
Deng, Y. et al. Spatial-CUT&Tag: spatially resolved chromatin modification profiling at the cellular level. Science 375, 681–686 (2022).
pubmed: 35143307
doi: 10.1126/science.abg7216
Harada, A. et al. A chromatin integration labelling method enables epigenomic profiling with lower input. Nat. Cell Biol. 21, 287–296 (2019).
pubmed: 30532068
doi: 10.1038/s41556-018-0248-3
Altemose, N. et al. DiMeLo-seq: a long-read, single-molecule method for mapping protein-DNA interactions genome-wide. Preprint at bioRxiv https://doi.org/10.1101/2021.07.06.451383v1 (2021).
doi: 10.1101/2021.07.06.451383v1
Armeev, G. A., Kniazeva, A. S., Komarova, G. A., Kirpichnikov, M. P. & Shaytan, A. K. Histone dynamics mediate DNA unwrapping and sliding in nucleosomes. Nat. Commun. 12, 2387 (2021).
pubmed: 33888707
pmcid: 8062685
doi: 10.1038/s41467-021-22636-9
Xia, W. et al. Resetting histone modifications during human parental-to-zygotic transition. Science 365, 353–360 (2019).
pubmed: 31273069
doi: 10.1126/science.aaw5118
van de Werken, C. et al. Paternal heterochromatin formation in human embryos is H3K9/HP1 directed and primed by sperm-derived histone modifications. Nat. Commun. 5, 5868 (2014).
pubmed: 25519718
doi: 10.1038/ncomms6868
Wang, C. et al. Reprogramming of H3K9me3-dependent heterochromatin during mammalian embryo development. Nat. Cell Biol. 20, 620–631 (2018).
pubmed: 29686265
doi: 10.1038/s41556-018-0093-4
Boskovic, A. et al. Analysis of active chromatin modifications in early mammalian embryos reveals uncoupling of H2A.Z acetylation and H3K36 trimethylation from embryonic genome activation. Epigenetics 7, 747–757 (2012).
pubmed: 22647320
doi: 10.4161/epi.20584
Zheng, H. et al. Resetting epigenetic memory by reprogramming of histone modifications in mammals. Mol. Cell 63, 1066–1079 (2016).
pubmed: 27635762
doi: 10.1016/j.molcel.2016.08.032
Lindeman, L. C. et al. Prepatterning of developmental gene expression by modified histones before zygotic genome activation. Dev. Cell 21, 993–1004 (2011).
pubmed: 22137762
doi: 10.1016/j.devcel.2011.10.008
Vastenhouw, N. L. et al. Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464, 922–926 (2010).
pubmed: 20336069
pmcid: 2874748
doi: 10.1038/nature08866
Laue, K., Rajshekar, S., Courtney, A. J., Lewis, Z. A. & Goll, M. G. The maternal to zygotic transition regulates genome-wide heterochromatin establishment in the zebrafish embryo. Nat. Commun. 10, 1551 (2019).
pubmed: 30948728
pmcid: 6449393
doi: 10.1038/s41467-019-09582-3
Zhang, B. et al. Widespread enhancer dememorization and promoter priming during parental-to-zygotic transition. Mol. Cell 72, 673–686.e6 (2018).
pubmed: 30444999
doi: 10.1016/j.molcel.2018.10.017
Akkers, R. C. et al. A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos. Dev. Cell 17, 425–434 (2009).
pubmed: 19758566
pmcid: 2746918
doi: 10.1016/j.devcel.2009.08.005
Oikawa, M. et al. Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription. Nat. Commun. 11, 3491 (2020).
pubmed: 32661239
pmcid: 7359334
doi: 10.1038/s41467-020-17238-w
Chen, K. et al. A global change in RNA polymerase II pausing during the Drosophila midblastula transition. eLife 2, e00861 (2013).
pubmed: 23951546
pmcid: 3743134
doi: 10.7554/eLife.00861
Li, X. Y., Harrison, M. M., Villalta, J. E., Kaplan, T. & Eisen, M. B. Establishment of regions of genomic activity during the Drosophila maternal to zygotic transition. eLife 3, e03737 (2014).
pmcid: 4358338
doi: 10.7554/eLife.03737
Seller, C. A., Cho, C. Y. & O’Farrell, P. H. Rapid embryonic cell cycles defer the establishment of heterochromatin by Eggless/SetDB1 in Drosophila. Genes Dev. 33, 403–417 (2019).
pubmed: 30808658
pmcid: 6446540
doi: 10.1101/gad.321646.118
Mutlu, B. et al. Regulated nuclear accumulation of a histone methyltransferase times the onset of heterochromatin formation in C. elegans embryos. Sci. Adv. 4, eaat6224 (2018).
pubmed: 30140741
pmcid: 6105299
doi: 10.1126/sciadv.aat6224
Wang, S., Fisher, K. & Poulin, G. B. Lineage specific trimethylation of H3 on lysine 4 during C. elegans early embryogenesis. Dev. Biol. 355, 227–238 (2011).
pubmed: 21549110
doi: 10.1016/j.ydbio.2011.04.010
Kaneshiro, K. R., Rechtsteiner, A. & Strome, S. Sperm-inherited H3K27me3 impacts offspring transcription and development in C. elegans. Nat. Commun. 10, 1271 (2019).
pubmed: 30894520
pmcid: 6426959
doi: 10.1038/s41467-019-09141-w
Kreher, J. et al. Distinct roles of two histone methyltransferases in transmitting H3K36me3-based epigenetic memory across generations in Caenorhabditis elegans. Genetics 210, 969–982 (2018).
pubmed: 30217796
pmcid: 6218224
doi: 10.1534/genetics.118.301353
Methot, S. P. et al. H3K9me selectively blocks transcription factor activity and ensures differentiated tissue integrity. Nat. Cell Biol. 23, 1163–1175 (2021).
pubmed: 34737442
pmcid: 8572725
doi: 10.1038/s41556-021-00776-w
Bhattacharyya, T. et al. Prdm9 and meiotic cohesin proteins cooperatively promote DNA double-strand break formation in mammalian spermatocytes. Curr. Biol. 31, 1351 (2021).
pubmed: 33756132
pmcid: 8063969
doi: 10.1016/j.cub.2021.03.002
Gibson, B. A. et al. Organization of chromatin by intrinsic and regulated phase separation. Cell 179, 470–484.e21 (2019).
pubmed: 31543265
pmcid: 6778041
doi: 10.1016/j.cell.2019.08.037
Sabari, B. R. et al. Coactivator condensation at super-enhancers links phase separation and gene control. Science 361, eaar3958 (2018).
pubmed: 29930091
pmcid: 6092193
doi: 10.1126/science.aar3958
Cho, W. K. et al. Mediator and RNA polymerase II clusters associate in transcription-dependent condensates. Science 361, 412–415 (2018).
pubmed: 29930094
pmcid: 6543815
doi: 10.1126/science.aar4199
Chong, S. et al. Imaging dynamic and selective low-complexity domain interactions that control gene transcription. Science 361, eaar2555 (2018).
pubmed: 29930090
pmcid: 6961784
doi: 10.1126/science.aar2555
Strickfaden, H. et al. Condensed chromatin behaves like a solid on the mesoscale in vitro and in living cells. Cell 183, 1772–1784.e13 (2020).
pubmed: 33326747
doi: 10.1016/j.cell.2020.11.027
Strom, A. R. et al. Phase separation drives heterochromatin domain formation. Nature 547, 241–245 (2017).
pubmed: 28636597
pmcid: 6022742
doi: 10.1038/nature22989
Larson, A. G. et al. Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin. Nature 547, 236–240 (2017).
pubmed: 28636604
pmcid: 5606208
doi: 10.1038/nature22822
Wang, L. et al. Histone modifications regulate chromatin compartmentalization by contributing to a phase separation mechanism. Mol. Cell 76, 646–659.e6 (2019).
pubmed: 31543422
doi: 10.1016/j.molcel.2019.08.019
Erdel, F. et al. Mouse heterochromatin adopts digital compaction states without showing hallmarks of HP1-driven liquid-liquid phase separation. Mol. Cell 78, 236–249.e7 (2020).
pubmed: 32101700
pmcid: 7163299
doi: 10.1016/j.molcel.2020.02.005
McSwiggen, D. T., Mir, M., Darzacq, X. & Tjian, R. Evaluating phase separation in live cells: diagnosis, caveats, and functional consequences. Genes Dev. 33, 1619–1634 (2019).
pubmed: 31594803
pmcid: 6942051
doi: 10.1101/gad.331520.119
Gallego, L. D. et al. Phase separation directs ubiquitination of gene-body nucleosomes. Nature 579, 592–597 (2020).
pubmed: 32214243
pmcid: 7481934
doi: 10.1038/s41586-020-2097-z
Eeftens, J. M., Kapoor, M., Michieletto, D. & Brangwynne, C. P. Polycomb condensates can promote epigenetic marks but are not required for sustained chromatin compaction. Nat. Commun. 12, 5888 (2021).
pubmed: 34620850
pmcid: 8497513
doi: 10.1038/s41467-021-26147-5
Snowden, A. W., Gregory, P. D., Case, C. C. & Pabo, C. O. Gene-specific targeting of H3K9 methylation is sufficient for initiating repression in vivo. Curr. Biol. 12, 2159–2166 (2002).
pubmed: 12498693
doi: 10.1016/S0960-9822(02)01391-X
Gaj, T., Gersbach, C. A. & Barbas, C. F. 3rd ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 31, 397–405 (2013).
pubmed: 23664777
pmcid: 3694601
doi: 10.1016/j.tibtech.2013.04.004
Martinez-Balbas, M. A. et al. The acetyltransferase activity of CBP stimulates transcription. EMBO J. 17, 2886–2893 (1998).
pubmed: 9582282
pmcid: 1170629
doi: 10.1093/emboj/17.10.2886
Chiarella, A. M. et al. Dose-dependent activation of gene expression is achieved using CRISPR and small molecules that recruit endogenous chromatin machinery. Nat. Biotechnol. 38, 50–55 (2020).
pubmed: 31712774
doi: 10.1038/s41587-019-0296-7
Kearns, N. A. et al. Functional annotation of native enhancers with a Cas9–histone demethylase fusion. Nat. Methods 12, 401–403 (2015).
pubmed: 25775043
pmcid: 4414811
doi: 10.1038/nmeth.3325
Hilton, I. B. et al. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat. Biotechnol. 33, 510–517 (2015).
pubmed: 25849900
pmcid: 4430400
doi: 10.1038/nbt.3199
Kwon, D. Y., Zhao, Y. T., Lamonica, J. M. & Zhou, Z. Locus-specific histone deacetylation using a synthetic CRISPR-Cas9-based HDAC. Nat. Commun. 8, 15315 (2017).
pubmed: 28497787
pmcid: 5437308
doi: 10.1038/ncomms15315
O’Geen, H. et al. dCas9-based epigenome editing suggests acquisition of histone methylation is not sufficient for target gene repression. Nucleic Acids Res. 45, 9901–9916 (2017).
pubmed: 28973434
pmcid: 5622328
doi: 10.1093/nar/gkx578
Verkuijl, S. A. & Rots, M. G. The influence of eukaryotic chromatin state on CRISPR–Cas9 editing efficiencies. Curr. Opin. Biotechnol. 55, 68–73 (2019).
pubmed: 30189348
doi: 10.1016/j.copbio.2018.07.005
Jain, S. et al. TALEN outperforms Cas9 in editing heterochromatin target sites. Nat. Commun. 12, 606 (2021).
pubmed: 33504770
pmcid: 7840734
doi: 10.1038/s41467-020-20672-5