The biogenesis and function of nucleosome arrays.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
01 12 2021
01 12 2021
Historique:
received:
08
04
2020
accepted:
09
11
2021
entrez:
2
12
2021
pubmed:
3
12
2021
medline:
29
12
2021
Statut:
epublish
Résumé
Numerous chromatin remodeling enzymes position nucleosomes in eukaryotic cells. Aside from these factors, transcription, DNA sequence, and statistical positioning of nucleosomes also shape the nucleosome landscape. The precise contributions of these processes remain unclear due to their functional redundancy in vivo. By incisive genome engineering, we radically decreased their redundancy in Saccharomyces cerevisiae. The transcriptional machinery strongly disrupts evenly spaced nucleosomes. Proper nucleosome density and DNA sequence are critical for their biogenesis. The INO80 remodeling complex helps space nucleosomes in vivo and positions the first nucleosome over genes in an H2A.Z-independent fashion. INO80 requires its Arp8 subunit but unexpectedly not the Nhp10 module for spacing. Cells with irregularly spaced nucleosomes suffer from genotoxic stress including DNA damage, recombination and transpositions. We derive a model of the biogenesis of the nucleosome landscape and suggest that it evolved not only to regulate but also to protect the genome.
Identifiants
pubmed: 34853297
doi: 10.1038/s41467-021-27285-6
pii: 10.1038/s41467-021-27285-6
pmc: PMC8636622
doi:
Substances chimiques
ARP8 protein, S cerevisiae
0
Chromatin
0
High Mobility Group Proteins
0
Histones
0
Microfilament Proteins
0
NHP10 protein, S cerevisiae
0
Nucleosomes
0
Saccharomyces cerevisiae Proteins
0
Transcription Factors
0
DNA
9007-49-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7011Informations de copyright
© 2021. The Author(s).
Références
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
Jiang, C. & Pugh, B. F. Nucleosome positioning and gene regulation: advances through genomics. Nat. Rev. Genet. 10, 161–172 (2009).
pubmed: 19204718
pmcid: 4860946
doi: 10.1038/nrg2522
Kubik, S. et al. Opposing chromatin remodelers control transcription initiation frequency and start site selection. Nat. Struct. Mol. Biol. 26, 744–754 (2019).
pubmed: 31384063
doi: 10.1038/s41594-019-0273-3
Weber, C. M., Ramachandran, S. & Henikoff, S. Nucleosomes Are Context-Specific, H2A.Z-Modulated Barriers to RNA Polymerase. Mol. Cell 53, 819–830 (2014).
pubmed: 24606920
doi: 10.1016/j.molcel.2014.02.014
Groth, A., Rocha, W., Verreault, A. & Almouzni, G. Chromatin Challenges during DNA Replication and Repair. Cell 128, 721–733 (2007).
pubmed: 17320509
doi: 10.1016/j.cell.2007.01.030
Yadav, T. & Whitehouse, I. Replication-Coupled Nucleosome Assembly and Positioning by ATP-Dependent Chromatin-Remodeling Enzymes. Cell Rep. 15, 715–723 (2016).
pubmed: 27149855
pmcid: 5063657
doi: 10.1016/j.celrep.2016.03.059
Vasseur, P. et al. Dynamics of Nucleosome Positioning Maturation following Genomic Replication. Cell Rep. 16, 2651–2665 (2016).
pubmed: 27568571
pmcid: 5014762
doi: 10.1016/j.celrep.2016.07.083
Kubik, S. et al. Sequence-Directed Action of RSC Remodeler and General Regulatory Factors Modulates +1 Nucleosome Position to Facilitate Transcription. Mol. Cell 71, 89–102.e5 (2018).
pubmed: 29979971
doi: 10.1016/j.molcel.2018.05.030
Ocampo, J., Chereji, R. V., Eriksson, P. R. & Clark, D. J. Contrasting roles of the RSC and ISW1/CHD1 chromatin remodelers in RNA polymerase II elongation and termination. Genome Res 29, 407–417 (2019).
pubmed: 30683752
pmcid: 6396426
doi: 10.1101/gr.242032.118
Ocampo, J., Chereji, R. V., Eriksson, P. R. & Clark, D. J. The ISW1 and CHD1 ATP-dependent chromatin remodelers compete to set nucleosome spacing in vivo. Nucleic Acids Res 44, 4625–4635 (2016).
pubmed: 26861626
pmcid: 4889916
doi: 10.1093/nar/gkw068
Gkikopoulos, T. et al. A Role for Snf2-Related Nucleosome-Spacing Enzymes in Genome-Wide Nucleosome. Organ. Sci. 333, 1758–1760 (2011).
Lieleg, C. et al. Nucleosome Spacing Generated by ISWI and CHD1 Remodelers Is Constant Regardless of Nucleosome Density. Mol. Cell. Biol. 35, 1588–1605 (2015).
pubmed: 25733687
pmcid: 4387221
doi: 10.1128/MCB.01070-14
Yamada, K. et al. Structure and mechanism of the chromatin remodelling factor ISW1a. Nature 472, 448–453 (2011).
pubmed: 21525927
doi: 10.1038/nature09947
Yang, J. G., Madrid, T. S., Sevastopoulos, E. & Narlikar, G. J. The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing. Nat. Struct. Mol. Biol. 13, 1078–1083 (2006).
pubmed: 17099699
doi: 10.1038/nsmb1170
Stockdale, C., Flaus, A., Ferreira, H. & Owen-Hughes, T. Analysis of Nucleosome Repositioning by Yeast ISWI and Chd1 Chromatin Remodeling Complexes. J. Biol. Chem. 281, 16279–16288 (2006).
pubmed: 16606615
doi: 10.1074/jbc.M600682200
Udugama, M., Sabri, A. & Bartholomew, B. The INO80 ATP-Dependent Chromatin Remodeling Complex Is a Nucleosome Spacing Factor. Mol. Cell. Biol. 31, 662–673 (2011).
pubmed: 21135121
doi: 10.1128/MCB.01035-10
Zhou, C. Y. et al. The Yeast INO80 Complex Operates as a Tunable DNA Length-Sensitive Switch to Regulate Nucleosome Sliding. Mol. Cell 69, 677–688.e9 (2018).
pubmed: 29452642
pmcid: 5897057
doi: 10.1016/j.molcel.2018.01.028
Brahma, S., Ngubo, M., Paul, S., Udugama, M. & Bartholomew, B. The Arp8 and Arp4 module acts as a DNA sensor controlling INO80 chromatin remodeling. Nat. Commun. 9, 3309 (2018).
pubmed: 30120252
pmcid: 6098158
doi: 10.1038/s41467-018-05710-7
Knoll, K. R. et al. The nuclear actin-containing Arp8 module is a linker DNA sensor driving INO80 chromatin remodeling. Nat. Struct. Mol. Biol. 25, 823–832 (2018).
pubmed: 30177756
doi: 10.1038/s41594-018-0115-8
Kornberg, R. D. & Stryer, L. Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res 16, 6677–6690 (1988).
pubmed: 3399412
pmcid: 338322
doi: 10.1093/nar/16.14.6677
Celona, B. et al. Substantial Histone Reduction Modulates Genomewide Nucleosomal Occupancy and Global Transcriptional Output. PLoS Biol. 9, e1001086 (2011).
pubmed: 21738444
pmcid: 3125158
doi: 10.1371/journal.pbio.1001086
Gossett, A. J. & Lieb, J. D. In Vivo Effects of Histone H3 Depletion on Nucleosome Occupancy and Position in Saccharomyces cerevisiae. PLoS Genet 8, e1002771 (2012).
pubmed: 22737086
pmcid: 3380831
doi: 10.1371/journal.pgen.1002771
van Bakel, H. et al. A Compendium of Nucleosome and Transcript Profiles Reveals Determinants of Chromatin Architecture and Transcription. PLoS Genet 9, e1003479 (2013).
pubmed: 23658529
pmcid: 3642058
doi: 10.1371/journal.pgen.1003479
Hughes, A. L., Jin, Y., Rando, O. J. & Struhl, K. A Functional Evolutionary Approach to Identify Determinants of Nucleosome Positioning: A Unifying Model for Establishing the Genome-wide Pattern. Mol. Cell 48, 5–15 (2012).
pubmed: 22885008
pmcid: 3472102
doi: 10.1016/j.molcel.2012.07.003
Struhl, K. & Segal, E. Determinants of nucleosome positioning. Nat. Struct. Mol. Biol. 20, 267–273 (2013).
pubmed: 23463311
pmcid: 3740156
doi: 10.1038/nsmb.2506
Krietenstein, N. et al. Genomic Nucleosome Organization Reconstituted with Pure Proteins. Cell 167, 709–721.e12 (2016).
pubmed: 27768892
pmcid: 5240917
doi: 10.1016/j.cell.2016.09.045
Tsukiyama, T., Palmer, J., Landel, C. C., Shiloach, J. & Wu, C. Characterization of the Imitation Switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae. Genes Dev. 13, 686–697 (1999).
pubmed: 10090725
pmcid: 316555
doi: 10.1101/gad.13.6.686
Mann, R. K. & Grunstein, M. Histone H3 N-terminal mutations allow hyperactivation of the yeast GAL1 gene in vivo. EMBO J. 11, 3297–3306 (1992).
pubmed: 1505519
pmcid: 556864
doi: 10.1002/j.1460-2075.1992.tb05408.x
Kim, U. J., Han, M., Kayne, P. & Grunstein, M. Effects of histone H4 depletion on the cell cycle and transcription of Saccharomyces cerevisiae. EMBO J. 7, 2211–2219 (1988).
pubmed: 3046933
pmcid: 454562
doi: 10.1002/j.1460-2075.1988.tb03060.x
Haruki, H., Nishikawa, J. & Laemmli, U. K. The Anchor-Away Technique: Rapid, Conditional Establishment of Yeast Mutant Phenotypes. Mol. Cell 31, 925–932 (2008).
pubmed: 18922474
doi: 10.1016/j.molcel.2008.07.020
Shivaswamy, S. et al. Dynamic Remodeling of Individual Nucleosomes Across a Eukaryotic Genome in Response to Transcriptional Perturbation. PLoS Biol. 6, e65 (2008).
pubmed: 18351804
pmcid: 2267817
doi: 10.1371/journal.pbio.0060065
Lu, Z. & Lin, Z. Pervasive and dynamic transcription initiation in Saccharomyces cerevisiae. Genome Res 29, 1198–1210 (2019).
pubmed: 31076411
pmcid: 6633255
doi: 10.1101/gr.245456.118
Zhang, Y. et al. Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat. Struct. Mol. Biol. 16, 847–852 (2009).
pubmed: 19620965
pmcid: 2823114
doi: 10.1038/nsmb.1636
Tramantano, M. et al. Constitutive turnover of histone H2A.Z at yeast promoters requires the preinitiation complex. eLife 5, e14243 (2016).
pubmed: 27438412
pmcid: 4995100
doi: 10.7554/eLife.14243
Kubik, S. et al. Nucleosome Stability Distinguishes Two Different Promoter Types at All Protein-Coding Genes in Yeast. Mol. Cell 60, 422–434 (2015).
pubmed: 26545077
doi: 10.1016/j.molcel.2015.10.002
Yen, K., Vinayachandran, V., Batta, K., Koerber, R. T. & Pugh, B. F. Genome-wide Nucleosome Specificity and Directionality of Chromatin Remodelers. Cell 149, 1461–1473 (2012).
pubmed: 22726434
pmcid: 3397793
doi: 10.1016/j.cell.2012.04.036
Klein-Brill, A., Joseph-Strauss, D., Appleboim, A. & Friedman, N. Dynamics of Chromatin and Transcription during Transient Depletion of the RSC Chromatin Remodeling Complex. Cell Rep. 26, 279–292.e5 (2019).
pubmed: 30605682
pmcid: 6315372
doi: 10.1016/j.celrep.2018.12.020
Papamichos-Chronakis, M. & Peterson, C. L. The Ino80 chromatin-remodeling enzyme regulates replisome function and stability. Nat. Struct. Mol. Biol. 15, 338–345 (2008).
pubmed: 18376411
doi: 10.1038/nsmb.1413
Deniz, Ö., Flores, O., Aldea, M., Soler-López, M. & Orozco, M. Nucleosome architecture throughout the cell cycle. Sci. Rep. 6, 19729 (2016).
pubmed: 26818620
pmcid: 4730144
doi: 10.1038/srep19729
Cutler, S., Lee, L. J. & Tsukiyama, T. Chromatin Remodeling Factors Isw2 and Ino80 Regulate Chromatin, Replication, and Copy Number of the Saccharomyces cerevisiae Ribosomal DNA Locus. Genetics 210, 1543–1556 (2018).
pubmed: 30355728
pmcid: 6283175
doi: 10.1534/genetics.118.301579
Tosi, A. et al. Structure and Subunit Topology of the INO80 Chromatin Remodeler and Its Nucleosome Complex. Cell 154, 1207–1219 (2013).
pubmed: 24034245
doi: 10.1016/j.cell.2013.08.016
Watanabe, S. et al. Structural analyses of the chromatin remodelling enzymes INO80-C and SWR-C. Nat. Commun. 6, 7108 (2015).
pubmed: 25964121
doi: 10.1038/ncomms8108
Chen, K. et al. DANPOS: Dynamic analysis of nucleosome position and occupancy by sequencing. Genome Res 23, 341–351 (2013).
pubmed: 23193179
pmcid: 3561875
doi: 10.1101/gr.142067.112
Eustermann, S. et al. Structural basis for ATP-dependent chromatin remodelling by the INO80 complex. Nature 556, 386–390 (2018).
pubmed: 29643509
pmcid: 6071913
doi: 10.1038/s41586-018-0029-y
Brahma, S. et al. INO80 exchanges H2A.Z for H2A by translocating on DNA proximal to histone dimers. Nat. Commun. 8, 15616 (2017).
pubmed: 28604691
pmcid: 5472786
doi: 10.1038/ncomms15616
Ioshikhes, I. P., Albert, I., Zanton, S. J. & Pugh, B. F. Nucleosome positions predicted through comparative genomics. Nat. Genet. 38, 1210–1215 (2006).
pubmed: 16964265
doi: 10.1038/ng1878
Ganguli, D., Chereji, R. V., Iben, J. R., Cole, H. A. & Clark, D. J. RSC-dependent constructive and destructive interference between opposing arrays of phased nucleosomes in yeast. Genome Res 24, 1637–1649 (2014).
pubmed: 25015381
pmcid: 4199373
doi: 10.1101/gr.177014.114
Kato, H., Shimizu, M. & Urano, T. Chemical map-based prediction of nucleosome positioning using the Bioconductor package nuCpos. BMC Bioinforma. 22, 322 (2021).
doi: 10.1186/s12859-021-04240-2
Alabert, C., Bianco, J. N. & Pasero, P. Differential regulation of homologous recombination at DNA breaks and replication forks by the Mrc1 branch of the S-phase checkpoint. EMBO J. 28, 1131–1141 (2009).
pubmed: 19322196
pmcid: 2683710
doi: 10.1038/emboj.2009.75
Morrison, A. J. Genome maintenance functions of the INO80 chromatin remodeller. Philos. Trans. R. Soc. B Biol. Sci. 372, 20160289 (2017).
doi: 10.1098/rstb.2016.0289
Mimitou, E. P. & Symington, L. S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455, 770–774 (2008).
pubmed: 18806779
doi: 10.1038/nature07312
van Attikum, H., Fritsch, O., Hohn, B. & Gasser, S. M. Recruitment of the INO80 Complex by H2A Phosphorylation Links ATP-Dependent Chromatin Remodeling with DNA Double-Strand Break Repair. Cell 119, 777–788 (2004).
pubmed: 15607975
doi: 10.1016/j.cell.2004.11.033
Hauer, M. H. et al. Histone degradation in response to DNA damage enhances chromatin dynamics and recombination rates. Nat. Struct. Mol. Biol. 24, 99–107 (2017).
pubmed: 28067915
doi: 10.1038/nsmb.3347
Michel, A. H. et al. Functional mapping of yeast genomes by saturated transposition. eLife 6, e23570 (2017).
pubmed: 28481201
pmcid: 5466422
doi: 10.7554/eLife.23570
Gamarra, N. & Narlikar, G. J. Collaboration through chromatin: motors of transcription and chromatin structure. J. Mol. Biol. 433, 166876 (2021).
pubmed: 33556407
doi: 10.1016/j.jmb.2021.166876
Smolle, M. et al. Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat. Struct. Mol. Biol. 19, 884–892 (2012).
pubmed: 22922743
pmcid: 3560298
doi: 10.1038/nsmb.2312
Oberbeckmann, E. et al. Ruler elements in chromatin remodelers set nucleosome array spacing and phasing. Nat. Commun. 12, 3232 (2021).
pubmed: 34050140
pmcid: 8163753
doi: 10.1038/s41467-021-23015-0
Stergachis, A. B., Debo, B. M., Haugen, E., Churchman, L. S. & Stamatoyannopoulos, J. A. Single-molecule regulatory architectures captured by chromatin fiber sequencing. Science 368, 1449–1454 (2020).
pubmed: 32587015
doi: 10.1126/science.aaz1646
Abdulhay, N. J. et al. Massively multiplex single-molecule oligonucleosome footprinting. eLife 9, e59404 (2020).
pubmed: 33263279
pmcid: 7735760
doi: 10.7554/eLife.59404
Morrison, A. J. et al. INO80 and gamma-H2AX Interaction Links ATP-Dependent Chromatin Remodeling to DNA Damage Repair. Cell 119, 775–767 (2004).
doi: 10.1016/j.cell.2004.11.037
Baldi, S., Krebs, S., Blum, H. & Becker, P. B. Genome-wide measurement of local nucleosome array regularity and spacing by nanopore sequencing. Nat. Struct. Mol. Biol. 25, 894–901 (2018).
pubmed: 30127356
doi: 10.1038/s41594-018-0110-0
Cole, H. A., Ocampo, J., Iben, J. R., Chereji, R. V. & Clark, D. J. Heavy transcription of yeast genes correlates with differential loss of histone H2B relative to H4 and queued RNA polymerases. Nucleic Acids Res 42, 12512–12522 (2014).
pubmed: 25348398
pmcid: 4227747
doi: 10.1093/nar/gku1013
Schwabish, M. A. & Struhl, K. Evidence for Eviction and Rapid Deposition of Histones upon Transcriptional Elongation by RNA Polymerase II. Mol. Cell. Biol. 24, 10111–10117 (2004).
pubmed: 15542822
pmcid: 529037
doi: 10.1128/MCB.24.23.10111-10117.2004
Shen, C.-H., Leblanc, B. P., Alfieri, J. A. & Clark, D. J. Remodeling of Yeast CUP1 Chromatin Involves Activator-Dependent Repositioning of Nucleosomes over the Entire Gene and Flanking Sequences. Mol. Cell. Biol. 21, 534–547 (2001).
pubmed: 11134341
pmcid: 86616
doi: 10.1128/MCB.21.2.534-547.2001
Petesch, S. J. & Lis, J. T. Rapid, Transcription-Independent Loss of Nucleosomes over a Large Chromatin Domain at Hsp70 Loci. Cell 134, 74–84 (2008).
pubmed: 18614012
pmcid: 2527511
doi: 10.1016/j.cell.2008.05.029
Oberbeckmann, E. et al. Absolute nucleosome occupancy map for the Saccharomyces cerevisiae genome. Genome Res 29, 1996–2009 (2019).
pubmed: 31694866
pmcid: 6886505
doi: 10.1101/gr.253419.119
Weiner, A., Hughes, A., Yassour, M., Rando, O. J. & Friedman, N. High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res 20, 90–100 (2010).
pubmed: 19846608
pmcid: 2798834
doi: 10.1101/gr.098509.109
Singh, A. K. & Mueller-Planitz, F. Nucleosome Positioning and Spacing: From Mechanism to Function. J. Mol. Biol. 433, 166847 (2021).
pubmed: 33539878
doi: 10.1016/j.jmb.2021.166847
Hartley, P. D. & Madhani, H. D. Mechanisms that Specify Promoter Nucleosome Location and Identity. Cell 137, 445–458 (2009).
pubmed: 19410542
pmcid: 2677553
doi: 10.1016/j.cell.2009.02.043
Wittschieben, B. O. Overlapping roles for the histone acetyltransferase activities of SAGA and Elongator in vivo. EMBO J. 19, 3060–3068 (2000).
pubmed: 10856249
pmcid: 203375
doi: 10.1093/emboj/19.12.3060
Almer, A. & Horz, W. Nuclease hypersensitive regions with adjacent positioned nucleosomes mark the gene boundaries of the PH05/PH03 locus. EMBO J. 5, 2681–2687 (1986).
pubmed: 3023055
pmcid: 1167169
doi: 10.1002/j.1460-2075.1986.tb04551.x
Schep, A. N. et al. Structured nucleosome fingerprints enable high-resolution mapping of chromatin architecture within regulatory regions. Genome Res 25, 1757–1770 (2015).
pubmed: 26314830
pmcid: 4617971
doi: 10.1101/gr.192294.115
Chereji, R. V., Ramachandran, S., Bryson, T. D. & Henikoff, S. Precise genome-wide mapping of single nucleosomes and linkers in vivo. Genome Biol. 19, 19 (2018).
pubmed: 29426353
pmcid: 5807854
doi: 10.1186/s13059-018-1398-0
Gittens, W. H. et al. A nucleotide resolution map of Top2-linked DNA breaks in the yeast and human genome. Nat. Commun. 10, 4846 (2019).
pubmed: 31649282
pmcid: 6813358
doi: 10.1038/s41467-019-12802-5