April 28, 2024
Establishment and function of chromatin organization at replication origins – Nature

Establishment and function of chromatin organization at replication origins – Nature

  • Bell, S. P. & Labib, K. Chromosome duplication in Saccharomyces cerevisiae. Genetics 203, 1027–1067 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Eaton, M. L., Galani, K., Kang, S., Bell, S. P. & MacAlpine, D. M. Conserved nucleosome positioning defines replication origins. Genes Dev. 24, 748–753 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Berbenetz, N. M., Nislow, C. & Brown, G. W. Diversity of eukaryotic DNA replication origins revealed by genome-wide analysis of chromatin structure. PLoS Genet. 6, e1001092 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rossi, M. J. et al. A high-resolution protein architecture of the budding yeast genome. Nature 592, 309–314 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Broach, J. R. et al. Localization and sequence analysis of yeast origins of DNA replication. Cold Spring Harb. Symp. Quant. Biol. 47, 1165–1173 (1983).

    Article 
    PubMed 

    Google Scholar
     

  • Siow, C. C., Nieduszynska, S. R., Müller, C. A. & Nieduszynski, C. A. OriDB, the DNA replication origin database updated and extended. Nucleic Acids Res. 40, 682–686 (2012).

    Article 

    Google Scholar
     

  • Nieduszynski, C. A., Knox, Y. & Donaldson, A. D. Genome-wide identification of replication origins in yeast by comparative genomics. Genes Dev. 20, 1874–1879 (2006).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xu, W., Aparicio, J. G., Aparicio, O. M. & Tavaré, S. Genome-wide mapping of ORC and Mcm2p binding sites on tiling arrays and identification of essential ARS consensus sequences in S. cerevisiae. BMC Genomics 7, 276 (2006).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liachko, I., Youngblood, R. A., Keich, U. & Dunham, M. J. High-resolution mapping, characterization, and optimization of autonomously replicating sequences in yeast. Genome Res. 23, 698–704 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kornberg, R. D. & Lorch, Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98, 285–294 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lorch, Y., LaPointe, J. W. & Kornberg, R. D. Nucleosomes inhibit the initiation of transcription but allow chain elongation with the displacement of histones. Cell 49, 203–210 (1987).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Devbhandari, S., Jiang, J., Kumar, C., Whitehouse, I. & Remus, D. Chromatin constrains the initiation and elongation of DNA replication. Mol. Cell 65, 131–141 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Azmi, I. F. et al. Nucleosomes influence multiple steps during replication initiation. eLife 6, e22512 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kurat, C. F., Yeeles, J. T. P., Patel, H., Early, A. & Diffley, J. F. X. Chromatin controls DNA replication origin selection, lagging-strand synthesis, and replication fork rates. Mol. Cell 65, 117–130 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Clapier, C. R., Iwasa, J., Cairns, B. R. & Peterson, C. L. Mechanisms of action and regulation of ATP-dependent chromatin-remodelling complexes. Nat. Rev. Mol. Cell Biol. 18, 407–422 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hartley, P. & Madhani, D. Mechanisms that specify promoter nucleosome location and identity. Cell 137, 445–458 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gkikopoulos, T. et al. A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science 333, 1758–1760 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Krietenstein, N. et al. Genomic nucleosome organization reconstituted with pure proteins. Cell 167, 709–721 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kubik, S. et al. Opposing chromatin remodelers control transcription initiation frequency and start site selection. Nat. Struct. Mol. Biol. 26, 744–754 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Oberbeckmann, E. et al. Ruler elements in chromatin remodelers set nucleosome array spacing and phasing. Nat. Commun. 12, 3232 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 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).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nagai, S., Davis, R. E., Mattei, P. J., Eagen, K. P. & Kornberg, R. D. Chromatin potentiates transcription. Proc. Natl Acad. Sci. USA 114, 1536–1541 (2017).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kornberg, R. D. & Lorch, Y. Primary role of the nucleosome. Mol. Cell 79, 371–375 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lipford, J. R. & Bell, S. P. Nucleosomes positioned by ORC facilitate the initiation of DNA replication. Mol. Cell 7, 21–30 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Oberbeckmann, E. et al. Genome information processing by the INO80 chromatin remodeler positions nucleosomes. Nat. Commun. 12, 3231 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Oberbeckmann, E. et al. Absolute nucleosome occupancy map for the Saccharomyces cerevisiae genome. Genome Res. 29, 1996–2009 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kaplan, N. et al. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458, 362–366 (2009).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Barnes, T. & Korber, P. The active mechanism of nucleosome depletion by poly(dA:dT) tracts in vivo. Int. J. Mol. Sci. 22, 8233 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Singh, A. K., Schauer, T., Pfaller, L., Straub, T. & Mueller-Planitz, F. The biogenesis and function of nucleosome arrays. Nat. Commun. 12, 7011 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • De Ioannes, P. et al. Structure and function of the Orc1 BAH–nucleosome complex. Nat. Commun. 10, 2894 (2019).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Müller, P. et al. The conserved bromo-adjacent homology domain of yeast Orc1 functions in the selection of DNA replication origins within chromatin. Genes Dev. 24, 1418–1433 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Klemm, R. D., Austin, R. J. & Bell, S. P. Coordinate binding of ATP and origin DNA regulates the ATPase activity of the origin recognition complex. Cell 88, 493–502 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bowers, J. L., Randell, J. C. W., Chen, S. & Bell, S. P. ATP hydrolysis by ORC catalyzes reiterative Mcm2–7 assembly at a defined origin of replication. Mol. Cell 16, 967–978 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Evrin, C. et al. In the absence of ATPase activity, pre-RC formation is blocked prior to MCM2–7 hexamer dimerization. Nucleic Acids Res. 41, 3162–3172 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Klemm, R. D. & Bell, S. P. ATP bound to the origin recognition complex is important for preRC formation. Proc. Natl Acad. Sci. USA 98, 8361–8367 (2001).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Coster, G., Frigola, J., Beuron, F., Morris, E. P. & Diffley, J. F. X. Origin licensing requires ATP binding and hydrolysis by the MCM replicative helicase. Mol. Cell 55, 666–677 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, N. et al. Structure of the origin recognition complex bound to DNA replication origin. Nature 559, 217–222 (2018).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Feng, X. et al. The structure of ORC–Cdc6 on an origin DNA reveals the mechanism of ORC activation by the replication initiator Cdc6. Nat. Commun. 12, 2894 (2021).

    Article 
    ADS 

    Google Scholar
     

  • Haberle, V. et al. Two independent transcription initiation codes overlap on vertebrate core promoters. Nature 507, 381–385 (2014).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Soriano, I., Morafraile, E. C., Vázquez, E., Antequera, F. & Segurado, M. Different nucleosomal architectures at early and late replicating origins in Saccharomyces cerevisiae. BMC Genomics 15, 791 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tsankov, A. M., Thompson, D. A., Socha, A., Regev, A. & Rando, O. J. The role of nucleosome positioning in the evolution of gene regulation. PLoS Biol. 8, e1000414 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tsankov, A., Yanagisawa, Y., Rhind, N., Regev, A. & Rando, O. J. Evolutionary divergence of intrinsic and trans-regulated nucleosome positioning sequences reveals plastic rules for chromatin organization. Genome Res. 21, 1851–1862 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yan, C., Chen, H. & Bai, L. Systematic study of nucleosome-displacing factors in budding yeast. Mol. Cell 71, 294–305 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Donovan, B. T., Chen, H., Jipa, C., Bai, L. & Poirier, M. G. Dissociation rate compensation mechanism for budding yeast pioneer transcription factors. eLife 8, e43008 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fernandez Garcia, M. et al. Structural features of transcription factors associating with nucleosome binding. Mol. Cell 75, 921–932.e6 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hsieh, L. J. et al. A hexasome is the preferred substrate for the INO80 chromatin remodeling complex, allowing versatility of function. Mol. Cell 82, 2098–2112.e4 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, S. et al. Origin recognition complex harbors an intrinsic nucleosome remodeling activity. Proc. Natl Acad. Sci. USA 119, e2211568119 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bell, S. P., Mitchell, J., Leber, J., Kobayashi, R. & Stillman, B. The multidomain structure of Orc1 p reveals similarity to regulators of DNA replication and transcriptional silencing. Cell 83, 563–568 (1995).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gavin, K. A., Hidaka, M. & Stillman, B. Conserved initiator proteins in eukaryotes. Science 270, 1667–1671 (1995).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Parker, M. W. et al. A new class of disordered elements controls DNA replication through initiator self-assembly. eLife 8, e48562 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jaremko, M. J., On, K. F., Thomas, D. R., Stillman, B. & Joshua-Tor, L. The dynamic nature of the human origin recognition complex revealed through five cryoEM structures. eLife 9, e58622 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 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).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee, C. S. K. et al. Humanizing the yeast origin recognition complex. Nat. Commun. 12, 33 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, S. et al. Nucleosome-directed replication origin licensing independent of a consensus DNA sequence. Nat. Commun. 13, 4947 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Smith, D. J. & Whitehouse, I. Intrinsic coupling of lagging-strand synthesis to chromatin assembly. Nature 483, 434–438 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jones, G. M. et al. A systematic library for comprehensive overexpression screens in Saccharomyces cerevisiae. Nat. Methods 5, 239–241 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Krietenstein, N., Wippo, C. J., Lieleg, C. & Korber, P. Genome-wide in vitro reconstitution of yeast chromatin with in vivo-like nucleosome positioning. Methods Enzymol. 513, 205–232 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ruone, S., Rhoades, A. R. & Formosa, T. Multiple Nhp6 molecules are required to recruit Spt16–Pob3 to form yFACT complexes and to reorganize nucleosomes. J. Biol. Chem. 278, 45288–45295 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kingston, I. J., Yung, J. S. Y. & Singleton, M. R. Biophysical characterization of the centromere-specific nucleosome from budding yeast. J. Biol. Chem. 286, 4021–4026 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Simon, R. H. & Felsenfeld, G. A new procedure for purifying histone pairs H2A + H2B and H3 + H4 from chromatin using hydroxylapatite. Nucleic Acids Res. 6, 689–696 (1979).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shen, X. Preparation and analysis of the INO80 complex. Methods Enzymol. 377, 401–412 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Vary, J. C., Fazzio, T. G. & Tsukiyama, T. Assembly of yeast chromatin using ISWI complexes. Methods Enzymol. 375, 88–102 (2003).

    Article 

    Google Scholar
     

  • Wittmeyer, J., Saha, A. & Cairns, B. DNA translocation and nucleosome remodeling assays by the RSC chromatin remodeling complex. Methods Enzymol. 377, 322–343 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bantele, S. C. S., Ferreira, P., Gritenaite, D., Boos, D. & Pfander, B. Targeting of the Fun30 nucleosome remodeller by the Dpb11 scaffold facilitates cell cycle-regulated DNA end resection. Elife 6, e21687 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Biswas, D., Yu, Y., Prall, M., Formosa, T. & Stillman, D. J. The yeast FACT complex has a role in transcriptional initiation. Mol. Cell. Biol. 25, 5812–5822 (2005).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chacin, E. et al. A CDK-regulated chromatin segregase promoting chromosome replication. Nat. Commun. 12, 5224 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Frigola, J., Remus, D., Mehanna, A. & Diffley, J. F. X. ATPase-dependent quality control of DNA replication origin licensing. Nature 495, 339–343 (2013).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Callebaut, I., Courvalin, J. C. & Mornon, J. P. The BAH (bromo-adjacent homology) domain: a link between DNA methylation, replication and transcriptional regulation. FEBS Lett. 446, 189–193 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mészáros, B., Erdös, G. & Dosztányi, Z. IUPred2A: context-dependent prediction of protein disorder as a function of redox state and protein binding. Nucleic Acids Res. 46, 329–337 (2018).

    Article 

    Google Scholar
     

  • 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).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dechassa, M. L. et al. Architecture of the SWI/SNF–nucleosome complex. Mol. Cell. Biol. 28, 6010–6021 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Almer, A. & Hörz, W. Nuclease hypersensitive regions with adjacent positioned nucleosomes mark the gene boundaries of the PHO5/PHO3 locus in yeast. EMBO J. 5, 2681–2687 (1986).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Remus, D. et al. Concerted loading of Mcm2–7 double hexamers around DNA during DNA replication origin licensing. Cell 139, 719–730 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Evrin, C. et al. A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc. Natl Acad. Sci. USA 106, 20240–20245 (2009).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yeeles, J. T. P., Deegan, T. D., Janska, A., Early, A. & Diffley, J. F. X. Regulated eukaryotic DNA replication origin firing with purified proteins. Nature 519, 431–435 (2015).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fernández-Cid, A. et al. An ORC/Cdc6/MCM2–7 complex is formed in a multistep reaction to serve as a platform for MCM double-hexamer assembly. Mol. Cell 50, 577–588 (2013).

    Article 
    PubMed 

    Google Scholar
     

  • Reusswig, K. et al. Unscheduled DNA replication in G1 causes genome instability and damage signatures indicative of replication collisions. Nat. Commun. 13, 7014 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lawrence, M. et al. Software for computing and annotating genomic ranges. PLoS Comput. Biol. 9, e1003118 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chereji, R. V., Bryson, T. D. & Henikoff, S. Quantitative MNase-seq accurately maps nucleosome occupancy levels. Genome Biol. 20, 198 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

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