Generation of Remosomes by the SWI/SNF Chromatin Remodeler Family
Language English Country Great Britain, England Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
Grant support
MC_U105178783
Medical Research Council - United Kingdom
PubMed
31578361
PubMed Central
PMC6775096
DOI
10.1038/s41598-019-50572-8
PII: 10.1038/s41598-019-50572-8
Knihovny.cz E-resources
- MeSH
- Adenosine Triphosphate metabolism pharmacology MeSH
- Cell-Free System MeSH
- Chromosomal Proteins, Non-Histone physiology MeSH
- DNA, Bacterial metabolism MeSH
- DNA Footprinting MeSH
- Fungal Proteins physiology MeSH
- Histones genetics metabolism MeSH
- Microscopy, Atomic Force MeSH
- Multiprotein Complexes physiology MeSH
- Nucleosomes physiology ultrastructure MeSH
- Plasmids chemistry MeSH
- RNA-Binding Proteins physiology MeSH
- Recombinant Proteins metabolism MeSH
- Deoxyribonucleases, Type II Site-Specific MeSH
- Chromatin Assembly and Disassembly genetics physiology MeSH
- Saccharomyces cerevisiae metabolism ultrastructure MeSH
- Xenopus laevis genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Adenosine Triphosphate MeSH
- Chromosomal Proteins, Non-Histone MeSH
- DNA, Bacterial MeSH
- Fungal Proteins MeSH
- GGCC-specific type II deoxyribonucleases MeSH Browser
- Histones MeSH
- Multiprotein Complexes MeSH
- Nucleosomes MeSH
- RNA-Binding Proteins MeSH
- Recombinant Proteins MeSH
- Deoxyribonucleases, Type II Site-Specific MeSH
Chromatin remodelers are complexes able to both alter histone-DNA interactions and to mobilize nucleosomes. The mechanism of their action and the conformation of remodeled nucleosomes remain a matter of debates. In this work we compared the type and structure of the products of nucleosome remodeling by SWI/SNF and ACF complexes using high-resolution microscopy combined with novel biochemical approaches. We find that SWI/SNF generates a multitude of nucleosome-like metastable particles termed "remosomes". Restriction enzyme accessibility assay, DNase I footprinting and AFM experiments reveal perturbed histone-DNA interactions within these particles. Electron cryo-microscopy shows that remosomes adopt a variety of different structures with variable irregular DNA path, similar to those described upon RSC remodeling. Remosome DNA accessibility to restriction enzymes is also markedly increased. We suggest that the generation of remosomes is a common feature of the SWI/SNF family remodelers. In contrast, the ACF remodeler, belonging to ISWI family, only produces repositioned nucleosomes and no evidence for particles associated with extra DNA, or perturbed DNA paths was found. The remosome generation by the SWI/SNF type of remodelers may represent a novel mechanism involved in processes where nucleosomal DNA accessibility is required, such as DNA repair or transcription regulation.
Cellule LBMC 46 Allée d'Italie 69007 Lyon France
Izmir Biomedicine and Genome Center Izmir Turkey
MRC Laboratory of Molecular Biology Hills Road Cambridge CB2 2QH UK
Pharmacology Division CSIR IIIM Sanatnagar Srinagar 190005 Jammu and Kashmir India
See more in PubMed
van Holde, K. Chromatin. (Springer-Verlag KG, Berlin, Germany, 1988).
Arents G, Burlingame RW, Wang B-C, Love WE, Moudrianakis EN. The nucleosomal core histone octamer at 3.1 A resolution: A tripartite protein assembly and a left-handed superhelix. Proc. Natl. Acad. Sci. USA. 1991;88:10148–10152. doi: 10.1073/pnas.88.22.10148. PubMed DOI PMC
Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997;389:251–260. doi: 10.1038/38444. PubMed DOI
Dimitrov SI, Russanova VR, Pashev IG. The globular domain of histone H5 is internally located in the 30 nm chromatin fiber: an immunochemical study. Embo J. 1987;6:2387–2392. doi: 10.1002/j.1460-2075.1987.tb02516.x. PubMed DOI PMC
Syed SH, et al. Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome. Proc Natl Acad Sci USA. 2010;107:9620–9625. doi: 10.1073/pnas.1000309107. PubMed DOI PMC
Thoma F, Koller T, Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol. 1979;83:403–427. doi: 10.1083/jcb.83.2.403. PubMed DOI PMC
Makarov VL, Dimitrov SI, Tsaneva IR, Pashev IG. The role of histone H1 and non-structured domains of core histones in maintaining the orientation of nucleosomes within the chromatin fiber. Biochem Biophys Res Commun. 1984;122:1021–1027. doi: 10.1016/0006-291X(84)91193-8. PubMed DOI
Hayes JJ, Hansen JC. Nucleosomes and the chromatin fiber. Curr Opin Genet Dev. 2001;11:124–129. doi: 10.1016/S0959-437X(00)00168-4. PubMed DOI
Stefanovsky V, Dimitrov SI, Russanova VR, Angelov D, Pashev IG. Laser-induced crosslinking of histones to DNA in chromatin and core particles: implications in studying histone-DNA interactions. Nucleic Acids Res. 1989;17:10069–10081. doi: 10.1093/nar/17.23.10069. PubMed DOI PMC
de la Barre AE, Angelov D, Molla A, Dimitrov S. The N-terminus of histone H2B, but not that of histone H3 or its phosphorylation, is essential for chromosome condensation. Embo J. 2001;20:6383–6393. doi: 10.1093/emboj/20.22.6383. PubMed DOI PMC
Scrittori L, et al. pEg2 aurora-A kinase, histone H3 phosphorylation, and chromosome assembly in Xenopus egg extract. J Biol Chem. 2001;276:30002–30010. doi: 10.1074/jbc.M102701200. PubMed DOI
Beato M, Eisfeld K. Transcription factor access to chromatin. Nucleic Acids Research. 1997;25:3559–3563. doi: 10.1093/nar/25.18.3559. PubMed DOI PMC
Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000;403:41–45. doi: 10.1038/47412. PubMed DOI
Boulard M, Bouvet P, Kundu TK, Dimitrov S. Histone variant nucleosomes: structure, function and implication in disease. Subcell Biochem. 2007;41:71–89. PubMed
Becker PB. Nucleosome sliding: facts and fiction. Embo J. 2002;21:4749–4753. doi: 10.1093/emboj/cdf486. PubMed DOI PMC
Clapier CR, Cairns BR. The Biology of Chromatin Remodeling Complexes. Annu. Rev. Biochem. 2009;78:273–304. doi: 10.1146/annurev.biochem.77.062706.153223. PubMed DOI
Peterson CL, Workman JL. Promoter targeting and chromatin remodeling by the SWI/SNF complex. Current Opinion in Genetics & Development. 2000;10:187–192. doi: 10.1016/S0959-437X(00)00068-X. PubMed DOI
Langst G, Becker PB. Nucleosome mobilization and positioning by ISWI-containing chromatin-remodeling factors. J. Cell Science. 2001;114:2561–2568. PubMed
Havas K, Whitehouse I, Owen-Hughes T. ATP-dependent chromatin remodeling activities. Cell Mol Life Sci. 2001;58:673–682. doi: 10.1007/PL00000891. PubMed DOI PMC
Gangaraju VK, Bartholomew B. Mechanisms of ATP dependent chromatin remodeling. Mutat Res. 2007;618:3–17. doi: 10.1016/j.mrfmmm.2006.08.015. PubMed DOI PMC
Langst G, Bonte EJ, Corona DF, Becker PB. Nucleosome movement by CHRAC and ISWI without disruption or trans- displacement of the histone octamer. Cell. 1999;97:843–852. doi: 10.1016/S0092-8674(00)80797-7. PubMed DOI
Côté J, Peterson CL, Workman JL. Perturbation of nucleosome core structure by the SWI/SNF complex persists after its detachement, enhancing subsequent transcription factor binding. Proc. Natl. Acad. Sci. USA. 1998;95:4947–4952. doi: 10.1073/pnas.95.9.4947. PubMed DOI PMC
Lorch Y, Zhang M, Kornberg RD. Histone octamer transfer by a chromatin-remodeling complex. Cell. 1999;96:389–392. doi: 10.1016/S0092-8674(00)80551-6. PubMed DOI
Montel F, et al. RSC remodeling of oligo-nucleosomes: an atomic force microscopy study. Nucleic Acids Research. 2011;39:2571–2579. doi: 10.1093/nar/gkq1254. PubMed DOI PMC
Mizuguchi G, et al. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science. 2004;303:343–348. doi: 10.1126/science.1090701. PubMed DOI
Angelov D, et al. SWI/SNF remodeling and p300-dependent transcription of histone variant H2ABbd nucleosomal arrays. Embo J. 2004;23:3815–3824. doi: 10.1038/sj.emboj.7600400. PubMed DOI PMC
Doyen CM, et al. Dissection of the unusual structural and functional properties of the variant H2A.Bbd nucleosome. EMBO J. 2006;25:4234–4244. doi: 10.1038/sj.emboj.7601310. PubMed DOI PMC
Shukla MS, et al. The docking domain of histone H2A is required for H1 binding and RSC-mediated nucleosome remodeling. Nucleic Acids Research. 2011;39:2559–2570. doi: 10.1093/nar/gkq1174. PubMed DOI PMC
Peterson CL, Herskowitz I. Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription. Cell. 1992;68:573–583. doi: 10.1016/0092-8674(92)90192-F. PubMed DOI
Chai B, Huang J, Cairns BR, Laurent BC. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 2005;19:1656–1661. doi: 10.1101/gad.1273105. PubMed DOI PMC
Batsche E, Yaniv M, Muchardt C. The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nat Struct Mol Biol. 2006;13:22–29. doi: 10.1038/nsmb1030. PubMed DOI
Dror V, Winston F. The Swi/Snf chromatin remodeling complex is required for ribosomal DNA and telomeric silencing in Saccharomyces cerevisiae. Mol Cell Biol. 2004;24:8227–8235. doi: 10.1128/MCB.24.18.8227-8235.2004. PubMed DOI PMC
Smith CL, Horowitz-Scherer R, Flanagan JF, Woodcock CL, Peterson CL. Structural analysis of the yeast SWI/SNF chromatin remodeling complex. Nat Struct Biol. 2003;10:141–145. doi: 10.1038/nsb888. PubMed DOI
Chaban Y, et al. Structure of a RSC-nucleosome complex and insights into chromatin remodeling. Nature Structural & Molecular Biology. 2008;15:1272–1277. doi: 10.1038/nsmb.1524. PubMed DOI PMC
Fyodorov DV, Blower MD, Karpen GH, Kadonaga JT. Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes & Development. 2004;18:170–183. doi: 10.1101/gad.1139604. PubMed DOI PMC
Ito T, Bulger M, Pazin MJ, Kobayashi R, Kadonaga JT. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell. 1997;90:145–155. doi: 10.1016/S0092-8674(00)80321-9. PubMed DOI
Fazzio TG, et al. Widespread collaboration of Isw2 and Sin3-Rpd3 chromatin remodeling complexes in transcriptional repression. Mol Cell Biol. 2001;21:6450–6460. doi: 10.1128/MCB.21.19.6450-6460.2001. PubMed DOI PMC
Lusser A, Urwin DL, Kadonaga JT. Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nature Structural & Molecular Biology. 2005;12:160–166. doi: 10.1038/nsmb884. PubMed DOI
Ito T, Bulger M, Kobayashi R, Kadonaga JT. Drosophila NAP-1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays. Mol Cell Biol. 1996;16:3112–3124. doi: 10.1128/MCB.16.6.3112. PubMed DOI PMC
Yang JG, Madrid TS, Sevastopoulos E, Narlikar GJ. The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing. Nat Struct Mol Biol. 2006;13:1078–1083. doi: 10.1038/nsmb1170. PubMed DOI
Zhang Y, et al. DNA translocation and loop formation mechanism of chromatin remodeling by SWI/SNF and RSC. Mol Cell. 2006;24:559–568. doi: 10.1016/j.molcel.2006.10.025. PubMed DOI PMC
Shukla MS, et al. Remosomes: RSC generated non-mobilized particles with approximately 180 bp DNA loosely associated with the histone octamer. Proc Natl Acad Sci USA. 2010;107:1936–1941. doi: 10.1073/pnas.0904497107. PubMed DOI PMC
Montel F, Fontaine E, St-Jean P, Castelnovo M, Faivre-Moskalenko C. Atomic force microscopy imaging of SWI/SNF action: Mapping the nucleosome remodeling and sliding. Biophysical Journal. 2007;93:566–578. doi: 10.1529/biophysj.107.105569. PubMed DOI PMC
Wu C, Travers A. A ‘one-pot’ assay for the accessibility of DNA in a nucleosome core particle. Nucleic Acids Res. 2004;32:e122. doi: 10.1093/nar/gnh121. PubMed DOI PMC
Zhou CY, et al. The Yeast INO80 Complex Operates as a Tunable DNA Length-Sensitive Switch to Regulate Nucleosome Sliding. Mol Cell. 2018;69:677–688 e679. doi: 10.1016/j.molcel.2018.01.028. PubMed DOI PMC
Angelov D, et al. The histone octamer is invisible when NF-kappaB binds to the nucleosome. J Biol Chem. 2004;279:42374–42382. doi: 10.1074/jbc.M407235200. PubMed DOI
Syed SH, et al. The incorporation of the novel histone variant H2AL2 confers unusual structural and functional properties of the nucleosome. Nucleic Acids Research. 2009;37:4684–4695. doi: 10.1093/nar/gkp473. PubMed DOI PMC
Luger K, Rechsteiner TJ, Richmond TJ. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 1999;119:1–16. PubMed
Duband-Goulet I, Ouararhni K, Hamiche A. Methods for chromatin assembly and remodeling. Methods. 2004;33:12–17. doi: 10.1016/j.ymeth.2003.10.015. PubMed DOI
Mutskov V, et al. Persistent interactions of core histone tails with nucleosomal DNA following acetylation and transcription factor binding. Mol Cell Biol. 1998;18:6293–6304. doi: 10.1128/MCB.18.11.6293. PubMed DOI PMC
Angelov D, et al. Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J. 2006;25:1669–1679. doi: 10.1038/sj.emboj.7601046. PubMed DOI PMC
Dubochet J, et al. Cryo-electron microscopy of vitrified specimens. Q Rev Biophys. 1988;21:129–228. doi: 10.1017/S0033583500004297. PubMed DOI