Nucleosome sliding mechanisms: new twists in a looped history (original) (raw)

• Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F. & Richmond, T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251–260 (1997).
  Article CAS PubMed Google Scholar
• Davey, C.A., Sargent, D.F., Luger, K., Maeder, A.W. & Richmond, T.J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319, 1097–1113 (2002).
  Article CAS PubMed Google Scholar
• Flaus, A., Martin, D.M., Barton, G.J. & Owen-Hughes, T. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res. 34, 2887–2905 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Clapier, C.R. & Cairns, B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273–304 (2009).
  Article CAS PubMed Google Scholar
• Lorch, Y., Zhang, M. & Kornberg, R.D. Histone octamer transfer by a chromatin-remodeling complex. Cell 96, 389–392 (1999).
  Article CAS PubMed Google Scholar
• Bouazoune, K., Miranda, T.B., Jones, P.A. & Kingston, R.E. Analysis of individual remodeled nucleosomes reveals decreased histone-DNA contacts created by hSWI/SNF. Nucleic Acids Res. 37, 5279–5294 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Ulyanova, N.P. & Schnitzler, G.R. Human SWI/SNF generates abundant, structurally altered dinucleosomes on polynucleosomal templates. Mol. Cell Biol. 25, 11156–11170 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Bruno, M. et al. Histone H2A/H2B dimer exchange by ATP-dependent chromatin remodeling activities. Mol. Cell 12, 1599–1606 (2003).
  Article CAS PubMed Google Scholar
• Boeger, H., Griesenbeck, J. & Kornberg, R.D. Nucleosome retention and the stochastic nature of promoter chromatin remodeling for transcription. Cell 133, 716–726 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Patel, A. et al. Decoupling nucleosome recognition from DNA binding dramatically alters the properties of the Chd1 chromatin remodeler. Nucleic Acids Res. 41, 1637–1648 (2013).Chd1 acquired SWI/SNF-like properties when its DBD was substituted for streptavidin, and the remodeler was targeted to nucleosomes through a biotin tag on histones. This result suggested that binding of the remodeler to linker DNA constrains nucleosome mobility and alters the specificity of the reaction.
  Article CAS PubMed Google Scholar
• Hennig, B.P., Bendrin, K., Zhou, Y. & Fischer, T. Chd1 chromatin remodelers maintain nucleosome organization and repress cryptic transcription. EMBO Rep. 13, 997–1003 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Yadon, A.N. et al. Chromatin remodeling around nucleosome-free regions leads to repression of noncoding RNA transcription. Mol. Cell Biol. 30, 5110–5122 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Shim, Y.S. et al. Hrp3 controls nucleosome positioning to suppress non-coding transcription in eu- and heterochromatin. EMBO J. 31, 4375–4387 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Tirosh, I., Sigal, N. & Barkai, N. Widespread remodeling of mid-coding sequence nucleosomes by Isw1. Genome Biol. 11, R49 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Cheung, V. et al. Chromatin- and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol. 6, e277 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Struhl, K. & Segal, E. Determinants of nucleosome positioning. Nat. Struct. Mol. Biol. 20, 267–273 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Wippo, C.J. et al. The RSC chromatin remodelling enzyme has a unique role in directing the accurate positioning of nucleosomes. EMBO J. 30, 1277–1288 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, Z. et al. A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 332, 977–980 (2011).
  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 CAS PubMed PubMed Central Google Scholar
• Pointner, J. et al. CHD1 remodelers regulate nucleosome spacing in vitro and align nucleosomal arrays over gene coding regions in S. pombe. EMBO J. 31, 4388–4403 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Korber, P. & Becker, P.B. Nucleosome dynamics and epigenetic stability. Essays Biochem. 48, 63–74 (2010).
  Article CAS PubMed Google Scholar
• Badis, G. et al. A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol. Cell 32, 878–887 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Fazzio, T.G. & Tsukiyama, T. Chromatin remodeling in vivo: evidence for a nucleosome sliding mechanism. Mol. Cell 12, 1333–1340 (2003).
  Article CAS PubMed Google Scholar
• Whitehouse, I. & Tsukiyama, T. Antagonistic forces that position nucleosomes in vivo. Nat. Struct. Mol. Biol. 13, 633–640 (2006).
  Article CAS PubMed Google Scholar
• Whitehouse, I., Rando, O.J., Delrow, J. & Tsukiyama, T. Chromatin remodelling at promoters suppresses antisense transcription. Nature 450, 1031–1035 (2007).
  Article CAS PubMed Google Scholar
• Liu, N., Peterson, C.L. & Hayes, J.J. SWI/SNF- and RSC-catalyzed nucleosome mobilization requires internal DNA loop translocation within nucleosomes. Mol. Cell Biol. 31, 4165–4175 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Strohner, R. et al. A 'loop recapture' mechanism for ACF-dependent nucleosome remodeling. Nat. Struct. Mol. Biol. 12, 683–690 (2005).
  Article CAS PubMed Google Scholar
• Längst, G. & Becker, P.B. ISWI induces nucleosome sliding on nicked DNA. Mol. Cell 8, 1085–1092 (2001).
  Article PubMed Google Scholar
• Bowman, G.D. Mechanisms of ATP-dependent nucleosome sliding. Curr. Opin. Struct. Biol. 20, 73–81 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, Y. et al. DNA translocation and loop formation mechanism of chromatin remodeling by SWI/SNF and RSC. Mol. Cell 24, 559–568 (2006).
  Article CAS PubMed Google Scholar
• Lia, G. et al. Direct observation of DNA distortion by the RSC complex. Mol. Cell 21, 417–425 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Aoyagi, S. & Hayes, J.J. hSWI/SNF-catalyzed nucleosome sliding does not occur solely via a twist-diffusion mechanism. Mol. Cell Biol. 22, 7484–7490 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Aoyagi, S., Wade, P.A. & Hayes, J.J. Nucleosome sliding induced by the xMi-2 complex does not occur exclusively via a simple twist-diffusion mechanism. J. Biol. Chem. 278, 30562–30568 (2003).
  Article CAS PubMed Google Scholar
• Lorch, Y., Davis, B. & Kornberg, R.D. Chromatin remodeling by DNA bending, not twisting. Proc. Natl. Acad. Sci. USA 102, 1329–1332 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Saha, A., Wittmeyer, J. & Cairns, B.R. Chromatin remodeling by RSC involves ATP-dependent DNA translocation. Genes Dev. 16, 2120–2134 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Fan, H.Y., He, X., Kingston, R.E. & Narlikar, G.J. Distinct strategies to make nucleosomal DNA accessible. Mol. Cell 11, 1311–1322 (2003).
  Article CAS PubMed Google Scholar
• Whitehouse, I., Stockdale, C., Flaus, A., Szczelkun, M.D. & Owen-Hughes, T. Evidence for DNA translocation by the ISWI chromatin-remodeling enzyme. Mol. Cell Biol. 23, 1935–1945 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Zofall, M., Persinger, J., Kassabov, S.R. & Bartholomew, B. Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nat. Struct. Mol. Biol. 13, 339–346 (2006).
  Article CAS PubMed Google Scholar
• Saha, A., Wittmeyer, J. & Cairns, B.R. Chromatin remodeling through directional DNA translocation from an internal nucleosomal site. Nat. Struct. Mol. Biol. 12, 747–755 (2005).
  Article CAS PubMed Google Scholar
• Schwanbeck, R., Xiao, H. & Wu, C. Spatial contacts and nucleosome step movements induced by the NURF chromatin remodeling complex. J. Biol. Chem. 279, 39933–39941 (2004).
  Article CAS PubMed Google Scholar
• Dang, W., Kagalwala, M.N. & Bartholomew, B. Regulation of ISW2 by concerted action of histone H4 tail and extranucleosomal DNA. Mol. Cell Biol. 26, 7388–7396 (2006).
  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
• Havas, K. et al. Generation of superhelical torsion by ATP-dependent chromatin remodeling activities. Cell 103, 1133–1142 (2000).
  Article CAS PubMed Google Scholar
• Richmond, T.J. & Davey, C.A. The structure of DNA in the nucleosome core. Nature 423, 145–150 (2003).
  Article CAS PubMed Google Scholar
• Tan, S. & Davey, C.A. Nucleosome structural studies. Curr. Opin. Struct. Biol. 21, 128–136 (2011).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Mueller-Planitz, F., Klinker, H., Ludwigsen, J. & Becker, P.B. The ATPase domain of ISWI is an autonomous nucleosome remodeling machine. Nat. Struct. Mol. Biol. 20, 82–89 (2013).This quantitative study showed that the ATPase domain of ISWI is an autonomous, rudimentary nucleosome-remodeling machine. It can recognize and remodel nucleosomes, and its ATPase is properly regulated by the nucleosomal substrate.
  Article CAS PubMed Google Scholar
• Clapier, C.R. & Cairns, B.R. Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes. Nature 492, 280–284 (2012).Identified two autoinhibitory modules in the N and C termini of ISWI that regulate the enzyme. These inhibitory structures are released when the remodeler interacts with the histone H4 tail and extranucleosomal DNA.
  Article CAS PubMed PubMed Central Google Scholar
• Clapier, C.R., Langst, G., Corona, D.F., Becker, P.B. & Nightingale, K.P. Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol. Cell Biol. 21, 875–883 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Bouazoune, K. & Kingston, R.E. Chromatin remodeling by the CHD7 protein is impaired by mutations that cause human developmental disorders. Proc. Natl. Acad. Sci. USA 109, 19238–19243 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Hauk, G., McKnight, J.N., Nodelman, I.M. & Bowman, G.D. The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. Mol. Cell 39, 711–723 (2010).This work presented the crystal structure of Chd1 comprising the NTR and ATPase domain and provided evidence that the NTR regulates the enzyme's ATPase activity by occluding its binding site for nucleic acids.
  Article CAS PubMed PubMed Central Google Scholar
• McKnight, J.N., Jenkins, K.R., Nodelman, I.M., Escobar, T. & Bowman, G.D. Extranucleosomal DNA binding directs nucleosome sliding by Chd1. Mol. Cell Biol. 31, 4746–4759 (2011).Sequence-specific DBDs of unrelated proteins could substitute for the DBD of Chd1, a result suggesting that the DBD and ATPase domains can function as independent modules. Notably, the chimeric remodeler shifted nucleosomes towards and onto the corresponding DNA consensus site.
  Article CAS PubMed PubMed Central Google Scholar
• Grüne, T. et al. Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol. Cell 12, 449–460 (2003).
  Article PubMed Google Scholar
• Ryan, D.P., Sundaramoorthy, R., Martin, D., Singh, V. & Owen-Hughes, T. The DNA-binding domain of the Chd1 chromatin-remodelling enzyme contains SANT and SLIDE domains. EMBO J. 30, 2596–2609 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Pinskaya, M., Nair, A., Clynes, D., Morillon, A. & Mellor, J. Nucleosome remodeling and transcriptional repression are distinct functions of Isw1 in Saccharomyces cerevisiae. Mol. Cell Biol. 29, 2419–2430 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Dechassa, M.L. et al. Disparity in the DNA translocase domains of SWI/SNF and ISW2. Nucleic Acids Res. 40, 4412–4421 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Hall, M.A. et al. High-resolution dynamic mapping of histone-DNA interactions in a nucleosome. Nat. Struct. Mol. Biol. 16, 124–129 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Hota, S.K. et al. Nucleosome mobilization by ISW2 requires the concerted action of the ATPase and SLIDE domains. Nat. Struct. Mol. Biol. 20, 222–229 (2013).Showed that interactions of Isw2 with extranucleosomal DNA promote nucleosome mobilization. The authors resolved several nonsimultaneous structural changes within the nucleosome well before its being shifted to a new DNA location.
  Article CAS PubMed PubMed Central Google Scholar
• Deindl, S. et al. ISWI remodelers slide nucleosomes with coordinated multi-base-pair entry steps and single-base-pair exit steps. Cell 152, 442–452 (2013).Single-molecule fluorescence resonance energy transfer experiments revealed the succession of events during nucleosome sliding by ISWI remodelers in unprecedented detail: the remodelers extruded several base pairs of DNA in single-base-pair increments from the nucleosome before adjacent DNA entered from the opposite end.
  Article CAS PubMed PubMed Central Google Scholar
• Ha, T., Kozlov, A.G. & Lohman, T.M. Single-molecule views of protein movement on single-stranded DNA. Annu. Rev. Biophys. 41, 295–319 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Lorch, Y., Maier-Davis, B. & Kornberg, R.D. Mechanism of chromatin remodeling. Proc. Natl. Acad. Sci. USA 107, 3458–3462 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Chaban, Y. et al. Structure of a RSC-nucleosome complex and insights into chromatin remodeling. Nat. Struct. Mol. Biol. 15, 1272–1277 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Böhm, V. et al. Nucleosome accessibility governed by the dimer/tetramer interface. Nucleic Acids Res. 39, 3093–3102 (2011).
  Article PubMed CAS Google Scholar
• Gangaraju, V.K., Prasad, P., Srour, A., Kagalwala, M.N. & Bartholomew, B. Conformational changes associated with template commitment in ATP-dependent chromatin remodeling by ISW2. Mol. Cell 35, 58–69 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Ryan, D.P. & Owen-Hughes, T. Snf2-family proteins: chromatin remodellers for any occasion. Curr. Opin. Chem. Biol. 15, 649–656 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Dang, W. & Bartholomew, B. Domain architecture of the catalytic subunit in the ISW2-nucleosome complex. Mol. Cell Biol. 27, 8306–8317 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Yamada, K. et al. Structure and mechanism of the chromatin remodelling factor ISW1a. Nature 472, 448–453 (2011).
  Article CAS PubMed Google Scholar
• Sen, P. et al. The SnAC domain of SWI/SNF is a histone anchor required for remodeling. Mol. Cell Biol. 33, 360–370 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Patel, A., McKnight, J.N., Genzor, P. & Bowman, G.D. Identification of residues in Chromodomain helicase dna-binding protein 1 (Chd1) required for coupling atp hydrolysis to nucleosome sliding. J. Biol. Chem. 286, 43984–43993 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Lewis, R., Durr, H., Hopfner, K.P. & Michaelis, J. Conformational changes of a Swi2/Snf2 ATPase during its mechano-chemical cycle. Nucleic Acids Res. 36, 1881–1890 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Forne, I., Ludwigsen, J., Imhof, A., Becker, P.B. & Mueller-Planitz, F. Probing the conformation of the ISWI ATPase domain with genetically encoded photoreactive crosslinkers and mass spectrometry. Mol. Cell Proteomics 11, M111 012088 (2012).
  Article PubMed CAS Google Scholar
• Clapier, C.R., Nightingale, K.P. & Becker, P.B. A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI. Nucleic Acids Res. 30, 649–655 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Hamiche, A., Kang, J.G., Dennis, C., Xiao, H. & Wu, C. Histone tails modulate nucleosome mobility and regulate ATP-dependent nucleosome sliding by NURF. Proc. Natl. Acad. Sci. USA 98, 14316–14321 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Fan, H.Y., Trotter, K.W., Archer, T.K. & Kingston, R.E. Swapping function of two chromatin remodeling complexes. Mol. Cell 17, 805–815 (2005).
  Article CAS PubMed Google Scholar
• Eberharter, A. et al. Acf1, the largest subunit of CHRAC, regulates ISWI-induced nucleosome remodelling. EMBO J. 20, 3781–3788 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Eberharter, A., Vetter, I., Ferreira, R. & Becker, P.B. ACF1 improves the effectiveness of nucleosome mobilization by ISWI through PHD-histone contacts. EMBO J. 23, 4029–4039 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Watson, A.A. et al. The PHD and Chromo domains regulate the ATPase activity of the human chromatin remodeler CHD4. J. Mol. Biol. 422, 3–17 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• He, X., Fan, H.Y., Narlikar, G.J. & Kingston, R.E. Human ACF1 alters the remodeling strategy of SNF2h. J. Biol. Chem. 281, 28636–28647 (2006).
  Article CAS PubMed Google Scholar
• Hargreaves, D.C. & Crabtree, G.R. ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res. 21, 396–420 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Sims, H.I., Lane, J.M., Ulyanova, N.P. & Schnitzler, G.R. Human SWI/SNF drives sequence-directed repositioning of nucleosomes on C-myc promoter DNA minicircles. Biochemistry 46, 11377–11388 (2007).
  Article CAS PubMed Google Scholar
• Rippe, K. et al. DNA sequence- and conformation-directed positioning of nucleosomes by chromatin-remodeling complexes. Proc. Natl. Acad. Sci. USA 104, 15635–15640 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• van Vugt, J.J. et al. Multiple aspects of ATP-dependent nucleosome translocation by RSC and Mi-2 are directed by the underlying DNA sequence. PLoS ONE 4, e6345 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Floer, M. et al. A RSC/nucleosome complex determines chromatin architecture and facilitates activator binding. Cell 141, 407–418 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Gangaraju, V.K. & Bartholomew, B. Dependency of ISW1a chromatin remodeling on extranucleosomal DNA. Mol. Cell Biol. 27, 3217–3225 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Kagalwala, M.N., Glaus, B.J., Dang, W., Zofall, M. & Bartholomew, B. Topography of the ISW2-nucleosome complex: insights into nucleosome spacing and chromatin remodeling. EMBO J. 23, 2092–2104 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Zentner, G.E., Tsukiyama, T. & Henikoff, S. ISWI and CHD chromatin remodelers bind promoters but act in gene bodies. PLoS Genet. 9, e1003317 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Dechassa, M.L. et al. SWI/SNF has intrinsic nucleosome disassembly activity that is dependent on adjacent nucleosomes. Mol. Cell 38, 590–602 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Ballaré, C. et al. Nucleosome-driven transcription factor binding and gene regulation. Mol. Cell 49, 67–79 (2013).
  Article PubMed CAS Google Scholar
• Engeholm, M. et al. Nucleosomes can invade DNA territories occupied by their neighbors. Nat. Struct. Mol. Biol. 16, 151–158 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Lorch, Y., Griesenbeck, J., Boeger, H., Maier-Davis, B. & Kornberg, R.D. Selective removal of promoter nucleosomes by the RSC chromatin-remodeling complex. Nat. Struct. Mol. Biol. 18, 881–885 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Racki, L.R. et al. The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes. Nature 462, 1016–1021 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Blosser, T.R., Yang, J.G., Stone, M.D., Narlikar, G.J. & Zhuang, X. Dynamics of nucleosome remodelling by individual ACF complexes. Nature 462, 1022–1027 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Lusser, A., Urwin, D.L. & Kadonaga, J.T. Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat. Struct. Mol. Biol. 12, 160–166 (2005).
  Article CAS PubMed Google Scholar