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Chromatin Remodeling Complexes

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Fundamentals of Chromatin

Abstract

The packaging of chromosomal DNA by nucleosomes not only condenses and organizes the genome but also blocks access of DNA-binding proteins to regulatory DNA elements. However, this process also allows nucleosomes and other chromatin components to actively participate in the regulation of transcription, DNA replication, DNA repair, and other chromosomal processes. To enable dynamic regulation of nucleosomes, cells have evolved a set of specialized chromatin remodeling complexes (termed Remodelers) that use the energy of ATP hydrolysis to slide, destabilize, eject, or edit/restructure nucleosomes. Here, we address many aspects of Remodeler function, including their composition, specialization, mechanisms, and regulation. We also address their roles in embryonic stem cells, differentiation, development, cancer, and human disease syndromes.

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Abbreviations

ARP:

Actin-related protein

ACF:

ATP-utilizing chromatin assembly and remodeling factor

ATRX:

α-Thalassemia X-linked mental retardation

CHARGE:

Coloboma heart defect, atresia choanae, retarded growth and development, genital hypoplasia, ear anomalies/deafness

CHRAC:

Chromatin accessibility complex

DCC:

Dosage compensation complex

DSB:

Double-strand break

EMT:

Epithelial-to-mesenchymal transition

ES:

Embryonic stem

HAT:

Histone acetyltransferase

HDAC:

Histone deacetylase

HR:

Homologous recombination

MRT:

Malignant rhabdoid tumor

NDR:

Nucleosome-depleted region

NHEJ:

Nonhomologous end-joining

NURF:

Nucleosome remodeling factor

PTM:

Posttranslational modification

RNAPI/II/III:

RNA polymerases I, II, or III

RPA:

Replication protein A

TC-NER:

Transcription-coupled nucleotide-excision repair

TSS:

Transcription start site

References

  • Ahel D, Horejsi Z, Wiechens N, Polo SE, Garcia-Wilson E, Ahel I, Flynn H, Skehel M, West SC, Jackson SP, Owen-Hughes T, Boulton SJ (2009) Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325(5945):1240–1243

    PubMed  CAS  Google Scholar 

  • Ahmad K, Henikoff S (2002) Histone H3 variants specify modes of chromatin assembly. Proc Natl Acad Sci USA 99(Suppl 4):16477–16484

    PubMed  CAS  Google Scholar 

  • Aichinger E, Villar CB, Farrona S, Reyes JC, Hennig L, Kohler C (2009) CHD3 proteins and polycomb group proteins antagonistically determine cell identity in Arabidopsis. PLoS Genet 5(8):e1000605

    PubMed  Google Scholar 

  • Aichinger E, Villar CB, Di Mambro R, Sabatini S, Kohler C (2011) The CHD3 chromatin remodeler PICKLE and polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root. Plant Cell 23(3):1047–1060

    PubMed  CAS  Google Scholar 

  • Alen C, Kent NA, Jones HS, O'Sullivan J, Aranda A, Proudfoot NJ (2002) A role for chromatin remodeling in transcriptional termination by RNA polymerase II. Mol Cell 10(6):1441–1452

    PubMed  CAS  Google Scholar 

  • Altaf M, Auger A, Monnet-Saksouk J, Brodeur J, Piquet S, Cramet M, Bouchard N, Lacoste N, Utley RT, Gaudreau L, Cote J (2010) NuA4-dependent acetylation of nucleosomal histones H4 and H2A directly stimulates incorporation of H2A.Z by the SWR1 complex. J Biol Chem 285(21):15966–15977

    PubMed  CAS  Google Scholar 

  • Anindya R, Mari PO, Kristensen U, Kool H, Giglia-Mari G, Mullenders LH, Fousteri M, Vermeulen W, Egly JM, Svejstrup JQ (2010) A ubiquitin-binding domain in Cockayne syndrome B required for transcription-coupled nucleotide excision repair. Mol Cell 38(5):637–648

    PubMed  CAS  Google Scholar 

  • Armache KJ, Garlick JD, Canzio D, Narlikar GJ, Kingston RE (2011) Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 A resolution. Science 334(6058):977–982

    PubMed  CAS  Google Scholar 

  • Armstrong JA, Papoulas O, Daubresse G, Sperling AS, Lis JT, Scott MP, Tamkun JW (2002) The Drosophila BRM complex facilitates global transcription by RNA polymerase II. EMBO J 21(19):5245–5254

    PubMed  CAS  Google Scholar 

  • Asturias FJ, Chung WH, Kornberg RD, Lorch Y (2002) Structural analysis of the RSC chromatin-remodeling complex. Proc Natl Acad Sci USA 99(21):13477–13480

    PubMed  CAS  Google Scholar 

  • Awad S, Ryan D, Prochasson P, Owen-Hughes T, Hassan AH (2010) The Snf2 homolog Fun30 acts as a homodimeric ATP-dependent chromatin-remodeling enzyme. J Biol Chem 285(13):9477–9484

    PubMed  CAS  Google Scholar 

  • Badenhorst P, Voas M, Rebay I, Wu C (2002) Biological functions of the ISWI chromatin remodeling complex NURF. Genes Dev 16(24):3186–3198

    PubMed  CAS  Google Scholar 

  • Bagchi A, Papazoglu C, Wu Y, Capurso D, Brodt M, Francis D, Bredel M, Vogel H, Mills AA (2007) CHD5 is a tumor suppressor at human 1p36. Cell 128(3):459–475

    PubMed  CAS  Google Scholar 

  • Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y, Helms J, Chang CP, Zhao Y, Swigut T, Wysocka J (2010) CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463(7283):958–962

    PubMed  CAS  Google Scholar 

  • Bao Y, Shen X (2007) SnapShot: chromatin remodeling complexes. Cell 129(3):632

    PubMed  CAS  Google Scholar 

  • Batenburg NL, Mitchell TR, Leach DM, Rainbow AJ, Zhu XD (2012) Cockayne Syndrome group B protein interacts with TRF2 and regulates telomere length and stability. Nucleic Acids Res 40(19):9661–9674

    PubMed  CAS  Google Scholar 

  • Beerens N, Hoeijmakers JH, Kanaar R, Vermeulen W, Wyman C (2005) The CSB protein actively wraps DNA. J Biol Chem 280(6):4722–4729

    PubMed  CAS  Google Scholar 

  • Bezhani S, Winter C, Hershman S, Wagner JD, Kennedy JF, Kwon CS, Pfluger J, Su Y, Wagner D (2007) Unique, shared, and redundant roles for the Arabidopsis SWI/SNF chromatin remodeling ATPases BRAHMA and SPLAYED. Plant Cell 19(2):403–416

    PubMed  CAS  Google Scholar 

  • Biswas D, Takahata S, Xin H, Dutta-Biswas R, Yu Y, Formosa T, Stillman DJ (2008) A role for Chd1 and Set2 in negatively regulating DNA replication in Saccharomyces cerevisiae. Genetics 178(2):649–659

    PubMed  CAS  Google Scholar 

  • Blosser TR, Yang JG, Stone MD, Narlikar GJ, Zhuang X (2009) Dynamics of nucleosome remodelling by individual ACF complexes. Nature 462(7276):1022–1027

    PubMed  CAS  Google Scholar 

  • Boeger H, Griesenbeck J, Strattan JS, Kornberg RD (2003) Nucleosomes unfold completely at a transcriptionally active promoter. Mol Cell 11(6):1587–1598

    PubMed  CAS  Google Scholar 

  • Boeger H, Griesenbeck J, Kornberg RD (2008) Nucleosome retention and the stochastic nature of promoter chromatin remodeling for transcription. Cell 133(4):716–726

    PubMed  CAS  Google Scholar 

  • Bonaldi T, Langst G, Strohner R, Becker PB, Bianchi ME (2002) The DNA chaperone HMGB1 facilitates ACF/CHRAC-dependent nucleosome sliding. EMBO J 21(24):6865–6873

    PubMed  CAS  Google Scholar 

  • Bouazoune K, Brehm A (2005) dMi-2 chromatin binding and remodeling activities are regulated by dCK2 phosphorylation. J Biol Chem 280(51):41912–41920

    PubMed  CAS  Google Scholar 

  • Bouazoune K, Kingston RE (2012) Chromatin remodeling by the CHD7 protein is impaired by mutations that cause human developmental disorders. Proc Natl Acad Sci USA 109(47):19238–19243

    PubMed  CAS  Google Scholar 

  • Bouazoune K, Mitterweger A, Langst G, Imhof A, Akhtar A, Becker PB, Brehm A (2002) The dMi-2 chromodomains are DNA binding modules important for ATP-dependent nucleosome mobilization. EMBO J 21(10):2430–2440

    PubMed  CAS  Google Scholar 

  • Bourachot B, Yaniv M, Muchardt C (2003) Growth inhibition by the mammalian SWI-SNF subunit Brm is regulated by acetylation. EMBO J 22(24):6505–6515

    PubMed  CAS  Google Scholar 

  • Bowman GD (2010) Mechanisms of ATP-dependent nucleosome sliding. Curr Opin Struct Biol 20(1):73–81

    PubMed  CAS  Google Scholar 

  • Boyer LA, Latek RR, Peterson CL (2004) The SANT domain: a unique histone-tail-binding module? Nat Rev Mol Cell Biol 5(2):158–163

    PubMed  CAS  Google Scholar 

  • Brehm A, Tufteland KR, Aasland R, Becker PB (2004) The many colours of chromodomains. Bioessays 26(2):133–140

    PubMed  CAS  Google Scholar 

  • Brown SA, Imbalzano AN, Kingston RE (1996) Activator-dependent regulation of transcriptional pausing on nucleosomal templates. Genes Dev 10(12):1479–1490

    PubMed  CAS  Google Scholar 

  • Brzeski J, Jerzmanowski A (2003) Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors. J Biol Chem 278(2):823–828

    PubMed  CAS  Google Scholar 

  • Brzeski J, Podstolski W, Olczak K, Jerzmanowski A (1999) Identification and analysis of the Arabidopsis thaliana BSH gene, a member of the SNF5 gene family. Nucleic Acids Res 27(11):2393–2399

    PubMed  CAS  Google Scholar 

  • Bultman S, Gebuhr T, Yee D, La Mantia C, Nicholson J, Gilliam A, Randazzo F, Metzger D, Chambon P, Crabtree G, Magnuson T (2000) A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol Cell 6(6):1287–1295

    PubMed  CAS  Google Scholar 

  • Bultman SJ, Gebuhr TC, Pan H, Svoboda P, Schultz RM, Magnuson T (2006) Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev 20(13):1744–1754

    PubMed  CAS  Google Scholar 

  • Burgio G, La Rocca G, Sala A, Arancio W, Di Gesu D, Collesano M, Sperling AS, Armstrong JA, van Heeringen SJ, Logie C, Tamkun JW, Corona DF (2008) Genetic identification of a network of factors that functionally interact with the nucleosome remodeling ATPase ISWI. PLoS Genet 4(6):e1000089

    PubMed  Google Scholar 

  • Burrows AE, Smogorzewska A, Elledge SJ (2010) Polybromo-associated BRG1-associated factor components BRD7 and BAF180 are critical regulators of p53 required for induction of replicative senescence. Proc Natl Acad Sci USA 107(32):14280–14285

    PubMed  CAS  Google Scholar 

  • Cai Y, Jin J, Yao T, Gottschalk AJ, Swanson SK, Wu S, Shi Y, Washburn MP, Florens L, Conaway RC, Conaway JW (2007) YY1 functions with INO80 to activate transcription. Nat Struct Mol Biol 14(9):872–874

    PubMed  CAS  Google Scholar 

  • Cairns BR (2007) Chromatin remodeling: insights and intrigue from single-molecule studies. Nat Struct Mol Biol 14(11):989–996

    PubMed  CAS  Google Scholar 

  • Cairns BR (2009) The logic of chromatin architecture and remodelling at promoters. Nature 461(7261):193–198

    PubMed  CAS  Google Scholar 

  • Cairns BR, Erdjument-Bromage H, Tempst P, Winston F, Kornberg RD (1998) Two actin-related proteins are shared functional components of the chromatin-remodeling complexes RSC and SWI/SNF. Mol Cell 2(5):639–651

    PubMed  CAS  Google Scholar 

  • Carey M, Li B, Workman JL (2006) RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation. Mol Cell 24(3):481–487

    PubMed  CAS  Google Scholar 

  • Cavellan E, Asp P, Percipalle P, Farrants AK (2006) The WSTF-SNF2h chromatin remodeling complex interacts with several nuclear proteins in transcription. J Biol Chem 281(24):16264–16271

    PubMed  CAS  Google Scholar 

  • Chaban Y, Ezeokonkwo C, Chung WH, Zhang F, Kornberg RD, Maier-Davis B, Lorch Y, Asturias FJ (2008) Structure of a RSC-nucleosome complex and insights into chromatin remodeling. Nat Struct Mol Biol 15(12):1272–1277

    PubMed  CAS  Google Scholar 

  • Chai B, Huang J, Cairns BR, Laurent BC (2005) Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev 19(14):1656–1661

    PubMed  CAS  Google Scholar 

  • Chambers AL, Ormerod G, Durley SC, Sing TL, Brown GW, Kent NA, Downs JA (2012) The INO80 chromatin remodeling complex prevents polyploidy and maintains normal chromatin structure at centromeres. Genes Dev 26(23):2590–2603

    PubMed  CAS  Google Scholar 

  • Chatterjee N, Sinha D, Lemma-Dechassa M, Tan S, Shogren-Knaak MA, Bartholomew B (2011) Histone H3 tail acetylation modulates ATP-dependent remodeling through multiple mechanisms. Nucleic Acids Res 39(19):8378–8391

    PubMed  CAS  Google Scholar 

  • Chen X, Cui D, Papusha A, Zhang X, Chu CD, Tang J, Chen K, Pan X, Ira G (2012) The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 489(7417):576–580

    PubMed  CAS  Google Scholar 

  • Cherry CM, Matunis EL (2010) Epigenetic regulation of stem cell maintenance in the Drosophila testis via the nucleosome-remodeling factor NURF. Cell Stem Cell 6(6):557–567

    PubMed  CAS  Google Scholar 

  • Chi TH, Wan M, Zhao K, Taniuchi I, Chen L, Littman DR, Crabtree GR (2002) Reciprocal regulation of CD4/CD8 expression by SWI/SNF-like BAF complexes. Nature 418(6894):195–199

    PubMed  CAS  Google Scholar 

  • Chioda M, Vengadasalam S, Kremmer E, Eberharter A, Becker PB (2010) Developmental role for ACF1-containing nucleosome remodellers in chromatin organisation. Development 137(20):3513–3522

    PubMed  CAS  Google Scholar 

  • Choi K, Park C, Lee J, Oh M, Noh B, Lee I (2007) Arabidopsis homologs of components of the SWR1 complex regulate flowering and plant development. Development 134(10):1931–1941

    PubMed  CAS  Google Scholar 

  • Chou DM, Adamson B, Dephoure NE, Tan X, Nottke AC, Hurov KE, Gygi SP, Colaiacovo MP, Elledge SJ (2010) A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc Natl Acad Sci USA 107(43):18475–18480

    PubMed  CAS  Google Scholar 

  • Citterio E, Van Den Boom V, Schnitzler G, Kanaar R, Bonte E, Kingston RE, Hoeijmakers JH, Vermeulen W (2000) ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor. Mol Cell Biol 20(20):7643–7653

    PubMed  CAS  Google Scholar 

  • Clapier CR, Cairns BR (2012) Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes. Nature 492(7428):280–284

    PubMed  CAS  Google Scholar 

  • Clapier CR, Langst G, Corona DF, Becker PB, Nightingale KP (2001) Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol Cell Biol 21(3):875–883

    PubMed  CAS  Google Scholar 

  • Clapier CR, Nightingale KP, Becker PB (2002) A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI. Nucleic Acids Res 30(3):649–655

    PubMed  CAS  Google Scholar 

  • Clausell J, Happel N, Hale TK, Doenecke D, Beato M (2009) Histone H1 subtypes differentially modulate chromatin condensation without preventing ATP-dependent remodeling by SWI/SNF or NURF. PLoS One 4(10):e0007243

    PubMed  Google Scholar 

  • Collins N, Poot RA, Kukimoto I, Garcia-Jimenez C, Dellaire G, Varga-Weisz PD (2002) An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nat Genet 32(4):627–632

    PubMed  CAS  Google Scholar 

  • Corona DF, Clapier CR, Becker PB, Tamkun JW (2002) Modulation of ISWI function by site-specific histone acetylation. EMBO Rep 3(3):242–247

    PubMed  CAS  Google Scholar 

  • Corona DF, Siriaco G, Armstrong JA, Snarskaya N, McClymont SA, Scott MP, Tamkun JW (2007) ISWI regulates higher-order chromatin structure and histone H1 assembly in vivo. PLoS Biol 5(9):e232

    PubMed  Google Scholar 

  • Cosma MP, Tanaka T, Nasmyth K (1999) Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter. Cell 97(3): 299–311

    PubMed  CAS  Google Scholar 

  • Costelloe T, Louge R, Tomimatsu N, Mukherjee B, Martini E, Khadaroo B, Dubois K, Wiegant WW, Thierry A, Burma S, van Attikum H, Llorente B (2012) The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 489(7417):581–584

    PubMed  CAS  Google Scholar 

  • Dang W, Bartholomew B (2007) Domain architecture of the catalytic subunit in the ISW2-nucleosome complex. Mol Cell Biol 27(23):8306–8317

    PubMed  CAS  Google Scholar 

  • Dang W, Kagalwala MN, Bartholomew B (2007) The Dpb4 subunit of ISW2 is anchored to extranucleosomal DNA. J Biol Chem 282(27):19418–19425

    PubMed  CAS  Google Scholar 

  • De La Fuente R, Viveiros MM, Wigglesworth K, Eppig JJ (2004) ATRX, a member of the SNF2 family of helicase/ATPases, is required for chromosome alignment and meiotic spindle organization in metaphase II stage mouse oocytes. Dev Biol 272(1):1–14

    Google Scholar 

  • de la Serna IL, Carlson KA, Imbalzano AN (2001) Mammalian SWI/SNF complexes promote MyoD-mediated muscle differentiation. Nat Genet 27(2):187–190

    PubMed  Google Scholar 

  • de la Serna IL, Ohkawa Y, Berkes CA, Bergstrom DA, Dacwag CS, Tapscott SJ, Imbalzano AN (2005) MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex. Mol Cell Biol 25(10):3997–4009

    PubMed  Google Scholar 

  • Deal RB, Kandasamy MK, McKinney EC, Meagher RB (2005) The nuclear actin-related protein ARP6 is a pleiotropic developmental regulator required for the maintenance of FLOWERING LOCUS C expression and repression of flowering in Arabidopsis. Plant Cell 17(10): 2633–2646

    PubMed  CAS  Google Scholar 

  • Deal RB, Topp CN, McKinney EC, Meagher RB (2007) Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z. Plant Cell 19(1):74–83

    PubMed  CAS  Google Scholar 

  • Dechassa ML, Zhang B, Horowitz-Scherer R, Persinger J, Woodcock CL, Peterson CL, Bartholomew B (2008) Architecture of the SWI/SNF-nucleosome complex. Mol Cell Biol 28(19):6010–6021

    PubMed  CAS  Google Scholar 

  • Dechassa ML, Sabri A, Pondugula S, Kassabov SR, Chatterjee N, Kladde MP, Bartholomew B (2010) SWI/SNF has intrinsic nucleosome disassembly activity that is dependent on adjacent nucleosomes. Mol Cell 38(4):590–602

    PubMed  CAS  Google Scholar 

  • Deindl S, Hwang WL, Hota SK, Blosser TR, Prasad P, Bartholomew B, Zhuang X (2013) ISWI remodelers slide nucleosomes with coordinated multi-base-pair entry steps and single-base-pair exit steps. Cell 152(3):442–452

    PubMed  CAS  Google Scholar 

  • Denslow SA, Wade PA (2007) The human Mi-2/NuRD complex and gene regulation. Oncogene 26(37):5433–5438

    PubMed  CAS  Google Scholar 

  • Deuring R, Fanti L, Armstrong JA, Sarte M, Papoulas O, Prestel M, Daubresse G, Verardo M, Moseley SL, Berloco M, Tsukiyama T, Wu C, Pimpinelli S, Tamkun JW (2000) The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol Cell 5(2):355–365

    PubMed  CAS  Google Scholar 

  • Dimova D, Nackerdien Z, Furgeson S, Eguchi S, Osley MA (1999) A role for transcriptional repressors in targeting the yeast Swi/Snf complex. Mol Cell 4(1):75–83

    PubMed  CAS  Google Scholar 

  • Dion V, Shimada K, Gasser SM (2010) Actin-related proteins in the nucleus: life beyond chromatin remodelers. Curr Opin Cell Biol 22(3):383–391

    PubMed  CAS  Google Scholar 

  • Dorigo B, Schalch T, Bystricky K, Richmond TJ (2003) Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J Mol Biol 327(1):85–96

    PubMed  CAS  Google Scholar 

  • Downs JA, Allard S, Jobin-Robitaille O, Javaheri A, Auger A, Bouchard N, Kron SJ, Jackson SP, Cote J (2004) Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol Cell 16(6):979–990

    PubMed  CAS  Google Scholar 

  • Doyen CM, An W, Angelov D, Bondarenko V, Mietton F, Studitsky VM, Hamiche A, Roeder RG, Bouvet P, Dimitrov S (2006) Mechanism of polymerase II transcription repression by the histone variant macroH2A. Mol Cell Biol 26(3):1156–1164

    PubMed  CAS  Google Scholar 

  • Drane P, Ouararhni K, Depaux A, Shuaib M, Hamiche A (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 24(12):1253–1265

    PubMed  CAS  Google Scholar 

  • Drost J, Mantovani F, Tocco F, Elkon R, Comel A, Holstege H, Kerkhoven R, Jonkers J, Voorhoeve PM, Agami R, Del Sal G (2010) BRD7 is a candidate tumour suppressor gene required for p53 function. Nat Cell Biol 12(4):380–389

    PubMed  CAS  Google Scholar 

  • Durand-Dubief M, Will WR, Petrini E, Theodorou D, Harris RR, Crawford MR, Paszkiewicz K, Krueger F, Correra RM, Vetter AT, Miller JR, Kent NA, Varga-Weisz P (2012) SWI/SNF-like chromatin remodeling factor Fun30 supports point centromere function in S. cerevisiae. PLoS Genet 8(9):e1002974

    PubMed  CAS  Google Scholar 

  • Eapen VV, Sugawara N, Tsabar M, Wu WH, Haber JE (2012) The Saccharomyces cerevisiae chromatin remodeler Fun30 regulates DNA end resection and checkpoint deactivation. Mol Cell Biol 32(22):4727–4740

    PubMed  CAS  Google Scholar 

  • Eberharter A, Vetter I, Ferreira R, Becker PB (2004) ACF1 improves the effectiveness of nucleosome mobilization by ISWI through PHD-histone contacts. EMBO J 23(20):4029–4039

    PubMed  CAS  Google Scholar 

  • Eckey M, Kuphal S, Straub T, Rummele P, Kremmer E, Bosserhoff AK, Becker PB (2012) Nucleosome remodeler SNF2L suppresses cell proliferation and migration and attenuates Wnt signaling. Mol Cell Biol 32(13):2359–2371

    PubMed  CAS  Google Scholar 

  • Ehrensberger AH, Kornberg RD (2011) Isolation of an activator-dependent, promoter-specific chromatin remodeling factor. Proc Natl Acad Sci USA 108(25):10115–10120

    PubMed  CAS  Google Scholar 

  • Elsasser SJ, Huang H, Lewis PW, Chin JW, Allis CD, Patel DJ (2012) DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature 491(7425):560–565

    PubMed  Google Scholar 

  • Emelyanov AV, Vershilova E, Ignatyeva MA, Pokrovsky DK, Lu X, Konev AY, Fyodorov DV (2012) Identification and characterization of ToRC, a novel ISWI-containing ATP-dependent chromatin assembly complex. Genes Dev 26(6):603–614

    PubMed  CAS  Google Scholar 

  • Engelen E, Akinci U, Bryne JC, Hou J, Gontan C, Moen M, Szumska D, Kockx C, van Ijcken W, Dekkers DH, Demmers J, Rijkers EJ, Bhattacharya S, Philipsen S, Pevny LH, Grosveld FG, Rottier RJ, Lenhard B, Poot RA (2011) Sox2 cooperates with Chd7 to regulate genes that are mutated in human syndromes. Nat Genet 43(6):607–611

    PubMed  CAS  Google Scholar 

  • Falbo KB, Alabert C, Katou Y, Wu S, Han J, Wehr T, Xiao J, He X, Zhang Z, Shi Y, Shirahige K, Pasero P, Shen X (2009) Involvement of a chromatin remodeling complex in damage tolerance during DNA replication. Nat Struct Mol Biol 16(11):1167–1172

    PubMed  CAS  Google Scholar 

  • Farrona S, Hurtado L, March-Diaz R, Schmitz RJ, Florencio FJ, Turck F, Amasino RM, Reyes JC (2011) Brahma is required for proper expression of the floral repressor FLC in Arabidopsis. PloS One 6(3):e17997

    PubMed  CAS  Google Scholar 

  • Fasulo B, Deuring R, Murawska M, Gause M, Dorighi KM, Schaaf CA, Dorsett D, Brehm A, Tamkun JW (2012) The Drosophila MI-2 chromatin-remodeling factor regulates higher-order chromatin structure and cohesin dynamics in vivo. PLoS Genet 8(8):e1002878

    PubMed  CAS  Google Scholar 

  • Fazzio TG, Huff JT, Panning B (2008) An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity. Cell 134(1):162–174

    PubMed  CAS  Google Scholar 

  • Ferreira H, Flaus A, Owen-Hughes T (2007a) Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms. J Mol Biol 374(3):563–579

    PubMed  CAS  Google Scholar 

  • Ferreira R, Eberharter A, Bonaldi T, Chioda M, Imhof A, Becker PB (2007b) Site-specific acetylation of ISWI by GCN5. BMC Mol Biol 8:73

    PubMed  Google Scholar 

  • Flanagan JF, Peterson CL (1999) A role for the yeast SWI/SNF complex in DNA replication. Nucleic Acids Res 27(9):2022–2028

    PubMed  CAS  Google Scholar 

  • Flanagan JF, Mi LZ, Chruszcz M, Cymborowski M, Clines KL, Kim Y, Minor W, Rastinejad F, Khorasanizadeh S (2005) Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438(7071):1181–1185

    PubMed  CAS  Google Scholar 

  • Flaus A, Owen-Hughes T (2011) Mechanisms for ATP-dependent chromatin remodelling: the means to the end. FEBS J 278(19):3579–3595

    PubMed  Google Scholar 

  • Flaus A, Martin DM, Barton GJ, Owen-Hughes T (2006) Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res 34(10):2887–2905

    PubMed  CAS  Google Scholar 

  • Flowers S, Nagl NG Jr, Beck GR Jr, Moran E (2009) Antagonistic roles for BRM and BRG1 SWI/SNF complexes in differentiation. J Biol Chem 284(15):10067–10075

    PubMed  CAS  Google Scholar 

  • Forcales SV, Albini S, Giordani L, Malecova B, Cignolo L, Chernov A, Coutinho P, Saccone V, Consalvi S, Williams R, Wang K, Wu Z, Baranovskaya S, Miller A, Dilworth FJ, Puri PL (2012) Signal-dependent incorporation of MyoD-BAF60c into Brg1-based SWI/SNF chromatin-remodelling complex. EMBO J 31(2):301–316

    PubMed  CAS  Google Scholar 

  • Ford J, Odeyale O, Shen CH (2008) Activator-dependent recruitment of SWI/SNF and INO80 during INO1 activation. Biochem Biophys Res Commun 373(4):602–606

    PubMed  CAS  Google Scholar 

  • Fu J, Qin L, He T, Qin J, Hong J, Wong J, Liao L, Xu J (2011) The TWIST/Mi2/NuRD protein complex and its essential role in cancer metastasis. Cell Res 21(2):275–289

    PubMed  CAS  Google Scholar 

  • Fujita N, Jaye DL, Kajita M, Geigerman C, Moreno CS, Wade PA (2003) MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 113(2):207–219

    PubMed  CAS  Google Scholar 

  • Fujita N, Jaye DL, Geigerman C, Akyildiz A, Mooney MR, Boss JM, Wade PA (2004) MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation. Cell 119(1):75–86

    PubMed  CAS  Google Scholar 

  • Fyodorov DV, Blower MD, Karpen GH, Kadonaga JT (2004) Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev 18(2):170–183

    PubMed  CAS  Google Scholar 

  • Gao X, Tate P, Hu P, Tjian R, Skarnes WC, Wang Z (2008) ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. Proc Natl Acad Sci USA 105(18):6656–6661

    PubMed  CAS  Google Scholar 

  • Gaspar-Maia A, Alajem A, Polesso F, Sridharan R, Mason MJ, Heidersbach A, Ramalho-Santos J, McManus MT, Plath K, Meshorer E, Ramalho-Santos M (2009) Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 460(7257):863–868

    PubMed  CAS  Google Scholar 

  • Gelbart ME, Larschan E, Peng S, Park PJ, Kuroda MI (2009) Drosophila MSL complex globally acetylates H4K16 on the male X chromosome for dosage compensation. Nat Struct Mol Biol 16(8):825–832

    PubMed  CAS  Google Scholar 

  • Gendrel AV, Lippman Z, Yordan C, Colot V, Martienssen RA (2002) Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297(5588):1871–1873

    PubMed  CAS  Google Scholar 

  • Geng F, Cao Y, Laurent BC (2001) Essential roles of Snf5p in Snf-Swi chromatin remodeling in vivo. Mol Cell Biol 21(13):4311–4320

    PubMed  CAS  Google Scholar 

  • Gerhold CB, Winkler DD, Lakomek K, Seifert FU, Fenn S, Kessler B, Witte G, Luger K, Hopfner KP (2012) Structure of actin-related protein 8 and its contribution to nucleosome binding. Nucleic Acids Res 40(21):11036–11046

    PubMed  CAS  Google Scholar 

  • Gibbons RJ, Pellagatti A, Garrick D, Wood WG, Malik N, Ayyub H, Langford C, Boultwood J, Wainscoat JS, Higgs DR (2003) Identification of acquired somatic mutations in the gene encoding chromatin-remodeling factor ATRX in the alpha-thalassemia myelodysplasia syndrome (ATMDS). Nat Genet 34(4):446–449

    PubMed  CAS  Google Scholar 

  • Gkikopoulos T, Schofield P, Singh V, Pinskaya M, Mellor J, Smolle M, Workman JL, Barton GJ, Owen-Hughes T (2011a) A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science 333(6050):1758–1760

    PubMed  CAS  Google Scholar 

  • Gkikopoulos T, Singh V, Tsui K, Awad S, Renshaw MJ, Scholfield P, Barton GJ, Nislow C, Tanaka TU, Owen-Hughes T (2011b) The SWI/SNF complex acts to constrain distribution of the centromeric histone variant Cse4. EMBO J 30(10):1919–1927

    PubMed  CAS  Google Scholar 

  • Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, Dewell S, Law M, Guo X, Li X, Wen D, Chapgier A, DeKelver RC, Miller JC, Lee YL, Boydston EA, Holmes MC, Gregory PD, Greally JM, Rafii S, Yang C, Scambler PJ, Garrick D, Gibbons RJ, Higgs DR, Cristea IM, Urnov FD, Zheng D, Allis CD (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140(5):678–691

    PubMed  CAS  Google Scholar 

  • Goldman JA, Garlick JD, Kingston RE (2010) Chromatin remodeling by imitation switch (ISWI) class ATP-dependent remodelers is stimulated by histone variant H2A.Z. J Biol Chem 285(7):4645–4651

    PubMed  CAS  Google Scholar 

  • Goldmark JP, Fazzio TG, Estep PW, Church GM, Tsukiyama T (2000) The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell 103(3):423–433

    PubMed  CAS  Google Scholar 

  • Gong F, Fahy D, Smerdon MJ (2006) Rad4-Rad23 interaction with SWI/SNF links ATP-dependent chromatin remodeling with nucleotide excision repair. Nat Struct Mol Biol 13(10):902–907

    PubMed  CAS  Google Scholar 

  • Goodarzi AA, Kurka T, Jeggo PA (2011) KAP-1 phosphorylation regulates CHD3 nucleosome remodeling during the DNA double-strand break response. Nat Struct Mol Biol 18(7):831–839

    PubMed  CAS  Google Scholar 

  • Gottschalk AJ, Timinszky G, Kong SE, Jin J, Cai Y, Swanson SK, Washburn MP, Florens L, Ladurner AG, Conaway JW, Conaway RC (2009) Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc Natl Acad Sci USA 106(33):13770–13774

    PubMed  CAS  Google Scholar 

  • Gottschalk AJ, Trivedi RD, Conaway JW, Conaway RC (2012) Activation of the SNF2 family ATPase ALC1 by poly(ADP-ribose) in a stable ALC1.PARP1.nucleosome intermediate. J Biol Chem 287(52):43527–43532

    PubMed  CAS  Google Scholar 

  • Grune T, Brzeski J, Eberharter A, Clapier CR, Corona DF, Becker PB, Muller CW (2003) Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol Cell 12(2):449–460

    PubMed  Google Scholar 

  • Gururaj AE, Singh RR, Rayala SK, Holm C, den Hollander P, Zhang H, Balasenthil S, Talukder AH, Landberg G, Kumar R (2006) MTA1, a transcriptional activator of breast cancer amplified sequence 3. Proc Natl Acad Sci USA 103(17):6670–6675

    PubMed  CAS  Google Scholar 

  • Hakimi MA, Bochar DA, Schmiesing JA, Dong Y, Barak OG, Speicher DW, Yokomori K, Shiekhattar R (2002) A chromatin remodelling complex that loads cohesin onto human chromosomes. Nature 418(6901):994–998

    PubMed  CAS  Google Scholar 

  • Hamiche A, Kang JG, Dennis C, Xiao H, Wu C (2001) Histone tails modulate nucleosome mobility and regulate ATP-dependent nucleosome sliding by NURF. Proc Natl Acad Sci USA 98(25):14316–14321

    PubMed  CAS  Google Scholar 

  • Han HJ, Russo J, Kohwi Y, Kohwi-Shigematsu T (2008) SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 452(7184):187–193

    PubMed  CAS  Google Scholar 

  • Hanai K, Furuhashi H, Yamamoto T, Akasaka K, Hirose S (2008) RSF governs silent chromatin formation via histone H2Av replacement. PLoS Genet 4(2):e1000011

    PubMed  Google Scholar 

  • Hang CT, Yang J, Han P, Cheng HL, Shang C, Ashley E, Zhou B, Chang CP (2010) Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature 466(7302):62–67

    PubMed  CAS  Google Scholar 

  • Harada A, Okada S, Konno D, Odawara J, Yoshimi T, Yoshimura S, Kumamaru H, Saiwai H, Tsubota T, Kurumizaka H, Akashi K, Tachibana T, Imbalzano AN, Ohkawa Y (2012) Chd2 interacts with H3.3 to determine myogenic cell fate. EMBO J 31(13):2994–3007

    PubMed  CAS  Google Scholar 

  • Hartlepp KF, Fernandez-Tornero C, Eberharter A, Grune T, Muller CW, Becker PB (2005) The histone fold subunits of Drosophila CHRAC facilitate nucleosome sliding through dynamic DNA interactions. Mol Cell Biol 25(22):9886–9896

    PubMed  CAS  Google Scholar 

  • Hassan AH, Prochasson P, Neely KE, Galasinski SC, Chandy M, Carrozza MJ, Workman JL (2002) Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell 111(3):369–379

    PubMed  CAS  Google Scholar 

  • Hauk G, McKnight JN, Nodelman IM, Bowman GD (2010) The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. Mol Cell 39(5):711–723

    PubMed  CAS  Google Scholar 

  • He X, Fan HY, Narlikar GJ, Kingston RE (2006) Human ACF1 alters the remodeling strategy of SNF2h. J Biol Chem 281(39):28636–28647

    PubMed  CAS  Google Scholar 

  • He X, Fan HY, Garlick JD, Kingston RE (2008) Diverse regulation of SNF2h chromatin remodeling by noncatalytic subunits. Biochemistry 47(27):7025–7033

    PubMed  CAS  Google Scholar 

  • Henderson A, Holloway A, Reeves R, Tremethick DJ (2004) Recruitment of SWI/SNF to the human immunodeficiency virus type 1 promoter. Mol Cell Biol 24(1):389–397

    PubMed  CAS  Google Scholar 

  • Hill DA, Imbalzano AN (2000) Human SWI/SNF nucleosome remodeling activity is partially inhibited by linker histone H1. Biochemistry 39(38):11649–11656

    PubMed  CAS  Google Scholar 

  • Hirochika H, Okamoto H, Kakutani T (2000) Silencing of retrotransposons in arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12(3):357–369

    PubMed  CAS  Google Scholar 

  • Hirschhorn JN, Brown SA, Clark CD, Winston F (1992) Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev 6(12A):2288–2298

    PubMed  CAS  Google Scholar 

  • Ho L, Crabtree GR (2010) Chromatin remodelling during development. Nature 463(7280):474–484

    PubMed  CAS  Google Scholar 

  • Ho L, Jothi R, Ronan JL, Cui K, Zhao K, Crabtree GR (2009a) An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc Natl Acad Sci USA 106(13):5187–5191

    PubMed  CAS  Google Scholar 

  • Ho L, Ronan JL, Wu J, Staahl BT, Chen L, Kuo A, Lessard J, Nesvizhskii AI, Ranish J, Crabtree GR (2009b) An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc Natl Acad Sci USA 106(13):5181–5186

    PubMed  CAS  Google Scholar 

  • Hochheimer A, Zhou S, Zheng S, Holmes MC, Tjian R (2002) TRF2 associates with DREF and directs promoter-selective gene expression in Drosophila. Nature 420(6914):439–445

    PubMed  CAS  Google Scholar 

  • Hogan CJ, Aligianni S, Durand-Dubief M, Persson J, Will WR, Webster J, Wheeler L, Mathews CK, Elderkin S, Oxley D, Ekwall K, Varga-Weisz PD (2010) Fission yeast Iec1-ino80-mediated nucleosome eviction regulates nucleotide and phosphate metabolism. Mol Cell Biol 30(3):657–674

    PubMed  CAS  Google Scholar 

  • Hood RL, Lines MA, Nikkel SM, Schwartzentruber J, Beaulieu C, Nowaczyk MJ, Allanson J, Kim CA, Wieczorek D, Moilanen JS, Lacombe D, Gillessen-Kaesbach G, Whiteford ML, Quaio CR, Gomy I, Bertola DR, Albrecht B, Platzer K, McGillivray G, Zou R, McLeod DR, Chudley AE, Chodirker BN, Marcadier J, Majewski J, Bulman DE, White SM, Boycott KM (2012) Mutations in SRCAP, encoding SNF2-related CREBBP activator protein, cause floating-harbor syndrome. Am J Hum Genet 90(2):308–313

    PubMed  CAS  Google Scholar 

  • Horn PJ, Carruthers LM, Logie C, Hill DA, Solomon MJ, Wade PA, Imbalzano AN, Hansen JC, Peterson CL (2002) Phosphorylation of linker histones regulates ATP-dependent chromatin remodeling enzymes. Nat Struct Biol 9(4):263–267

    PubMed  CAS  Google Scholar 

  • Hsiao PW, Fryer CJ, Trotter KW, Wang W, Archer TK (2003) BAF60a mediates critical interactions between nuclear receptors and the BRG1 chromatin-remodeling complex for transactivation. Mol Cell Biol 23(17):6210–6220

    PubMed  CAS  Google Scholar 

  • Hsu JM, Huang J, Meluh PB, Laurent BC (2003) The yeast RSC chromatin-remodeling complex is required for kinetochore function in chromosome segregation. Mol Cell Biol 23(9):3202–3215

    PubMed  CAS  Google Scholar 

  • Huang J, Laurent BC (2004) A Role for the RSC chromatin remodeler in regulating cohesion of sister chromatid arms. Cell Cycle 3(8):973–975

    PubMed  CAS  Google Scholar 

  • Huang X, Gao X, Diaz-Trelles R, Ruiz-Lozano P, Wang Z (2008) Coronary development is regulated by ATP-dependent SWI/SNF chromatin remodeling component BAF180. Dev Biol 319(2):258–266

    PubMed  CAS  Google Scholar 

  • Hurd EA, Capers PL, Blauwkamp MN, Adams ME, Raphael Y, Poucher HK, Martin DM (2007) Loss of Chd7 function in gene-trapped reporter mice is embryonic lethal and associated with severe defects in multiple developing tissues. Mamm Genome 18(2):94–104

    PubMed  CAS  Google Scholar 

  • Hurd EA, Poucher HK, Cheng K, Raphael Y, Martin DM (2010) The ATP-dependent chromatin remodeling enzyme CHD7 regulates pro-neural gene expression and neurogenesis in the inner ear. Development 137(18):3139–3150

    PubMed  CAS  Google Scholar 

  • Ieda M, Fu JD, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau BG, Srivastava D (2010) Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142(3):375–386

    PubMed  CAS  Google Scholar 

  • Ishihara K, Oshimura M, Nakao M (2006) CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol Cell 23(5):733–742

    PubMed  CAS  Google Scholar 

  • Ivanov AV, Peng H, Yurchenko V, Yap KL, Negorev DG, Schultz DC, Psulkowski E, Fredericks WJ, White DE, Maul GG, Sadofsky MJ, Zhou MM, Rauscher FJ III (2007) PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol Cell 28(5):823–837

    PubMed  CAS  Google Scholar 

  • Iwase S, Xiang B, Ghosh S, Ren T, Lewis PW, Cochrane JC, Allis CD, Picketts DJ, Patel DJ, Li H, Shi Y (2011) ATRX ADD domain links an atypical histone methylation recognition mechanism to human mental-retardation syndrome. Nat Struct Mol Biol 18(7):769–776

    PubMed  CAS  Google Scholar 

  • Jackson EM, Sievert AJ, Gai X, Hakonarson H, Judkins AR, Tooke L, Perin JC, Xie H, Shaikh TH, Biegel JA (2009) Genomic analysis using high-density single nucleotide polymorphism-based oligonucleotide arrays and multiplex ligation-dependent probe amplification provides a comprehensive analysis of INI1/SMARCB1 in malignant rhabdoid tumors. Clin Cancer Res 15(6):1923–1930

    PubMed  CAS  Google Scholar 

  • Jha S, Dutta A (2009) RVB1/RVB2: running rings around molecular biology. Mol Cell 34(5):521–533

    PubMed  CAS  Google Scholar 

  • Jin C, Zang C, Wei G, Cui K, Peng W, Zhao K, Felsenfeld G (2009) H3.3/H2A.Z double variant-containing nucleosomes mark ‘nucleosome-free regions’ of active promoters and other regulatory regions. Nat Genet 41(8):941–945

    PubMed  CAS  Google Scholar 

  • Jonsson ZO, Jha S, Wohlschlegel JA, Dutta A (2004) Rvb1p/Rvb2p recruit Arp5p and assemble a functional Ino80 chromatin remodeling complex. Mol Cell 16(3):465–477

    PubMed  CAS  Google Scholar 

  • Kadam S, Emerson BM (2003) Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol Cell 11(2):377–389

    PubMed  CAS  Google Scholar 

  • Kaji K, Caballero IM, MacLeod R, Nichols J, Wilson VA, Hendrich B (2006) The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat Cell Biol 8(3):285–292

    PubMed  CAS  Google Scholar 

  • Kandasamy MK, McKinney EC, Deal RB, Smith AP, Meagher RB (2009) Arabidopsis actin-related protein ARP5 in multicellular development and DNA repair. Dev Biol 335(1):22–32

    PubMed  CAS  Google Scholar 

  • Kashiwaba S, Kitahashi K, Watanabe T, Onoda F, Ohtsu M, Murakami Y (2010) The mammalian INO80 complex is recruited to DNA damage sites in an ARP8 dependent manner. Biochem Biophys Res Commun 402(4):619–625

    PubMed  CAS  Google Scholar 

  • Kasten M, Szerlong H, Erdjument-Bromage H, Tempst P, Werner M, Cairns BR (2004) Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14. EMBO J 23(6):1348–1359

    PubMed  CAS  Google Scholar 

  • Kazantseva A, Sepp M, Kazantseva J, Sadam H, Pruunsild P, Timmusk T, Neuman T, Palm K (2009) N-terminally truncated BAF57 isoforms contribute to the diversity of SWI/SNF complexes in neurons. J Neurochem 109(3):807–818

    PubMed  CAS  Google Scholar 

  • Kehle J, Beuchle D, Treuheit S, Christen B, Kennison JA, Bienz M, Muller J (1998) dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 282(5395):1897–1900

    PubMed  CAS  Google Scholar 

  • Kim JH, Saraf A, Florens L, Washburn M, Workman JL (2010) Gcn5 regulates the dissociation of SWI/SNF from chromatin by acetylation of Swi2/Snf2. Genes Dev 24(24):2766–2771

    PubMed  CAS  Google Scholar 

  • Kitayama K, Kamo M, Oma Y, Matsuda R, Uchida T, Ikura T, Tashiro S, Ohyama T, Winsor B, Harata M (2009) The human actin-related protein hArp5: nucleo-cytoplasmic shuttling and involvement in DNA repair. Exp Cell Res 315(2):206–217

    PubMed  CAS  Google Scholar 

  • Knizewski L, Ginalski K, Jerzmanowski A (2008) Snf2 proteins in plants: gene silencing and beyond. Trends Plant Sci 13(10):557–565

    PubMed  CAS  Google Scholar 

  • Konev AY, Tribus M, Park SY, Podhraski V, Lim CY, Emelyanov AV, Vershilova E, Pirrotta V, Kadonaga JT, Lusser A, Fyodorov DV (2007) CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science 317(5841):1087–1090

    PubMed  CAS  Google Scholar 

  • Kornberg RD (1974) Chromatin structure: a repeating unit of histones and DNA. Science 184(139):868–871

    PubMed  CAS  Google Scholar 

  • Krasteva V, Buscarlet M, Diaz-Tellez A, Bernard MA, Crabtree GR, Lessard JA (2012) The BAF53a subunit of SWI/SNF-like BAF complexes is essential for hemopoietic stem cell function. Blood 120(24):4720–4732

    PubMed  CAS  Google Scholar 

  • Kukimoto I, Elderkin S, Grimaldi M, Oelgeschlager T, Varga-Weisz PD (2004) The histone-fold protein complex CHRAC-15/17 enhances nucleosome sliding and assembly mediated by ACF. Mol Cell 13(2):265–277

    PubMed  CAS  Google Scholar 

  • Kunert N, Wagner E, Murawska M, Klinker H, Kremmer E, Brehm A (2009) dMec: a novel Mi-2 chromatin remodelling complex involved in transcriptional repression. EMBO J 28(5):533–544

    PubMed  CAS  Google Scholar 

  • Kusch T, Florens L, Macdonald WH, Swanson SK, Glaser RL, Yates JR III, Abmayr SM, Washburn MP, Workman JL (2004) Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306(5704):2084–2087

    PubMed  CAS  Google Scholar 

  • Kwon H, Imbalzano AN, Khavari PA, Kingston RE, Green MR (1994) Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex [see comments]. Nature 370(6489):477–481

    PubMed  CAS  Google Scholar 

  • Kwon SY, Xiao H, Glover BP, Tjian R, Wu C, Badenhorst P (2008) The nucleosome remodeling factor (NURF) regulates genes involved in Drosophila innate immunity. Dev Biol 316(2):538–547

    PubMed  CAS  Google Scholar 

  • Kwon SY, Xiao H, Wu C, Badenhorst P (2009) Alternative splicing of NURF301 generates distinct NURF chromatin remodeling complexes with altered modified histone binding specificities. PLoS Genet 5(7):e1000574

    PubMed  Google Scholar 

  • Lai AY, Wade PA (2011) Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat Rev Cancer 11(8):588–596

    PubMed  CAS  Google Scholar 

  • Lake RJ, Geyko A, Hemashettar G, Zhao Y, Fan HY (2010) UV-induced association of the CSB remodeling protein with chromatin requires ATP-dependent relief of N-terminal autorepression. Mol Cell 37(2):235–246

    PubMed  CAS  Google Scholar 

  • Lake RJ, Basheer A, Fan HY (2011) Reciprocally regulated chromatin association of Cockayne syndrome protein B and p53 protein. J Biol Chem 286(40):34951–34958

    PubMed  CAS  Google Scholar 

  • Lan L, Ui A, Nakajima S, Hatakeyama K, Hoshi M, Watanabe R, Janicki SM, Ogiwara H, Kohno T, Kanno S, Yasui A (2010) The ACF1 complex is required for DNA double-strand break repair in human cells. Mol Cell 40(6):976–987

    PubMed  CAS  Google Scholar 

  • Landry JW, Banerjee S, Taylor B, Aplan PD, Singer A, Wu C (2011) Chromatin remodeling complex NURF regulates thymocyte maturation. Genes Dev 25(3):275–286

    PubMed  CAS  Google Scholar 

  • Larschan E, Bishop EP, Kharchenko PV, Core LJ, Lis JT, Park PJ, Kuroda MI (2011) X chromosome dosage compensation via enhanced transcriptional elongation in Drosophila. Nature 471(7336):115–118

    PubMed  CAS  Google Scholar 

  • Larsen DH, Poinsignon C, Gudjonsson T, Dinant C, Payne MR, Hari FJ, Rendtlew Danielsen JM, Menard P, Sand JC, Stucki M, Lukas C, Bartek J, Andersen JS, Lukas J (2010) The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J Cell Biol 190(5):731–740

    PubMed  CAS  Google Scholar 

  • Law MJ, Lower KM, Voon HP, Hughes JR, Garrick D, Viprakasit V, Mitson M, De Gobbi M, Marra M, Morris A, Abbott A, Wilder SP, Taylor S, Santos GM, Cross J, Ayyub H, Jones S, Ragoussis J, Rhodes D, Dunham I, Higgs DR, Gibbons RJ (2010) ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner. Cell 143(3):367–378

    PubMed  CAS  Google Scholar 

  • Lee K, Kang MJ, Kwon SJ, Kwon YK, Kim KW, Lim JH, Kwon H (2007) Expansion of chromosome territories with chromatin decompaction in BAF53-depleted interphase cells. Mol Biol Cell 18(10):4013–4023

    PubMed  CAS  Google Scholar 

  • Lee HS, Park JH, Kim SJ, Kwon SJ, Kwon J (2010) A cooperative activation loop among SWI/SNF, gamma-H2AX and H3 acetylation for DNA double-strand break repair. EMBO J 29(8):1434–1445

    PubMed  CAS  Google Scholar 

  • Lemon B, Inouye C, King DS, Tjian R (2001) Selectivity of chromatin-remodelling cofactors for ligand-activated transcription. Nature 414(6866):924–928

    PubMed  CAS  Google Scholar 

  • Leschziner AE, Lemon B, Tjian R, Nogales E (2005) Structural studies of the human PBAF chromatin-remodeling complex. Structure (Camb) 13(2):267–275

    CAS  Google Scholar 

  • Leschziner AE, Saha A, Wittmeyer J, Zhang Y, Bustamante C, Cairns BR, Nogales E (2007) Conformational flexibility in the chromatin remodeler RSC observed by electron microscopy and the orthogonal tilt reconstruction method. Proc Natl Acad Sci USA 104(12):4913–4918

    PubMed  CAS  Google Scholar 

  • Lessard J, Wu JI, Ranish JA, Wan M, Winslow MM, Staahl BT, Wu H, Aebersold R, Graef IA, Crabtree GR (2007) An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55(2):201–215

    PubMed  CAS  Google Scholar 

  • Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD (2010) Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc Natl Acad Sci USA 107(32):14075–14080

    PubMed  CAS  Google Scholar 

  • Li J, Santoro R, Koberna K, Grummt I (2005) The chromatin remodeling complex NoRC controls replication timing of rRNA genes. EMBO J 24(1):120–127

    PubMed  Google Scholar 

  • Li J, Langst G, Grummt I (2006) NoRC-dependent nucleosome positioning silences rRNA genes. EMBO J 25(24):5735–5741

    PubMed  CAS  Google Scholar 

  • Li M, Belozerov VE, Cai HN (2010) Modulation of chromatin boundary activities by nucleosome-remodeling activities in Drosophila melanogaster. Mol Cell Biol 30(4):1067–1076

    PubMed  Google Scholar 

  • Li X, Wang S, Li Y, Deng C, Steiner LA, Xiao H, Wu C, Bungert J, Gallagher PG, Felsenfeld G, Qiu Y, Huang S (2011) Chromatin boundaries require functional collaboration between the hSET1 and NURF complexes. Blood 118(5):1386–1394

    PubMed  CAS  Google Scholar 

  • Lickert H, Takeuchi JK, Von Both I, Walls JR, McAuliffe F, Adamson SL, Henkelman RM, Wrana JL, Rossant J, Bruneau BG (2004) Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 432(7013):107–112

    PubMed  CAS  Google Scholar 

  • Linder B, Mentele E, Mansperger K, Straub T, Kremmer E, Rupp RA (2007) CHD4/Mi-2beta activity is required for the positioning of the mesoderm/neuroectoderm boundary in Xenopus. Genes Dev 21(8):973–983

    PubMed  CAS  Google Scholar 

  • Logie C, Peterson CL (1997) Catalytic activity of the yeast SWI/SNF complex on reconstituted nucleosome arrays. EMBO J 16(22):6772–6782

    PubMed  CAS  Google Scholar 

  • Lorch Y, Maier-Davis B, Kornberg RD (2006) Chromatin remodeling by nucleosome disassembly in vitro. Proc Natl Acad Sci USA 103(9):3090–3093

    PubMed  CAS  Google Scholar 

  • Luk E, Ranjan A, Fitzgerald PC, Mizuguchi G, Huang Y, Wei D, Wu C (2010) Stepwise histone replacement by SWR1 requires dual activation with histone H2A.Z and canonical nucleosome. Cell 143(5):725–736

    PubMed  CAS  Google Scholar 

  • Lusser A, Urwin DL, Kadonaga JT (2005) Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat Struct Mol Biol 12(2):160–166

    PubMed  CAS  Google Scholar 

  • Magdinier F, Wolffe AP (2001) Selective association of the methyl-CpG binding protein MBD2 with the silent p14/p16 locus in human neoplasia. Proc Natl Acad Sci USA 98(9):4990–4995

    PubMed  CAS  Google Scholar 

  • Maier VK, Chioda M, Rhodes D, Becker PB (2008) ACF catalyses chromatosome movements in chromatin fibres. EMBO J 27(6):817–826

    PubMed  CAS  Google Scholar 

  • Maltby VE, Martin BJ, Schulze JM, Johnson I, Hentrich T, Sharma A, Kobor MS, Howe L (2012) Histone H3 lysine 36 methylation targets the Isw1b remodeling complex to chromatin. Mol Cell Biol 32(17):3479–3485

    PubMed  CAS  Google Scholar 

  • March-Diaz R, Reyes JC (2009) The beauty of being a variant: H2A.Z and the SWR1 complex in plants. Mol Plant 2(4):565–577

    PubMed  CAS  Google Scholar 

  • March-Diaz R, Garcia-Dominguez M, Lozano-Juste J, Leon J, Florencio FJ, Reyes JC (2008) Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J 53(3):475–487

    PubMed  CAS  Google Scholar 

  • Marfella CG, Imbalzano AN (2007) The Chd family of chromatin remodelers. Mutat Res 618(1–2):30–40

    PubMed  CAS  Google Scholar 

  • Marfella CG, Ohkawa Y, Coles AH, Garlick DS, Jones SN, Imbalzano AN (2006) Mutation of the SNF2 family member Chd2 affects mouse development and survival. J Cell Physiol 209(1):162–171

    PubMed  CAS  Google Scholar 

  • Mathieu EL, Finkernagel F, Murawska M, Scharfe M, Jarek M, Brehm A (2012) Recruitment of the ATP-dependent chromatin remodeler dMi-2 to the transcribed region of active heat shock genes. Nucleic Acids Res 40(11):4879–4891

    PubMed  CAS  Google Scholar 

  • Mazumdar A, Wang RA, Mishra SK, Adam L, Bagheri-Yarmand R, Mandal M, Vadlamudi RK, Kumar R (2001) Transcriptional repression of oestrogen receptor by metastasis-associated protein 1 corepressor. Nat Cell Biol 3(1):30–37

    PubMed  CAS  Google Scholar 

  • McConnell AD, Gelbart ME, Tsukiyama T (2004) Histone fold protein Dls1p is required for Isw2-dependent chromatin remodeling in vivo. Mol Cell Biol 24(7):2605–2613

    PubMed  CAS  Google Scholar 

  • McDowell TL, Gibbons RJ, Sutherland H, O'Rourke DM, Bickmore WA, Pombo A, Turley H, Gatter K, Picketts DJ, Buckle VJ, Chapman L, Rhodes D, Higgs DR (1999) Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes. Proc Natl Acad Sci USA 96(24):13983–13988

    PubMed  CAS  Google Scholar 

  • McKnight JN, Jenkins KR, Nodelman IM, Escobar T, Bowman GD (2011) Extranucleosomal DNA binding directs nucleosome sliding by Chd1. Mol Cell Biol 31(23):4746–4759

    PubMed  CAS  Google Scholar 

  • Menon T, Yates JA, Bochar DA (2010) Regulation of androgen-responsive transcription by the chromatin remodeling factor CHD8. Mol Endocrinol 24(6):1165–1174

    PubMed  CAS  Google Scholar 

  • Mizuguchi G, Shen X, Landry J, Wu WH, Sen S, Wu C (2004) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303(5656):343–348

    PubMed  CAS  Google Scholar 

  • Moreau JL, Lee M, Mahachi N, Vary J, Mellor J, Tsukiyama T, Goding CR (2003) Regulated displacement of TBP from the PHO8 promoter in vivo requires Cbf1 and the Isw1 chromatin remodeling complex. Mol Cell 11(6):1609–1620

    PubMed  CAS  Google Scholar 

  • Morettini S, Tribus M, Zeilner A, Sebald J, Campo-Fernandez B, Scheran G, Worle H, Podhraski V, Fyodorov DV, Lusser A (2011) The chromodomains of CHD1 are critical for enzymatic activity but less important for chromatin localization. Nucleic Acids Res 39(8):3103–3115

    PubMed  CAS  Google Scholar 

  • Morillon A, Karabetsou N, O'Sullivan J, Kent N, Proudfoot N, Mellor J (2003) Isw1 chromatin remodeling ATPase coordinates transcription elongation and termination by RNA polymerase II. Cell 115(4):425–435

    PubMed  CAS  Google Scholar 

  • Morrison AJ, Highland J, Krogan NJ, Arbel-Eden A, Greenblatt JF, Haber JE, Shen X (2004) INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119(6):767–775

    PubMed  CAS  Google Scholar 

  • Morrison AJ, Kim JA, Person MD, Highland J, Xiao J, Wehr TS, Hensley S, Bao Y, Shen J, Collins SR, Weissman JS, Delrow J, Krogan NJ, Haber JE, Shen X (2007) Mec1/Tel1 phosphorylation of the INO80 chromatin remodeling complex influences DNA damage checkpoint responses. Cell 130(3):499–511

    PubMed  CAS  Google Scholar 

  • Moshkin YM, Mohrmann L, van Ijcken WF, Verrijzer CP (2007) Functional differentiation of SWI/SNF remodelers in transcription and cell cycle control. Mol Cell Biol 27(2):651–661

    PubMed  CAS  Google Scholar 

  • Muchardt C, Reyes JC, Bourachot B, Leguoy E, Yaniv M (1996) The hbrm and BRG-1 proteins, components of the human SNF/SWI complex, are phosphorylated and excluded from the condensed chromosomes during mitosis. EMBO J 15(13):3394–3402

    PubMed  CAS  Google Scholar 

  • Mueller-Planitz F, Klinker H, Ludwigsen J, Becker PB (2013) The ATPase domain of ISWI is an autonomous nucleosome remodeling machine. Nat Struct Mol Biol 20(1):82–89

    PubMed  CAS  Google Scholar 

  • Murawska M, Kunert N, van Vugt J, Langst G, Kremmer E, Logie C, Brehm A (2008) dCHD3, a novel ATP-dependent chromatin remodeler associated with sites of active transcription. Mol Cell Biol 28(8):2745–2757

    PubMed  CAS  Google Scholar 

  • Murawska M, Hassler M, Renkawitz-Pohl R, Ladurner A, Brehm A (2011) Stress-induced PARP activation mediates recruitment of Drosophila Mi-2 to promote heat shock gene expression. PLoS Genet 7(7):e1002206

    PubMed  CAS  Google Scholar 

  • Murawsky CM, Brehm A, Badenhorst P, Lowe N, Becker PB, Travers AA (2001) Tramtrack69 interacts with the dMi-2 subunit of the Drosophila NuRD chromatin remodelling complex. EMBO Rep 2(12):1089–1094

    PubMed  CAS  Google Scholar 

  • Musselman CA, Ramirez J, Sims JK, Mansfield RE, Oliver SS, Denu JM, Mackay JP, Wade PA, Hagman J, Kutateladze TG (2012) Bivalent recognition of nucleosomes by the tandem PHD fingers of the CHD4 ATPase is required for CHD4-mediated repression. Proc Natl Acad Sci USA 109(3):787–792

    PubMed  CAS  Google Scholar 

  • Nagaich AK, Walker DA, Wolford R, Hager GL (2004) Rapid periodic binding and displacement of the glucocorticoid receptor during chromatin remodeling. Mol Cell 14(2):163–174

    PubMed  CAS  Google Scholar 

  • Nagarajan P, Onami TM, Rajagopalan S, Kania S, Donnell R, Venkatachalam S (2009) Role of chromodomain helicase DNA-binding protein 2 in DNA damage response signaling and tumorigenesis. Oncogene 28(8):1053–1062

    PubMed  CAS  Google Scholar 

  • Nair SS, Li DQ, Kumar R (2013) A core chromatin remodeling factor instructs global chromatin signaling through multivalent reading of nucleosome codes. Mol Cell 49(4):704–718

    PubMed  CAS  Google Scholar 

  • Nakayama T, Shimojima T, Hirose S (2012) The PBAP remodeling complex is required for histone H3.3 replacement at chromatin boundaries and for boundary functions. Development 139(24): 4582–4590

    PubMed  CAS  Google Scholar 

  • Natarajan K, Jackson BM, Zhou H, Winston F, Hinnebusch AG (1999) Transcriptional activation by Gcn4p involves independent interactions with the SWI/SNF complex and the SRB/mediator. Mol Cell 4(4):657–664

    PubMed  CAS  Google Scholar 

  • Neumann FR, Dion V, Gehlen LR, Tsai-Pflugfelder M, Schmid R, Taddei A, Gasser SM (2012) Targeted INO80 enhances subnuclear chromatin movement and ectopic homologous recombination. Genes Dev 26(4):369–383

    PubMed  CAS  Google Scholar 

  • Neves-Costa A, Will WR, Vetter AT, Miller JR, Varga-Weisz P (2009) The SNF2-family member Fun30 promotes gene silencing in heterochromatic loci. PLoS One 4(12):e8111

    PubMed  Google Scholar 

  • Nishiyama M, Skoultchi AI, Nakayama KI (2012) Histone H1 recruitment by CHD8 is essential for suppression of the Wnt-beta-catenin signaling pathway. Mol Cell Biol 32(2):501–512

    PubMed  CAS  Google Scholar 

  • Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci USA 96(24):13839–13844

    PubMed  CAS  Google Scholar 

  • Ohshiro K, Rayala SK, Wigerup C, Pakala SB, Natha RS, Gururaj AE, Molli PR, Mansson SS, Ramezani A, Hawley RG, Landberg G, Lee NH, Kumar R (2010) Acetylation-dependent oncogenic activity of metastasis-associated protein 1 co-regulator. EMBO Rep 11(9):691–697

    PubMed  CAS  Google Scholar 

  • Okada M, Okawa K, Isobe T, Fukagawa T (2009) CENP-H-containing complex facilitates centromere deposition of CENP-A in cooperation with FACT and CHD1. Mol Biol Cell 20(18):3986–3995

    PubMed  CAS  Google Scholar 

  • Onishi M, Liou GG, Buchberger JR, Walz T, Moazed D (2007) Role of the conserved Sir3-BAH domain in nucleosome binding and silent chromatin assembly. Mol Cell 28(6):1015–1028

    PubMed  CAS  Google Scholar 

  • Papamichos-Chronakis M, Peterson CL (2008) The Ino80 chromatin-remodeling enzyme regulates replisome function and stability. Nat Struct Mol Biol 15(4):338–345

    PubMed  CAS  Google Scholar 

  • Papamichos-Chronakis M, Krebs JE, Peterson CL (2006) Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev 20(17):2437–2449

    PubMed  CAS  Google Scholar 

  • Papamichos-Chronakis M, Watanabe S, Rando OJ, Peterson CL (2011) Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 144(2):200–213

    PubMed  CAS  Google Scholar 

  • Papoulas O, Daubresse G, Armstrong JA, Jin J, Scott MP, Tamkun JW (2001) The HMG-domain protein BAP111 is important for the function of the BRM chromatin-remodeling complex in vivo. Proc Natl Acad Sci USA 98(10):5728–5733

    PubMed  CAS  Google Scholar 

  • Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, Jarmuz A, Canzonetta C, Webster Z, Nesterova T, Cobb BS, Yokomori K, Dillon N, Aragon L, Fisher AG, Merkenschlager M (2008) Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132(3):422–433

    PubMed  CAS  Google Scholar 

  • Parnell TJ, Huff JT, Cairns BR (2008) RSC regulates nucleosome positioning at Pol II genes and density at Pol III genes. EMBO J 27(1):100–110

    PubMed  CAS  Google Scholar 

  • Paul S, Kuo A, Schalch T, Vogel H, Joshua-Tor L, McCombie WR, Gozani O, Hammell M, Mills AA (2013) Chd5 requires PHD-mediated histone 3 binding for tumor suppression. Cell Rep 3(1):92–102

    PubMed  CAS  Google Scholar 

  • Percipalle P, Fomproix N, Cavellan E, Voit R, Reimer G, Kruger T, Thyberg J, Scheer U, Grummt I, Farrants AK (2006) The chromatin remodelling complex WSTF-SNF2h interacts with nuclear myosin 1 and has a role in RNA polymerase I transcription. EMBO Rep 7(5):525–530

    PubMed  CAS  Google Scholar 

  • Perpelescu M, Nozaki N, Obuse C, Yang H, Yoda K (2009) Active establishment of centromeric CENP-A chromatin by RSF complex. J Cell Biol 185(3):397–407

    PubMed  CAS  Google Scholar 

  • Pinskaya M, Nair A, Clynes D, Morillon A, Mellor J (2009) Nucleosome remodeling and transcriptional repression are distinct functions of Isw1 in Saccharomyces cerevisiae. Mol Cell Biol 29(9):2419–2430

    PubMed  CAS  Google Scholar 

  • Pointner J, Persson J, Prasad P, Norman-Axelsson U, Stralfors A, Khorosjutina O, Krietenstein N, Svensson JP, Ekwall K, Korber P (2012) CHD1 remodelers regulate nucleosome spacing in vitro and align nucleosomal arrays over gene coding regions in S. pombe. EMBO J 31(23):4388–4403

    PubMed  CAS  Google Scholar 

  • Polo SE, Kaidi A, Baskcomb L, Galanty Y, Jackson SP (2010) Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J 29(18):3130–3139

    PubMed  CAS  Google Scholar 

  • Poot RA, Bozhenok L, van den Berg DL, Steffensen S, Ferreira F, Grimaldi M, Gilbert N, Ferreira J, Varga-Weisz PD (2004) The Williams syndrome transcription factor interacts with PCNA to target chromatin remodelling by ISWI to replication foci. Nat Cell Biol 6(12):1236–1244

    PubMed  CAS  Google Scholar 

  • Potts RC, Zhang P, Wurster AL, Precht P, Mughal MR, Wood WH III, Zhang Y, Becker KG, Mattson MP, Pazin MJ (2011) CHD5, a brain-specific paralog of Mi2 chromatin remodeling enzymes, regulates expression of neuronal genes. PLoS One 6(9):e24515

    PubMed  CAS  Google Scholar 

  • Racki LR, Narlikar GJ (2008) ATP-dependent chromatin remodeling enzymes: two heads are not better, just different. Curr Opin Genet Dev 18(2):137–144

    PubMed  CAS  Google Scholar 

  • Racki LR, Yang JG, Naber N, Partensky PD, Acevedo A, Purcell TJ, Cooke R, Cheng Y, Narlikar GJ (2009) The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes. Nature 462(7276):1016–1021

    PubMed  CAS  Google Scholar 

  • Radman-Livaja M, Quan TK, Valenzuela L, Armstrong JA, van Welsem T, Kim T, Lee LJ, Buratowski S, van Leeuwen F, Rando OJ, Hartzog GA (2012) A key role for Chd1 in histone H3 dynamics at the 3' ends of long genes in yeast. PLoS Genet 8(7):e1002811

    PubMed  CAS  Google Scholar 

  • Raisner RM, Hartley PD, Meneghini MD, Bao MZ, Liu CL, Schreiber SL, Rando OJ, Madhani HD (2005) Histone variant H2A.Z marks the 5' ends of both active and inactive genes in euchromatin. Cell 123(2):233–248

    PubMed  CAS  Google Scholar 

  • Ramirez-Carrozzi VR, Nazarian AA, Li CC, Gore SL, Sridharan R, Imbalzano AN, Smale ST (2006) Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response. Genes Dev 20(3):282–296

    PubMed  CAS  Google Scholar 

  • Ratnakumar K, Duarte LF, LeRoy G, Hasson D, Smeets D, Vardabasso C, Bonisch C, Zeng T, Xiang B, Zhang DY, Li H, Wang X, Hake SB, Schermelleh L, Garcia BA, Bernstein E (2012) ATRX-mediated chromatin association of histone variant macroH2A1 regulates alpha-globin expression. Genes Dev 26(5):433–438

    PubMed  CAS  Google Scholar 

  • Rattner BP, Yusufzai T, Kadonaga JT (2009) HMGN proteins act in opposition to ATP-dependent chromatin remodeling factors to restrict nucleosome mobility. Mol Cell 34(5):620–626

    PubMed  CAS  Google Scholar 

  • Rea S, Xouri G, Akhtar A (2007) Males absent on the first (MOF): from flies to humans. Oncogene 26(37):5385–5394

    PubMed  CAS  Google Scholar 

  • Reddy BA, Bajpe PK, Bassett A, Moshkin YM, Kozhevnikova E, Bezstarosti K, Demmers JA, Travers AA, Verrijzer CP (2010) Drosophila transcription factor Tramtrack69 binds MEP1 to recruit the chromatin remodeler NuRD. Mol Cell Biol 30(21):5234–5244

    PubMed  CAS  Google Scholar 

  • Reinke H, Horz W (2003) Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol Cell 11(6):1599–1607

    PubMed  CAS  Google Scholar 

  • Reynolds N, Latos P, Hynes-Allen A, Loos R, Leaford D, O’Shaughnessy A, Mosaku O, Signolet J, Brennecke P, Kalkan T, Costello I, Humphreys P, Mansfield W, Nakagawa K, Strouboulis J, Behrens A, Bertone P, Hendrich B (2012) NuRD suppresses pluripotency gene expression to promote transcriptional heterogeneity and lineage commitment. Cell Stem Cell 10(5):583–594

    PubMed  CAS  Google Scholar 

  • Roberts CW, Orkin SH (2004) The SWI/SNF complex–chromatin and cancer. Nat Rev Cancer 4(2):133–142

    PubMed  CAS  Google Scholar 

  • Rodriguez-Paredes M, Ceballos-Chavez M, Esteller M, Garcia-Dominguez M, Reyes JC (2009) The chromatin remodeling factor CHD8 interacts with elongating RNA polymerase II and controls expression of the cyclin E2 gene. Nucleic Acids Res 37(8):2449–2460

    PubMed  CAS  Google Scholar 

  • Rowbotham SP, Barki L, Neves-Costa A, Santos F, Dean W, Hawkes N, Choudhary P, Will WR, Webster J, Oxley D, Green CM, Varga-Weisz P, Mermoud JE (2011) Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Mol Cell 42(3):285–296

    PubMed  CAS  Google Scholar 

  • Ruthenburg AJ, Li H, Milne TA, Dewell S, McGinty RK, Yuen M, Ueberheide B, Dou Y, Muir TW, Patel DJ, Allis CD (2011) Recognition of a mononucleosomal histone modification pattern by BPTF via multivalent interactions. Cell 145(5):692–706

    PubMed  CAS  Google Scholar 

  • Ryan DP, Sundaramoorthy R, Martin D, Singh V, Owen-Hughes T (2011) The DNA-binding domain of the Chd1 chromatin-remodelling enzyme contains SANT and SLIDE domains. EMBO J 30(13):2596–2609

    PubMed  CAS  Google Scholar 

  • Saeki H, Ohsumi K, Aihara H, Ito T, Hirose S, Ura K, Kaneda Y (2005) Linker histone variants control chromatin dynamics during early embryogenesis. Proc Natl Acad Sci USA 102(16):5697–5702

    PubMed  CAS  Google Scholar 

  • Saha A, Wittmeyer J, Cairns BR (2005) Chromatin remodeling through directional DNA translocation from an internal nucleosomal site. Nat Struct Mol Biol 12(9):747–755

    PubMed  CAS  Google Scholar 

  • Sala A, La Rocca G, Burgio G, Kotova E, Di Gesu D, Collesano M, Ingrassia AM, Tulin AV, Corona DF (2008) The nucleosome-remodeling ATPase ISWI is regulated by poly-ADP-ribosylation. PLoS Biol 6(10):e252

    PubMed  Google Scholar 

  • Sanchez-Molina S, Mortusewicz O, Bieber B, Auer S, Eckey M, Leonhardt H, Friedl AA, Becker PB (2011) Role for hACF1 in the G2/M damage checkpoint. Nucleic Acids Res 39(19):8445–8456

    PubMed  CAS  Google Scholar 

  • Sang Y, Silva-Ortega CO, Wu S, Yamaguchi N, Wu MF, Pfluger J, Gillmor CS, Gallagher KL, Wagner D (2012) Mutations in two non-canonical Arabidopsis SWI2/SNF2 chromatin remodeling ATPases cause embryogenesis and stem cell maintenance defects. Plant J. doi:10.1111/tpj.12009

    PubMed  Google Scholar 

  • Sankar S, Bell R, Stephens B, Zhuo R, Sharma S, Bearss DJ, Lessnick SL (2012) Mechanism and relevance of EWS/FLI-mediated transcriptional repression in Ewing sarcoma. Oncogene. doi:10.1038/onc.2012.525

    PubMed  Google Scholar 

  • Sansom OJ, Berger J, Bishop SM, Hendrich B, Bird A, Clarke AR (2003) Deficiency of Mbd2 suppresses intestinal tumorigenesis. Nat Genet 34(2):145–147

    PubMed  CAS  Google Scholar 

  • Saravanan M, Wuerges J, Bose D, McCormack EA, Cook NJ, Zhang X, Wigley DB (2012) Interactions between the nucleosome histone core and Arp8 in the INO80 chromatin remodeling complex. Proc Natl Acad Sci USA 109(51):20883–20888

    PubMed  CAS  Google Scholar 

  • Schmid A, Fascher KD, Horz W (1992) Nucleosome disruption at the yeast PHO5 promoter upon PHO5 induction occurs in the absence of DNA replication. Cell 71(5):853–864

    PubMed  CAS  Google Scholar 

  • Schnetz MP, Bartels CF, Shastri K, Balasubramanian D, Zentner GE, Balaji R, Zhang X, Song L, Wang Z, Laframboise T, Crawford GE, Scacheri PC (2009) Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res 19(4):590–601

    PubMed  CAS  Google Scholar 

  • Schnetz MP, Handoko L, Akhtar-Zaidi B, Bartels CF, Pereira CF, Fisher AG, Adams DJ, Flicek P, Crawford GE, Laframboise T, Tesar P, Wei CL, Scacheri PC (2010) CHD7 targets active gene enhancer elements to modulate ES cell-specific gene expression. PLoS Genet 6(7):e1001023

    PubMed  Google Scholar 

  • Schubert HL, Wittmeyer J, Kasten MM, Hinata K, Rawling DC, Heroux A, Cairns BR, Hill CP (2013) Structure of an actin-related subcomplex of the SWI/SNF chromatin remodeler. Proc Natl Acad Sci USA 110(9):3345–3350

    PubMed  CAS  Google Scholar 

  • Schultz DC, Friedman JR, Rauscher FJ III (2001) Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2alpha subunit of NuRD. Genes Dev 15(4):428–443

    PubMed  CAS  Google Scholar 

  • Schwabish MA, Struhl K (2004) Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol Cell Biol 24(23):10111–10117

    PubMed  CAS  Google Scholar 

  • Schwertman P, Lagarou A, Dekkers DH, Raams A, van der Hoek AC, Laffeber C, Hoeijmakers JH, Demmers JA, Fousteri M, Vermeulen W, Marteijn JA (2012) UV-sensitive syndrome protein UVSSA recruits USP7 to regulate transcription-coupled repair. Nat Genet 44(5):598–602

    PubMed  CAS  Google Scholar 

  • Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, Moore IK, Wang JP, Widom J (2006) A genomic code for nucleosome positioning. Nature 442(7104):772–778

    PubMed  CAS  Google Scholar 

  • Sen P, Vivas P, Dechassa ML, Mooney AM, Poirier MG, Bartholomew B (2013) The SnAC domain of SWI/SNF is a histone anchor required for remodeling. Mol Cell Biol 33(2):360–370

    PubMed  CAS  Google Scholar 

  • Shain AH, Pollack JR (2013) The spectrum of SWI/SNF mutations, ubiquitous in human cancers. PLoS One 8(1):e55119

    PubMed  Google Scholar 

  • Shen X, Mizuguchi G, Hamiche A, Wu C (2000) A chromatin remodelling complex involved in transcription and DNA processing. Nature 406(6795):541–544

    PubMed  CAS  Google Scholar 

  • Shen X, Ranallo R, Choi E, Wu C (2003) Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol Cell 12(1):147–155

    PubMed  CAS  Google Scholar 

  • Shen H, Powers N, Saini N, Comstock CE, Sharma A, Weaver K, Revelo MP, Gerald W, Williams E, Jessen WJ, Aronow BJ, Rosson G, Weissman B, Muchardt C, Yaniv M, Knudsen KE (2008) The SWI/SNF ATPase Brm is a gatekeeper of proliferative control in prostate cancer. Cancer Res 68(24):10154–10162

    PubMed  CAS  Google Scholar 

  • Shim EY, Hong SJ, Oum JH, Yanez Y, Zhang Y, Lee SE (2007) RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol Cell Biol 27(5):1602–1613

    PubMed  CAS  Google Scholar 

  • Shimada K, Oma Y, Schleker T, Kugou K, Ohta K, Harata M, Gasser SM (2008) Ino80 chromatin remodeling complex promotes recovery of stalled replication forks. Curr Biol 18(8):566–575

    PubMed  CAS  Google Scholar 

  • Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311(5762):844–847

    PubMed  CAS  Google Scholar 

  • Shur I, Solomon R, Benayahu D (2006) Dynamic interactions of chromatin-related mesenchymal modulator, a chromodomain helicase-DNA-binding protein, with promoters in osteoprogenitors. Stem Cells 24(5):1288–1293

    PubMed  CAS  Google Scholar 

  • Siatecka M, Xue L, Bieker JJ (2007) Sumoylation of EKLF promotes transcriptional repression and is involved in inhibition of megakaryopoiesis. Mol Cell Biol 27(24):8547–8560

    PubMed  CAS  Google Scholar 

  • Sif S, Stukenberg PT, Kirschner MW, Kingston RE (1998) Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes Dev 12(18):2842–2851

    PubMed  CAS  Google Scholar 

  • Simic R, Lindstrom DL, Tran HG, Roinick KL, Costa PJ, Johnson AD, Hartzog GA, Arndt KM (2003) Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes. EMBO J 22(8):1846–1856

    PubMed  CAS  Google Scholar 

  • Simon JA, Tamkun JW (2002) Programming off and on states in chromatin: mechanisms of Polycomb and trithorax group complexes. Curr Opin Genet Dev 12(2):210–218

    PubMed  CAS  Google Scholar 

  • Simpson RT (1990) Nucleosome positioning can affect the function of a cis-acting DNA element in vivo. Nature 343(6256):387–389

    PubMed  CAS  Google Scholar 

  • Sims RJ III, Chen CF, Santos-Rosa H, Kouzarides T, Patel SS, Reinberg D (2005) Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J Biol Chem 280(51):41789–41792

    PubMed  CAS  Google Scholar 

  • Sinha M, Watanabe S, Johnson A, Moazed D, Peterson CL (2009) Recombinational repair within heterochromatin requires ATP-dependent chromatin remodeling. Cell 138(6):1109–1121

    PubMed  CAS  Google Scholar 

  • Siriaco G, Deuring R, Chioda M, Becker PB, Tamkun JW (2009) Drosophila ISWI regulates the association of histone H1 with interphase chromosomes in vivo. Genetics 182(3):661–669

    PubMed  CAS  Google Scholar 

  • Sirinakis G, Clapier CR, Gao Y, Viswanathan R, Cairns BR, Zhang Y (2011) The RSC chromatin remodelling ATPase translocates DNA with high force and small step size. EMBO J 30(12):2364–2372

    PubMed  CAS  Google Scholar 

  • Skiniotis G, Moazed D, Walz T (2007) Acetylated histone tail peptides induce structural rearrangements in the RSC chromatin remodeling complex. J Biol Chem 282(29):20804–20808

    PubMed  CAS  Google Scholar 

  • Smolle M, Venkatesh S, Gogol MM, Li H, Zhang Y, Florens L, Washburn MP, Workman JL (2012) Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat Struct Mol Biol 19(9):884–892

    PubMed  CAS  Google Scholar 

  • Soutourina J, Bordas-Le Floch V, Gendrel G, Flores A, Ducrot C, Dumay-Odelot H, Soularue P, Navarro F, Cairns BR, Lefebvre O, Werner M (2006) Rsc4 connects the chromatin remodeler RSC to RNA polymerases. Mol Cell Biol 26(13):4920–4933

    PubMed  CAS  Google Scholar 

  • Srinivasan S, Armstrong JA, Deuring R, Dahlsveen IK, McNeill H, Tamkun JW (2005) The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA Polymerase II. Development 132(7):1623–1635

    PubMed  CAS  Google Scholar 

  • Srinivasan S, Dorighi KM, Tamkun JW (2008) Drosophila Kismet regulates histone H3 lysine 27 methylation and early elongation by RNA polymerase II. PLoS Genet 4(10):e1000217

    PubMed  Google Scholar 

  • Stielow B, Sapetschnig A, Kruger I, Kunert N, Brehm A, Boutros M, Suske G (2008) Identification of SUMO-dependent chromatin-associated transcriptional repression components by a genome-wide RNAi screen. Mol Cell 29(6):742–754

    PubMed  CAS  Google Scholar 

  • Stralfors A, Walfridsson J, Bhuiyan H, Ekwall K (2011) The FUN30 chromatin remodeler, Fft3, protects centromeric and subtelomeric domains from euchromatin formation. PLoS Genet 7(3):e1001334

    PubMed  Google Scholar 

  • Strohner R, Nemeth A, Jansa P, Hofmann-Rohrer U, Santoro R, Langst G, Grummt I (2001) NoRC – a novel member of mammalian ISWI-containing chromatin remodeling machines. EMBO J 20(17):4892–4900

    PubMed  CAS  Google Scholar 

  • Strohner R, Nemeth A, Nightingale KP, Grummt I, Becker PB, Langst G (2004) Recruitment of the nucleolar remodeling complex NoRC establishes ribosomal DNA silencing in chromatin. Mol Cell Biol 24(4):1791–1798

    PubMed  CAS  Google Scholar 

  • Strohner R, Wachsmuth M, Dachauer K, Mazurkiewicz J, Hochstatter J, Rippe K, Langst G (2005) A ‘loop recapture’ mechanism for ACF-dependent nucleosome remodeling. Nat Struct Mol Biol 12(8):683–690

    PubMed  CAS  Google Scholar 

  • Sugiyama T, Cam HP, Sugiyama R, Noma K, Zofall M, Kobayashi R, Grewal SI (2007) SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 128(3):491–504

    PubMed  CAS  Google Scholar 

  • Szerlong H, Saha A, Cairns BR (2003) The nuclear actin-related proteins Arp7 and Arp9: a dimeric module that cooperates with architectural proteins for chromatin remodeling. EMBO J 22(12):3175–3187

    PubMed  CAS  Google Scholar 

  • Szerlong H, Hinata K, Viswanathan R, Erdjument-Bromage H, Tempst P, Cairns BR (2008) The HSA domain binds nuclear actin-related proteins to regulate chromatin-remodeling ATPases. Nat Struct Mol Biol 15(5):469–476

    PubMed  CAS  Google Scholar 

  • Takeuchi JK, Bruneau BG (2009) Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 459(7247):708–711

    PubMed  CAS  Google Scholar 

  • Takeuchi JK, Lickert H, Bisgrove BW, Sun X, Yamamoto M, Chawengsaksophak K, Hamada H, Yost HJ, Rossant J, Bruneau BG (2007) Baf60c is a nuclear Notch signaling component required for the establishment of left-right asymmetry. Proc Natl Acad Sci USA 104(3):846–851

    PubMed  CAS  Google Scholar 

  • Takeuchi JK, Lou X, Alexander JM, Sugizaki H, Delgado-Olguin P, Holloway AK, Mori AD, Wylie JN, Munson C, Zhu Y, Zhou YQ, Yeh RF, Henkelman RM, Harvey RP, Metzger D, Chambon P, Stainier DY, Pollard KS, Scott IC, Bruneau BG (2011) Chromatin remodelling complex dosage modulates transcription factor function in heart development. Nat Commun 2:187

    PubMed  Google Scholar 

  • Tamkun JW, Deuring R, Scott M-P, Kissinger M, Pattatucci AM, Kaufmann TC, Kennison JA (1992) brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68:561–572

    PubMed  CAS  Google Scholar 

  • Tea JS, Luo L (2011) The chromatin remodeling factor Bap55 functions through the TIP60 complex to regulate olfactory projection neuron dendrite targeting. Neural Dev 6:5

    PubMed  CAS  Google Scholar 

  • Thompson BA, Tremblay V, Lin G, Bochar DA (2008) CHD8 is an ATP-dependent chromatin remodeling factor that regulates beta-catenin target genes. Mol Cell Biol 28(12):3894–3904

    PubMed  CAS  Google Scholar 

  • Tirosh I, Sigal N, Barkai N (2010) Widespread remodeling of mid-coding sequence nucleosomes by Isw1. Genome Biol 11(5):R49

    PubMed  Google Scholar 

  • Treand C, du Chene I, Bres V, Kiernan R, Benarous R, Benkirane M, Emiliani S (2006) Requirement for SWI/SNF chromatin-remodeling complex in Tat-mediated activation of the HIV-1 promoter. EMBO J 25(8):1690–1699

    PubMed  CAS  Google Scholar 

  • Tsai WW, Wang Z, Yiu TT, Akdemir KC, Xia W, Winter S, Tsai CY, Shi X, Schwarzer D, Plunkett W, Aronow B, Gozani O, Fischle W, Hung MC, Patel DJ, Barton MC (2010) TRIM24 links a non-canonical histone signature to breast cancer. Nature 468(7326):927–932

    PubMed  CAS  Google Scholar 

  • Tsurusaki Y, Okamoto N, Ohashi H, Kosho T, Imai Y, Hibi-Ko Y, Kaname T, Naritomi K, Kawame H, Wakui K, Fukushima Y, Homma T, Kato M, Hiraki Y, Yamagata T, Yano S, Mizuno S, Sakazume S, Ishii T, Nagai T, Shiina M, Ogata K, Ohta T, Niikawa N, Miyatake S, Okada I, Mizuguchi T, Doi H, Saitsu H, Miyake N, Matsumoto N (2012) Mutations affecting components of the SWI/SNF complex cause Coffin-Siris syndrome. Nat Genet 44(4):376–378

    PubMed  CAS  Google Scholar 

  • van Attikum H, Fritsch O, Hohn B, Gasser SM (2004) Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119(6):777–788

    PubMed  Google Scholar 

  • van Attikum H, Fritsch O, Gasser SM (2007) Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J 26(18):4113–4125

    PubMed  Google Scholar 

  • Van Houdt JK, Nowakowska BA, Sousa SB, van Schaik BD, Seuntjens E, Avonce N, Sifrim A, Abdul-Rahman OA, van den Boogaard MJ, Bottani A, Castori M, Cormier-Daire V, Deardorff MA, Filges I, Fryer A, Fryns JP, Gana S, Garavelli L, Gillessen-Kaesbach G, Hall BD, Horn D, Huylebroeck D, Klapecki J, Krajewska-Walasek M, Kuechler A, Lines MA, Maas S, Macdermot KD, McKee S, Magee A, de Man SA, Moreau Y, Morice-Picard F, Obersztyn E, Pilch J, Rosser E, Shannon N, Stolte-Dijkstra I, Van Dijck P, Vilain C, Vogels A, Wakeling E, Wieczorek D, Wilson L, Zuffardi O, van Kampen AH, Devriendt K, Hennekam R, Vermeesch JR (2012) Heterozygous missense mutations in SMARCA2 cause Nicolaides-Baraitser syndrome. Nat Genet 44(4):445–449, S441

    PubMed  Google Scholar 

  • VanDemark AP, Kasten MM, Ferris E, Heroux A, Hill CP, Cairns BR (2007) Autoregulation of the rsc4 tandem bromodomain by gcn5 acetylation. Mol Cell 27(5):817–828

    PubMed  CAS  Google Scholar 

  • Varela I, Tarpey P, Raine K, Huang D, Ong CK, Stephens P, Davies H, Jones D, Lin ML, Teague J, Bignell G, Butler A, Cho J, Dalgliesh GL, Galappaththige D, Greenman C, Hardy C, Jia M, Latimer C, Lau KW, Marshall J, McLaren S, Menzies A, Mudie L, Stebbings L, Largaespada DA, Wessels LF, Richard S, Kahnoski RJ, Anema J, Tuveson DA, Perez-Mancera PA, Mustonen V, Fischer A, Adams DJ, Rust A, Chan-on W, Subimerb C, Dykema K, Furge K, Campbell PJ, Teh BT, Stratton MR, Futreal PA (2011) Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 469(7331):539–542

    PubMed  CAS  Google Scholar 

  • Varga-Weisz PD, Becker PB (2006) Regulation of higher-order chromatin structures by nucleosome-remodelling factors. Curr Opin Genet Dev 16(2):151–156

    PubMed  CAS  Google Scholar 

  • Verdaasdonk JS, Gardner R, Stephens AD, Yeh E, Bloom K (2012) Tension-dependent nucleosome remodeling at the pericentromere in yeast. Mol Biol Cell 23(13):2560–2570

    PubMed  CAS  Google Scholar 

  • Versteege I, Sevenet N, Lange J, Rousseau-Merck MF, Ambros P, Handgretinger R, Aurias A, Delattre O (1998) Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 394(6689):203–206

    PubMed  CAS  Google Scholar 

  • Vincent JA, Kwong TJ, Tsukiyama T (2008) ATP-dependent chromatin remodeling shapes the DNA replication landscape. Nat Struct Mol Biol 15(5):477–484

    PubMed  CAS  Google Scholar 

  • Vintermist A, Bohm S, Sadeghifar F, Louvet E, Mansen A, Percipalle P, Ostlund Farrants AK (2011) The chromatin remodelling complex B-WICH changes the chromatin structure and recruits histone acetyl-transferases to active rRNA genes. PLoS One 6(4):e19184

    PubMed  CAS  Google Scholar 

  • Vissers LE, van Ravenswaaij CM, Admiraal R, Hurst JA, de Vries BB, Janssen IM, van der Vliet WA, Huys EH, de Jong PJ, Hamel BC, Schoenmakers EF, Brunner HG, Veltman JA, van Kessel AG (2004) Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat Genet 36(9):955–957

    PubMed  CAS  Google Scholar 

  • Walfridsson J, Bjerling P, Thalen M, Yoo EJ, Park SD, Ekwall K (2005) The CHD remodeling factor Hrp1 stimulates CENP-A loading to centromeres. Nucleic Acids Res 33(9):2868–2879

    PubMed  CAS  Google Scholar 

  • Walfridsson J, Khorosjutina O, Matikainen P, Gustafsson CM, Ekwall K (2007) A genome-wide role for CHD remodelling factors and Nap1 in nucleosome disassembly. EMBO J 26(12):2868–2879

    PubMed  CAS  Google Scholar 

  • Wang Z, Zhai W, Richardson JA, Olson EN, Meneses JJ, Firpo MT, Kang C, Skarnes WC, Tjian R (2004) Polybromo protein BAF180 functions in mammalian cardiac chamber maturation. Genes Dev 18(24):3106–3116

    PubMed  CAS  Google Scholar 

  • Wang L, Baiocchi RA, Pal S, Mosialos G, Caligiuri M, Sif S (2005) The BRG1- and hBRM-associated factor BAF57 induces apoptosis by stimulating expression of the cylindromatosis tumor suppressor gene. Mol Cell Biol 25(18):7953–7965

    PubMed  CAS  Google Scholar 

  • Wang X, Sansam CG, Thom CS, Metzger D, Evans JA, Nguyen PT, Roberts CW (2009a) Oncogenesis caused by loss of the SNF5 tumor suppressor is dependent on activity of BRG1, the ATPase of the SWI/SNF chromatin remodeling complex. Cancer Res 69(20):8094–8101

    PubMed  CAS  Google Scholar 

  • Wang Y, Zhang H, Chen Y, Sun Y, Yang F, Yu W, Liang J, Sun L, Yang X, Shi L, Li R, Li Y, Zhang Y, Li Q, Yi X, Shang Y (2009b) LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138(4):660–672

    PubMed  CAS  Google Scholar 

  • Wang Y, Wong RH, Tang T, Hudak CS, Yang D, Duncan RE, Sul HS (2013) Phosphorylation and recruitment of BAF60c in chromatin remodeling for lipogenesis in response to insulin. Mol Cell 49(2):283–297

    PubMed  CAS  Google Scholar 

  • Watson AA, Mahajan P, Mertens HD, Deery MJ, Zhang W, Pham P, Du X, Bartke T, Edlich C, Berridge G, Chen Y, Burgess-Brown NA, Kouzarides T, Wiechens N, Owen-Hughes T, Svergun DI, Gileadi O, Laue ED (2012) The PHD and chromo domains regulate the ATPase activity of the human chromatin remodeler CHD4. J Mol Biol 422(1):3–17

    PubMed  CAS  Google Scholar 

  • Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, Yahata K, Imamoto F, Aburatani H, Nakao M, Imamoto N, Maeshima K, Shirahige K, Peters JM (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451(7180):796–801

    PubMed  CAS  Google Scholar 

  • Whitehouse I, Tsukiyama T (2006) Antagonistic forces that position nucleosomes in vivo. Nat Struct Mol Biol 13(7):633–640

    PubMed  CAS  Google Scholar 

  • Whitehouse I, Rando OJ, Delrow J, Tsukiyama T (2007) Chromatin remodelling at promoters suppresses antisense transcription. Nature 450(7172):1031–1035

    PubMed  CAS  Google Scholar 

  • Whyte WA, Bilodeau S, Orlando DA, Hoke HA, Frampton GM, Foster CT, Cowley SM, Young RA (2012) Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 482(7384):221–225

    PubMed  CAS  Google Scholar 

  • Wilson BG, Roberts CW (2011) SWI/SNF nucleosome remodellers and cancer. Nat Rev Cancer 11(7):481–492

    PubMed  CAS  Google Scholar 

  • Wilson BG, Wang X, Shen X, McKenna ES, Lemieux ME, Cho YJ, Koellhoffer EC, Pomeroy SL, Orkin SH, Roberts CW (2010) Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer CELL 18(4):316–328

    PubMed  CAS  Google Scholar 

  • Winston F, Carlson M (1992) Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet 8(11):387–391

    PubMed  CAS  Google Scholar 

  • Wong LH, McGhie JD, Sim M, Anderson MA, Ahn S, Hannan RD, George AJ, Morgan KA, Mann JR, Choo KH (2010) ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res 20(3):351–360

    PubMed  CAS  Google Scholar 

  • Woudstra EC, Gilbert C, Fellows J, Jansen L, Brouwer J, Erdjument-Bromage H, Tempst P, Svejstrup JQ (2002) A Rad26-Def1 complex coordinates repair and RNA pol II proteolysis in response to DNA damage. Nature 415(6874):929–933

    PubMed  CAS  Google Scholar 

  • Wu WH, Alami S, Luk E, Wu CH, Sen S, Mizuguchi G, Wei D, Wu C (2005) Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange. Nat Struct Mol Biol 12(12):1064–1071

    PubMed  CAS  Google Scholar 

  • Wu JI, Lessard J, Olave IA, Qiu Z, Ghosh A, Graef IA, Crabtree GR (2007a) Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56(1):94–108

    PubMed  CAS  Google Scholar 

  • Wu S, Shi Y, Mulligan P, Gay F, Landry J, Liu H, Lu J, Qi HH, Wang W, Nickoloff JA, Wu C (2007b) A YY1-INO80 complex regulates genomic stability through homologous recombination-based repair. Nat Struct Mol Biol 14(12):1165–1172

    PubMed  CAS  Google Scholar 

  • Wykoff DD, O’Shea EK (2005) Identification of sumoylated proteins by systematic immunoprecipitation of the budding yeast proteome. Mol Cell Proteomics 4(1):73–83

    PubMed  CAS  Google Scholar 

  • Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J, Kauer M, Tackett AJ, Chait BT, Badenhorst P, Wu C, Allis CD (2006) A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442(7098):86–90

    PubMed  CAS  Google Scholar 

  • Xi R, Xie T (2005) Stem cell self-renewal controlled by chromatin remodeling factors. Science 310(5753):1487–1489

    PubMed  CAS  Google Scholar 

  • Xiao H, Sandaltzopoulos R, Wang HM, Hamiche A, Ranallo R, Lee KM, Fu D, Wu C (2001) Dual functions of largest NURF subunit NURF301 in nucleosome sliding and transcription factor interactions. Mol Cell 8(3):531–543

    PubMed  CAS  Google Scholar 

  • Xie W, Ling T, Zhou Y, Feng W, Zhu Q, Stunnenberg HG, Grummt I, Tao W (2012) The chromatin remodeling complex NuRD establishes the poised state of rRNA genes characterized by bivalent histone modifications and altered nucleosome positions. Proc Natl Acad Sci USA 109(21):8161–8166

    PubMed  CAS  Google Scholar 

  • Xu Y, Ayrapetov MK, Xu C, Gursoy-Yuzugullu O, Hu Y, Price BD (2012) Histone H2A.Z controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol Cell 48(5):723–733

    PubMed  CAS  Google Scholar 

  • Xue Y, Gibbons R, Yan Z, Yang D, McDowell TL, Sechi S, Qin J, Zhou S, Higgs D, Wang W (2003) The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc Natl Acad Sci USA 100(19):10635–10640

    PubMed  CAS  Google Scholar 

  • Yadon AN, Van de Mark D, Basom R, Delrow J, Whitehouse I, Tsukiyama T (2010) Chromatin remodeling around nucleosome-free regions leads to repression of noncoding RNA transcription. Mol Cell Biol 30(21):5110–5122

    PubMed  CAS  Google Scholar 

  • Yajima M, Fairbrother WG, Wessel GM (2012) ISWI contributes to ArsI insulator function in development of the sea urchin. Development 139(19):3613–3622

    PubMed  CAS  Google Scholar 

  • Yamada K, Frouws TD, Angst B, Fitzgerald DJ, DeLuca C, Schimmele K, Sargent DF, Richmond TJ (2011) Structure and mechanism of the chromatin remodelling factor ISW1a. Nature 472(7344):448–453

    PubMed  CAS  Google Scholar 

  • Yamane K, Mizuguchi T, Cui B, Zofall M, Noma K, Grewal SI (2011) Asf1/HIRA facilitate global histone deacetylation and associate with HP1 to promote nucleosome occupancy at heterochromatic loci. Mol Cell 41(1):56–66

    PubMed  CAS  Google Scholar 

  • Yamasaki Y, Nishida Y (2006) Mi-2 chromatin remodeling factor functions in sensory organ development through proneural gene repression in Drosophila. Dev Growth Differ 48(7):411–418

    PubMed  CAS  Google Scholar 

  • Yan Z, Cui K, Murray DM, Ling C, Xue Y, Gerstein A, Parsons R, Zhao K, Wang W (2005) PBAF chromatin-remodeling complex requires a novel specificity subunit, BAF200, to regulate expression of selective interferon-responsive genes. Genes Dev 19(14):1662–1667

    PubMed  CAS  Google Scholar 

  • Yan Z, Wang Z, Sharova L, Sharov AA, Ling C, Piao Y, Aiba K, Matoba R, Wang W, Ko MS (2008) BAF250B-associated SWI/SNF chromatin-remodeling complex is required to maintain undifferentiated mouse embryonic stem cells. Stem Cells 26(5):1155–1165

    PubMed  CAS  Google Scholar 

  • Yang X, Zaurin R, Beato M, Peterson CL (2007) Swi3p controls SWI/SNF assembly and ATP-dependent H2A-H2B displacement. Nat Struct Mol Biol 14(6):540–547

    PubMed  CAS  Google Scholar 

  • Yao H, Brick K, Evrard Y, Xiao T, Camerini-Otero RD, Felsenfeld G (2010) Mediation of CTCF transcriptional insulation by DEAD-box RNA-binding protein p68 and steroid receptor RNA activator SRA. Genes Dev 24(22):2543–2555

    PubMed  CAS  Google Scholar 

  • Yasui D, Miyano M, Cai S, Varga-Weisz P, Kohwi-Shigematsu T (2002) SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419(6907):641–645

    PubMed  CAS  Google Scholar 

  • Yates JA, Menon T, Thompson BA, Bochar DA (2010) Regulation of HOXA2 gene expression by the ATP-dependent chromatin remodeling enzyme CHD8. FEBS Lett 584(4):689–693

    PubMed  CAS  Google Scholar 

  • Yen K, Vinayachandran V, Batta K, Koerber RT, Pugh BF (2012) Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell 149(7):1461–1473

    PubMed  CAS  Google Scholar 

  • Yildirim O, Li R, Hung JH, Chen PB, Dong X, Ee LS, Weng Z, Rando OJ, Fazzio TG (2011) Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell 147(7):1498–1510

    PubMed  CAS  Google Scholar 

  • Yokoyama H, Rybina S, Santarella-Mellwig R, Mattaj IW, Karsenti E (2009) ISWI is a RanGTP-dependent MAP required for chromosome segregation. J Cell Biol 187(6):813–829

    PubMed  CAS  Google Scholar 

  • Yoo AS, Staahl BT, Chen L, Crabtree GR (2009) MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460(7255):642–646

    PubMed  CAS  Google Scholar 

  • Yoshida T, Hazan I, Zhang J, Ng SY, Naito T, Snippert HJ, Heller EJ, Qi X, Lawton LN, Williams CJ, Georgopoulos K (2008) The role of the chromatin remodeler Mi-2beta in hematopoietic stem cell self-renewal and multilineage differentiation. Genes Dev 22(9):1174–1189

    PubMed  CAS  Google Scholar 

  • Yoshida T, Shimada K, Oma Y, Kalck V, Akimura K, Taddei A, Iwahashi H, Kugou K, Ohta K, Gasser SM, Harata M (2010) Actin-related protein Arp6 influences H2A.Z-dependent and -independent gene expression and links ribosomal protein genes to nuclear pores. PLoS Genet 6(4):e1000910

    PubMed  Google Scholar 

  • Yoshimura K, Kitagawa H, Fujiki R, Tanabe M, Takezawa S, Takada I, Yamaoka I, Yonezawa M, Kondo T, Furutani Y, Yagi H, Yoshinaga S, Masuda T, Fukuda T, Yamamoto Y, Ebihara K, Li DY, Matsuoka R, Takeuchi JK, Matsumoto T, Kato S (2009) Distinct function of 2 chromatin remodeling complexes that share a common subunit, Williams syndrome transcription factor (WSTF). Proc Natl Acad Sci USA 106(23):9280–9285

    PubMed  CAS  Google Scholar 

  • Yu EY, Steinberg-Neifach O, Dandjinou AT, Kang F, Morrison AJ, Shen X, Lue NF (2007) Regulation of telomere structure and functions by subunits of the INO80 chromatin remodeling complex. Mol Cell Biol 27(16):5639–5649

    PubMed  CAS  Google Scholar 

  • Yuan GC, Liu YJ, Dion MF, Slack MD, Wu LF, Altschuler SJ, Rando OJ (2005) Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309(5734):626–630

    PubMed  CAS  Google Scholar 

  • Yuan X, Feng W, Imhof A, Grummt I, Zhou Y (2007) Activation of RNA polymerase I transcription by cockayne syndrome group B protein and histone methyltransferase G9a. Mol Cell 27(4):585–595

    PubMed  CAS  Google Scholar 

  • Yudkovsky N, Logie C, Hahn S, Peterson CL (1999) Recruitment of the SWI/SNF chromatin remodeling complex by transcriptional activators. Genes Dev 13(18):2369–2374

    PubMed  CAS  Google Scholar 

  • Zemach A, Li Y, Wayburn B, Ben-Meir H, Kiss V, Avivi Y, Kalchenko V, Jacobsen SE, Grafi G (2005) DDM1 binds Arabidopsis methyl-CpG binding domain proteins and affects their subnuclear localization. Plant Cell 17(5):1549–1558

    PubMed  CAS  Google Scholar 

  • Zhang H, Roberts DN, Cairns BR (2005) Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123(2):219–231

    PubMed  CAS  Google Scholar 

  • Zhang H, Stephens LC, Kumar R (2006a) Metastasis tumor antigen family proteins during breast cancer progression and metastasis in a reliable mouse model for human breast cancer. Clin Cancer Res 12(5):1479–1486

    PubMed  CAS  Google Scholar 

  • Zhang Y, Smith CL, Saha A, Grill SW, Mihardja S, Smith SB, Cairns BR, Peterson CL, Bustamante C (2006b) DNA translocation and loop formation mechanism of chromatin remodeling by SWI/SNF and RSC. Mol Cell 24(4):559–568

    PubMed  CAS  Google Scholar 

  • Zhang H, Rider SD Jr, Henderson JT, Fountain M, Chuang K, Kandachar V, Simons A, Edenberg HJ, Romero-Severson J, Muir WM, Ogas J (2008) The CHD3 remodeler PICKLE promotes trimethylation of histone H3 lysine 27. J Biol Chem 283(33):22637–22648

    PubMed  CAS  Google Scholar 

  • Zhang J, Jackson AF, Naito T, Dose M, Seavitt J, Liu F, Heller EJ, Kashiwagi M, Yoshida T, Gounari F, Petrie HT, Georgopoulos K (2012) Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat Immunol 13(1):86–94

    CAS  Google Scholar 

  • Zhao K, Wang W, Rando OJ, Xue Y, Swiderek K, Kuo A, Crabtree GR (1998) Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95(5):625–636

    PubMed  CAS  Google Scholar 

  • Zhou Y, Grummt I (2005) The PHD finger/bromodomain of NoRC interacts with acetylated histone H4K16 and is sufficient for rDNA silencing. Curr Biol 15(15):1434–1438

    PubMed  CAS  Google Scholar 

  • Zhou J, Chau CM, Deng Z, Shiekhattar R, Spindler MP, Schepers A, Lieberman PM (2005) Cell cycle regulation of chromatin at an origin of DNA replication. EMBO J 24(7):1406–1417

    PubMed  CAS  Google Scholar 

  • Zhu Y, Rowley MJ, Bohmdorfer G, Wierzbicki AT (2013) A SWI/SNF chromatin-remodeling complex acts in noncoding rna-mediated transcriptional silencing. Mol Cell 49(2):298–309

    PubMed  CAS  Google Scholar 

  • Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S (2008) Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456(7218):125–129

    PubMed  CAS  Google Scholar 

  • Zofall M, Persinger J, Kassabov SR, Bartholomew B (2006) Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nat Struct Mol Biol 13(4):339–346

    PubMed  CAS  Google Scholar 

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Clapier, C.R., Cairns, B.R. (2014). Chromatin Remodeling Complexes. In: Workman, J., Abmayr, S. (eds) Fundamentals of Chromatin. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8624-4_3

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