Regulating the chromatin landscape: structural and mechanistic perspectives.

A large family of chromatin remodelers that noncovalently modify chromatin is crucial in cell development and differentiation. They are often the targets of cancer, neurological disorders, and other human diseases. These complexes alter nucleosome positioning, higher-order chromatin structure, and nuclear organization. They also assemble chromatin, exchange out histone variants, and disassemble chromatin at defined locations. We review aspects of the structural organization of these complexes, the functional properties of their protein domains, and variation between complexes. We also address the mechanistic details of these complexes in mobilizing nucleosomes and altering chromatin structure. A better understanding of these issues will be vital for further analyses of subunits of these chromatin remodelers, which are being identified as targets in human diseases by NGS (next-generation sequencing).

[1]  Jeffrey N. McKnight,et al.  Identification of Residues in Chromodomain Helicase DNA-Binding Protein 1 (Chd1) Required for Coupling ATP Hydrolysis to Nucleosome Sliding* , 2011, The Journal of Biological Chemistry.

[2]  H. Szerlong,et al.  Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14 , 2004, The EMBO journal.

[3]  L. Aravind,et al.  The SWIRM domain: a conserved module found in chromosomal proteins points to novel chromatin-modifying activities , 2002, Genome Biology.

[4]  Carlos Bustamante,et al.  DNA translocation and loop formation mechanism of chromatin remodeling by SWI/SNF and RSC. , 2006, Molecular cell.

[5]  G. Goodwin,et al.  The BAH domain, polybromo and the RSC chromatin remodelling complex. , 2001, Gene.

[6]  J Seth Strattan,et al.  Nucleosomes unfold completely at a transcriptionally active promoter. , 2003, Molecular cell.

[7]  Xi He,et al.  Distinct strategies to make nucleosomal DNA accessible. , 2003, Molecular cell.

[8]  Thomas A. Milne,et al.  A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling , 2006, Nature.

[9]  B. Maier-Davis,et al.  Chromatin remodeling by nucleosome disassembly in vitro. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Julia M. Schulze,et al.  Histone H3 Lysine 36 Methylation Targets the Isw1b Remodeling Complex to Chromatin , 2012, Molecular and Cellular Biology.

[11]  T. Richmond,et al.  DNA stretching and extreme kinking in the nucleosome core. , 2007, Journal of molecular biology.

[12]  Ying Gao,et al.  The RSC chromatin remodelling ATPase translocates DNA with high force and small step size , 2011, The EMBO journal.

[13]  C. Obuse,et al.  Active establishment of centromeric CENP-A chromatin by RSF complex , 2009, The Journal of cell biology.

[14]  G. Bowman Mechanisms of ATP-dependent nucleosome sliding. , 2010, Current opinion in structural biology.

[15]  J. Palmer,et al.  Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae. , 1999, Genes & development.

[16]  Anindya Dutta,et al.  RVB1/RVB2: running rings around molecular biology. , 2009, Molecular cell.

[17]  V. Pirrotta,et al.  CHD1 Motor Protein Is Required for Deposition of Histone Variant H3.3 into Chromatin in Vivo , 2007, Science.

[18]  Vijender Singh,et al.  The DNA-binding domain of the Chd1 chromatin-remodelling enzyme contains SANT and SLIDE domains , 2011, The EMBO journal.

[19]  H. Szerlong,et al.  The HSA domain binds nuclear actin-related proteins to regulate chromatin-remodeling ATPases , 2008, Nature Structural &Molecular Biology.

[20]  R. Kingston,et al.  Generation and interconversion of multiple distinct nucleosomal states as a mechanism for catalyzing chromatin fluidity. , 2001, Molecular cell.

[21]  B. Bartholomew,et al.  Domain Architecture of the Catalytic Subunit in the ISW2-Nucleosome Complex , 2007, Molecular and Cellular Biology.

[22]  Peer Bork,et al.  Systematic identification of novel protein domain families associated with nuclear functions. , 2002, Genome research.

[23]  R. Kingston,et al.  Diverse regulation of SNF2h chromatin remodeling by noncatalytic subunits. , 2008, Biochemistry.

[24]  Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin , 2011 .

[25]  R. Kingston,et al.  Interaction of HP1 and Brg1/Brm with the Globular Domain of Histone H3 Is Required for HP1-Mediated Repression , 2009, PLoS genetics.

[26]  C. Kooperberg,et al.  Yeast Isw1p Forms Two Separable Complexes In Vivo , 2003, Molecular and Cellular Biology.

[27]  T. Owen-Hughes,et al.  SWI/SNF and Asf1p Cooperate To Displace Histones during Induction of the Saccharomyces cerevisiae HO Promoter , 2009, Molecular and Cellular Biology.

[28]  Roger D. Kornberg,et al.  Nucleosome Retention and the Stochastic Nature of Promoter Chromatin Remodeling for Transcription , 2008, Cell.

[29]  Jeffrey N. McKnight,et al.  The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. , 2010, Molecular cell.

[30]  M. L. Dechassa,et al.  Disparity in the DNA translocase domains of SWI/SNF and ISW2 , 2012, Nucleic acids research.

[31]  C. Peterson,et al.  SWI/SNF- and RSC-Catalyzed Nucleosome Mobilization Requires Internal DNA Loop Translocation within Nucleosomes , 2011, Molecular and Cellular Biology.

[32]  W. Houry,et al.  Chaperone-like activity of the AAA+ proteins Rvb1 and Rvb2 in the assembly of various complexes , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[33]  J. Workman,et al.  Function and Selectivity of Bromodomains in Anchoring Chromatin-Modifying Complexes to Promoter Nucleosomes , 2002, Cell.

[34]  D. Patel,et al.  DAXX envelops a histone H3.3–H4 dimer for H3.3-specific recognition , 2012, Nature.

[35]  T. Richmond,et al.  Structure and mechanism of the chromatin remodelling factor ISW1a , 2011, Nature.

[36]  D. Dunlap,et al.  Direct observation of DNA distortion by the RSC complex. , 2006, Molecular cell.

[37]  G. Mizuguchi,et al.  Stepwise Histone Replacement by SWR1 Requires Dual Activation with Histone H2A.Z and Canonical Nucleosome , 2010, Cell.

[38]  William L. Hwang,et al.  ISWI Remodelers Slide Nucleosomes with Coordinated Multi-Base-Pair Entry Steps and Single-Base-Pair Exit Steps , 2013, Cell.

[39]  J. Workman,et al.  Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange , 2012, Nature Structural &Molecular Biology.

[40]  M. Sanchez-Cespedes,et al.  The SWI/SNF genetic blockade: effects in cell differentiation, cancer and developmental diseases , 2014, Oncogene.

[41]  R. Kingston,et al.  Human ACF1 Alters the Remodeling Strategy of SNF2h* , 2006, Journal of Biological Chemistry.

[42]  Pierre Baldi,et al.  The Neuron-specific Chromatin Regulatory Subunit BAF53b is Necessary for Synaptic Plasticity and Memory , 2013, Nature Neuroscience.

[43]  R. Brenk,et al.  Nucleosomes can invade DNA territories occupied by their neighbors , 2009, Nature Structural &Molecular Biology.

[44]  Hua Xiao,et al.  Spatial Contacts and Nucleosome Step Movements Induced by the NURF Chromatin Remodeling Complex* , 2004, Journal of Biological Chemistry.

[45]  S. Rafii,et al.  Distinct Factors Control Histone Variant H3.3 Localization at Specific Genomic Regions , 2010, Cell.

[46]  Andrew Flaus,et al.  Mechanisms for nucleosome mobilization. , 2003, Biopolymers.

[47]  D. Patel,et al.  Readout of epigenetic modifications. , 2013, Annual review of biochemistry.

[48]  J. Brennan,et al.  ARID1a-DNA Interactions Are Required for Promoter Occupancy by SWI/SNF , 2012, Molecular and Cellular Biology.

[49]  C. Baumann,et al.  Loss of Maternal ATRX Results in Centromere Instability and Aneuploidy in the Mammalian Oocyte and Pre-Implantation Embryo , 2010, PLoS genetics.

[50]  R. McLendon,et al.  Altered Telomeres in Tumors with ATRX and DAXX Mutations , 2011, Science.

[51]  Sean D. Taverna,et al.  How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers , 2007, Nature Structural &Molecular Biology.

[52]  C. Peterson,et al.  Architecture of the SWI/SNF-Nucleosome Complex , 2008, Molecular and Cellular Biology.

[53]  Wei Wu,et al.  From neural development to cognition: unexpected roles for chromatin , 2013, Nature Reviews Genetics.

[54]  Jeffrey N. McKnight,et al.  Decoupling nucleosome recognition from DNA binding dramatically alters the properties of the Chd1 chromatin remodeler , 2012, Nucleic acids research.

[55]  C. Peterson,et al.  A Conserved Swi2/Snf2 ATPase Motif Couples ATP Hydrolysis to Chromatin Remodeling , 2005, Molecular and Cellular Biology.

[56]  Taekjip Ha,et al.  Spring-Loaded Mechanism of DNA Unwinding by Hepatitis C Virus NS3 Helicase , 2007, Science.

[57]  Carl Wu,et al.  Involvement of actin-related proteins in ATP-dependent chromatin remodeling. , 2003, Molecular cell.

[58]  Karl-Peter Hopfner,et al.  Structure and mechanism of the Swi2/Snf2 remodeller Mot1 in complex with its substrate TBP , 2011, Nature.

[59]  P. van de Putte,et al.  Helicase motifs V and VI of the Escherichia coli UvrB protein of the UvrABC endonuclease are essential for the formation of the preincision complex. , 1994, Journal of molecular biology.

[60]  Andres E Leschziner,et al.  Conformational flexibility in the chromatin remodeler RSC observed by electron microscopy and the orthogonal tilt reconstruction method , 2007, Proceedings of the National Academy of Sciences.

[61]  G. Narlikar,et al.  ATP-dependent chromatin remodeling enzymes: two heads are not better, just different. , 2008, Current opinion in genetics & development.

[62]  M. Kirschner,et al.  Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. , 1998, Genes & development.

[63]  Wei-Hua Wu,et al.  ATP-Driven Exchange of Histone H2AZ Variant Catalyzed by SWR1 Chromatin Remodeling Complex , 2004, Science.

[64]  Michael D. Stone,et al.  Dynamics of nucleosome remodelling by individual ACF complexes , 2009, Nature.

[65]  R. Kingston,et al.  Functional selectivity of recombinant mammalian SWI/SNF subunits. , 2000, Genes & development.

[66]  Wei Yang,et al.  UvrD Helicase Unwinds DNA One Base Pair at a Time by a Two-Part Power Stroke , 2006, Cell.

[67]  Song Tan,et al.  Histone H3 tail acetylation modulates ATP-dependent remodeling through multiple mechanisms , 2011, Nucleic acids research.

[68]  M. Pazin,et al.  Histone H4-K16 Acetylation Controls Chromatin Structure and Protein Interactions , 2006, Science.

[69]  J. Workman,et al.  Histone Acetyltransferase Complexes Stabilize SWI/SNF Binding to Promoter Nucleosomes , 2001, Cell.

[70]  Vamsi K. Gangaraju,et al.  Conformational changes associated with template commitment in ATP-dependent chromatin remodeling by ISW2. , 2009, Molecular cell.

[71]  B. Bartholomew,et al.  SWI/SNF unwraps, slides, and rewraps the nucleosome. , 2003, Molecular cell.

[72]  J. Tamkun,et al.  Modulation of ISWI function by site‐specific histone acetylation , 2002, EMBO reports.

[73]  Anindya Dutta,et al.  Supplemental Data Rvb 1 p / Rvb 2 p Recruit Arp 5 p and Assemble a Functional Ino 80 Chromatin Remodeling Complex , 2022 .

[74]  X. Zhuang,et al.  Nucleosome mobilization by ISW2 requires the concerted action of the ATPase and SLIDE domains , 2013, Nature Structural &Molecular Biology.

[75]  M. Yaniv,et al.  The hbrm and BRG‐1 proteins, components of the human SNF/SWI complex, are phosphorylated and excluded from the condensed chromosomes during mitosis. , 1996, The EMBO journal.

[76]  M. Thompson,et al.  Polybromo-1-bromodomains bind histone H3 at specific acetyl-lysine positions. , 2007, Biochemical and biophysical research communications.

[77]  P. Wade,et al.  SnapShot: Chromatin Remodeling: CHD , 2011, Cell.

[78]  I. Tinoco,et al.  Single–Base Pair Unwinding and Asynchronous RNA Release by the Hepatitis C Virus NS3 Helicase , 2011, Science.

[79]  J Seth Strattan,et al.  Removal of promoter nucleosomes by disassembly rather than sliding in vivo. , 2004, Molecular cell.

[80]  B. Bartholomew Monomeric actin required for INO80 remodeling , 2013, Nature Structural &Molecular Biology.

[81]  K. Rippe,et al.  A 'loop recapture' mechanism for ACF-dependent nucleosome remodeling , 2005, Nature Structural &Molecular Biology.

[82]  B. Cairns,et al.  Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes , 2012, Nature.

[83]  G. Crabtree,et al.  Kinetic Analysis of npBAF to nBAF Switching Reveals Exchange of SS18 with CREST and Integration with Neural Developmental Pathways , 2013, The Journal of Neuroscience.

[84]  A. Alexeev,et al.  Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54 , 2005, Nature Structural &Molecular Biology.

[85]  D. Patel,et al.  Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF , 2006, Nature.

[86]  Anindya Dutta,et al.  Rvb1p/Rvb2p recruit Arp5p and assemble a functional Ino80 chromatin remodeling complex. , 2004, Molecular cell.

[87]  Tad A. Holak,et al.  DNA-binding properties of the recombinant high-mobility-group-like AT-hook-containing region from human BRG1 protein , 2006, Biological chemistry.

[88]  Rebecca A Dagg,et al.  Loss of Wild-Type ATRX Expression in Somatic Cell Hybrids Segregates with Activation of Alternative Lengthening of Telomeres , 2012, PloS one.

[89]  Jonathan R. Pollack,et al.  The Spectrum of SWI/SNF Mutations, Ubiquitous in Human Cancers , 2013, PloS one.

[90]  T. Owen-Hughes,et al.  Mechanisms and Functions of ATP-Dependent Chromatin-Remodeling Enzymes , 2013, Cell.

[91]  T. Richmond,et al.  Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. , 2002, Journal of molecular biology.

[92]  M. L. Dechassa,et al.  SWI/SNF has intrinsic nucleosome disassembly activity that is dependent on adjacent nucleosomes. , 2010, Molecular cell.

[93]  G. Crabtree,et al.  ATP-dependent chromatin remodeling in neural development , 2009, Current Opinion in Neurobiology.

[94]  G. Crabtree,et al.  Chromatin remodelling during development , 2010, Nature.

[95]  O. Rando,et al.  Global Regulation of H2A.Z Localization by the INO80 Chromatin-Remodeling Enzyme Is Essential for Genome Integrity , 2011, Cell.

[96]  Ming-Ming Zhou,et al.  Structure and chromosomal DNA binding of the SWIRM domain , 2005, Nature Structural &Molecular Biology.

[97]  P. Quail,et al.  HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. , 2000, Genes & development.

[98]  M. Thompson Polybromo-1: the chromatin targeting subunit of the PBAF complex. , 2009, Biochimie.

[99]  Monika S. Kowalczyk,et al.  Structural consequences of disease-causing mutations in the ATRX-DNMT3-DNMT3L (ADD) domain of the chromatin-associated protein ATRX , 2007, Proceedings of the National Academy of Sciences.

[100]  K. Rippe,et al.  DNA sequence- and conformation-directed positioning of nucleosomes by chromatin-remodeling complexes , 2007, Proceedings of the National Academy of Sciences.

[101]  J. Workman,et al.  Gcn5 regulates the dissociation of SWI/SNF from chromatin by acetylation of Swi2/Snf2. , 2010, Genes & development.

[102]  G. Narlikar,et al.  The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing , 2006, Nature Structural &Molecular Biology.

[103]  K. Luger,et al.  Evidence for monomeric actin function in INO80 chromatin remodeling , 2013, Nature Structural &Molecular Biology.

[104]  V. Blinov,et al.  A conserved NTP-motif in putative helicases , 1988, Nature.

[105]  C. Allis,et al.  Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres , 2010, Proceedings of the National Academy of Sciences.

[106]  K. Luger,et al.  Structure of Actin-related protein 8 and its contribution to nucleosome binding , 2012, Nucleic acids research.

[107]  C. Müller,et al.  Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. , 2003, Molecular cell.

[108]  K. Robinson,et al.  Replication-Independent Assembly of Nucleosome Arrays in a Novel Yeast Chromatin Reconstitution System Involves Antisilencing Factor Asf1p and Chromodomain Protein Chd1p , 2003, Molecular and Cellular Biology.

[109]  Geoffrey J. Barton,et al.  Identification of multiple distinct Snf2 subfamilies with conserved structural motifs , 2006, Nucleic acids research.

[110]  B. Cairns,et al.  Autoregulation of the rsc4 tandem bromodomain by gcn5 acetylation. , 2007, Molecular cell.

[111]  Georgios Skiniotis,et al.  Acetylated Histone Tail Peptides Induce Structural Rearrangements in the RSC Chromatin Remodeling Complex* , 2007, Journal of Biological Chemistry.

[112]  P. Dallas,et al.  The DNA-binding properties of the ARID-containing subunits of yeast and mammalian SWI/SNF complexes. , 2004, Nucleic acids research.

[113]  H. Madhani,et al.  Combinatorial, site-specific requirement for heterochromatic silencing factors in the elimination of nucleosome-free regions. , 2010, Genes & development.

[114]  M. Zofall,et al.  Topography of the ISW2–nucleosome complex: insights into nucleosome spacing and chromatin remodeling , 2004, The EMBO journal.

[115]  I. Tinoco,et al.  RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP , 2006, Nature.

[116]  Xuecheng Zhang,et al.  Solution structure of SWI1 AT‐rich interaction domain from Saccharomyces cerevisiae and its nonspecific binding to DNA , 2012, Proteins.

[117]  D. S. Hsu,et al.  Structure and Function of the UvrB Protein (*) , 1995, The Journal of Biological Chemistry.

[118]  B. Pugh,et al.  A new, highly conserved domain in Swi2/Snf2 is required for SWI/SNF remodeling , 2011, Nucleic acids research.

[119]  T. Bonaldi,et al.  Site-specific acetylation of ISWI by GCN5 , 2007, BMC Molecular Biology.

[120]  B. Cairns,et al.  Two actin-related proteins are shared functional components of the chromatin-remodeling complexes RSC and SWI/SNF. , 1998, Molecular cell.

[121]  M. Zofall,et al.  Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome , 2006, Nature Structural &Molecular Biology.

[122]  Eugene V. Koonin,et al.  Helicases: amino acid sequence comparisons and structure-function relationships , 1993 .

[123]  C. Peterson,et al.  The SANT domain: a unique histone-tail-binding module? , 2004, Nature Reviews Molecular Cell Biology.

[124]  J A Eisen,et al.  Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. , 1995, Nucleic acids research.

[125]  Jeffrey N. McKnight,et al.  Extranucleosomal DNA Binding Directs Nucleosome Sliding by Chd1 , 2011, Molecular and Cellular Biology.

[126]  P. Dallas,et al.  ARID proteins: a diverse family of DNA binding proteins implicated in the control of cell growth, differentiation, and development. , 2002, Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research.

[127]  Ye Zhang,et al.  A switch from hBrm to Brg1 at IFNγ-activated sequences mediates the activation of human genes , 2010, Cell Research.

[128]  Fan Zhang,et al.  Structure of a RSC–nucleosome complex and insights into chromatin remodeling , 2008, Nature Structural &Molecular Biology.

[129]  K. Rippe,et al.  Human ISWI chromatin-remodeling complexes sample nucleosomes via transient binding reactions and become immobilized at active sites , 2010, Proceedings of the National Academy of Sciences.

[130]  A. Burlingame,et al.  The Site-Specific Installation of Methyl-Lysine Analogs into Recombinant Histones , 2007, Cell.

[131]  D. Landsman,et al.  AT-hook motifs identified in a wide variety of DNA-binding proteins. , 1998, Nucleic acids research.

[132]  C. Körner,et al.  X-Ray Structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase Core and Its Complex with DNA , 2005, Cell.

[133]  J. T. Kadonaga,et al.  Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly , 2005, Nature Structural &Molecular Biology.

[134]  Hua Xiao,et al.  N Terminus of Swr1 Binds to Histone H2AZ and Provides a Platform for Subunit Assembly in the Chromatin Remodeling Complex* , 2009, Journal of Biological Chemistry.

[135]  G. Längst,et al.  ISWI induces nucleosome sliding on nicked DNA. , 2001, Molecular cell.

[136]  T. Ha,et al.  PcrA Helicase Dismantles RecA Filaments by Reeling in DNA in Uniform Steps , 2010, Cell.

[137]  R. Kingston,et al.  Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. , 1999, Molecular cell.

[138]  Y. Hayashizaki,et al.  Structural and functional differences of SWIRM domain subtypes. , 2007, Journal of molecular biology.

[139]  D. Wigley,et al.  Demonstration of unidirectional single-stranded DNA translocation by PcrA helicase: measurement of step size and translocation speed. , 2000, Biochemistry.

[140]  M. Zofall,et al.  High-Resolution Mapping of Changes in Histone-DNA Contacts of Nucleosomes Remodeled by ISW2 , 2002, Molecular and Cellular Biology.

[141]  J. Hayes,et al.  hSWI/SNF-Catalyzed Nucleosome Sliding Does Not Occur Solely via a Twist-Diffusion Mechanism , 2002, Molecular and Cellular Biology.

[142]  Gabriel Waksman,et al.  Major Domain Swiveling Revealed by the Crystal Structures of Complexes of E. coli Rep Helicase Bound to Single-Stranded DNA and ADP , 1997, Cell.

[143]  R. Kornberg,et al.  Chromatin remodeling by DNA bending, not twisting. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[144]  Yifan Cheng,et al.  The chromatin remodeler ACF acts as a dimeric motor to space nucleosomes , 2009, Nature.

[145]  P. Becker,et al.  The ATPase domain of ISWI is an autonomous nucleosome remodeling machine , 2012, Nature Structural &Molecular Biology.

[146]  C. Tsang,et al.  Nutrient regulates Tor1 nuclear localization and association with rDNA promoter , 2006, Nature.

[147]  B. Cairns,et al.  Structure of an actin-related subcomplex of the SWI/SNF chromatin remodeler , 2013, Proceedings of the National Academy of Sciences.

[148]  D. Reinberg,et al.  Reconstitution of recombinant chromatin establishes a requirement for histone-tail modifications during chromatin assembly and transcription. , 2001, Genes & development.

[149]  B. Cairns,et al.  Structure and function of the SWIRM domain, a conserved protein module found in chromatin regulatory complexes , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[150]  S. Velankar,et al.  Crystal Structures of Complexes of PcrA DNA Helicase with a DNA Substrate Indicate an Inchworm Mechanism , 1999, Cell.

[151]  T. Richmond,et al.  Crystal structure of the nucleosome core particle at 2.8 Å resolution , 1997, Nature.

[152]  D. Wigley,et al.  Structure and mechanism of helicases and nucleic acid translocases. , 2007, Annual review of biochemistry.

[153]  R. Aebersold,et al.  An Essential Switch in Subunit Composition of a Chromatin Remodeling Complex during Neural Development , 2007, Neuron.

[154]  B. Bartholomew,et al.  Regulation of ISW2 by Concerted Action of Histone H4 Tail and Extranucleosomal DNA , 2006, Molecular and Cellular Biology.

[155]  P. Bjerling,et al.  The CHD remodeling factor Hrp1 stimulates CENP-A loading to centromeres , 2005, Nucleic acids research.

[156]  A. Hamiche,et al.  The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. , 2010, Genes & development.

[157]  G. Crabtree,et al.  MicroRNA-mediated switching of chromatin-remodelling complexes in neural development , 2009, Nature.

[158]  E. Moran,et al.  Nomenclature of the ARID family of DNA-binding proteins. , 2005, Genomics.

[159]  S. Fenn,et al.  Structural biochemistry of nuclear actin‐related proteins 4 and 8 reveals their interaction with actin , 2011, The EMBO journal.

[160]  B. Bartholomew,et al.  The INO80 ATP-Dependent Chromatin Remodeling Complex Is a Nucleosome Spacing Factor , 2010, Molecular and Cellular Biology.

[161]  Anjanabha Saha,et al.  Chromatin remodeling through directional DNA translocation from an internal nucleosomal site , 2005, Nature Structural &Molecular Biology.

[162]  Vamsi K. Gangaraju,et al.  Dependency of ISW1a Chromatin Remodeling on Extranucleosomal DNA , 2007, Molecular and Cellular Biology.

[163]  Andrew Flaus,et al.  Mechanisms for ATP-dependent chromatin remodelling: farewell to the tuna-can octamer? , 2004, Current opinion in genetics & development.

[164]  J. Workman,et al.  Perturbation of nucleosome core structure by the SWI/SNF complex persists after its detachment, enhancing subsequent transcription factor binding. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[165]  Michelle D. Wang,et al.  High resolution dynamic mapping of histone-DNA interactions in a nucleosome , 2008, Nature Structural &Molecular Biology.

[166]  C. Peterson,et al.  The RSC chromatin remodelling enzyme has a unique role in directing the accurate positioning of nucleosomes , 2011, The EMBO journal.

[167]  Wei-Hua Wu,et al.  Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange , 2005, Nature Structural &Molecular Biology.

[168]  M. Poirier,et al.  The SnAC Domain of SWI/SNF Is a Histone Anchor Required for Remodeling , 2012, Molecular and Cellular Biology.