Functional Delineation of Three Groups of the ATP-dependent Family of Chromatin Remodeling Enzymes*

ATP-dependent chromatin remodeling enzymes antagonize the inhibitory effects of chromatin. We compare six different remodeling complexes: ySWI/SNF, yRSC, hSWI/SNF, xMi-2, dCHRAC, and dNURF. We find that each complex uses similar amounts of ATP to remodel nucleosomal arrays at nearly identical rates. We also perform assays with arrays reconstituted with hyperacetylated or trypsinized histones and isolated histone (H3/H4)2tetramers. The results define three groups of the ATP-dependent family of remodeling enzymes. In addition we investigate the ability of an acidic activator to recruit remodeling complexes to nucleosomal arrays. We propose that ATP-dependent chromatin remodeling enzymes share a common reaction mechanism and that a key distinction between complexes is in their mode of regulation or recruitment.

[1]  A. Wolffe Transcriptional Activation: Switched-on chromatin , 1994, Current Biology.

[2]  A. Wolffe,et al.  A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase , 1998, Current Biology.

[3]  J. Hansen,et al.  Hybrid trypsinized nucleosomal arrays: identification of multiple functional roles of the H2A/H2B and H3/H4 N-termini in chromatin fiber compaction. , 1997, Biochemistry.

[4]  E. Bradbury,et al.  Mobility of positioned nucleosomes on 5 S rDNA. , 1991, Journal of molecular biology.

[5]  K. V. van Holde,et al.  Homogeneous reconstituted oligonucleosomes, evidence for salt-dependent folding in the absence of histone H1. , 1989, Biochemistry.

[6]  S. Schreiber,et al.  Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex , 1998, Nature.

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

[8]  J. Kennison,et al.  dMi-2, a hunchback-interacting protein that functions in polycomb repression. , 1998, Science.

[9]  L. G. Burns,et al.  Protein complexes for remodeling chromatin. , 1997, Biochimica et biophysica acta.

[10]  Achim Leutz,et al.  A C/EBPβ Isoform Recruits the SWI/SNF Complex to Activate Myeloid Genes , 1999 .

[11]  C. Peterson,et al.  SWI-SNF-Mediated Nucleosome Remodeling: Role of Histone Octamer Mobility in the Persistence of the Remodeled State , 2000, Molecular and Cellular Biology.

[12]  Carl Wu,et al.  The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. , 2000, Molecular cell.

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

[14]  Ali Hamiche,et al.  ATP-Dependent Histone Octamer Sliding Mediated by the Chromatin Remodeling Complex NURF , 1999, Cell.

[15]  J. Widom,et al.  Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. , 1995, Journal of molecular biology.

[16]  K. V. van Holde,et al.  DNA and protein determinants of nucleosome positioning on sea urchin 5S rRNA gene sequences in vitro. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[17]  R. Kingston,et al.  Stable Remodeling of Tailless Nucleosomes by the Human SWI-SNF Complex , 1999, Molecular and Cellular Biology.

[18]  Thomas C. Kaufman,et al.  brahma: A regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2 SWI2 , 1992, Cell.

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

[20]  C. Allis,et al.  The language of covalent histone modifications , 2000, Nature.

[21]  K. V. van Holde,et al.  The mechanism of nucleosome assembly onto oligomers of the sea urchin 5 S DNA positioning sequence. , 1991, The Journal of biological chemistry.

[22]  T. Tsukiyama,et al.  Role of histone tails in nucleosome remodeling by Drosophila NURF , 1997, The EMBO journal.

[23]  B. Cairns,et al.  Chromatin remodeling machines: similar motors, ulterior motives. , 1998, Trends in biochemical sciences.

[24]  Michael R. Green,et al.  Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex , 1994, Nature.

[25]  Paul Tempst,et al.  RSC, an Essential, Abundant Chromatin-Remodeling Complex , 1996, Cell.

[26]  J. Workman,et al.  Control of class II gene transcription during in vitro nucleosome assembly. , 1991, Methods in cell biology.

[27]  C. Peterson,et al.  Purification and biochemical properties of yeast SWI/SNF complex. , 1999, Methods in enzymology.

[28]  A. Stein DNA folding by histones: the kinetics of chromatin core particle reassembly and the interaction of nucleosomes with histones. , 1979, Journal of molecular biology.

[29]  B. Cairns,et al.  A multisubunit complex containing the SWI1/ADR6, SWI2/SNF2, SWI3, SNF5, and SNF6 gene products isolated from yeast. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[30]  M. R. Murphy,et al.  Targeting a SWI/SNF-related chromatin remodeling complex to the beta-globin promoter in erythroid cells. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[31]  R. Kingston,et al.  ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. , 1999, Genes & development.

[32]  C. Peterson,et al.  The core histone N-terminal domains are required for multiple rounds of catalytic chromatin remodeling by the SWI/SNF and RSC complexes. , 1999, Biochemistry.

[33]  Carl Wu,et al.  Purification and properties of an ATP-dependent nucleosome remodeling factor , 1995, Cell.

[34]  Toshio Tsukiyama,et al.  ISWI, a member of the SWl2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor , 1995, Cell.

[35]  R. Ebright,et al.  Roles of the Histone H2A-H2B Dimers and the (H3-H4)2Tetramer in Nucleosome Remodeling by the SWI-SNF Complex* , 2000, The Journal of Biological Chemistry.

[36]  R. Paro,et al.  The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

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

[38]  G. Längst,et al.  ISWI is an ATP-dependent nucleosome remodeling factor. , 1999, Molecular cell.

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

[40]  C Logie,et al.  Catalytic activity of the yeast SWI/SNF complex on reconstituted nucleosome arrays , 1997, The EMBO journal.

[41]  C. McCallum,et al.  Identification and characterization of Drosophila relatives of the yeast transcriptional activator SNF2/SWI2 , 1994, Molecular and cellular biology.

[42]  T. Gibson,et al.  The SANT domain: a putative DNA-binding domain in the SWI-SNF and ADA complexes, the transcriptional co-repressor N-CoR and TFIIIB. , 1996, Trends in biochemical sciences.

[43]  G. Längst,et al.  Nucleosome Movement by CHRAC and ISWI without Disruption or trans-Displacement of the Histone Octamer , 1999, Cell.

[44]  C. Peterson,et al.  Chromatin remodeling: a marriage between two families? , 1998, BioEssays : news and reviews in molecular, cellular and developmental biology.

[45]  Matthias Mann,et al.  Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II , 1997, Nature.

[46]  T. Archer,et al.  Chromatin remodelling by the glucocorticoid receptor requires the BRG1 complex , 1998, Nature.

[47]  R. Kingston,et al.  Mammalian SWI-SNF Complexes Contribute to Activation of the hsp70 Gene , 2000, Molecular and Cellular Biology.

[48]  C Logie,et al.  Recruitment of the SWI/SNF chromatin remodeling complex by transcriptional activators. , 1999, Genes & development.

[49]  C. Peterson SWI/SNF complex: dissection of a chromatin remodeling cycle. , 1998, Cold Spring Harbor symposia on quantitative biology.

[50]  M. Yaniv,et al.  ATP-dependent chromatin remodelling: SWI/SNF and Co. are on the job. , 1999, Journal of molecular biology.

[51]  E. Ballestar,et al.  Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation , 1999, Nature Genetics.

[52]  J. Widom,et al.  A model for the cooperative binding of eukaryotic regulatory proteins to nucleosomal target sites. , 1996, Journal of molecular biology.

[53]  Weidong Wang,et al.  NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. , 1998, Molecular cell.

[54]  C. McCallum,et al.  The Drosophila trithorax group proteins BRM, ASH1 and ASH2 are subunits of distinct protein complexes. , 1998, Development.

[55]  J. Workman,et al.  Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. , 1994, Science.

[56]  D. Reinberg,et al.  The Dermatomyositis-Specific Autoantigen Mi2 Is a Component of a Complex Containing Histone Deacetylase and Nucleosome Remodeling Activities , 1998, Cell.

[57]  Ryuji Kobayashi,et al.  ACF, an ISWI-Containing and ATP-Utilizing Chromatin Assembly and Remodeling Factor , 1997, Cell.

[58]  Andrew Flaus,et al.  Nucleosome mobilization catalysed by the yeast SWI/SNF complex , 1999, Nature.

[59]  G. Orphanides,et al.  Requirement of RSF and FACT for transcription of chromatin templates in vitro. , 1998, Science.