Chromatin Remodeling and the Control of Gene Expression*

Biochemical and genetic findings accumulated over the past decade have established that the condensation of eukaryotic DNA in chromatin functions not only to constrain the genome within the boundaries of the cell nucleus but also to suppress gene activity in a general manner. This genetic repression extends from the level of the nucleosome, the primary unit of chromatin organization, where coiling of DNA on the surface of the nucleosome core particle impedes access to the transcriptional apparatus, to the higher order folding of nucleosome arrays and the organization of silent regions of chromatin (for reviews see Refs. 1–6 and 105). Chromatin structure is inextricably linked to transcriptional regulation, and recent studies show how chromatin is perturbed so as to facilitate transcription (for reviews see Refs. 7–12). Here, we review the substantial advances in the identification of histone acetyltransferases and histone deacetylases, whose opposing activities establish the steady-state level of histone acetylation, and progress in studies of multicomponent systems that require energy for the process of nucleosome disruption.

[1]  M. Ikura,et al.  The Histone Folds in Transcription Factor TFIID (*) , 1996, The Journal of Biological Chemistry.

[2]  C. Sardet,et al.  A human protein with homology to Saccharomyces cerevisiae SNF5 interacts with the potential helicase hbrm. , 1995, Nucleic acids research.

[3]  M. Vidal,et al.  RPD3 encodes a second factor required to achieve maximum positive and negative transcriptional states in Saccharomyces cerevisiae , 1991, Molecular and cellular biology.

[4]  I. Herskowitz,et al.  A negative regulator of HO transcription, SIN1 (SPT2), is a nonspecific DNA-binding protein related to HMG1 , 1991, Molecular and cellular biology.

[5]  R. Young,et al.  RNA Polymerase II Holoenzyme Contains SWI/SNF Regulators Involved in Chromatin Remodeling , 1996, Cell.

[6]  M. Ptashne,et al.  RNA Polymerase II Holoenzyme Recruitment Is Sufficient to Remodel Chromatin at the Yeast PHO5 Promoter , 1997, Cell.

[7]  L. Guarente,et al.  Yeast ADA2 protein binds to the VP16 protein activation domain and activates transcription. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[8]  C. Peterson,et al.  Functional analysis of the DNA-stimulated ATPase domain of yeast SWI2/SNF2. , 1996, Nucleic acids research.

[9]  C. Peterson Multiple SWItches to turn on chromatin? , 1996, Current opinion in genetics & development.

[10]  H. Chiba,et al.  Two human homologues of Saccharomyces cerevisiae SWI2/SNF2 and Drosophila brahma are transcriptional coactivators cooperating with the estrogen receptor and the retinoic acid receptor. , 1994, Nucleic acids research.

[11]  M. Scott,et al.  The Drosophila snr1 and brm proteins are related to yeast SWI/SNF proteins and are components of a large protein complex. , 1995, Molecular biology of the cell.

[12]  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.

[13]  J. T. Kadonaga,et al.  Potentiation of RNA polymerase II transcription by Gal4-VP16 during but not after DNA replication and chromatin assembly. , 1993, Genes & development.

[14]  P. Becker,et al.  Energy‐dependent chromatin accessibility and nucleosome mobility in a cell‐free system. , 1995, The EMBO journal.

[15]  L. Chin,et al.  Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression , 1997, nature.

[16]  M. Grunstein,et al.  HDA1 and HDA3 Are Components of a Yeast Histone Deacetylase (HDA) Complex* , 1996, The Journal of Biological Chemistry.

[17]  C. Allis,et al.  Special HATs for special occasions: linking histone acetylation to chromatin assembly and gene activation. , 1996, Current opinion in genetics & development.

[18]  G. Chinnadurai,et al.  Identification of a cellular protein that specifically interacts with the essential cysteine region of the HIV-1 Tat transactivator. , 1996, Virology.

[19]  K. Struhl,et al.  The histone deacetylase RPD3 counteracts genomic silencing in Drosophila and yeast , 1996, Nature.

[20]  T. Hunter,et al.  A growing coactivator network , 1996, Nature.

[21]  R. Tjian,et al.  TAFII250 Is a Bipartite Protein Kinase That Phosphorylates the Basal Transcription Factor RAP74 , 1996, Cell.

[22]  K. Struhl,et al.  Repression by Ume6 Involves Recruitment of a Complex Containing Sin3 Corepressor and Rpd3 Histone Deacetylase to Target Promoters , 1997, Cell.

[23]  Stuart L Schreiber,et al.  Histone Deacetylase Activity Is Required for Full Transcriptional Repression by mSin3A , 1997, Cell.

[24]  G. Felsenfeld,et al.  Chromatin structure and gene expression. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[25]  S. Berger,et al.  Functional similarity and physical association between GCN5 and ADA2: putative transcriptional adaptors. , 1994, The EMBO journal.

[26]  P. Becker,et al.  Cell-free system for assembly of transcriptionally repressed chromatin from Drosophila embryos. , 1992, Molecular and cellular biology.

[27]  G. Crabtree,et al.  Diversity and specialization of mammalian SWI/SNF complexes. , 1996, Genes & development.

[28]  D. Edmondson,et al.  Repression domain of the yeast global repressor Tup1 interacts directly with histones H3 and H4. , 1996, Genes & development.

[29]  S. Berger,et al.  Histone acetyltransferase activity and interaction with ADA2 are critical for GCN5 function in vivo , 1997, The EMBO journal.

[30]  Craig L. Peterson,et al.  DNA-binding properties of the yeast SWI/SNF complex , 1996, Nature.

[31]  A. Wolffe,et al.  Influence of chromatin folding on transcription initiation and elongation by RNA polymerase III. , 1992, Biochemistry.

[32]  Wen‐Ming Yang,et al.  Histone Deacetylases Associated with the mSin3 Corepressor Mediate Mad Transcriptional Repression , 1997, Cell.

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

[34]  Wen‐Ming Yang,et al.  Transcriptional repression by YY1 is mediated by interaction with a mammalian homolog of the yeast global regulator RPD3. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[35]  A. Mirsky,et al.  ACETYLATION AND METHYLATION OF HISTONES AND THEIR POSSIBLE ROLE IN THE REGULATION OF RNA SYNTHESIS. , 1964, Proceedings of the National Academy of Sciences of the United States of America.

[36]  I. Herskowitz,et al.  Roles of SWI1, SWI2, and SWI3 proteins for transcriptional enhancement by steroid receptors. , 1992, Science.

[37]  B. Turner,et al.  Histone acetylation in chromatin and chromosomes. , 1995, Seminars in cell biology.

[38]  S. Elgin,et al.  Chromatin: Pushing nucleosomes around , 1996, Current Biology.

[39]  B. Howard,et al.  The Transcriptional Coactivators p300 and CBP Are Histone Acetyltransferases , 1996, Cell.

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

[41]  Steven A. Brown,et al.  Activator-dependent regulation of transcriptional pausing on nucleosomal templates. , 1996, Genes & development.

[42]  M. Pazin,et al.  ATP-dependent nucleosome reconfiguration and transcriptional activation from preassembled chromatin templates. , 1994, Science.

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

[44]  Michael Grunstein,et al.  Histone H3 amino terminus is required for telomeric and silent mating locus repression in yeast , 1994, Nature.

[45]  B. Turner,et al.  Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei , 1992, Cell.

[46]  J. Hansen,et al.  The nucleosomal array: structure/function relationships. , 1996, Critical reviews in eukaryotic gene expression.

[47]  C. Allis,et al.  Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines , 1996, Nature.

[48]  A. Hoffmann,et al.  A histone octamer-like structure within TFIID , 1996, Nature.

[49]  E. Geiduschek,et al.  Nucleosome mobility and the maintenance of nucleosome positioning. , 1997, Science.

[50]  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.

[51]  M. Scott,et al.  Five SWI/SNF gene products are components of a large multisubunit complex required for transcriptional enhancement. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Carl Wu,et al.  ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor , 1994, Nature.

[53]  R. Perry,et al.  DNA-binding and chromatin localization properties of CHD1 , 1995, Molecular and cellular biology.

[54]  R. Sandaltzopoulos,et al.  Chromatin remodeling by GAGA factor and heat shock factor at the hypersensitive Drosophila hsp26 promoter in vitro. , 1995, The EMBO journal.

[55]  S. Schreiber,et al.  Nuclear Receptor Repression Mediated by a Complex Containing SMRT, mSin3A, and Histone Deacetylase , 1997, Cell.

[56]  Andrew J. Bannister,et al.  The CBP co-activator is a histone acetyltransferase , 1996, Nature.

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

[58]  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.

[59]  A. Wolffe,et al.  Nucleosomal anatomy--where are the histones? , 1995, BioEssays : news and reviews in molecular, cellular and developmental biology.

[60]  R. Perry,et al.  A mammalian DNA-binding protein that contains a chromodomain and an SNF2/SWI2-like helicase domain. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[61]  J. Lucchesi,et al.  mof, a putative acetyl transferase gene related to the Tip60 and MOZ human genes and to the SAS genes of yeast, is required for dosage compensation in Drosophila , 1997, The EMBO journal.

[62]  Steven L. Cohen,et al.  Structural similarity between TAFs and the heterotetrameric core of the histone octamer , 1996, Nature.

[63]  D. Reinberg,et al.  Histone Deacetylases and SAP18, a Novel Polypeptide, Are Components of a Human Sin3 Complex , 1997, Cell.

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

[65]  G. Schroth,et al.  Studies of the DNA binding properties of histone H4 amino terminus. Thermal denaturation studies reveal that acetylation markedly reduces the binding constant of the H4 "tail" to DNA. , 1993, The Journal of biological chemistry.

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

[67]  James T Kadonaga,et al.  SWI2/SNF2 and Related Proteins: ATP-Driven Motors That Disrupt-Protein–DNA Interactions? , 1997, Cell.

[68]  M. Pazin,et al.  NF-kappa B-mediated chromatin reconfiguration and transcriptional activation of the HIV-1 enhancer in vitro. , 1996, Genes & development.

[69]  J. Ausió,et al.  Modulation of Chromatin Folding by Histone Acetylation (*) , 1995, The Journal of Biological Chemistry.

[70]  C. Glass,et al.  A complex containing N-CoR, mSln3 and histone deacetylase mediates transcriptional repression , 1997, nature.

[71]  B. Emerson,et al.  NF-E2 disrupts chromatin structure at human beta-globin locus control region hypersensitive site 2 in vitro , 1996, Molecular and cellular biology.

[72]  S. Berger,et al.  Characterization of Physical Interactions of the Putative Transcriptional Adaptor, ADA2, with Acidic Activation Domains and TATA-binding Protein (*) , 1995, The Journal of Biological Chemistry.

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

[74]  R. Kingston,et al.  Nucleosome Disruption by Human SWI/SNF Is Maintained in the Absence of Continued ATP Hydrolysis* , 1996, The Journal of Biological Chemistry.

[75]  I. Herskowitz,et al.  Amino acid substitutions in the structured domains of histones H3 and H4 partially relieve the requirement of the yeast SWI/SNF complex for transcription. , 1995, Genes & development.

[76]  S. Berger,et al.  Identification of human proteins functionally conserved with the yeast putative adaptors ADA2 and GCN5 , 1996, Molecular and cellular biology.

[77]  M. Yaniv,et al.  Purification and biochemical heterogeneity of the mammalian SWI‐SNF complex. , 1996, The EMBO journal.

[78]  M. Grunstein,et al.  HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[79]  Andreas Hecht,et al.  Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: A molecular model for the formation of heterochromatin in yeast , 1995, Cell.

[80]  Paul A. Khavari,et al.  BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription , 1993, Nature.

[81]  L. Guarente,et al.  ADA3, a putative transcriptional adaptor, consists of two separable domains and interacts with ADA2 and GCN5 in a trimeric complex , 1995, Molecular and cellular biology.

[82]  S. Schreiber,et al.  A Mammalian Histone Deacetylase Related to the Yeast Transcriptional Regulator Rpd3p , 1996, Science.

[83]  B M Turner,et al.  Efficient transcriptional silencing in Saccharomyces cerevisiae requires a heterochromatin histone acetylation pattern , 1996, Molecular and cellular biology.

[84]  C. Disteche,et al.  The translocation t(8;16)(p11;p13) of acute myeloid leukaemia fuses a putative acetyltransferase to the CREB–binding protein , 1996, Nature Genetics.

[85]  Andrew J. Bannister,et al.  The TAFII250 Subunit of TFIID Has Histone Acetyltransferase Activity , 1996, Cell.

[86]  L. Pillus,et al.  Yeast SAS silencing genes and human genes associated with AML and HIV–1 Tat interactions are homologous with acetyltransferases , 1996, Nature Genetics.

[87]  R. Kornberg,et al.  Interplay between chromatin structure and transcription. , 1995, Current opinion in cell biology.

[88]  Jerry L. Workman,et al.  Nucleosome displacement in transcription , 1993, Cell.

[89]  D. Koshland,et al.  Mitotic chromosome condensation. , 1996, Annual review of cell and developmental biology.

[90]  B. Howard,et al.  A p300/CBP-associated factor that competes with the adenoviral oncoprotein E1A , 1996, Nature.

[91]  Michael R. Green,et al.  Facilitated binding of TATA-binding protein to nucleosomal DNA , 1994, Nature.

[92]  V. Ramakrishnan,et al.  Histone structure and the organization of the nucleosome. , 1997, Annual review of biophysics and biomolecular structure.

[93]  Stephen K Burley,et al.  Architectural Transcription Factors: Proteins That-Remodel DNA , 1997, Cell.

[94]  M. Carlson,et al.  The yeast SNF2/SWI2 protein has DNA-stimulated ATPase activity required for transcriptional activation. , 1993, Genes & development.

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

[96]  Steven A. Brown,et al.  Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. , 1992, Genes & development.

[97]  M. Beato,et al.  Nucleosome-mediated synergism between transcription factors on the mouse mammary tumor virus promoter. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[99]  J. Workman,et al.  Persistent Site-Specific Remodeling of a Nucleosome Array by Transient Action of the SWI/SNF Complex , 1996, Science.

[100]  R. Perry,et al.  CHD1 is concentrated in interbands and puffed regions of Drosophila polytene chromosomes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[101]  C. Allis,et al.  Tetrahymena Histone Acetyltransferase A: A Homolog to Yeast Gcn5p Linking Histone Acetylation to Gene Activation , 1996, Cell.

[102]  M. Carlson,et al.  The SNF/SWI family of global transcriptional activators. , 1994, Current opinion in cell biology.

[103]  S. Berger,et al.  Histone acetyltransferase activity is conserved between yeast and human GCN5 and is required for complementation of growth and transcriptional activation , 1997, Molecular and cellular biology.