Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions.

Chromatin fibers are dynamic macromolecular assemblages that are intimately involved in nuclear function. This review focuses on recent advances centered on the molecular mechanisms and determinants of chromatin fiber dynamics in solution. Major points of emphasis are the functions of the core histone tail domains, linker histones, and a new class of proteins that assemble supramolecular chromatin structures. The discussion of important structural issues is set against a background of possible functional significance.

[1]  J. O. Thomas,et al.  Histone H1: location and role. , 1999, Current opinion in cell biology.

[2]  M. Bustin,et al.  The chromatin unfolding domain of chromosomal protein HMG-14 targets the N-terminal tail of histone H3 in nucleosomes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[3]  K. V. van Holde,et al.  Dynamics and equilibria of nucleosomes at elevated ionic strength. , 1984, The Journal of biological chemistry.

[4]  F. Thoma,et al.  Involvement of the domains of histones H1 and H5 in the structural organization of soluble chromatin. , 1983, Journal of molecular biology.

[5]  C. Bustamante,et al.  Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Anne E Carpenter,et al.  Large-scale chromatin structure and function. , 1999, Current opinion in cell biology.

[7]  Jerry Workman,et al.  Persistent Interactions of Core Histone Tails with Nucleosomal DNA following Acetylation and Transcription Factor Binding , 1998, Molecular and Cellular Biology.

[8]  V. Ramakrishnan,et al.  Histone H1 and chromatin higher-order structure. , 1997, Critical reviews in eukaryotic gene expression.

[9]  J. Ausió,et al.  Role of the histone "tails" in the folding of oligonucleosomes depleted of histone H1. , 1992, The Journal of biological chemistry.

[10]  R. Bambara,et al.  Human DNA ligase I efficiently seals nicks in nucleosomes , 2000, The EMBO journal.

[11]  G. Hager,et al.  Structure and Dynamic Properties of a Glucocorticoid Receptor-Induced Chromatin Transition , 2000, Molecular and Cellular Biology.

[12]  H. Eisenberg,et al.  Nucleosome core particle stability and conformational change. Effect of temperature, particle and NaCl concentrations, and crosslinking of histone H3 sulfhydryl groups. , 1984, Journal of molecular biology.

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

[14]  G. Arents,et al.  Structure of the histone octamer core of the nucleosome and its potential interactions with DNA. , 1993, Cold Spring Harbor symposia on quantitative biology.

[15]  D. Bazett-Jones,et al.  High resolution microanalysis and three-dimensional nucleosome structure associated with transcribing chromatin. , 1997, Micron.

[16]  W. Beard,et al.  DNA lesion bypass polymerases open up. , 2001, Structure.

[17]  C. Bustamante,et al.  Pulling chromatin fibers: computer simulations of direct physical micromanipulations. , 2000, Journal of molecular biology.

[18]  J. Widom.  Physicochemical studies of the folding of the 100 A nucleosome filament into the 300 A filament. Cation dependence. , 1986, Journal of molecular biology.

[19]  J. Ausió,et al.  Major role of the histones H3-H4 in the folding of the chromatin fiber. , 1997, Biochemical and biophysical research communications.

[20]  J. M. Gale,et al.  Photofootprint of nucleosome core DNA in intact chromatin having different structural states. , 1988, Journal of molecular biology.

[21]  D. Crothers,et al.  Condensation of chromatin: role of multivalent cations. , 1986, Biochemistry.

[22]  S. Dimitrov,et al.  Higher-order structure of chromatin and chromosomes. , 2001, Current opinion in genetics & development.

[23]  A. Annunziato,et al.  Role of histone acetylation in the assembly and modulation of chromatin structures. , 2000, Gene expression.

[24]  C. Crane-Robinson.  How do linker histones mediate differential gene expression? , 1999, BioEssays : news and reviews in molecular, cellular and developmental biology.

[25]  J. Widom,et al.  Sequence and position-dependence of the equilibrium accessibility of nucleosomal DNA target sites. , 2000, Journal of molecular biology.

[26]  M. Grunstein,et al.  Histone H3 N‐terminal mutations allow hyperactivation of the yeast GAL1 gene in vivo. , 1992, The EMBO journal.

[27]  G. Arents,et al.  Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Alan P. Wolffe,et al.  Disruption of Higher-Order Folding by Core Histone Acetylation Dramatically Enhances Transcription of Nucleosomal Arrays by RNA Polymerase III , 1998, Molecular and Cellular Biology.

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

[30]  J. Banères,et al.  The N tails of histones H3 and H4 adopt a highly structured conformation in the nucleosome. , 1997, Journal of molecular biology.

[31]  B. Wang,et al.  The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[32]  C. Crane-Robinson.  Where is the globular domain of linker histone located on the nucleosome? , 1997, Trends in biochemical sciences.

[33]  K. V. van Holde,et al.  Salt-induced release of DNA from nucleosome core particles. , 1989, Biochemistry.

[34]  L. Pillus,et al.  Silent chromatin in yeast: an orchestrated medley featuring Sir3p , 1998, BioEssays : news and reviews in molecular, cellular and developmental biology.

[35]  A. Wolffe,et al.  Review: chromatin structural features and targets that regulate transcription. , 2000, Journal of structural biology.

[36]  A. Wolffe,et al.  Asymmetric linker histone association directs the asymmetric rearrangement of core histone interactions in a positioned nucleosome containing a thyroid hormone response element. , 1998, Biochemistry.

[37]  P. Butler,et al.  Changes in chromatin folding in solution. , 1980, Journal of molecular biology.

[38]  T. Richmond,et al.  Preparation of nucleosome core particle from recombinant histones. , 1999, Methods in enzymology.

[39]  F. Thoma,et al.  Influence of histone H1 on chromatin structure , 1977, Cell.

[40]  M. Bustin,et al.  Histone H1 Is a Specific Repressor of Core Histone Acetylation in Chromatin , 2000, Molecular and Cellular Biology.

[41]  K. V. van Holde,et al.  Chromatin structure revisited. , 1999, Critical reviews in eukaryotic gene expression.

[42]  E. Bradbury,et al.  Magnetic Resonance Studies of Deoxyribonucleoprotein , 1973, Nature.

[43]  K. Luger,et al.  The essential histone variant H2A.Z regulates the equilibrium between different chromatin conformational states , 2002, Nature Structural Biology.

[44]  E. Bradbury,et al.  Control of Cell Division by Very Lysine Rich Histone (F1) Phosphorylation , 1974, Nature.

[45]  K. V. van Holde,et al.  Linker histone tails and N-tails of histone H3 are redundant: scanning force microscopy studies of reconstituted fibers. , 1998, Biophysical journal.

[46]  J. Hansen,et al.  Enhanced transcription factor access to arrays of histone H3/H4 tetramer.DNA complexes in vitro: implications for replication and transcription. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[47]  V. Allfrey,et al.  Reversible and irreversible changes in nucleosome structure along the c-fos and c-myc oncogenes following inhibition of transcription. , 1990, Journal of molecular biology.

[48]  S. Grigoryev,et al.  Chromatin Structure in Granulocytes , 1998, The Journal of Biological Chemistry.

[49]  J. Ausió,et al.  Effects of Histone Acetylation on the Solubility and Folding of the Chromatin Fiber* , 2001, The Journal of Biological Chemistry.

[50]  J. Whitlock,et al.  Localization of the sites along nucleosome DNA which interact with NH2-terminal histone regions. , 1977, The Journal of biological chemistry.

[51]  J. Hansen,et al.  Reversible oligonucleosome self-association: dependence on divalent cations and core histone tail domains. , 1996, Biochemistry.

[52]  J. Bednar,et al.  MENT, a Heterochromatin Protein That Mediates Higher Order Chromatin Folding, Is a New Serpin Family Member* , 1999, The Journal of Biological Chemistry.

[53]  D. Gottschling.  Gene silencing: Two faces of SIR2 , 2000, Current Biology.

[54]  J. Davie,et al.  Histone acetylation alters the capacity of the H1 histones to condense transcriptionally active/competent chromatin. , 1990, The Journal of biological chemistry.

[55]  K. V. van Holde,et al.  Self-association of linker histone H5 and of its globular domain: evidence for specific self-contacts. , 1998, Biochemistry.

[56]  J. Hansen,et al.  Formation and stability of higher order chromatin structures. Contributions of the histone octamer. , 1994, Journal of Biological Chemistry.

[57]  D. Lohr,et al.  Assembly and structural properties of subsaturated chromatin arrays. , 1993, The Journal of biological chemistry.

[58]  J. Widom.  Structure, dynamics, and function of chromatin in vitro. , 1998, Annual review of biophysics and biomolecular structure.

[59]  J. Maman,et al.  Self-association of the globular domain of histone H5. , 1994, Biochemistry.

[60]  James G. McNally,et al.  Large-scale chromatin decondensation and recondensation regulated by transcription from a natural promoter , 2001, The Journal of cell biology.

[61]  G. Felsenfeld,et al.  Histone hyperacetylation has little effect on the higher order folding of chromatin. , 1983, Nucleic acids research.

[62]  A. Travers.  The location of the linker histone on the nucleosome. , 1999, Trends in biochemical sciences.

[63]  J. Hayes,et al.  The N-terminal tail of histone H2A binds to two distinct sites within the nucleosome core. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[64]  T. Richmond,et al.  DNA binding within the nucleosome core. , 1998, Current opinion in structural biology.

[65]  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.

[66]  P. N. Lewis,et al.  Assembly, Remodeling, and Histone Binding Capabilities of Yeast Nucleosome Assembly Protein 1* , 1998, The Journal of Biological Chemistry.

[67]  Tom Misteli,et al.  Dynamic binding of histone H1 to chromatin in living cells , 2000, Nature.

[68]  A. Wolffe,et al.  The histone core exerts a dominant constraint on the structure of DNA in a nucleosome. , 1991, Biochemistry.

[69]  P. Georgel,et al.  Linker histone function in chromatin: dual mechanisms of action. , 2001, Biochemistry and cell biology = Biochimie et biologie cellulaire.

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

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

[72]  J. Widom,et al.  Effects of core histone tail domains on the equilibrium constants for dynamic DNA site accessibility in nucleosomes. , 2000, Journal of molecular biology.

[73]  D. Lohr,et al.  Evidence for nonrandom behavior in 208-12 subsaturated nucleosomal array populations analyzed by AFM. , 1999, Biochemistry.

[74]  T. Richmond,et al.  The histone tails of the nucleosome. , 1998, Current opinion in genetics & development.

[75]  C. Allis,et al.  Translating the Histone Code , 2001, Science.

[76]  J. A. Subirana.  Order and disorder in 30 nm chromatin fibers , 1992, FEBS letters.

[77]  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.

[78]  A J Koster,et al.  Nucleosomes, linker DNA, and linker histone form a unique structural motif that directs the higher-order folding and compaction of chromatin. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[79]  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.

[80]  P. Rathjen,et al.  Histone variant H2A.Z is required for early mammalian development , 2001, Current Biology.

[81]  K. Horwitz,et al.  The Mouse Mammary Tumor Virus Promoter Adopts Distinct Chromatin Structures in Human Breast Cancer Cells with and without Glucocorticoid Receptor* , 2000, The Journal of Biological Chemistry.

[82]  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.

[83]  K. V. van Holde,et al.  Use of selectively trypsinized nucleosome core particles to analyze the role of the histone "tails" in the stabilization of the nucleosome. , 1989, Journal of molecular biology.

[84]  D. Tremethick,et al.  Regions of variant histone His2AvD required for Drosophila development , 1999, Nature.

[85]  K. V. van Holde,et al.  Three-dimensional structure of extended chromatin fibers as revealed by tapping-mode scanning force microscopy. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[86]  James Allan,et al.  Roles of H1 domains in determining higher order chromatin structure and H1 location. , 1986, Journal of molecular biology.

[87]  R. Glaser,et al.  Histone H2A.Z Is Widely but Nonrandomly Distributed in Chromosomes of Drosophila melanogaster * , 2000, The Journal of Biological Chemistry.

[88]  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.

[89]  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.

[90]  C. Woodcock,et al.  Treatment with sodium butyrate inhibits the complete condensation of interphase chromatin , 2004, Chromosoma.

[91]  D. Crothers,et al.  Binding of daunomycin to calf thymus nucleosomes. , 1983, Biochemistry.

[92]  J. Workman,et al.  Alteration of nucleosome structure as a mechanism of transcriptional regulation. , 1998, Annual review of biochemistry.

[93]  K. V. van Holde,et al.  Boundary analysis of sedimentation‐velocity experiments with monodisperse and paucidisperse solutes , 1978 .

[94]  K. Khrapko,et al.  Distribution of high mobility group proteins 1/2, E and 14/17 and linker histones H1 and H5 on transcribed and non-transcribed regions of chicken erythrocyte chromatin. , 1991, Nucleic acids research.

[95]  K. V. van Holde,et al.  Chromatin fiber structure: morphology, molecular determinants, structural transitions. , 1998, Biophysical journal.

[96]  C. Bustamante,et al.  Analysis of chromatin by scanning force microscopy. , 1999, Methods in molecular biology.

[97]  Claudio Nicolini,et al.  Chromatin Structure and Function , 1979, NATO Advanced Study Institutes Series.

[98]  K. V. van Holde,et al.  Chromatin Higher Order Structure: Chasing a Mirage?(*) , 1995, The Journal of Biological Chemistry.

[99]  A. Wolffe,et al.  Nuclear visions: functional flexibility from structural instability. , 2001 .

[100]  P. Serwer,et al.  Quantitative analysis of macromolecular conformational changes using agarose gel electrophoresis: application to chromatin folding. , 1994, Biochemistry.

[101]  E. Bradbury,et al.  Linker histones H1 and H5 prevent the mobility of positioned nucleosomes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[102]  D. Angelov,et al.  Preferential interaction of the core histone tail domains with linker DNA , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[103]  A. Wolffe,et al.  Structure and function of the core histone N-termini: more than meets the eye. , 1998, Biochemistry.

[104]  J. Bednar,et al.  Linker histones stabilize the intrinsic salt-dependent folding of nucleosomal arrays: mechanistic ramifications for higher-order chromatin folding. , 1998, Biochemistry.

[105]  J. Hansen,et al.  The Core Histone N Termini Function Independently of Linker Histones during Chromatin Condensation* , 2000, The Journal of Biological Chemistry.

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

[107]  A Klug,et al.  Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin , 1979, The Journal of cell biology.

[108]  K. Luger,et al.  Crystal structure of a nucleosome core particle containing the variant histone H2A.Z , 2000, Nature Structural Biology.

[109]  C. Peterson,et al.  Chromatin remodeling enzymes: who's on first? , 2001, Current Biology.

[110]  J. Hayes,et al.  Nucleosomes and the chromatin fiber. , 2001, Current opinion in genetics & development.

[111]  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.

[112]  R. Simpson.  Structure of the chromatosome, a chromatin particle containing 160 base pairs of DNA and all the histones. , 1978, Biochemistry.

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

[114]  M. Grunstein,et al.  25 years after the nucleosome model: chromatin modifications. , 2000, Trends in biochemical sciences.

[115]  J. Ausió,et al.  Analysis of the changes in the structure and hydration of the nucleosome core particle at moderate ionic strengths. , 1990, Biochemistry.

[116]  A. Mirzabekov,et al.  Change in the pattern of histone binding to DNA upon transcriptional activation , 1989, Cell.

[117]  V. Ramakrishnan,et al.  Crystal structure of globular domain of histone H5 and its implications for nucleosome binding , 1993, Nature.

[118]  J. Widom,et al.  Equilibrium and dynamic nucleosome stability. , 1999, Methods in molecular biology.

[119]  A. Belmont,et al.  Visualization of G1 chromosomes: a folded, twisted, supercoiled chromonema model of interphase chromatid structure , 1994, The Journal of cell biology.

[120]  J. Hansen,et al.  Assembly of defined nucleosomal and chromatin arrays from pure components. , 1999, Methods in enzymology.

[121]  F. Ottensmeyer,et al.  Structural States of the Nucleosome (*) , 1996, The Journal of Biological Chemistry.

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

[123]  J. Hansen,et al.  Core Histone Tail Domains Mediate Oligonucleosome Folding and Nucleosomal DNA Organization through Distinct Molecular Mechanisms (*) , 1995, The Journal of Biological Chemistry.

[124]  C. Woodcock,et al.  Chromatin organization re-viewed. , 1995, Trends in cell biology.

[125]  Walker Io.  Differential dissociation of histone tails from core chromatin. , 1984 .

[126]  T. Kimura,et al.  Electrostatic mechanism of chromatin folding. , 1990, Journal of molecular biology.

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

[128]  E. Bradbury,et al.  Rearrangement of the histone H2A C-terminal domain in the nucleosome. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[129]  J. Hayes,et al.  Linker DNA and H1-dependent reorganization of histone-DNA interactions within the nucleosome. , 1998, Biochemistry.

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

[131]  C. Allis,et al.  Histone methylation versus histone acetylation: new insights into epigenetic regulation. , 2001, Current opinion in cell biology.

[132]  A. Wolffe,et al.  Chromatin disruption and modification. , 1999, Nucleic acids research.

[133]  C. Peterson,et al.  Global Role for Chromatin Remodeling Enzymes in Mitotic Gene Expression , 2000, Cell.

[134]  R. Simpson,et al.  The organized chromatin domain of the repressed yeast a cell‐specific gene STE6 contains two molecules of the corepressor Tup1p per nucleosome , 2000, The EMBO journal.

[135]  A. Wolffe,et al.  What do linker histones do in chromatin? , 1997, BioEssays : news and reviews in molecular, cellular and developmental biology.

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

[137]  C. Allis,et al.  Signaling to Chromatin through Histone Modifications , 2000, Cell.

[138]  H. Eisenberg,et al.  Hydrodynamic studies of the interaction between nucleosome core particles and core histones. , 1981, Journal of molecular biology.

[139]  J. Dubochet,et al.  Chromatin conformation and salt-induced compaction: three-dimensional structural information from cryoelectron microscopy , 1995, The Journal of cell biology.

[140]  G. Arents,et al.  The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[141]  A. Wolffe,et al.  A role for histones H2A/H2B in chromatin folding and transcriptional repression. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[142]  T Schlick,et al.  Computational modeling predicts the structure and dynamics of chromatin fiber. , 2001, Structure.

[143]  C. Peterson,et al.  Functional interaction between GCN5 and polyamines: a new role for core histone acetylation , 1999, The EMBO journal.

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

[145]  L. Böhm,et al.  Proteases as structural probes for chromatin: The domain structure of histones , 1984, Bioscience reports.

[146]  K. E. Van Holde,et al.  Nucleosome Motion: Evidence and Models , 1985 .

[147]  A. Mirzabekov,et al.  A highly basic histone H4 domain bound to the sharply bent region of nucleosomal DNA , 1988, Nature.

[148]  P. Cary,et al.  Nuclear-magnetic resonance and optical-spectroscopic studies of conformation and interactions in the cleaved halves of histone F2B. , 1972, European journal of biochemistry.

[149]  D. Landsman,et al.  A variety of DNA-binding and multimeric proteins contain the histone fold motif. , 1995, Nucleic acids research.

[150]  M. Hendzel,et al.  Rapid exchange of histone H1.1 on chromatin in living human cells , 2000, Nature.

[151]  A. Wolffe,et al.  Histone-DNA contacts in a nucleosome core containing a Xenopus 5S rRNA gene. , 1993, Biochemistry.

[152]  J. Widom,et al.  Chromatin structure: Linking structure to function with histone H1 , 1998, Current Biology.

[153]  P. Georgel,et al.  Sir3-dependent assembly of supramolecular chromatin structures in vitro , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[154]  J. Ausió,et al.  Acetylation Increases the α-Helical Content of the Histone Tails of the Nucleosome* , 2000, The Journal of Biological Chemistry.

[155]  F. Thoma,et al.  Chromatin reconstituted from tandemly repeated cloned DNA fragments and core histones: A model system for study of higher order structure , 1985, Cell.

[156]  D. Lilley,et al.  Chromatin core particle unfolding induced by tryptic cleavage of histones. , 1977, Nucleic acids research.

[157]  R. Kingston,et al.  What does 'chromatin remodeling' mean? , 2000, Trends in biochemical sciences.

[158]  J. Widom,et al.  Toward a unified model of chromatin folding. , 1989, Annual review of biophysics and biophysical chemistry.

[159]  J. Ausió,et al.  Magnesium-dependent Association and Folding of Oligonucleosomes Reconstituted with Ubiquitinated H2A* , 2001, The Journal of Biological Chemistry.