Histone variants--the structure behind the function.

In recent years, the chromatin field has witnessed a renewed interest in histone variants as pertaining to their structural role, but mainly because of the functional specificity they impart to chromatin. In this review, I am going to discuss several of the most recent structural studies on core histone (H2A.Bbd, H2A.Z, H2A.X, macroH2A, H3.3, CENP-A) and linker histone variants (histone H1 microheterogeneity) focusing on their role in nucleosome stability and chromatin fibre dynamics with special emphasis on their possible functional implications. The data accumulated to date indicates that histone variability plays an important role in the histone-mediated regulation of chromatin metabolism. Understanding and deciphering the underlying structural amino acid code behind such variability remains one of the most exciting future challenges in chromatin research.

[1]  K. Choo,et al.  Building the centromere: from foundation proteins to 3D organization. , 2004, Trends in cell biology.

[2]  Thomas Ried,et al.  Response to RAG-mediated V(D)J cleavage by NBS1 and γ-H2AX , 2000 .

[3]  V. Fried,et al.  MacroH2A, a core histone containing a large nonhistone region. , 1992, Science.

[4]  Steven Henikoff,et al.  Histone variants, nucleosome assembly and epigenetic inheritance. , 2004, Trends in genetics : TIG.

[5]  Benjamin A. Shoemaker,et al.  Histone structure and nucleosome stability , 2005, Expert review of proteomics.

[6]  R. Cole A minireview of microheterogeneity in H1 histone and its possible significance. , 1984, Analytical biochemistry.

[7]  J. Hackstein Spermatogenesis in Drosophila. , 1987, Results and problems in cell differentiation.

[8]  H. Willard,et al.  Chromatin of the Barr body: histone and non-histone proteins associated with or excluded from the inactive X chromosome. , 2003, Human molecular genetics.

[9]  K. Yoda,et al.  CENP-A, -B, and -C Chromatin Complex That Contains the I-Type α-Satellite Array Constitutes the Prekinetochore in HeLa Cells , 2002, Molecular and Cellular Biology.

[10]  B. Turner,et al.  Reading signals on the nucleosome with a new nomenclature for modified histones , 2005, Nature Structural &Molecular Biology.

[11]  K. Scheffzek,et al.  Splicing regulates NAD metabolite binding to histone macroH2A , 2005, Nature Structural &Molecular Biology.

[12]  D. Reinberg,et al.  Histone variants meet their match , 2005, Nature Reviews Molecular Cell Biology.

[13]  T. Richmond,et al.  X-ray structure of a tetranucleosome and its implications for the chromatin fibre , 2005, Nature.

[14]  K. Sullivan,et al.  A solid foundation: functional specialization of centromeric chromatin. , 2001, Current opinion in genetics & development.

[15]  R. Baker,et al.  The N Terminus of the Centromere H3-Like Protein Cse4p Performs an Essential Function Distinct from That of the Histone Fold Domain , 2000, Molecular and Cellular Biology.

[16]  J. Hayes,et al.  Chromatin in need of a fix: phosphorylation of H2AX connects chromatin to DNA repair. , 2005, Molecular cell.

[17]  K. Choo,et al.  Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. Suzuki,et al.  SPKK, a new nucleic acid‐binding unit of protein found in histone. , 1989, The EMBO journal.

[19]  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.

[20]  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.

[21]  D. Angelov,et al.  The histone variant macroH2A interferes with transcription factor binding and SWI/SNF nucleosome remodeling. , 2003, Molecular cell.

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

[23]  J. Ausió,et al.  New twists on H2A.Z: a histone variant with a controversial structural and functional past. , 2004, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[24]  J. Greally,et al.  Mammalian linker-histone subtypes differentially affect gene expression in vivo , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[25]  E. Bradbury,et al.  Photobleaching of GFP-labeled H2AX in chromatin: H2AX has low diffusional mobility in the nucleus. , 2002, Biochemical and biophysical research communications.

[26]  Huiming Ding,et al.  A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. , 2003, Molecular cell.

[27]  Stephen P. Jackson,et al.  A role for Saccharomyces cerevisiae histone H2A in DNA repair , 2000, Nature.

[28]  B. Loppin,et al.  The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus , 2005, Nature.

[29]  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.

[30]  Y. Tsujimoto,et al.  Involvement of Histone H1.2 in Apoptosis Induced by DNA Double-Strand Breaks , 2003, Cell.

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

[32]  M. Hendzel,et al.  The C-terminal Domain Is the Primary Determinant of Histone H1 Binding to Chromatin in Vivo* , 2004, Journal of Biological Chemistry.

[33]  Nevan J Krogan,et al.  INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. , 2004, Cell.

[34]  A. Annunziato Split Decision: What Happens to Nucleosomes during DNA Replication?* , 2005, Journal of Biological Chemistry.

[35]  A. Gineitis,et al.  Novel human testis-specific histone H2B encoded by the interrupted gene on the X chromosome. , 2004, Genomics.

[36]  K. Luger,et al.  Structure and dynamic properties of nucleosome core particles , 2005, FEBS letters.

[37]  J. Ausió Analytical ultracentrifugation and the characterization of chromatin structure. , 2000, Biophysical chemistry.

[38]  Eric D. Ross,et al.  Intrinsic Protein Disorder, Amino Acid Composition, and Histone Terminal Domains* , 2006, Journal of Biological Chemistry.

[39]  P. Bhargava,et al.  Histones in functional diversification , 2005, The FEBS journal.

[40]  J. Davie,et al.  Effects of histone acetylation, ubiquitination and variants on nucleosome stability. , 1993, The Biochemical journal.

[41]  Ilya Ioshikhes,et al.  Structural dynamics of nucleosome core particle: Comparison with nucleosomes containing histone variants , 2004, Proteins.

[42]  C. Bonifer,et al.  The replacement histone H2A.Z in a hyperacetylated form is a feature of active genes in the chicken , 2005, Nucleic acids research.

[43]  M. Hurt,et al.  A Mouse Histone H1 Variant, H1b, Binds Preferentially to a Regulatory Sequence within a Mouse H3.2 Replication-dependent Histone Gene* , 1997, The Journal of Biological Chemistry.

[44]  G. Cross,et al.  Histone H2AZ dimerizes with a novel variant H2B and is enriched at repetitive DNA in Trypanosoma brucei , 2005, Journal of Cell Science.

[45]  S. Khochbin,et al.  Histone H1 diversity: bridging regulatory signals to linker histone function. , 2001, Gene.

[46]  K. Nagata,et al.  Assembly and Disassembly of Nucleosome Core Particles Containing Histone Variants by Human Nucleosome Assembly Protein I , 2005, Molecular and Cellular Biology.

[47]  C. Dharia,et al.  Developmental and tissue expression patterns of histone macroH2A1 subtypes , 1997, Journal of cellular biochemistry.

[48]  B. Sendov,et al.  Possible molecular mechanism for cell differentiation in multicellular organisms. , 1971, Journal of theoretical biology.

[49]  Jordanka Zlatanova,et al.  Chromatin fibers, one-at-a-time. , 2003, Journal of molecular biology.

[50]  K. Luger,et al.  Structural Characterization of the Histone Variant macroH2A , 2005, Molecular and Cellular Biology.

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

[52]  B. Hamkalo,et al.  Distribution of somatic H1 subtypes is non‐random on active vs. inactive chromatin II: Distribution in human adult fibroblasts , 2001, Journal of cellular biochemistry.

[53]  Hiroshi Kimura,et al.  Histone dynamics in living cells revealed by photobleaching. , 2005, DNA repair.

[54]  K. V. van Holde,et al.  Nucleosome positioning is determined by the (H3-H4)2 tetramer. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[55]  D. Doenecke,et al.  Characterisation of human histone H1x , 2005, Biological chemistry.

[56]  V. Ramakrishnan,et al.  Crystallization of the globular domain of histone H5. , 1990, Journal of molecular biology.

[57]  J. Turner,et al.  M31 and macroH2A1.2 colocalise at the pseudoautosomal region during mouse meiosis. , 2001, Journal of cell science.

[58]  J. Krebs,et al.  Histone modifications and DNA double-strand break repair. , 2004, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[59]  J. Downs,et al.  Histone H2A phosphorylation in DNA double‐strand break repair , 2005, The FEBS journal.

[60]  A. Gansmuller,et al.  Polar nuclear localization of H1T2, a histone H1 variant, required for spermatid elongation and DNA condensation during spermiogenesis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[62]  S. Jackson,et al.  Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. , 2004, Molecular cell.

[63]  A. Ehrenhofer-Murray,et al.  Chromatin dynamics at DNA replication, transcription and repair. , 2004, European journal of biochemistry.

[64]  A. Gineitis,et al.  Human Testis/Sperm-specific Histone H2B (hTSH2B) , 2002, The Journal of Biological Chemistry.

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

[66]  W. Kistler,et al.  H1 histone subfractions of mammalian testes. 1. Organ specificity in the rat. , 1979, Biochemistry.

[67]  Y. Pommier,et al.  Initiation of DNA Fragmentation during Apoptosis Induces Phosphorylation of H2AX Histone at Serine 139* , 2000, The Journal of Biological Chemistry.

[68]  C. Caron,et al.  The role of histones in chromatin remodelling during mammalian spermiogenesis. , 2004, European journal of biochemistry.

[69]  S. Henikoff,et al.  Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[70]  James T Kadonaga,et al.  Chromatin remodeling by ATP-dependent molecular machines. , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[71]  J. Ausió,et al.  H2AX: tailoring histone H2A for chromatin-dependent genomic integrity. , 2005, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[72]  D. W. Abbott,et al.  Histone variant H2ABbd confers lower stability to the nucleosome , 2004, EMBO reports.

[73]  K. V. van Holde,et al.  What happens to nucleosomes during transcription? , 1992, The Journal of biological chemistry.

[74]  T. Ried,et al.  Response to RAG-mediated VDJ cleavage by NBS1 and gamma-H2AX. , 2000, Science.

[75]  Paul R. Selvin,et al.  The renaissance of fluorescence resonance energy transfer , 2000, Nature Structural Biology.

[76]  Michael Bustin,et al.  The dynamics of histone H1 function in chromatin. , 2005, Molecular cell.

[77]  G. Almouzni,et al.  Histone chaperones, a supporting role in the limelight. , 2004, Biochimica et biophysica acta.

[78]  S. Schreiber,et al.  Histone Variant H2A.Z Marks the 5′ Ends of Both Active and Inactive Genes in Euchromatin , 2006, Cell.

[79]  J. M. Kinkade,et al.  A structural comparison of different lysine-rich histones of calf thymus. , 1966, The Journal of biological chemistry.

[80]  M.Mitchell Smith,et al.  Centromeres and variant histones: what, where, when and why? , 2002, Current opinion in cell biology.

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

[82]  H. Willard,et al.  Barring gene expression after XIST: maintaining facultative heterochromatin on the inactive X. , 2003, Seminars in cell & developmental biology.

[83]  J. E. Halley,et al.  Telomeric heterochromatin boundaries require NuA4-dependent acetylation of histone variant H2A.Z in Saccharomyces cerevisiae. , 2006, Genes & development.

[84]  Steven Henikoff,et al.  Phylogenomics of the nucleosome , 2003, Nature Structural Biology.

[85]  J. Widom,et al.  Nucleosomes facilitate their own invasion , 2004, Nature Structural &Molecular Biology.

[86]  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.

[87]  R. Bouillon,et al.  A structural basis for the unique binding features of the human vitamin D-binding protein , 2002, Nature Structural Biology.

[88]  K. Luger,et al.  A New Fluorescence Resonance Energy Transfer Approach Demonstrates That the Histone Variant H2AZ Stabilizes the Histone Octamer within the Nucleosome* , 2004, Journal of Biological Chemistry.

[89]  David T. Brown Histone H1 and the dynamic regulation of chromatin function. , 2003, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[90]  C. Bustamante,et al.  Rapid spontaneous accessibility of nucleosomal DNA , 2005, Nature Structural &Molecular Biology.

[91]  A. Nussenzweig,et al.  Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. , 2003, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[92]  W. Bonner,et al.  Changes in histone H3 composition and synthesis pattern during lymphocyte activation. , 1983, Biochemistry.

[93]  W. Bonner,et al.  Histones and their modifications. , 1986, CRC critical reviews in biochemistry.

[94]  R. Margolis,et al.  A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones , 1987, The Journal of cell biology.

[95]  K. Luger,et al.  A new FRET approach demonstrates that the histone variant H 2 AZ stabilizes the histone octamer within the nucleosome , 2004 .

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

[97]  W. Kistler,et al.  Isolation and characterization of rat testis H1t. An H1 histone variant associated with spermatogenesis. , 1980, The Journal of biological chemistry.

[98]  Beatrix Ueberheide,et al.  Protein identification using sequential ion/ion reactions and tandem mass spectrometry. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[99]  H. Willard,et al.  A Novel Chromatin Protein, Distantly Related to Histone H2a, Is Largely Excluded from the Inactive X Chromosome , 2001, The Journal of cell biology.

[100]  S. Keeney,et al.  Recombinational DNA double-strand breaks in mice precede synapsis , 2001, Nature Genetics.

[101]  N. Krogan,et al.  The Saccharomyces cerevisiae histone H2A variant Htz1 is acetylated by NuA4. , 2006, Genes & development.

[102]  E. Rogakou,et al.  DNA Double-stranded Breaks Induce Histone H2AX Phosphorylation on Serine 139* , 1998, The Journal of Biological Chemistry.

[103]  R. Kingston,et al.  Noncovalent modification of chromatin: different remodeled products with different ATPase domains. , 2004, Cold Spring Harbor symposia on quantitative biology.

[104]  S. Henikoff,et al.  Adaptive evolution of the histone fold domain in centromeric histones. , 2004, Molecular biology and evolution.

[105]  M. Bycroft,et al.  The macro domain is an ADP‐ribose binding module , 2004, The EMBO journal.

[106]  D. Speiser,et al.  Fast , long-range , reversible conformational fluctuations in nucleosomes revealed by single-pair fluorescence resonance energy transfer , 2008 .

[107]  V. Roberts,et al.  Structural characterization of histone H2A variants. , 2004, Cold Spring Harbor symposia on quantitative biology.

[108]  M. Grunstein,et al.  Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. , 2006, Genes & development.

[109]  Ali Hamiche,et al.  A chromatin remodelling complex involved in transcription and DNA processing , 2000, Nature.

[110]  Carl Wu,et al.  Histone tails modulate nucleosome mobility and regulate ATP-dependent nucleosome sliding by NURF , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[111]  G. Almouzni,et al.  Histone H3.1 and H3.3 Complexes Mediate Nucleosome Assembly Pathways Dependent or Independent of DNA Synthesis , 2004, Cell.

[112]  E. Bradbury Histone nomenclature. , 1977, Methods in cell biology.

[113]  K. Sullivan,et al.  Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere , 1994, The Journal of cell biology.

[114]  Brian E. Schwartz,et al.  Transcriptional activation triggers deposition and removal of the histone variant H3.3. , 2005, Genes & development.

[115]  D. W. Abbott,et al.  Histone variants and histone modifications: a structural perspective. , 2001, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[116]  D. W. Abbott,et al.  The role of histone variability in chromatin stability and folding , 2004 .

[117]  N. Iguchi,et al.  Isolation and characterization of a novel cDNA encoding a DNA-binding protein (Hils1) specifically expressed in testicular haploid germ cells. , 2003, International journal of andrology.

[118]  Huntington F. Willard,et al.  Histone variant macroH2A contains two distinct macrochromatin domains capable of directing macroH2A to the inactive X chromosome , 2001, Nucleic Acids Res..

[119]  J. Pehrson,et al.  Evolutionary conservation of histone macroH2A subtypes and domains. , 1998, Nucleic acids research.

[120]  J. Zlatanova,et al.  Single-molecule analysis of chromatin. , 2004, Methods in enzymology.

[121]  C. Lavelle,et al.  Sequence-dependent nucleosome structural and dynamic polymorphism. Potential involvement of histone H2B N-terminal tail proximal domain. , 2003, Journal of molecular biology.

[122]  J. Lieberman,et al.  A phosphatase complex that dephosphorylates γH2AX regulates DNA damage checkpoint recovery , 2006, Nature.

[123]  J. O. Thomas,et al.  Exchange of histone H1 between segments of chromatin. , 1981, Journal of molecular biology.

[124]  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.

[125]  Junjie Chen,et al.  Histone H2AX Is Phosphorylated in an ATR-dependent Manner in Response to Replicational Stress* , 2001, The Journal of Biological Chemistry.

[126]  J. E. Godfrey,et al.  H2a-specific proteolysis as a unique probe in the analysis of the histone octamer. , 1988, The Journal of biological chemistry.

[127]  R. Chalkley,et al.  A cysteine-containing H2B-like histone found in mature mammalian testis. , 1976, The Journal of biological chemistry.

[128]  N. Krogan,et al.  INO80 and γ-H2AX Interaction Links ATP-Dependent Chromatin Remodeling to DNA Damage Repair , 2004, Cell.

[129]  H. Willard,et al.  Cell cycle–dependent localization of macroH2A in chromatin of the inactive X chromosome , 2002, The Journal of cell biology.

[130]  K. Yoda,et al.  Human centromere protein A (CENP-A) can replace histone H3 in nucleosome reconstitution in vitro. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[131]  D. W. Abbott,et al.  Structural characterization of macroH2A containing chromatin. , 2004, Biochemistry.

[132]  Karolin Luger,et al.  Structural determinants for generating centromeric chromatin , 2004, Nature.

[133]  K. Ueda,et al.  The appearance of male gamete-specific histones gH2B and gH3 during pollen development in Lilium longiflorum. , 1995, Developmental biology.

[134]  A. Mirzabekov,et al.  Structure of nucleosomes and organization of internucleosomal DNA in chromatin. , 1990, Journal of molecular biology.

[135]  J. Ausió,et al.  Characterization of nucleosomes consisting of the human testis/sperm-specific histone H2B variant (hTSH2B). , 2005, Biochemistry.

[136]  K. Ueda,et al.  Unusual core histones specifically expressed in male gametic cells of Lilium longiflorum , 2000, Chromosoma.

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

[138]  R. Cole Microheterogeneity in H1 histones and its consequences. , 2009, International journal of peptide and protein research.

[139]  W. Bonner,et al.  Histone 2A, a heteromorphous family of eight protein species. , 1980, Biochemistry.

[140]  J. Hayes,et al.  Probing core histone tail-DNA interactions in a model dinucleosome system. , 2004, Methods in enzymology.

[141]  W. Albig,et al.  Characterization of the H1.5 gene completes the set of human H1 subtype genes. , 1997, Gene.

[142]  Danny Reinberg,et al.  Elongation by RNA polymerase II: the short and long of it. , 2004, Genes & development.

[143]  V. Ramakrishnan,et al.  Position and orientation of the globular domain of linker histone H5 on the nucleosome , 1998, Nature.

[144]  C. Tyler-Smith,et al.  Many Paths to the Top of the Mountain Diverse Evolutionary Solutions to Centromere Structure , 2000, Cell.

[145]  S. Henikoff,et al.  Genome-scale profiling of histone H3.3 replacement patterns , 2005, Nature Genetics.

[146]  K. Luger,et al.  Nucleosomes containing the histone variant H2A.Bbd organize only 118 base pairs of DNA , 2004, The EMBO journal.

[147]  Andrew Flaus,et al.  Sin mutations alter inherent nucleosome mobility , 2004, The EMBO journal.

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

[149]  Andrew J Link,et al.  A Protein Complex Containing the Conserved Swi2/Snf2-Related ATPase Swr1p Deposits Histone Variant H2A.Z into Euchromatin , 2004, PLoS biology.

[150]  N. Gilbert,et al.  Distinctive higher-order chromatin structure at mammalian centromeres , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[151]  K. Luger,et al.  H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding. , 2004, Molecular cell.

[152]  M. Hendzel,et al.  H1 Family Histones in the Nucleus , 2005, Journal of Biological Chemistry.

[153]  Christophe E. Redon,et al.  Characteristics of γ-H2AX foci at DNA double-strand breaks sites , 2003 .

[154]  T. Fukagawa Centromere DNA, proteins and kinetochore assembly in vertebrate cells , 2004, Chromosome Research.

[155]  A. Zalensky,et al.  Male germline-specific histones in mouse and man , 2004, Cytogenetic and Genome Research.

[156]  R. Habas,et al.  Msx1 Cooperates with Histone H1b for Inhibition of Transcription and Myogenesis , 2004, Science.

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

[158]  J. Ausió,et al.  Common Evolutionary Origin and Birth-and-Death Process in the Replication-Independent Histone H1 Isoforms from Vertebrate and Invertebrate Genomes , 2005, Journal of Molecular Evolution.

[159]  B. Roux,et al.  Role of histones H1 and H3 in the maintenance of chromatin in a compact conformation , 1983, FEBS letters.

[160]  Karolin Luger,et al.  Nucleosome and chromatin fiber dynamics. , 2005, Current opinion in structural biology.

[161]  Andrés Martínez,et al.  Birth-and-death evolution with strong purifying selection in the histone H1 multigene family and the origin of orphon H1 genes. , 2004, Molecular biology and evolution.

[162]  R. Roeder,et al.  SWI/SNF remodeling and p300‐dependent transcription of histone variant H2ABbd nucleosomal arrays , 2004, The EMBO journal.

[163]  J. Ausió,et al.  Protamines, in the Footsteps of Linker Histone Evolution* , 2006, Journal of Biological Chemistry.

[164]  D. W. Abbott,et al.  A haploid affair: core histone transitions during spermatogenesis. , 2003, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[165]  T. Eickbush,et al.  A chromatin-bound proteolytic activity with unique specificity for histone H2A , 1976, Cell.

[166]  Emil L. Smith,et al.  2 – Chromosomal Proteins , 1979 .

[167]  J. M. Kinkade,et al.  The resolution of four lysine-rich histones derived from calf thymus. , 1966, The Journal of biological chemistry.

[168]  B. Placek,et al.  The H2A.Z/H2B dimer is unstable compared to the dimer containing the major H2A isoform , 2005, Protein science : a publication of the Protein Society.

[169]  A. Travers,et al.  Relative affinities of DNA sequences for the histone octamer depend strongly upon both the temperature and octamer concentration. , 2005, Biochemistry.

[170]  B. Hamkalo,et al.  A compendium of the histone H1 family of somatic subtypes: an elusive cast of characters and their characteristics. , 2001, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[171]  D. W. Abbott,et al.  Characterization of the Stability and Folding of H2A.Z Chromatin Particles , 2001, The Journal of Biological Chemistry.

[172]  C. Costanzi,et al.  Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals , 1998, Nature.

[173]  A. Zweidler,et al.  Regulation of nucleosomal core histone variant levels in differentiating murine erythroleukemia cells. , 1984, Biochemistry.

[174]  Wei Yan,et al.  HILS1 is a spermatid-specific linker histone H1-like protein implicated in chromatin remodeling during mammalian spermiogenesis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[175]  Mathieu Blanchette,et al.  Variant Histone H2A.Z Is Globally Localized to the Promoters of Inactive Yeast Genes and Regulates Nucleosome Positioning , 2005, PLoS biology.

[176]  E. Stedman,et al.  THE CHEMICAL NATURE AND FUNCTIONS OF THE COMPONENTS OF CELL NUCLEI , 1947 .

[177]  S. Henikoff,et al.  Centromeric chromatin: what makes it unique? , 2005, Current opinion in genetics & development.

[178]  D. W. Abbott,et al.  Beyond the Xi , 2005, Journal of Biological Chemistry.

[179]  Maki Kihara,et al.  H1oo: a pre-embryonic H1 linker histone in search of a function , 2003, Molecular and Cellular Endocrinology.

[180]  H. Woodland Histone Genes: Structure, Organization and Regulation , 1985 .

[181]  J. Ausió,et al.  Nucleoplasmin: a nuclear chaperone. , 2004, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[182]  W. Hennig Chromosomal proteins in the spermatogenesis of Drosophila , 2003, Chromosoma.

[183]  B. Hamkalo,et al.  A proposal for a coherent mammalian histone H1 nomenclature correlated with amino acid sequences , 1994, Protein science : a publication of the Protein Society.