Chromosomal histone modification patterns--from conservation to diversity.

The organization of DNA into chromatin regulates expression and maintenance (replication, repair, recombination, segregation) of genetic information in a dynamic manner. The N-terminal tails of the nucleosomal core histones are subjected to post-translational modifications such as acetylation, methylation, phosphorylation, ubiquitination, glycosylation, ADP-ribosylation, carbonylation and sumoylation. These modifications, together with DNA methylation, control the folding of the nucleosomal array into higher order structures and mediate signalling for cellular processes. Although histones and their modifications are highly conserved, recent data show that chromosomal distribution of individual modifications (acetylation, methylation, phosphorylation) can differ along the cell cycle as well as among and between groups of eukaryotes. This implies the possibility of evolutionary divergence in reading the "histone code".

[1]  Richard R. Adams,et al.  Essential Roles of Drosophila Inner Centromere Protein (Incenp) and Aurora B in Histone H3 Phosphorylation, Metaphase Chromosome Alignment, Kinetochore Disjunction, and Chromosome Segregation , 2001, The Journal of cell biology.

[2]  A. Houben,et al.  The temporal and spatial pattern of histone H3 phosphorylation at serine 28 and serine 10 is similar in plants but differs between mono- and polycentric chromosomes , 2003, Cytogenetic and Genome Research.

[3]  M. Murata,et al.  Visualization of Diffuse Centromeres with Centromere-Specific Histone H3 in the Holocentric Plant Luzula niveaw⃞ , 2005, The Plant Cell Online.

[4]  A. Probst,et al.  Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis , 2005, The EMBO journal.

[5]  J. Bender,et al.  Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. , 2001, Genes & development.

[6]  Alexander W. Bird,et al.  Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair , 2002, Nature.

[7]  J. Boyes,et al.  Stimulation of V(D)J recombination by histone acetylation , 2000, Current Biology.

[8]  T. Jenuwein,et al.  Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3 , 2004, The EMBO journal.

[9]  Victor G Corces,et al.  Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. , 2004, Trends in genetics : TIG.

[10]  T. Sugiyama,et al.  The nucleation and maintenance of heterochromatin by a histone deacetylase in fission yeast. , 2005, Molecular cell.

[11]  Hengbin Wang,et al.  Role of Histone H3 Lysine 27 Methylation in X Inactivation , 2003, Science.

[12]  J. Fuchs,et al.  Molecular--cytogenetic characterization of the Vicia faba genome -- heterochromatin differentiation, replication patterns and sequence localization , 1998, Chromosome Research.

[13]  E. Thompson,et al.  Plasticity of histone modifications across the invertebrate to vertebrate transition: histone H3 lysine 4 trimethylation in heterochromatin , 2005, Chromosome Research.

[14]  Brian D. Strahl,et al.  Role of Histone H3 Lysine 9 Methylation in Epigenetic Control of Heterochromatin Assembly , 2001, Science.

[15]  K. Fukui,et al.  Characterization of plant Aurora kinases during mitosis , 2005, Plant Molecular Biology.

[16]  G. Schotta,et al.  Functional mammalian homologues of the Drosophila PEV‐modifier Su(var)3‐9 encode centromere‐associated proteins which complex with the heterochromatin component M31 , 1999, The EMBO journal.

[17]  K. Nakahigashi,et al.  The Arabidopsis heterochromatin protein1 homolog (TERMINAL FLOWER2) silences genes within the euchromatic region but not genes positioned in heterochromatin. , 2005, Plant & cell physiology.

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

[19]  A. Houben,et al.  The chromosomal distribution of phosphorylated histone H3 differs between plants and animals at meiosis , 2000, Chromosoma.

[20]  B. Turner,et al.  Histone modifications in Arabidopsis- high methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. , 2003, The Plant journal : for cell and molecular biology.

[21]  Benjamin A. Garcia,et al.  Regulation of HP1–chromatin binding by histone H3 methylation and phosphorylation , 2005, Nature.

[22]  C. Allis,et al.  Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

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

[24]  N. Belyaev,et al.  The acetylation patterns of histones H3 and H4 along Vicia faba chromosomes are different , 2004, Chromosome Research.

[25]  K. Scheidtmann,et al.  Novel phosphorylation of histone H3 at threonine 11 that temporally correlates with condensation of mitotic and meiotic chromosomes in plant cells , 2005, Cytogenetic and Genome Research.

[26]  A. Bird.  DNA methylation patterns and epigenetic memory. , 2002, Genes & development.

[27]  A. Meister,et al.  Chromatin organization and its relation to replication and histone acetylation during the cell cycle in barley , 2001, Chromosoma.

[28]  J. P. Jackson,et al.  Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase , 2002, Nature.

[29]  G. Schotta,et al.  Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. , 2004, Genes & development.

[30]  B. Turner,et al.  Differential underacetylation of histones H2A, H3 and H4 on the inactive X chromosome in human female cells , 1996, Human Genetics.

[31]  Zu-Wen Sun,et al.  Mitotic Phosphorylation of Histone H3 Is Governed by Ipl1/aurora Kinase and Glc7/PP1 Phosphatase in Budding Yeast and Nematodes , 2000, Cell.

[32]  P. Loidl.  A plant dialect of the histone language. , 2004, Trends in plant science.

[33]  M. Matzke,et al.  HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double‐stranded RNA , 2002, The EMBO journal.

[34]  E. Selker,et al.  A histone H3 methyltransferase controls DNA methylation in Neurospora crassa , 2001, Nature.

[35]  J. P. Jackson,et al.  Requirement of CHROMOMETHYLASE3 for Maintenance of CpXpG Methylation , 2001, Science.

[36]  D. Geelen,et al.  Identification and Dynamics of Two Classes of Aurora-Like Kinases in Arabidopsis and Other Plantsw⃞ , 2005, The Plant Cell Online.

[37]  H. Erdjument-Bromage,et al.  Histone demethylation by a family of JmjC domain-containing proteins , 2006, Nature.

[38]  M. Krangel,et al.  A role for histone acetylation in the developmental regulation of VDJ recombination. , 2000, Science.

[39]  I. Leitch,et al.  Nuclear DNA amounts in angiosperms: progress, problems and prospects. , 2005, Annals of botany.

[40]  Berend Snijder,et al.  The Arabidopsis LHP1 protein is a component of euchromatin , 2005, Planta.

[41]  Xiaofeng Cao,et al.  Interplay between Two Epigenetic Marks DNA Methylation and Histone H3 Lysine 9 Methylation , 2002, Current Biology.

[42]  A. Probst,et al.  Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[43]  T. James,et al.  Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene , 1986, Molecular and cellular biology.

[44]  Jesse J. Lipp,et al.  Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin , 2005, Nature.

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

[46]  J. Martens,et al.  Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. , 2003, Molecular cell.

[47]  N. Belyaev,et al.  Histone H4 acetylation in plant heterochromatin is altered during the cell cycle , 1997, Chromosoma.

[48]  S. Jacobsen,et al.  Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Ken-ichi Noma,et al.  Transitions in Distinct Histone H3 Methylation Patterns at the Heterochromatin Domain Boundaries , 2001, Science.

[50]  Danny Reinberg,et al.  A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. , 2004, Genes & development.

[51]  B. Turner,et al.  Duplication and Maintenance of Heterochromatin Domains , 1999, The Journal of cell biology.

[52]  E. Finnegan,et al.  Plant DNA methyltransferases , 2000, Plant Molecular Biology.

[53]  R. Doerge,et al.  Reversible Histone Acetylation and Deacetylation Mediate Genome-Wide, Promoter-Dependent and Locus-Specific Changes in Gene Expression During Plant Development , 2005, Genetics.

[54]  P. Mourrain,et al.  Arabidopsis Histone Deacetylase HDA6 Is Required for Maintenance of Transcriptional Gene Silencing and Determines Nuclear Organization of rDNA Repeats , 2004, The Plant Cell Online.

[55]  K. Ríha,et al.  Histone H4 Underacetylation in Plant Facultative Heterochromatin , 1998, Biological chemistry.

[56]  Beatrix Ueberheide,et al.  Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. , 2003, Molecular cell.

[57]  B. Turner,et al.  Euchromatic domains in plant chromosomes as revealed by H4 histone acetylation and early DNA replication. , 1999, Genome.

[58]  N. Brockdorff,et al.  Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. , 2003, Developmental cell.

[59]  R. Jaenisch,et al.  Development: DNA methylation in Drosophila melanogaster , 2000, Nature.

[60]  François Fuks,et al.  DNA methylation and histone modifications: teaming up to silence genes. , 2005, Current opinion in genetics & development.

[61]  U. Preuss,et al.  Novel mitosis-specific phosphorylation of histone H3 at Thr11 mediated by Dlk/ZIP kinase. , 2003, Nucleic acids research.

[62]  C. Peterson,et al.  Histones and histone modifications , 2004, Current Biology.

[63]  S. Dimitrov,et al.  Phosphorylation of serine 10 in histone H3, what for? , 2003, Journal of Cell Science.

[64]  Lianna Johnson,et al.  Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana , 2004, Chromosoma.

[65]  B. Strahl,et al.  Methylation of Histone H3 Lysine 36 Is Required for Normal Development in Neurospora crassa , 2005, Eukaryotic Cell.

[66]  D. Zink,et al.  Comparative analysis of the functional genome architecture of animal andplant cell nuclei , 2004, Chromosome Research.

[67]  M. Inagaki,et al.  Identification of a Novel Phosphorylation Site on Histone H3 Coupled with Mitotic Chromosome Condensation* , 1999, The Journal of Biological Chemistry.

[68]  G. Schotta,et al.  Trilogies of histone lysine methylation as epigenetic landmarks of the eukaryotic genome. , 2004, Cold Spring Harbor symposia on quantitative biology.

[69]  A. Meister,et al.  Methylation of histone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. , 2003, The Plant journal : for cell and molecular biology.

[70]  D. Moazed,et al.  Heterochromatin and Epigenetic Control of Gene Expression , 2003, Science.

[71]  W. Z. Cande,et al.  Phosphorylation of histone H3 is correlated with changes in the maintenance of sister chromatid cohesion during meiosis in maize, rather than the condensation of the chromatin. , 2000, Journal of cell science.

[72]  G. Blobel,et al.  Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. , 2005, Molecular cell.

[73]  C. Allis,et al.  Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa , 2003, Nature Genetics.

[74]  E. Selker,et al.  HP1 is essential for DNA methylation in neurospora. , 2004, Molecular cell.

[75]  J. Mata,et al.  Methylation of Histone H4 Lysine 20 Controls Recruitment of Crb2 to Sites of DNA Damage , 2004, Cell.

[76]  M. Osley,et al.  Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae , 2005, Nature.

[77]  B M Turner,et al.  Histone acetylation and an epigenetic code. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[78]  C. Allis,et al.  Follicle-stimulating Hormone Stimulates Protein Kinase A-mediated Histone H3 Phosphorylation and Acetylation Leading to Select Gene Activation in Ovarian Granulosa Cells* , 2001, The Journal of Biological Chemistry.

[79]  R. Dawe,et al.  Phosphoserines on Maize CENTROMERIC HISTONE H3 and Histone H3 Demarcate the Centromere and Pericentromere during Chromosome Segregation , 2005, The Plant Cell Online.

[80]  T. Rutten,et al.  Alterations in the distribution of histone H3 phosphorylation in mitotic plant chromosomes in response to cold treatment and the protein phosphatase inhibitor cantharidin , 2004, Chromosome Research.

[81]  B. Turner,et al.  The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression , 1993, Cell.

[82]  P. Loidl,et al.  Histone acetylation: lessons from the plant kingdom. , 2001, Trends in plant science.

[83]  P. Sassone-Corsi,et al.  Analysis of histone phosphorylation: coupling intracellular signaling to chromatin remodeling. , 2004, Methods in enzymology.

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

[85]  R. Martienssen,et al.  Arabidopsis thaliana DNA methylation mutants. , 1993, Science.

[86]  G. Karpen,et al.  Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin , 2004, Nature Structural &Molecular Biology.

[87]  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.

[88]  Jun Qin,et al.  Involvement of the TIP60 Histone Acetylase Complex in DNA Repair and Apoptosis , 2000, Cell.

[89]  M. Kozubek,et al.  Nuclear levels and patterns of histone H3 modification and HP1 proteins after inhibition of histone deacetylases , 2005, Journal of Cell Science.

[90]  Thomas Cremer,et al.  Nuclear Organization of Mammalian Genomes , 1999, The Journal of cell biology.

[91]  E. Heard.  Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. , 2005, Current opinion in genetics & development.

[92]  J. Paszkowski,et al.  Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis , 2003, Nature Genetics.

[93]  Tony Kouzarides,et al.  Crosstalk between CARM1 Methylation and CBP Acetylation on Histone H3 , 2002, Current Biology.

[94]  J. Friesner,et al.  Ionizing radiation-dependent gamma-H2AX focus formation requires ataxia telangiectasia mutated and ataxia telangiectasia mutated and Rad3-related. , 2005, Molecular biology of the cell.

[95]  Rieko Furushima-Shimogawara,et al.  Short communication: the cell cycle dependent phosphorylation of histone H3 is correlated with the condensation of plant mitotic chromosomes , 1999, The Plant journal : for cell and molecular biology.

[96]  Zu-Wen Sun,et al.  Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast , 2002, Nature.

[97]  C. Allis,et al.  Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. , 2000, Molecular cell.

[98]  S. Grewal,et al.  Ubiquitin ligase component Cul4 associates with Clr4 histone methyltransferase to assemble heterochromatin , 2005, Nature Cell Biology.

[99]  Steven E. Jacobsen,et al.  Gardening the genome: DNA methylation in Arabidopsis thaliana , 2005, Nature Reviews Genetics.

[100]  S. Grewal,et al.  Histone H3 K36 Methylation Is Associated with Transcription Elongation in Schizosaccharomyces pombe , 2005, Eukaryotic Cell.

[101]  T. Jenuwein,et al.  Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis , 2005, The EMBO journal.

[102]  A. Kelley,et al.  Loss of Drosophila borealin causes polyploidy, delayed apoptosis and abnormal tissue development , 2005, Development.

[103]  S. Jacobsen,et al.  DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis , 2002, The EMBO journal.

[104]  C. Allis,et al.  Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. , 1998, Journal of cell science.

[105]  B. Turner,et al.  Histone H4 Acetylation of Euchromatin and Heterochromatin Is Cell Cycle Dependent and Correlated with Replication Rather Than with Transcription , 2000, Plant Cell.