Role of histone modifications in defining chromatin structure and function

Abstract Chromosomes in eukaryotic cell nuclei are not uniformly organized, but rather contain distinct chromatin elements, with each state having a defined biochemical structure and biological function. These are recognizable by their distinct architectures and molecular components, which can change in response to cellular stimuli or metabolic requirements. Chromatin elements are characterized by the fundamental histone and DNA components, as well as other associated non-histone proteins and factors. Post-translational modifications of histone proteins in particular often correlate with a specific chromatin structure and function. Patterns of histone modifications are implicated as having a role in directing the level of chromatin compaction, as well as playing roles in multiple functional pathways directing the readout of distinct regions of the genome. We review the properties of various chromatin elements and the apparent links of histone modifications with chromatin organization and functional output.

[1]  Wolfgang Fischle,et al.  Structural basis for lower lysine methylation state-specific readout by MBT repeats of L3MBTL1 and an engineered PHD finger. , 2007, Molecular cell.

[2]  C. Allis,et al.  DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA , 2007, Nature.

[3]  J. Zeitlinger,et al.  Polycomb complexes repress developmental regulators in murine embryonic stem cells , 2006, Nature.

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

[5]  Michael Grunstein,et al.  Genome-wide patterns of histone modifications in yeast , 2006, Nature Reviews Molecular Cell Biology.

[6]  Thomas A. Milne,et al.  WDR5 Associates with Histone H3 Methylated at K4 and Is Essential for H3 K4 Methylation and Vertebrate Development , 2005, Cell.

[7]  Malgorzata Schelder,et al.  DNA-binding and selective methyl-lysine-binding activities A Polycomb group protein complex with sequence-specific Material Supplemental , 2006 .

[8]  Michael Grunstein,et al.  Sir2 deacetylates histone H3 lysine 56 to regulate telomeric heterochromatin structure in yeast. , 2007, Molecular cell.

[9]  Kristian Helin,et al.  Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. , 2006, Genes & development.

[10]  K. Luger,et al.  A charged and contoured surface on the nucleosome regulates chromatin compaction , 2007, Nature Structural &Molecular Biology.

[11]  I B Dawid,et al.  The bromodomain: a conserved sequence found in human, Drosophila and yeast proteins. , 1992, Nucleic acids research.

[12]  Steven J Altschuler,et al.  Genomic characterization reveals a simple histone H4 acetylation code. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[13]  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.

[14]  Jun S. Song,et al.  High-throughput mapping of the chromatin structure of human promoters , 2007, Nature Biotechnology.

[15]  C. Pabo,et al.  Gene-Specific Targeting of H3K9 Methylation Is Sufficient for Initiating Repression In Vivo , 2002, Current Biology.

[16]  J. Ausió,et al.  H2A.Bbd: a quickly evolving hypervariable mammalian histone that destabilizes nucleosomes in an acetylation‐independent way , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[17]  B. Garcia,et al.  Organismal Differences in Post-translational Modifications in Histones H3 and H4* , 2007, Journal of Biological Chemistry.

[18]  D. Clark,et al.  Mapping histone modifications by nucleosome immunoprecipitation. , 2006, Methods in enzymology.

[19]  S. Khorasanizadeh,et al.  Double chromodomains cooperate to recognize the methylated histone H3 tail , 2005, Nature.

[20]  J H Waterborg,et al.  Dynamics of histone acetylation in Saccharomyces cerevisiae. , 2001, Biochemistry.

[21]  Christopher J. Oldfield,et al.  Intrinsically disordered protein. , 2001, Journal of molecular graphics & modelling.

[22]  Megan F. Cole,et al.  Genome-wide Map of Nucleosome Acetylation and Methylation in Yeast , 2005, Cell.

[23]  Karl Mechtler,et al.  Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins , 2001, Nature.

[24]  N. Friedman,et al.  Single-Nucleosome Mapping of Histone Modifications in S. cerevisiae , 2005, PLoS biology.

[25]  V. Uversky Intrinsically Disordered Proteins , 2000 .

[26]  R. Paro,et al.  A sequence motif found in a Drosophila heterochromatin protein is conserved in animals and plants. , 1991, Nucleic acids research.

[27]  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.

[28]  Brian D. Strahl,et al.  Identification of Histone H3 Lysine 36 Acetylation as a Highly Conserved Histone Modification* , 2007, Journal of Biological Chemistry.

[29]  H. Stunnenberg,et al.  Histone modification patterns associated with the human X chromosome , 2006, EMBO reports.

[30]  G. Cross,et al.  Unusual histone modifications in Trypanosoma brucei , 2006, FEBS letters.

[31]  Thomas A. Milne,et al.  A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling , 2006, Nature.

[32]  Dustin E. Schones,et al.  High-Resolution Profiling of Histone Methylations in the Human Genome , 2007, Cell.

[33]  Louise Fairall,et al.  EM measurements define the dimensions of the "30-nm" chromatin fiber: evidence for a compact, interdigitated structure. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Yi Zhang,et al.  Tudor, MBT and chromo domains gauge the degree of lysine methylation , 2006, EMBO reports.

[35]  T. Kouzarides Chromatin Modifications and Their Function , 2007, Cell.

[36]  T. Richmond,et al.  Nucleosome Arrays Reveal the Two-Start Organization of the Chromatin Fiber , 2004, Science.

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

[38]  D. Reinberg,et al.  L3MBTL1, a Histone-Methylation-Dependent Chromatin Lock , 2007, Cell.

[39]  Wolfgang Fischle,et al.  Binary switches and modification cassettes in histone biology and beyond , 2003, Nature.

[40]  Tony Kouzarides,et al.  Histone H3 Lysine 4 Methylation Disrupts Binding of Nucleosome Remodeling and Deacetylase (NuRD) Repressor Complex* , 2002, The Journal of Biological Chemistry.

[41]  Grant W. Brown,et al.  Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map , 2007, Nature.

[42]  Yi Zhang,et al.  Recognition of Histone H3 Lysine-4 Methylation by the Double Tudor Domain of JMJD2A , 2006, Science.

[43]  G. Almouzni,et al.  Marking histone H3 variants: how, when and why? , 2007, Trends in biochemical sciences.

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

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

[46]  H. Sass,et al.  The Drosophila melanogaster tumor suppressor gene lethal(3)malignant brain tumor encodes a proline-rich protein with a novel zinc finger , 1995, Mechanisms of Development.

[47]  William Stafford Noble,et al.  Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project , 2007, Nature.

[48]  Tamar Schlick,et al.  Role of histone tails in chromatin folding revealed by a mesoscopic oligonucleosome model , 2006, Proceedings of the National Academy of Sciences.

[49]  Thomas Ried,et al.  From Silencing to Gene Expression Real-Time Analysis in Single Cells , 2004, Cell.

[50]  D. Tremethick,et al.  The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression , 2007, Nature Structural &Molecular Biology.

[51]  T. Mikkelsen,et al.  Genome-wide maps of chromatin state in pluripotent and lineage-committed cells , 2007, Nature.

[52]  A. Shilatifard,et al.  Covalent modifications of histones during development and disease pathogenesis , 2007, Nature Structural &Molecular Biology.

[53]  T. Richmond,et al.  Chromatin fiber folding: requirement for the histone H4 N-terminal tail. , 2003, Journal of molecular biology.

[54]  A. Benecke,et al.  Chromatin code, local non-equilibrium dynamics, and the emergence of transcription regulatory programs , 2006, The European physical journal. E, Soft matter.

[55]  D. Tremethick,et al.  Higher-Order Structures of Chromatin: The Elusive 30 nm Fiber , 2007, Cell.

[56]  A. Cashmore,et al.  HAT3.1, a novel Arabidopsis homeodomain protein containing a conserved cysteine-rich region. , 1993, The Plant journal : for cell and molecular biology.

[57]  James A. Cuff,et al.  A Bivalent Chromatin Structure Marks Key Developmental Genes in Embryonic Stem Cells , 2006, Cell.

[58]  Charles Kooperberg,et al.  The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. , 2004, Genes & development.

[59]  B. Sarg,et al.  Histone H4-Lysine 20 Monomethylation Is Increased in Promoter and Coding Regions of Active Genes and Correlates with Hyperacetylation* , 2005, Journal of Biological Chemistry.

[60]  Saeed Tavazoie,et al.  Mapping Global Histone Acetylation Patterns to Gene Expression , 2004, Cell.

[61]  A. West,et al.  Insulators and boundaries: versatile regulatory elements in the eukaryotic genome. , 2001, Science.

[62]  Keji Zhao,et al.  Genome-wide prediction of conserved and nonconserved enhancers by histone acetylation patterns. , 2006, Genome research.

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

[64]  Irene K. Moore,et al.  A genomic code for nucleosome positioning , 2006, Nature.

[65]  Lani F. Wu,et al.  Genome-Scale Identification of Nucleosome Positions in S. cerevisiae , 2005, Science.

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

[67]  Kami Ahmad,et al.  Rules and regulation in the primary structure of chromatin. , 2007, Current opinion in cell biology.

[68]  J. M. Lee,et al.  Locus-specific variation in phosphorylation state of RNA polymerase II in vivo: correlations with gene activity and transcript processing. , 1993, Genes & development.

[69]  Charles Kooperberg,et al.  Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing , 2002, Nature Genetics.

[70]  M. Pazin,et al.  Histone H4-K16 Acetylation Controls Chromatin Structure and Protein Interactions , 2006, Science.

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

[72]  J. Hayes,et al.  Detection of interactions between nucleosome arrays mediated by specific core histone tail domains. , 2007, Methods.

[73]  Megan F. Cole,et al.  Control of Developmental Regulators by Polycomb in Human Embryonic Stem Cells , 2006, Cell.

[74]  J. Hansen,et al.  Chromatin architectural proteins , 2006, Chromosome Research.

[75]  Cory M. Valley,et al.  Chromosome-wide, allele-specific analysis of the histone code on the human X chromosome. , 2006, Human molecular genetics.

[76]  Michael Grunstein,et al.  Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin , 2002, Nature Genetics.

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

[78]  S. Henikoff,et al.  The HP1 chromo shadow domain binds a consensus peptide pentamer , 2000, Current Biology.

[79]  D. Reinberg,et al.  PR-Set7-dependent methylation of histone H4 Lys 20 functions in repression of gene expression and is essential for mitosis. , 2005, Genes & development.

[80]  R. Kamakaka,et al.  Braking the silence: how heterochromatic gene repression is stopped in its tracks. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.