HP1 and the dynamics of heterochromatin maintenance

Heterochromatin maintenance is crucial for the clonal inheritance of cell identity, to ensure the proper segregation of chromosomes and the regulation of gene expression. Although it is architecturally stable, heterochromatin has to be flexible to cope with disrupting events such as replication. Recent progress has shed light on the paradoxical properties of heterochromatin in the nucleus, and highlights the roles of heterochromatin protein-1 and, more unexpectedly, RNA molecules in heterochromatin maintenance.

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

[2]  P. Dollé,et al.  Transcripts from opposite strands of γ satellite DNA are differentially expressed during mouse development , 1995, Mammalian Genome.

[3]  E. Finnegan,et al.  The small RNA world , 2003, Journal of Cell Science.

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

[5]  N. Tommerup,et al.  Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene , 1999, Nature.

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

[7]  Ira M. Hall,et al.  Regulation of Heterochromatic Silencing and Histone H3 Lysine-9 Methylation by RNAi , 2002, Science.

[8]  R. Festenstein,et al.  Unravelling heterochromatin: competition between positive and negative factors regulates accessibility. , 2002, Trends in genetics : TIG.

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

[10]  R. Allshire,et al.  Hairpin RNAs and Retrotransposon LTRs Effect RNAi and Chromatin-Based Gene Silencing , 2003, Science.

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

[12]  B. Buendia,et al.  HP1γ associates with euchromatin and heterochromatin in mammalian nuclei and chromosomes , 2000, Cytogenetic and Genome Research.

[13]  Ira M. Hall,et al.  Establishment and Maintenance of a Heterochromatin Domain , 2002, Science.

[14]  S. Elgin,et al.  Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Mitzi I. Kuroda,et al.  Epigenetic Aspects of X-Chromosome Dosage Compensation , 2001, Science.

[16]  B. Turner,et al.  Transient Inhibition of Histone Deacetylation Alters the Structural and Functional Imprint at Fission Yeast Centromeres , 1997, Cell.

[17]  M. Matzke,et al.  RNA: Guiding Gene Silencing , 2001, Science.

[18]  R. Meehan,et al.  HP1 binding to native chromatin in vitro is determined by the hinge region and not by the chromodomain , 2003, The EMBO journal.

[19]  Alexey G. Murzin,et al.  Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9 , 2002, Nature.

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

[21]  P. Grandi,et al.  A CAF-1–PCNA-Mediated Chromatin Assembly Pathway Triggered by Sensing DNA Damage , 2000, Molecular and Cellular Biology.

[22]  Petr Svoboda,et al.  RNAi: mammalian oocytes do it without RNA-dependent RNA polymerase. , 2003, RNA.

[23]  P. Wade,et al.  WSTF–ISWI chromatin remodeling complex targets heterochromatic replication foci , 2002, The EMBO journal.

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

[25]  A. Pombo,et al.  Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  D. Haber,et al.  DNA Methyltransferases Dnmt3a and Dnmt3b Are Essential for De Novo Methylation and Mammalian Development , 1999, Cell.

[27]  Karl Mechtler,et al.  Loss of the Suv39h Histone Methyltransferases Impairs Mammalian Heterochromatin and Genome Stability , 2001, Cell.

[28]  D. Kioussis,et al.  Modulation of Heterochromatin Protein 1 Dynamics in Primary Mammalian Cells , 2003, Science.

[29]  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.

[30]  S. Henikoff,et al.  The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. , 2002, Molecular cell.

[31]  Robin C. Allshire,et al.  Dimerisation of a chromo shadow domain and distinctions from the chromodomain as revealed by structural analysis , 2000, Current Biology.

[32]  S. Eddy.  Non–coding RNA genes and the modern RNA world , 2001, Nature Reviews Genetics.

[33]  F. Jeanmougin,et al.  A possible involvement of TIF1 alpha and TIF1 beta in the epigenetic control of transcription by nuclear receptors. , 1996, The EMBO journal.

[34]  A. Murzin,et al.  Structure of the chromatin binding (chromo) domain from mouse modifier protein 1 , 1997, The EMBO journal.

[35]  A. Wolffe,et al.  DNA replication in vitro erases a Xenopus 5S RNA gene transcription complex , 1986, Cell.

[36]  A. Bird,et al.  Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Mark Groudine,et al.  A Functional Enhancer Suppresses Silencing of a Transgene and Prevents Its Localization Close to Centromeric Heterochromatin , 1999, Cell.

[38]  Taddel Angela,et al.  Reversible Disruption of pericentric Heterochromatin and Centromere Function by Inhibiting Deacetylases , 2001 .

[39]  S. Jacobs,et al.  Structure of HP1 Chromodomain Bound to a Lysine 9-Methylated Histone H3 Tail , 2002, Science.

[40]  P. Chambon,et al.  Selective interaction between the chromatin‐remodeling factor BRG1 and the heterochromatin‐associated protein HP1α , 2002, The EMBO journal.

[41]  P. Avner,et al.  X-chromosome inactivation: counting, choice and initiation , 2001, Nature Reviews Genetics.

[42]  J. Wu,et al.  Disruption of the nucleosomes at the replication fork. , 1993, The EMBO journal.

[43]  P. Chambon,et al.  Heterochromatin formation in mammalian cells: interaction between histones and HP1 proteins. , 2001, Molecular cell.

[44]  S. Henikoff.  Position-effect variegation after 60 years. , 1990, Trends in genetics : TIG.

[45]  T. Kouzarides,et al.  The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. , 2003, Nucleic acids research.

[46]  B. Stillman,et al.  Replication-Dependent Marking of DNA by PCNA Facilitates CAF-1-Coupled Inheritance of Chromatin , 1999, Cell.

[47]  Gary H. Karpen,et al.  Determining centromere identity: cyclical stories and forking paths , 2001, Nature Reviews Genetics.

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

[49]  G. Storz.  An Expanding Universe of Noncoding RNAs , 2002, Science.

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

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

[52]  Ira M. Hall,et al.  RNA interference machinery regulates chromosome dynamics during mitosis and meiosis in fission yeast , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[54]  A. Protopopov,et al.  mSin3-associated protein, mSds3, is essential for pericentric heterochromatin formation and chromosome segregation in mammalian cells. , 2003, Genes & development.

[55]  En Li,et al.  Suv 39 h-Mediated Histone H 3 Lysine 9 Methylation Directs DNA Methylation to Major Satellite Repeats at Pericentric Heterochromatin , 2003 .

[56]  Michael Q. Zhang,et al.  The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. , 2002, Genes & development.

[57]  T. Yamada,et al.  Human homolog of Drosophila heterochromatin-associated protein 1 (HP1) is a DNA-binding protein which possesses a DNA-binding motif with weak similarity to that of human centromere protein C (CENP-C). , 1996, Journal of biochemistry.

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

[59]  T. Jenuwein,et al.  Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component , 2002, Nature Genetics.

[60]  A. Dejean,et al.  Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1α , 2002, EMBO reports.

[61]  B. Reinhart,et al.  Small RNAs Correspond to Centromere Heterochromatic Repeats , 2002, Science.

[62]  G. Almouzni,et al.  The ins and outs of nucleosome assembly. , 2001, Current opinion in genetics & development.

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

[64]  B. Stillman,et al.  Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. , 1999, Molecular cell.

[65]  S. Elgin,et al.  Distribution patterns of HP1, a heterochromatin-associated nonhistone chromosomal protein of Drosophila. , 1989, European journal of cell biology.

[66]  T. Misteli.  The concept of self-organization in cellular architecture , 2001, The Journal of cell biology.

[67]  K. Robertson.  DNA methylation and chromatin – unraveling the tangled web , 2002, Oncogene.

[68]  B. Vissel,et al.  Mouse major (gamma) satellite DNA is highly conserved and organized into extremely long tandem arrays: implications for recombination between nonhomologous chromosomes. , 1989, Genomics.

[69]  R. Martienssen,et al.  Maintenance of heterochromatin by RNA interference of tandem repeats , 2003, Nature Genetics.

[70]  G. Almouzni,et al.  Maintenance of nucleolar machineries and pre-rRNAs in remnant nucleolus of erythrocyte nuclei and remodeling in Xenopus egg extracts. , 2001, Experimental cell research.

[71]  W. Filipowicz,et al.  Specific interference with gene expression induced by long, double-stranded RNA in mouse embryonal teratocarcinoma cell lines , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[72]  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.

[73]  Songtao Jia,et al.  RNAi-Mediated Targeting of Heterochromatin by the RITS Complex , 2004, Science.

[74]  B. Turner,et al.  Antibodies to defined histone epitopes reveal variations in chromatin conformation and underacetylation of centric heterochromatin in human metaphase chromosomes , 1992, Chromosoma.

[75]  D. Kirschmann,et al.  Does heterochromatin protein 1 always follow code? , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[76]  B. Turner,et al.  Cellular Memory and the Histone Code , 2002, Cell.

[77]  D. Zink,et al.  Chromodomains are protein–RNA interaction modules , 2000, Nature.

[78]  N. Brockdorff,et al.  Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin , 2002, Nature Genetics.

[79]  T. Volpe,et al.  RNA interference is required for normal centromere function infission yeast , 2004, Chromosome Research.

[80]  A. Fisher,et al.  Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. , 1999, Molecular cell.

[81]  Steven Henikoff,et al.  Epigenetic Consequences of Nucleosome Dynamics , 2002, Cell.

[82]  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.

[83]  Brian O. Smith,et al.  The structure of mouse HP1 suggests a unique mode of single peptide recognition by the shadow chromo domain dimer , 2000, The EMBO journal.

[84]  Tom Misteli,et al.  Maintenance of Stable Heterochromatin Domains by Dynamic HP1 Binding , 2003, Science.

[85]  Youngchang Kim,et al.  Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. , 2003, Genes & development.

[86]  Andrew J. Bannister,et al.  Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain , 2001, Nature.

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

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

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

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

[91]  James Allan,et al.  Formation of facultative heterochromatin in the absence of HP1 , 2003, The EMBO journal.

[92]  S. Henikoff,et al.  Maintenance of chromatin states: an open-and-shut case. , 2003, Current opinion in cell biology.

[93]  R. Poot,et al.  An ACF1–ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin , 2002, Nature Genetics.

[94]  Prim B. Singh,et al.  Mammalian chromodomain proteins: their role in genome organisation and expression. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[95]  Phillip D Zamore,et al.  Ancient Pathways Programmed by Small RNAs , 2002, Science.