Structural basis of HP1/PXVXL motif peptide interactions and HP1 localisation to heterochromatin

EMBO Journal

Volumn 23, Issue 3, 2004, Pages 489-499

  Thiru, Abarna ^a   Nietlispach, Daniel ^a   Mott, Helen R ^a   Okuwaki, Mitsuru ^b   Lyon, Debbie ^b   Nielsen, Peter R ^a   Hirshberg, Miriam ^a   Verreault, Alain ^b   Murzina, Natalia V ^a   Laue, Ernest D ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Chromatin localisation; Chromo domain; Heterochromatin; Heterochromatin protein 1; NMR spectroscopy; Protein structure

Indexed keywords

ADAPTOR PROTEIN; HETEROCHROMATIN PROTEIN 1; HISTONE H3; LYSINE; MONOMER; PEPTIDE; PROTEIN PXVXL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BETA SHEET; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; COMPLEX FORMATION; DIMERIZATION; GENE SILENCING; HETEROCHROMATIN; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTEIN TARGETING; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHROMOSOMAL PROTEINS, NON-HISTONE; HETEROCHROMATIN; HISTONES; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

ANIMALIA;

EID: 10744228652     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600088     Document Type: Article

References (55)

1. Aasland R, Stewart AF (1995) The chromo shadow domain, a second chromo domain in heterochromatin-binding protein 1, HP1. Nucleic Acids Res 23: 3168-3174
2. Ball LJ, Murzina NV, Broadhurst RW, Raine AR, Archer SJ, Stott FJ, Murzin AG, Singh PB, Domaille PJ, Laue ED (1997) Structure of the chromatin binding (chromo) domain from mouse modifier protein 1. EMBO J 16: 2473-2481
3. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120-124
4. Brasher SV, Smith BO, Fogh RH, Nietlispach D, Thiru A, Nielsen PR, Broadhurst RW, Ball LJ, Murzina NV, Laue ED (2000) The structure of mouse HP1 suggests a unique mode of single peptide recognition by the shadow chromo domain dimer. EMBO J 19: 1587-1597
5. Brown KE, Baxter J, Graf D, Merkenschlager M, Fisher AG (1999) Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol Cell 3: 207-217
6. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D 54: 905-921
7. Cammas F, Oulad-Abdelghani M, Vonesch JL, Huss-Garcia Y, Chambon P, Losson R (2002) Cell differentiation induces TIF1beta association with centromeric heterochromatin via an HP1 interaction. J Cell Sci 115: 3439-3448
8. Cavanagh J, Fairbrother WJ, Palmer AG, Skelton NJ (1996) Protein NMR Spectroscopy Principles and Practice. Academic Press Inc.: London, UK
9. Cheutin T, McNairn AJ, Jenuwein T, Gilbert DM, Singh PB, Misteli T (2003) Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science 299: 721-725
10. Cowieson NP, Partridge JF, Allshire RC, McLaughlin PJ (2000) Dimerisation of a chromo shadow domain and distinctions from the chromodomain as revealed by structural analysis. Curr Biol 10: 517-525
11. Cryderman DE, Cuaycong MH, Elgin SCR, Wallrath LL (1998) Characterization of sequences associated with position-effect variegation at pericentric sites in D. melanogaster heterochromatin. Chromosoma 107: 277-285
12. Cryderman DE, Tang H, Bell C, Gilmour DS, Wallrath LL (1999) Heterochromatic silencing of D. melanogaster heat shock genes acts at the level of promoter potentiation. Nucleic Acids Res 27: 3364-3370
13. Eissenberg JC, Elgin SC (2000) The HP1 protein family: getting a grip on chromatin. Curr Opin Genet Dev 10: 204-210
14. Epstein H, James TC, Singh PB (1992) Cloning and expression of D. melanogaster HP1 homologs from a mealybug, Planococcus citri. J Cell Sci 101: 463-474
15. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, Khorasanizadeh S (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17: 1870-1881
16. Francastel C, Walters MC, Groudine M, Martin DI (1999) A functional enhancer suppresses silencing of a transgene and prevents its localization close to centrometric heterochromatin. Cell 99: 259-269
17. Gaillard PH, Martini EM, Kaufman PD, Stillman B, Moustacchi E, Almouzni G (1996) Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell 86: 887-896
18. Hall IM, Shankaranarayana GD, Noma K, Ayoub N, Cohen A, Grewal SI (2002) Establishment and maintenance of a heterochromatin domain. Science 297: 2232-2237
19. Hwang KK, Eissenberg JC, Worman HJ (2001) Transcriptional repression of euchromatic genes by D. melanogaster heterochromatin protein 1 and histone modifiers. Proc Natl Acad Sci USA 98: 11423-11427
20. Jacobs SA, Khorasanizadeh S (2002) Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295: 2080-2083
21. James TC, Elgin SC (1986) Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol 6: 3862-3872
22. Jenuwein T (2002) Molecular biology. An RNA-guided pathway for the epigenome. Science 297: 2215-2218
23. Kaufman PD, Kobayashi R, Kessler N, Stillman B (1995) The p150 and p60 subunits of chromatin assembly factor I: a molecular link between newly synthesized histones and DNA replication. Cell 81: 1105-1114
24. Koonin EV, Zhou S, Lucchesi JC (1995) The chromo superfamily: new members, duplication of the chromo domain and possible role in delivering transcription regulators to chromatin. Nucleic Acids Res 23: 4229-4233
25. Kraulis PJ (1989) ANSIG: a program for the assignment of protein 1 H 2D NMR spectra by interactive graphics. J Magn Reson 24: 627-633
26. Kraulis PJ, Domaille PJ, Campbell-Burk SL, Aken Tv, Laue ED (1994) Solution structure and dynamics of Ras p21.GDP determined by heteronuclear three- and four-dimensional NMR spectroscopy. Biochemistry 33: 3515-3531
27. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120
28. Lechner MS, Begg GE, Speicher DW, Rauscher III FJ (2000) Molecular determinants for targeting heterochromatin protein 1-mediated gene silencing: direct chromoshadow domain-KAP-1 corepressor interaction is essential. Mol Cell Biol 20: 6449-6465
29. LeDouarin B, Nielsen AL, Garnier JM, Ichinose H, Jeanmougin F, Losson R, Chambon P (1996) A possible involvement of TIF1 alpha and TIF1 beta in the epigenetic control of transcription by nuclear receptors. EMBO J 15: 6701-6715
30. Li Y, Kirschmann DA, Wallrath LL (2002) Does heterochromatin protein 1 always follow code? Proc Natl Acad Sci USA 31: 31
31. Linge JP, O'Donoghue SJ, Nilges M (2001) Automated assignment of ambiguous NOEs with ARIA. Methods Enzymol 339: 71-90
32. Lu BY, Emtage PC, Duyf BJ, Hilliker AJ, Eissenberg JC (2000) Heterochromatin protein 1 is required for the normal expression of two heterochromatin genes in D. melanogaster. Genetics 155: 699-708
33. Min J, Zhang Y, Xu RM (2003) Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev 17: 1823-1828
34. Minc E, Allory Y, Courvalin JC, Buendia B (2001) Immunolocalization of HP1 proteins in metaphasic mammalian chromosomes. Methods Cell Sci 23: 171-174
35. Minc E, Allory V, Worman HJ, Courvalin JC, Buendia B (1999) Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells. Chromosoma 108: 220-234
36. Minc E, Courvalin JC, Buendia B (2000) HP1gamma associates with euchromatin and heterochromatin in mammalian nuclei and chromosomes. Cytogenet Cell Genet 90: 279-284
37. Muchardt C, Guilleme M, Seeler JS, Trouche D, Dejean A, Yaniv M (2002) Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1alpha. EMBO Rep 3: 975-981
38. Murzina N, Verreault A, Laue E, Stillman B (1999) Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. Mol Cell 4: 1-20
39. Nielsen PR, Nietlispach D, Mott HR, Callaghan J, Bannister A, Kouzarides T, Murzin AG, Murzina NV, Laue ED (2002) Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9. Nature 416: 103-107
40. Noma K, Allis CD, Grewal SI (2001) Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293: 1150-1155
41. Paro R, Hogness DS (1991) The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of D. melanogaster. Proc Natl Acad Sci USA 88: 263-267
42. Pawson T, Gish GD, Nash P (2001) SH2 domains, interaction modules and cellular wiring. Trends Cell Biol 11: 504-511
43. Piacentini L, Fanti L, Berloco M, Perrini B, Pimpinelli S (2003) Heterochromatin protein 1 (HP1) is associated with induced gene expression in D. melanogaster euchromatin. J Cell Biol 161: 707-714
44. Platero JS, Hartnett T, Eissenberg JC (1995) Functional analysis of the chromo domain of HP1. EMBO J 14: 3977-3986
45. Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593-599
46. Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher III FJ (2002) SETDBI: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HPl-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 16: 919-932
47. Smith S, Stillman B (1989) Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58: 15-25
48. Smothers JF, Henikoff S (2000) The HP1 chromo shadow domain binds a consensus peptide pentamer. Curr Biol 10: 27-30
49. Smothers JF, Henikoff S (2001) The hinge and chromo shadow domain impart distinct targeting of HP1-like proteins. Mol Cell Biol 21: 2555-2569
50. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45
51. Vassallo MF, Tanese N (2002) Isoform-specific interaction of HP1 with human TAFII130. Proc Natl Acad Sci USA 99: 5919-5924
52. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297: 1833-1837
53. Wang G, Ma A, Chow CM, Horsley D, Brown NR, Cowell IG, Singh PB (2000) Conservation of heterochromatin protein 1 function. Mol Cell Biol 20: 6970-6983
54. Zhao T, Eissenberg JC (1999) Phosphorylation of heterochromatin protein 1 by casein kinase II is required for efficient heterochromatin binding in D. melanogaster. J Biol Chem 274: 15095-15100
55. Zwahlen C, Legault P, Vincent SJF, Greenblatt J, Konrat R, Kay LE (1997) Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage lambda N-peptide/boxB RNA complex. J Am Chem Soc 119: 6711-6721