HP1a Recruitment to Promoters Is Independent of H3K9 Methylation in Drosophila melanogaster

PLoS Genetics

Volumn 8, Issue 11, 2012, Pages

  Figueiredo, Margarida L A ^a   Philip, Philge ^a   Stenberg, Per ^a   Larsson, Jan ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; HETEROCHROMATIN PROTEIN 1; HETEROCHROMATIN PROTEIN 1A; HETEROCHROMATIN PROTEIN 2; HISTONE H3; HISTONE H3 LYSINE 9; HISTONE LYSINE METHYLTRANSFERASE; HISTONE LYSINE METHYLTRANSFERASE G9A; HISTONE LYSINE METHYLTRANSFERASE SETDB1; HISTONE LYSINE METHYLTRANSFERASE SU(VAR) 3 9; NUCLEAR PROTEIN; PAINTING OF FOURTH PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

2L 31 REGION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CHROMOSOME 4; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EUCHROMATIC REGION; GENE EXPRESSION; GENETIC PARAMETERS; HISTONE METHYLATION; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PERICENTROMERIC REGION; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN MOTIF; SENSITIVITY ANALYSIS; WILD TYPE;

ANIMALS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE SILENCING; HETEROCHROMATIN; HISTONE DEMETHYLASES; HISTONES; METHYLATION; METHYLTRANSFERASES; PROMOTER REGIONS, GENETIC;

DROSOPHILA MELANOGASTER;

EID: 84870665542     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003061     Document Type: Article

References (82)

1. Eissenberg JC, Reuter G, (2009) Cellular mechanism for targeting heterochromatin formation in Drosophila. Int Rev Cell Mol Biol 273: 1-47.
2. Filion GJ, van Bemmel JG, Braunschweig U, Talhout W, Kind J, et al. (2010) Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143: 212-224.
3. Yoon J, Lee KS, Park JS, Yu K, Paik SG, et al. (2008) dSETDB1 and SU(VAR)3-9 sequentially function during germline-stem cell differentiation in Drosophila melanogaster. PLoS ONE 3: e2234 doi:10.1371/journal.pone.0002234.
4. Clough E, Moon W, Wang S, Smith K, Hazelrigg T, (2007) Histone methylation is required for oogenesis in Drosophila. Development 134: 157-165.
5. Koch CM, Honemann-Capito M, Egger-Adam D, Wodarz A, (2009) Windei, the Drosophila homolog of mAM/MCAF1, is an essential cofactor of the H3K9 methyl transferase dSETDB1/Eggless in germ line development. PLoS Genet 5: e1000644 doi:10.1371/journal.pgen.1000644.
6. Seum C, Bontron S, Reo E, Delattre M, Spierer P, (2007) Drosophila G9a is a nonessential gene. Genetics 177: 1955-1957.
7. Brower-Toland B, Riddle NC, Jiang H, Huisinga KL, Elgin SC, (2009) Multiple SET methyltransferases are required to maintain normal heterochromatin domains in the genome of Drosophila melanogaster. Genetics 181: 1303-1319.
8. Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, et al. (2002) Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J 21: 1121-1131.
9. Stabell M, Eskeland R, Bjørkmo M, Larsson J, Aalen RB, et al. (2006) The Drosophila G9a gene encodes a multi-catalytic histone methyltransferase required for normal development. Nucleic Acids Res 34: 4609-4621.
10. Ebert A, Schotta G, Lein S, Kubicek S, Krauss V, et al. (2004) Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev 18: 2973-2983.
11. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, et al. (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185-196.
12. Seum C, Reo E, Peng H, Rauscher FJ, Spierer P, et al. (2007) Drosophila SETDB1 is required for chromosome 4 silencing. PLoS Genet 3: e76 doi:10.1371/journal.pgen.0030076.
13. Tzeng TY, Lee CH, Chan LW, Shen CK, (2007) Epigenetic regulation of the Drosophila chromosome 4 by the histone H3K9 methyltransferase dSETDB1. Proc Natl Acad Sci U S A 104: 12691-12696.
14. Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, et al. (2011) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471: 480-485.
15. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, et al. (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120-124.
16. 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.
17. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI, (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292: 110-113.
18. Jacobs SA, Khorasanizadeh S, (2002) Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295: 2080-2083.
19. Vermaak D, Malik HS, (2009) Multiple roles for heterochromatin protein 1 genes in Drosophila. Annu Rev Genet 43: 467-492.
20. Zhao T, Heyduk T, Allis CD, Eissenberg JC, (2000) Heterochromatin protein 1 binds to nucleosomes and DNA in vitro. J Biol Chem 275: 28332-28338.
21. Billur M, Bartunik HD, Singh PB, (2010) The essential function of HP1β: a case of the tail wagging the dog? Trends Biochem Sci 35: 115-123.
22. Dialynas GK, Makatsori D, Kourmouli N, Theodoropoulos PA, McLean K, et al. (2006) Methylation-independent binding to histone H3 and cell cycle-dependent incorporation of HP1β into heterochromatin. J Biol Chem 281: 14350-14360.
23. Nielsen AL, Oulad-Abdelghani M, Ortiz JA, Remboutsika E, Chambon P, et al. (2001) Heterochromatin formation in mammalian cells: interaction between histones and HP1 proteins. Mol Cell 7: 729-739.
24. Lavigne M, Eskeland R, Azebi S, Saint-André V, Jang SM, et al. (2009) Interaction of HP1 and Brg1/Brm with the globular domain of histone H3 is required for HP1-mediated repression. PLoS Genet 5: e1000769 doi:10.1371/journal.pgen.1000769.
25. Haddrill PR, Waldron FM, Charlesworth B, (2008) Elevated levels of expression associated with regions of the Drosophila genome that lack crossing over. Biol Lett 4: 758-761.
26. Johansson AM, Stenberg P, Allgardsson A, Larsson J, (2012) POF regulates the expression of genes on the 4th chromosome in D. melanogaster by binding to nascent RNA. Mol Cell Biol doi:10.1128/MCB.06622-11.
27. Johansson AM, Stenberg P, Bernhardsson C, Larsson J, (2007) Painting of fourth and chromosome-wide regulation of the 4th chromosome in Drosophila melanogaster. EMBO J 26: 2307-2316.
28. Larsson J, Chen JD, Rasheva V, Rasmuson Lestander A, Pirrotta V, (2001) Painting of fourth, a chromosome-specific protein in Drosophila. Proc Natl Acad Sci U S A 98: 6273-6278.
29. Larsson J, Svensson MJ, Stenberg P, Mäkitalo M, (2004) Painting of fourth in genus Drosophila suggests autosome-specific gene regulation. Proc Natl Acad Sci U S A 101: 9728-9733.
30. Larsson J, Meller VH, (2006) Dosage compensation, the origin and the afterlife of sex chromosomes. Chromosome Res 14: 417-431.
31. Stenberg P, Larsson J, (2011) Buffering and the evolution of chromosome-wide gene regulation. Chromosoma 120: 213-225.
32. Johansson AM, Stenberg P, Pettersson F, Larsson J, (2007) POF and HP1 bind expressed exons, suggesting a balancing mechanism for gene regulation. PLoS Genet 3: e209 doi:10.1371/journal.pgen.0030209.
33. Stenberg P, Lundberg LE, Johansson AM, Rydén P, Svensson MJ, et al. (2009) Buffering of segmental and chromosomal aneuploidies in Drosophila melanogaster. PLoS Genet 5: e1000465 doi:10.1371/journal.pgen.1000465.
34. Riddle NC, Elgin SC, (2006) The dot chromosome of Drosophila: insights into chromatin states and their change over evolutionary time. Chromosome Res 14: 405-416.
35. Riddle NC, Minoda A, Kharchenko PV, Alekseyenko AA, Schwartz YB, et al. (2011) Plasticity in patterns of histone modifications and chromosomal proteins in Drosophila heterochromatin. Genome Res 21: 147-163.
36. Cryderman DE, Grade SK, Li Y, Fanti L, Pimpinelli S, et al. (2005) Role of Drosophila HP1 in euchromatic gene expression. Dev Dyn 232: 767-774.
37. Piacentini L, Fanti L, Berloco M, Perrini B, Pimpinelli S, (2003) Heterochromatin protein 1 (HP1) is associated with induced gene expression in Drosophila euchromatin. J Cell Biol 161: 707-714.
38. Piacentini L, Fanti L, Negri R, Del Vescovo V, Fatica A, et al. (2009) Heterochromatin protein 1 (HP1a) positively regulates euchromatic gene expression through RNA transcript association and interaction with hnRNPs in Drosophila. PLoS Genet 5: e1000670 doi:10.1371/journal.pgen.1000670.
39. Schwaiger M, Kohler H, Oakeley EJ, Stadler MB, Schübeler D, (2010) Heterochromatin protein 1 (HP1) modulates replication timing of the Drosophila genome. Genome Res 20: 771-780.
40. de Wit E, Greil F, van Steensel B, (2005) Genome-wide HP1 binding in Drosophila: developmental plasticity and genomic targeting signals. Genome Res 15: 1265-1273.
41. de Wit E, Greil F, van Steensel B, (2007) High-resolution mapping reveals links of HP1 with active and inactive chromatin components. PLoS Genet 3: e38 doi:10.1371/journal.pgen.0030038.
42. Yin H, Sweeney S, Raha D, Snyder M, Lin H, (2011) A high-resolution whole-genome map of key chromatin modifications in the adult Drosophila melanogaster. PLoS Genet 7: e1002380 doi:10.1371/journal.pgen.1002380.
43. Fanti L, Berloco M, Piacentini L, Pimpinelli S, (2003) Chromosomal distribution of heterochromatin protein 1 (HP1) in Drosophila: a cytological map of euchromatic HP1 binding sites. Genetica 117: 135-147.
44. James TC, Eissenberg JC, Craig C, Dietrich V, Hobson A, et al. (1989) Distribution patterns of HP1, a heterochromatin-associated nonhistone chromosomal protein of Drosophila. Eur J Cell Biol 50: 170-180.
45. Greil F, van der Kraan I, Delrow J, Smothers JF, de Wit E, et al. (2003) Distinct HP1 and Su(var)3-9 complexes bind to sets of developmentally coexpressed genes depending on chromosomal location. Genes Dev 17: 2825-2838.
46. Eissenberg JC, Morris GD, Reuter G, Hartnett T, (1992) The heterochromatin-associated protein HP1 is an essential protein in Drosophila with dosage-dependent effects on position effect variegation. Genetics 131: 345-352.
47. Locke J, Podemski L, Roy K, Pilgrim D, Hodgetts R, (1999) Analysis of two cosmid clones from chromosome 4 of Drosophila melanogaster reveals two new genes amid an unusual arrangement of repeated sequences. Genome Res 9: 137-149.
48. Locke J, Howard L T, Aippersbach N, Podemski L, Hodgetts R B, (1999) The characterization of DINE-1, a short, interspersed repetitive element present on chromosome and in the centric heterochromatin of Drosophila melanogaster. Chromosoma 108: 356-366.
49. Miklos GLG, Yamamoto MT, Davies J, Pirrotta V, (1988) Microcloning reveals a high frequency of repetitive sequences characteristic of chromosome four and the β-heterochromatin of Drosophila melanogaster. Proc Natl Acad Sci U S A 85: 2051-2055.
50. Pimpinelli S, Berloco M, Fanti L, Dimitri P, Bonaccorsi S, et al. (1995) Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proc Natl Acad Sci U S A 92: 3804-3808.
51. Kaminker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R, et al. (2002) The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3: RESEARCH0084.
52. Stenberg P, Pettersson F, Saura AO, Berglund A, Larsson J, (2005) Sequence analysis of chromosome identity in three Drosophila species. BMC Bioinformatics 6: 1-17.
53. Sun FL, Cuaycong MH, Craig CA, Wallrath LL, Locke J, et al. (2000) The fourth chromosome of Drosophila melanogaster: interspersed euchromatic and heterochromatic domains. Proc Natl Acad Sci U S A 97: 5340-5345.
54. Sun FL, Haynes K, Simpson CL, Lee SD, Collins L, et al. (2004) cis-Acting determinants of heterochromatin formation on Drosophila melanogaster chromosome four. Mol Cell Biol 24: 8210-8220.
55. Wallrath LL, Elgin SC, (1995) Position effect variegation in Drosophila is associated with an altered chromatin structure. Genes Dev 9: 1263-1277.
56. Wallrath LL, Guntur VP, Rosman LE, Elgin SC, (1996) DNA representation of variegating heterochromatic P-element inserts in diploid and polytene tissues of Drosophila melanogaster. Chromosoma 104: 519-527.
57. Eskeland R, Eberharter A, Imhof A, (2007) HP1 binding to chromatin methylated at H3K9 is enhanced by auxiliary factors. Mol Cell Biol 27: 453-465.
58. Meehan RR, Kao CF, Pennings S, (2003) HP1 binding to native chromatin in vitro is determined by the hinge region and not by the chromodomain. EMBO J 22: 3164-3174.
59. Jacobs SA, Taverna SD, Zhang Y, Briggs SD, Li J, et al. (2001) Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. EMBO J 20: 5232-5241.
60. Fan JY, Rangasamy D, Luger K, Tremethick DJ, (2004) H2A.Z alters the nucleosome surface to promote HP1α-mediated chromatin fiber folding. Mol Cell 16: 655-661.
61. Raveh-Sadka T, Levo M, Shabi U, Shany B, Keren L, et al. (2012) Manipulating nucleosome disfavoring sequences allows fine-tune regulation of gene expression in yeast. Nat Genet 44: 743-750.
62. Segal E, Widom J, (2009) Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr Opin Struct Biol 19: 65-71.
63. Cryderman DE, Vitalini MW, Wallrath LL, (2011) Heterochromatin protein 1a is required for an open chromatin structure. Transcription 2: 95-99.
64. Mendez DL, Kim D, Chruszcz M, Stephens GE, Minor W, et al. (2011) The HP1a disordered C terminus and chromo shadow domain cooperate to select target peptide partners. Chembiochem 12: 1084-1096.
65. Stephens GE, Slawson EE, Craig CA, Elgin SC, (2005) Interaction of heterochromatin protein 2 with HP1 defines a novel HP1-binding domain. Biochemistry 44: 13394-13403.
66. Stephens GE, Xiao H, Lankenau DH, Wu C, Elgin SC, (2006) Heterochromatin protein 2 interacts with Nap-1 and NURF: a link between heterochromatin-induced gene silencing and the chromatin remodeling machinery in Drosophila. Biochemistry 45: 14990-14999.
67. Pak DT, Pflumm M, Chesnokov I, Huang DW, Kellum R, et al. (1997) Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes. Cell 91: 311-323.
68. Auth T, Kunkel E, Grummt F, (2006) Interaction between HP1α and replication proteins in mammalian cells. Exp Cell Res 312: 3349-3359.
69. Prasanth SG, Shen Z, Prasanth KV, Stillman B, (2010) Human origin recognition complex is essential for HP1 binding to chromatin and heterochromatin organization. Proc Natl Acad Sci U S A 107: 15093-15098.
70. Schwartz YB, Kahn TG, Nix DA, Li XY, Bourgon R, et al. (2006) Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet 38: 700-705.
71. Schwartz YB, Pirrotta V, (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8: 9-22.
72. Kahn TG, Schwartz YB, Dellino GI, Pirrotta V, (2006) Polycomb complexes and the propagation of the methylation mark at the Drosophila ubx gene. J Biol Chem 281: 29064-29075.
73. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, et al. (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17: 1870-1881.
74. Luco RF, Pan Q, Tominaga K, Blencowe BJ, Pereira-Smith OM, et al. (2010) Regulation of alternative splicing by histone modifications. Science 327: 996-1000.
75. Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T, (2011) Epigenetics in alternative pre-mRNA splicing. Cell 144: 16-26.
76. Haynes KA, Gracheva E, Elgin SC, (2007) A distinct type of heterochromatin within Drosophila melanogaster chromosome 4. Genetics 175: 1539-1542.
77. Swaminathan J, Baxter EM, Corces VG, (2005) The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev 19: 65-76.
78. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, et al. (2011) The developmental transcriptome of Drosophila melanogaster. Nature 471: 473-479.
79. Johansson AM, Allgardsson A, Stenberg P, Larsson J, (2011) msl2 mRNA is bound by free nuclear MSL complex in Drosophila melanogaster. Nucleic Acids Res 39: 6428-6439.
80. Kuttippurathu L, Hsing M, Liu Y, Schmidt B, Maskell DL, et al. (2011) CompleteMOTIFs: DNA motif discovery platform for transcription factor binding experiments. Bioinformatics 27: 715-717.
81. Celniker SE, Dillon LA, Gerstein MB, Gunsalus KC, Henikoff S, et al. (2009) Unlocking the secrets of the genome. Nature 459: 927-930.
82. Thomas S, Li XY, Sabo PJ, Sandstrom R, Thurman RE, et al. (2011) Dynamic reprogramming of chromatin accessibility during Drosophila embryo development. Genome Biol 12: R43.