DNA polymerase , acetylases and remodellers cooperate to form a specialized chromatin structure at a tRNA insulator

EMBO Journal

Volumn 28, Issue 17, 2009, Pages 2583-2600

  Dhillon, Namrita ^a   Raab, Jesse ^a   Guzzo, Julie ^b   Szyjka, Shawn J ^c   Gangadharan, Sunil ^a   Aparicio, Oscar M ^c   Andrews, Brenda ^b   Kamakaka, Rohinton T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DNA DIRECTED DNA POLYMERASE EPSILON; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE NUA4; HISTONE ACETYLTRANSFERASE RTT109; HISTONE ACETYLTRANSFERASE SAS I; PROTEIN RSC; TRANSCRIPTION FACTOR IIIB; TRANSFER RNA; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE ALPHA; HISTONE; RSC COMPLEX, S CEREVISIAE; RTT109 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CELL DIVISION; CELL GROWTH; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA REPLICATION; CHEMISTRY; CHROMATIN; ENZYMOLOGY; GENETICS; INSULATOR ELEMENT; METABOLISM; SACCHAROMYCES CEREVISIAE;

CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA POLYMERASE II; DNA-BINDING PROTEINS; HISTONE ACETYLTRANSFERASES; HISTONES; INSULATOR ELEMENTS; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 69849111326     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.198     Document Type: Article

References (85)

1. Adkins MW, Howar SR, Tyler JK (2004) Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcrip-tional activation of the yeast PHO5 and PHO8 genes. Mol Cell 14: 657-666
2. Annunziato AT, Schindler RK, Thomas Jr CA, Seale RL (1981) Dual nature of newly replicated chromatin. Evidence for nucleosomal and non-nucleosomal DNA at the site of native replication forks. J Biol Chem 256: 11880-11886
3. Annunziato AT, Seale RL (1983) Histone deacetylation is required for the maturation of newly replicated chromatin. J Biol Chem 258: 12675-12684
4. Antczak AJ, Tsubota T, Kaufman PD, Berger JM (2006) Structure of the yeast histone H3-ASF1 interaction: implications for chaperone mechanism, species-specific interactions, and epigenetics. BMC Struct Biol 6: 26
5. Asturias FJ, Cheung IK, Sabouri N, Chilkova O, Wepplo D, Johansson E (2006) Structure of Saccharomyces cerevisiae DNA polymerase epsilon by cryo-electron microscopy. Nat Struct Mol Biol 13: 35-43
6. Bachman N, Gelbart ME, Tsukiyama T, Boeke JD (2005) TFIIIB subunit Bdp1p is required for periodic integration of the Ty1 retrotransposon and targeting of Isw2p to S. cerevisiae tDNAs. Genes Dev 19: 955-964
7. Bell AC, West AG, Felsenfeld G (1999) The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98: 387-396
8. Bi X (2002) Domains of gene silencing near the left end of chromosome III in Saccharomyces cerevisiae. Genetics 160: 1401-1407
9. Brewer BJ, Fangman WL (1991) Mapping replication origins in yeast chromosomes. Bioessays 13: 317-322
10. Carey M, Li B, Workman JL (2006) RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation. Mol Cell 24: 481-487
11. Celic I, Masumoto H, Griffith WP, Meluh P, Cotter RJ, Boeke JD, Verreault A (2006) The sirtuins hst3 and Hst4p preserve genome integrity by controlling histone h3 lysine 56 deacetylation. Curr Biol 16: 1280-1289
12. Celic I, Verreault A, Boeke JD (2008) Histone H3 K56 hyperacetyla-tion perturbs replisomes and causes DNA damage. Genetics 179: 1769-1784
13. 0 element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell 74: 505-514
14. Damelin M, Simon I, Moy TI, Wilson B, Komili S, Tempst P, Roth FP, Young RA, Cairns BR, Silver PA (2002) The genome-wide localization of Rsc9, a component of the RSC chromatin-remodeling complex, changes in response to stress. Mol Cell 9: 563-573
15. Deshpande AM, Newlon CS (1996) DNA replication fork pause sites dependent on transcription. Science 272: 1030-1033
16. Dion MF, Kaplan T, Kim M, Buratowski S, Friedman N, Rando OJ (2007) Dynamics of replication-independent histone turnover in budding yeast. Science 315: 1405-1408
17. Donze D, Adams CR, Rine J, Kamakaka RT (1999) The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev 13: 698-708
18. Donze D, Kamakaka RT (2001) RNA polymerase III and RNA polymerase II promoter complexes are heterochromatin barriers in Saccharomyces cerevisiae. EMBO J 20: 520-531
19. Dua R, Edwards S, Levy DL, Campbell JL (2000) Subunit interactions within the Saccharomyces cerevisiae DNA polymerase epsilon (pol epsilon) complex. Demonstration of a dimeric pol epsilon. J Biol Chem 275: 28816-28825
20. Fera H, Flaus A, Owen-Hughes T (2007) Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms. J Mol Biol 374: 563-579
21. Fillingham J, Greenblatt JF (2008) A histone code for chromatin assembly. Cell 134: 206-208
22. Gasser R, Koller T, Sogo JM (1996) The stability of nucleosomes at the replication fork. J Mol Biol 258: 224-239
23. Geiduschek EP, Kassavetis GA (2001) The RNA polymerase III transcription apparatus. J Mol Biol 310 : 1-26
24. Gelbart ME, Bachman N, Delrow J, Boeke JD, Tsukiyama T (2005) Genome-wide identification of Isw2 chromatin-remodeling targets by localization of a catalytically inactive mutant. Genes Dev 19: 942-954
25. Govind CK, Yoon S, Qiu H, Govind S, Hinnebusch AG (2005) Simultaneous recruitment of coactivators by Gcn4p stimulates multiple steps of transcription in vivo. Mol Cell Biol 25: 5626-5638
26. Govind CK, Zhang F, Qiu H, Hofmeyer K, Hinnebusch AG (2007) Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions. Mol Cell 25: 31-42
27. Green EM, Antczak AJ, Bailey AO, Franco AA, Wu KJ, Yates III JR, Kaufman PD (2005) Replication-independent histone deposition by the HIR complex and Asf1. Curr Biol 15: 2044-2049
28. Hake SB, is CD (2006) Histone H3 variants and their potential role in indexing mammalian genomes: the 'H3 barcode hypothesis'. Proc Natl Acad Sci USA 103: 6428-6435
29. Haldar D, Kamakaka RT (2006) tRNA genes as chromatin barriers. Nat Struct Mol Biol 13: 192-193
30. Haldar D, Kamakaka RT (2008) Schizosaccharomyces pombe Hst4 functions in DNA damage response by regulating histone H3 K56 acetylation. Eukaryot Cell 7: 800-813
31. Han J, Zhou H, Li Z, Xu RM, Zhang Z (2007) Acetylation of lysine 56 of histone H3 catalyzed by RTT109 and regulated by ASF1 is required for replisome integrity. J Biol Chem 282: 28587-28596
32. Huisinga KL, Brower-Toland B, Elgin SC (2006) The contradictory definitions of heterochromatin: transcription and silencing. Chromosoma 115: 110-122
33. Iida T, Araki H (2004) Noncompetitive counteractions of DNA polymerase epsilon and ISW2/yCHRAC for epigenetic inheritance of telomere position effect in Saccharomyces cerevisiae. Mol Cell Biol 24: 217-227
34. Jackson V, Granner D, Chalkley R (1976) Deposition of histone onto the replicating chromosome: newly synthesized histone is not found near the replication fork. Proc Natl Acad Sci USA 73: 2266-2269
35. Jambunathan N, Martinez AW, Robert EC, Agochukwu NB, Ibos ME, Dugas SL, Donze D (2005) Multiple bromodomain genes are involved in restricting the spread of heterochromatic silencing at the Saccharomyces cerevisiae HMR-tRNA boundary. Genetics 171: 913-922
36. Kaplan T, Liu CL, Erkmann JA, Holik J, Grunstein M, Kaufman PD, Friedman N, Rando OJ (2008) Cell cycle-and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet 4: e1000270
37. Kasten M, Szerlong H, Erdjument-Bromage H, Tempst P, Werner M, Cairns BR (2004) Tandem bromodomains in the chromatin re-modeler RSC recognize acetylated histone H3 Lys14. EMBO J 23: 1348-1359
38. Kimura A, Umehara T, Horikoshi M (2002) Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nat Genet 32: 370-377
39. Kurdistani SK, Tavazoie S, Grunstein M (2004) Mapping global histone acetylation patterns to gene expression. Cell 117: 721-733
40. Maas NL, Miller KM, DeFazio LG, Toczyski DP (2006) Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell 23: 109-119
41. Masumoto H, Hawke D, Kobayashi R, Verreault A (2005) A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436: 294-298
42. Mavrich TN, Ioshikhes IP, Venters BJ, Jiang C, Tomsho LP, Qi J, Schuster SC, Albert I, Pugh BF (2008) A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 18: 1073-1083
43. McConnell AD, Gelbart ME, Tsukiyama T (2004) Histone fold protein Dls1p is required for Isw2-dependent chromatin remodeling in vivo. Mol Cell Biol 24: 2605-2613
44. McKnight SL, Miller Jr OL (1977) Electron microscopic analysis of chromatin replication in the cellular blastoderm Drosophila melanogaster embryo. Cell 12: 795-804
45. Meluh PB, Broach JR (1999) Immunological analysis of yeast chromatin. Methods Enzymol 304: 414-430
46. Meneghini MD, Wu M, Madhani HD (2003) Conserved histone variant H2A. Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112: 725-736
47. Mousson F, Ochsenbein F, Mann C (2007) The histone chaperone Asf1 at the crossroads of chromatin and DNA checkpoint pathways. Chromosoma 116: 79-93
48. Nasmyth KA (1982) The regulation of yeast mating-type chromatin structure by SIR: an action at a distance affecting both transcription and transposition. Cell 30: 567-578
49. Nelson JD, Denisenko O, Sova P, Bomsztyk K (2006) Fast chromatin immunoprecipitation assay. Nucleic Acids Res 34: e2
50. Ng HH, Robert F, Young RA, Struhl K (2002) Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex. Genes Dev 16: 806-819
51. Ohya T, Maki S, Kawasaki Y, Sugino A (2000) Structure and function of the fourth subunit (Dpb4p) of DNA polymerase epsilon in Saccharomyces cerevisiae. Nucleic Acids Res 28: 3846-3852
52. Oki M, Kamakaka RT (2005) Barrier function at HMR. Mol Cell 19: 707-716
53. Parnell TJ, Huff JT, Cairns BR (2008) RSC regulates nucleosome positioning at Pol II genes and density at Pol III genes. EMBO J 27: 100-110
54. Parthun MR, Widom J, Gottschling DE (1996) The major cytoplas-mic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell 87: 85-94
55. 0 ends of both active and inactive genes in euchromatin. Cell 123: 233-248
56. Roberts TM, Zaidi IW, Vaisica JA, Peter M, Brown GW (2008) Regulation of rtt107 recruitment to stalled DNA replication forks by the cullin rtt101 and the rtt109 acetyltransferase. Mol Biol Cell 19: 171-180
57. Rufiange A, Jacques PE, Bhat W, Robert F, Nourani A (2007) Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell 27: 393-405
58. Saha A, Wittmeyer J, Cairns BR (2006) Chromatin remodelling: the industrial revolution of DNA around histones. Nat Rev Mol Cell Biol 7: 437-447
59. Selth LA, Lorch Y, Ocampo-Hafalla MT, Mitter R, Shales M, Krogan NJ, Kornberg RD, Svejstrup JQ (2009) An Rtt109-independent role for Vps75 in transcription-associated nucleosome dynamics. Mol Cell Biol (e-pub ahead of print; PMID: 19470761)
60. Shibahara K, Stillman B (1999) Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96: 575-585
61. 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
62. Solomon MJ, Varshavsky A (1987) A nuclease-hypersensitive region forms de novo after chromosome replication. Mol Cell Biol 7: 3822-3825
63. Soutourina J, Bordas-Le Floch V, Gendrel G, Flores A, Ducrot C, Dumay-Odelot H, Soularue P, Navarro F, Cairns BR, Lefebvre O, Werner M (2006) Rsc4 connects the chromatin remodeler RSC to RNA polymerases. Mol Cell Biol 26: 4920-4933
64. Stillman B (2008) DNA polymerases at the replication fork in eukaryotes. Mol Cell 30: 259-260
65. Suka N, Luo K, Grunstein M (2002) Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin. Nat Genet 32: 378-383
66. Suka N, Suka Y, Carmen AA, Wu J, Grunstein M (2001) Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol Cell 8: 473-479
67. Tackett AJ, Dilworth DJ, Davey MJ, O'Donnell M, Aitchison JD, Rout MP, Chait BT (2005) Proteomic and genomic haracterization of chromatin complexes at a boundary. J Cell Biol 169: 35-47
68. Thomas JO, Furber V (1976) Yeast chromatin structure. FEBS Lett 66: 274-280
69. Tompa R, Madhani HD (2007) Histone H3 lysine 36 methylation antagonizes silencing in Saccharomyces cerevisiae independently of the Rpd3S histone deacetylase complex. Genetics 175: 585-593
70. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, Page N, Robinson M, Raghibizadeh S, Hogue CW, Bussey H, Andrews B, Tyers M, Boone C (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368
71. Trojer P, Reinberg D (2007) Facultative heterochromatin: is there a distinctive molecular signature? Mol Cell 28: 1-13
72. Tsubota T, Tajima R, Ode K, Kubota H, Fukuhara N, Kawabata T, Maki S, Maki H (2006) Double-stranded DNA binding, an unusual property of DNA polymerase epsilon, promotes epigenetic silencing in Saccharomyces cerevisiae. J Biol Chem 281: 32898-32908
73. Udvardy A, Maine E, Schedl P (1985) The 87A7 chromomere. Identification of novel chromatin structures flanking the heat shock locus that may define the boundaries of higher order domains. J Mol Biol 185: 341-358
74. Valenzuela L, Gangadharan S, Kamakaka RT (2006) Analyses of SUM1-1-mediated long-range repression. Genetics 172: 99-112
75. Valenzuela L, Kamakaka RT (2006) Chromatin insulators. Annu Rev Genet 40: 107-138
76. van Leeuwen F, Gottschling DE (2002) Assays for gene silencing in yeast. Methods Enzymol 350: 165-186
77. VanDemark AP, Kasten MM, Ferris E, Heroux A, Hill CP, Cairns BR (2007) Autoregulation of the rsc4 tandem bromodomain by gcn5 acetylation. Mol Cell 27: 817-828
78. Waga S, Stillman B (1998) The DNA replication fork in eukaryotic cells. Annu Rev Biochem 67: 721-751
79. Wang A, Kurdistani SK, Grunstein M (2002) Requirement of Hos2 histone deacetylase for gene activity in yeast. Science 298: 1412-1414
80. West AG, Gaszner M, Felsenfeld G (2002) Insulators: many functions, many mechanisms. Genes Dev 16: 271-288
81. West AG, Huang S, Gaszner M, Litt MD, Felsenfeld G (2004) Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Mol Cell 16: 453-463
82. Worcel A, Han S, Wong ML (1978) Assembly of newly replicated chromatin. Cell 15: 969-977
83. Xu F, Zhang Q, Zhang K, Xie W, Grunstein M (2007) Sir2 deacety-lates histone H3 lysine 56 to regulate telomeric heterochromatin structure in yeast. Mol Cell 27: 890-900
84. Yuan GC, Liu YJ, Dion MF, Slack MD, Wu LF, Altschuler SJ, Rando OJ (2005) Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309: 626-630
85. Zhang H, Roberts DN, Cairns BR (2005) Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/ basal promoters for activation through histone loss. Cell 123: 219-231