Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription

Cell

Volumn 123, Issue 4, 2005, Pages 581-592

  Carrozza, Michael J ^a   Li, Bing ^a   Florens, Laurence ^a   Suganuma, Tamaki ^a   Swanson, Selene K ^a   Lee, Kenneth K ^a   Shia, Wei Jong ^a   Anderson, Scott ^b   Yates, John ^b   Washburn, Michael P ^a   Workman, Jerry L ^a  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL ENZYME; HISTONE DEACETYLASE; HISTONE DEACETYLASE RPD3L; HISTONE DEACETYLASE RPD3S; HISTONE H3; METHYLTRANSFERASE; PROTEIN EAF3; PROTEIN RCO1; PROTEIN SUBUNIT; RNA POLYMERASE II; RNA POLYMERASE II ASSOCIATED SET2 HISTONE METHYLTRANSFERASE; TRANSCRIPTION ELONGATION FACTOR; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; DEACETYLATION; METHYLATION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION INITIATION; YEAST;

EID: 27744577727     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2005.10.023     Document Type: Article

References (68)

1. A.J. Bannister, P. Zegerman, J.F. Partridge, E.A. Miska, J.O. Thomas, R.C. Allshire, and T. Kouzarides Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain Nature 410 2001 120 124
2. R. Belotserkovskaya, S. Oh, V.A. Bondarenko, G. Orphanides, V.M. Studitsky, and D. Reinberg FACT facilitates transcription-dependent nucleosome alteration Science 301 2003 1090 1093
3. M.J. Bertram, N.G. Berube, X. Hang-Swanson, Q. Ran, J.K. Leung, S. Bryce, K. Spurgers, R.J. Bick, A. Baldini, and Y. Ning Identification of a gene that reverses the immortal phenotype of a subset of cells and is a member of a novel family of transcription factor-like genes Mol. Cell. Biol. 19 1999 1479 1485
4. A. Bortvin, and F. Winston Evidence that Spt6p controls chromatin structure by a direct interaction with histones Science 272 1996 1473 1476
5. S.D. Briggs, T. Xiao, Z.W. Sun, J.A. Caldwell, J. Shabanowitz, D.F. Hunt, C.D. Allis, and B.D. Strahl Gene silencing: trans-histone regulatory pathway in chromatin Nature 418 2002 498
6. Carrozza, M.J., Florens, L., Swanson, S.K., Shia, W.-J., Anderson, S., Yates, J., Washburn, M.P., and Workman, J.L. (2005). Stable incorporation of sequence specific repressors Ash1 and Ume6 into the Rpd3L complex. BBA - Gene Structure and Expression. in press.
7. E. De Nadal, M. Zapater, P.M. Alepuz, L. Sumoy, G. Mas, and F. Posas The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes Nature 427 2004 370 374
8. A. Eisen, R.T. Utley, A. Nourani, S. Allard, P. Schmidt, W.S. Lane, J.C. Lucchesi, and J. Cote The yeast NuA4 and Drosophila MSL complexes contain homologous subunits important for transcription regulation J. Biol. Chem. 276 2001 3484 3491
9. J.K. Eng, A.L. McCormack, and J.R. Yates 3rd. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database J. Am. Soc. Mass Spectrom. 5 1994 976 989
10. A.C. Gavin, M. Bosche, R. Krause, P. Grandi, M. Marzioch, A. Bauer, J. Schultz, J.M. Rick, A.M. Michon, and C.M. Cruciat Functional organization of the yeast proteome by systematic analysis of protein complexes Nature 415 2002 141 147
11. C. Guthrie, and G.R. Fink Guide to yeast genetics and molecular biology 1991 Academic Press San Diego
12. A. Hecht, and M. Grunstein Mapping DNA interaction sites of chromosomal proteins using immunoprecipitation and polymerase chain reaction Methods Enzymol. 304 1999 399 414
13. Y. Ho, A. Gruhler, A. Heilbut, G.D. Bader, L. Moore, S.L. Adams, A. Millar, P. Taylor, K. Bennett, and K. Boutilier Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry Nature 415 2002 180 183
14. D. Kadosh, and K. Struhl Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters Cell 89 1997 365 371
15. D. Kadosh, and K. Struhl Targeted recruitment of the Sin3-Rpd3 histone deacetylase complex generates a highly localized domain of repressed chromatin in vivo Mol. Cell. Biol. 18 1998 5121 5127
16. C.D. Kaplan, L. Laprade, and F. Winston Transcription elongation factors repress transcription initiation from cryptic sites Science 301 2003 1096 1099
17. M.M. Kasten, S. Dorland, and D.J. Stillman A large protein complex containing the yeast Sin3p and Rpd3p transcriptional regulators Mol. Cell. Biol. 17 1997 4852 4858
18. K.O. Kizer, H.P. Phatnani, Y. Shibata, H. Hall, A.L. Greenleaf, and B.D. Strahl A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation Mol. Cell. Biol. 25 2005 3305 3316
19. A. Kristjuhan, and J.Q. Svejstrup Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo EMBO J. 23 2004 4243 4252
20. A. Kristjuhan, J. Walker, N. Suka, M. Grunstein, D. Roberts, B.R. Cairns, and J.Q. Svejstrup Transcriptional inhibition of genes with severe histone h3 hypoacetylation in the coding region Mol. Cell 10 2002 925 933
21. N.J. Krogan, J. Dover, S. Khorrami, J.F. Greenblatt, J. Schneider, M. Johnston, and A. Shilatifard COMPASS, a histone H3 (Lysine 4) methyltransferase required for telomeric silencing of gene expression J. Biol. Chem. 277 2002 10753 10755
22. N.J. Krogan, J. Dover, A. Wood, J. Schneider, J. Heidt, M.A. Boateng, K. Dean, O.W. Ryan, A. Golshani, and M. Johnston The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation Mol. Cell 11 2003 721 729
23. N.J. Krogan, M. Kim, A. Tong, A. Golshani, G. Cagney, V. Canadien, D.P. Richards, B.K. Beattie, A. Emili, and C. Boone Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II Mol. Cell. Biol. 23 2003 4207 4218
24. S.K. Kurdistani, and M. Grunstein Histone acetylation and deacetylation in yeast Nat. Rev. Mol. Cell Biol. 4 2003 276 284
25. S.K. Kurdistani, D. Robyr, S. Tavazoie, and M. Grunstein Genome-wide binding map of the histone deacetylase Rpd3 in yeast Nat. Genet. 31 2002 248 254
26. T. Kusch, L. Florens, W.H. Macdonald, S.K. Swanson, R.L. Glaser, J.R. Yates 3rd, S.M. Abmayr, M.P. Washburn, and J.L. Workman Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions Science 306 2004 2084 2087
27. M. Lachner, D. O'Carroll, S. Rea, K. Mechtler, and T. Jenuwein Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins Nature 410 2001 116 120
28. T. Lechner, M.J. Carrozza, Y. Yu, P.A. Grant, A. Eberharter, D. Vannier, G. Brosch, D.J. Stillman, D. Shore, and J.L. Workman Sds3 (suppressor of defective silencing 3) is an integral component of the yeast Sin3[middle dot]Rpd3 histone deacetylase complex and is required for histone deacetylase activity J. Biol. Chem. 275 2000 40961 40966
29. B. Li, L. Howe, S. Anderson, J.R. Yates 3rd, and J.L. Workman The Set2 histone methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II J. Biol. Chem. 278 2003 8897 8903
30. B. Li, and J.C. Reese Ssn6-Tup1 regulates RNR3 by positioning nucleosomes and affecting the chromatin structure at the upstream repression sequence J. Biol. Chem. 276 2001 33788 33797
31. H. Liu, R.G. Sadygov, and J.R. Yates 3rd. A model for random sampling and estimation of relative protein abundance in shotgun proteomics Anal. Chem. 76 2004 4193 4201
32. R. Loewith, J.S. Smith, M. Meijer, T.J. Williams, N. Bachman, J.D. Boeke, and D. Young Pho23 is associated with the Rpd3 histone deacetylase and is required for its normal function in regulation of gene expression and silencing in Saccharomyces cerevisiae J. Biol. Chem. 276 2001 24068 24074
33. P.B. Mason, and K. Struhl The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo Mol. Cell. Biol. 23 2003 8323 8333
34. W.H. McDonald, R. Ohi, D.T. Miyamoto, T.J. Mitchison, and J.R. Yates Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single-dimension LCMS/MS, 2-phase MudPIT, and 3-phase MudPIT Int. J. Mass Spectrom. 219 2002 245 251
35. A. Morillon, N. Karabetsou, A. Nair, and J. Mellor Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription Mol. Cell 18 2005 723 734
36. P.L. Nagy, J. Griesenbeck, R.D. Kornberg, and M.L. Cleary A trithorax-group complex purified from Saccharomyces cerevisiae is required for methylation of histone H3 Proc. Natl. Acad. Sci. USA 99 2002 90 94
37. H.H. Ng, F. Robert, R.A. Young, and K. Struhl Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity Mol. Cell 11 2003 709 719
38. H.H. Ng, R.M. Xu, Y. Zhang, and K. Struhl Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79 J. Biol. Chem. 277 2002 34655 34657
39. D.K. Pokholok, C.T. Harbison, S. Levine, M. Cole, N.M. Hannett, T.I. Lee, G.W. Bell, K. Walker, P.A. Rolfe, and E. Herbolsheimer Genome-wide map of nucleosome acetylation and methylation in yeast Cell 122 2005 517 527
40. M.G. Pray-Grant, J.A. Daniel, D. Schieltz, J.R. Yates 3rd, and P.A. Grant Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation Nature 433 2005 434 438
41. O. Puig, F. Caspary, G. Rigaut, B. Rutz, E. Bouveret, E. Bragado-Nilsson, M. Wilm, and B. Seraphin The tandem affinity purification (TAP) method: a general procedure of protein complex purification Methods 24 2001 218 229
42. S. Puig, M. Lau, and D.J. Thiele Cti6 is an Rpd3-Sin3 histone deacetylase-associated protein required for growth under iron-limiting conditions in Saccharomyces cerevisiae J. Biol. Chem. 279 2004 30298 30306
43. D. Ray-Gallet, J.P. Quivy, C. Scamps, E.M. Martini, M. Lipinski, and G. Almouzni HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis Mol. Cell 9 2002 1091 1100
44. J.L. Reid, Z. Moqtaderi, and K. Struhl Eaf3 regulates the global pattern of histone acetylation in Saccharomyces cerevisiae Mol. Cell. Biol. 24 2004 757 764
45. D. Robyr, Y. Suka, I. Xenarios, S.K. Kurdistani, A. Wang, N. Suka, and M. Grunstein Microarray deacetylation maps determine genome-wide functions for yeast histone deacetylases Cell 109 2002 437 446
46. A. Roguev, D. Schaft, A. Shevchenko, W.W. Pijnappel, M. Wilm, R. Aasland, and A.F. Stewart The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4 EMBO J. 20 2001 7137 7148
47. S.E. Rundlett, A.A. Carmen, R. Kobayashi, S. Bavykin, B.M. Turner, and M. Grunstein HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription Proc. Natl. Acad. Sci. USA 93 1996 14503 14508
48. S.E. Rundlett, A.A. Carmen, N. Suka, B.M. Turner, and M. Grunstein Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3 Nature 392 1998 831 835
49. R.G. Sadygov, J. Eng, E. Durr, A. Saraf, H. McDonald, M.J. MacCoss, and J.R. Yates 3rd. Code developments to improve the efficiency of automated MS/MS spectra interpretation J. Proteome Res. 1 2002 211 215
50. A. Saunders, J. Werner, E.D. Andrulis, T. Nakayama, S. Hirose, D. Reinberg, and J.T. Lis Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo Science 301 2003 1094 1096
51. D. Schaft, A. Roguev, K.M. Kotovic, A. Shevchenko, M. Sarov, K.M. Neugebauer, and A.F. Stewart The histone 3 lysine 36 methyltransferase, SET2, is involved in transcriptional elongation Nucleic Acids Res. 31 2003 2475 2482
52. B.E. Schwartz, and K. Ahmad Transcriptional activation triggers deposition and removal of the histone variant H3.3 Genes Dev. 19 2005 804 814
53. F. Storici, C.L. Durham, D.A. Gordenin, and M.A. Resnick Chromosomal site-specific double-strand breaks are efficiently targeted for repair by oligonucleotides in yeast Proc. Natl. Acad. Sci. USA 100 2003 14994 14999
54. Z.W. Sun, and C.D. Allis Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast Nature 418 2002 104 108
55. D.L. Tabb, W.H. McDonald, and J.R. Yates 3rd. DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics J. Proteome Res. 1 2002 21 26
56. H. Tagami, D. Ray-Gallet, G. Almouzni, and Y. Nakatani Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis Cell 116 2004 51 61
57. K. Tominaga, B. Kirtane, J.G. Jackson, Y. Ikeno, T. Ikeda, C. Hawks, J.R. Smith, M.M. Matzuk, and O.M. Pereira-Smith MRG15 regulates embryonic development and cell proliferation Mol. Cell. Biol. 25 2005 2924 2937
58. A. Verreault, P.D. Kaufman, R. Kobayashi, and B. Stillman Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4 Cell 87 1996 95 104
59. M. Vidal, and R.F. Gaber RPD3 encodes a second factor required to achieve maximum positive and negative transcriptional states in Saccharomyces cerevisiae Mol. Cell. Biol. 11 1991 6317 6327
60. M. Vogelauer, J. Wu, N. Suka, and M. Grunstein Global histone acetylation and deacetylation in yeast Nature 408 2000 495 498
61. M.P. Washburn, D. Wolters, and J.R. Yates 3rd. Large-scale analysis of the yeast proteome by multidimensional protein identification technology Nat. Biotechnol. 19 2001 242 247
62. B.O. Wittschieben, G. Otero, T. de Bizemont, J. Fellows, H. Erdjument-Bromage, R. Ohba, Y. Li, C.D. Allis, P. Tempst, and J.Q. Svejstrup A novel histone acetyltransferase is an integral subunit of elongating RNA polymerase II holoenzyme Mol. Cell 4 1999 123 128
63. D.A. Wolters, M.P. Washburn, and J.R. Yates 3rd. An automated multidimensional protein identification technology for shotgun proteomics Anal. Chem. 73 2001 5683 5690
64. A. Wood, J. Schneider, J. Dover, M. Johnston, and A. Shilatifard The Paf1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p J. Biol. Chem. 278 2003 34739 34742
65. P.Y. Wu, and F. Winston Analysis of Spt7 function in the Saccharomyces cerevisiae SAGA coactivator complex Mol. Cell. Biol. 22 2002 5367 5379
66. T. Xiao, H. Hall, K.O. Kizer, Y. Shibata, M.C. Hall, C.H. Borchers, and B.D. Strahl Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast Genes Dev. 17 2003 654 663
67. G.S. Yochum, and D.E. Ayer Role for the mortality factors MORF4, MRGX, and MRG15 in transcriptional repression via associations with Pf1, mSin3A, and Transducin-Like Enhancer of Split Mol. Cell. Biol. 22 2002 7868 7876
68. Y. Zhang, Z.W. Sun, R. Iratni, H. Erdjument-Bromage, P. Tempst, M. Hampsey, and D. Reinberg SAP30, a novel protein conserved between human and yeast, is a component of a histone deacetylase complex Mol. Cell 1 1998 1021 1031