Identification of a role for histone H2B ubiquitylation in noncoding RNA 3'-end formation through mutational analysis of Rtf1 in Saccharomyces cerevisiae

Genetics

Volumn 188, Issue 2, 2011, Pages 273-289

  Tomson, Brett N ^a   Davis, Christopher P ^a   Warner, Marcie H ^a   Arndt, Karen M ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; HISTONE H2B; RTF1 PROTEIN; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; FUNGUS GROWTH; GENE MUTATION; HISTONE METHYLATION; HISTONE MODIFICATION; HISTONE UBIQUITINATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA TRANSCRIPTION; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; BLOTTING, NORTHERN; BLOTTING, WESTERN; GENE EXPRESSION REGULATION, FUNGAL; HISTONES; HUMANS; LYSINE; METHYLATION; MOLECULAR SEQUENCE DATA; MUTATION; RNA, SMALL NUCLEOLAR; RNA, UNTRANSLATED; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TATA-BOX BINDING PROTEIN; UBIQUITINATION;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 79958184449     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.111.128645     Document Type: Article

References (106)

1. Adams, A., D. E. Gottschling, C. A. Kaiser and T. Stearns, 1997 Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Adelman, K., W. Wei, M. B. Ardehali, J. Werner, B. Zhu et al., 2006 Drosophila Paf1 modulates chromatin structure at actively transcribed genes. Mol. Cell. Biol. 26: 250-260.
3. Akanuma, T., S. Koshida, A. Kawamura, Y. Kishimoto and S. Takada, 2007 Paf1 complex homologues are required for Notch-regulated transcription during somite segmentation. EMBO Rep. 8: 858-863.
4. Amaral, P. P., M. E. Dinger, T. R. Mercer and J. S. Mattick, 2008 The eukaryotic genome as an RNA machine. Science 319: 1787-1789.
5. Arigo, J. T., D. E. Eyler, K. L. Carroll and J. L. Corden, 2006 Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol. Cell 23: 841-851.
6. Ausubel, F.M., R. Brent, R. E. Kingston, D.D. Moore, J.G. Seidman et al., 1988 Current Protocols in Molecular Biology. Green Publishing Associates and Wiley-Interscience, New York.
7. Bannister, A. J., R. Schneider, F. A. Myers, A. W. Thorne, C. Crane-Robinson et al., 2005 Spatial distribution of di-and tri-methyl lysine 36 of histone H3 at active genes. J. Biol. Chem. 280: 17732-17736.
8. Braun, M. A., P. J. Costa, E. M. Crisucci and K. M. Arndt, 2007 Identification of Rkr1, a nuclear RING domain protein with functional connections to chromatin modification in Saccharomyces cerevisiae. Mol. Cell. Biol. 27: 2800-2811.
9. Briggs, S. D., T. Xiao, Z. W. Sun, J. A. Caldwell, J. Shabanowitz et al., 2002 Gene silencing: trans-histone regulatory pathway in chromatin. Nature 418: 498.
10. Carninci, P., 2009 Molecular biology: the long and short of RNAs. Nature 457: 974-975.
11. Carroll, K. L., D. A. Pradhan, J. A. Granek, N. D. Clarke and J. L. Corden, 2004 Identification of cis elements directing termination of yeast nonpolyadenylated snoRNA transcripts. Mol. Cell. Biol. 24: 6241-6252.
12. Chandrasekharan, M. B., F. Huang and Z. W. Sun, 2009 Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc. Natl. Acad. Sci. USA 106: 16686-16691.
13. Chaudhary, K., S. Deb, N. Moniaux, M. P. Ponnusamy and S. K. Batra, 2007 Human RNA polymerase II-associated factor complex: dysregulation in cancer. Oncogene 26: 7499-7507.
14. Chen, Y., Y. Yamaguchi, Y. Tsugeno, J. Yamamoto, T. Yamada et al., 2009 DSIF, the Paf1 complex, and Tat-SF1 have nonredundant, cooperative roles in RNA polymerase II elongation. Genes Dev. 23: 2765-2777.
15. Cheung, V., G. Chua, N. N. Batada, C. R. Landry, S.W. Michnick et al., 2008 Chromatin-and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol. 6: e277.
16. Chu, Y., R. Simic, M. H. Warner, K. M. Arndt and G. Prelich, 2007 Regulation of histone modification and cryptic transcription by the Bur1 and Paf1 complexes. EMBO J. 26: 4646-4656.
17. Costa, F. F., 2005 Non-coding RNAs: new players in eukaryotic biology. Gene 357: 83-94.
18. Costa, P. J., and K. M. Arndt, 2000 Synthetic lethal interactions suggest a role for the Saccharomyces cerevisiae Rtf1 protein in transcription elongation. Genetics 156: 535-547.
19. de Almeida, S. F., A. Garcia-Sacristan, N. Custodio and M. Carmo-Fonseca, 2010 A link between nuclear RNA surveillance, the human exosome and RNA polymerase II transcriptional termination. Nucleic Acids Res. 38: 8015-8026.
20. Ding, L., M. Paszkowski-Rogacz, A. Nitzsche, M. M. Slabicki, A. K. Heninger et al., 2009 A genome-scale RNAi screen for Oct4 modulators defines a role of the Paf1 complex for embryonic stem cell identity. Cell Stem Cell 4: 403-415.
21. Ender, C., A. Krek, M. R. Friedlander, M. Beitzinger, L. Weinmann et al., 2008 A human snoRNA with microRNA-like functions. Mol. Cell 32: 519-528.
22. Exinger, F., and F. Lacroute, 1992 6-Azauracil inhibition of GTP biosynthesis in Saccharomyces cerevisiae. Curr. Genet. 22: 9-11.
23. Fan, X., Z. Moqtaderi, Y. Jin, Y. Zhang, X. S. Liu et al., 2010 Nucleosome depletion at yeast terminators is not intrinsic and can occur by a transcriptional mechanism linked to 39-end formation. Proc. Natl. Acad. Sci. USA 107: 17945-17950.
24. Fierz, B., C. Chatterjee, R. K. McGinty, M. Bar-Dagan, D. P. Raleigh et al., 2011 Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat. Chem. Biol. 7: 113-119.
25. Fleming, A. B., C. F. Kao, C. Hillyer, M. Pikaart and M. A. Osley, 2008 H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol. Cell 31: 57-66.
26. Goodrich, J. A., and J. F. Kugel, 2006 Non-coding-RNA regulators of RNA polymerase II transcription. Nat. Rev. Mol. Cell Biol. 7: 612-616.
27. Honorine, R., C. Mosrin-Huaman, N. Hervouet-Coste, D. Libri and A. R. Rahmouni, 2011 Nuclear mRNA quality control in yeast is mediated by Nrd1 co-transcriptional recruitment, as revealed by the targeting of Rho-induced aberrant transcripts. Nucleic Acids Res. 39: 2809-2820.
28. Houseley, J., and D. Tollervey, 2009 The many pathways of RNA degradation. Cell 136: 763-776.
29. Jaehning, J. A., 2010 The Paf1 complex: Platform or player in RNA polymerase II transcription? Biochim. Biophys. Acta 1799: 379-388.
30. Kim, J., M. Guermah, R. K. McGinty, J. S. Lee, Z. Tang et al., 2009 RAD6-Mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 137: 459-471.
31. Kim, J., M. Guermah and R. G. Roeder, 2010 The human PAF1 complex acts in chromatin transcription elongation both independently and cooperatively with SII/TFIIS. Cell 140: 491-503.
32. Kim, K. Y., and D. E. Levin, 2011 Mpk1 MAPK association with the paf1 complex blocks sen1-mediated premature transcription termination. Cell 144: 745-756.
33. Kim, M., S.H. Ahn, N. J. Krogan, J. F. Greenblatt and S. Buratowski, 2004 Transitions in RNA polymerase II elongation complexes at the 39 ends of genes. EMBO J. 23: 354-364.
34. Kim, T., and S. Buratowski, 2009 Dimethylation of H3K4 by Set1 recruits the Set3 histone deacetylase complex to 59 transcribed regions. Cell 137: 259-272.
35. Krivtsov, A. V., and S. A. Armstrong, 2007 MLL translocations, histone modifications and leukaemia stem-cell development. Nat. Rev. Cancer 7: 823-833.
36. Krogan, N. J., M. Kim, S. H. Ahn, G. Zhong, M. S. Kobor et al., 2002 RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol. Cell. Biol. 22: 6979-6992.
37. Krogan, N. J., J. Dover, A. Wood, J. Schneider, J. Heidt et al., 2003 The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol. Cell 11: 721-729.
38. Kuehner, J. N., and D. A. Brow, 2008 Regulation of a eukaryotic gene by GTP-dependent start site selection and transcription attenuation. Mol. Cell 31: 201-211.
39. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan et al., 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
40. Lee, J. S., A. Shukla, J. Schneider, S. K. Swanson, M. P. Washburn et al., 2007a Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131: 1084-1096.
41. Lee, W., D. Tillo, N. Bray, R. H. Morse, R. W. Davis et al., 2007b A high-resolution atlas of nucleosome occupancy in yeast. Nat. Genet. 39: 1235-1244.
42. Lickwar, C. R., B. Rao, A. A. Shabalin, A. B. Nobel, B. D. Strahl et al., 2009 The Set2/Rpd3S pathway suppresses cryptic transcription without regard to gene length or transcription frequency. PLoS One 4: e4886.
43. Lin, L., J. H. Zhang, L. M. Panicker and W. F. Simonds, 2008 The parafibromin tumor suppressor protein inhibits cell proliferation by repression of the c-myc proto-oncogene. Proc. Natl. Acad. Sci. USA 105: 17420-17425.
44. Mallardo, M., P. Poltronieri and O. F. D'Urso, 2008 Non-protein coding RNA biomarkers and differential expression in cancers: a review. J. Exp. Clin. Cancer Res. 27: 19.
45. Martin, D. G., K. Baetz, X. Shi, K. L. Walter, V. E. MacDonald et al., 2006 The Yng1p plant homeodomain finger is a methylhistone binding module that recognizes lysine 4-methylated histone H3. Mol. Cell. Biol. 26: 7871-7879.
46. Matera, A. G., R. M. Terns and M. P. Terns, 2007 Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs. Nat. Rev. Mol. Cell Biol. 8: 209-220.
47. Mavrich, T. N., I. P. Ioshikhes, B. J. Venters, C. Jiang, L. P. Tomsho et al., 2008 A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res. 18: 1073-1083.
48. Mayer, A., M. Lidschreiber, M. Siebert, K. Leike, J. Soding et al., 2010 Uniform transitions of the general RNA polymerase II transcription complex. Nat. Struct. Mol. Biol. 17: 1272-1278.
49. McGinty, R. K., J. Kim, C. Chatterjee, R. G. Roeder and T. W. Muir, 2008 Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation. Nature 453: 812-816.
50. Moniaux, N., C. Nemos, B. M. Schmied, S. C. Chauhan, S. Deb et al., 2006 The human homologue of the RNA polymerase II-associated factor 1 (hPaf1), localized on the 19q13 amplicon, is associated with tumorigenesis. Oncogene 25: 3247-3257.
51. Morillon, A., N. Karabetsou, A. Nair and J. Mellor, 2005 Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol. Cell 18: 723-734.
52. Mosimann, C., G. Hausmann and K. Basler, 2006 Parafibromin/Hyrax activates Wnt/Wg target gene transcription by direct association with beta-catenin/Armadillo. Cell 125: 327-341.
53. Mueller, C. L., and J. A. Jaehning, 2002 Ctr9, Rtf1, and Leo1 are components of the Paf1/RNA polymerase II complex. Mol. Cell. Biol. 22: 1971-1980.
54. Mueller, C. L., S. E. Porter, M. G. Hoffman and J. A. Jaehning, 2004 The Paf1 complex has functions independent of actively transcribing RNA polymerase II. Mol. Cell 14: 447-456.
55. Muhlrad, D., R. Hunter and R. Parker, 1992 A rapid method for localized mutagenesis of yeast genes. Yeast 8: 79-82.
56. Mutiu, A. I., S. M. Hoke, J. Genereaux, G. Liang and C. J. Brandl, 2007 The role of histone ubiquitylation and deubiquitylation in gene expression as determined by the analysis of an HTB1 (K123R) Saccharomyces cerevisiae strain. Mol. Genet. Genomics 277: 491-506.
57. Neil, H., C. Malabat, Y. d'Aubenton-Carafa, Z. Xu, L.M. Steinmetz et al., 2009 Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 457: 1038-1042.
58. Ng, H. H., R. M. Xu, Y. Zhang and K. Struhl, 2002 Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J. Biol. Chem. 277: 34655-34657.
59. Ng, H. H., S. Dole and K. Struhl, 2003a The Rtf1 component of the Paf1 transcriptional elongation complex is required for ubiquitination of histone H2B. J. Biol. Chem. 278: 33625-33628.
60. Ng, H. H., F. Robert, R. A. Young and K. Struhl, 2003b Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 11: 709-719.
61. Nordick, K., M. G. Hoffman, J. L. Betz and J. A. Jaehning, 2008 Direct interactions between the Paf1 complex and a cleavage and polyadenylation factor are revealed by dissociation of Paf1 from RNA polymerase II. Eukaryot. Cell 7: 1158-1167.
62. Oh, S., S. Park and S. van Nocker, 2008 Genic and global functions for Paf1C in chromatin modification and gene expression in Arabidopsis. PLoS Genet. 4: e1000077.
63. Pavri, R., B. Zhu, G. Li, P. Trojer, S. Mandal et al., 2006 Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125: 703-717.
64. Penheiter, K. L., T. M. Washburn, S. E. Porter, M. G. Hoffman and J. A. Jaehning, 2005 A posttranscriptional role for the yeast Paf1-RNA polymerase II complex is revealed by identification of primary targets. Mol. Cell 20: 213-223.
65. Pokholok, D. K., N. M. Hannett and R. A. Young, 2002 Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol. Cell 9: 799-809.
66. Pokholok, D. K., C. T. Harbison, S. Levine, M. Cole, N. M. Hannett et al., 2005 Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517-527.
67. Porter, S. E., T. M. Washburn, M. Chang and J. A. Jaehning, 2002 The yeast pafl-rNA polymerase II complex is required for full expression of a subset of cell cycle-regulated genes. Eukaryot. Cell 1: 830-842.
68. Preker, P., J. Nielsen, S. Kammler, S. Lykke-Andersen, M. S. Christensen et al., 2008 RNA exosome depletion reveals transcription upstream of active human promoters. Science 322: 1851-1854.
69. Rao, B., Y. Shibata, B. D. Strahl and J. D. Lieb, 2005 Dimethylation of histone H3 at lysine 36 demarcates regulatory and nonregulatory chromatin genome-wide. Mol. Cell. Biol. 25: 9447-9459.
70. Rondon, A. G., M. Gallardo, M. Garcia-Rubio and A. Aguilera, 2004 Molecular evidence indicating that the yeast PAF complex is required for transcription elongation. EMBO Rep. 5: 47-53.
71. Rose, M. D., F. Winston and P. Heiter, 1991 Methods in Yeast Genetics: A Laboratory Course Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
72. Rothstein, R., 1991 Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 194: 281-301.
73. Rozenblatt-Rosen, O., C. M. Hughes, S. J. Nannepaga, K. S. Shanmugam, T. D. Copeland et al., 2005 The parafibromin tumor suppressor protein is part of a human Paf1 complex. Mol. Cell. Biol. 25: 612-620.
74. Rozenblatt-Rosen, O., T. Nagaike, J. M. Francis, S. Kaneko, K. A. Glatt et al., 2009 The tumor suppressor Cdc73 functionally associates with CPSF and CstF 39 mRNA processing factors. Proc. Natl. Acad. Sci. USA 106: 755-760.
75. Santos-Rosa, H., R. Schneider, A. J. Bannister, J. Sherriff, B. E. Bernstein et al., 2002 Active genes are tri-methylated at K4 of histone H3. Nature 419: 407-411.
76. Shahbazian, M. D., K. Zhang and M. Grunstein, 2005 Histone H2B ubiquitylation controls processive methylation but not monomethylation by Dot1 and Set1. Mol. Cell 19: 271-277.
77. Shattuck, T. M., S. Valimaki, T. Obara, R. D. Gaz, O. H. Clark et al., 2003 Somatic and germ-line mutations of the HRPT2 gene in sporadic parathyroid carcinoma. N. Engl. J. Med. 349: 1722-1729.
78. Sheldon, K. E., D. M. Mauger and K. M. Arndt, 2005 A requirement for the Saccharomyces cerevisiae Paf1 complex in snoRNA 39 end formation. Mol. Cell 20: 225-236.
79. Shema, E., I. Tirosh, Y. Aylon, J. Huang, C. Ye et al., 2008 The histone H2B-specific ubiquitin ligase RNF20/hBRE1 acts as a putative tumor suppressor through selective regulation of gene expression. Genes Dev. 22: 2664-2676.
80. Shi, X., A. Finkelstein, A. J. Wolf, P. A. Wade, Z. F. Burton et al., 1996 Paf1p, an RNA polymerase II-associated factor in Saccharomyces cerevisiae, may have both positive and negative roles in transcription. Mol. Cell. Biol. 16: 669-676.
81. Shi, X., M. Chang, A. J. Wolf, C. H. Chang, A. A. Frazer-Abel et al., 1997 Cdc73p and Paf1p are found in a novel RNA polymerase II-containing complex distinct from the Srbp-containing holoenzyme. Mol. Cell. Biol. 17: 1160-1169.
82. Sikorski, R. S., and P. Hieter, 1989 A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
83. Squazzo, S. L., P. J. Costa, D. L. Lindstrom, K. E. Kumer, R. Simic et al., 2002 The Paf1 complex physically and functionally associates with transcription elongation factors in vivo. EMBO J. 21: 1764-1774.
84. Steinmetz, E. J., and D. A. Brow, 2003 Ssu72 protein mediates both poly(A)-coupled and poly(A)-independent termination of RNA polymerase II transcription. Mol. Cell. Biol. 23: 6339-6349.
85. Steinmetz, E. J., N. K. Conrad, D. A. Brow and J. L. Corden, 2001 RNA-binding protein Nrd1 directs poly(A)-independent 39-end formation of RNA polymerase II transcripts. Nature 413: 327-331.
86. Steinmetz, E. J., C. L. Warren, J. N. Kuehner, B. Panbehi, A. Z. Ansari et al., 2006 Genome-wide distribution of yeast RNA polymerase II and its control by Sen1 helicase. Mol. Cell 24: 735-746.
87. Stolinski, L. A., D. M. Eisenmann and K. M. Arndt, 1997 Identification of RTF1, a novel gene important for TATA site selection by TATA box-binding protein in Saccharomyces cerevisiae. Mol. Cell. Biol. 17: 4490-4500.
88. Sun, Z. W., and C. D. Allis, 2002 Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418: 104-108.
89. Swanson, M. S., E. A. Malone and F. Winston, 1991 SPT5, an essential gene important for normal transcription in Saccharomyces cerevisiae, encodes an acidic nuclear protein with a carboxyterminal repeat. Mol. Cell. Biol. 11: 3009-3019.
90. Taft, R. J., E. A. Glazov, T. Lassmann, Y. Hayashizaki, P. Carninci et al., 2009 Small RNAs derived from snoRNAs. RNA 15: 1233-1240.
91. Tenney, K., M. Gerber, A. Ilvarsonn, J. Schneider, M. Gause et al., 2006 Drosophila Rtf1 functions in histone methylation, gene expression, and Notch signaling. Proc. Natl. Acad. Sci. USA 103: 11970-11974.
92. Thiebaut, M., E. Kisseleva-Romanova, M. Rougemaille, J. Boulay and D. Libri, 2006 Transcription termination and nuclear degradation of cryptic unstable transcripts: a role for the nrd1-nab3 pathway in genome surveillance. Mol. Cell 23: 853-864.
93. Thiebaut, M., J. Colin, H. Neil, A. Jacquier, B. Seraphin et al., 2008 Futile cycle of transcription initiation and termination modulates the response to nucleotide shortage in S. cerevisiae. Mol. Cell 31: 671-682.
94. Wade, P. A., W. Werel, R. C. Fentzke, N. E. Thompson, J. F. Leykam et al., 1996 A novel collection of accessory factors associated with yeast RNA polymerase II. Protein Expr. Purif. 8: 85-90.
95. Walter, D., A. Matter and B. Fahrenkrog, 2010 Bre1p-mediated histone H2B ubiquitylation regulates apoptosis in Saccharomyces cerevisiae. J. Cell Sci. 123: 1931-1939.
96. Wang, G. G., J. Song, Z. Wang, H. L. Dormann, F. Casadio et al., 2009 Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 459: 847-851.
97. Warner, M. H., K. L. Roinick and K. M. Arndt, 2007 Rtf1 is a multifunctional component of the Paf1 complex that regulates gene expression by directing cotranscriptional histone modification. Mol. Cell. Biol. 27: 6103-6115.
98. Winston, F., C. Dollard and S. L. Ricupero-Hovasse, 1995 Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11: 53-55.
99. Winston, F., and P. Sudarsanam, 1998 The SAGA of Spt proteins and transcriptional analysis in yeast: past, present, and future. Cold Spring Harb. Symp. Quant. Biol. 63: 553-561.
100. Wood, A., J. Schneider, J. Dover, M. Johnston and A. Shilatifard, 2003 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: 34739-34742.
101. Wyce, A., T. Xiao, K. A. Whelan, C. Kosman, W. Walter et al., 2007 H2B ubiquitylation acts as a barrier to Ctk1 nucleosomal recruitment prior to removal by Ubp8 within a SAGA-related complex. Mol. Cell 27: 275-288.
102. Wyers, F., M. Rougemaille, G. Badis, J. C. Rousselle, M. E. Dufour et al., 2005 Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725-737.
103. Xiao, T., H. Hall, K. O. Kizer, Y. Shibata, M. C. Hall et al., 2003 Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev. 17: 654-663.
104. Yuan, G. C., Y. J. Liu, M. F. Dion, M. D. Slack, L. F. Wu et al., 2005 Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309: 626-630.
105. Zhu, B., S. S. Mandal, A. D. Pham, Y. Zheng, H. Erdjument-Bromage et al., 2005a The human PAF complex coordinates transcription with events downstream of RNA synthesis. Genes Dev. 19: 1668-1673.
106. Zhu, B., Y. Zheng, A. D. Pham, S. S. Mandal, H. Erdjument-Bromage et al., 2005b Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Mol. Cell 20: 601-611.