Roles for Ctk1 and Spt6 in regulating the different methylation states of histone H3 lysine 36

Molecular and Cellular Biology

Volumn 28, Issue 16, 2008, Pages 4915-4926

  Youdell, Michael L ^a   Kizer, Kelby O ^b   Kisseleva Romanova, Elena ^a   Fuchs, Stephen M ^b   Duro, Eris ^a   Strahl, Brian D ^b   Mellor, Jane ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; LYSINE; PROTEIN; PROTEIN CTK 1; PROTEIN SPT 6;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEACETYLATION; ENZYME PHOSPHORYLATION; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN;

ACETYLATION; CHROMATIN; GENE EXPRESSION REGULATION, FUNGAL; HISTONES; LYSINE; METHYLATION; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 49449095333     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00001-08     Document Type: Article

References (49)

1. Adkins, M. W., and J. K. Tyler. 2006. Transcriptional activators are dispensable for transcription in the absence of spt6-mediated chromatin reassembly of promoter regions. Mol. Cell 21:405-416.
2. Belle, A., A. Tanay, L. Bitincka, R. Shamir, and E. K. O'Shea. 2006. Quantification of protein half-lives in the budding yeast proteome. Proc. Natl. Acad. Sci. USA 103:13004-13009.
3. Biswas, D., R. Dutta-Biswas, D. Mitra, Y. Shibata, B. D. Strahl, T. Formosa, and D. J. Stillman. 2006. Opposing roles for Set2 and yFACT in regulating TBP binding at promoters. EMBO J. 25:4479-4489.
4. Bortvin, A., and F. Winston. 1996. Evidence that Spt6p controls chromatin structure by a direct interaction with histones. Science 272:1473-1476.
5. Carrozza, M. J., B. Li, L. Florens, T. Suganuma, S. K. Swanson, K. K. Lee, W. J. Shia, S. Anderson, J. Yates, M. P. Washburn, and J. L. Workman. 2005. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123:581-592.
6. Cho, E. J., M. S. Kobor, M. Kim, J. Greenblatt, and S. Buratowski. 2001. Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser 2 of the RNA polymerase II C-terminal domain. Genes Dev. 15:3319-3329.
7. 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.
8. Chu, Y., A. Sutton, R. Sternglanz, and G. Prelich. 2006. The BUR1 cyclin-dependent protein kinase is required for the normal pattern of histone methylation by SET2. Mol. Cell. Biol. 26:3029-3038.
9. Clark-Adams, C. D., and F. Winston. 1987. The SPT6 gene is essential for growth and is required for delta-mediated transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 7:679-686.
10. Hartzog, G. A., T. Wada, H. Handa, and F. Winston. 1998. Evidence that Spt4, Spt5 and Spt6 control transcription elongation by RNA polymerase II. Genes Dev. 12:357-369.
11. Joshi, A. A., and K. Struhl. 2005. Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol. Cell 20:971-978.
12. Kaplan, C. D., M. J. Holland, and F. Winston. 2005. Interaction between transcription elongation factors and mRNA 3′-end formation at the Saccharomyces cerevisiae GAL10-GAL7 locus. J. Biol. Chem. 280:913-922.
13. Kaplan, C. D., L. Laprade, and F. Winston. 2003. Transcription elongation factors repress transcription initiation from cryptic sites. Science 301:1096-1099.
14. Kaplan, C. D., J. R. Morris, C.-T. Wu, and F. Winston. 2000. Spt5 and Spt6 are associated with active transcription and have characteristics of general elongation factors in D. melanogaster. Genes Dev. 14:2623-2634.
15. Keogh, M. C., S. K. Kurdistani, S. A. Morris, S. H. Ahn, V. Podolny, S. R. Collins, M. Schuldiner, K. Chin, T. Punna, N. J. Thompson, C. Boone, A. Emili, J. S. Weissman, T. R. Hughes, B. D. Strahl, M. Grunstein, J. F. Greenblatt, S. Buratowski, and N. J. Krogan. 2005. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123:593-605.
16. Kizer, K. O., H. P. Phatnani, Y. Shibata, H. Hall, A. L. Greenleaf, and B. D. Strahl. 2005. A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol. Cell. Biol. 25:3305-3316.
17. Kizer, K. O., T. Xiao, and B. D. Strahl. 2006. Accelerated nuclei preparation and methods for analysis of histone modifications in yeast. Methods 40:296-302.
18. Krogan, N. J., M. Kim, S. H. Ahn, G. Zhong, M. S. Kobor, G. Cagney, A. Emili, A. Shilatifard, S. Buratowski, and J. F. Greenblatt. 2002. RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol. Cell. Biol. 22:6979-6992.
19. Krogan, N. J., M. Kim, A. Tong, A. Golshani, G. Cagney, V. Canadien, D. P. Richards, B. K. Beattie, A. Emili, C. Boone, A. Shilatifard, S. Buratowski, and J. Greenblatt. 2003. Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 23:4207-4218.
20. Landry, J., A. Sutton, T. Hesman, J. Min, R.-M. Xu, M. Johnston, and R. Sternglanz. 2003. Set2-catalyzed methylation of histone H3 represses basal expression of GAL4 in Saccharomyces cerevisiae. Mol. Cell. Biol. 23:5972-5978.
21. Lee, J. M., and A. L. Greenleaf. 1991. CTD kinase large subunit is encoded by CTK1, a gene required for normal growth of Saccharomyces cerevisiae. Gene Expr. 1:149-167.
22. Li, B., M. Gogol, M. Carey, D. Lee, C. Seidel, and J. L. Workman. 2007. Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science 316:1050-1054.
23. Li, B., M. Gogol, M. Carey, S. G. Pattenden, C. Seidel, and J. L. Workman. 2007. Infrequently transcribed long genes depend on the Set2/Rpd3S pathway for accurate transcription. Genes Dev. 21:1422-1430.
24. Li, B., L. Howe, S. Anderson, J. R. Yates III, and J. L. Workman. 2003. The Set2 histone methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 278:8897-8903.
25. Li, J., D. Moazed, and S. P. Gygi. 2002. Association of the histone methyltransferase Set2 with RNA polymerase II plays a role in transcription elongation. J. Biol. Chem. 277:49383-49388.
26. Li, M., H. P. Phatnani, Z. Guan, H. Sage, A. L. Greenleaf, and P. Zhou. 2005. Solution structure of the Set2-Rpb1 interacting domain of human Set2 and its interaction with the hyperphosphorylated C-terminal domain of Rpb1. Proc. Natl. Acad. Sci. USA 102:17636-17641.
27. Lindstrom, D. L., S. L. Squazzo, N. Muster, T. A. Burckin, K. C. Wachter, C. A. Emigh, J. A. McCleery, J. R. Yates IIII, and G. A. Hartzog. 2003. Dual roles for Spt5 in pre-mRNA processing and transcription elongation revealed by identification of Spt5-associated proteins. Mol. Cell. Biol. 23:1368-1378.
28. Liu, C. L., T. Kaplan, M. Kim, S. Buratowski, S. L. Schreiber, N. Friedman, and O. J. Rando. 2005. Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 3:e28.
29. Longtine, M. S., A. McKenzie, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
30. Meluh, P. D., and J. R. Broach. 1999. Immunological analysis of yeast chromatin. Methods Enzymol. 304:414-430.
31. 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.
32. Mumberg, D., R. Muller, and M. Funk. 1995. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156:119-122.
33. Murray, S., R. Udupa, S. Yao, G. A. Hartzog, and G. Prelich. 2001. Phosphorylation of the RNA polymerase II carboxy-terminal domain by the Bur1 cyclin dependent kinase. Mol. Cell. Biol. 21:4089-4096.
34. Nelson, C. J., H. Santos-Rosa, and T. Kouzarides. 2006. Proline isomerization of histone H3 regulates lysine methylation and gene expression. Cell 126:905-916.
35. Nonet, M., D. Sweetser, and R. A. Young. 1987. Functional redundancy and structural polymorphism in the large subunit of RNA polymerase II. Cell 50:909-915.
36. Patturajan, M., N. K. Conrad, D. B. Bregman, and J. L. Corden. 1999. Yeast carboxyl-terminal domain kinase I positively and negatively regulates RNA polymerase II carboxyl-terminal domain phosphorylation. J. Biol. Chem. 274:27823-27828.
37. 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.
38. Pokholok, D. K., C. T. Harbison, S. Levine, M. Cole, N. M. Hannett, T. I. Lee, G. W. Bell, K. Walker, P. A. Rolfe, E. Herbolsheimer, J. Zeitlinger, F. Lewitter, D. K. Gifford, and R. A. Young. 2005. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122:517-527.
39. 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.
40. Rother, S., and K. Strasser. 2007. The RNA polymerase II CTD kinase Ctk1 functions in translation elongation. Genes Dev. 21:1409-1421.
41. Schaft, D., A. Roguev, K. M. Kotovic, A. Shevchenko, M. Sarov, A. Shevchenko, K. M. Neugebauer, and A. F. Stewart. 2003. The histone 3 lysine 36 methyltransferase, SET2, is involved in transcriptional elongation. Nucleic Acids Res. 31:2475-2482.
42. Strahl, B. D., P. A. Grant, S. D. Briggs, Z. W. Sun, J. R. Bone, J. A. Caldwell, S. Mollah, R. G. Cook, J. Shabanowitz, D. F. Hunt, and C. D. Allis. 2002. Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol. Cell. Biol. 22:1298-1306.
43. Tompa, R., and H. D. Madhani. 2007. Histone H3 lysine 36 methylation antagonizes silencing in Saccharomyces cerevisiae independently of the Rpd3S histone deacetylase complex. Genetics 175:585-593.
44. Tripic, T., D. G. Edmondson, J. K. Davie, B. D. Strahl, and S. Y. Dent. 2006. The Set2 methyltransferase associates with Ssn6 yet Tup1-Ssn6 repression is independent of histone methylation. Biochem. Biophys. Res. Commun. 339:905-914.
45. Vojnic, E., B. Simon, B. D. Strahl, M. Sattler, and P. Cramer. 2006. Structure and carboxyl-terminal domain (CTD) binding of the Set2 SRI domain that couples histone H3 Lys36 methylation to transcription. J. Biol. Chem. 281: 13-15.
46. Xiao, T., H. Hall, K. O. Kizer, Y. Shibata, M. C. Hall, C. H. Borchers, and B. D. Strahl. 2003. Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev. 17:654-663.
47. Xiao, T., Y. Shibata, B. Rao, R. N. Laribee, R. O'Rourke, M. J. Buck, J. F. Greenblatt, N. J. Krogan, J. D. Lieb, and B. D. Strahl. 2007. The RNA polymerase II kinase Ctk1 regulates positioning of a 5′ histone methylation boundary along genes. Mol. Cell. Biol. 27:721-731.
48. Yoh, S. M., H. Cho, L. Pickle, R. M. Evans, and K. A. Jones. 2007. The Spt6 SH2 domain binds Ser2-P RNAPII to direct Iws1-dependent mRNA splicing and export. Genes Dev. 21:160-174.
49. Zhang, W., J. R. Bone, D. G. Edmondson, B. M. Turner, and S. Y. Roth. 1998. Essential and redundant functions of histone acetylation revealed by mutation of target lysines and loss of the Gcn5p acetyltransferase. EMBO J. 17:3155-3167.