Dimethylation of histone H3 at lysine 36 demarcates regulatory and nonregulatory chromatin genome-wide

Molecular and Cellular Biology

Volumn 25, Issue 21, 2005, Pages 9447-9459

  Rao, Bhargavi ^a   Shibata, Yoichiro ^b   Strahl, Brian D ^a,b   Lieb, Jason D ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE H3; LYSINE; METHYLTRANSFERASE; METHYLTRANSFERASE SET2P; PEPTIDE; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; DNA MICROARRAY; DNA TEMPLATE; ENZYME ACTIVITY; GENE AMPLIFICATION; GENETIC TRANSCRIPTION; GENOME; METHYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; YEAST;

CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA PRIMERS; GENOME, FUNGAL; HISTONES; LYSINE; METHYLATION; METHYLTRANSFERASES; NUCLEOSOMES; OPEN READING FRAMES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 27144458417     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.21.9447-9459.2005     Document Type: Article

References (57)

1. Bannister, A. J., R. Schneider, F. A. Myers, A. W. Thorne, C. Crane-Robinson, and T. Kouzarides. 2005. Spatial distribution of di-and tri-methyl lysine 36 of histone H3 at active genes. J. Biol. Chem. 280:17732-17736.
2. Bernstein, B. E., C. L. Liu, E. L. Humphrey, E. O. Perlstein, and S. L. Schreiber. 2004. Global nucleosome occupancy in yeast. Genome Biol. 5:R62.
3. Boeger, H., J. Griesenbeck, J. S. Strattan, and R. D. Kornberg. 2003. Nucleosomes unfold completely at a transcriptionally active promoter. Mol. Cell 11:1587-1598.
4. Boeger, H., J. Griesenbeck, J. S. Strattan, and R. D. Kornberg. 2004. Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Mol. Cell 14:667-673.
5. Bohlander, S. K., R. Espinosa III, M. M. Le Beau, J. D. Rowley, and M. O. Diaz. 1992. A method for the rapid sequence-independent amplification of microdissected chromosomal material. Genomics 13:1322-1324.
6. Buck, M. J., and J. D. Lieb. 2004. ChIP-chip: considerations for the design, analysis, and application of genome-wide chromatin immunoprecipitation experiments. Genomics 83:349-360.
7. Causton, H. C., B. Ren, S. S. Koh, C. T. Harbison, E. Kanin, E. G. Jennings, T. I. Lee, H. L. True, E. S. Lander, and R. A. Young. 2001. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 12:323-337.
8. 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.
9. Deckert, J., and K. Struhl. 2002. Targeted recruitment of Rpd3 histone deacetylase represses transcription by inhibiting recruitment of Swi/Snf, SAGA, and TATA binding protein. Mol. Cell. Biol. 22:6458-6470.
10. Gasch, A. P., P. T. Spellman, C. M. Kao, O. Carmel-Harel, M. B. Eisen, G. Storz, D. Botstein, and P. O. Brown. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11: 4241-4257.
11. Gavin, A. C., M. Bosche, R. Krause, P. Grandi, M. Marzioch, A. Bauer, J. Schultz, J. M. Rick, A. M. Michon, C. M. Cruciat, M. Remor, C. Hofert, M. Schelder, M. Brajenovic, H. Ruffner, A. Merino, K. Klein, M. Hudak, D. Dickson, T. Rudi, V. Gnau, A. Bauch, S. Bastuck, B. Huhse, C. Leutwein, M. A. Heurtier, R. R. Copley, A. Edelmann, E. Querfurth, V. Rybin, G. Drewes, M. Raida, T. Bouwmeester, P. Bork, B. Seraphin, B. Kuster, G. Neubauer, and G. Superti-Furga. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141-147.
12. Gerton, J. L., J. DeRisi, R. Shroff, M. Lichten, P. O. Brown, and T. D. Petes. 2000. Inaugural article: global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 97:11383-11390.
13. Hanlon, S. E., and J. D. Lieb. 2004. Progress and challenges in profiling the dynamics of chromatin and transcription factor binding with DNA microarrays. Curr. Opin. Genet. Dev. 14:697-705.
14. Holstege, F. C., E. G. Jennings, J. J. Wyrick, T. I. Lee, C. J. Hengartner, M. R. Green, T. R. Golub, E. S. Lander, and R. A. Young. 1998. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95:717-728.
15. Hurowitz, E. H., and P. O. Brown. 2003. Genome-wide analysis of mRNA lengths in Saccharomyces cerevisiae. Genome Biol. 5:R2.
16. Iyer, V. R., C. E. Horak, C. S. Scafe, D. Botstein, M. Snyder, and P. O. Brown. 2001. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 409:533-538.
17. Jones, J. C., H. P. Phatnani, T. A. Haystead, J. A. MacDonald, S. M. Alam, and A. L. Greenleaf. 2004. C-terminal repeat domain kinase I phosphorylates Ser2 and Ser5 of RNA polymerase II C-terminal domain repeats. J. Biol. Chem. 279:24957-24964.
18. 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.
19. Komarnitsky, P., E. J. Cho, and S. Buratowski. 2000. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14:2452-2460.
20. Kristjuhan, A., and J. Q. Svejstrup. 2004. Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. EMBO J. 23: 4243-4252.
21. 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.
22. 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.
23. Kuo, M. H., and C. D. Allis. 1999. In vivo cross-linking and immunoprecipitation for studying dynamic protein:DNA associations in a chromatin environment. Methods 19:425-433.
24. Kuo, M. H., E. vom Baur, K. Struhl, and C. D. Allis. 2000. Gcn4 activator targets Gcn5 histone acetyltransferase to specific promoters independently of transcription. Mol. Cell 6:1309-1320.
25. 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.
26. Lee, C. K., Y. Shibata, B. Rao, B. D. Strahl, and J. D. Lieb. 2004. Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat. Genet. 36:900-905.
27. Lee, D. Y., J. J. Hayes, D. Pruss, and A. P. Wolffe. 1993. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 72:73-84.
28. 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.
29. 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.
30. Licatalosi, D. D., G. Geiger, M. Minet, S. Schroeder, K. Cilli, J. B. McNeil, and D. L. Bentley. 2002. Functional interaction of yeast pre-mRNA 3′ end processing factors with RNA polymerase II. Mol. Cell 9:1101-1111.
31. Lieb, J. D., X. Liu, D. Botstein, and P. O. Brown. 2001. Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association. Nat. Genet. 28:327-334.
32. Loden, M., and B. van Steensel. 2005. Whole-genome views of chromatin structure. Chromosome Res. 13:289-298.
33. Mai, X., S. Chou, and K. Struhl. 2000. Preferential accessibility of the yeast his3 promoter is determined by a general property of the DNA sequence, not by specific elements. Mol. Cell. Biol. 20:6668-6676.
34. Martens, J. A., and F. Winston. 2003. Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr. Opin. Genet. Dev. 13: 136-142.
35. Morse, R. H. 2000. RAP, RAP, open up! New wrinkles for RAP1 in yeast. Trends Genet. 16:51-53.
36. Nagy, P. L., M. L. Cleary, P. O. Brown, and J. D. Lieb. 2003. Genomewide demarcation of RNA polymerase II transcription units revealed by physical fractionation of chromatin. Proc. Natl. Acad. Sci. USA 100:6364-6369.
37. Ng, H. H., D. N. Ciccone, K. B. Morshead, M. A. Oettinger, and K. Struhl. 2003. Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: a potential mechanism for position-effect variegation. Proc. Natl. Acad. Sci. USA 100:1820-1825.
38. Ng, H. H., Q. Feng, H. Wang, H. Erdjument-Bromage, P. Tempst, Y. Zhang, and K. Struhl. 2002. Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev. 16:1518-1527.
39. Ng, H. H., F. Robert, R. A. Young, and K. Struhl. 2003. 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.
40. 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.
41. Rea, S., F. Eisenhaber, D. O'Carroll, B. D. Strahl, Z. W. Sun, M. Schmid, S. Opravil, K. Mechtler, C. P. Ponting, C. D. Allis, and T. Jenuwein. 2000. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593-599.
42. Reid, J. L., Z. Moqtaderi, and K. Struhl. 2004. Eaf3 regulates the global pattern of histone acetylation in Saccharomyces cerevisiae. Mol. Cell. Biol. 24:757-764.
43. Reinke, H., and W. Horz. 2003. Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol. Cell 11:1599-1607.
44. Rice, J. C., and C. D. Allis. 2001. Histone methylation versus histone acetylation: new insights into epigenetic regulation. Curr. Opin. Cell Biol. 13: 263-273.
45. Schaft, D., A. Roguev, K. M. Kotovic, A. Shevchenko, M. Sarov, 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.
46. Schwabish, M. A., and K. Struhl. 2004. Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 24:10111-10117.
47. Sekinger, E. A., Z. Moqtaderi, and K. Struhl. 2005. Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Mol. Cell 18:735-748.
48. Sewack, G. F., T. W. Ellis, and U. Hansen. 2001. Binding of TATA binding protein to a naturally positioned nucleosome is facilitated by histone acetylation. Mol. Cell. Biol. 21:1404-1415.
49. Squazzo, S. L., P. J. Costa, D. L. Lindstrom, K. E. Kumer, R. Simic, J. L. Jennings, A. J. Link, K. M. Arndt, and G. A. Hartzog. 2002. The Paf1 complex physically and functionally associates with transcription elongation factors in vivo. EMBO J. 21:1764-1774.
50. Stapleton, A., and T. D. Petes. 1991. The Tn3 beta-lactamase gene acts as a hotspot for meiotic recombination in yeast. Genetics 127:39-51.
51. 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.
52. Svaren, J., and W. Horz. 1997. Transcription factors vs nucleosomes: regulation of the PHO5 promoter in yeast. Trends Biochem. Sci. 22:93-97.
53. Turner, B. M. 2005. Reading signals on the nucleosome with a new nomenclature for modified histones. Nat. Struct. Mol. Biol. 12:110-112.
54. van Steensel, B., and S. Henikoff. 2003. Epigenomic profiling using microarrays. BioTechniques 35:346-357.
55. Wu, T. C., and M. Lichten. 1994. Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science 263:515-518.
56. 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.
57. Xiao, T., C.-F. Kao, N. J. Krogan, Z.-W. Sun, J. F. Greenblatt, M. A. Osley, and B. D. Strahl. 2005. Histone H2B ubiquitylation is associated with elongating RNA polymerase II. Mol. Cell. Biol. 25:637-651.