Histone H3 lysine 4 hypermethylation prevents aberrant nucleosome remodeling at the PHO5 promoter

Molecular and Cellular Biology

Volumn 31, Issue 15, 2011, Pages 3171-3181

  Wang, Shan Shan ^a   Zhou, Bo O ^a   Zhou, Jin Qiu ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE H3 LYSINE 4; LYSINE; PHO2 PROTEIN; PHO4 PROTEIN; PHO5 PROTEIN; RNA POLYMERASE II; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DEACETYLATION; GENE CONTROL; HISTONE METHYLATION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; TRANSCRIPTION REGULATION;

ACETYLATION; ACID PHOSPHATASE; CARRIER PROTEINS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HISTONE DEACETYLASES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HOMEODOMAIN PROTEINS; METHYLATION; NUCLEAR PROTEINS; NUCLEOSOMES; ORGANISMS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC;

SACCHAROMYCES CEREVISIAE;

EID: 79960303572     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05017-11     Document Type: Article

References (72)

1. Adkins, M. W., S. R. Howar, and J. K. Tyler. 2004. Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. Mol. Cell 14:657-666.
2. 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.
3. Adkins, M. W., S. K. Williams, J. Linger, and J. K. Tyler. 2007. Chromatin disassembly from the PHO5 promoter is essential for the recruitment of the general transcription machinery and coactivators. Mol. Cell. Biol. 27:6372-6382.
4. Almer, A., and W. Hörz. 1986. Nuclease hypersensitive regions with adjacent positioned nucleosomes mark the gene boundaries of the PHO5/PHO3 locus in yeast. EMBO J. 5:2681-2687.
5. Almer, A., H. Rudolph, A. Hinnen, and W. Hörz. 1986. Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J. 5:2689-2696.
6. Barbaric, S., M. Munsterkotter, J. Svaren, and W. Hörz. 1996. The homeodomain protein Pho2 and the basic-helix-loop-helix protein Pho4 bind DNA cooperatively at the yeast PHO5 promoter. Nucleic Acids Res. 24:4479-4486.
7. Barbaric, S., H. Reinke, and W. Hörz. 2003. Multiple mechanistically distinct functions of SAGA at the PHO5 promoter. Mol. Cell. Biol. 23:3468-3476.
8. Berretta, J., M. Pinskaya, and A. Morillon. 2008. A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae. Genes Dev. 22:615-626.
9. 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.
10. Briggs, S. D., et al. 2001. Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 15:3286-3295.
11. Cairns, B. R. 2005. Chromatin remodeling complexes: strength in diversity, precision through specialization. Curr. Opin. Genet. Dev. 15:185-190.
12. Camblong, J., et al. 2009. Trans-acting antisense RNAs mediate transcriptional gene cosuppression in S. cerevisiae. Genes Dev. 23:1534-1545.
13. Carmen, A. A., S. E. Rundlett, and M. Grunstein. 1996. HDA1 and HDA3 are components of a yeast histone deacetylase (HDA) complex. J. Biol. Chem. 271:15837-15844.
14. Carrozza, M. J., et al. 2005. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123:581-592.
15. Carvin, C. D., and M. P. Kladde. 2004. Effectors of lysine 4 methylation of histone H3 in Saccharomyces cerevisiae are negative regulators of PHO5 and GAL1-10. J. Biol. Chem. 279:33057-33062.
16. Colina, A. R., and D. Young. 2005. Raf60, a novel component of the Rpd3 histone deacetylase complex required for Rpd3 activity in Saccharomyces cerevisiae. J. Biol. Chem. 280:42552-42556.
17. Dhasarathy, A., and M. P. Kladde. 2005. Promoter occupancy is a major determinant of chromatin remodeling enzyme requirements. Mol. Cell. Biol. 25:2698-2707.
18. Ertel, F., et al. 2010. In vitro reconstitution of PHO5 promoter chromatin remodeling points to a role for activator-nucleosome competition in vivo. Mol. Cell. Biol. 30:4060-4076.
19. Fascher, K. D., J. Schmitz, and W. Hörz. 1990. Role of trans-activating proteins in the generation of active chromatin at the PHO5 promoter in S. cerevisiae. EMBO J. 9:2523-2528.
20. Fascher, K. D., J. Schmitz, and W. Hörz. 1993. Structural and functional requirements for the chromatin transition at the PHO5 promoter in Saccharomyces cerevisiae upon PHO5 activation. J. Mol. Biol. 231:658-667.
21. Gaudreau, L., A. Schmid, D. Blaschke, M. Ptashne, and W. Hörz. 1997. RNA polymerase II holoenzyme recruitment is sufficient to remodel chromatin at the yeast PHO5 promoter. Cell 89:55-62.
22. Gregory, P. D., et al. 1998. Absence of Gcn5 HAT activity defines a novel state in the opening of chromatin at the PHO5 promoter in yeast. Mol. Cell 1:495-505.
23. Gregory, P. D., A. Schmid, M. Zavari, M. Munsterkotter, and W. Hörz. 1999. Chromatin remodelling at the PHO8 promoter requires SWI-SNF and SAGA at a step subsequent to activator binding. EMBO J. 18:6407-6414.
24. Houseley, J., L. Rubbi, M. Grunstein, D. Tollervey, and M. Vogelauer. 2008. A ncRNA modulates histone modification and mRNA induction in the yeast GAL gene cluster. Mol. Cell 32:685-695.
25. Kadosh, D., and K. Struhl. 1998. Histone deacetylase activity of Rpd3 is important for transcriptional repression in vivo. Genes Dev. 12:797-805.
26. Kasten, M. M., S. Dorland, and D. J. Stillman. 1997. A large protein complex containing the yeast Sin3p and Rpd3p transcriptional regulators. Mol. Cell. Biol. 17:4852-4858.
27. Keogh, M. C., et al. 2005. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123:593-605.
28. Kolodziej, P., and R. A. Young. 1989. RNA polymerase II subunit RPB3 is an essential component of the mRNA transcription apparatus. Mol. Cell. Biol. 9:5387-5394.
29. Korber, P., et al. 2006. The histone chaperone Asf1 increases the rate of histone eviction at the yeast PHO5 and PHO8 promoters. J. Biol. Chem. 281:5539-5545.
30. Kornberg, R. D. 1974. Chromatin structure: a repeating unit of histones and DNA. Science 184:868-871.
31. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
32. Krogan, N. J., 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.
33. Lau, W. W., K. R. Schneider, and E. K. O'Shea. 1998. A genetic study of signaling processes for repression of PHO5 transcription in Saccharomyces cerevisiae. Genetics 150:1349-1359.
34. Lechner, T., et al. 2000. 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. 275:40961-40966.
35. 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.
36. Li, B., M. Carey, and J. L. Workman. 2007. The role of chromatin during transcription. Cell 128:707-719.
37. Li, B., et al. 2007. Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science 316:1050-1054.
38. Li, B., et al. 2007. Infrequently transcribed long genes depend on the Set2/Rpd3S pathway for accurate transcription. Genes Dev. 21:1422-1430.
39. Li, B., et al. 2009. Histone H3 lysine 36 dimethylation (H3K36me2) is sufficient to recruit the Rpd3s histone deacetylase complex and to repress spurious transcription. J. Biol. Chem. 284:7970-7976.
40. Loewith, R., et al. 2001. 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. 276:24068-24074.
41. McManus, K. J., V. L. Biron, R. Heit, D. A. Underhill, and M. J. Hendzel. 2006. Dynamic changes in histone H3 lysine 9 methylations: identification of a mitosis-specific function for dynamic methylation in chromosome congression and segregation. J. Biol. Chem. 281:8888-8897.
42. Mellor, J. 2006. Dynamic nucleosomes and gene transcription. Trends Genet. 22:320-329.
43. 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.
44. Nourani, A., R. T. Utley, S. Allard, and J. Cêté. 2004. Recruitment of the NuA4 complex poises the PHO5 promoter for chromatin remodeling and activation. EMBO J. 23:2597-2607.
45. O'Neill, E. M., A. Kaffman, E. R. Jolly, and E. K. O'Shea. 1996. Regulation of PHO4 nuclear localization by the PHO80-PHO85 cyclin-CDK complex. Science 271:209-212.
46. Oshima, Y., N. Ogawa, and S. Harashima. 1996. Regulation of phosphatase synthesis in Saccharomyces cerevisiae-a review. Gene 179:171-177.
47. Pinskaya, M., S. Gourvennec, and A. Morillon. 2009. H3 lysine 4 di- and tri-methylation deposited by cryptic transcription attenuates promoter activation. EMBO J. 28:1697-1707.
48. Pokholok, D. K., et al. 2005. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122:517-527.
49. Puig, S., M. Lau, and D. J. Thiele. 2004. Cti6 is an Rpd3-Sin3 histone deacetylase-associated protein required for growth under iron-limiting conditions in Saccharomyces cerevisiae. J. Biol. Chem. 279:30298-30306.
50. Reinke, H., P. D. Gregory, and W. Hörz. 2001. A transient histone hyperacetylation signal marks nucleosomes for remodeling at the PHO8 promoter in vivo. Mol. Cell 7:529-538.
51. Reinke, H., and W. Hörz. 2003. Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol. Cell 11:1599-1607.
52. Schultz, J. 1936. Variegation in Drosophila and the inert chromosome regions. Proc. Natl. Acad. Sci. U. S. A. 22:27-33.
53. 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.
54. Sharma, V. M., R. S. Tomar, A. E. Dempsey, and J. C. Reese. 2007. Histone deacetylases RPD3 and HOS2 regulate the transcriptional activation of DNA damage-inducible genes. Mol. Cell. Biol. 27:3199-3210.
55. Shi, X., et al. 2006. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442:96-99.
56. Shi, X., et al. 2007. Proteome-wide analysis in Saccharomyces cerevisiae identifies several PHD fingers as novel direct and selective binding modules of histone H3 methylated at either lysine 4 or lysine 36. J. Biol. Chem. 282:2450-2455.
57. Shilatifard, A. 2006. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu. Rev. Biochem. 75:243-269.
58. Shogren-Knaak, M., et al. 2006. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311:844-847.
59. Sims, R. J., III, and D. Reinberg. 2006. Histone H3 Lys 4 methylation: caught in a bind? Genes Dev. 20:2779-2786.
60. Straka, C., and W. Hörz. 1991. A functional role for nucleosomes in the repression of a yeast promoter. EMBO J. 10:361-368.
61. Suganuma, T., and J. L. Workman. 2008. Crosstalk among histone modifications. Cell 135:604-607.
62. Svaren, J., and W. Hörz. 1995. Interplay between nucleosomes and transcription factors at the yeast PHO5 promoter. Semin. Cell Biol. 6:177-183.
63. Svaren, J., J. Schmitz, and W. Hörz. 1994. The transactivation domain of Pho4 is required for nucleosome disruption at the PHO5 promoter. EMBO J. 13:4856-4862.
64. Szerlong, H. J., J. E. Prenni, J. K. Nyborg, and J. C. Hansen. 2010. Activatordependent p300 acetylation of chromatin in vitro: enhancement of transcription by disruption of repressive nucleosome-nucleosome interactions. J. Biol. Chem. 285:31954-31964.
65. Uhler, J. P., C. Hertel, and J. Q. Svejstrup. 2007. A role for noncoding transcription in activation of the yeast PHO5 gene. Proc. Natl. Acad. Sci. U. S. A. 104:8011-8016.
66. Venter, U., J. Svaren, J. Schmitz, A. Schmid, and W. Hörz. 1994. A nucleosome precludes binding of the transcription factor Pho4 in vivo to a critical target site in the PHO5 promoter. EMBO J. 13:4848-4855.
67. Wang, Z., et al. 2009. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138:1019-1031.
68. Williams, S. K., D. Truong, and J. K. Tyler. 2008. Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc. Natl. Acad. Sci. U. S. A. 105:9000-9005.
69. Xu, Z., et al. 2009. Bidirectional promoters generate pervasive transcription in yeast. Nature 457:1033-1037.
70. Yang, X. J., and E. Seto. 2008. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 9:206-218.
71. Zhang, Y., et al. 1998. SAP30, a novel protein conserved between human and yeast, is a component of a histone deacetylase complex. Mol. Cell 1:1021-1031.
72. Zhou, J., B. O. Zhou, B. A. Lenzmeier, and J. Q. Zhou. 2009. Histone deacetylase Rpd3 antagonizes Sir2-dependent silent chromatin propagation. Nucleic Acids Res. 37:3699-3713.