Linking Cell Cycle to Histone Modifications: SBF and H2B Monoubiquitination Machinery and Cell-Cycle Regulation of H3K79 Dimethylation

Molecular Cell

Volumn 35, Issue 5, 2009, Pages 626-641

  Schulze, Julia M ^a,b   Jackson, Jessica ^c   Nakanishi, Shima ^e   Gardner, Jennifer M ^e   Hentrich, Thomas ^d   Haug, Jeff ^e   Johnston, Mark ^c   Jaspersen, Sue L ^e,f   Kobor, Michael S ^a,b   Shilatifard, Ali ^e  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d SIMON FRASER UNIVERSITY   (Canada)

^e STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^f UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

CELLCYCLE; DNA; PROTEINS

Indexed keywords

HISTONE H2B; HISTONE H3; HISTONE H3 ON LYSINE 79; NEGATIVE REULATOR OF MBF TARGETS 1; REPRESSOR PROTEIN; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MBF; TRANSCRIPTION FACTOR SBF; UNCLASSIFIED DRUG; WHI3 PROTEIN;

ARTICLE; BINDING SITE; CELL CYCLE G1 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CONTROLLED STUDY; DOT HYBRIDIZATION; FUNGAL GENE; GENE DELETION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC SCREENING; GENETIC TRANSCRIPTION; NONHUMAN; PROMOTER REGION; PROTEIN METHYLATION; PROTEIN MODIFICATION; PROTEOMICS; REGULATOR GENE; UBIQUITINATION; YEAST;

CELL CYCLE; DNA, INTERGENIC; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; LYSINE; METHYLATION; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OPEN READING FRAMES; PROMOTER REGIONS, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; REPRESSOR PROTEINS; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

EID: 69749117490     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.07.017     Document Type: Article

References (49)

1. Altaf M., Utley R.T., Lacoste N., Tan S., Briggs S.D., and Côté J. Interplay of chromatin modifiers on a short basic patch of histone H4 tail defines the boundary of telomeric heterochromatin. Mol. Cell 28 (2007) 1002-1014
2. Andrews B.J., and Herskowitz I. The yeast SWI4 protein contains a motif present in developmental regulators and is part of a complex involved in cell-cycle-dependent transcription. Nature 342 (1989) 830-833
3. Barski A., Cuddapah S., Cui K., Roh T.Y., Schones D.E., Wang Z., Wei G., Chepelev I., and Zhao K. High-resolution profiling of histone methylations in the human genome. Cell 129 (2007) 823-837
4. Bean J.M., Siggia E.D., and Cross F.R. High functional overlap between MluI cell-cycle box binding factor and Swi4/6 cell-cycle box binding factor in the G1/S transcriptional program in Saccharomyces cerevisiae. Genetics 171 (2005) 49-61
5. Biggins S., and Murray A.W. The budding yeast protein kinase Ipl1/Aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev. 15 (2001) 3118-3129
6. Breeden L. Start-specific transcription in yeast. Curr. Top. Microbiol. Immunol. 208 (1996) 95-127
7. Breeden L., and Nasmyth K. Cell cycle control of the yeast HO gene: cis- and trans-acting regulators. Cell 48 (1987) 389-397
8. de Bruin R.A., Kalashnikova T.I., Chahwan C., McDonald W.H., Wohlschlegel J., Yates III J., Russell P., and Wittenberg C. Constraining G1-specific transcription to late G1 phase: the MBF-associated corepressor Nrm1 acts via negative feedback. Mol. Cell 23 (2006) 483-496
9. Dover J., Schneider J., Tawiah-Boateng M.A., Wood A., Dean K., Johnston M., and Shilatifard A. Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J. Biol. Chem. 277 (2002) 28368-28371
10. Feng Q., Wang H., Ng H.H., Erdjument-Bromage H., Tempst P., Struhl K., and Zhang Y. Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr. Biol. 12 (2002) 1052-1058
11. Frederiks F., Tzouros M., Oudgenoeg G., van Welsem T., Fornerod M., Krijgsveld J., and van Leeuwen F. Nonprocessive methylation by Dot1 leads to functional redundancy of histone H3K79 methylation states. Nat. Struct. Mol. Biol. 15 (2008) 550-557
12. Harbison C.T., Gordon D.B., Lee T.I., Rinaldi N.J., Macisaac K.D., Danford T.W., Hannett N.M., Tagne J.B., Reynolds D.B., Yoo J., et al. Transcriptional regulatory code of a eukaryotic genome. Nature 431 (2004) 99-104
13. Harrington L.A., and Andrews B.J. Binding to the yeast SwI4,6-dependent cell cycle box, CACGAAA, is cell cycle regulated in vivo. Nucleic Acids Res. 24 (1996) 558-565
14. Hereford L.M., Osley M.A., Ludwig II T.R., and McLaughlin C.S. Cell-cycle regulation of yeast histone mRNA. Cell 24 (1981) 367-375
15. Hogan G.J., Lee C.K., and Lieb J.D. Cell cycle-specified fluctuation of nucleosome occupancy at gene promoters. PLoS Genet. 2 (2006) e158
16. Holstege F.C., Jennings E.G., Wyrick J.J., Lee T.I., Hengartner C.J., Green M.R., Golub T.R., Lander E.S., and Young R.A. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95 (1998) 717-728
17. Hwang W.W., Venkatasubrahmanyam S., Ianculescu A.G., Tong A., Boone C., and Madhani H.D. A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol. Cell 11 (2003) 261-266
18. Im H., Park C., Feng Q., Johnson K.D., Kiekhaefer C.M., Choi K., Zhang Y., and Bresnick E.H. Dynamic regulation of histone H3 methylated at lysine 79 within a tissue-specific chromatin domain. J. Biol. Chem. 278 (2003) 18346-18352
19. Iyer V.R., Horak C.E., Scafe C.S., Botstein D., Snyder M., and Brown P.O. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 409 (2001) 533-538
20. Janzen C.J., Hake S.B., Lowell J.E., and Cross G.A. Selective di- or trimethylation of histone H3 lysine 76 by two DOT1 homologs is important for cell cycle regulation in Trypanosoma brucei. Mol. Cell 23 (2006) 497-507
21. Johnson W.E., Li W., Meyer C.A., Gottardo R., Carroll J.S., Brown M., and Liu X.S. Model-based analysis of tiling-arrays for ChIP-chip. Proc. Natl. Acad. Sci. USA 103 (2006) 12457-12462
22. Koch C., Moll T., Neuberg M., Ahorn H., and Nasmyth K. A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase. Science 261 (1993) 1551-1557
23. Krivtsov A.V., Feng Z., Lemieux M.E., Faber J., Vempati S., Sinha A.U., Xia X., Jesneck J., Bracken A.P., Silverman L.B., et al. H3K79 methylation profiles define murine and human MLL-AF4 leukemias. Cancer Cell 14 (2008) 355-368
24. Krogan N.J., Dover J., Wood A., Schneider J., Heidt J., Boateng M.A., Dean K., Ryan O.W., Golshani A., Johnston M., et al. 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
25. Lacoste N., Utley R.T., Hunter J.M., Poirier G.G., and Côte J. Disruptor of telomeric silencing-1 is a chromatin-specific histone H3 methyltransferase. J. Biol. Chem. 277 (2002) 30421-30424
26. Lee W., Tillo D., Bray N., Morse R.H., Davis R.W., Hughes T.R., and Nislow C. A high-resolution atlas of nucleosome occupancy in yeast. Nat. Genet. 39 (2007) 1235-1244
27. Lu X., Simon M.D., Chodaparambil J.V., Hansen J.C., Shokat K.M., and Luger K. The effect of H3K79 dimethylation and H4K20 trimethylation on nucleosome and chromatin structure. Nat. Struct. Mol. Biol. 15 (2008) 1122-1124
28. Luger K., Mäder A.W., Richmond R.K., Sargent D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 (1997) 251-260
29. Martin C., and Zhang Y. The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 6 (2005) 838-849
30. Miao F., and Natarajan R. Mapping global histone methylation patterns in the coding regions of human genes. Mol. Cell. Biol. 25 (2005) 4650-4661
31. Ng H.H., Feng Q., Wang H., Erdjument-Bromage H., Tempst P., Zhang Y., and Struhl K. Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev. 16 (2002) 1518-1527
32. Okada Y., Feng Q., Lin Y., Jiang Q., Li Y., Coffield V.M., Su L., Xu G., and Zhang Y. hDOT1L links histone methylation to leukemogenesis. Cell 121 (2005) 167-178
33. Onishi M., Liou G.G., Buchberger J.R., Walz T., and Moazed D. Role of the conserved Sir3-BAH domain in nucleosome binding and silent chromatin assembly. Mol. Cell 28 (2007) 1015-1028
34. Piatti S., Lengauer C., and Nasmyth K. Cdc6 is an unstable protein whose de novo synthesis in G1 is important for the onset of S phase and for preventing a "reductional" anaphase in the budding yeast Saccharomyces cerevisiae. EMBO J. 14 (1995) 3788-3799
35. Pokholok D.K., Harbison C.T., Levine S., Cole M., Hannett N.M., Lee T.I., Bell G.W., Walker K., Rolfe P.A., Herbolsheimer E., et al. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122 (2005) 517-527
36. Schneider J., Dover J., Johnston M., and Shilatifard A. Global proteomic analysis of S. cerevisiae (GPS) to identify proteins required for histone modifications. Methods Enzymol. 377 (2004) 227-234
37. Schübeler D., MacAlpine D.M., Scalzo D., Wirbelauer C., Kooperberg C., van Leeuwen F., Gottschling D.E., O'Neill L.P., Turner B.M., Delrow J., et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18 (2004) 1263-1271
38. Shahbazian M.D., Zhang K., and Grunstein M. Histone H2B ubiquitylation controls processive methylation but not monomethylation by Dot1 and Set1. Mol. Cell 19 (2005) 271-277
39. Shilatifard A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu. Rev. Biochem. 75 (2006) 243-269
40. Simon I., Barnett J., Hannett N., Harbison C.T., Rinaldi N.J., Volkert T.L., Wyrick J.J., Zeitlinger J., Gifford D.K., Jaakkola T.S., et al. Serial regulation of transcriptional regulators in the yeast cell cycle. Cell 106 (2001) 697-708
41. Spellman P.T., Sherlock G., Zhang M.Q., Iyer V.R., Anders K., Eisen M.B., Brown P.O., Botstein D., and Futcher B. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 9 (1998) 3273-3297
42. Stern B.M., and Murray A.W. Lack of tension at kinetochores activates the spindle checkpoint in budding yeast. Curr. Biol. 11 (2001) 1462-1467
43. Sun Z.W., and Allis C.D. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418 (2002) 104-108
44. Tavazoie S., Hughes J.D., Campbell M.J., Cho R.J., and Church G.M. Systematic determination of genetic network architecture. Nat. Genet. 22 (1999) 281-285
45. van Bakel H., van Werven F.J., Radonjic M., Brok M.O., van Leenen D., Holstege F.C., and Timmers H.T. Improved genome-wide localization by ChIP-chip using double-round T7 RNA polymerase-based amplification. Nucleic Acids Res. 36 (2008) e21
46. van Leeuwen F., Gafken P.R., and Gottschling D.E. Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 109 (2002) 745-756
47. Wood A., Krogan N.J., Dover J., Schneider J., Heidt J., Boateng M.A., Dean K., Golshani A., Zhang Y., Greenblatt J.F., et al. Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol. Cell 11 (2003) 267-274
48. Young Lab (2005). Holstege Genome-Wide Expression Data (http://web.wi.mit.edu/young/pub/holstege.html).
49. Zhou H., Madden B.J., Muddiman D.C., and Zhang Z. Chromatin assembly factor 1 interacts with histone H3 methylated at lysine 79 in the processes of epigenetic silencing and DNA repair. Biochemistry 45 (2006) 2852-2861