Histone H2B ubiquitylation and H3 lysine 4 methylation prevent ectopic silencing of euchromatic loci important for the cellular response to heat

Molecular Biology of the Cell

Volumn 22, Issue 15, 2011, Pages 2741-2753

  Leung, Amy ^a,b,e   Cajigas, Ivelisse ^c   Jia, Peilin ^b   Ezhkova, Elena ^a,d   Brickner, Jason H ^c   Zhao, Zhongming ^b   Geng, Fuqiang ^a,b   Tansey, William P ^a,b  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

^e CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA ADENINE METHYLTRANSFERASE; FUNGAL PROTEIN; FUNGAL RNA; HISTONE H2B; HISTONE H3; LYSINE; SILENT INFORMATION REGULATOR PROTEIN 2; SIR 3 PROTEIN; SIR4 PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; CELL WALL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENZYME ASSAY; FUNGAL CELL; FUNGAL GENE; GENE DISRUPTION; GENE FUNCTION; GENE IDENTIFICATION; GENE SILENCING; HEAT STRESS; HISTONE METHYLATION; HISTONE UBIQUITINATION; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

CELL WALL; EUCHROMATIN; GENE EXPRESSION REGULATION, FUNGAL; GENE SILENCING; GENETIC LOCI; GENOME, FUNGAL; HETEROCHROMATIN; HISTONES; HOT TEMPERATURE; LYSINE; METHYLATION; PLASMIDS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, DNA; SILENT INFORMATION REGULATOR PROTEINS, SACCHAROMYCES CEREVISIAE; SITE-SPECIFIC DNA-METHYLTRANSFERASE (ADENINE-SPECIFIC); TRANSCRIPTION, GENETIC; TRANSFECTION; UBIQUITINATION;

SACCHAROMYCES CEREVISIAE;

EID: 79961047028     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-05-0426     Document Type: Article

References (66)

1. Ahn SH, Cheung WL, Hsu JY, Diaz RL, Smith MM, Allis CD (2005). Sterile 20 kinase phosphorylates histone H2B at serine 10 during hydrogen peroxide-induced apoptosis in S. cerevisiae. Cell 120, 25-36. (Pubitemid 40094600)
2. Anna-Arriola SS, Herskowitz I (1994). Isolation and DNA sequence of the STE13 gene encoding dipeptidyl aminopeptidase. Yeast 10, 801-810. (Pubitemid 24192701)
3. Ashburner M et al. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25, 25-29. (Pubitemid 30257031)
4. Benjamini Y, Hochberg Y (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc. B Methodol 57, 289-300.
5. Brickner DG, Cajigas I, Fondufe-Mittendorf Y, Ahmed S, Lee PC, Widom J, Brickner JH (2007). H2A.Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol 5, e81.
6. Brickner DG, Light W, Brickner JH (2010). Quantitative localization of chromosomal loci by immunofluorescence. Methods Enzymol 470, 569-580.
7. Briggs SD, Bryk M, Strahl BD, Cheung WL, Davie JK, Dent SY, Winston F, Allis CD (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. (Pubitemid 34008193)
8. Bystricky K, Laroche T, van Houwe G, Blaszczyk M, Gasser SM (2005). Chromosome looping in yeast: telomere pairing and coordinated movement reflect anchoring efficiency and territorial organization. J Cell Biol 168, 375-387. (Pubitemid 40205061)
9. Cabal GG et al. (2006). SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441, 770-773. (Pubitemid 43865225)
10. Chandrasekharan MB, Huang F, Sun ZW (2009). Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc Natl Acad Sci USA 106, 16686-16691.
11. Chandrasekharan MB, Huang F, Sun ZW (2010). Histone H2B ubiquitination and beyond: regulation of nucleosome stability, chromatin dynamics and the trans-histone H3 methylation. Epigenetics 5, 460-468.
12. Chen HY, Sun JM, Zhang Y, Davie JR, Meistrich ML (1998). Ubiquitination of histone H3 in elongating spermatids of rat testes. J Biol Chem 273, 13165-13169. (Pubitemid 28246885)
13. Chu Y, Simic R, Warner MH, Arndt KM, Prelich G (2007). Regulation of histone modification and cryptic transcription by the Bur1 and Paf1 complexes. EMBO J 26, 4646-4656. (Pubitemid 350126792)
14. Collart MA, Oliviero S (2001). Preparation of yeast RNA. Curr Protoc Mol Biol Chapter 13, Unit13.12.
15. Duncan D, Prodduturi N, Zhang B (2010). WebGestalt2: an updated and expanded version of the Web-based Gene Set Analysis Toolkit. BMC Bioinformatics 11, P10.
16. Dwight SS et al. (2002). Saccharomyces Genome Database (SGD) provides secondary gene annotation using the Gene Ontology (GO). Nucleic Acids Res 30, 69-72. (Pubitemid 34679507)
17. Gatbonton T, Imbesi M, Nelson M, Akey JM, Ruderfer DM, Kruglyak L, Simon JA, Bedalov A (2006). Telomere length as a quantitative trait: genome-wide survey and genetic mapping of telomere length-control genes in yeast. PLoS Genet 2, e35.
18. Geng F, Tansey WP (2008). Polyubiquitylation of histone H2B. Mol Biol Cell 19, 3616-3624.
19. Gietz RD, Schiestl RH (2007). Large-scale high-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2, 38-41. (Pubitemid 47040067)
20. Goldknopf IL, Busch H (1977). Isopeptide linkage between nonhistone and histone 2A polypeptides of chromosomal conjugate-protein A24. Proc Natl Acad Sci USA 74, 864-868. (Pubitemid 8068703)
21. Goldstein AL, McCusker JH (1999). Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15, 1541-1553. (Pubitemid 29472165)
22. Hediger F, Neumann FR, Van Houwe G, Dubrana K, Gasser SM (2002). Live imaging of telomeres: yKu and Sir proteins define redundant telomere-anchoring pathways in yeast. Curr Biol 12, 2076-2089. (Pubitemid 36021885)
23. Hirano Y, Fukunaga K, Sugimoto K (2009). Rif1 and rif2 inhibit localization of tel1 to DNA ends. Mol Cell 33, 312-322.
24. Huang da W, Sherman BT, Lempicki RA (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4, 44-57.
25. Hwang WW, Venkatasubrahmanyam S, Ianculescu AG, Tong A, Boone C, Madhani HD (2003). A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol Cell 11, 261-266. (Pubitemid 36126606)
26. Johnston HD, Foote C, Santeford A, Nothwehr SF (2005). Golgi-to-late endosome trafficking of the yeast pheromone processing enzyme Ste13p is regulated by a phosphorylation site in its cytosolic domain. Mol Biol Cell 16, 1456-1468. (Pubitemid 40349579)
27. Jones GM, Stalker J, Humphray S, West A, Cox T, Rogers J, Dunham I, Prelich G (2008). A systematic library for comprehensive overexpression screens in Saccharomyces cerevisiae. Nat Methods 5, 239-241. (Pubitemid 351325647)
28. Kao CF, Hillyer C, Tsukuda T, Henry K, Berger S, Osley MA (2004). Rad6 plays a role in transcriptional activation through ubiquitylation of histone H2B. Genes Dev 18, 184-195. (Pubitemid 38141786)
29. Kramer KM, Haber JE (1993). New telomeres in yeast are initiated with a highly selected subset of TG1-3 repeats. Genes Dev 7, 2345-2356. (Pubitemid 24003238)
30. Kuo MH, Zhou J, Jambeck P, Churchill ME, Allis CD (1998). Histone acetyltransferase activity of yeast Gcn5p is required for the activation of target genes in vivo. Genes Dev 12, 627-639. (Pubitemid 28134296)
31. Langmead B (2010). Aligning short sequencing reads with Bowtie. Curr Protoc Bioinformatics 17Chapter 11, Unit 11.
32. Lee JS, Shukla A, Schneider J, Swanson SK, Washburn MP, Florens L, Bhaumik SR, Shilatifard A (2007). Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131, 1084-1096. (Pubitemid 350235018)
33. Levin DE (2005). Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69, 262-291.
34. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961. (Pubitemid 28328001)
35. Maillet L, Boscheron C, Gotta M, Marcand S, Gilson E, Gasser SM (1996). Evidence for silencing compartments within the yeast nucleus: a role for telomere proximity and Sir protein concentration in silencer-mediated repression. Genes Dev 10, 1796-1811. (Pubitemid 26272385)
36. Marshall M, Mahoney D, Rose A, Hicks JB, Broach JR (1987). Functional domains of SIR4, a gene required for position effect regulation in Saccharomyces cerevisiae. Mol Cell Biol 7, 4441-4452.
37. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5, 621-628. (Pubitemid 351911867)
38. Murr R (2010). Interplay between different epigenetic modifications and mechanisms. Adv Genet 70, 101-141.
39. Mutiu AI, Hoke SM, Genereaux J, Liang G, Brandl CJ (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. (Pubitemid 46644072)
40. Nagalakshmi U, Waern K, Snyder M (2010). RNA-Seq: a method for comprehensive transcriptome analysis. Curr Protoc Mol Biol Chapter 4, Unit 4.11.1-4.11-13.
41. Ng HH, Feng Q, Wang H, Erdjument-Bromage H, Tempst P, Zhang Y, Struhl K (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. (Pubitemid 34686333)
42. Nislow C, Ray E, Pillus L (1997). SET1, a yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Mol Biol Cell 8, 2421-2436. (Pubitemid 27528211)
43. Palladino F, Laroche T, Gilson E, Axelrod A, Pillus L, Gasser SM (1993). SIR3 and SIR4 proteins are required for the positioning and integrity of yeast telomeres. Cell 75, 543-555. (Pubitemid 23335079)
44. Pavri R, Zhu B, Li G, Trojer P, Mandal S, Shilatifard A, Reinberg D (2006). Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125, 703-717. (Pubitemid 43732350)
45. Pinskaya M, Gourvennec S, Morillon A (2009). H3 lysine 4 di- and tri-methylation deposited by cryptic transcription attenuates promoter activation. EMBO J 28, 1697-1707.
46. Rine J, Herskowitz I (1987). Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics 116, 9-22.
47. Robzyk K, Recht J, Osley MA (2000). Rad6-dependent ubiquitination of histone H2B in yeast. Science 287, 501-504.
48. Santos-Rosa H, Bannister AJ, Dehe PM, Geli V, Kouzarides T (2004). Methylation of H3 lysine 4 at euchromatin promotes Sir3p association with heterochromatin. J Biol Chem 279, 47506-47512. (Pubitemid 39540894)
49. Sexton T, Schober H, Fraser P, Gasser SM (2007). Gene regulation through nuclear organization. Nat Struct Mol Biol 14, 1049-1055. (Pubitemid 350060340)
50. Stellwagen AE, Haimberger ZW, Veatch JR, Gottschling DE (2003). Ku interacts with telomerase RNA to promote telomere addition at native and broken chromosome ends. Genes Dev 17, 2384-2395. (Pubitemid 37214787)
51. Strahl BD, Allis CD (2000). The language of covalent histone modifications. Nature 403, 41-45. (Pubitemid 30038513)
52. Straight AF, Belmont AS, Robinett CC, Murray AW (1996). GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr Biol 6, 1599-1608. (Pubitemid 27050227)
53. Sun ZW, Allis CD (2002). Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418, 104-108.
54. Taddei A, Gasser SM (2004). Multiple pathways for telomere tethering: functional implications of subnuclear position for heterochromatin formation. Biochim Biophys Acta 1677, 120-128. (Pubitemid 38327096)
55. Van Mullem V, Wery M, De Bolle X, Vandenhaute J (2003). Construction of a set of Saccharomyces cerevisiae vectors designed for recombinational cloning. Yeast 20, 739-746. (Pubitemid 36764059)
56. van Steensel B, Henikoff S (2000). Identification of in vivo DNA targets of chromatin proteins using tethered Dam methyltransferase. Nat Biotechnol 18, 424-428.
57. Varier RA, Timmers HT (2010). Histone lysine methylation and demethylation pathways in cancer. Biochim Biophys Acta 8515, 75-89.
58. Venkatasubrahmanyam S, Hwang WW, Meneghini MD, Tong AH, Madhani HD (2007). Genome-wide, as opposed to local, antisilencing is mediated redundantly by the euchromatic factors Set1 and H2A.Z. Proc Natl Acad Sci USA 104, 16609-16614. (Pubitemid 350211064)
59. Wang L, Feng Z, Wang X, Zhang X (2010). DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26, 136-138.
60. West MH, Bonner WM (1980). Histone 2B can be modified by the attachment of ubiquitin. Nucleic Acids Res 8, 4671-4680.
61. Wieser R, Adam G, Wagner A, Schuller C, Marchler G, Ruis H, Krawiec Z, Bilinski T (1991). Heat shock factor-independent heat control of transcription of the CTT1 gene encoding the cytosolic catalase T of Saccharomyces cerevisiae. J Biol Chem 266, 12406-12411. (Pubitemid 21907108)
62. Wood A et al. (2003a). Bre1, an e3 ubiquitin ligase required for recruitment and substrate selection of rad6 at a promoter. Mol Cell 11, 267-274. (Pubitemid 36126607)
63. Wood A, Schneider J, Dover J, Johnston M, Shilatifard A (2003b). 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.
64. Wood A, Schneider J, Dover J, Johnston M, Shilatifard A (2005). The Bur1/Bur2 complex is required for histone H2B monoubiquitination by Rad6/Bre1 and histone methylation by COMPASS. Mol Cell 20, 589-599. (Pubitemid 41668643)
65. Wyce A, Xiao T, Whelan KA, Kosman C, Walter W, Eick D, Hughes TR, Krogan NJ, Strahl BD, Berger SL (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. (Pubitemid 47058302)
66. Yan Q, Dutt S, Xu R, Graves K, Juszczynski P, Manis JP, Shipp MA (2009). BBAP monoubiquitylates histone H4 at lysine 91 and selectively modulates the DNA damage response. Mol Cell 36, 110-120.