Dynamic remodeling of histone modifications in response to osmotic stress in Saccharomyces cerevisiae

BMC Genomics

Vicente Tordera²  María Dolores Coloma²  Vicent Pelechano¹  Lorena Magraner-Pardo² 

[1] Genome Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany;Departament de Bioquímica i Biologia Molecular, Universitat de València, C/Dr. Moliner 50, 46100 Burjassot, València, Spain

关键词: ChIP-Chip;    Osmotic stress;    Transcription;    Genome-wide;    Gene regulation;    Epigenetics;    Chromatin;    Histone modification;   

Others  :  1217595
DOI  :  10.1186/1471-2164-15-247

 received in 2013-02-19, accepted in 2014-03-24,  发布年份 2014

【 摘 要 】

Background

Specific histone modifications play important roles in chromatin functions; i.e., activation or repression of gene transcription. This participation must occur as a dynamic process. Nevertheless, most of the histone modification maps reported to date provide only static pictures that link certain modifications with active or silenced states. This study, however, focuses on the global histone modification variation that occurs in response to the transcriptional reprogramming produced by a physiological perturbation in yeast.

Results

We did a genome-wide chromatin immunoprecipitation analysis for eight specific histone modifications before and after saline stress. The most striking change was rapid acetylation loss in lysines 9 and 14 of H3 and in lysine 8 of H4, associated with gene repression. The genes activated by saline stress increased the acetylation levels at these same sites, but this acetylation process was quantitatively minor if compared to that of the deacetylation of repressed genes. The changes in the tri-methylation of lysines 4, 36 and 79 of H3 and the di-methylation of lysine 79 of H3 were slighter than those of acetylation. Furthermore, we produced new genome-wide maps for seven histone modifications, and we analyzed, for the first time in S. cerevisiae, the genome-wide profile of acetylation of lysine 8 of H4.

Conclusions

This research reveals that the short-term changes observed in the post-stress methylation of histones are much more moderate than those of acetylation, and that the dynamics of the acetylation state of histones during activation or repression of transcription is a much quicker process than methylation.

【 授权许可】

   
2014 Magraner-Pardo et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】

• [1]Bannister AJ, Kouzarides T: Regulation of chromatin by histone modifications. Cell Res 2011, 21:381-395.
• [2]Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL: Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006, 311:844-847.
• [3]Turner BM: Decoding the nucleosome. Cell 1993, 75:5-8.
• [4]Tordera V, Sendra R, Pérez-Ortín JE: The role of histones and their modifications in the informative content of chromatin. Experientia 1993, 49:780-788.
• [5]Strahl BD, Allis CD: The language of covalent histone modifications. Nature 2000, 403:41-45.
• [6]Jenuwein T, Allis CD: Translating the histone code. Science 2001, 293:1074-1080.
• [7]Berger SL: The complex language of chromatin regulation during transcription. Nature 2007, 447:407-412.
• [8]Bernstein BE, Humphrey EL, Erlich RL, Schneider R, Bouman P, Liu JS, Kouzarides T, Schreiber SL: Methylation of histone H3 Lys 4 in coding regions of active genes. Proc Natl Acad Sci U S A 2002, 99:8695-8700.
• [9]Kurdistani SK, Tavazoie S, Grunstein M: Mapping global histone acetylation patterns to gene expression. Cell 2004, 117:721-733.
• [10]Lee CK, Shibata Y, Rao B, Strahl BD, Lieb JD: Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat Genet 2004, 36:900-905.
• [11]Liu CL, Kaplan T, Kim M, Buratowski S, Schreiber SL, Friedman N, Rando OJ: Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol 2005, 3(10):e328.
• [12]Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, Bell GW, Walker K, Rolfe PA, Herbolsheimer E, Zeitlinger Lewitter JF, Gifford DK, Young RA: Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 2005, 122:517-527.
• [13]Henikoff S, Shilatifard A: Histone modification: cause or cog? Trends Genet 2011, 27:389-396.
• [14]Rando OJ, Chang HY: Genome-wide views of chromatin structure. Annu Rev Biochem 2009, 78:245-271.
• [15]Kirmizis A, Santos-Rosa H, Penkett CJ, Singer MA, Vermeulen M, Mann M, Bähler J, Green RD, Kouzarides T: Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature 2007, 449:928-932.
• [16]Schulze JM, Jackson J, Nakanishi S, Gardner JM, Hentrich T, Haug J, Johnston M, Jaspersen SL, Kobor MS, Shilatifard A: Linking cell cycle to histone modifications: SBF and H2B monoubiquitination machinery and cell cycle regulation of H3K79 dimethylation. Mol Cell 2009, 35:626-641.
• [17]Guillemette B, Drogaris P, Lin H-HS, Armstrong H, Hiragami-Hamada K, Imhof A, Bonneil E, Thibault P, Verreault A, Festenstein RJ: H3 lysine 4 is acetylated at active gene promoters and is regulated by H3 lysine 4 methylation. PLoS Genet 2011, 7(3):e1001354.
• [18]Batta K, Zhang Z, Yen K, Goffman DB, Pugh BF: Genome-wide function of H2B ubiquitylation in promoter and genic regions. Genes Dev 2011, 25:2254-2265.
• [19]Lee J-S, Garrett AS, Yen K, Takahashi Y-H, Hu D, Jackson J, Seidel C, Pugh BF, Shilatifard A: Codependency of H2B monoubiquitination and nucleosome reassembly on Chd1. Genes Dev 2012, 26:914-919.
• [20]Brownell JE, Zhou J, Ranalli T, Kobayashi R, Edmondson DG, Roth SY, Allis CD: Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 1996, 84:843-851.
• [21]Robert F, Pokholok DK, Hannett NM, Rinaldi NJ, Chandy M, Rolfe A, Workman JL, Gifford DK, Young RA: Global position and recruitment of HATs and HDACs in the yeast genome. Mol Cell 2004, 16:199-209.
• [22]Rosaleny LE, Ruiz-García AB, García-Martínez J, Pérez-Ortín JE, Tordera V: The Sas3p and Gcn5p histone acetyltransferases are recruited to similar genes. Genome Biol 2007, 8(6):R119. BioMed Central Full Text
• [23]Utley RT, Ikeda K, Grant PA, Côté J, Steger DJ, Eberharter A, John S, Workman JL: Transcriptional activators direct histone acetyltransferase complexes to nucleosomes. Nature 1998, 394:498-502.
• [24]Ikeda K, Steger DJ, Eberharter A, Workman JL: Activation domain-specific and general transcription stimulation by native histone acetyltransferase complexes. Mol Cell Biol 1999, 19:855-863.
• [25]Allard S, Utley RT, Savard J, Clarke A, Grant P, Brandl CJ, Pillus L, Workman JL, Côté J: NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J 1999, 18:5108-5119.
• [26]Briggs SD, Bryk M, Strahl BD, Cheung WL, Davie JK, Dent SY, Winston F, Allis CD: Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 2001, 15:3286-3295.
• [27]Roguev A, Schaft D, Shevchenko A, Pijnappel WW, Wilm M, Aasland R, Stewart AF: The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J 2001, 20:7137-7148.
• [28]Krogan NJ, Dover J, Khorrami S, Greenblatt JF, Schneider J, Johnston M, Shilatifard A: COMPASS, a histone H3 (Lysine 4) methyltransferase required for telomeric silencing of gene expression. J Biol Chem 2002, 277:10753-10755.
• [29]Ng HH, Robert F, Young RA, Struhl K: Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 2003, 11:709-719.
• [30]Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC, Schreiber SL, Mellor J, Kouzarides T: Active genes are tri-methylated at K4 of histone H3. Nature 2002, 419:407-411.
• [31]Nagy PL, Griesenbeck J, Kornberg RD, Cleary ML: A trithorax-group complex purified from Saccharomyces cerevisiae is required for methylation of histone H3. Proc Natl Acad Sci U S A 2002, 99:90-94.
• [32]Strahl BD, Grant PA, Briggs SD, Sun ZW, Bone JR, Caldwell JA, Mollah S, Cook RG, Shabanowitz J, Hunt DF, Allis CD: Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol Cell Biol 2002, 22:1298-1306.
• [33]Lacoste N, Utley RT, Hunter JM, Poirier GG, Côte J: Disruptor of telomeric silencing-1 is a chromatin specific histone H3 methyltransferase. J Biol Chem 2002, 277:30421-30424.
• [34]van Leeuwen F, Gafken PR, Gottschling DE: Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 2002, 109:745-756.
• [35]Ng HH, Feng Q, Wang H, Erdjument-Bromage H, Tempst P, Zhang Y, Struhl K: Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev 2002, 16:1518-1527.
• [36]Feng Q, Wang H, Ng HH, Erdjument-Bromage H, Tempst P, Struhl K, Zhang Y: Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr Biol 2002, 12:1052-1058.
• [37]Morillon A, Karabetsou N, Nair A, Mellor J: Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol Cell 2005, 18:723-734.
• [38]Xu Z, Wei W, Gagneur J, Perocchi F, Clauder-Münster S, Camblong J, Guffanti E, Stutz F, Huber W, Steinmetz LM: Bidirectional promoters generate pervasive transcription in yeast. Nature 2009, 457:1033-1037.
• [39]Xue-Franzén Y, Johnsson A, Brodin D, Henriksson J, Bürglin TR, Wright AP: Genome-wide characterisation of the Gcn5 histone acetyltransferase in budding yeast during stress adaptation reveals evolutionarily conserved and diverged roles. BMC Genomics 2010, 11:200. BioMed Central Full Text
• [40]Johnsson A, Durand-Dubief M, Xue-Franzén Y, Rönnerblad M, Ekwall K, Wright A: HAT–HDAC interplay modulates global histone H3K14 acetylation in gene-coding regions during stress. EMBO Rep 2009, 10:1009-1014.
• [41]Pelechano V, Chávez S, Pérez-Ortín JE: A Complete set of nascent transcription rates for yeast genes. PLoS ONE 2010, 5(11):e15442.
• [42]Sun M, Schwalb B, Schulz D, Pirkl N, Etzold S, Larivière L, Maier KC, Seizl M, Tresch A, Cramer P: Comparative dynamic transcriptome analysis (cDTA) reveals mutual feedback between mRNA synthesis and degradation. Genome Res 2012, 22:1350-1359.
• [43]Yuan GC, Liu YJ, Dion MF, Slack MD, Wu LF, Altschuler SJ, Rando OJ: Genome-scale identification of nucleosome positions in S. cerevisiae. Science 2005, 309:626-630.
• [44]Albert I, Mavrich TN, Tomsho LP, Qi J, Zanton SJ, Schuster SC, Pugh BF: Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 2007, 446:572-576.
• [45]Zaugg JB, Luscombe NM: A genomic model of condition-specific nucleosome behavior explains transcriptional activity in yeast. Genome Res 2012, 22:84-94.
• [46]Venters BJ, Pugh BF: A canonical promoter organization of the transcription machinery and its regulators in the Saccharomyces genome. Genome Res 2009, 19:360-371.
• [47]Dehé P-M, Pamblanco M, Luciano P, Lebrun R, le Moinier D, Sendra R, Verreault A, Tordera V, Géli V: Histone H3 lysine 4 mono-methylation does not require ubiquitination of histone H2B. J Mol Biol 2005, 353:477-484.
• [48]Jasiak AJ, Hartmann H, Karakasili E, Kalocsay M, Flatley A, Kremmer E, Strässer K, Martin DE, Söding J, Cramer P: Genome-associated RNA polymerase II includes the dissociable Rpb4/7 subcomplex. J Biol Chem 2008, 283:26423-26427.
• [49]Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, Golub TR, Lander ES, Young RA: Dissecting the regulatory circuitry of a eukaryotic genome. Cell 1998, 95:717-728.
• [50]Steger DJ, Lefterova MI, Ying L, Stonestrom AJ, Schupp M, Zhuo D, Vakoc AL, Kim JE, Chen J, Lazar MA, Blobel GA, Vakoc CR: DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol Cell Biol 2008, 28:2825-2839.
• [51]Yun M, Wu J, Workman JL, Li B: Readers of histone modifications. Cell Res 2011, 21:564-578.
• [52]de Nadal E, Posas F: Multilayered control of gene expression by stress-activated protein kinases. EMBO J 2010, 29:4-13.
• [53]Rep M, Krant M, Thevelein JM, Hohmann S: The transcriptional response of Saccharomyces cerevisiae to osmotic shock. J Biol Chem 2000, 275:8290-8300.
• [54]Posas F, Chambersi JR, Heymani JA, Hoeffleri JP, de Nadal E, Ariño J: The transcriptional response of yeast to saline stress. J Biol Chem 2000, 275:17249-17255.
• [55]Romero-Santacreu L, Moreno J, Pérez-Ortín JE, Alepuz P: Specific and global regulation of mRNA stability during osmotic stress in Saccharomyces cerevisiae. RNA 2009, 15:1110-1120.
• [56]García-Martínez J, Aranda A, Pérez-Ortín JE: Genomic run-on evaluates transcription rates for all yeast genes and identifies gene regulatory mechanisms. Mol Cell 2004, 15:303-313.
• [57]de Nadal E, Zapater M, Alepuz PM, Sumoy L, Mas G, Posas F: The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes. Nature 2004, 427:370-374.
• [58]Waterborg JH: Dynamics of histone acetylation in Saccharomyces cerevisiae. Biochemistry 2001, 40:2599-2605.
• [59]Weiner A, Hughes A, Yassour M, Rando OJ, Friedman N: High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res 2010, 20:90-100.
• [60]Pelechano V, Jimeno-González S, Rodríguez-Gil A, García-Martínez J, Pérez-Ortín JE, Chávez S: 11. Regulon-specific control of transcription elongation across the yeast genome. PLoS Genet 2009, 5(8):e1000614.
• [61]Suka N, Suka Y, Carmen AA, Wu J, Grunstein M: Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol Cell 2001, 8:473-479.
• [62]Zapater M, Sohrmann M, Peter M, Posas F, de Nadal E: Selective requirement for SAGA in hog1-mediated gene expression depending on the severity of the external osmostress conditions. Mol Cell Biol 2007, 27:3900-3910.
• [63]Weiner A, Chen HV, Liu CL, Rahat A, Klien A, Soares L, Gudipati M, Pfeffner J, Regev A, Buratowski S, Pleiss JA, Friedman N, Rando OJ: Systematic dissection of roles for chromatin regulators in a yeast stress response. PLoS Biol 2012, 10:e1001369.
• [64]Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H, Li H, Baker L, Boyle J, Blair LP, Chait BT, Patel DJ, Aitchison JD, Tackett AJ, Allis CD: Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol Cell 2006, 24:785-796.
• [65]Pray-Grant MG, Daniel JA, Schieltz D, Yates JR 3rd, Grant PA: Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 2005, 433:434-438.
• [66]Nakanishi S, Sanderson BW, Delventhal KM, Bradford WD, Staehling-Hampton K, Shilatifard A: A comprehensive library of histone mutants identifies nucleosomal residues required for H3K4 methylation. Nat Struct Mol Biol 2008, 15:881-888.
• [67]Maltbya VE, Martina BJE, Brind’Amourb J, Chruscickia AT, McBurneya KL, Schulzec JM, Johnsona IJ, Hillsd M, Hentrichc T, Koborc MS, Lorinczb MC, Howe LJ: Histone H3K4 demethylation is negatively regulated by histone H3 acetylation in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2012, 109:18505-18510.
• [68]Ren B, Robert F, Wyrick JJ, Aparicio O, Jennings EG, Simon I, Zeitlinger J, Schreiber J, Hannett N, Kanin E, Volkert TL, Wilson CJ, Bell SP, Young RA: Genome-wide location and function of DNA binding proteins. Science 2000, 290:2306-2309.
• [69]Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J: Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80. BioMed Central Full Text