Dynamic Changes in Nucleosome Occupancy Are Not Predictive of Gene Expression Dynamics but Are Linked to Transcription and Chromatin Regulators

REFERENCES

• Adkins MW, Howar SR, Tyler JK. 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.
   PubMed Web of Science ®Google Scholar
• Albert I, et al. 2007. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446:572–576.
   PubMed Web of Science ®Google Scholar
• Alejandro-Osorio AL, et al. 2009. The histone deacetylase Rpd3p is required for transient changes in genomic expression in response to stress. Genome Biol. 10:R57.
   PubMed Web of Science ®Google Scholar
• Almer A, Rudolph H, Hinnen A, Horz W. 1986. Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J. 5:2689–2696.
   PubMed Web of Science ®Google Scholar
• Archer TK, Cordingley MG, Wolford RG, Hager GL. 1991. Transcription factor access is mediated by accurately positioned nucleosomes on the mouse mammary tumor virus promoter. Mol. Cell. Biol. 11:688–698.
   PubMed Web of Science ®Google Scholar
• Badis G, et al. 2008. A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol. Cell 32:878–887.
   PubMed Web of Science ®Google Scholar
• Bailey TL, et al. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37:W202–W208.
   PubMed Web of Science ®Google Scholar
• Basehoar AD, Zanton SJ, Pugh BF. 2004. Identification and distinct regulation of yeast TATA box-containing genes. Cell 116:699–709.
   PubMed Web of Science ®Google Scholar
• Beck T, Hall MN. 1999. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402:689–692.
   PubMed Web of Science ®Google Scholar
• Berry DB, Gasch AP. 2008. Stress-activated genomic expression changes serve a preparative role for impending stress in yeast. Mol. Biol. Cell 19:4580–4587.
   PubMed Web of Science ®Google Scholar
• Bose S, Dutko JA, Zitomer RS. 2005. Genetic factors that regulate the attenuation of the general stress response of yeast. Genetics 169:1215–1226.
   PubMedGoogle Scholar
• Brickner DG, et al. 2007. H2A. Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol. 5:e81.
   PubMed Web of Science ®Google Scholar
• Causton HC, et al. 2001. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 12:323–337.
   PubMed Web of Science ®Google Scholar
• Chi Y, et al. 2001. Negative regulation of Gcn4 and Msn2 transcription factors by Srb10 cyclin-dependent kinase. Genes Dev. 15:1078–1092.
   PubMed Web of Science ®Google Scholar
• Durrin LK, Mann RK, Grunstein M. 1992. Nucleosome loss activates CUP1 and HIS3 promoters to fully induced levels in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 12:1621–1629.
   PubMedGoogle Scholar
• Erkina TY, Tschetter PA, Erkine AM. 2008. Different requirements of the SWI/SNF complex for robust nucleosome displacement at promoters of heat shock factor and Msn2- and Msn4-regulated heat shock genes. Mol. Cell. Biol. 28:1207–1217.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Field Y, et al. 2008. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput. Biol. 4:e1000216.
   PubMed Web of Science ®Google Scholar
• Floer M, et al. 2010. A RSC/nucleosome complex determines chromatin architecture and facilitates activator binding. Cell 141:407–418.
   PubMed Web of Science ®Google Scholar
• Fraley C, Raftery AE. 2002. Model-based clustering, discriminant analysis, and density estimation. J. Am. Stat. Assoc. 97:611–631.
   Web of Science ®Google Scholar
• Gasch AP. 2002. The environmental stress response: a common yeast response to environmental stresses. Springer-Verlag, Heidelberg, Germany.
   Google Scholar
• Gasch AP. 2002. Yeast genomic expression studies using DNA microarrays. Methods Enzymol. 350:393–414.
   PubMedGoogle Scholar
• Gasch AP, et al. 2004. Conservation and evolution of cis-regulatory systems in ascomycete fungi. PLoS Biol. 2:e398.
   PubMed Web of Science ®Google Scholar
• Gasch AP, et al. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11:4241–4257.
   PubMed Web of Science ®Google Scholar
• Geng F, Laurent BC. 2004. Roles of SWI/SNF and HATs throughout the dynamic transcription of a yeast glucose-repressible gene. EMBO J. 23:127–137.
   PubMedGoogle Scholar
• Görner W, et al. 1998. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 12:586–597.
   PubMed Web of Science ®Google Scholar
• Gross DS, Adams CC, Lee S, Stentz B. 1993. A critical role for heat shock transcription factor in establishing a nucleosome-free region over the TATA-initiation site of the yeast HSP82 heat shock gene. EMBO J. 12:3931–3945.
   PubMedGoogle Scholar
• Guillemette B, et al. 2005. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol. 3:e384.
   PubMed Web of Science ®Google Scholar
• Hager GL, McNally JG, Misteli T. 2009. Transcription dynamics. Mol. Cell 35:741–753.
   PubMed Web of Science ®Google Scholar
• Han M, Kim UJ, Kayne P, Grunstein M. 1988. Depletion of histone H4 and nucleosomes activates the PHO5 gene in Saccharomyces cerevisiae. EMBO J. 7:2221–2228.
   PubMedGoogle Scholar
• Hogan GJ, Lee CK, Lieb JD. 2006. Cell cycle-specified fluctuation of nucleosome occupancy at gene promoters. PLoS Genet. 2:e158.
   PubMedGoogle Scholar
• Jiang C, Pugh BF. 2009. A compiled and systematic reference map of nucleosome positions across the Saccharomyces cerevisiae genome. Genome Biol. 10:R109.
   PubMedGoogle Scholar
• John S, et al. 2008. Interaction of the glucocorticoid receptor with the chromatin landscape. Mol. Cell 29:611–624.
   PubMed Web of Science ®Google Scholar
• Kaplan N, et al. 2009. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458:362–366.
   PubMed Web of Science ®Google Scholar
• Kuan PF, Huebert D, Gasch A, Keles S. 2009. A non-homogeneous hidden-state model on first order differences for automatic detection of nucleosome positions. Stat. Appl. Genet. Mol. Biol. 8: Article29.
   PubMedGoogle Scholar
• Kundu S, Horn PJ, Peterson CL. 2007. SWI/SNF is required for transcriptional memory at the yeast GAL gene cluster. Genes Dev. 21:997–1004.
   PubMedGoogle Scholar
• Lallet S, et al. 2006. Role of Gal11, a component of the RNA polymerase II mediator in stress-induced hyperphosphorylation of Msn2 in Saccharomyces cerevisiae. Mol. Microbiol. 62:438–452.
   PubMedGoogle Scholar
• Lallet S, Garreau H, Poisier C, Boy-Marcotte E, Jacquet M. 2004. Heat shock-induced degradation of Msn2p, a Saccharomyces cerevisiae transcription factor, occurs in the nucleus. Mol. Genet. Genomics 272:353–362.
   PubMedGoogle Scholar
• Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25.
   PubMed Web of Science ®Google Scholar
• Lee CK, Shibata Y, Rao B, Strahl BD, Lieb JD. 2004. Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat. Genet. 36:900–905.
   PubMed Web of Science ®Google Scholar
• Lee MV, et al. 2011. A dynamic model of proteome changes reveals new roles for transcript alteration in yeast. Mol. Syst. Biol. 7:514.
   PubMed Web of Science ®Google Scholar
• Lee W, et al. 2007. A high-resolution atlas of nucleosome occupancy in yeast. Nat. Genet. 39:1235–1244.
   PubMed Web of Science ®Google Scholar
• Li H, Ruan J, Durbin R. 2008. Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 18:1851–1858.
   PubMed Web of Science ®Google Scholar
• Lieb JD, Liu X, Botstein D, Brown PO. 2001. Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association. Nat. Genet. 28:327–334.
   PubMed Web of Science ®Google Scholar
• Light WH, Brickner DG, Brand VR, Brickner JH. 2010. Interaction of a DNA zip code with the nuclear pore complex promotes H2A.Z incorporation and INO1 transcriptional memory. Mol. Cell 40:112–125.
   PubMed Web of Science ®Google Scholar
• Liko D, Conway MK, Grunwald DS, Heideman W. 2010. Stb3 plays a role in the glucose-induced transition from quiescence to growth in Saccharomyces cerevisiae. Genetics 185:797–810.
   PubMed Web of Science ®Google Scholar
• Lindstrom KC, Vary JC, Parthun MR, Delrow J, Tsukiyama T. 2006. Isw1 functions in parallel with the NuA4 and Swr1 complexes in stress-induced gene repression. Mol. Cell. Biol. 26:6117–6129.
   PubMedGoogle Scholar
• Lippman SI, Broach JR. 2009. Protein kinase A and TORC1 activate genes for ribosomal biogenesis by inactivating repressors encoded by Dot6 and its homolog Tod6. Proc. Natl. Acad. Sci. U. S. A. 106:19928–19933.
   PubMed Web of Science ®Google Scholar
• Liu CL, et al. 2005. Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 3:e328.
   PubMed Web of Science ®Google Scholar
• Lohr D, Lopez J. 1995. GAL4/GAL80-dependent nucleosome disruption/deposition on the upstream regions of the yeast GAL1-10 and GAL80 genes. J. Biol. Chem. 270:27671–27678.
   PubMedGoogle Scholar
• Molina-Navarro MM, et al. 2008. Comprehensive transcriptional analysis of the oxidative response in yeast. J. Biol. Chem. 283:17908–17918.
   PubMedGoogle Scholar
• Nagaich AK, Walker DA, Wolford R, Hager GL. 2004. Rapid periodic binding and displacement of the glucocorticoid receptor during chromatin remodeling. Mol. Cell 14:163–174.
   PubMed Web of Science ®Google Scholar
• Ni L, et al. 2009. Dynamic and complex transcription factor binding during an inducible response in yeast. Genes Dev. 23:1351–1363.
   PubMed Web of Science ®Google Scholar
• Ohsawa R, Adkins M, Tyler JK. 2009. Epigenetic inheritance of an inducibly nucleosome-depleted promoter and its associated transcriptional state in the apparent absence of transcriptional activators. Epigenetics Chromatin 2:11.
   PubMedGoogle Scholar
• Perlmann T, Wrange O. 1988. Specific glucocorticoid receptor binding to DNA reconstituted in a nucleosome. EMBO J. 7:3073–3079.
   PubMedGoogle Scholar
• Polach KJ, Widom J. 1995. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J. Mol. Biol. 254:130–149.
   PubMed Web of Science ®Google Scholar
• Polach KJ, Widom J. 1996. A model for the cooperative binding of eukaryotic regulatory proteins to nucleosomal target sites. J. Mol. Biol. 258:800–812.
   PubMed Web of Science ®Google Scholar
• Raisner RM, et al. 2005. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123:233–248.
   PubMed Web of Science ®Google Scholar
• Rando OJ, Ahmad K. 2007. Rules and regulation in the primary structure of chromatin. Curr. Opin. Cell Biol. 19:250–256.
   PubMed Web of Science ®Google Scholar
• Ransom M, et al. 2009. FACT and the proteasome promote promoter chromatin disassembly and transcriptional initiation. J. Biol. Chem. 284:23461–23471.
   PubMed Web of Science ®Google Scholar
• Segal E, et al. 2006. A genomic code for nucleosome positioning. Nature 442:772–778.
   PubMed Web of Science ®Google Scholar
• Shivaswamy S, et al. 2008. Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol. 6:e65.
   PubMed Web of Science ®Google Scholar
• Smyth G. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3: Article3.
   PubMedGoogle Scholar
• Song JS, et al. 2007. Model-based analysis of two-color arrays (MA2C). Genome Biol. 8:R178.
   PubMedGoogle Scholar
• Stavreva DA, Muller WG, Hager GL, Smith CL, McNally JG. 2004. Rapid glucocorticoid receptor exchange at a promoter is coupled to transcription and regulated by chaperones and proteasomes. Mol. Cell. Biol. 24:2682–2697.
   PubMed Web of Science ®Google Scholar
• Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U. S. A. 100:9440–9445.
   PubMed Web of Science ®Google Scholar
• Venters BJ, et al. 2011. A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol. Cell 41:480–492.
   PubMed Web of Science ®Google Scholar
• Weiner A, Hughes A, Yassour M, Rando OJ, Friedman N. 2010. High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res. 20:90–100.
   PubMed Web of Science ®Google Scholar
• Wolffe AP. 1991. Activating chromatin. Curr. Biol. 1:366–368.
   PubMedGoogle Scholar
• Workman JL. 2006. Nucleosome displacement in transcription. Genes Dev. 20:2009–2017.
   PubMedGoogle Scholar
• Xu Z, et al. 2011. Antisense expression increases gene expression variability and locus interdependency. Mol. Syst. Biol. 7:468.
   PubMedGoogle Scholar
• Xu Z, et al. 2009. Bidirectional promoters generate pervasive transcription in yeast. Nature 457:1033–1037.
   PubMed Web of Science ®Google Scholar
• Yassour M, et al. 2010. Strand-specific RNA sequencing reveals extensive regulated long antisense transcripts that are conserved across yeast species. Genome Biol. 11:R87.
   PubMedGoogle Scholar
• Yoon OK, Brem RB. 2010. Noncanonical transcript forms in yeast and their regulation during environmental stress. RNA 16:1256–1267.
   PubMed Web of Science ®Google Scholar
• Yosef N, Regev A. 2011. Impulse control: temporal dynamics in gene transcription. Cell 144:886–896.
   PubMed Web of Science ®Google Scholar
• Yuan GC, et al. 2005. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309:626–630.
   PubMed Web of Science ®Google Scholar
• Zanton SJ, Pugh BF. 2004. Changes in genomewide occupancy of core transcriptional regulators during heat stress. Proc. Natl. Acad. Sci. U. S. A. 101:16843–16848.
   PubMedGoogle Scholar
• Zanton SJ, Pugh BF. 2006. Full and partial genome-wide assembly and disassembly of the yeast transcription machinery in response to heat shock. Genes Dev. 20:2250–2265.
   PubMedGoogle Scholar
• Zawadzki KA, Morozov AV, Broach JR. 2009. Chromatin-dependent transcription factor accessibility rather than nucleosome remodeling predominates during global transcriptional restructuring in Saccharomyces cerevisiae. Mol. Biol. Cell 20:3503–3513.
   PubMedGoogle Scholar
• Zhang H, Roberts DN, Cairns BR. 2005. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123:219–231.
   PubMed Web of Science ®Google Scholar
• Zhang L, Ma H, Pugh BF. 2011. Stable and dynamic nucleosome states during a meiotic developmental process. Genome Res. 21:875–884.
   PubMedGoogle Scholar
• Zhu C, et al. 2009. High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res. 19:556–566.
   PubMed Web of Science ®Google Scholar