دورية أكاديمية
Dynamic epistasis analysis reveals how chromatin remodeling regulates transcriptional bursting.
العنوان: | Dynamic epistasis analysis reveals how chromatin remodeling regulates transcriptional bursting. |
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المؤلفون: | Brouwer I; Division of Gene Regulation, the Netherlands Cancer Institute, Oncode Institute, Amsterdam, the Netherlands., Kerklingh E; Division of Gene Regulation, the Netherlands Cancer Institute, Oncode Institute, Amsterdam, the Netherlands., van Leeuwen F; Division of Gene Regulation, the Netherlands Cancer Institute, Amsterdam, the Netherlands.; Department of Medical Biology, Amsterdam UMC, University of Amsterdam, Amsterdam, the Netherlands., Lenstra TL; Division of Gene Regulation, the Netherlands Cancer Institute, Oncode Institute, Amsterdam, the Netherlands. t.lenstra@nki.nl. |
المصدر: | Nature structural & molecular biology [Nat Struct Mol Biol] 2023 May; Vol. 30 (5), pp. 692-702. Date of Electronic Publication: 2023 May 01. |
نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't |
اللغة: | English |
بيانات الدورية: | Publisher: Nature Pub. Group Country of Publication: United States NLM ID: 101186374 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1545-9985 (Electronic) Linking ISSN: 15459985 NLM ISO Abbreviation: Nat Struct Mol Biol Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: New York : Nature Pub. Group, c2004- |
مواضيع طبية MeSH: | Nucleosomes*/metabolism , Saccharomyces cerevisiae Proteins*/genetics , Saccharomyces cerevisiae Proteins*/metabolism, Chromatin Assembly and Disassembly ; Epistasis, Genetic ; Transcription Factors/metabolism ; Chromatin/metabolism ; Saccharomyces cerevisiae/genetics ; Saccharomyces cerevisiae/metabolism ; Transcription, Genetic |
مستخلص: | Transcriptional bursting has been linked to the stochastic positioning of nucleosomes. However, how bursting is regulated by the remodeling of promoter nucleosomes is unknown. Here, we use single-molecule live-cell imaging of GAL10 transcription in Saccharomyces cerevisiae to measure how bursting changes upon combined perturbations of chromatin remodelers, the transcription factor Gal4 and preinitiation complex components. Using dynamic epistasis analysis, we reveal how the remodeling of different nucleosomes regulates transcriptional bursting parameters. At the nucleosome covering the Gal4 binding sites, RSC and Gal4 binding synergistically facilitate each burst. Conversely, nucleosome remodeling at the TATA box controls only the first burst upon galactose induction. At canonical TATA boxes, the nucleosomes are displaced by TBP binding to allow for transcription activation even in the absence of remodelers. Overall, our results reveal how promoter nucleosome remodeling together with Gal4 and preinitiation complex binding regulates transcriptional bursting. (© 2023. The Author(s).) |
References: | Rodriguez, J. et al. Intrinsic dynamics of a human gene reveal the basis of expression heterogeneity. Cell 176, 213–226 (2019). (PMID: 3055487610.1016/j.cell.2018.11.026) Bartman, C. R., Hsu, S. C., Hsiung, C. C. S., Raj, A. & Blobel, G. A. Enhancer regulation of transcriptional bursting parameters revealed by forced chromatin looping. Mol. Cell 62, 237–247 (2016). (PMID: 27067601484214810.1016/j.molcel.2016.03.007) Fukaya, T., Lim, B. & Levine, M. Enhancer control of transcriptional bursting. Cell 166, 358–368 (2016). (PMID: 27293191497075910.1016/j.cell.2016.05.025) Donovan, B. T. et al. Live-cell imaging reveals the interplay between transcription factors, nucleosomes, and bursting. EMBO J. 38, e100809 (2019). (PMID: 31101674657617410.15252/embj.2018100809) Pimmett, V. L. et al. Quantitative imaging of transcription in living Drosophila embryos reveals the impact of core promoter motifs on promoter state dynamics. Nat. Commun. 12, 4504 (2021). (PMID: 34301936830261210.1038/s41467-021-24461-6) Tunnacliffe, E. & Chubb, J. R. What is a transcriptional burst? Trends Genet. 36, 288–297 (2020). (PMID: 3203565610.1016/j.tig.2020.01.003) Zoller, B., Little, S. C. & Gregor, T. Diverse spatial expression patterns emerge from unified kinetics of transcriptional bursting. Cell 175, 835–847 (2018). (PMID: 30340044677912510.1016/j.cell.2018.09.056) Mehta, G. D. et al. Single-molecule analysis reveals linked cycles of RSC chromatin remodeling and Ace1p transcription factor binding in yeast. Mol. Cell 72, 875–887 (2018). (PMID: 30318444628971910.1016/j.molcel.2018.09.009) Dadiani, M. et al. Two DNA-encoded strategies for increasing expression with opposing effects on promoter dynamics and transcriptional noise. Genome Res. 23, 966–976 (2013). (PMID: 23403035366836410.1101/gr.149096.112) Shelansky, R. & Boeger, H. Nucleosomal proofreading of activator–promoter interactions. Proc. Natl Acad. Sci. USA 117, 2456–2461 (2020). (PMID: 31964832700751810.1073/pnas.1911188117) Eck, E. et al. Quantitative dissection of transcription in development yields evidence for transcription factor-driven chromatin accessibility. eLife 9, 1–99 (2020). (PMID: 10.7554/eLife.56429) Brown, C. R., Mao, C., Falkovskaia, E., Jurica, M. S. & Boeger, H. Linking stochastic fluctuations in chromatin structure and gene expression. PLoS Biol. 11, e1001621 (2013). (PMID: 23940458373546710.1371/journal.pbio.1001621) Raser, J. M. & O’Shea, E. K. Control of stochasticity in eukaryotic gene expression. Science 304, 1811–1814 (2004). (PMID: 15166317141081110.1126/science.1098641) Weinberger, L. et al. Expression noise and acetylation profiles distinguish HDAC functions. Mol. Cell 47, 193–202 (2012). (PMID: 22683268340886110.1016/j.molcel.2012.05.008) Small, E. C., Xi, L., Wang, J.-P., Widom, J. & Licht, J. D. Single-cell nucleosome mapping reveals the molecular basis of gene expression heterogeneity. Proc. Natl Acad. Sci. 111, E2462–E2471 (2014). (PMID: 24889621406651110.1073/pnas.1400517111) Prajapati, H. K., Ocampo, J. & Clark, D. J. Interplay among ATP-dependent chromatin remodelers determines chromatin organisation in yeast. Biol. (Basel). 9, 1–23 (2020). Rawal, Y. et al. SWI/SNF and RSC cooperate to reposition and evict promoter nucleosomes at highly expressed genes in yeast. Genes Dev. 32, 695–710 (2018). (PMID: 29785963600407810.1101/gad.312850.118) Kubik, S. et al. Opposing chromatin remodelers control transcription initiation frequency and start site selection. Nat. Struct. Mol. Biol. 26, 744–754 (2019). (PMID: 3138406310.1038/s41594-019-0273-3) Kubik, S. et al. Sequence-directed action of RSC remodeler and general regulatory factors modulates +1 nucleosome position to facilitate transcription. Mol. Cell 71, 89–102 (2018). (PMID: 2997997110.1016/j.molcel.2018.05.030) Klein-Brill, A., Joseph-Strauss, D., Appleboim, A. & Friedman, N. Dynamics of chromatin and transcription during transient depletion of the RSC chromatin remodeling complex. Cell Rep. 26, 279–292 (2019). (PMID: 30605682631537210.1016/j.celrep.2018.12.020) Brahma, S. & Henikoff, S. RSC-associated subnucleosomes define MNase-sensitive promoters in yeast. Mol. Cell 73, 238–249 (2019). (PMID: 3055494410.1016/j.molcel.2018.10.046) Floer, M. et al. A RSC/nucleosome complex determines chromatin architecture and facilitates activator binding. Cell 141, 407–418 (2010). (PMID: 20434983303259910.1016/j.cell.2010.03.048) Kubik, S. et al. Nucleosome stability distinguishes two different promoter types at all protein-coding genes in yeast. Mol. Cell 60, 422–434 (2015). (PMID: 2654507710.1016/j.molcel.2015.10.002) Xi, Y., Yao, J., Chen, R., Li, W. & He, X. Nucleosome fragility reveals novel functional states of chromatin and poises genes for activation. Genome Res. 21, 718–724 (2011). (PMID: 21363969308308810.1101/gr.117101.110) Weiner, A., Hughes, A., Yassour, M., Rando, O. J. & Friedman, N. High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res. 20, 90–100 (2010). (PMID: 19846608279883410.1101/gr.098509.109) Kim, J. M. et al. Single-molecule imaging of chromatin remodelers reveals role of atpase in promoting fast kinetics of target search and dissociation from chromatin. eLife 10, e69387 (2021). (PMID: 34313223835258910.7554/eLife.69387) Zhu, F. et al. The interaction landscape between transcription factors and the nucleosome. Nature 562, 76–81 (2018). (PMID: 30250250617330910.1038/s41586-018-0549-5) Mivelaz, M. et al. Chromatin fiber invasion and nucleosome displacement by the Rap1 transcription factor. Mol. Cell 77, 488–500 (2020). (PMID: 31761495700567410.1016/j.molcel.2019.10.025) Donovan, B. T., Chen, H., Jipa, C., Bai, L. & Poirier, M. G. Dissociation rate compensation mechanism for budding yeast pioneer transcription factors. eLife 8, 1–24 (2019). (PMID: 10.7554/eLife.43008) Luo, Y., North, J. A., Rose, S. D. & Poirier, M. G. Nucleosomes accelerate transcription factor dissociation. Nucleic Acids Res. 42, 3017–3027 (2014). (PMID: 2435331610.1093/nar/gkt1319) Nguyen, V. Q. et al. Spatiotemporal coordination of transcription preinitiation complex assembly in live cells. Mol. Cell 81, 3560–3575 (2021). (PMID: 34375585842087710.1016/j.molcel.2021.07.022) Wang, H., Xiong, L. & Cramer, P. Structures and implications of TBP–nucleosome complexes. Proc. Natl Acad. Sci. USA. 118, 1–7 (2021). Bryant, G. O. et al. Activator control of nucleosome occupancy in activation and repression of transcription. PLoS Biol. 6, 2928–2939 (2008). (PMID: 1910860510.1371/journal.pbio.0060317) Haruki, H., Nishikawa, J. & Laemmli, U. K. The anchor-away technique: Rapid, conditional establishment of yeast mutant phenotypes. Mol. Cell 31, 925–932 (2008). (PMID: 1892247410.1016/j.molcel.2008.07.020) Larson, D. R., Zenklusen, D., Wu, B., Chao, J. A. & Singer, R. H. Real-time observation of transcription initiation and elongation on an endogenous yeast gene. Science 332, 475–478 (2011). (PMID: 21512033315297610.1126/science.1202142) van Leeuwen, J., Boone, C. & Andrews, B. J. Mapping a diversity of genetic interactions in yeast. Curr. Opin. Syst. Biol. 6, 14–21 (2017). (PMID: 30505984626914210.1016/j.coisb.2017.08.002) Kundu, S. & Peterson, C. L. Dominant role for signal transduction in the transcriptional memory of yeast GAL genes. Mol. Cell. Biol. 30, 2330–2340 (2010). (PMID: 20212085286369310.1128/MCB.01675-09) Blake, W. J. et al. Phenotypic consequences of promoter-mediated transcriptional noise. Mol. Cell 24, 853–865 (2006). (PMID: 1718918810.1016/j.molcel.2006.11.003) Zentner, G. E. & Henikoff, S. Mot1 redistributes TBP from TATA-containing to TATA-less promoters. Mol. Cell. Biol. 33, 4996–5004 (2013). (PMID: 24144978388955210.1128/MCB.01218-13) Andrau, J. C. et al. Mot1p is essential for TBP recruitment to selected promoters during in vivo gene activation. EMBO J. 21, 5173–5183 (2002). (PMID: 1235673312902510.1093/emboj/cdf485) Dasgupta, A., Darst, R. P., Martin, K. J., Afshari, C. A. & Auble, D. T. Mot1 activates and represses transcription by direct, ATPase-dependent mechanisms. Proc. Natl Acad. Sci. USA 99, 2666–2671 (2002). (PMID: 1188062112240510.1073/pnas.052397899) Van Leeuwen, F., Gafken, P. R. & Gottschling, D. E. Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 109, 745–756 (2002). (PMID: 1208667310.1016/S0092-8674(02)00759-6) Joo, Y. J. et al. Downstream promoter interactions of TFIID TAFs facilitate transcription reinitiation. Genes Dev. 31, 2162–2174 (2017). (PMID: 29203645574916410.1101/gad.306324.117) Tramantano, M. et al. Constitutive turnover of histone H2A.Z at yeast promoters requires the preinitiation complex. eLife 5, 1–30 (2016). (PMID: 10.7554/eLife.14243) Ryan, M. P., Stafford, G. A., Yu, L. & Morse, R. H. Artificially recruited TATA-binding protein fails to remodel chromatin and does not activate three promoters that require chromatin remodeling. Mol. Cell. Biol. 20, 5847–5857 (2000). (PMID: 109131688606210.1128/MCB.20.16.5847-5857.2000) Heiss, G. et al. Conformational changes and catalytic inefficiency associated with Mot1-mediated TBP-DNA dissociation. Nucleic Acids Res. 47, 2793–2806 (2019). (PMID: 30649478645109410.1093/nar/gky1322) Koster, M. J. E. & Timmers, H. T. M. Regulation of anti-sense transcription by Mot1p and NC2 via removal of TATA-binding protein (TBP) from the 3′-end of genes. Nucleic Acids Res. 43, 143–152 (2015). (PMID: 2543295610.1093/nar/gku1263) Xue, Y. et al. Mot1, Ino80C, and NC2 function coordinately to regulate pervasive transcription in yeast and mammals. Mol. Cell 67, 594–607 (2017). (PMID: 28735899557368110.1016/j.molcel.2017.06.029) Spedale, G. et al. Tight cooperation between Mot1p and NC2β in regulating genome-wide transcription, repression of transcription following heat shock induction and genetic interaction with SAGA. Nucleic Acids Res. 40, 996–1008 (2012). (PMID: 2197673010.1093/nar/gkr784) Lenstra, T. L., Coulon, A., Chow, C. C. & Larson, D. R. Single-molecule imaging reveals a switch between spurious and functional ncRNA transcription. Mol. Cell 60, 597–610 (2015). (PMID: 26549684465608910.1016/j.molcel.2015.09.028) Polach, K. J. & Widom, J. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J. Mol. Biol. 254, 130–149 (1995). (PMID: 749073810.1006/jmbi.1995.0606) Lomvardas, S. & Thanos, D. Nucleosome sliding via TBP DNA binding in vivo. Cell 106, 685–696 (2001). (PMID: 1157277510.1016/S0092-8674(01)00490-1) MacKinnon, J. G. Bootstrap Hypothesis Testing https://ideas.repec.org/p/qed/wpaper/1127.html (2007). Jonge, W. J. et al. Molecular mechanisms that distinguish TFIID housekeeping from regulatable SAGA promoters. EMBO J. 36, 274–290 (2017). (PMID: 2797992010.15252/embj.201695621) Laughery, M. F. et al. New vectors for simple and streamlined CRISPR-Cas9 genome editing in Saccharomyces cerevisiae. Yeast 32, 711–720 (2015). (PMID: 2630504010.1002/yea.3098) Wosika, V. et al. New families of single integration vectors and gene tagging plasmids for genetic manipulations in budding yeast. Mol. Genet. Genomics 291, 2231–2240 (2016). (PMID: 2763748910.1007/s00438-016-1249-1) Brouwer, I., Patel, H. P., Meeussen, J. V. W., Pomp, W. & Lenstra, T. L. Single-molecule fluorescence imaging in living saccharomyces cerevisiae cells. STAR Protoc. 1, 100142 (2020). (PMID: 33377036775728910.1016/j.xpro.2020.100142) Edelstein, A. D. et al. Advanced methods of microscope control using μManager software. J. Biol. Methods 1, e10 (2014). (PMID: 2560657110.14440/jbm.2014.36) Coulon, A. et al. Kinetic competition during the transcription cycle results in stochastic RNA processing. eLife 3, 1–22 (2014). (PMID: 10.7554/eLife.03939) Patel, H. P., Brouwer, I. & Lenstra, T. L. Optimized protocol for single-molecule RNA FISH to visualize gene expression in S. cerevisiae. STAR Protoc. 2, 100647 (2021). (PMID: 34278333826474510.1016/j.xpro.2021.100647) Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012). (PMID: 22388286332238110.1038/nmeth.1923) Edgar, R., Domrachev, M. & Lash, A. E. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207–210 (2002). (PMID: 117522959912210.1093/nar/30.1.207) Cherry, J. M. et al. Saccharomyces genome database: the genomics resource of budding yeast. Nucleic Acids Res. 40, 700–705 (2012). (PMID: 10.1093/nar/gkr1029) Rhee, H. S. & Pugh, B. F. Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 483, 295–301 (2012). (PMID: 22258509330652710.1038/nature10799) Frederiks, F. et al. Nonprocessive methylation by Dot1 leads to functional redundancy of histone H3K79 methylation states. Nat. Struct. Mol. Biol. 15, 550–557 (2008). (PMID: 1851194310.1038/nsmb.1432) |
المشرفين على المادة: | 0 (Nucleosomes) 0 (Transcription Factors) 0 (Chromatin) 0 (Saccharomyces cerevisiae Proteins) |
تواريخ الأحداث: | Date Created: 20230501 Date Completed: 20230519 Latest Revision: 20230630 |
رمز التحديث: | 20231215 |
مُعرف محوري في PubMed: | PMC10191856 |
DOI: | 10.1038/s41594-023-00981-1 |
PMID: | 37127821 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1545-9985 |
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DOI: | 10.1038/s41594-023-00981-1 |