153
Views
1
CrossRef citations to date
0
Altmetric
Research Article

Reb1, Cbf1, and Pho4 Bias Histone Sliding and Deposition Away from Their Binding Sites

ORCID Icon & ORCID Icon
Article: e00472-21 | Received 29 Sep 2021, Accepted 04 Dec 2021, Published online: 27 Feb 2023

REFERENCES

  • Knezetic JA, Luse DS. 1986. The presence of nucleosomes on a DNA template prevents initiation by RNA polymerase II in vitro. Cell 45:95–104. https://doi.org/10.1016/0092-8674(86)90541-6.
  • Lorch Y, LaPointe JW, Kornberg RD. 1987. Nucleosomes inhibit the initiation of transcription but allow chain elongation with the displacement of histones. Cell 49:203–210. https://doi.org/10.1016/0092-8674(87)90561-7.
  • Han M, Grunstein M. 1988. Nucleosome loss activates yeast downstream promoters in vivo. Cell 55:1137–1145. https://doi.org/10.1016/0092-8674(88)90258-9.
  • Kornberg RD, Lorch Y. 1999. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285–294. https://doi.org/10.1016/s0092-8674(00)81958-3.
  • Lee W, Tillo D, Bray N, Morse RH, Davis RW, Hughes TR, Nislow C. 2007. A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39:1235–1244. https://doi.org/10.1038/ng2117.
  • Jiang C, Pugh BF. 2009. Nucleosome positioning and gene regulation: advances through genomics. Nat Rev Genet 10:161–172. https://doi.org/10.1038/nrg2522.
  • Struhl K, Segal E. 2013. Determinants of nucleosome positioning. Nat Struct Mol Biol 20:267–273. https://doi.org/10.1038/nsmb.2506.
  • Rhee HS, Bataille AR, Zhang L, Pugh BF. 2014. Subnucleosomal structures and nucleosome asymmetry across a genome. Cell 159:1377–1388. https://doi.org/10.1016/j.cell.2014.10.054.
  • Clapier CR, Cairns BR. 2009. The biology of chromatin remodeling complexes. Annu Rev Biochem 78:273–304. https://doi.org/10.1146/annurev.biochem.77.062706.153223.
  • Bartholomew B. 2014. Regulating the chromatin landscape: structural and mechanistic perspectives. Annu Rev Biochem 83:671–696. https://doi.org/10.1146/annurev-biochem-051810-093157.
  • Mueller-Planitz F, Klinker H, Becker PB. 2013. Nucleosome sliding mechanisms: new twists in a looped history. Nat Struct Mol Biol 20:1026–1032. https://doi.org/10.1038/nsmb.2648.
  • Längst G, Manelyte L. 2015. Chromatin remodelers: from function to dysfunction. Genes 6:299–324. https://doi.org/10.3390/genes6020299.
  • Flaus A, Martin DMA, Barton GJ, Owen-Hughes T. 2006. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res 34:2887–2905. https://doi.org/10.1093/nar/gkl295.
  • Lusser A, Urwin DL, Kadonaga JT. 2005. Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat Struct Mol Biol 12:160–166. https://doi.org/10.1038/nsmb884.
  • Gkikopoulos T, Schofield P, Singh V, Pinskaya M, Mellor J, Smolle M, Workman JL, Barton GJ, Owen-Hughes T. 2011. A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science 333:1758–1760. https://doi.org/10.1126/science.1206097.
  • Pointner J, Persson J, Prasad P, Norman-Axelsson U, Strålfors A, Khorosjutina O, Krietenstein N, Svensson JP, Ekwall K, Korber P. 2012. CHD1 remodelers regulate nucleosome spacing in vitro and align nucleosomal arrays over gene coding regions in S. pombe. EMBO J 31:4388–4403. https://doi.org/10.1038/emboj.2012.289.
  • Imbalzano AN, Schnitzler GR, Kingston RE. 1996. Nucleosome disruption by human SWI/SNF is maintained in the absence of continued ATP hydrolysis. J Biol Chem 271:20726–20733. https://doi.org/10.1074/jbc.271.34.20726.
  • Logie C, Peterson CL. 1997. Catalytic activity of the yeast SWI/SNF complex on reconstituted nucleosome arrays. EMBO J 16:6772–6782. https://doi.org/10.1093/emboj/16.22.6772.
  • Aoyagi S, Narlikar G, Zheng C, Sif S, Kingston RE, Hayes JJ. 2002. Nucleosome remodeling by the human SWI/SNF complex requires transient global disruption of histone-DNA interactions. Mol Cell Biol 22:3653–3662. https://doi.org/10.1128/MCB.22.11.3653-3662.2002.
  • Stockdale C, Flaus A, Ferreira H, Owen-Hughes T. 2006. Analysis of nucleosome repositioning by yeast ISWI and Chd1 chromatin remodeling complexes. J Biol Chem 281:16279–16288. https://doi.org/10.1074/jbc.M600682200.
  • Saha A, Wittmeyer J, Cairns BR. 2005. Chromatin remodeling through directional DNA translocation from an internal nucleosomal site. Nat Struct Mol Biol 12:747–755. https://doi.org/10.1038/nsmb973.
  • Kassabov SR, Zhang B, Persinger J, Bartholomew B. 2003. SWI/SNF unwraps, slides, and rewraps the nucleosome. Mol Cell 11:391–403. https://doi.org/10.1016/s1097-2765(03)00039-x.
  • Flaus A, Owen-Hughes T. 2003. Dynamic properties of nucleosomes during thermal and ATP-driven mobilization. Mol Cell Biol 23:7767–7779. https://doi.org/10.1128/MCB.23.21.7767-7779.2003.
  • Nodelman IM, Horvath KC, Levendosky RF, Winger J, Ren R, Patel A, Li M, Wang MD, Roberts E, Bowman GD. 2016. The Chd1 chromatin remodeler can sense both entry and exit sides of the nucleosome. Nucleic Acids Res 44:7580–7591. https://doi.org/10.1093/nar/gkw406.
  • Zofall M, Persinger J, Kassabov SR, Bartholomew B.2006. Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nat Struct Mol Biol 13:339–346. https://doi.org/10.1038/nsmb1071.
  • Fletcher TM, Xiao N, Mautino G, Baumann CT, Wolford R, Warren BS, Hager GL. 2002. ATP-dependent mobilization of the glucocorticoid receptor during chromatin remodeling. Mol Cell Biol 22:3255–3263. https://doi.org/10.1128/MCB.22.10.3255-3263.2002.
  • 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. https://doi.org/10.1016/s1097-2765(04)00178-9.
  • Li M, Hada A, Sen P, Olufemi L, Hall MA, Smith BY, Forth S, McKnight JN, Patel A, Bowman GD, Bartholomew B, Wang MD. 2015. Dynamic regulation of transcription factors by nucleosome remodeling. Elife 4:e06249. https://doi.org/10.7554/eLife.06249.
  • Hartley PD, Madhani HD. 2009. Mechanisms that specify promoter nucleosome location and identity. Cell 137:445–458. https://doi.org/10.1016/j.cell.2009.02.043.
  • Ganguli D, Chereji RV, Iben JR, Cole HA, Clark DJ. 2014. RSC-dependent constructive and destructive interference between opposing arrays of phased nucleosomes in yeast. Genome Res 24:1637–1649. https://doi.org/10.1101/gr.177014.114.
  • Kubik S, Bruzzone MJ, Jacquet P, Falcone J-L, Rougemont J, Shore D. 2015. Nucleosome stability distinguishes two different promoter types at all protein-coding genes in yeast. Mol Cell 60:422–434. https://doi.org/10.1016/j.molcel.2015.10.002.
  • Klein-Brill A, Joseph-Strauss D, Appleboim A, Friedman N. 2019. Dynamics of chromatin and transcription during transient depletion of the RSC chromatin remodeling complex. Cell Rep 26:279–292.e5. https://doi.org/10.1016/j.celrep.2018.12.020.
  • Planta RJ, Gonçalves PM, Mager WH. 1995. Global regulators of ribosome biosynthesis in yeast. Biochem Cell Biol 73:825–834. https://doi.org/10.1139/o95-090.
  • Chasman DI, Lue NF, Buchman AR, LaPointe JW, Lorch Y, Kornberg RD. 1990. A yeast protein that influences the chromatin structure of UASG and functions as a powerful auxiliary gene activator. Genes Dev 4:503–514. https://doi.org/10.1101/gad.4.4.503.
  • Jaiswal R, Choudhury M, Zaman S, Singh S, Santosh V, Bastia D, Escalante CR. 2016. Functional architecture of the Reb1-Ter complex of Schizosaccharomyces pombe. Proc Natl Acad Sci USA 113:E2267–E2276. https://doi.org/10.1073/pnas.1525465113.
  • Elemento O, Tavazoie S. 2005. Fast and systematic genome-wide discovery of conserved regulatory elements using a non-alignment based approach. Genome Biol 6:R18. https://doi.org/10.1186/gb-2005-6-2-r18.
  • Badis G, Chan ET, van Bakel H, Pena-Castillo L, Tillo D, Tsui K, Carlson CD, Gossett AJ, Hasinoff MJ, Warren CL, Gebbia M, Talukder S, Yang A, Mnaimneh S, Terterov D, Coburn D, Li Yeo A, Yeo ZX, Clarke ND, Lieb JD, Ansari AZ, Nislow C, Hughes TR. 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. https://doi.org/10.1016/j.molcel.2008.11.020.
  • Yan C, Chen H, Bai L. 2018. Systematic study of nucleosome-displacing factors in budding yeast. Mol Cell 71:294–305.e4. https://doi.org/10.1016/j.molcel.2018.06.017.
  • Yu L, Morse RH. 1999. Chromatin opening and transactivator potentiation by RAP1 in Saccharomyces cerevisiae. Mol Cell Biol 19:5279–5288. https://doi.org/10.1128/MCB.19.8.5279.
  • Donovan BT, Chen H, Jipa C, Bai L, Poirier MG. 2019. Dissociation rate compensation mechanism for budding yeast pioneer transcription factors. Elife 8:e43008. https://doi.org/10.7554/eLife.43008.
  • Bai L, Ondracka A, Cross FR. 2011. Multiple sequence-specific factors generate the nucleosome-depleted region on CLN2 promoter. Mol Cell 42:465–476. https://doi.org/10.1016/j.molcel.2011.03.028.
  • Raisner RM, Hartley PD, Meneghini MD, Bao MZ, Liu CL, Schreiber SL, Rando OJ, Madhani HD. 2005. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123:233–248. https://doi.org/10.1016/j.cell.2005.10.002.
  • Ghaemmaghami S, Huh W-K, Bower K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS. 2003. Global analysis of protein expression in yeast. Nature 425:737–741. https://doi.org/10.1038/nature02046.
  • Cai M, Davis RW. 1990. Yeast centromere binding protein CBF1, of the helix-loop-helix protein family, is required for chromosome stability and methionine prototrophy. Cell 61:437–446. https://doi.org/10.1016/0092-8674(90)90525-j.
  • Zhou X, O’Shea EK. 2011. Integrated approaches reveal determinants of genome-wide binding and function of the transcription factor Pho4. Mol Cell 42:826–836. https://doi.org/10.1016/j.molcel.2011.05.025.
  • Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, Danford TW, Hannett NM, Tagne J-B, Reynolds DB, Yoo J, Jennings EG, Zeitlinger J, Pokholok DK, Kellis M, Rolfe PA, Takusagawa KT, Lander ES, Gifford DK, Fraenkel E, Young RA. 2004. Transcriptional regulatory code of a eukaryotic genome. Nature 431:99–104. https://doi.org/10.1038/nature02800.
  • MacIsaac KD, Wang T, Gordon DB, Gifford DK, Stormo GD, Fraenkel E. 2006. An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 7:113. https://doi.org/10.1186/1471-2105-7-113.
  • O’Connell KF, Baker RE. 1992. Possible cross-regulation of phosphate and sulfate metabolism in Saccharomyces cerevisiae. Genetics 132:63–73. https://doi.org/10.1093/genetics/132.1.63.
  • Zaret KS, Carroll JS. 2011. Pioneer transcription factors: establishing competence for gene expression. Genes Dev 25:2227–2241. https://doi.org/10.1101/gad.176826.111.
  • Lowary PT, Widom J. 1998. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol 276:19–42. https://doi.org/10.1006/jmbi.1997.1494.
  • Winger J, Bowman GD. 2017. The sequence of nucleosomal DNA modulates sliding by the Chd1 chromatin remodeler. J Mol Biol 429:808–822. https://doi.org/10.1016/j.jmb.2017.02.002.
  • Koerber RT, Rhee HS, Jiang C, Pugh BF. 2009. Interaction of transcriptional regulators with specific nucleosomes across the Saccharomyces genome. Mol Cell 35:889–902. https://doi.org/10.1016/j.molcel.2009.09.011.
  • Marshall LE, Graham DR, Reich KA, Sigman DS. 1981. Cleavage of deoxyribonucleic acid by the 1,10-phenanthroline-cuprous complex. Hydrogen peroxide requirement and primary and secondary structure specificity. Biochemistry 20:244–250. https://doi.org/10.1021/bi00505a003.
  • Drew HR, Travers AA. 1984. DNA structural variations in the E. coli tyrT promoter. Cell 37:491–502. https://doi.org/10.1016/0092-8674(84)90379-9.
  • Ferreira H, Somers J, Webster R, Flaus A, Owen-Hughes T. 2007. Histone tails and the H3 alphaN helix regulate nucleosome mobility and stability. Mol Cell Biol 27:4037–4048. https://doi.org/10.1128/MCB.02229-06.
  • Fei J, Torigoe SE, Brown CR, Khuong MT, Kassavetis GA, Boeger H, Kadonaga JT. 2015. The prenucleosome, a stable conformational isomer of the nucleosome. Genes Dev 29:2563–2575. https://doi.org/10.1101/gad.272633.115.
  • Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260. https://doi.org/10.1038/38444.
  • Luger K, Rechsteiner TJ, Richmond TJ. 1999. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol Biol 119:1–16. https://doi.org/10.1385/1-59259-681-9:1.
  • Levendosky RF, Sabantsev A, Deindl S, Bowman GD. 2016. The Chd1 chromatin remodeler shifts hexasomes unidirectionally. Elife 5:e21356. https://doi.org/10.7554/eLife.21356.
  • Arimura Y, Tachiwana H, Oda T, Sato M, Kurumizaka H. 2012. Structural analysis of the hexasome, lacking one histone H2A/H2B dimer from the conventional nucleosome. Biochemistry 51:3302–3309. https://doi.org/10.1021/bi300129b.
  • Gelbart ME, Rechsteiner T, Richmond TJ, Tsukiyama T. 2001. Interactions of Isw2 chromatin remodeling complex with nucleosomal arrays: analyses using recombinant yeast histones and immobilized templates. Mol Cell Biol 21:2098–2106. https://doi.org/10.1128/MCB.21.6.2098-2106.2001.
  • Clapier CR, Längst G, Corona DV, Becker PB, Nightingale KP. 2001. Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol Cell Biol 21:875–883. https://doi.org/10.1128/MCB.21.3.875-883.2001.
  • Ramachandran S, Henikoff S. 2016. Nucleosome dynamics during chromatin remodeling in vivo. Nucleus 7:20–26. https://doi.org/10.1080/19491034.2016.1149666.
  • Brogaard K, Xi L, Wang J-P, Widom J. 2012. A map of nucleosome positions in yeast at base-pair resolution. Nature 486:496–501. https://doi.org/10.1038/nature11142.
  • Henikoff S, Ramachandran S, Krassovsky K, Bryson TD, Codomo CA, Brogaard K, Widom J, Wang J-P, Henikoff JG. 2014. The budding yeast centromere DNA element II wraps a stable Cse4 hemisome in either orientation in vivo. Elife 3:e01861. https://doi.org/10.7554/eLife.01861.
  • Kruger W, Peterson CL, Sil A, Coburn C, Arents G, Moudrianakis EN, Herskowitz I. 1995. Amino acid substitutions in the structured domains of histones H3 and H4 partially relieve the requirement of the yeast SWI/SNF complex for transcription. Genes Dev 9:2770–2779. https://doi.org/10.1101/gad.9.22.2770.
  • Kurumizaka H, Wolffe AP. 1997. Sin mutations of histone H3: influence on nucleosome core structure and function. Mol Cell Biol 17:6953–6969. https://doi.org/10.1128/MCB.17.12.6953.
  • Flaus A, Rencurel C, Ferreira H, Wiechens N, Owen-Hughes T. 2004. Sin mutations alter inherent nucleosome mobility. EMBO J 23:343–353. https://doi.org/10.1038/sj.emboj.7600047.
  • Fleming AB, Pennings S. 2001. Antagonistic remodelling by Swi-Snf and Tup1-Ssn6 of an extensive chromatin region forms the background for FLO1 gene regulation. EMBO J 20:5219–5231. https://doi.org/10.1093/emboj/20.18.5219.
  • Kubik S, O’Duibhir E, de Jonge WJ, Mattarocci S, Albert B, Falcone J-L, Bruzzone MJ, Holstege FCP, Shore D. 2018. Sequence-directed action of RSC remodeler and general regulatory factors modulates +1 nucleosome position to facilitate transcription. Mol Cell 71:89–102.e5. https://doi.org/10.1016/j.molcel.2018.05.030.
  • Fennessy RT, Owen-Hughes T. 2016. Establishment of a promoter-based chromatin architecture on recently replicated DNA can accommodate variable inter-nucleosome spacing. Nucleic Acids Res 44:7189–7203. https://doi.org/10.1093/nar/gkw331.
  • Vasseur P, Tonazzini S, Ziane R, Camasses A, Rando OJ, Radman-Livaja M. 2016. Dynamics of nucleosome positioning maturation following genomic replication. Cell Rep 16:2651–2665. https://doi.org/10.1016/j.celrep.2016.07.083.
  • Yadav T, Whitehouse I. 2016. Replication-coupled nucleosome assembly and positioning by ATP-dependent chromatin-remodeling enzymes. Cell Rep 15:715–723. https://doi.org/10.1016/j.celrep.2016.03.059.
  • Patel A, Chakravarthy S, Morrone S, Nodelman IM, McKnight JN, Bowman GD. 2013. Decoupling nucleosome recognition from DNA binding dramatically alters the properties of the Chd1 chromatin remodeler. Nucleic Acids Res 41:1637–1648. https://doi.org/10.1093/nar/gks1440.
  • Luger K, Rechsteiner TJ, Richmond TJ. 1999. Preparation of nucleosome core particle from recombinant histones. Methods Enzymol 304:3–19. https://doi.org/10.1016/s0076-6879(99)04003-3.
  • Bowman A, Ward R, Wiechens N, Singh V, El-Mkami H, Norman DG, Owen-Hughes T. 2011. The histone chaperones Nap1 and Vps75 bind histones H3 and H4 in a tetrameric conformation. Mol Cell 41:398–408. https://doi.org/10.1016/j.molcel.2011.01.025.
  • Nodelman IM, Patel A, Levendosky RF, Bowman GD. 2020. Reconstitution and purification of nucleosomes with recombinant histones and purified DNA. Curr Protoc Mol Biol 133:e130. https://doi.org/10.1002/cpmb.130.
  • Reference deleted.
  • Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.