IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0006345.html
   My bibliography  Save this article

Multiple Aspects of ATP-Dependent Nucleosome Translocation by RSC and Mi-2 Are Directed by the Underlying DNA Sequence

Author

Listed:
  • Joke J F A van Vugt
  • Martijn de Jager
  • Magdalena Murawska
  • Alexander Brehm
  • John van Noort
  • Colin Logie

Abstract

Background: Chromosome structure, DNA metabolic processes and cell type identity can all be affected by changing the positions of nucleosomes along chromosomal DNA, a reaction that is catalysed by SNF2-type ATP-driven chromatin remodelers. Recently it was suggested that in vivo, more than 50% of the nucleosome positions can be predicted simply by DNA sequence, especially within promoter regions. This seemingly contrasts with remodeler induced nucleosome mobility. The ability of remodeling enzymes to mobilise nucleosomes over short DNA distances is well documented. However, the nucleosome translocation processivity along DNA remains elusive. Furthermore, it is unknown what determines the initial direction of movement and how new nucleosome positions are adopted. Methodology/Principal Findings: We have used AFM imaging and high resolution PAGE of mononucleosomes on 600 and 2500 bp DNA molecules to analyze ATP-dependent nucleosome repositioning by native and recombinant SNF2-type enzymes. We report that the underlying DNA sequence can control the initial direction of translocation, translocation distance, as well as the new positions adopted by nucleosomes upon enzymatic mobilization. Within a strong nucleosomal positioning sequence both recombinant Drosophila Mi-2 (CHD-type) and native RSC from yeast (SWI/SNF-type) repositioned the nucleosome at 10 bp intervals, which are intrinsic to the positioning sequence. Furthermore, RSC-catalyzed nucleosome translocation was noticeably more efficient when beyond the influence of this sequence. Interestingly, under limiting ATP conditions RSC preferred to position the nucleosome with 20 bp intervals within the positioning sequence, suggesting that native RSC preferentially translocates nucleosomes with 15 to 25 bp DNA steps. Conclusions/Significance: Nucleosome repositioning thus appears to be influenced by both remodeler intrinsic and DNA sequence specific properties that interplay to define ATPase-catalyzed repositioning. Here we propose a successive three-step framework consisting of initiation, translocation and release steps to describe SNF2-type enzyme mediated nucleosome translocation along DNA. This conceptual framework helps resolve the apparent paradox between the high abundance of ATP-dependent remodelers per nucleus and the relative success of sequence-based predictions of nucleosome positioning in vivo.

Suggested Citation

  • Joke J F A van Vugt & Martijn de Jager & Magdalena Murawska & Alexander Brehm & John van Noort & Colin Logie, 2009. "Multiple Aspects of ATP-Dependent Nucleosome Translocation by RSC and Mi-2 Are Directed by the Underlying DNA Sequence," PLOS ONE, Public Library of Science, vol. 4(7), pages 1-14, July.
  • Handle: RePEc:plo:pone00:0006345
    DOI: 10.1371/journal.pone.0006345
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0006345
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0006345&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0006345?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Sina Ghaemmaghami & Won-Ki Huh & Kiowa Bower & Russell W. Howson & Archana Belle & Noah Dephoure & Erin K. O'Shea & Jonathan S. Weissman, 2003. "Global analysis of protein expression in yeast," Nature, Nature, vol. 425(6959), pages 737-741, October.
    2. Andrew J. Bannister & Philip Zegerman & Janet F. Partridge & Eric A. Miska & Jean O. Thomas & Robin C. Allshire & Tony Kouzarides, 2001. "Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain," Nature, Nature, vol. 410(6824), pages 120-124, March.
    3. John F. Flanagan & Li-Zhi Mi & Maksymilian Chruszcz & Marcin Cymborowski & Katrina L. Clines & Youngchang Kim & Wladek Minor & Fraydoon Rastinejad & Sepideh Khorasanizadeh, 2005. "Double chromodomains cooperate to recognize the methylated histone H3 tail," Nature, Nature, vol. 438(7071), pages 1181-1185, December.
    4. Eran Segal & Yvonne Fondufe-Mittendorf & Lingyi Chen & AnnChristine Thåström & Yair Field & Irene K. Moore & Ji-Ping Z. Wang & Jonathan Widom, 2006. "A genomic code for nucleosome positioning," Nature, Nature, vol. 442(7104), pages 772-778, August.
    5. Won-Ki Huh & James V. Falvo & Luke C. Gerke & Adam S. Carroll & Russell W. Howson & Jonathan S. Weissman & Erin K. O'Shea, 2003. "Global analysis of protein localization in budding yeast," Nature, Nature, vol. 425(6959), pages 686-691, October.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Nebojsa Jukic & Alma P. Perrino & Frédéric Humbert & Aurélien Roux & Simon Scheuring, 2022. "Snf7 spirals sense and alter membrane curvature," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Oliver M Crook & Aikaterini Geladaki & Daniel J H Nightingale & Owen L Vennard & Kathryn S Lilley & Laurent Gatto & Paul D W Kirk, 2020. "A semi-supervised Bayesian approach for simultaneous protein sub-cellular localisation assignment and novelty detection," PLOS Computational Biology, Public Library of Science, vol. 16(11), pages 1-21, November.
    3. Jae Kyoung Kim & Eduardo D Sontag, 2017. "Reduction of multiscale stochastic biochemical reaction networks using exact moment derivation," PLOS Computational Biology, Public Library of Science, vol. 13(6), pages 1-24, June.
    4. Julia P. Schessner & Vincent Albrecht & Alexandra K. Davies & Pavel Sinitcyn & Georg H. H. Borner, 2023. "Deep and fast label-free Dynamic Organellar Mapping," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. Ji-Ping Wang & Yvonne Fondufe-Mittendorf & Liqun Xi & Guei-Feng Tsai & Eran Segal & Jonathan Widom, 2008. "Preferentially Quantized Linker DNA Lengths in Saccharomyces cerevisiae," PLOS Computational Biology, Public Library of Science, vol. 4(9), pages 1-10, September.
    6. Kazunari Iwamoto & Yuki Shindo & Koichi Takahashi, 2016. "Modeling Cellular Noise Underlying Heterogeneous Cell Responses in the Epidermal Growth Factor Signaling Pathway," PLOS Computational Biology, Public Library of Science, vol. 12(11), pages 1-18, November.
    7. Zengyu Shao & Jiuwei Lu & Nelli Khudaverdyan & Jikui Song, 2024. "Multi-layered heterochromatin interaction as a switch for DIM2-mediated DNA methylation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    8. Arthur Fischbach & Angela Johns & Kara L. Schneider & Xinxin Hao & Peter Tessarz & Thomas Nyström, 2023. "Artificial Hsp104-mediated systems for re-localizing protein aggregates," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    9. Zing Tsung-Yeh Tsai & Shin-Han Shiu & Huai-Kuang Tsai, 2015. "Contribution of Sequence Motif, Chromatin State, and DNA Structure Features to Predictive Models of Transcription Factor Binding in Yeast," PLOS Computational Biology, Public Library of Science, vol. 11(8), pages 1-22, August.
    10. Xinhao Hou & Mingjing Xu & Chengming Zhu & Jianing Gao & Meili Li & Xiangyang Chen & Cheng Sun & Björn Nashan & Jianye Zang & Ying Zhou & Shouhong Guang & Xuezhu Feng, 2023. "Systematic characterization of chromodomain proteins reveals an H3K9me1/2 reader regulating aging in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    11. Segal Mark R, 2008. "Re-Cracking the Nucleosome Positioning Code," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 7(1), pages 1-24, April.
    12. Louis-François Handfield & Yolanda T Chong & Jibril Simmons & Brenda J Andrews & Alan M Moses, 2013. "Unsupervised Clustering of Subcellular Protein Expression Patterns in High-Throughput Microscopy Images Reveals Protein Complexes and Functional Relationships between Proteins," PLOS Computational Biology, Public Library of Science, vol. 9(6), pages 1-19, June.
    13. Anneke Brümmer & Carlos Salazar & Vittoria Zinzalla & Lilia Alberghina & Thomas Höfer, 2010. "Mathematical Modelling of DNA Replication Reveals a Trade-off between Coherence of Origin Activation and Robustness against Rereplication," PLOS Computational Biology, Public Library of Science, vol. 6(5), pages 1-13, May.
    14. Emma Pierson & the GTEx Consortium & Daphne Koller & Alexis Battle & Sara Mostafavi, 2015. "Sharing and Specificity of Co-expression Networks across 35 Human Tissues," PLOS Computational Biology, Public Library of Science, vol. 11(5), pages 1-19, May.
    15. Moser Carlee & Gupta Mayetri, 2012. "A Generalized Hidden Markov Model for Determining Sequence-based Predictors of Nucleosome Positioning," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 11(2), pages 1-23, January.
    16. Maya Dinur-Mills & Merav Tal & Ophry Pines, 2008. "Dual Targeted Mitochondrial Proteins Are Characterized by Lower MTS Parameters and Total Net Charge," PLOS ONE, Public Library of Science, vol. 3(5), pages 1-8, May.
    17. Monica Naughtin & Zofia Haftek-Terreau & Johan Xavier & Sam Meyer & Maud Silvain & Yan Jaszczyszyn & Nicolas Levy & Vincent Miele & Mohamed Salah Benleulmi & Marc Ruff & Vincent Parissi & Cédric Vaill, 2015. "DNA Physical Properties and Nucleosome Positions Are Major Determinants of HIV-1 Integrase Selectivity," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-28, June.
    18. Zhdanov, Vladimir P., 2011. "Periodic perturbation of the bistable kinetics of gene expression," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 390(1), pages 57-64.
    19. Shinsuke Ohnuki & Yoshikazu Ohya, 2018. "High-dimensional single-cell phenotyping reveals extensive haploinsufficiency," PLOS Biology, Public Library of Science, vol. 16(5), pages 1-23, May.
    20. Anthony Mathelier & Wyeth W Wasserman, 2013. "The Next Generation of Transcription Factor Binding Site Prediction," PLOS Computational Biology, Public Library of Science, vol. 9(9), pages 1-18, September.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pone00:0006345. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.