IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43739-5.html
   My bibliography  Save this article

CENP-A and CENP-B collaborate to create an open centromeric chromatin state

Author

Listed:
  • Harsh Nagpal

    (SB ISIC LCBM)

  • Ahmad Ali-Ahmad

    (University of Oslo)

  • Yasuhiro Hirano

    (Osaka University)

  • Wei Cai

    (SB ISIC LCBM)

  • Mario Halic

    (St. Jude Children’s Research Hospital)

  • Tatsuo Fukagawa

    (Osaka University)

  • Nikolina Sekulić

    (University of Oslo
    University of Oslo)

  • Beat Fierz

    (SB ISIC LCBM)

Abstract

Centromeres are epigenetically defined via the presence of the histone H3 variant CENP-A. Contacting CENP-A nucleosomes, the constitutive centromere associated network (CCAN) and the kinetochore assemble, connecting the centromere to spindle microtubules during cell division. The DNA-binding centromeric protein CENP-B is involved in maintaining centromere stability and, together with CENP-A, shapes the centromeric chromatin state. The nanoscale organization of centromeric chromatin is not well understood. Here, we use single-molecule fluorescence and cryoelectron microscopy (cryoEM) to show that CENP-A incorporation establishes a dynamic and open chromatin state. The increased dynamics of CENP-A chromatin create an opening for CENP-B DNA access. In turn, bound CENP-B further opens the chromatin fiber structure and induces nucleosomal DNA unwrapping. Finally, removal of CENP-A increases CENP-B mobility in cells. Together, our studies show that the two centromere-specific proteins collaborate to reshape chromatin structure, enabling the binding of centromeric factors and establishing a centromeric chromatin state.

Suggested Citation

  • Harsh Nagpal & Ahmad Ali-Ahmad & Yasuhiro Hirano & Wei Cai & Mario Halic & Tatsuo Fukagawa & Nikolina Sekulić & Beat Fierz, 2023. "CENP-A and CENP-B collaborate to create an open centromeric chromatin state," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43739-5
    DOI: 10.1038/s41467-023-43739-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43739-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43739-5?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. Nikolina Sekulic & Emily A. Bassett & Danielle J. Rogers & Ben E. Black, 2010. "The structure of (CENP-A–H4)2 reveals physical features that mark centromeres," Nature, Nature, vol. 467(7313), pages 347-351, September.
    2. Thomas Schalch & Sylwia Duda & David F. Sargent & Timothy J. Richmond, 2005. "X-ray structure of a tetranucleosome and its implications for the chromatin fibre," Nature, Nature, vol. 436(7047), pages 138-141, July.
    3. Viviana Barra & Glennis A. Logsdon & Andrea Scelfo & Sebastian Hoffmann & Solène Hervé & Aaron Aslanian & Yael Nechemia-Arbely & Don W. Cleveland & Ben E. Black & Daniele Fachinetti, 2019. "Phosphorylation of CENP-A on serine 7 does not control centromere function," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    4. Bing-Rui Zhou & K. N. Sathish Yadav & Mario Borgnia & Jingjun Hong & Baohua Cao & Ada L. Olins & Donald E. Olins & Yawen Bai & Ping Zhang, 2019. "Atomic resolution cryo-EM structure of a native-like CENP-A nucleosome aided by an antibody fragment," Nature Communications, Nature, vol. 10(1), pages 1-7, December.
    5. Hiroaki Tachiwana & Wataru Kagawa & Tatsuya Shiga & Akihisa Osakabe & Yuta Miya & Kengo Saito & Yoko Hayashi-Takanaka & Takashi Oda & Mamoru Sato & Sam-Yong Park & Hiroshi Kimura & Hitoshi Kurumizaka, 2011. "Crystal structure of the human centromeric nucleosome containing CENP-A," Nature, Nature, vol. 476(7359), pages 232-235, August.
    6. Kaige Yan & Jing Yang & Ziguo Zhang & Stephen H. McLaughlin & Leifu Chang & Domenico Fasci & Ann E. Ehrenhofer-Murray & Albert J. R. Heck & David Barford, 2019. "Structure of the inner kinetochore CCAN complex assembled onto a centromeric nucleosome," Nature, Nature, vol. 574(7777), pages 278-282, October.
    7. Ravindra D. Makde & Joseph R. England & Hemant P. Yennawar & Song Tan, 2010. "Structure of RCC1 chromatin factor bound to the nucleosome core particle," Nature, Nature, vol. 467(7315), pages 562-566, September.
    8. Sinan Kilic & Andreas L. Bachmann & Louise C. Bryan & Beat Fierz, 2015. "Multivalency governs HP1α association dynamics with the silent chromatin state," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    9. 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.
    10. Sinan Kilic & Suren Felekyan & Olga Doroshenko & Iuliia Boichenko & Mykola Dimura & Hayk Vardanyan & Louise C. Bryan & Gaurav Arya & Claus A. M. Seidel & Beat Fierz, 2018. "Single-molecule FRET reveals multiscale chromatin dynamics modulated by HP1α," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    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. 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.
    2. Khalil Joron & Juliane Oliveira Viegas & Liam Haas-Neill & Sariel Bier & Paz Drori & Shani Dvir & Patrick Siang Lin Lim & Sarah Rauscher & Eran Meshorer & Eitan Lerner, 2023. "Fluorescent protein lifetimes report densities and phases of nuclear condensates during embryonic stem-cell differentiation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. Wolfram Möbius & Ulrich Gerland, 2010. "Quantitative Test of the Barrier Nucleosome Model for Statistical Positioning of Nucleosomes Up- and Downstream of Transcription Start Sites," PLOS Computational Biology, Public Library of Science, vol. 6(8), pages 1-11, August.
    9. Zhen Hou & Frank Nightingale & Yanan Zhu & Craig MacGregor-Chatwin & Peijun Zhang, 2023. "Structure of native chromatin fibres revealed by Cryo-ET in situ," Nature Communications, Nature, vol. 14(1), pages 1-7, December.
    10. Francesca Maggioni & Marida Bertocchi & Ettore Mosca & Rolland Reinbold & Ileana Zucchi, 2013. "Modeling chromatin fibre folding for human embryonic stem cells," Working Papers (2013-) 1301_qum, University of Bergamo, Department of Management, Economics and Quantitative Methods.
    11. Guo-Cheng Yuan & Jun S Liu, 2008. "Genomic Sequence Is Highly Predictive of Local Nucleosome Depletion," PLOS Computational Biology, Public Library of Science, vol. 4(1), pages 1-11, January.
    12. Leelavati Narlikar & Raluca Gordân & Alexander J Hartemink, 2007. "A Nucleosome-Guided Map of Transcription Factor Binding Sites in Yeast," PLOS Computational Biology, Public Library of Science, vol. 3(11), pages 1-10, November.
    13. Matti Annala & Kirsti Laurila & Harri Lähdesmäki & Matti Nykter, 2011. "A Linear Model for Transcription Factor Binding Affinity Prediction in Protein Binding Microarrays," PLOS ONE, Public Library of Science, vol. 6(5), pages 1-13, May.
    14. Rina Hirano & Haruhiko Ehara & Tomoya Kujirai & Tamami Uejima & Yoshimasa Takizawa & Shun-ichi Sekine & Hitoshi Kurumizaka, 2022. "Structural basis of RNA polymerase II transcription on the chromatosome containing linker histone H1," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    15. Wei Chen & Hao Lin & Peng-Mian Feng & Chen Ding & Yong-Chun Zuo & Kuo-Chen Chou, 2012. "iNuc-PhysChem: A Sequence-Based Predictor for Identifying Nucleosomes via Physicochemical Properties," PLOS ONE, Public Library of Science, vol. 7(10), pages 1-9, October.
    16. Uwe Schneider & Fabiano Vasi & Jürgen Besserer, 2016. "The Impact of the Geometrical Structure of the DNA on Parameters of the Track-Event Theory for Radiation Induced Cell Kill," PLOS ONE, Public Library of Science, vol. 11(10), pages 1-13, October.
    17. 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.
    18. Meng Zhang & César Díaz-Celis & Jianfang Liu & Jinhui Tao & Paul D. Ashby & Carlos Bustamante & Gang Ren, 2024. "Angle between DNA linker and nucleosome core particle regulates array compaction revealed by individual-particle cryo-electron tomography," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    19. Ai Kiyomitsu & Toshiya Nishimura & Shiang Jyi Hwang & Satoshi Ansai & Masato T. Kanemaki & Minoru Tanaka & Tomomi Kiyomitsu, 2024. "Ran-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    20. Markus Götz & Anders Barth & Søren S.-R. Bohr & Richard Börner & Jixin Chen & Thorben Cordes & Dorothy A. Erie & Christian Gebhardt & Mélodie C. A. S. Hadzic & George L. Hamilton & Nikos S. Hatzakis &, 2022. "A blind benchmark of analysis tools to infer kinetic rate constants from single-molecule FRET trajectories," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

    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:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43739-5. 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: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    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.