IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43968-8.html
   My bibliography  Save this article

Structure of the complete Saccharomyces cerevisiae Rpd3S-nucleosome complex

Author

Listed:
  • Jonathan W. Markert

    (Harvard Medical School)

  • Seychelle M. Vos

    (Massachusetts Institute of Technology)

  • Lucas Farnung

    (Harvard Medical School)

Abstract

Acetylation of histones is a key post-translational modification that guides gene expression regulation. In yeast, the class I histone deacetylase containing Rpd3S complex plays a critical role in the suppression of spurious transcription by removing histone acetylation from actively transcribed genes. The S. cerevisiae Rpd3S complex has five subunits (Rpd3, Sin3, Rco1, Eaf3, and Ume1) but its subunit stoichiometry and how the complex engages nucleosomes to achieve substrate specificity remains elusive. Here we report the cryo-EM structure of the complete Rpd3S complex bound to a nucleosome. Sin3 and two copies of subunits Rco1 and Eaf3 encircle the deacetylase subunit Rpd3 and coordinate the positioning of Ume1. The Rpd3S complex binds both trimethylated H3 tails at position lysine 36 and makes multiple additional contacts with the nucleosomal DNA and the H2A–H2B acidic patch. Direct regulation via the Sin3 subunit coordinates binding of the acetylated histone substrate to achieve substrate specificity.

Suggested Citation

  • Jonathan W. Markert & Seychelle M. Vos & Lucas Farnung, 2023. "Structure of the complete Saccharomyces cerevisiae Rpd3S-nucleosome complex," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43968-8
    DOI: 10.1038/s41467-023-43968-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43968-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43968-8?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. Colin R Lickwar & Bhargavi Rao & Andrey A Shabalin & Andrew B Nobel & Brian D Strahl & Jason D Lieb, 2009. "The Set2/Rpd3S Pathway Suppresses Cryptic Transcription without Regard to Gene Length or Transcription Frequency," PLOS ONE, Public Library of Science, vol. 4(3), pages 1-7, March.
    2. Haipeng Guan & Pei Wang & Pei Zhang & Chun Ruan & Yutian Ou & Bo Peng & Xiangdong Zheng & Jianlin Lei & Bing Li & Chuangye Yan & Haitao Li, 2023. "Diverse modes of H3K36me3-guided nucleosomal deacetylation by Rpd3S," Nature, Nature, vol. 620(7974), pages 669-675, August.
    3. Lucas Farnung & Seychelle M. Vos & Christoph Wigge & Patrick Cramer, 2017. "Nucleosome–Chd1 structure and implications for chromatin remodelling," Nature, Nature, vol. 550(7677), pages 539-542, October.
    4. Peter J. Watson & Louise Fairall & Guilherme M. Santos & John W. R. Schwabe, 2012. "Structure of HDAC3 bound to co-repressor and inositol tetraphosphate," Nature, Nature, vol. 481(7381), pages 335-340, January.
    5. Stephen E. Rundlett & Andrew A. Carmen & Noriyuki Suka & Bryan M. Turner & Michael Grunstein, 1998. "Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3," Nature, Nature, vol. 392(6678), pages 831-835, April.
    6. Avinash B. Patel & Jinkang Qing & Kelly H. Tam & Sara Zaman & Maria Luiso & Ishwar Radhakrishnan & Yuan He, 2023. "Cryo-EM structure of the Saccharomyces cerevisiae Rpd3L histone deacetylase complex," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    7. Robert E. Turnbull & Louise Fairall & Almutasem Saleh & Emma Kelsall & Kyle L. Morris & T. J. Ragan & Christos G. Savva & Aditya Chandru & Christopher J. Millard & Olga V. Makarova & Corinne J. Smith , 2020. "The MiDAC histone deacetylase complex is essential for embryonic development and has a unique multivalent structure," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    8. Ji Hyun Kim & Bo Bae Lee & Young Mi Oh & Chenchen Zhu & Lars M. Steinmetz & Yookyeong Lee & Wan Kyu Kim & Sung Bae Lee & Stephen Buratowski & TaeSoo Kim, 2016. "Modulation of mRNA and lncRNA expression dynamics by the Set2–Rpd3S pathway," Nature Communications, Nature, vol. 7(1), pages 1-11, 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. Mandy S. M. Wan & Reyhan Muhammad & Marios G. Koliopoulos & Theodoros I. Roumeliotis & Jyoti S. Choudhary & Claudio Alfieri, 2023. "Mechanism of assembly, activation and lysine selection by the SIN3B histone deacetylase complex," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Mengting Xu & Qi Zhang & Huanbin Shi & Zhongling Wu & Wei Zhou & Fucheng Lin & Yanjun Kou & Zeng Tao, 2024. "A repressive H3K36me2 reader mediates Polycomb silencing," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Avinash B. Patel & Jinkang Qing & Kelly H. Tam & Sara Zaman & Maria Luiso & Ishwar Radhakrishnan & Yuan He, 2023. "Cryo-EM structure of the Saccharomyces cerevisiae Rpd3L histone deacetylase complex," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    4. Luka Bacic & Guillaume Gaullier & Jugal Mohapatra & Guanzhong Mao & Klaus Brackmann & Mikhail Panfilov & Glen Liszczak & Anton Sabantsev & Sebastian Deindl, 2024. "Asymmetric nucleosome PARylation at DNA breaks mediates directional nucleosome sliding by ALC1," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    5. Benjamin M. Spector & Mrutyunjaya Parida & Ming Li & Christopher B. Ball & Jeffery L. Meier & Donal S. Luse & David H. Price, 2022. "Differences in RNA polymerase II complexes and their interactions with surrounding chromatin on human and cytomegalovirus genomes," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. Sofía Muñoz & Andrew Jones & Céline Bouchoux & Tegan Gilmore & Harshil Patel & Frank Uhlmann, 2022. "Functional crosstalk between the cohesin loader and chromatin remodelers," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. David Flores-Solis & Irina P. Lushpinskaia & Anton A. Polyansky & Arya Changiarath & Marc Boehning & Milana Mirkovic & James Walshe & Lisa M. Pietrek & Patrick Cramer & Lukas S. Stelzl & Bojan Zagrovi, 2023. "Driving forces behind phase separation of the carboxy-terminal domain of RNA polymerase II," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Un Seng Chio & Eugene Palovcak & Anton A. A. Smith & Henriette Autzen & Elise N. Muñoz & Zanlin Yu & Feng Wang & David A. Agard & Jean-Paul Armache & Geeta J. Narlikar & Yifan Cheng, 2024. "Functionalized graphene-oxide grids enable high-resolution cryo-EM structures of the SNF2h-nucleosome complex without crosslinking," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    9. Melissa S Gildenberg & M Todd Washington, 2019. "Conformational flexibility of fork-remodeling helicase Rad5 shown by full-ensemble hybrid methods," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-16, October.
    10. Ko Sato & Amarjeet Kumar & Keisuke Hamada & Chikako Okada & Asako Oguni & Ayumi Machiyama & Shun Sakuraba & Tomohiro Nishizawa & Osamu Nureki & Hidetoshi Kono & Kazuhiro Ogata & Toru Sengoku, 2021. "Structural basis of the regulation of the normal and oncogenic methylation of nucleosomal histone H3 Lys36 by NSD2," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    11. Yichen Zhong & Hakimeh Moghaddas Sani & Bishnu P. Paudel & Jason K. K. Low & Ana P. G. Silva & Stefan Mueller & Chandrika Deshpande & Santosh Panjikar & Xavier J. Reid & Max J. Bedward & Antoine M. Oi, 2022. "The role of auxiliary domains in modulating CHD4 activity suggests mechanistic commonality between enzyme families," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    12. Leonie G. Graf & Carlos Moreno-Yruela & Chuan Qin & Sabrina Schulze & Gottfried J. Palm & Ole Schmöker & Nancy Wang & Dianna M. Hocking & Leila Jebeli & Britta Girbardt & Leona Berndt & Babett Dörre &, 2024. "Distribution and diversity of classical deacylases in bacteria," Nature Communications, Nature, vol. 15(1), pages 1-31, 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_s41467-023-43968-8. 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.