IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-32657-7.html
   My bibliography  Save this article

Nucleosome-directed replication origin licensing independent of a consensus DNA sequence

Author

Listed:
  • Sai Li

    (The Rockefeller University)

  • Michael R. Wasserman

    (The Rockefeller University
    Syros Pharmaceuticals)

  • Olga Yurieva

    (The Rockefeller University
    The Rockefeller University)

  • Lu Bai

    (The Pennsylvania State University
    The Pennsylvania State University
    The Pennsylvania State University)

  • Michael E. O’Donnell

    (The Rockefeller University
    The Rockefeller University)

  • Shixin Liu

    (The Rockefeller University)

Abstract

The numerous enzymes and cofactors involved in eukaryotic DNA replication are conserved from yeast to human, and the budding yeast Saccharomyces cerevisiae (S.c.) has been a useful model organism for these studies. However, there is a gap in our knowledge of why replication origins in higher eukaryotes do not use a consensus DNA sequence as found in S.c. Using in vitro reconstitution and single-molecule visualization, we show here that S.c. origin recognition complex (ORC) stably binds nucleosomes and that ORC-nucleosome complexes have the intrinsic ability to load the replicative helicase MCM double hexamers onto adjacent nucleosome-free DNA regardless of sequence. Furthermore, we find that Xenopus laevis nucleosomes can substitute for yeast ones in engaging with ORC. Combined with re-analyses of genome-wide ORC binding data, our results lead us to propose that the yeast origin recognition machinery contains the cryptic capacity to bind nucleosomes near a nucleosome-free region and license origins, and that this nucleosome-directed origin licensing paradigm generalizes to all eukaryotes.

Suggested Citation

  • Sai Li & Michael R. Wasserman & Olga Yurieva & Lu Bai & Michael E. O’Donnell & Shixin Liu, 2022. "Nucleosome-directed replication origin licensing independent of a consensus DNA sequence," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32657-7
    DOI: 10.1038/s41467-022-32657-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-32657-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-32657-7?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. Istvan Albert & Travis N. Mavrich & Lynn P. Tomsho & Ji Qi & Sara J. Zanton & Stephan C. Schuster & B. Franklin Pugh, 2007. "Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome," Nature, Nature, vol. 446(7135), pages 572-576, March.
    2. Joseph T. P. Yeeles & Tom D. Deegan & Agnieszka Janska & Anne Early & John F. X. Diffley, 2015. "Regulated eukaryotic DNA replication origin firing with purified proteins," Nature, Nature, vol. 519(7544), pages 431-435, March.
    3. Matthew J. Rossi & Prashant K. Kuntala & William K. M. Lai & Naomi Yamada & Nitika Badjatia & Chitvan Mittal & Guray Kuzu & Kylie Bocklund & Nina P. Farrell & Thomas R. Blanda & Joshua D. Mairose & An, 2021. "A high-resolution protein architecture of the budding yeast genome," Nature, Nature, vol. 592(7853), pages 309-314, April.
    4. Pablo De Ioannes & Victor A. Leon & Zheng Kuang & Miao Wang & Jef D. Boeke & Andreas Hochwagen & Karim-Jean Armache, 2019. "Structure and function of the Orc1 BAH-nucleosome complex," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    5. Ningning Li & Wai Hei Lam & Yuanliang Zhai & Jiaxuan Cheng & Erchao Cheng & Yongqian Zhao & Ning Gao & Bik-Kwoon Tye, 2018. "Structure of the origin recognition complex bound to DNA replication origin," Nature, Nature, vol. 559(7713), pages 217-222, July.
    6. Thomas C. R. Miller & Julia Locke & Julia F. Greiwe & John F. X. Diffley & Alessandro Costa, 2019. "Mechanism of head-to-head MCM double-hexamer formation revealed by cryo-EM," Nature, Nature, vol. 575(7784), pages 704-710, November.
    7. Haizhen Long & Liwei Zhang & Mengjie Lv & Zengqi Wen & Wenhao Zhang & Xiulan Chen & Peitao Zhang & Tongqing Li & Luyuan Chang & Caiwei Jin & Guozhao Wu & Xi Wang & Fuquan Yang & Jianfeng Pei & Ping Ch, 2020. "H2A.Z facilitates licensing and activation of early replication origins," Nature, Nature, vol. 577(7791), pages 576-581, January.
    8. Alex J. Kuo & Jikui Song & Peggie Cheung & Satoko Ishibe-Murakami & Sayumi Yamazoe & James K. Chen & Dinshaw J. Patel & Or Gozani, 2012. "The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier–Gorlin syndrome," Nature, Nature, vol. 484(7392), pages 115-119, April.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Jérémy Poulet-Benedetti & Caroline Tonnerre-Doncarli & Anne-Laure Valton & Marc Laurent & Marie Gérard & Natalja Barinova & Nikolaos Parisis & Florian Massip & Franck Picard & Marie-Noëlle Prioleau, 2023. "Dimeric G-quadruplex motifs-induced NFRs determine strong replication origins in vertebrates," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Humberto Sánchez & Zhaowei Liu & Edo Veen & Theo Laar & John F. X. Diffley & Nynke H. Dekker, 2023. "A chromatinized origin reduces the mobility of ORC and MCM through interactions and spatial constraint," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

    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. Humberto Sánchez & Zhaowei Liu & Edo Veen & Theo Laar & John F. X. Diffley & Nynke H. Dekker, 2023. "A chromatinized origin reduces the mobility of ORC and MCM through interactions and spatial constraint," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. L. Maximilian Reuter & Sanjay P. Khadayate & Audrey Mossler & Korbinian Liebl & Sarah V. Faull & Mohammad M. Karimi & Christian Speck, 2024. "MCM2-7 loading-dependent ORC release ensures genome-wide origin licensing," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Yue Wu & Qiongdan Zhang & Yuhan Lin & Wai Hei Lam & Yuanliang Zhai, 2024. "Replication licensing regulated by a short linear motif within an intrinsically disordered region of origin recognition complex," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    4. Jan Marten Schmidt & Ran Yang & Ashish Kumar & Olivia Hunker & Jan Seebacher & Franziska Bleichert, 2022. "A mechanism of origin licensing control through autoinhibition of S. cerevisiae ORC·DNA·Cdc6," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Aina Maria Mas & Enrique Goñi & Igor Ruiz de los Mozos & Aida Arcas & Luisa Statello & Jovanna González & Lorea Blázquez & Wei Ting Chelsea Lee & Dipika Gupta & Álvaro Sejas & Shoko Hoshina & Alexandr, 2023. "ORC1 binds to cis-transcribed RNAs for efficient activation of replication origins," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    6. Zaida Vergara & María S. Gomez & Bénédicte Desvoyes & Joana Sequeira-Mendes & Kinda Masoud & Celina Costas & Sandra Noir & Elena Caro & Victoria Mora-Gil & Pascal Genschik & Crisanto Gutierrez, 2023. "Distinct roles of Arabidopsis ORC1 proteins in DNA replication and heterochromatic H3K27me1 deposition," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. 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.
    8. László Imre & Péter Nánási & Ibtissem Benhamza & Kata Nóra Enyedi & Gábor Mocsár & Rosevalentine Bosire & Éva Hegedüs & Erfaneh Firouzi Niaki & Ágota Csóti & Zsuzsanna Darula & Éva Csősz & Szilárd Pól, 2024. "Epigenetic modulation via the C-terminal tail of H2A.Z," Nature Communications, Nature, vol. 15(1), pages 1-21, 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. Yi Li & James Lee & Lu Bai, 2024. "DNA methylation-based high-resolution mapping of long-distance chromosomal interactions in nucleosome-depleted regions," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Dayana E. Salas-Leiva & Eelco C. Tromer & Bruce A. Curtis & Jon Jerlström-Hultqvist & Martin Kolisko & Zhenzhen Yi & Joan S. Salas-Leiva & Lucie Gallot-Lavallée & Shelby K. Williams & Geert J. P. L. K, 2021. "Genomic analysis finds no evidence of canonical eukaryotic DNA processing complexes in a free-living protist," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    12. 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.
    13. Daniel Ramírez Montero & Humberto Sánchez & Edo Veen & Theo Laar & Belén Solano & John F. X. Diffley & Nynke H. Dekker, 2023. "Nucleotide binding halts diffusion of the eukaryotic replicative helicase during activation," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    14. 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.
    15. 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.
    16. Wenting Zhang & Yue Wang & Yongjie Liu & Cuifang Liu & Yizhou Wang & Lin He & Xiao Cheng & Yani Peng & Lu Xia & Xiaodi Wu & Jiajing Wu & Yu Zhang & Luyang Sun & Ping Chen & Guohong Li & Qiang Tu & Jin, 2023. "NFIB facilitates replication licensing by acting as a genome organizer," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    17. Jiayi Fan & Andrew T. Moreno & Alexander S. Baier & Joseph J. Loparo & Craig L. Peterson, 2022. "H2A.Z deposition by SWR1C involves multiple ATP-dependent steps," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    18. Qiliang Ding & Matthew M. Edwards & Ning Wang & Xiang Zhu & Alexa N. Bracci & Michelle L. Hulke & Ya Hu & Yao Tong & Joyce Hsiao & Christine J. Charvet & Sulagna Ghosh & Robert E. Handsaker & Kevin Eg, 2021. "The genetic architecture of DNA replication timing in human pluripotent stem cells," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    19. Ananya Acharya & Hélène Bret & Jen-Wei Huang & Martin Mütze & Martin Göse & Vera Maria Kissling & Ralf Seidel & Alberto Ciccia & Raphaël Guérois & Petr Cejka, 2024. "Mechanism of DNA unwinding by MCM8-9 in complex with HROB," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    20. Jiaxuan Cheng & Ningning Li & Yunjing Huo & Shangyu Dang & Bik-Kwoon Tye & Ning Gao & Yuanliang Zhai, 2022. "Structural Insight into the MCM double hexamer activation by Dbf4-Cdc7 kinase," Nature Communications, Nature, vol. 13(1), pages 1-13, 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:13:y:2022:i:1:d:10.1038_s41467-022-32657-7. 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.