IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34310-9.html
   My bibliography  Save this article

Profilin-1 regulates DNA replication forks in a context-dependent fashion by interacting with SNF2H and BOD1L

Author

Listed:
  • Cuige Zhu

    (Washington University School of Medicine)

  • Mari Iwase

    (Washington University School of Medicine)

  • Ziqian Li

    (Washington University School of Medicine
    Sun Yat-sen University)

  • Faliang Wang

    (Washington University School of Medicine)

  • Annabel Quinet

    (Washington University School of Medicine
    University of Paris and University of Paris-Saclay, INSERM, iRCM/IBFJ CEA)

  • Alessandro Vindigni

    (Washington University School of Medicine
    Washington University School of Medicine)

  • Jieya Shao

    (Washington University School of Medicine
    Washington University School of Medicine)

Abstract

DNA replication forks are tightly controlled by a large protein network consisting of well-known core regulators and many accessory factors which remain functionally undefined. In this study, we report previously unknown nuclear functions of the actin-binding factor profilin-1 (PFN1) in DNA replication, which occur in a context-dependent fashion and require its binding to poly-L-proline (PLP)-containing proteins instead of actin. In unperturbed cells, PFN1 increases DNA replication initiation and accelerates fork progression by binding and stimulating the PLP-containing nucleosome remodeler SNF2H. Under replication stress, PFN1/SNF2H increases fork stalling and functionally collaborates with fork reversal enzymes to enable the over-resection of unprotected forks. In addition, PFN1 binds and functionally attenuates the PLP-containing fork protector BODL1 to increase the resection of a subset of stressed forks. Accordingly, raising nuclear PFN1 level decreases genome stability and cell survival during replication stress. Thus, PFN1 is a multi-functional regulator of DNA replication with exploitable anticancer potential.

Suggested Citation

  • Cuige Zhu & Mari Iwase & Ziqian Li & Faliang Wang & Annabel Quinet & Alessandro Vindigni & Jieya Shao, 2022. "Profilin-1 regulates DNA replication forks in a context-dependent fashion by interacting with SNF2H and BOD1L," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34310-9
    DOI: 10.1038/s41467-022-34310-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34310-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-34310-9?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. Sofija Mijic & Ralph Zellweger & Nagaraja Chappidi & Matteo Berti & Kurt Jacobs & Karun Mutreja & Sebastian Ursich & Arnab Ray Chaudhuri & Andre Nussenzweig & Pavel Janscak & Massimo Lopes, 2017. "Replication fork reversal triggers fork degradation in BRCA2-defective cells," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    2. Apolinar Maya-Mendoza & Pavel Moudry & Joanna Maria Merchut-Maya & MyungHee Lee & Robert Strauss & Jiri Bartek, 2018. "High speed of fork progression induces DNA replication stress and genomic instability," Nature, Nature, vol. 559(7713), pages 279-284, July.
    3. Chirantani Mukherjee & Vivek Tripathi & Eleni Maria Manolika & Anne Margriet Heijink & Giulia Ricci & Sarra Merzouk & H. Rudolf Boer & Jeroen Demmers & Marcel A. T. M. Vugt & Arnab Ray Chaudhuri, 2019. "RIF1 promotes replication fork protection and efficient restart to maintain genome stability," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    4. Arnab Ray Chaudhuri & Elsa Callen & Xia Ding & Ewa Gogola & Alexandra A. Duarte & Ji-Eun Lee & Nancy Wong & Vanessa Lafarga & Jennifer A. Calvo & Nicholas J. Panzarino & Sam John & Amanda Day & Anna V, 2016. "Replication fork stability confers chemoresistance in BRCA-deficient cells," Nature, Nature, vol. 535(7612), pages 382-387, July.
    5. Flavie Coquel & Maria-Joao Silva & Hervé Técher & Karina Zadorozhny & Sushma Sharma & Jadwiga Nieminuszczy & Clément Mettling & Elodie Dardillac & Antoine Barthe & Anne-Lyne Schmitz & Alexy Promonet &, 2018. "SAMHD1 acts at stalled replication forks to prevent interferon induction," Nature, Nature, vol. 557(7703), pages 57-61, May.
    6. Karen J. Mackenzie & Paula Carroll & Carol-Anne Martin & Olga Murina & Adeline Fluteau & Daniel J. Simpson & Nelly Olova & Hannah Sutcliffe & Jacqueline K. Rainger & Andrea Leitch & Ruby T. Osborn & A, 2017. "cGAS surveillance of micronuclei links genome instability to innate immunity," Nature, Nature, vol. 548(7668), pages 461-465, August.
    7. Xuetong Shen & Gaku Mizuguchi & Ali Hamiche & Carl Wu, 2000. "A chromatin remodelling complex involved in transcription and DNA processing," Nature, Nature, vol. 406(6795), pages 541-544, August.
    8. Arnab Ray Chaudhuri & Elsa Callen & Xia Ding & Ewa Gogola & Alexandra A. Duarte & Ji-Eun Lee & Nancy Wong & Vanessa Lafarga & Jennifer A. Calvo & Nicholas J. Panzarino & Sam John & Amanda Day & Anna V, 2016. "Erratum: Replication fork stability confers chemoresistance in BRCA-deficient cells," Nature, Nature, vol. 539(7629), pages 456-456, November.
    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. Arindam Datta & Kajal Biswas & Joshua A. Sommers & Haley Thompson & Sanket Awate & Claudia M. Nicolae & Tanay Thakar & George-Lucian Moldovan & Robert H. Shoemaker & Shyam K. Sharan & Robert M. Brosh, 2021. "WRN helicase safeguards deprotected replication forks in BRCA2-mutated cancer cells," Nature Communications, Nature, vol. 12(1), pages 1-22, December.
    2. Inés Paniagua & Zainab Tayeh & Mattia Falcone & Santiago Hernández Pérez & Aurora Cerutti & Jacqueline J. L. Jacobs, 2022. "MAD2L2 promotes replication fork protection and recovery in a shieldin-independent and REV3L-dependent manner," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Ramona N. Moro & Uddipta Biswas & Suhas S. Kharat & Filip D. Duzanic & Prosun Das & Maria Stavrou & Maria C. Raso & Raimundo Freire & Arnab Ray Chaudhuri & Shyam K. Sharan & Lorenza Penengo, 2023. "Interferon restores replication fork stability and cell viability in BRCA-defective cells via ISG15," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Zu Ye & Shengfeng Xu & Yin Shi & Xueqian Cheng & Yuan Zhang & Sunetra Roy & Sarita Namjoshi & Michael A. Longo & Todd M. Link & Katharina Schlacher & Guang Peng & Dihua Yu & Bin Wang & John A. Tainer , 2024. "GRB2 stabilizes RAD51 at reversed replication forks suppressing genomic instability and innate immunity against cancer," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Maria Dilia Palumbieri & Chiara Merigliano & Daniel González-Acosta & Danina Kuster & Jana Krietsch & Henriette Stoy & Thomas Känel & Svenja Ulferts & Bettina Welter & Joël Frey & Cyril Doerdelmann & , 2023. "Nuclear actin polymerization rapidly mediates replication fork remodeling upon stress by limiting PrimPol activity," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Daipayan Banerjee & Kurt Langberg & Salar Abbas & Eric Odermatt & Praveen Yerramothu & Martin Volaric & Matthew A. Reidenbach & Kathy J. Krentz & C. Dustin Rubinstein & David L. Brautigan & Tarek Abba, 2021. "A non-canonical, interferon-independent signaling activity of cGAMP triggers DNA damage response signaling," Nature Communications, Nature, vol. 12(1), pages 1-24, December.
    7. Anastasia Hale & Ashna Dhoonmoon & Joshua Straka & Claudia M. Nicolae & George-Lucian Moldovan, 2023. "Multi-step processing of replication stress-derived nascent strand DNA gaps by MRE11 and EXO1 nucleases," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    8. Ashna Dhoonmoon & Claudia M. Nicolae & George-Lucian Moldovan, 2022. "The KU-PARP14 axis differentially regulates DNA resection at stalled replication forks by MRE11 and EXO1," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    9. Anne Margriet Heijink & Colin Stok & David Porubsky & Eleni Maria Manolika & Jurrian K. Kanter & Yannick P. Kok & Marieke Everts & H. Rudolf Boer & Anastasia Audrey & Femke J. Bakker & Elles Wierenga , 2022. "Sister chromatid exchanges induced by perturbed replication can form independently of BRCA1, BRCA2 and RAD51," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    10. Tanay Thakar & Ashna Dhoonmoon & Joshua Straka & Emily M. Schleicher & Claudia M. Nicolae & George-Lucian Moldovan, 2022. "Lagging strand gap suppression connects BRCA-mediated fork protection to nucleosome assembly through PCNA-dependent CAF-1 recycling," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    11. Rishi Kumar Jaiswal & Kai-Hang Lei & Megan Chastain & Yuan Wang & Olga Shiva & Shan Li & Zhongsheng You & Peter Chi & Weihang Chai, 2023. "CaMKK2 and CHK1 phosphorylate human STN1 in response to replication stress to protect stalled forks from aberrant resection," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    12. Diego Dibitetto & Martin Liptay & Francesca Vivalda & Hülya Dogan & Ewa Gogola & Martín González Fernández & Alexandra Duarte & Jonas A. Schmid & Morgane Decollogny & Paola Francica & Sara Przetocka &, 2024. "H2AX promotes replication fork degradation and chemosensitivity in BRCA-deficient tumours," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    13. Nikolaos Parisis & Pablo D. Dans & Muhammad Jbara & Balveer Singh & Diane Schausi-Tiffoche & Diego Molina-Serrano & Isabelle Brun-Heath & Denisa Hendrychová & Suman Kumar Maity & Diana Buitrago & Rafa, 2023. "Histone H3 serine-57 is a CHK1 substrate whose phosphorylation affects DNA repair," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    14. Hervé Técher & Diyavarshini Gopaul & Jonathan Heuzé & Nail Bouzalmad & Baptiste Leray & Audrey Vernet & Clément Mettling & Jérôme Moreaux & Philippe Pasero & Yea-Lih Lin, 2024. "MRE11 and TREX1 control senescence by coordinating replication stress and interferon signaling," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    15. Antonios Revythis & Anu Limbu & Christos Mikropoulos & Aruni Ghose & Elisabet Sanchez & Matin Sheriff & Stergios Boussios, 2022. "Recent Insights into PARP and Immuno-Checkpoint Inhibitors in Epithelial Ovarian Cancer," IJERPH, MDPI, vol. 19(14), pages 1-19, July.
    16. Domagoj Vugic & Isaac Dumoulin & Charlotte Martin & Anna Minello & Lucia Alvaro-Aranda & Jesus Gomez-Escudero & Rady Chaaban & Rana Lebdy & Catharina Nicolai & Virginie Boucherit & Cyril Ribeyre & Ang, 2023. "Replication gap suppression depends on the double-strand DNA binding activity of BRCA2," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    17. Vera M. Kissling & Giordano Reginato & Eliana Bianco & Kristina Kasaciunaite & Janny Tilma & Gea Cereghetti & Natalie Schindler & Sung Sik Lee & Raphaël Guérois & Brian Luke & Ralf Seidel & Petr Cejka, 2022. "Mre11-Rad50 oligomerization promotes DNA double-strand break repair," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    18. Nagham Ghaddar & Yves Corda & Pierre Luciano & Martina Galli & Ylli Doksani & Vincent Géli, 2023. "The COMPASS subunit Spp1 protects nascent DNA at the Tus/Ter replication fork barrier by limiting DNA availability to nucleases," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    19. Ivo A. Hendriks & Sara C. Buch-Larsen & Evgeniia Prokhorova & Jonas D. Elsborg & Alexandra K.L.F.S. Rebak & Kang Zhu & Dragana Ahel & Claudia Lukas & Ivan Ahel & Michael L. Nielsen, 2021. "The regulatory landscape of the human HPF1- and ARH3-dependent ADP-ribosylome," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    20. Kate E. Coleman & Yandong Yin & Sarah Kit Leng Lui & Sarah Keegan & David Fenyo & Duncan J. Smith & Eli Rothenberg & Tony T. Huang, 2022. "USP1-trapping lesions as a source of DNA replication stress and genomic instability," Nature Communications, Nature, vol. 13(1), pages 1-19, 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_s41467-022-34310-9. 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.