IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47709-3.html
   My bibliography  Save this article

Phosphorylation of the F-BAR protein Hof1 drives septin ring splitting in budding yeast

Author

Listed:
  • Maritzaida Varela Salgado

    (University of Montpellier)

  • Ingrid E. Adriaans

    (University of Montpellier)

  • Sandra A. Touati

    (Institut Jacques Monod)

  • Sandy Ibanes

    (University of Montpellier)

  • Joséphine Lai-Kee-Him

    (University of Montpellier)

  • Aurélie Ancelin

    (University of Montpellier)

  • Luca Cipelletti

    (University of Montpellier
    IUF (Institut Universitaire de France)

  • Laura Picas

    (University of Montpellier)

  • Simonetta Piatti

    (University of Montpellier)

Abstract

A double septin ring accompanies cytokinesis in yeasts and mammalian cells. In budding yeast, reorganisation of the septin collar at the bud neck into a dynamic double ring is essential for actomyosin ring constriction and cytokinesis. Septin reorganisation requires the Mitotic Exit Network (MEN), a kinase cascade essential for cytokinesis. However, the effectors of MEN in this process are unknown. Here we identify the F-BAR protein Hof1 as a critical target of MEN in septin remodelling. Phospho-mimicking HOF1 mutant alleles overcome the inability of MEN mutants to undergo septin reorganisation by decreasing Hof1 binding to septins and facilitating its translocation to the actomyosin ring. Hof1-mediated septin rearrangement requires its F-BAR domain, suggesting that it may involve a local membrane remodelling that leads to septin reorganisation. In vitro Hof1 can induce the formation of intertwined septin bundles, while a phosphomimetic Hof1 protein has impaired septin-bundling activity. Altogether, our data indicate that Hof1 modulates septin architecture in distinct ways depending on its phosphorylation status.

Suggested Citation

  • Maritzaida Varela Salgado & Ingrid E. Adriaans & Sandra A. Touati & Sandy Ibanes & Joséphine Lai-Kee-Him & Aurélie Ancelin & Luca Cipelletti & Laura Picas & Simonetta Piatti, 2024. "Phosphorylation of the F-BAR protein Hof1 drives septin ring splitting in budding yeast," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47709-3
    DOI: 10.1038/s41467-024-47709-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47709-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-47709-3?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. Simon Gemble & René Wardenaar & Kristina Keuper & Nishit Srivastava & Maddalena Nano & Anne-Sophie Macé & Andréa E. Tijhuis & Sara Vanessa Bernhard & Diana C. J. Spierings & Anthony Simon & Oumou Goun, 2022. "Author Correction: Genetic instability from a single S phase after whole-genome duplication," Nature, Nature, vol. 608(7923), pages 27-27, August.
    2. Katy Ong & Carsten Wloka & Satoshi Okada & Tatyana Svitkina & Erfei Bi, 2014. "Architecture and dynamic remodelling of the septin cytoskeleton during the cell cycle," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
    3. Davide Tamborrini & Maria Angeles Juanes & Sandy Ibanes & Giulia Rancati & Simonetta Piatti, 2018. "Recruitment of the mitotic exit network to yeast centrosomes couples septin displacement to actomyosin constriction," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    4. Takeshi Fujiwara & Madhavi Bandi & Masayuki Nitta & Elena V. Ivanova & Roderick T. Bronson & David Pellman, 2005. "Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells," Nature, Nature, vol. 437(7061), pages 1043-1047, October.
    5. Alexandre Beber & Cyntia Taveneau & Manuela Nania & Feng-Ching Tsai & Aurelie Cicco & Patricia Bassereau & Daniel Lévy & João T. Cabral & Hervé Isambert & Stéphanie Mangenot & Aurélie Bertin, 2019. "Membrane reshaping by micrometric curvature sensitive septin filaments," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    6. Alina M. Vrabioiu & Timothy J. Mitchison, 2006. "Structural insights into yeast septin organization from polarized fluorescence microscopy," Nature, Nature, vol. 443(7110), pages 466-469, September.
    7. Simon Gemble & René Wardenaar & Kristina Keuper & Nishit Srivastava & Maddalena Nano & Anne-Sophie Macé & Andréa E. Tijhuis & Sara Vanessa Bernhard & Diana C. J. Spierings & Anthony Simon & Oumou Goun, 2022. "Genetic instability from a single S phase after whole-genome duplication," Nature, Nature, vol. 604(7904), pages 146-151, April.
    8. Laura Picas & Julien Viaud & Kristine Schauer & Stefano Vanni & Karim Hnia & Vincent Fraisier & Aurélien Roux & Patricia Bassereau & Frédérique Gaits-Iacovoni & Bernard Payrastre & Jocelyn Laporte & J, 2014. "BIN1/M-Amphiphysin2 induces clustering of phosphoinositides to recruit its downstream partner dynamin," Nature Communications, Nature, vol. 5(1), pages 1-12, 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. G. Yahya & P. Menges & P. S. Amponsah & D. A. Ngandiri & D. Schulz & A. Wallek & N. Kulak & M. Mann & P. Cramer & V. Savage & M. Räschle & Z. Storchova, 2022. "Sublinear scaling of the cellular proteome with ploidy," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Adam C. Weiner & Marc J. Williams & Hongyu Shi & Ignacio Vázquez-García & Sohrab Salehi & Nicole Rusk & Samuel Aparicio & Sohrab P. Shah & Andrew McPherson, 2024. "Inferring replication timing and proliferation dynamics from single-cell DNA sequencing data," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. Dadong Dai & Chuanshuai Xie & Yayi Zhou & Dexin Bo & Shurong Zhang & Shengqiang Mao & Yucheng Liao & Simeng Cui & Zhaolu Zhu & Xueyu Wang & Fanling Li & Donghai Peng & Jinshui Zheng & Ming Sun, 2023. "Unzipped chromosome-level genomes reveal allopolyploid nematode origin pattern as unreduced gamete hybridization," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Harrison M. York & Kunaal Joshi & Charles S. Wright & Laura Z. Kreplin & Samuel J. Rodgers & Ullhas K. Moorthi & Hetvi Gandhi & Abhishek Patil & Christina A. Mitchell & Srividya Iyer-Biswas & Senthil , 2023. "Deterministic early endosomal maturations emerge from a stochastic trigger-and-convert mechanism," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Chunyang Bao & Richard W. Tourdot & Gregory J. Brunette & Chip Stewart & Lili Sun & Hideo Baba & Masayuki Watanabe & Agoston T. Agoston & Kunal Jajoo & Jon M. Davison & Katie S. Nason & Gad Getz & Ken, 2023. "Genomic signatures of past and present chromosomal instability in Barrett’s esophagus and early esophageal adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    6. Priya Jaitly & Mélanie Legrand & Abhijit Das & Tejas Patel & Murielle Chauvel & Corinne Maufrais & Christophe d’Enfert & Kaustuv Sanyal, 2022. "A phylogenetically-restricted essential cell cycle progression factor in the human pathogen Candida albicans," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    7. Revati Darp & Marc A. Vittoria & Neil J. Ganem & Craig J. Ceol, 2022. "Oncogenic BRAF induces whole-genome doubling through suppression of cytokinesis," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    8. Ellen B. Garcia & Cynthia Alms & Albert W. Hinman & Conor Kelly & Adam Smith & Marina Vance & Jadranka Loncarek & Linsey C. Marr & Daniela Cimini, 2019. "Single-Cell Analysis Reveals that Chronic Silver Nanoparticle Exposure Induces Cell Division Defects in Human Epithelial Cells," IJERPH, MDPI, vol. 16(11), pages 1-22, June.
    9. Lorenza Garribba & Giuseppina De Feudis & Valentino Martis & Martina Galli & Marie Dumont & Yonatan Eliezer & René Wardenaar & Marica Rosaria Ippolito & Divya Ramalingam Iyer & Andréa E. Tijhuis & Dia, 2023. "Short-term molecular consequences of chromosome mis-segregation for genome stability," Nature Communications, Nature, vol. 14(1), pages 1-17, 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:15:y:2024:i:1:d:10.1038_s41467-024-47709-3. 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.