IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v11y2020i1d10.1038_s41467-020-17091-x.html
   My bibliography  Save this article

IRSp53 controls plasma membrane shape and polarized transport at the nascent lumen in epithelial tubules

Author

Listed:
  • Sara Bisi

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Stefano Marchesi

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Abrar Rizvi

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Davide Carra

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Galina V. Beznoussenko

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Ines Ferrara

    (University of Palermo School of Medicine)

  • Gianluca Deflorian

    (Cogentech, S.R.L.)

  • Alexander Mironov

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Giovanni Bertalot

    (European Institute of Oncology (IEO) IRCCS)

  • Federica Pisati

    (Cogentech, S.R.L.)

  • Amanda Oldani

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Angela Cattaneo

    (Cogentech, S.R.L.)

  • Ghazaleh Saberamoli

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Salvatore Pece

    (European Institute of Oncology (IEO) IRCCS
    Department of Oncology and Haemato-Oncology, University of Milan)

  • Giuseppe Viale

    (European Institute of Oncology (IEO) IRCCS)

  • Angela Bachi

    (IFOM, the FIRC Institute of Molecular Oncology)

  • Claudio Tripodo

    (IFOM, the FIRC Institute of Molecular Oncology
    University of Palermo School of Medicine)

  • Giorgio Scita

    (IFOM, the FIRC Institute of Molecular Oncology
    Department of Oncology and Haemato-Oncology, University of Milan)

  • Andrea Disanza

    (IFOM, the FIRC Institute of Molecular Oncology)

Abstract

It is unclear whether the establishment of apical–basal cell polarity during the generation of epithelial lumens requires molecules acting at the plasma membrane/actin interface. Here, we show that the I-BAR-containing IRSp53 protein controls lumen formation and the positioning of the polarity determinants aPKC and podocalyxin. Molecularly, IRSp53 acts by regulating the localization and activity of the small GTPase RAB35, and by interacting with the actin capping protein EPS8. Using correlative light and electron microscopy, we further show that IRSp53 ensures the shape and continuity of the opposing plasma membrane of two daughter cells, leading to the formation of a single apical lumen. Genetic removal of IRSp53 results in abnormal renal tubulogenesis, with altered tubular polarity and architectural organization. Thus, IRSp53 acts as a membrane curvature-sensing platform for the assembly of multi-protein complexes that control the trafficking of apical determinants and the integrity of the luminal plasma membrane.

Suggested Citation

  • Sara Bisi & Stefano Marchesi & Abrar Rizvi & Davide Carra & Galina V. Beznoussenko & Ines Ferrara & Gianluca Deflorian & Alexander Mironov & Giovanni Bertalot & Federica Pisati & Amanda Oldani & Angel, 2020. "IRSp53 controls plasma membrane shape and polarized transport at the nascent lumen in epithelial tubules," Nature Communications, Nature, vol. 11(1), pages 1-23, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-17091-x
    DOI: 10.1038/s41467-020-17091-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-020-17091-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-020-17091-x?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. David J. Kast & Roberto Dominguez, 2019. "Mechanism of IRSp53 inhibition by 14-3-3," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    2. Kerstin Klinkert & Murielle Rocancourt & Anne Houdusse & Arnaud Echard, 2016. "Rab35 GTPase couples cell division with initiation of epithelial apico-basal polarity and lumen opening," Nature Communications, Nature, vol. 7(1), pages 1-13, September.
    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. Michael J. Roy & Minglyanna G. Surudoi & Ashleigh Kropp & Jianmei Hou & Weiwen Dai & Joshua M. Hardy & Lung-Yu Liang & Thomas R. Cotton & Bernhard C. Lechtenberg & Toby A. Dite & Xiuquan Ma & Roger J., 2023. "Structural mapping of PEAK pseudokinase interactions identifies 14-3-3 as a molecular switch for PEAK3 signaling," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Caitlin R. Francis & Hayle Kincross & Erich J. Kushner, 2022. "Rab35 governs apicobasal polarity through regulation of actin dynamics during sprouting angiogenesis," Nature Communications, Nature, vol. 13(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:11:y:2020:i:1:d:10.1038_s41467-020-17091-x. 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.