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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
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    References listed on IDEAS

    as
    1. 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.
    2. David J. Kast & Roberto Dominguez, 2019. "Mechanism of IRSp53 inhibition by 14-3-3," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
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