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Actin polymerization promotes invagination of flat clathrin-coated lattices in mammalian cells by pushing at lattice edges

Author

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  • Changsong Yang

    (University of Pennsylvania)

  • Patricia Colosi

    (University of Pennsylvania)

  • Siewert Hugelier

    (University of Pennsylvania)

  • Daniel Zabezhinsky

    (University of Pennsylvania)

  • Melike Lakadamyali

    (University of Pennsylvania)

  • Tatyana Svitkina

    (University of Pennsylvania)

Abstract

Clathrin-mediated endocytosis (CME) requires energy input from actin polymerization in mechanically challenging conditions. The roles of actin in CME are poorly understood due to inadequate knowledge of actin organization at clathrin-coated structures (CCSs). Using platinum replica electron microscopy of mammalian cells, we show that Arp2/3 complex-dependent branched actin networks, which often emerge from microtubule tips, assemble along the CCS perimeter, lack interaction with the apical clathrin lattice, and have barbed ends oriented toward the CCS. This structure is hardly compatible with the widely held “apical pulling” model describing actin functions in CME. Arp2/3 complex inhibition or epsin knockout produce large flat non-dynamic CCSs, which split into invaginating subdomains upon recovery from Arp2/3 inhibition. Moreover, epsin localization to CCSs depends on Arp2/3 activity. We propose an “edge pushing” model for CME, wherein branched actin polymerization promotes severing and invagination of flat CCSs in an epsin-dependent manner by pushing at the CCS boundary, thus releasing forces opposing the intrinsic curvature of clathrin lattices.

Suggested Citation

  • Changsong Yang & Patricia Colosi & Siewert Hugelier & Daniel Zabezhinsky & Melike Lakadamyali & Tatyana Svitkina, 2022. "Actin polymerization promotes invagination of flat clathrin-coated lattices in mammalian cells by pushing at lattice edges," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33852-2
    DOI: 10.1038/s41467-022-33852-2
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    References listed on IDEAS

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    1. Francesco Baschieri & Stéphane Dayot & Nadia Elkhatib & Nathalie Ly & Anahi Capmany & Kristine Schauer & Timo Betz & Danijela Matic Vignjevic & Renaud Poincloux & Guillaume Montagnac, 2018. "Frustrated endocytosis controls contractility-independent mechanotransduction at clathrin-coated structures," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    2. Brandon L. Scott & Kem A. Sochacki & Shalini T. Low-Nam & Elizabeth M. Bailey & QuocAhn Luu & Amy Hor & Andrea M. Dickey & Steve Smith & Jason G. Kerkvliet & Justin W. Taraska & Adam D. Hoppe, 2018. "Membrane bending occurs at all stages of clathrin-coat assembly and defines endocytic dynamics," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    3. Nicholas I. Clarke & Stephen J. Royle, 2018. "FerriTag is a new genetically-encoded inducible tag for correlative light-electron microscopy," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
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    Cited by:

    1. Yiming Yu & Shige H. Yoshimura, 2023. "Self-assembly of CIP4 drives actin-mediated asymmetric pit-closing in clathrin-mediated endocytosis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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