IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33852-2.html
   My bibliography  Save this article

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

Author

Listed:
  • 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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33852-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-33852-2?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. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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.

    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. Kazuki Obashi & Kem A. Sochacki & Marie-Paule Strub & Justin W. Taraska, 2023. "A conformational switch in clathrin light chain regulates lattice structure and endocytosis at the plasma membrane of mammalian cells," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Tomasz J. Nawara & Yancey D. Williams & Tejeshwar C. Rao & Yuesong Hu & Elizabeth Sztul & Khalid Salaita & Alexa L. Mattheyses, 2022. "Imaging vesicle formation dynamics supports the flexible model of clathrin-mediated endocytosis," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Fabian Lukas & Claudia Matthaeus & Tania López-Hernández & Ines Lahmann & Nicole Schultz & Martin Lehmann & Dmytro Puchkov & Jan Pielage & Volker Haucke & Tanja Maritzen, 2024. "Canonical and non-canonical integrin-based adhesions dynamically interconvert," Nature Communications, Nature, vol. 15(1), pages 1-15, 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_s41467-022-33852-2. 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.