IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29317-1.html
   My bibliography  Save this article

Imaging vesicle formation dynamics supports the flexible model of clathrin-mediated endocytosis

Author

Listed:
  • Tomasz J. Nawara

    (University of Alabama at Birmingham)

  • Yancey D. Williams

    (University of Alabama at Birmingham)

  • Tejeshwar C. Rao

    (University of Alabama at Birmingham)

  • Yuesong Hu

    (Emory University)

  • Elizabeth Sztul

    (University of Alabama at Birmingham)

  • Khalid Salaita

    (Emory University)

  • Alexa L. Mattheyses

    (University of Alabama at Birmingham)

Abstract

Clathrin polymerization and changes in plasma membrane architecture are necessary steps in forming vesicles to internalize cargo during clathrin-mediated endocytosis (CME). Simultaneous analysis of clathrin dynamics and membrane structure is challenging due to the limited axial resolution of fluorescence microscopes and the heterogeneity of CME. This has fueled conflicting models of vesicle assembly and obscured the roles of flat clathrin assemblies. Here, using Simultaneous Two-wavelength Axial Ratiometry (STAR) microscopy, we bridge this critical knowledge gap by quantifying the nanoscale dynamics of clathrin-coat shape change during vesicle assembly. We find that de novo clathrin accumulations generate both flat and curved structures. High-throughput analysis reveals that the initiation of vesicle curvature does not directly correlate with clathrin accumulation. We show clathrin accumulation is preferentially simultaneous with curvature formation at shorter-lived clathrin-coated vesicles (CCVs), but favors a flat-to-curved transition at longer-lived CCVs. The broad spectrum of curvature initiation dynamics revealed by STAR microscopy supports multiple productive mechanisms of vesicle formation and advocates for the flexible model of CME.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29317-1
    DOI: 10.1038/s41467-022-29317-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29317-1
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-29317-1?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. Marcin Łyszkiewicz & Natalia Ziętara & Laura Frey & Ulrich Pannicke & Marcel Stern & Yanshan Liu & Yanxin Fan & Jacek Puchałka & Sebastian Hollizeck & Ido Somekh & Meino Rohlfs & Tuğba Yilmaz & Ekrem , 2020. "Author Correction: Human FCHO1 deficiency reveals role for clathrin-mediated endocytosis in development and function of T cells," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
    2. Gael Genet & Kevin Boyé & Thomas Mathivet & Roxana Ola & Feng Zhang & Alexandre Dubrac & Jinyu Li & Nafiisha Genet & Luiz Henrique Geraldo & Lorena Benedetti & Steffen Künzel & Laurence Pibouin-Fragne, 2019. "Endophilin-A2 dependent VEGFR2 endocytosis promotes sprouting angiogenesis," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    3. 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.
    4. Daniela Leyton-Puig & Tadamoto Isogai & Elisabetta Argenzio & Bram van den Broek & Jeffrey Klarenbeek & Hans Janssen & Kees Jalink & Metello Innocenti, 2017. "Flat clathrin lattices are dynamic actin-controlled hubs for clathrin-mediated endocytosis and signalling of specific receptors," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    5. Marcin Łyszkiewicz & Natalia Ziętara & Laura Frey & Ulrich Pannicke & Marcel Stern & Yanshan Liu & Yanxin Fan & Jacek Puchałka & Sebastian Hollizeck & Ido Somekh & Meino Rohlfs & Tuğba Yilmaz & Ekrem , 2020. "Human FCHO1 deficiency reveals role for clathrin-mediated endocytosis in development and function of T cells," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    6. Delia Bucher & Felix Frey & Kem A. Sochacki & Susann Kummer & Jan-Philip Bergeest & William J. Godinez & Hans-Georg Kräusslich & Karl Rohr & Justin W. Taraska & Ulrich S. Schwarz & Steeve Boulant, 2018. "Clathrin-adaptor ratio and membrane tension regulate the flat-to-curved transition of the clathrin coat during endocytosis," Nature Communications, Nature, vol. 9(1), pages 1-13, 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. 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. 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.
    3. Meiyan Jin & Cyna Shirazinejad & Bowen Wang & Amy Yan & Johannes Schöneberg & Srigokul Upadhyayula & Ke Xu & David G. Drubin, 2022. "Branched actin networks are organized for asymmetric force production during clathrin-mediated endocytosis in mammalian cells," Nature Communications, Nature, vol. 13(1), pages 1-12, 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_s41467-022-29317-1. 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.