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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
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    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
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    5. 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.
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