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Clathrin regenerates synaptic vesicles from endosomes

Author

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  • Shigeki Watanabe

    (University of Utah)

  • Thorsten Trimbuch

    (Neuroscience Research Center Charité Universitätsmedizin Berlin, Berlin 10117, Germany)

  • Marcial Camacho-Pérez

    (Neuroscience Research Center Charité Universitätsmedizin Berlin, Berlin 10117, Germany)

  • Benjamin R. Rost

    (Neuroscience Research Center Charité Universitätsmedizin Berlin, Berlin 10117, Germany
    German Center for Neurodegenerative Diseases (DZNE), 10117 Berlin, Germany)

  • Bettina Brokowski

    (Neuroscience Research Center Charité Universitätsmedizin Berlin, Berlin 10117, Germany)

  • Berit Söhl-Kielczynski

    (Neuroscience Research Center Charité Universitätsmedizin Berlin, Berlin 10117, Germany)

  • Annegret Felies

    (Neuroscience Research Center Charité Universitätsmedizin Berlin, Berlin 10117, Germany)

  • M. Wayne Davis

    (University of Utah)

  • Christian Rosenmund

    (Neuroscience Research Center Charité Universitätsmedizin Berlin, Berlin 10117, Germany)

  • Erik M. Jorgensen

    (University of Utah)

Abstract

Ultrafast endocytosis can retrieve a single, large endocytic vesicle as fast as 50–100 ms after synaptic vesicle fusion. However, the fate of the large endocytic vesicles is not known. Here we demonstrate that these vesicles transition to a synaptic endosome about one second after stimulation. The endosome is resolved into coated vesicles after 3 s, which in turn become small-diameter synaptic vesicles 5–6 s after stimulation. We disrupted clathrin function using RNA interference (RNAi) and found that clathrin is not required for ultrafast endocytosis but is required to generate synaptic vesicles from the endosome. Ultrafast endocytosis fails when actin polymerization is disrupted, or when neurons are stimulated at room temperature instead of physiological temperature. In the absence of ultrafast endocytosis, synaptic vesicles are retrieved directly from the plasma membrane by clathrin-mediated endocytosis. These results may explain discrepancies among published experiments concerning the role of clathrin in synaptic vesicle endocytosis.

Suggested Citation

  • Shigeki Watanabe & Thorsten Trimbuch & Marcial Camacho-Pérez & Benjamin R. Rost & Bettina Brokowski & Berit Söhl-Kielczynski & Annegret Felies & M. Wayne Davis & Christian Rosenmund & Erik M. Jorgense, 2014. "Clathrin regenerates synaptic vesicles from endosomes," Nature, Nature, vol. 515(7526), pages 228-233, November.
    • Handle: RePEc:nat:nature:v:515:y:2014:i:7526:d:10.1038_nature13846
    DOI: 10.1038/nature13846
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    Cited by:

    1. Wonchul Shin & Ben Zucker & Nidhi Kundu & Sung Hoon Lee & Bo Shi & Chung Yu Chan & Xiaoli Guo & Jonathan T. Harrison & Jaymie Moore Turechek & Jenny E. Hinshaw & Michael M. Kozlov & Ling-Gang Wu, 2022. "Molecular mechanics underlying flat-to-round membrane budding in live secretory cells," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Katherine Bonnycastle & Katharine L. Dobson & Eva-Maria Blumrich & Akshada Gajbhiye & Elizabeth C. Davenport & Marie Pronot & Moritz Steinruecke & Matthias Trost & Alfredo Gonzalez-Sulser & Michael A., 2023. "Reversal of cell, circuit and seizure phenotypes in a mouse model of DNM1 epileptic encephalopathy," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    3. Ling-Gang Wu & Chung Yu Chan, 2024. "Membrane transformations of fusion and budding," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    4. Tyler H. Ogunmowo & Haoyuan Jing & Sumana Raychaudhuri & Grant F. Kusick & Yuuta Imoto & Shuo Li & Kie Itoh & Ye Ma & Haani Jafri & Matthew B. Dalva & Edwin R. Chapman & Taekjip Ha & Shigeki Watanabe , 2023. "Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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