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Ultrafast endocytosis at mouse hippocampal synapses

Author

Listed:
  • Shigeki Watanabe

    (University of Utah)

  • Benjamin R. Rost

    (Neuroscience Research Centre, Charité Universitätsmedizin, 10117 Berlin, Germany
    Present address: German Center for Neurodegenerative Diseases (DZNE), 10117 Berlin, Germany.)

  • Marcial Camacho-Pérez

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

  • M. Wayne Davis

    (University of Utah)

  • Berit Söhl-Kielczynski

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

  • Christian Rosenmund

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

  • Erik M. Jorgensen

    (University of Utah)

Abstract

To sustain neurotransmission, synaptic vesicles and their associated proteins must be recycled locally at synapses. Synaptic vesicles are thought to be regenerated approximately 20 s after fusion by the assembly of clathrin scaffolds or in approximately 1 s by the reversal of fusion pores via ‘kiss-and-run’ endocytosis. Here we use optogenetics to stimulate cultured hippocampal neurons with a single stimulus, rapidly freeze them after fixed intervals and examine the ultrastructure using electron microscopy—‘flash-and-freeze’ electron microscopy. Docked vesicles fuse and collapse into the membrane within 30 ms of the stimulus. Compensatory endocytosis occurs within 50 to 100 ms at sites flanking the active zone. Invagination is blocked by inhibition of actin polymerization, and scission is blocked by inhibiting dynamin. Because intact synaptic vesicles are not recovered, this form of recycling is not compatible with kiss-and-run endocytosis; moreover, it is 200-fold faster than clathrin-mediated endocytosis. It is likely that ‘ultrafast endocytosis’ is specialized to restore the surface area of the membrane rapidly.

Suggested Citation

  • Shigeki Watanabe & Benjamin R. Rost & Marcial Camacho-Pérez & M. Wayne Davis & Berit Söhl-Kielczynski & Christian Rosenmund & Erik M. Jorgensen, 2013. "Ultrafast endocytosis at mouse hippocampal synapses," Nature, Nature, vol. 504(7479), pages 242-247, December.
    • Handle: RePEc:nat:nature:v:504:y:2013:i:7479:d:10.1038_nature12809
    DOI: 10.1038/nature12809
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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. Ling-Gang Wu & Chung Yu Chan, 2024. "Membrane transformations of fusion and budding," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. Dennis Vettkötter & Martin Schneider & Brady D. Goulden & Holger Dill & Jana Liewald & Sandra Zeiler & Julia Guldan & Yilmaz Arda Ateş & Shigeki Watanabe & Alexander Gottschalk, 2022. "Rapid and reversible optogenetic silencing of synaptic transmission by clustering of synaptic vesicles," Nature Communications, Nature, vol. 13(1), pages 1-17, 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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