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Synaptic vesicle traffic is supported by transient actin filaments and regulated by PKA and NO

Author

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  • Nicolas Chenouard

    (NYU Neuroscience Institute and Department of Neuroscience and Physiology, NYU Langone Medical Center
    Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297)

  • Feng Xuan

    (NYU Neuroscience Institute and Department of Neuroscience and Physiology, NYU Langone Medical Center
    Northwestern University)

  • Richard W. Tsien

    (NYU Neuroscience Institute and Department of Neuroscience and Physiology, NYU Langone Medical Center
    New York University)

Abstract

Synaptic vesicles (SVs) can be pooled across multiple synapses, prompting questions about their dynamic allocation for neurotransmission and plasticity. We find that the axonal traffic of recycling vesicles is not supported by ubiquitous microtubule-based motility but relies on actin instead. Vesicles freed from synaptic clusters undergo ~1 µm bouts of active transport, initiated by nearby elongation of actin filaments. Long distance translocation arises when successive bouts of active transport were linked by periods of free diffusion. The availability of SVs for active transport can be promptly increased by protein kinase A, a key player in neuromodulation. Vesicle motion is in turn impeded by shutting off axonal actin polymerization, mediated by nitric oxide-cyclic GMP signaling leading to inhibition of RhoA. These findings provide a potential framework for coordinating post-and pre-synaptic strength, using retrograde regulation of axonal actin dynamics to mobilize and recruit presynaptic SV resources.

Suggested Citation

  • Nicolas Chenouard & Feng Xuan & Richard W. Tsien, 2020. "Synaptic vesicle traffic is supported by transient actin filaments and regulated by PKA and NO," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-19120-1
    DOI: 10.1038/s41467-020-19120-1
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