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VGLUT1 functions as a glutamate/proton exchanger with chloride channel activity in hippocampal glutamatergic synapses

Author

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  • Magalie Martineau

    (University of Muenster
    University of Bordeaux and Centre National de la Recherche Scientifique, Interdisciplinary Institute for Neuroscience, UMR 5297)

  • Raul E. Guzman

    (Forschungszentrum Jülich)

  • Christoph Fahlke

    (Forschungszentrum Jülich)

  • Jürgen Klingauf

    (University of Muenster
    Cells in Motion (CiM))

Abstract

Glutamate is the major excitatory transmitter in the vertebrate nervous system. To maintain synaptic efficacy, recycling synaptic vesicles (SV) are refilled with glutamate by vesicular glutamate transporters (VGLUTs). The dynamics and mechanism of glutamate uptake in intact neurons are still largely unknown. Here, we show by live-cell imaging with pH- and chloride-sensitive fluorescent probes in cultured hippocampal neurons of wild-type and VGLUT1-deficient mice that in SVs VGLUT functions as a glutamate/proton exchanger associated with a channel-like chloride conductance. After endocytosis most internalized Cl− is substituted by glutamate in an electrically, and presumably osmotically, neutral manner, and this process is driven by both the Cl− gradient itself and the proton motive force provided by the vacuolar H+-ATPase. Our results shed light on the transport mechanism of VGLUT under physiological conditions and provide a framework for how modulation of glutamate transport via Cl− and pH can change synaptic strength.

Suggested Citation

  • Magalie Martineau & Raul E. Guzman & Christoph Fahlke & Jürgen Klingauf, 2017. "VGLUT1 functions as a glutamate/proton exchanger with chloride channel activity in hippocampal glutamatergic synapses," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_s41467-017-02367-6
    DOI: 10.1038/s41467-017-02367-6
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    Cited by:

    1. Jung-Hwan Choi & Lauren Bayer Horowitz & Niels Ringstad, 2021. "Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Bettina Kolen & Bart Borghans & Daniel Kortzak & Victor Lugo & Cora Hannack & Raul E. Guzman & Ghanim Ullah & Christoph Fahlke, 2023. "Vesicular glutamate transporters are H+-anion exchangers that operate at variable stoichiometry," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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