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Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit

Author

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  • Jung-Hwan Choi

    (Skirball Institute of Biomolecular Medicine, Neuroscience Institute, NYU School of Medicine)

  • Lauren Bayer Horowitz

    (Skirball Institute of Biomolecular Medicine, Neuroscience Institute, NYU School of Medicine)

  • Niels Ringstad

    (Skirball Institute of Biomolecular Medicine, Neuroscience Institute, NYU School of Medicine)

Abstract

At chemical synapses, neurotransmitters are packaged into synaptic vesicles that release their contents in response to depolarization. Despite its central role in synaptic function, regulation of the machinery that loads vesicles with neurotransmitters remains poorly understood. We find that synaptic glutamate signaling in a C. elegans chemosensory circuit is regulated by antagonistic interactions between the canonical vesicular glutamate transporter EAT-4/VGLUT and another vesicular transporter, VST-1. Loss of VST-1 strongly potentiates glutamate release from chemosensory BAG neurons and disrupts chemotaxis behavior. Analysis of the circuitry downstream of BAG neurons shows that excess glutamate release disrupts behavior by inappropriately recruiting RIA interneurons to the BAG-associated chemotaxis circuit. Our data indicate that in vivo the strength of glutamatergic synapses is controlled by regulation of neurotransmitter packaging into synaptic vesicles via functional coupling of VGLUT and VST-1.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26575-3
    DOI: 10.1038/s41467-021-26575-3
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    References listed on IDEAS

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    1. Gero Miesenböck & Dino A. De Angelis & James E. Rothman, 1998. "Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins," Nature, Nature, vol. 394(6689), pages 192-195, July.
    2. 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.
    3. Menachem Katz & Francis Corson & Wolfgang Keil & Anupriya Singhal & Andrea Bae & Yun Lu & Yupu Liang & Shai Shaham, 2019. "Glutamate spillover in C. elegans triggers repetitive behavior through presynaptic activation of MGL-2/mGluR5," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    4. Steven L. McIntire & Richard J. Reimer & Kim Schuske & Robert H. Edwards & Erik M. Jorgensen, 1997. "Identification and characterization of the vesicular GABA transporter," Nature, Nature, vol. 389(6653), pages 870-876, October.
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