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α-Neurexins couple Ca2+ channels to synaptic vesicle exocytosis

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  • Markus Missler

    (Center for Basic Neuroscience, Department of Molecular Genetics
    The University of Texas Southwestern Medical Center
    Zentrum Physiologie und Pathophysiologie, Georg-August Universität)

  • Weiqi Zhang

    (Zentrum Physiologie und Pathophysiologie, Georg-August Universität)

  • Astrid Rohlmann

    (Zentrum Physiologie und Pathophysiologie, Georg-August Universität)

  • Gunnar Kattenstroth

    (Lehrstuhl für Zellphysiologie, Ruhr-Universität Bochum)

  • Robert E. Hammer

    (Center for Basic Neuroscience, Department of Biochemistry
    The University of Texas Southwestern Medical Center)

  • Kurt Gottmann

    (Lehrstuhl für Zellphysiologie, Ruhr-Universität Bochum)

  • Thomas C. Südhof

    (Center for Basic Neuroscience, Department of Molecular Genetics
    The University of Texas Southwestern Medical Center)

Abstract

Synapses are specialized intercellular junctions in which cell adhesion molecules connect the presynaptic machinery for neurotransmitter release to the postsynaptic machinery for receptor signalling. Neurotransmitter release requires the presynaptic co-assembly of Ca2+ channels with the secretory apparatus, but little is known about how synaptic components are organized. α-Neurexins, a family of >1,000 presynaptic cell-surface proteins encoded by three genes, link the pre- and postsynaptic compartments of synapses by binding extracellularly to postsynaptic cell adhesion molecules and intracellularly to presynaptic PDZ domain proteins. Using triple-knockout mice, we show that α-neurexins are not required for synapse formation, but are essential for Ca2+-triggered neurotransmitter release. Neurotransmitter release is impaired because synaptic Ca2+ channel function is markedly reduced, although the number of cell-surface Ca2+ channels appears normal. These data suggest that α-neurexins organize presynaptic terminals by functionally coupling Ca2+ channels to the presynaptic machinery.

Suggested Citation

  • Markus Missler & Weiqi Zhang & Astrid Rohlmann & Gunnar Kattenstroth & Robert E. Hammer & Kurt Gottmann & Thomas C. Südhof, 2003. "α-Neurexins couple Ca2+ channels to synaptic vesicle exocytosis," Nature, Nature, vol. 423(6943), pages 939-948, June.
    • Handle: RePEc:nat:nature:v:423:y:2003:i:6943:d:10.1038_nature01755
    DOI: 10.1038/nature01755
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    Cited by:

    1. Justin H. Trotter & Cosmos Yuqi Wang & Peng Zhou & George Nakahara & Thomas C. Südhof, 2023. "A combinatorial code of neurexin-3 alternative splicing controls inhibitory synapses via a trans-synaptic dystroglycan signaling loop," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    2. Alessandra Sclip & Thomas C. Südhof, 2023. "Combinatorial expression of neurexins and LAR-type phosphotyrosine phosphatase receptors instructs assembly of a cerebellar circuit," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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