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A dual-Ca2+-sensor model for neurotransmitter release in a central synapse

Author

Listed:
  • Jianyuan Sun

    (Departments of Neuroscience and,
    Molecular Genetics, and,)

  • Zhiping P. Pang

    (Departments of Neuroscience and,)

  • Dengkui Qin

    (Departments of Neuroscience and,)

  • Abigail T. Fahim

    (The University of Texas M.D. Anderson Cancer Center, Houston, Texas 77030, USA)

  • Roberto Adachi

    (The University of Texas M.D. Anderson Cancer Center, Houston, Texas 77030, USA)

  • Thomas C. Südhof

    (Departments of Neuroscience and,
    Molecular Genetics, and,
    Howard Hughes Medical Institute, The University of Texas Southwestern Medical Center, Dallas, Texas 75390, USA)

Abstract

Ca2+-triggered synchronous neurotransmitter release is well described, but asynchronous release—in fact, its very existence—remains enigmatic. Here we report a quantitative description of asynchronous neurotransmitter release in calyx-of-Held synapses. We show that deletion of synaptotagmin 2 (Syt2) in mice selectively abolishes synchronous release, allowing us to study pure asynchronous release in isolation. Using photolysis experiments of caged Ca2+, we demonstrate that asynchronous release displays a Ca2+ cooperativity of ∼2 with a Ca2+ affinity of ∼44 μM, in contrast to synchronous release, which exhibits a Ca2+ cooperativity of ∼5 with a Ca2+ affinity of ∼38 μM. Our results reveal that release triggered in wild-type synapses at low Ca2+ concentrations is physiologically asynchronous, and that asynchronous release completely empties the readily releasable pool of vesicles during sustained elevations of Ca2+. We propose a dual-Ca2+-sensor model of release that quantitatively describes the contributions of synchronous and asynchronous release under conditions of different presynaptic Ca2+ dynamics.

Suggested Citation

  • Jianyuan Sun & Zhiping P. Pang & Dengkui Qin & Abigail T. Fahim & Roberto Adachi & Thomas C. Südhof, 2007. "A dual-Ca2+-sensor model for neurotransmitter release in a central synapse," Nature, Nature, vol. 450(7170), pages 676-682, November.
    • Handle: RePEc:nat:nature:v:450:y:2007:i:7170:d:10.1038_nature06308
    DOI: 10.1038/nature06308
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    Cited by:

    1. Alexander M Walter & Paulo S Pinheiro & Matthijs Verhage & Jakob B Sørensen, 2013. "A Sequential Vesicle Pool Model with a Single Release Sensor and a Ca2+-Dependent Priming Catalyst Effectively Explains Ca2+-Dependent Properties of Neurosecretion," PLOS Computational Biology, Public Library of Science, vol. 9(12), pages 1-15, December.

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