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The Journal of Neuroscience, March 10, 2004, 24(10):2496-2505; doi:10.1523/JNEUROSCI.5372-03.2004

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Cellular/Molecular
Synaptic Vesicles: Test for a Role in Presynaptic Calcium Regulation

Greg T. Macleod, Leo Marin, Milton P. Charlton, and Harold L. Atwood

Department of Physiology, University of Toronto, Toronto, Ontario, M5S 1A8, Canada

Membrane-bound organelles such as mitochondria and the endoplasmic reticulum play an important role in neuronal Ca²⁺ homeostasis. Synaptic vesicles (SVs), the organelles responsible for exocytosis of neurotransmitters, occupy more of the volume of presynaptic nerve terminals than any other organelle and, under some conditions, can accumulate Ca²⁺. They are also closely associated with voltage-gated Ca²⁺ channels (VGCCs) that trigger transmitter release by admitting Ca²⁺ into the nerve terminal in response to action potentials (APs). We tested the hypothesis that SVs can modulate Ca²⁺ signals in the presynaptic terminal. This has been a difficult question to address because neither pharmacological nor genetic approaches to block Ca²⁺ permeation of the SV membrane have been available. To investigate the possible role of SVs in Ca²⁺ regulation, we used imaging techniques to compare Ca²⁺ dynamics in motor nerve terminals before and after depletion of SVs. We used the temperature-sensitive Drosophila dynamin mutant shibire, in which SVs can be eliminated by stimulation. There was no difference in the amplitude or time course of Ca²⁺ responses during high-frequency trains of APs, or single APs, in individual presynaptic boutons before and after depletion of SVs. SVs have a limited role, if any, in the rapid sequestration of Ca²⁺ within the neuronal cytosol or the synaptic microdomain. We also conclude that SVs are not important for regulation of synaptic VGCCs.

Key words: calcium regulation; calcium channels; synaptic vesicles; Drosophila; temperature-sensitive mutant; shibire

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Received Dec 5, 2003; revised January 20, 2004; accepted January 20, 2004.

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