Synaptic Vesicles: Test for a Role in Presynaptic Calcium Regulation

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Abstract
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-sensitiveDrosophiladynamin mutantshibire, 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.