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The Journal of Neuroscience, July 18, 2007, 27(29):7799-7806; doi:10.1523/JNEUROSCI.1879-07.2007

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Cellular/Molecular
Presynaptic Ryanodine Receptor-Activated Calmodulin Kinase II Increases Vesicle Mobility and Potentiates Neuropeptide Release

Dinara Shakiryanova,¹ Markus K. Klose,² Yi Zhou,¹ Tingting Gu,³ David L. Deitcher,⁴ Harold L. Atwood,² Randall S. Hewes,³ and Edwin S. Levitan¹

¹Department of Pharmacology, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, ²Department of Physiology, University of Toronto, Toronto, Ontario, Canada M5S 1A8, ³Departments of Zoology and Cell Biology, University of Oklahoma, Norman, Oklahoma 73019, and ⁴Department of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853

Correspondence should be addressed to Dr. Edwin S. Levitan at the above address. Email: levitan{at}server.pharm.pitt.edu

Although it has been postulated that vesicle mobility is increased to enhance release of transmitters and neuropeptides, the mechanism responsible for increasing vesicle motion in nerve terminals and the effect of perturbing this mobilization on synaptic plasticity are unknown. Here, green fluorescent protein-tagged dense-core vesicles (DCVs) are imaged in Drosophila motor neuron terminals, where DCV mobility is increased for minutes after seconds of activity. Ca²⁺-induced Ca²⁺ release from presynaptic endoplasmic reticulum (ER) is shown to be necessary and sufficient for sustained DCV mobilization. However, this ryanodine receptor (RyR)-mediated effect is short-lived and only initiates signaling. Calmodulin kinase II (CaMKII), which is not activated directly by external Ca²⁺ influx, then acts as a downstream effector of released ER Ca²⁺. RyR and CaMKII are essential for post-tetanic potentiation of neuropeptide secretion. Therefore, the presynaptic signaling pathway for increasing DCV mobility is identified and shown to be required for synaptic plasticity.

Key words: vesicle mobility; mobilization; dense-core vesicle; neuropeptide release; synaptic plasticity; Drosophila

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Received April 25, 2007; revised June 13, 2007; accepted June 13, 2007.

Correspondence should be addressed to Dr. Edwin S. Levitan at the above address. Email: levitan{at}server.pharm.pitt.edu

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