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The Journal of Neuroscience, April 1, 1999, 19(7):2432-2441

Selective Effects of neuronal-synaptobrevin Mutations on Transmitter Release Evoked by Sustained Versus Transient Ca²⁺ Increases and by cAMP

Motojiro Yoshihara¹, Atsushi Ueda¹, Dawei Zhang¹, David L. Deitcher², Thomas L. Schwarz³, and Yoshiaki Kidokoro¹

¹ Gunma University School of Medicine, Maebashi 371-8511, Japan, ² Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853, and ³ Department of Molecular and Cellular Physiology, Stanford University Medical Center, Stanford, California 94305-5426

Synaptobrevin is a key constituent of the synaptic vesicle membrane. The neuronal-synaptobrevin (n-syb) gene in Drosophila is essential for nerve-evoked synaptic currents, but miniature excitatory synaptic currents (mESCs) remain even in the complete absence of this gene. To further characterize the defect in these mutants, we have examined conditions that stimulate secretion. Despite the inability of an action potential to trigger fusion, high K⁺ saline could increase the frequency of mESCs 4- to 17-fold in a Ca²⁺-dependent manner, and the rate of fusion approached 25% of that seen in wild-type synapses under the same conditions. Similarly, the mESC frequency in n-syb null mutants could be increased by a Ca²⁺ ionophore, A23187, and by black widow spider venom. Thus, the ability of the vesicles to fuse in response to sustained increases in cytosolic Ca²⁺ persisted in the absence of this protein. Tetanic stimulation could also increase the frequency of mESCs, particularly toward the end of a train and after the train of stimuli. In contrast, these mutants did not respond to an elevation of cAMP induced by an activator of adenylyl cyclase, forskolin, or a membrane-permeable analog of cAMP, dibutyryl cAMP, which in wild-type synapses causes a marked increase in the mESC frequency even in the absence of external Ca²⁺. These results are discussed in the context of models that invoke a special role for n-syb in coupling fusion to the transient, local changes in Ca²⁺ and an as yet unidentified target of cAMP.

Key words: neuronal-synaptobrevin; miniature synaptic current; high potassium stimulation; tetanic stimulation; cAMP; forskolin; neuromuscular junction; Drosophila

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Copyright © 1999 Society for Neuroscience  0270-6474/99/1972432-10$05.00/0

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