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The Journal of Neuroscience, July 2, 2003, 23(13):5897-5905

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Presynaptic Impairment of Synaptic Transmission in Drosophila Embryos Lacking Gs

Dongmei Hou,¹ Kazuhiro Suzuki,¹ William J. Wolfgang,² Catherine Clay,² Michael Forte,² and Yoshiaki Kidokoro¹

¹Gunma University School of Medicine, Maebashi 371-8511, Japan, and ²Vollum Institute, Oregon Health & Science University, Portland, Oregon 97201

Gs is a subunit of the heterotrimeric G-protein complex, expressed ubiquitously in all types of cells, including neurons. Drosophila larvae, which have mutations in the Gs gene, are lethargic, suggesting an impairment of neuronal functions. In this study, we examined synaptic transmission at the neuromuscular synapse in Gs-null (dgs^R60) embryos shortly before they hatched. At low-frequency nerve stimulation, synaptic transmission in mutant embryos was not very different from that in controls. In contrast, facilitation during tetanic stimulation was minimal in dgs^R60, and no post-tetanic potentiation was observed. Miniature synaptic currents (mSCs) were slightly smaller in amplitude and less frequent in dgs^R60 embryos in normal-K⁺ saline. In high-K⁺ saline, mSCs with distinctly large amplitude occurred frequently in controls at late embryonic stages, whereas those mSCs were rarely observed in dgs^R60 embryos, suggesting a developmental defect in the mutant. Using the Gal4-UAS expression system, we found that these phenotypes in dgs^R60 were caused predominantly by lack of Gs in presynaptic neurons and not in postsynaptic muscles. To test whether Gs couples presynaptic modulator receptors to adenylyl cyclase (AC), we examined the responses of two known G-protein-coupled receptors in dgs^R60 embryos. Both metabotropic glutamate and octopamine receptor responses were indistinguishable from those of controls, indicating that these receptors are not linked to AC by Gs. We therefore suggest that synaptic transmission is compromised in dgs^R60 embryos because of presynaptic defects in two distinct processes; one is uncoupling between the yet-to-be-known modulator receptor and AC activation, and the other is a defect in synapse formation.

Key words: Gs; Drosophila; synaptic transmission; metabotropic glutamate receptor; octopamine receptor; neuromuscular junction.

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Received Jan. 8, 2003; revised Mar. 7, 2003; accepted Apr. 9, 2003.

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