Abstract
BackgroundApproximately 10% of Caenorhabditis elegans nervous system synapses are electrical, that is, gap junctions composed of innexins. The locomotory nervous system consists of several pairs of interneurons and three major classes of motor neurons, all with stereotypical patterns of connectivity that include gap junctions. Mutations in the two innexin genes unc-7 and unc-9 result in identical uncoordinated movement phenotypes, and their respective gene products were investigated for their contribution to electrical synapse connectivity.Resultsunc-7 encodes three innexin isoforms. Two of these, UNC-7S and UNC-7SR, are functionally equivalent and play an essential role in coordinated locomotion. UNC-7S and UNC-7SR are widely expressed and co-localize extensively with green fluorescent protein-tagged innexin UNC-9 in the ventral and dorsal nerve cords. A subset of UNC-7S/SR expression visualizes gap junctions formed between the AVB forward command interneurons and their B class motor neuron partners. Experiments indicate that expression of UNC-7S/SR in AVB and expression of UNC-9 in B motor neurons is necessary for these gap junctions to form. In Xenopus oocyte pairs, both UNC-7S and UNC-9 form homomeric gap junctions, and together they form heterotypic channels. Xenopus oocyte studies and co-localization studies in C. elegans suggest that UNC-7S and UNC-9 do not heteromerize in the same hemichannel, leading to the model that hemichannels in AVB:B motor neuron gap junctions are homomeric and heterotypic.ConclusionUNC-7S and UNC-9 are widely expressed and contribute to a large number of the gap junctions identified in the locomotory nervous system. Proper AVB:B gap junction formation requires UNC-7S expression in AVB interneurons and UNC-9 expression in B motor neurons. More broadly, this illustrates that innexin identity is critical for electrical synapse specificity, but differential (compartmentalized) innexin expression cannot account for all of the specificity seen in C. elegans, and other factors must influence the determination of synaptic partners.
Highlights
10% of Caenorhabditis elegans nervous system synapses are electrical, that is, gap junctions composed of innexins
We demonstrate that the formation of specific gap junctions between AVB and B motor neurons depends on interactions between unc-7 and unc-9 gene products, and that the expression of unc-7 and unc-9 influences formation of a large proportion of the gap junctions in the locomotory nervous system
Innexins UNC-7 and UNC-9 contribute to a large number of electrical synapses in the C. elegans locomotory nervous system
Summary
10% of Caenorhabditis elegans nervous system synapses are electrical, that is, gap junctions composed of innexins. Mutations in the two innexin genes unc-7 and unc-9 result in identical uncoordinated movement phenotypes, and their respective gene products were investigated for their contribution to electrical synapse connectivity. Until recently it was thought that all vertebrate gap junction subunits are connexins, and invertebrate gap junction proteins are innexins [1,2]. Members of a third protein family, the pannexins, were recently shown to form gap junction channels [4]. Individual connexin, innexin and pannexin proteins have all been shown to form gap junction channels with similar properties as assayed in paired Xenopus oocytes (for example, [4,7,8])
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