Reconstitution of invertebrate glutamate receptor function depends on stargazin-like proteins

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Abstract
α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors (AMPARs) are a major subtype of ionotropic glutamate receptors (iGluRs) that mediate rapid excitatory synaptic transmission in the vertebrate brain. Putative AMPARs are also expressed in the nervous system of invertebrates. InCaenorhabditis elegans, the GLR-1 receptor subunit is expressed in neural circuits that mediate avoidance behaviors and is required for glutamate-gated current in the AVA and AVD interneurons. Glutamate-gated currents can be recorded from heterologous cells that express vertebrate AMPARs; however, whenC. elegansGLR-1 is expressed in heterologous cells, little or no glutamate-gated current is detected. This finding suggests that other receptor subunits or auxiliary proteins are required for function. Here, we identifyCeSTG-1, aC. elegansstargazin-like protein, and show that expression ofCeSTG-1 together with GLR-1 and the CUB-domain protein SOL-1 reconstitutes glutamate-gated currents inXenopusoocytes.CeSTG-1 and homologues cloned fromDrosophila(DroSTG1) andApis mellifera(ApisSTG1) have evolutionarily conserved functions and can partially substitute for one another to reconstitute glutamate-gated currents from rat,Drosophila, andC. elegans. Furthermore, we show thatCeSTG-1 andApisSTG1 are primarily required for function independent of possible roles in promoting the surface expression of invertebrate AMPARs.