Research Article

Glutamate signaling at cytoneme synapses

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Science  01 Mar 2019:
Vol. 363, Issue 6430, pp. 948-955
DOI: 10.1126/science.aat5053

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Cytoneme signaling in fly development

During development of certain tissues in the fruit fly, signaling from one tissue to another appears to occur through specialized filopodia called cytonemes. The cytonemes contain receptors and reach close toward the signal-producing cells. Huang et al. report that components of neuronal signaling at synapses also function in proper formation of cytoneme appositions and signaling. Various manipulations of calcium signaling, expression of dominant-negative glutamate receptor proteins, or depletion of vesicle transport proteins or components of voltage-gated calcium channels influenced the presence of cytonemes and signaling.

Science, this issue p. 948


We investigated the roles of components of neuronal synapses for development of the Drosophila air sac primordium (ASP). The ASP, an epithelial tube, extends specialized signaling filopodia called cytonemes that take up signals such as Dpp (Decapentaplegic, a homolog of the vertebrate bone morphogenetic protein) from the wing imaginal disc. Dpp signaling in the ASP was compromised if disc cells lacked Synaptobrevin and Synaptotagmin-1 (which function in vesicle transport at neuronal synapses), the glutamate transporter, and a voltage-gated calcium channel, or if ASP cells lacked Synaptotagmin-4 or the glutamate receptor GluRII. Transient elevations of intracellular calcium in ASP cytonemes correlate with signaling activity. Calcium transients in ASP cells depend on GluRII, are activated by l-glutamate and by stimulation of an optogenetic ion channel expressed in the wing disc, and are inhibited by EGTA and by the GluR inhibitor NASPM (1-naphthylacetyl spermine trihydrochloride). Activation of GluRII is essential but not sufficient for signaling. Cytoneme-mediated signaling is glutamatergic.

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