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Roles for cell autonomous neuromodulatory mechanisms in these processes have been well described. The importance of cell non-autonomous pathways for inter-tissue signaling, such as gut-to-brain or glia-to-neuron, has emerged more recently, but the cellular mechanisms mediating such regulation remain comparatively unexplored. Glycoproteins and their G protein-coupled receptors (GPCRs) are well-established orchestrators of multi-tissue signaling events that govern diverse physiological processes through both cell-autonomous and cell non-autonomous regulation. Here, we show that follicle stimulating hormone receptor, FSHR-1, the sole <jats:italic>Caenorhabditis elegans<\/jats:italic> ortholog of mammalian glycoprotein hormone GPCRs, is important for cell non-autonomous modulation of synaptic transmission. Inhibition of <jats:italic>fshr-1<\/jats:italic> expression reduces muscle contraction and leads to synaptic vesicle accumulation in cholinergic motor neurons. The neuromuscular and locomotor defects in <jats:italic>fshr-1<\/jats:italic> loss-of-function mutants are associated with an underlying accumulation of synaptic vesicles, build-up of the synaptic vesicle priming factor UNC-10\/RIM, and decreased synaptic vesicle release from cholinergic motor neurons. Restoration of FSHR-1 to the intestine is sufficient to restore neuromuscular activity and synaptic vesicle localization to <jats:italic>fshr-1-<\/jats:italic>deficient animals. Intestine-specific knockdown of FSHR-1 reduces neuromuscular function, indicating FSHR-1 is both necessary and sufficient in the intestine for its neuromuscular effects. Re-expression of FSHR-1 in other sites of endogenous expression, including glial cells and neurons, also restored some neuromuscular deficits, indicating potential cross-tissue regulation from these tissues as well. Genetic interaction studies provide evidence that downstream effectors <jats:italic>gsa-1<\/jats:italic>\/<jats:italic>G<\/jats:italic>\u03b1<jats:sub><jats:italic>S<\/jats:italic><\/jats:sub>, <jats:italic>acy-1<\/jats:italic>\/adenylyl cyclase and <jats:italic>sphk-1\/<\/jats:italic>sphingosine kinase and glycoprotein hormone subunit orthologs, GPLA-1\/GPA2 and GPLB-1\/GPB5, are important for intestinal FSHR-1 modulation of the NMJ. Together, our results demonstrate that FSHR-1 modulation directs inter-tissue signaling systems, which promote synaptic vesicle release at neuromuscular synapses.<\/jats:p>","DOI":"10.1371\/journal.pgen.1011461","type":"journal-article","created":{"date-parts":[[2024,11,19]],"date-time":"2024-11-19T18:40:04Z","timestamp":1732041604000},"page":"e1011461","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":1,"title":["Cell non-autonomous signaling through the conserved C. elegans glycoprotein hormone receptor FSHR-1 regulates cholinergic neurotransmission"],"prefix":"10.1371","volume":"20","author":[{"given":"Morgan","family":"Buckley","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-5872-2975","authenticated-orcid":true,"given":"William 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