Developing organisms use fine-tuning mechanisms to adjust body growth to ever-changing nutritional conditions. In Drosophila, the secretory activity of insulin-producing cells (IPCs) is central to couple systemic growth with amino acids availability. Here, we identify a subpopulation of inhibitory neurons contacting the IPCs (IPC-connecting neurons or ICNs) that play a key role in this coupling. We show that ICNs respond to growth-blocking peptides (GBPs), a family of fat-body-derived signals produced upon availability of dietary amino acids. We demonstrate that GBPs are atypical ligands for the fly EGF receptor (EGFR). Upon activation of EGFR by adipose GBPs, ICN-mediated inhibition of IPC function is relieved, allowing insulin secretion. Our study reveals an unexpected role for EGF-like metabolic hormones and EGFR signaling as critical modulators of neural activity, coupling insulin secretion to the nutritional status.

In Drosophila oocytes, dorso-anterior transport of gurken mRNA requires both the Dynein motor and the heterogeneous nuclear ribonucleoprotein (hnRNP) Squid. We show that gurken transcripts are transported directly on microtubules by Dynein in nonmembranous electron-dense transport particles that also contain Squid and the transport cofactors Egalitarian and Bicaudal-D. At its destination, gurken mRNA is statically anchored by Dynein within large electron-dense cytoplasmic structures known as sponge bodies. Egalitarian and Bicaudal-D contribute only to active transport, whereas Dynein and Squid are also required for gurken mRNA anchoring and the integrity of sponge bodies. Disrupting Dynein function disperses gurken mRNA homogeneously throughout the cytoplasm, whereas the loss of Squid function converts the sponge bodies into active transport particles. We propose that Dynein acts as a static structural component for the assembly of gurken mRNA transport and anchoring complexes, and that Squid is required for the dynamic conversion of transport particles to sponge bodies.

Molecular motors actively transport many types of cargo along the cytoskeleton in a wide range of organisms. One class of cargo is localized mRNAs, which are transported by myosin on actin filaments or by kinesin and dynein on microtubules. How the cargo is kept at its final intracellular destination and whether the motors are recycled after completion of transport are poorly understood. Here, we use a new RNA anchoring assay in living Drosophila blastoderm embryos to show that apical anchoring of mRNA after completion of dynein transport does not depend on actin or on continuous active transport by the motor. Instead, apical anchoring of RNA requires microtubules and involves dynein as a static anchor that remains with the cargo at its final destination. We propose a general principle that could also apply to other dynein cargo and to some other molecular motors, whereby cargo transport and anchoring reside in the same molecule.