Drosophila larval to pupal switch under nutrient stress requires IP3R/Ca2+ signalling in glutamatergic interneurons

Abstract

Neuronal circuits are known to integrate nutritional information, but the identity of the circuit components is not completely understood. Amino acids are a class of nutrients that are vital for the growth and function of an organism. Here, we report a neuronal circuit that allows Drosophila larvae to overcome amino acid deprivation and pupariate. We find that nutrient stress is sensed by the class IV multidendritic cholinergic neurons. Through live calcium imaging experiments, we show that these cholinergic stimuli are conveyed to glutamatergic neurons in the ventral ganglion through mAChR. We further show that IP3R-dependent calcium transients in the glutamatergic neurons convey this signal to downstream medial neurosecretory cells (mNSCs). The circuit ultimately converges at the ring gland and regulates expression of ecdysteroid biosynthetic genes. Activity in this circuit is thus likely to be an adaptation that provides a layer of regulation to help surpass nutritional stress during development.DOI: http://dx.doi.org/10.7554/eLife.17495.001

Nutrient‐dependent increased dendritic arborization of somatosensory neurons

“…Very recently, a circuit in the larval nervous system has been reported, which is proposed to sense amino acid deprivation and contribute to the juvenile-toadult transition (pupariation) under nutrient-sparse conditions (Jayakumar et al 2016). More specifically, Class IV neurons sense amino acid deprivation at a late larval stage and send inputs to glutamatergic neurons in the CNS, which release peptides to neurosecretory cells to modulate ecdysteroid gene expression.…”

“…Intriguingly, it was recently proposed that Class IV neurons also sense nutrient stress (Jayakumar et al . ). In contrast, Class I neurons function in a proprioceptive sensory feedback circuit for rhythmic locomotion (Hughes & Thomas ; Hwang et al .…”

“…Class IV neurons are polymodal nociceptors responsible for thermal, mechanical and light sensation (Tracey et al 2003;Hwang et al 2007;Xiang et al 2010;Zhong et al 2010;Im & Galko 2012;Terada et al 2016). Intriguingly, it was recently proposed that Class IV neurons also sense nutrient stress (Jayakumar et al 2016). In contrast, Class I neurons function in a proprioceptive sensory feedback circuit for rhythmic locomotion (Hughes & Thomas 2007;Hwang et al 2007;Im & Galko 2012).…”

“ER-Ca2+ sensor STIM regulates neuropeptides required for development under nutrient restriction in Drosophila”

“…In flies (Drosophila melanogaster; Dmel), dSTIM regulates functioning of neurons (7)(8)(9)(10)(11)(12), fat body cells (13) and intestinal stem cells (14). dSTIM-mediated SOCE has been demonstrated in Dmel neurons (7), with functional consequences in certain neuronal subtypes: regulation of flight in dopaminergic neurons (8,15) and development in proteindeprived media in glutamatergic neurons (10). Further, dSTIM over-expression in insulinproducing neuropeptidergic neurons could restore Ca 2+ homeostasis in a non-autonomous manner in other neurons of an IP 3 R mutant (16), indicating an important role for dSTIM in NE cell output as well as compensatory interplay between SOCE regulators IP 3 R and dSTIM.…”

FMRFa receptor stimulated Ca2+signals alter the activity of flight modulating central dopaminergic neurons inDrosophila melanogaster

“…To test this idea, we introduced a temperature sensitive cation channel, dTrpAl (37) in flies with adult specific FMRFaR knockdown. Activation of the dTrpA1 calcium channel can compensate in part for reduced Ca 2+ entry through voltage-gated channels (15, 38). Indeed, expression of dTrpAl significantly improved the maintenance of flight bouts in 6 and 8 day old FMRFaR knockdown adults (Fig 6E, S2A Fig - THD1;TARGET controls and S5D Fig - TrpA1/+;FMRFaR RNAi /+ controls).…”