Characterization of a set of abdominal neuroendocrine cells that regulate stress physiology using colocalized diuretic peptides in Drosophila

Meet Zandawala,Dick R Nässel,Richard Marley,Shireen A Davies

doi:10.1007/s00018-017-2682-y

Meet Zandawala, Dick R Nässel + Show 2 more

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https://doi.org/10.1007/s00018-017-2682-y

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Abstract

Multiple neuropeptides are known to regulate water and ion balance in Drosophila melanogaster. Several of these peptides also have other functions in physiology and behavior. Examples are corticotropin-releasing factor-like diuretic hormone (diuretic hormone 44; DH44) and leucokinin (LK), both of which induce fluid secretion by Malpighian tubules (MTs), but also regulate stress responses, feeding, circadian activity and other behaviors. Here, we investigated the functional relations between the LK and DH44 signaling systems. DH44 and LK peptides are only colocalized in a set of abdominal neurosecretory cells (ABLKs). Targeted knockdown of each of these peptides in ABLKs leads to increased resistance to desiccation, starvation and ionic stress. Food ingestion is diminished by knockdown of DH44, but not LK, and water retention is increased by LK knockdown only. Thus, the two colocalized peptides display similar systemic actions, but differ with respect to regulation of feeding and body water retention. We also demonstrated that DH44 and LK have additive effects on fluid secretion by MTs. It is likely that the colocalized peptides are coreleased from ABLKs into the circulation and act on the tubules where they target different cell types and signaling systems to regulate diuresis and stress tolerance. Additional targets seem to be specific for each of the two peptides and subserve regulation of feeding and water retention. Our data suggest that the ABLKs and hormonal actions are sufficient for many of the known DH44 and LK functions, and that the remaining neurons in the CNS play other functional roles.

Highlights

Orchestration of physiological and behavioral processes is commonly dependent on neuropeptide and peptide hormone signaling
We show that this subset of the LK neurons, designated abdominal LK neurons (ABLKs), produce corticotrophin-releasing factor-like diuretic hormone, known as diuretic hormone 44 (DH44)
Our study reveals that a portion of the LK-expressing neurosecretory cells (ABLKs) in abdominal ganglia co-express DH44, similar to earlier findings in the moth Manduca sexta [54], the locust Locusta migratoria [55], and blood-sucking bug Rhodnius prolixus [56]

Summary

Introduction

Orchestration of physiological and behavioral processes is commonly dependent on neuropeptide and peptide hormone signaling (see [1,2,3,4]). The question is whether peptidergic neurons of a large diverse population are functionally coupled and play a concerted physiological role, or if they are parts of distributed networks where the specific neuropeptide serve diverse functions To address this question, we have selected a set of neuroendocrine cells producing the neuropeptide leucokinin (LK) that consists of four morphological types of cells [20, 21], and is proposed to serve multiple functions in flies [6, 22,23,24,25,26]. We can show that the ABLKs, and hormonal actions of the two peptides, are sufficient for regulating water and ion homeostasis and associated stress functions, but can affect food intake, perhaps by an indirect action caused by diuretic activity This suggests that the LK and DH44 neurons in the brain are important for the additional functional roles listed above, and it remains to be determined whether these functions are in any way linked to those of the ABLKs

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