Functional Characterization of the Short Neuropeptide F Receptor in the Desert Locust, Schistocerca gregaria

Senne Dillen,Heleen Verlinden,Sven Zels,Pieter Van Wielendaele,Jornt Spit,Jozef Vanden Broeck,Hubert Vaudry

doi:10.1371/journal.pone.0053604

Abstract

Whereas short neuropeptide F (sNPF) has already been reported to stimulate feeding behaviour in a variety of insect species, the opposite effect was observed in the desert locust. In the present study, we cloned a G protein-coupled receptor (GPCR) cDNA from the desert locust, Schistocerca gregaria. Cell-based functional analysis of this receptor indicated that it is activated by both known isoforms of Schgr-sNPF in a concentration dependent manner, with EC50 values in the nanomolar range. This Schgr-sNPF receptor constitutes the first functionally characterized peptide GPCR in locusts. The in vivo effects of the sNPF signalling pathway on the regulation of feeding in locusts were further studied by knocking down the newly identified Schgr-sNPF receptor by means of RNA interference, as well as by means of peptide injection studies. While injection of sNPF caused an inhibitory effect on food uptake in the desert locust, knocking down the corresponding peptide receptor resulted in an increase of total food uptake when compared to control animals. This is the first comprehensive study in which a clearly negative correlation is described between the sNPF signalling pathway and feeding, prompting a reconsideration of the diverse roles of sNPFs in the physiology of insects.

Highlights

Peptides of the short neuropeptide F family are widely distributed throughout the phylum of Arthropoda
We describe the characterization of a short neuropeptide F (sNPF) receptor from the desert locust, Schistocerca gregaria, and discuss its role in the regulation of food uptake
The identification and characterization of its cognate receptor represents an important step towards the elucidation of its mode of action

Summary

Introduction

Peptides of the short neuropeptide F (sNPF) family are widely distributed throughout the phylum of Arthropoda. Their occurrence was demonstrated in all arthropod species of which ample sequence data are available. SNPF has not been observed in non-arthropod species [1]. Multiple sNPF isoforms are derived from a single peptide precursor. In Drosophila melanogaster, for example, the Drome-sNPF precursor encodes four sNPF isoforms [2], and three putative sNPF peptides were found in the sNPF precursor sequence of Bombyx mori [3]. In Rhodnius prolixus, the Rhopr-sNPF pre-pro-peptide precursor only yields one single sNPF-like peptide [4]

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Conclusion