Honey Bee Allatostatins Target Galanin/Somatostatin-Like Receptors and Modulate Learning: A Conserved Function?

Elodie Urlacher,Daniel Fourmy,Isabelle Massou,Laurent Soustelle,Marie-Julie Gherardi,Marie-Laure Parmentier,Heleen Verlinden,Alison R Mercer,Jean-Marc Devaud,Christian Wegener

doi:10.1371/journal.pone.0146248

Abstract

Sequencing of the honeybee genome revealed many neuropeptides and putative neuropeptide receptors, yet functional characterization of these peptidic systems is scarce. In this study, we focus on allatostatins, which were first identified as inhibitors of juvenile hormone synthesis, but whose role in the adult honey bee (Apis mellifera) brain remains to be determined. We characterize the bee allatostatin system, represented by two families: allatostatin A (Apime-ASTA) and its receptor (Apime-ASTA-R); and C-type allatostatins (Apime-ASTC and Apime-ASTCC) and their common receptor (Apime-ASTC-R). Apime-ASTA-R and Apime-ASTC-R are the receptors in bees most closely related to vertebrate galanin and somatostatin receptors, respectively. We examine the functional properties of the two honeybee receptors and show that they are transcriptionally expressed in the adult brain, including in brain centers known to be important for learning and memory processes. Thus we investigated the effects of exogenously applied allatostatins on appetitive olfactory learning in the bee. Our results show that allatostatins modulate learning in this insect, and provide important insights into the evolution of somatostatin/allatostatin signaling.

Highlights

Neuropeptide signaling is ubiquitous across animal phyla, and exerts a great variety of actions on animal physiology and behavior [1]
We examine the functional properties of the honey bee allatostatin receptors A (Apime-ASTA-R) and C (Apime-ASTC-R), we identify where in the brain the genes that encode these receptors are expressed, and we investigate the effects of exogenously applied allatostatins A (Apime-ASTA), C (Apime-ASTC) and CC (Apime-ASTCC) on appetitive olfactory learning in the bee
Three mRNA transcript variants exist for Apime-AstA-R as the genomic region contains several introns (Fig 1), but all result in the same cDNA (1083nt) and protein sequence (361AA, calculated mass: 41.23 kDa)

Summary

Introduction

Neuropeptide signaling is ubiquitous across animal phyla, and exerts a great variety of actions on animal physiology and behavior [1]. Through their actions as neuromodulators, neuropeptides play a central role in the coordinated regulation of an organism’s internal state [2] and in mammals, neuropeptidergic control of the motivational or emotional state has been shown in PLOS ONE | DOI:10.1371/journal.pone.0146248. Honey Bee ASTs Target GAL/SST-Like Receptors and Modulate Learning turn to have a significant impact on higher cognitive processes [3]. The identification of large numbers of neuropeptides in insects, and the expression of many of these peptides in the brain, suggest that neuropeptide signaling is likely to contribute significantly to normal brain function in insects and possibly modulate cognition in these animals [1,7,8,9,10]

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Results

Conclusion