Adipokinetic hormones and their G protein-coupled receptors emerged in Lophotrochozoa

Shizhong Li,Cornelis J P Grimmelikhuijzen,Signe K Skadborg,Nikolaj Kirketerp-Møller,Stine V Nielsen,Frank Hauser

doi:10.1038/srep32789

Shizhong Li, Cornelis J P Grimmelikhuijzen + Show 4 more

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https://doi.org/10.1038/srep32789

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Journal: Scientific Reports	Publication Date: Sep 15, 2016
Citations: 36	License type: CC BY 4.0

Affiliation: University of Copenhagen

Abstract

Most multicellular animals belong to two evolutionary lineages, the Proto– and Deuterostomia, which diverged 640–760 million years (MYR) ago. Neuropeptide signaling is abundant in animals belonging to both lineages, but it is often unclear whether there exist evolutionary relationships between the neuropeptide systems used by proto- or deuterostomes. An exception, however, are members of the gonadotropin-releasing hormone (GnRH) receptor superfamily, which occur in both evolutionary lineages, where GnRHs are the ligands in Deuterostomia and GnRH-like peptides, adipokinetic hormone (AKH), corazonin, and AKH/corazonin-related peptide (ACP) are the ligands in Protostomia. AKH is a well-studied insect neuropeptide that mobilizes lipids and carbohydrates from the insect fat body during flight. In our present paper, we show that AKH is not only widespread in insects, but also in other Ecdysozoa and in Lophotrochozoa. Furthermore, we have cloned and deorphanized two G protein-coupled receptors (GPCRs) from the oyster Crassostrea gigas (Mollusca) that are activated by low nanomolar concentrations of oyster AKH (pQVSFSTNWGSamide). Our discovery of functional AKH receptors in molluscs is especially significant, because it traces the emergence of AKH signaling back to about 550 MYR ago and brings us closer to a more complete understanding of the evolutionary origins of the GnRH receptor superfamily.

Highlights

Adipokinetic hormone (AKH) is an insect neuropeptide produced by the corpora cardiaca, two neurohemal organs, often fused, that are closely situated to the insect brain
The mature C. gigas adipokinetic hormone (AKH) sequence is ten amino acid residues long and contains all the hallmarks of insect AKHs. This AKH peptide is very similar to locust AKH-1 (Table 1), because the two peptides share five identical amino acid residues and three conserved residues, while the remaining two residues are not part of the hallmarks of insect AKH
During the nearly forty years that followed, a very large number of AKHs was isolated from insects and other arthropods[1], which established the view, among invertebrate endocrinologists, that AKH was an arthropod-specific neurohormone

Summary

Introduction

Adipokinetic hormone (AKH) is an insect neuropeptide produced by the corpora cardiaca, two neurohemal organs, often fused, that are closely situated to the insect brain. During genomic and EST database mining, we discovered other AKHs that were 10 amino-acid residues long and that had a WXGamide or WXPamide C terminus (see Table 1 of our current paper). We isolated the ligand for this receptor from Drosophila larvae, which to our surprise was not a GnRH-like peptide, but Drosophila AKH9. This discovery was the first finding indicating that an evolutionary link exists between insect AKH and vertebrate GnRH signaling.

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