Abstract
Molluscan pedal peptides (PPs) and arthropod orcokinins (OKs) are prototypes of a family of neuropeptides that have been identified in several phyla. Recently, starfish myorelaxant peptide (SMP) was identified as a PP/OK‐type neuropeptide in the starfish Patiria pectinifera (phylum Echinodermata). Furthermore, analysis of transcriptome sequence data from the starfish Asterias rubens revealed two PP/OK‐type precursors: an SMP‐type precursor (A. rubens PP‐like neuropeptide precursor 1; ArPPLNP1) and a second precursor (ArPPLNP2). We reported previously a detailed analysis of ArPPLNP1 expression in A. rubens and here we report the first functional characterization ArPPLNP2‐derived neuropeptides. Sequencing of a cDNA encoding ArPPLNP2 revealed that it comprises eleven related neuropeptides (ArPPLN2a‐k), the structures of several of which were confirmed using mass spectrometry. Analysis of the expression of ArPPLNP2 and neuropeptides derived from this precursor using mRNA in situ hybridization and immunohistochemistry revealed a widespread distribution, including expression in radial nerve cords, circumoral nerve ring, digestive system, tube feet and innervation of interossicular muscles. In vitro pharmacology revealed that the ArPPLNP2‐derived neuropeptide ArPPLN2h has no effect on the contractility of tube feet or the body wall‐associated apical muscle, contrasting with the relaxing effect of ArPPLN1b (ArSMP) on these preparations. ArPPLN2h does, however, cause dose‐dependent relaxation of cardiac stomach preparations, with greater potency/efficacy than ArPPLN1b and with similar potency/efficacy to the SALMFamide neuropeptide S2. In conclusion, there are similarities in the expression patterns of ArPPLNP1 and ArPPLNP2 but our data also indicate specialization in the roles of neuropeptides derived from these two PP/OK‐type precursors in starfish.
Highlights
The structures of neuropeptides derived from ArPPLNP2 were determined by MS/MS analysis of A. rubens radial nerve cords extracted in 90% methanol/9% acetic acid, employing use of methods described previously (Lin, Egertova et al, 2017; Lin, Mita et al, 2017)
We report the structural, anatomical and functional characterization of neuropeptides derived from A. rubens PP-like neuropeptide precursor 2 (ArPPLNP2)
FI G URE 11 ArPPLN2h causes dose-dependent relaxation of in vitro preparations of the cardiac stomach from A. rubens. (a) Representative recording showing the dose-dependent relaxing effect of ArPPLN2h (10210 to 1026 M) on a cardiac stomach preparation pre-contracted with artificial seawater containing 30 mM added KCl
Summary
Be traced to the bilaterian common ancestor of protostomes and deuterostomes (Jekely, 2013; Rowe & Elphick, 2012). In vitro pharmacological experiments revealed that SMP causes relaxation of three preparations from P. pectinifera—the apical muscle, tube feet, and cardiac stomach These data indicated that SMP may have a general role as a muscle relaxant in starfish (Kim et al, 2016). Investigation of the in vitro pharmacological effects of ArPPLN1b revealed that it causes dose-dependent relaxation of three preparations from A. rubens—apical muscle, tube feet and cardiac stomach (Lin, Egertova et al, 2017), consistent with previous findings from P. pectinifera (Kim et al, 2016). Collectively the data obtained from experimental studies on SMP/PPLN1-type neuropeptides in P. pectinifera and A. rubens indicate that a physiological role of these peptides is to act as inhibitory neuromuscular transmitters or modulators in starfish. The objective of this study was to investigate the expression pattern and pharmacological actions of neuropeptides derived from the second PP/OK-type neuropeptide precursor in A. rubens, ArPPLNP2
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