Functional characterization of a second pedal peptide/orcokinin‐type neuropeptide signaling system in the starfish Asterias rubens

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Molluscan pedal peptides (PPs) and arthropodan orcokinins (OKs) are structurally related neuropeptides that are the prototypes of a family of neuropeptides that have been identified in several phyla, including other protostomes (nematodes, annelids), and deuterostomes (echinoderms). Thus, the evolutionary origin of PP/OK‐type neuropeptides can be traced to the bilaterian common ancestor of protostomes and deuterostomes (Jekely, 2013; Rowe & Elphick, 2012). However, little is known about the physiological roles of PP/OK‐type neuropeptides in non‐molluscan/arthropodan phyla.
PP was discovered in the mollusk Aplysia californica on account of its expression by neurons in the pedal ganglia (Lloyd & Connolly, 1989). Subsequently, molecular analysis of Aplysia and other molluscan species has revealed the occurrence of multiple precursor proteins that each comprise “cocktails” of structurally related peptides (Moroz et al., 2006; Veenstra, 2010). Investigation of the effects of PPs in mollusks has revealed that these neuropeptides regulate foot muscle activity and increase the ciliary beat frequency of cells in the foot epithelium, actions that are indicative of physiological roles in the control of locomotor activity (Araki, Liu, Zhang, Takeuchi, & Munekata, 1995; Hall & Lloyd, 1990; Malyshev, Norekian, & Willows, 1999; Willows, Pavlova, & Phillips, 1997).
OK was identified in the crayfish Orconectes limosus as a neuropeptide that enhances the frequency and amplitude of spontaneous contractions of the hind‐gut (Stangier, Hilbich, Burdzik, & Keller, 1992). Subsequent studies have revealed that OKs also alter the rhythmic motor output of the stomatogastric nervous system in crustaceans (Li et al., 2002; Skiebe, Dreger, Meseke, Evers, & Hucho, 2002). Furthermore, experimental studies on insects have revealed that OKs cause a phase‐dependent shift in circadian locomotor activity in cockroaches (Hofer & Homberg, 2006), regulate “awakening” behavior in the beetle Tribolium castaneum (Jiang, Kim, & Park, 2015) and regulate ecdysis in the kissing bug Rhodnius prolixus (Wulff et al., 2017). Thus, PP/OK‐type neuropeptides have a variety of actions in mollusks and arthropods but with stimulatory actions appearing to be a common theme.
Discovery of two genes in the sea urchin Strongylocentrotus purpuratus (phylum Echinodermata) that encode precursors of PP‐like neuropeptides (SpPPLNP1, SpPPLNP2) provided the first evidence that PP/OK‐type peptides also occur in deuterostomes (Rowe & Elphick, 2012). However, nothing is known about the physiological roles of PP/OK‐type neuropeptides in sea urchins. Recently, a neuropeptide isolated from the starfish Patiria pectinifera that acts as a muscle relaxant (“starfish myorelaxant peptide” or SMP) was identified as a PP/OK‐type neuropeptide (Kim et al., 2016). Cloning and sequencing of a cDNA encoding the SMP precursor revealed that it comprises 12 copies of SMP and 7 copies of three other SMP‐like peptides. Analysis of the distribution of SMP precursor transcripts in P. pectinifera using quantitative PCR revealed a widespread pattern of expression. Furthermore, in vitro pharmacological experiments revealed that SMP causes relaxation of three preparations from P. pectinifera—the apical muscle, tube feet, and cardiac stomach. Collectively, these data indicated that SMP may have a general role as a muscle relaxant in starfish (Kim et al., 2016).
A homolog of the P. pectinifera SMP precursor comprising 8 copies of SMP‐like PP/OK‐type peptides has been identified in the common European starfish Asterias rubens (Kim et al., 2016). Furthermore, a partial sequence of a second PP/OK‐type precursor has also been identified in A. rubens (Semmens et al., 2016). Therefore, we have named the A. rubens SMP‐type precursor A. rubens PP‐like neuropeptide precursor 1 (ArPPLNP1) and we have named the other A. rubens PP/OK‐type precursor A. rubens PP‐like neuropeptide precursor 2 (ArPPLNP2).
Recently, we reported a detailed analysis of the anatomy of ArPPLNP1 expression in A. rubens using mRNA in situ hybridization and immunohistochemistry (Lin, Egertová, Zampronio, Jones, & Elphick, 2017).
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