Pedal peptide/orcokinin‐type neuropeptide signaling in a deuterostome: The anatomy and pharmacology of starfish myorelaxant peptide in Asterias rubens

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Neuropeptides are evolutionarily ancient neuronal signaling molecules that regulate diverse physiological processes and behaviors in animals. The isolation and structural identification of neuropeptides was first accomplished through use of bioassays to monitor chromatographic purification of pharmacologically active components in neural extracts (O'Shea & Schaffer, 1985). For example, using this approach the cardioactive neuropeptide FMRFamide was discovered in bivalve mollusks (Price & Greenberg, 1977). A different approach to neuropeptide discovery was adopted by Lloyd and Connolly (1989)—they sought to identify neuropeptides in the mollusk Aplysia californica that are synthesized preferentially in particular ganglia. A neuropeptide that is synthesized by cell bodies in the pedal ganglia was purified and sequenced (PLDSVYGTHGMSGFA) and then appropriately named “pedal peptide” (PP; Lloyd & Connolly, 1989).
Immunohistochemical localization of PP in Aplysia revealed that it is synthesized by a population of neurons located mostly in the pedal ganglia with processes projecting peripherally and predominantly innervating the foot (Hall & Lloyd, 1990; Pearson & Lloyd, 1989). Consistent with this pattern of expression, PP causes an increase in the amplitude and relaxation rate of nerve‐evoked contractions of Aplysia foot muscle (Hall & Lloyd, 1990). Furthermore, PP‐expressing neurons fire in phase with each pedal wave during locomotor activity and stop firing during defensive contractions of the foot (Hall & Lloyd, 1990). Thus, PP‐releasing neurons appear to modulate foot muscle contractility during locomotion. However, PP is not only involved in control of foot activity because PP‐expressing neurons also innervate other organs (e.g., the hermaphroditic duct) (Hall & Lloyd, 1990). Furthermore, sequencing of the Aplysia neural transcriptome revealed that PP is just one of a large family of related neuropeptides in this species, which are derived from four precursor proteins (Moroz et al., 2006).
Multiple PP‐type neuropeptides and precursor proteins have also been identified in other mollusks, including the limpet Lottia gigantea (Veenstra, 2010) and the nudibranch Tritonia diomedia (Lloyd, Phares, Phillips, & Willows, 1996). Investigation of the pharmacological effects of PPs in Tritonia revealed that they cause an increase in the ciliary beat frequency of cells in the pedal epithelium, again providing evidence of a physiological role in regulation of locomotor activity (Willows, Pavlova, & Phillips, 1997). Furthermore, immunohistochemical analysis of PP expression in Tritonia indicated roles in a variety of other behavioral activities, including orientation, swimming, and feeding (Beck, Cooper, & Willows, 2000; Gaston, 1998). Accordingly, a PP was found to cause an increase in the ciliary beat frequency of cells in the salivary duct of Tritonia, indicative of a physiological role in regulation of salivary transport associated with feeding (Gaston, 1998).
Molluscan PP‐type neuropeptides belong to a family of related neuropeptides that also occur in other phyla, including arthropod orcokinins (Jekely, 2013; Rowe & Elphick, 2012). Orcokinin was first identified in the crayfish Orconectes limosus as a neuropeptide (NFDEIDRSGFGFN) that is a potent stimulator of the hind‐gut, enhancing the frequency and amplitude of spontaneous contractions (Stangier, Hilbich, Burdzik, & Keller, 1992). Molecular characterization of orcokinins in the crayfish Procambarus clarkia revealed that orcokinin and other orcokinin‐like peptides are derived from two closely related precursor proteins—preproorcokinin‐A and ‐B (Yasuda‐Kamatani & Yasuda, 2000). Furthermore, orcokinin‐type neuropeptides have also been identified in other arthropods, including insects. This has revealed that multiple orcokinin isoforms occur in each species (Pascual, Castresana, Valero, Andreu, & Belles, 2004) and, as in crustaceans, alternatively spliced transcripts encoding preproorcokinin‐A and ‐B have been identified in Drosophila melanogaster and other insects (Liu et al., 2006; Sterkel et al., 2012; Veenstra & Ida, 2014).
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