A novel tachykinin‐related peptide receptor of Octopus vulgaris– evolutionary aspects of invertebrate tachykinin and tachykinin‐related peptide

Abstract

The tachykinin (TK) and tachykinin‐related peptide (TKRP) family represent one of the largest peptide families in the animal kingdom and exert their actions via a subfamily of structurally related G‐protein‐coupled receptors. In this study, we have identified a novel TKRP receptor from the Octopus heart, oct‐TKRPR. oct‐TKRPR includes domains and motifs typical of G‐protein‐coupled receptors. Xenopus oocytes that expressed oct‐TKRPR, like TK and TKRP receptors, elicited an induction of membrane chloride currents coupled to the inositol phosphate/calcium pathway in response to Octopus TKRPs (oct‐TKRP I–VII) with moderate ligand selectivity. Substance P and Octopus salivary gland‐specific TK, oct‐TK‐I, completely failed to activate oct‐TKRPR, whereas a Substance P analog containing a C‐terminal Arg‐NH2 exhibited equipotent activation of oct‐TKRPs. These functional analyses prove that oct‐TKRPs, but not oct‐TK‐I, serve as endogenous functional ligands through oct‐TKRPR, although both of the family peptides were identified in a single species, and the importance of C‐terminal Arg‐NH2 in the specific recognition of TKRPs by TKRPR is conserved through evolutionary lineages of Octopus. Southern blotting of RT‐PCR products revealed that the oct‐TKRPR mRNA was widely distributed in the central and peripheral nervous systems plus several peripheral tissues. These results suggest multiple physiologic functions of oct‐TKRPs as neuropeptides both in the Octopus central nervous system and in peripheral tissues. This is the first report on functional discrimination between invertebrate TKRPs and salivary gland‐specific TKs.

Neurokinin B and reproductive functions: “KNDy neuron” model in mammals and the emerging story in fish

“…The exocrine functions of tachykinins by acting as antimicrobial peptides are also suspected in lower vertebrates, as tachykinin expression has been demonstrated in the skin of amphibians (Li et al, 2006) and more recently in fish species (Mi et al, 2010). To date, two groups of tachykinins, invertebrate tachykinins (Inv-TK) and tachykinin-related peptides (TKRP), have been reported in protostomic invertebrates, including insects (Predel et al, 2005;Siviter et al, 2000), mollusks (Kanda et al, 2003;Kanda et al, 2007), and echiuroid worms (Kawada et al, 1999), and more recently in coelenterates (Anctil, 2009) ( Table.1). In representative species of invertebrates, cognate receptors with differential selectivity for Inv-TK and TKRP respectively have been identified (Satake et al, 2013;Satake et al, 2003) and found to be functionally linked with Ca 2+ signaling (Torfs et al, 2002a;Torfs et al, 2002b), IP 3 production (Torfs et al, 2000) and cAMP production (Poels et al, 2005) similar to that of mammalian NKRs (see introduction for details).…”

Characterization of a tachykinin signalling system in the bivalve mollusc Crassostrea gigas

“…Interestingly, some vertebrate-type TKs, derived from a distinct gene, have been identified in the salivary glands of cephalopod molluscs [9,10] and insects [11] serving respectively as neurotoxins [12] and as vasodilatory agents that act on vertebrate prey TK receptors (TKR) but not on endogenous receptors [13].…”

Coupled Genomic Evolutionary Histories as Signatures of Organismal Innovations in Cephalopods

“…They play a role in regulation of vasodilation and muscle contraction. In octopods, the existence of a tachykinin receptor throughout peripheral tissues and the heart suggests that these ancient roles are preserved, but in some species tachykinins have also been recruited as key active components of venom . It thus seems likely that the venom tachykinins have arisen through neofunctionalization of existing endogenous tachykinins.…”