Distinct or shared actions of peptide family isoforms: II. Multiple pyrokinins exert similar effects in the lobster stomatogastric nervous system

Abstract

Many neuropeptides are members of peptide families, with multiple structurally similar isoforms frequently found even within a single species. This raises the question of whether the individual peptides serve common or distinct functions. In the accompanying paper, we found high isoform specificity in the responses of the lobster (Homarus americanus) cardiac neuromuscular system to members of the pyrokinin peptide family: only one of five crustacean isoforms showed any bioactivity in the cardiac system. Because previous studies in other species had found little isoform specificity in pyrokinin actions, we examined the effects of the same five crustacean pyrokinins on the lobster stomatogastric nervous system (STNS). In contrast to our findings in the cardiac system, the effects of the five pyrokinin isoforms on the STNS were indistinguishable: they all activated or enhanced the gastric mill motor pattern, but did not alter the pyloric pattern. These results, in combination with those from the cardiac ganglion, suggest that members of a peptide family in the same species can be both isoform specific and highly promiscuous in their modulatory capacity. The mechanisms that underlie these differences in specificity have not yet been elucidated; one possible explanation, which has yet to be tested, is the presence and differential distribution of multiple receptors for members of this peptide family.

Distinct or shared actions of peptide family isoforms: I. Peptide-specific actions of pyrokinins in the lobster cardiac neuromuscular system

“…Such differences in receptor specificity have been seen, for example, in Drosophila, in which one receptor for tachykinin-related peptides is highly specific, responding only to a single isoform, whereas a second receptor is less specific (Poels et al, 2009). Whether this is a difference in the two species or in the receptors in the two parts of the nervous system is not clear from this study alone [but see our companion article (Dickinson et al, 2015)]. …”

“…We found that pyrokinins are likely to influence the heart via both local and hormonal pathways and they are bioactive in this system. However, to our surprise given the ubiquitous actions different isoforms elicit from the STNS (Saideman et al, 2007;Dickinson et al, 2015), bioactivity in the cardiac neuromuscular system is highly isoform specific.…”

“…The antibody used for these experiments was generated against the sequence FSPRLamide, the only pyrokinin thus far isolated from H. americanus (Ma et al, 2008); the production and characterization of this antibody are described in detail in a companion article to this report (Dickinson et al, 2015). In none of the cardiac ganglia examined (N=12) was any evidence for pyrokinin immunoreactivity noted in either the cardiac ganglion pacemaker or motor neurons (Fig.…”

“…Predel and Wegener, 2006;Rafaeli, 2009), while in crustaceans, information on bioactivity is limited to studies of their effects on the crab (Cancer borealis) and lobster (H. americanus) stomatogastric nervous system (STNS), a CPG-effector system that controls the rhythmic movement of the foregut, in which all isoforms tested elicit a similar motor output in both species [Saideman et al, 2007;Dickinson et al, 2015 (the companion article to the study presented here)]. Given the lack of information on the cardioactive properties of pyrokinins, we asked here whether members of this peptide family are likely to reach the heart as either local or hormonal modulators, and if so, whether they modulate the output of the lobster cardiac neuromuscular system.…”

Sources and range of long-term variability of rhythmic motor patternsin vivo.

“…One consequence of the ganglion sheath having a selective permeability could be that modulators in the hemolymph may not affect the activity of the STG motor circuits, or at least not with the expected magnitude. Furthermore, a recent study by Dickinson et al (2015) showed that although multiple modulators of the same species have similar effects on motor activity, others exhibit isoform-specific selectivity. So, although modulators may be present and permeate through the ganglion sheath, they may not necessarily influence motor output.…”