Abstract
C-type allatostatins (AST-Cs) are pleiotropic neuropeptides that are broadly conserved within arthropods; the presence of three AST-C isoforms, encoded by paralog genes, is common. However, these peptides are hypothesized to act through a single receptor, thereby exerting similar bioactivities within each species. We investigated this hypothesis in the American lobster, Homarus americanus, mapping the distributions of AST-C isoforms within relevant regions of the nervous system and digestive tract, and comparing their modulatory influences on the cardiac neuromuscular system. Immunohistochemistry showed that in the pericardial organ, a neuroendocrine release site, AST-C I and/or III and AST-C II are contained within distinct populations of release terminals. Moreover, AST-C I/III-like immunoreactivity was seen in midgut epithelial endocrine cells and the cardiac ganglion (CG), whereas AST-C II-like immunoreactivity was not seen in these tissues. These data suggest that AST-C I and/or III can modulate the CG both locally and hormonally; AST-C II likely acts on the CG solely as a hormonal modulator. Physiological studies demonstrated that all three AST-C isoforms can exert differential effects, including both increases and decreases, on contraction amplitude and frequency when perfused through the heart. However, in contrast to many state-dependent modulatory changes, the changes in contraction amplitude and frequency elicited by the AST-Cs were not functions of the baseline parameters. The responses to AST-C I and III, neither of which is COOH-terminally amidated, are more similar to one another than they are to the responses elicited by AST-C II, which is COOH-terminally amidated. These results suggest that the three AST-C isoforms are differentially distributed in the lobster nervous system/midgut and can elicit distinct behaviors from the cardiac neuromuscular system, with particular structural features, e.g., COOH-terminal amidation, likely important in determining the effects of the peptides.NEW & NOTEWORTHY Multiple isoforms of many peptides exert similar effects on neural circuits. In this study we show that each of the three isoforms of C-type allatostatin (AST-C) can exert differential effects, including both increases and decreases in contraction amplitude and frequency, on the lobster cardiac neuromuscular system. The distribution of effects elicited by the nonamidated isoforms AST-C I and III are more similar to one another than to the effects of the amidated AST-C II.
Highlights
The outputs of the pattern-generating networks responsible for controlling a wide range of rhythmic movements are remarkably flexible; this flexibility is due largely to modulation by amines and peptides
It is clear that interactions between different neuromodulators are critical in determining the effects of a given modulator. This is seen, for example, in the leech (Mesce et al 2001; Mesce 2002), in which the simultaneous application of octopamine and serotonin inhibits swimming, whereas each amine applied on its own enhances swimming, and in the spiny lobster (Dickinson et al 1997), in which the response of the cardiac sac pattern generator to the neuropeptide proctolin differs depending on its past history of exposure to another peptide, red pigment concentrating hormone (RPCH)
Our data showed that all three AST-C peptides elicited both increases and decreases in heart contraction amplitude. This led us to ask whether the effects of all three peptides were always the same in an individual lobster; that is, if one isoform of AST-C elicits an increase in contraction amplitude, do the others likewise elicit increases in amplitude? to determine whether the effects exerted by these peptides on the cardiac system are likely to be physiological, we explored the presence and distribution of the AST-C peptides in the cardiac ganglion (CG) and in endocrine/neuroendocrine tissues that might be responsible for providing AST-C to the cardiac neuromuscular system in the American lobster H. americanus via the circulatory system
Summary
The outputs of the pattern-generating networks responsible for controlling a wide range of rhythmic movements are remarkably flexible; this flexibility is due largely to modulation by amines and peptides. It is clear that interactions between different neuromodulators are critical in determining the effects of a given modulator This is seen, for example, in the leech (Mesce et al 2001; Mesce 2002), in which the simultaneous application of octopamine and serotonin inhibits swimming, whereas each amine applied on its own enhances swimming, and in the spiny lobster (Dickinson et al 1997), in which the response of the cardiac sac pattern generator to the neuropeptide proctolin differs depending on its past history of exposure to another peptide, red pigment concentrating hormone (RPCH). The effects of the neuropeptide allatotropin on the movements of the heart and aorta in several species of hemophagous insects are dependent on interactions with other modulators; this peptide increases the frequency of www.jn.org
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
