Abstract
Central pattern generators produce rhythmic behaviors independently of sensory input; however, their outputs can be modulated by neuropeptides, thereby allowing for functional flexibility. We investigated the effects of C-type allatostatins (AST-C) on the cardiac ganglion (CG), which is the central pattern generator that controls the heart of the American lobster, Homarus americanus, to identify the biological mechanism underlying the significant variability in individual responses to AST-C. We proposed that the presence of multiple receptors, and thus differential receptor distribution, was at least partly responsible for this observed variability. Using transcriptome mining and PCR-based cloning, we identified four AST-C receptors (ASTCRs) in the CG; we then characterized their cellular localization, binding potential, and functional activation. Only two of the four receptors, ASTCR1 and ASTCR2, were fully functional GPCRs that targeted to the cell surface and were activated by AST-C peptides in our insect cell expression system. All four, however, were amplified from CG cDNAs. Following the confirmation of ASTCR expression, we used physiological and bioinformatic techniques to correlate receptor expression with cardiac responses to AST-C across individuals. Expression of ASTCR1 in the CG showed a negative correlation with increasing contraction amplitude in response to AST-C perfusion through the lobster heart, suggesting that the differential expression of ASTCRs within the CG is partly responsible for the specific physiological response to AST-C exhibited by a given individual lobster.
Highlights
The neuronal networks that control rhythmic movements, such as locomotion and respiration, in both invertebrates and vertebrates [1,2,3] produce consistent, reliably patterned outputs
Homam-ASTCR4 conservation was more limited at ~20% (Figure 1A)
BLASTx analyses of the putative Homam-AST-C receptors (ASTCRs) revealed significant similarities with sequences annotated as somatostatin and/or AST receptor-like, including Homam-ASTCR4, which had weaker, but still highly significant E values (Table S2)
Summary
The neuronal networks that control rhythmic movements, such as locomotion and respiration, in both invertebrates and vertebrates [1,2,3] produce consistent, reliably patterned outputs. The effects of the C-type allatostatin peptides (AST-Cs) on networks of the stomatogastric system are more pronounced in slowly cycling preparations than in rapidly cycling ones; in this case, the peptide decreases activity, so that slowly cycling preparations become even slower and motor output is not altered in more active preparations [18]. In both instances, the action of the modulatory neuron can bias the system towards a specific output, but the extent of bias is state dependent
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