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Identification of an allatostatin C signaling system in mollusc Aplysia.

ABSTRACT: Neuropeptides, as pervasive intercellular signaling molecules in the CNS, modulate a variety of behavioral systems in both protostomes and deuterostomes. Allatostatins are neuropeptides in arthropods that inhibit the biosynthesis of juvenile hormones. Based on amino acid sequences, they are divided into three different types in arthropods: allatostatin A, allatostatin B, allatostatin C. Allatostatin C (AstC) was first isolated from Manduca sexta, and it has an important conserved feature of a disulfide bridge formed by two cysteine residues. Moreover, AstC appears to be the ortholog of mammalian somatostatin, and it has functions in common with somatostatin, such as modulating feeding behaviors. The AstC signaling system has been widely studied in arthropods, but minimally studied in molluscs. In this study, we seek to identify the AstC signaling system in the marine mollusc Aplysia californica. We cloned the AstC precursor from the cDNA of Aplysia. We predicted a 15-amino acid peptide with a disulfide bridge, i.e., AstC, using NeuroPred. We then cloned two putative allatostatin C-like receptors and through NCBI Conserved Domain Search we found that they belonged to the G protein-coupled receptor (GPCR) family. In addition, using an inositol monophosphate 1 (IP1) accumulation assay, we showed that Aplysia AstC could activate one of the putative receptors, i.e., the AstC-R, at the lowest EC₅₀, and AstC without the disulfide bridge (AstC') activated AstC-R with the highest EC₅₀. Moreover, four molluscan AstCs with variations of sequences from Aplysia AstC but with the disulfide bridge activated AstC-R at intermediate EC₅₀. In summary, our successful identification of the Aplysia AstC precursor and its receptor (AstC-R) represents the first example in molluscs, and provides an important basis for further studies of the AstC signaling system in Aplysia and other molluscs.

SUBMITTER: Jiang HM

PROVIDER: S-EPMC8786951 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundMarine molluscs, as is the case with most aquatic animals, rely heavily on olfactory cues for survival. In the mollusc Aplysia californica, mate-attraction is mediated by a blend of water-borne protein pheromones that are detected by sensory structures called rhinophores. The expression of G protein and phospholipase C signaling molecules in this organ is consistent with chemosensory detection being via a G-protein-coupled signaling mechanism.ResultsHere we show that novel multi-transmembrane proteins with similarity to rhodopsin G-protein coupled receptors are expressed in sensory epithelia microdissected from the Aplysia rhinophore. Analysis of the A. californica genome reveals that these are part of larger multigene families that possess features found in metazoan chemosensory receptor families (that is, these families chiefly consist of single exon genes that are clustered in the genome). Phylogenetic analyses show that the novel Aplysia G-protein coupled receptor-like proteins represent three distinct monophyletic subfamilies. Representatives of each subfamily are restricted to or differentially expressed in the rhinophore and oral tentacles, suggesting that they encode functional chemoreceptors and that these olfactory organs sense different chemicals. Those expressed in rhinophores may sense water-borne pheromones. Secondary signaling component proteins Galphaq, Galphai, and Galphao are also expressed in the rhinophore sensory epithelium.ConclusionThe novel rhodopsin G-protein coupled receptor-like gene subfamilies identified here do not have closely related identifiable orthologs in other metazoans, suggesting that they arose by a lineage-specific expansion as has been observed in chemosensory receptor families in other bilaterians. These candidate chemosensory receptors are expressed and often restricted to rhinophores and oral tentacles, lending support to the notion that water-borne chemical detection in Aplysia involves species- or lineage-specific families of chemosensory receptors.

Project description:BACKGROUND:The freshwater snail Lymnaea stagnalis (L. stagnalis) has served as a successful model for studies in the field of Neuroscience. However, a serious drawback in the molecular analysis of the nervous system of L. stagnalis has been the lack of large-scale genomic or neuronal transcriptome information, thereby limiting the use of this unique model. RESULTS:In this study, we report 7,712 distinct EST sequences (median length: 847 nucleotides) of a normalized L. stagnalis central nervous system (CNS) cDNA library, resulting in the largest collection of L. stagnalis neuronal transcriptome data currently available. Approximately 42% of the cDNAs can be translated into more than 100 consecutive amino acids, indicating the high quality of the library. The annotated sequences contribute 12% of the predicted transcriptome size of 20,000. Surprisingly, approximately 37% of the L. stagnalis sequences only have a tBLASTx hit in the EST library of another snail species Aplysia californica (A. californica) even using a low stringency e-value cutoff at 0.01. Using the same cutoff, approximately 67% of the cDNAs have a BLAST hit in the NCBI non-redundant protein and nucleotide sequence databases (nr and nt), suggesting that one third of the sequences may be unique to L. stagnalis. Finally, using the same cutoff (0.01), more than half of the cDNA sequences (54%) do not have a hit in nematode, fruitfly or human genome data, suggesting that the L. stagnalis transcriptome is significantly different from these species as well. The cDNA sequences are enriched in the following gene ontology functional categories: protein binding, hydrolase, transferase, and catalytic enzymes. CONCLUSION:This study provides novel molecular insights into the transcriptome of an important molluscan model organism. Our findings will contribute to functional analyses in neurobiology, and comparative evolutionary biology. The L. stagnalis CNS EST database is available at http://www.Lymnaea.org/.

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Identification of an allatostatin C signaling system in mollusc Aplysia.

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