Abstract:Although tachykinin-like neuropeptides have been identified in molluscs more than two decades ago, knowledge on their function and signalling has so far remained largely elusive. We developed a cell-based assay to address the functionality of the tachykinin G-protein coupled receptor (Cragi-TKR) in the oyster Crassostrea gigas. The oyster tachykinin neuropeptides that are derived from the tachykinin precursor gene Cragi-TK activate the Cragi-TKR in nanomolar concentrations. Receptor activation is sensitive to … Show more
“…The relatively high expression of oyster signalling components in the mantle edges (Dubos et al, 2003), a tissue involved in shell biomineralization (Geraerts, 1976), is strongly suggestive of such a role. In contrast to some oyster signalling systems (Bigot et al, 2012;Dubos et al, 2018;Schwartz et al, 2018), we found no involvement of the oyster CT signalling system in feeding regulation. This diverges from the role of DH31 in feeding regulation in arthropods (Nagata and Nagasawa, 2017).…”
Section: Biological Implications Of the Oyster Ct Signalling Systemscontrasting
confidence: 99%
“…Lophotrochozoa, including annelids (Bauknecht and Jékely, 2015) and molluscs (Veenstra, 2010;Adamson et al, 2015;Zatylny-Gaudin et al, 2016;Ahn et al, 2017;Zhang et al, 2018) such as the oyster Crassostrea gigas (Stewart et al, 2014). In this species, large-scale genomic and transcriptomic resources (Zhang et al, 2012;Riviere et al, 2015) are now available, and facilitate the study of signalling pathways (Bigot et al, 2014;Dubos et al, 2018;Li et al, 2016;Schwartz et al, 2018). The present study investigated the evolution of the calcitonin (CT)/diuretic hormone 31 (DH31) signalling system in the bivalve mollusc C. gigas.…”
In Protostoma, the diuretic hormone 31 (DH31) signalling system was long considered as the orthologue of the chordate calcitonin (CT) signalling system. Using the Pacific oyster (Crassostrea gigas) transcriptomic database GigaTON, we characterized seven G-protein-coupled receptors (GPCRs) named Cragi-CTR1-7 and phylogenetically related to chordate CT receptors (CTRs) and to protostome DH31 receptors. Two CT precursors (Cragi-CTP1 and Cragi-CTP2) containing two CT-type peptides and encoded by two distinct genes with a similar organization were also characterized. These oyster neuropeptides (Cragi-CT1/2) exhibit the two N-terminal paired cysteine residues and, except CTP2-derived peptide (Cragi-CTP2dp), show the C-terminal proline-amide motif typical of deuterostome CT-type peptides. All mature Cragi-CTs except Cragi-CTP2dp were detected in visceral ganglion extracts using mass spectrometry. Cell-based assays revealed that the previously characterized oyster receptors Cg-CT-R and Cragi-CTR2 were specifically activated by Cragi-CT1b and Cragi-CT2, respectively. This activation does not require the co-expression of receptor activitymodifying proteins (RAMPs). Thus, oyster CT signalling appears functionally more closely related to vertebrate CT/CTR signalling than to calcitonin gene-related peptide/calcitonin receptor-like receptor (CGRP/CLR) signalling. Gene expression profiles in different adult tissues and in oysters acclimated to brackish water suggest the potential implication of both Cg-CT-R/Cragi-CT1b and Cragi-CTR2/Cragi-CT2 in water and ionic regulations, although with apparently opposite effects. The present study represents the first comprehensive characterization of a functional CT-type signalling system in a protostome and provides evidence for its evolutionarily ancient origin and its early role in osmotic homeostasis.
“…The relatively high expression of oyster signalling components in the mantle edges (Dubos et al, 2003), a tissue involved in shell biomineralization (Geraerts, 1976), is strongly suggestive of such a role. In contrast to some oyster signalling systems (Bigot et al, 2012;Dubos et al, 2018;Schwartz et al, 2018), we found no involvement of the oyster CT signalling system in feeding regulation. This diverges from the role of DH31 in feeding regulation in arthropods (Nagata and Nagasawa, 2017).…”
Section: Biological Implications Of the Oyster Ct Signalling Systemscontrasting
confidence: 99%
“…Lophotrochozoa, including annelids (Bauknecht and Jékely, 2015) and molluscs (Veenstra, 2010;Adamson et al, 2015;Zatylny-Gaudin et al, 2016;Ahn et al, 2017;Zhang et al, 2018) such as the oyster Crassostrea gigas (Stewart et al, 2014). In this species, large-scale genomic and transcriptomic resources (Zhang et al, 2012;Riviere et al, 2015) are now available, and facilitate the study of signalling pathways (Bigot et al, 2014;Dubos et al, 2018;Li et al, 2016;Schwartz et al, 2018). The present study investigated the evolution of the calcitonin (CT)/diuretic hormone 31 (DH31) signalling system in the bivalve mollusc C. gigas.…”
In Protostoma, the diuretic hormone 31 (DH31) signalling system was long considered as the orthologue of the chordate calcitonin (CT) signalling system. Using the Pacific oyster (Crassostrea gigas) transcriptomic database GigaTON, we characterized seven G-protein-coupled receptors (GPCRs) named Cragi-CTR1-7 and phylogenetically related to chordate CT receptors (CTRs) and to protostome DH31 receptors. Two CT precursors (Cragi-CTP1 and Cragi-CTP2) containing two CT-type peptides and encoded by two distinct genes with a similar organization were also characterized. These oyster neuropeptides (Cragi-CT1/2) exhibit the two N-terminal paired cysteine residues and, except CTP2-derived peptide (Cragi-CTP2dp), show the C-terminal proline-amide motif typical of deuterostome CT-type peptides. All mature Cragi-CTs except Cragi-CTP2dp were detected in visceral ganglion extracts using mass spectrometry. Cell-based assays revealed that the previously characterized oyster receptors Cg-CT-R and Cragi-CTR2 were specifically activated by Cragi-CT1b and Cragi-CT2, respectively. This activation does not require the co-expression of receptor activitymodifying proteins (RAMPs). Thus, oyster CT signalling appears functionally more closely related to vertebrate CT/CTR signalling than to calcitonin gene-related peptide/calcitonin receptor-like receptor (CGRP/CLR) signalling. Gene expression profiles in different adult tissues and in oysters acclimated to brackish water suggest the potential implication of both Cg-CT-R/Cragi-CT1b and Cragi-CTR2/Cragi-CT2 in water and ionic regulations, although with apparently opposite effects. The present study represents the first comprehensive characterization of a functional CT-type signalling system in a protostome and provides evidence for its evolutionarily ancient origin and its early role in osmotic homeostasis.
“…The complement system is considered to be an important element of the innate immune system that also triggers the adaptive immunity in higher animals in the animal kingdom. Similar hemolytic complement-like activity was also reported against parasites and other pathogens in molluscs [20,21].…”
In common with other invertebrates, molluscs are known to have internal immune response against foreign particles and organisms. The innate immunity of molluscs reflects the inherent non-specific response that provides the first line of defense. Anatomic barriers, phagocytic cells, and physiological components are the main elements of the innate immune response in molluscs. It is composed of both cellular and humoral elements. The cellular components are the circulating hemocytes. Small invaders are eliminated by the phagocytic hemocytes, while large invaders are eliminated by encapsulation. The ingested foreign particles are then hemolyzed by the action of certain toxic enzymes that catalyze oxidative burst reactions capable of killing pathogens and foreign invaders. Humoral components of molluscan immunity involve nitric oxide, lysozyme activity, lectins, and the phenyloxidase system. The current chapter sheds light on the elements of the molluscan innate immune system and presents a case study of the immune response of Lymnaea stagnalis mollusc against Chaetogaster limnaei parasite. The effect of the parasite on some humoral immune response parameters such as nitric oxide, phenol oxidase, and lysozyme production was investigated. In conclusion, the snail Lymnaea stagnalis exerts humoral immune response against Chaetogaster limnaei parasite. However, this response is insufficient to eliminate the parasite.
“…Accordingly, new signalling systems have recently been discovered in the annelid Platynereis dumerilii 12 , 13 and in the mollusc Crassostrea. gigas 14 – 16 . The present study investigates the evolution of the gastrin/cholecystokinin (G/CCK)/sulfakinin (SK) signalling system in Lophotrochozoa, using the mollusc C. gigas as a representative species.…”
Chordate gastrin/cholecystokinin (G/CCK) and ecdysozoan sulfakinin (SK) signalling systems represent divergent evolutionary scenarios of a common ancestral signalling system. The present article investigates for the first time the evolution of the CCK/SK signalling system in a member of the Lophotrochozoa, the second clade of protostome animals. We identified two G protein-coupled receptors (GPCR) in the oyster Crassostrea gigas (Mollusca), phylogenetically related to chordate CCK receptors (CCKR) and to ecdysozoan sulfakinin receptors (SKR). These receptors, Cragi-CCKR1 and Cragi-CCKR2, were characterised functionally using a cell-based assay. We identified di- and mono-sulphated forms of oyster Cragi-CCK1 (pEGAWDY(SO3H)DY(SO3H)GLGGGRF-NH2) as the potent endogenous agonists for these receptors. The Cragi-CCK genes were expressed in the visceral ganglia of the nervous system. The Cragi-CCKR1 gene was expressed in a variety of tissues, while Cragi-CCKR2 gene expression was more restricted to nervous tissues. An in vitro bioassay revealed that different forms of Cragi-CCK1 decreased the frequency of the spontaneous contractions of oyster hindgut. Expression analyses in oysters with contrasted nutritional statuses or in the course of their reproductive cycle highlighted the plausible role of Cragi-CCK signalling in the regulation of feeding and its possible involvement in the coordination of nutrition and energy storage in the gonad. This study confirms the early origin of the CCK/SK signalling system from the common bilaterian ancestor and delivers new insights into its structural and functional evolution in the lophotrochozoan lineage.
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