The neuropeptidome of the Crown-of-Thorns Starfish, Acanthaster planci

Smith, Meaghan; Wang, Tianfang; Suwansa‐ard, Saowaros; Motti, Cherie A.; Elizur, Abigail; Zhao, Min; Rowe, Matthew L.; Hall, Michael R.; Elphick, Maurice R.; Cummins, Scott F.

doi:10.1016/j.jprot.2017.05.026

Cited by 48 publications

(56 citation statements)

References 42 publications

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“…In the future, it would be interesting to perform similar investigations in other starfish. Analysis of the genome/transcriptome of the crown‐of‐thorns starfish Acanthaster planci has revealed the presence of genes/transcripts encoding proteins that are orthologs of ArPPLNP1 and ArPPLNP2 (Smith et al, ). Furthermore, based on recent extensive molecular analysis of the phylogenetic relationships of extant Asteroidea (Linchangco et al, ), the occurrence of PPLNP1‐type (SMP‐type) and PPLNP2‐type proteins in A. rubens (order Forcipulatida) and in A. planci (order Valvatida) suggests that both of these PP/OK‐type precursors would have been present in the common ancestor of all extant starfish.…”

Section: Discussionmentioning

confidence: 99%

Functional characterization of a second pedal peptide/orcokinin‐type neuropeptide signaling system in the starfish Asterias rubens

Lin

Egertová

Zampronio

et al. 2017

J of Comparative Neurology

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Molluscan pedal peptides (PPs) and arthropod orcokinins (OKs) are prototypes of a family of neuropeptides that have been identified in several phyla. Recently, starfish myorelaxant peptide (SMP) was identified as a PP/OK‐type neuropeptide in the starfish Patiria pectinifera (phylum Echinodermata). Furthermore, analysis of transcriptome sequence data from the starfish Asterias rubens revealed two PP/OK‐type precursors: an SMP‐type precursor (A. rubens PP‐like neuropeptide precursor 1; ArPPLNP1) and a second precursor (ArPPLNP2). We reported previously a detailed analysis of ArPPLNP1 expression in A. rubens and here we report the first functional characterization ArPPLNP2‐derived neuropeptides. Sequencing of a cDNA encoding ArPPLNP2 revealed that it comprises eleven related neuropeptides (ArPPLN2a‐k), the structures of several of which were confirmed using mass spectrometry. Analysis of the expression of ArPPLNP2 and neuropeptides derived from this precursor using mRNA in situ hybridization and immunohistochemistry revealed a widespread distribution, including expression in radial nerve cords, circumoral nerve ring, digestive system, tube feet and innervation of interossicular muscles. In vitro pharmacology revealed that the ArPPLNP2‐derived neuropeptide ArPPLN2h has no effect on the contractility of tube feet or the body wall‐associated apical muscle, contrasting with the relaxing effect of ArPPLN1b (ArSMP) on these preparations. ArPPLN2h does, however, cause dose‐dependent relaxation of cardiac stomach preparations, with greater potency/efficacy than ArPPLN1b and with similar potency/efficacy to the SALMFamide neuropeptide S2. In conclusion, there are similarities in the expression patterns of ArPPLNP1 and ArPPLNP2 but our data also indicate specialization in the roles of neuropeptides derived from these two PP/OK‐type precursors in starfish.

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Section: Discussionmentioning

confidence: 99%

Functional characterization of a second pedal peptide/orcokinin‐type neuropeptide signaling system in the starfish Asterias rubens

Lin

Egertová

Zampronio

et al. 2017

J of Comparative Neurology

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“…In the sea cucumbers Apostichopus japonicus, Holothuria glaberrima, Holothuria scabra, and Holothuria leucospilota, the precursor comprises a single neuropeptide with the same predicted structure in all four species-KPYKFMRW-NH 2 (Rowe et al, 2014;Suwansa-Ard et al, 2018;Chen et al, 2019;Chieu et al, 2019). Luqin-type precursors identified in the starfish species A. rubens and Acanthaster planci comprise a single putative neuropeptide with the amino acid sequence EKGRFPKFMRW-NH 2 and EEKTRFPKFMRW-NH 2 , respectively Smith et al, 2017). Ophiuroid luqin-type precursors also comprise a single putative neuropeptide, which has the predicted sequence QGFNRDGPAKFMRW-NH 2 in Ophionotus victoriae, QGFNRGEGPAKFMRW-NH 2 in Ophiopsila aranea, and QGFSRDGPAKFMRW-NH 2 in Amphiura filiformis (Zandawala et al, 2017).…”

Section: Discovery Of Luqin-type Signaling In Ambulacrarian Deuterostmentioning

confidence: 99%

Evolution and Comparative Physiology of Luqin-Type Neuropeptide Signaling

Yáñez-Guerra

Elphick

2020

Front. Neurosci.

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Luqin is a neuropeptide that was discovered and named on account of its expression in left upper quadrant cells of the abdominal ganglion in the mollusc Aplysia californica. Subsequently, luqin-type peptides were identified as cardio-excitatory neuropeptides in other molluscs and a cognate receptor was discovered in the pond snail Lymnaea stagnalis. Phylogenetic analyses have revealed that orthologs of molluscan luqin-type neuropeptides occur in other phyla; these include neuropeptides in ecdysozoans (arthropods, nematodes) that have a C-terminal RYamide motif (RYamides) and neuropeptides in ambulacrarians (echinoderms, hemichordates) that have a C-terminal RWamide motif (RWamides). Furthermore, precursors of luqin-type neuropeptides typically have a conserved C-terminal motif containing two cysteine residues, although the functional significance of this is unknown. Consistent with the orthology of the neuropeptides and their precursors, phylogenetic and pharmacological studies have revealed that orthologous G-protein coupled receptors (GPCRs) mediate effects of luqin-type neuropeptides in spiralians, ecdysozoans, and ambulacrarians. Luqin-type signaling originated in a common ancestor of the Bilateria as a paralog of tachykinin-type signaling but, unlike tachykinin-type signaling, luqin-type signaling was lost in chordates. This may largely explain why luqin-type signaling has received less attention than many other neuropeptide signaling systems. However, insights into the physiological actions of luqin-type neuropeptides (RYamides) in ecdysozoans have been reported recently, with roles in regulation of feeding and diuresis revealed in insects and roles in regulation of feeding, egg laying, locomotion, and lifespan revealed in the nematode Caenorhabditis elegans. Furthermore, characterization of a luqin-type neuropeptide in the starfish Asterias rubens (phylum Echinodermata) has provided the first insights into the physiological roles of luqin-type signaling in a deuterostome. In conclusion, although luqin was discovered in Aplysia over 30 years ago, there is still much to be learnt about luqin-type neuropeptide signaling. This will be facilitated in the post-genomic era by the emerging opportunities for experimental studies on a variety of invertebrate taxa.

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“…Transcripts encoding putative NPPs were identified by tBLASTn searches using the CLC Main Workbench Version 7.7 (CLC Bio-Qaigen, AsiaPac, Taiwan). Briefly, the amino acid (aa) sequences of 57 known putative NPPs from other echinoderm species (Strongylocentrotus purpuratus [10], Apostichopus japonicus [11], Asterias rubens [12]), and Acanthaster planci [28] were used for tBLASTn searches with parameters set as follows: matrix, BLOSUM62; e-value, 100. BLAST hits were collected, translated, and then manually analyzed based on their similarities to the orthologous proteins from other species and the presence of conserved motifs.…”

Section: Npp Transcript Mining Comparative Sequence Analysis and Phmentioning

confidence: 99%

“…Recently, investigation of the occurrence of NPs in sea cucumbers and other echinoderms has been accelerated by transcriptomic analyses. Thus, many NPPs have been identified in sea urchins (Class Echinoidea), starfish (Class Asteroidea) and brittle stars (Class Ophiuroidea) [10,12,28,29].…”

Section: Introductionmentioning

confidence: 99%

Transcriptomic discovery and comparative analysis of neuropeptide precursors in sea cucumbers (Holothuroidea)

et al. 2018

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Neuropeptides synthesized and released by neuronal cells play important roles in the regulation of many processes, e.g. growth, feeding, reproduction, and behavior. In the past decade, next-generation sequencing technologies have helped to facilitate the identification of multiple neuropeptide genes in a variety of taxa, including arthropods, molluscs and echinoderms. In this study, we extend these studies to Holothuria scabra, a sea cucumber species that is widely cultured for human consumption. In silico analysis of H. scabra neural and gonadal transcriptomes enabled the identification of 28 transcripts that encode a total of 26 bilaterian and echinoderm-specific neuropeptide precursors. Furthermore, publicly available sequence data from another sea cucumber, Holothuria glaberrima, allowed a more in-depth comparative investigation. Interestingly, two isoforms of a calcitonin-type peptide precursor (CTPP) were deduced from the H. scabra transcriptome - HscCTPP-long and HscCTPP-short, likely the result of alternative splicing. We also identified a sea cucumber relaxin-type peptide precursor, which is of interest because relaxin-type peptides have been shown to act as gonadotropic hormones in starfish. Two neuropeptides that appear to be holothurian-specific are GLRFA, and GN-19. In H. scabra, the expression of GLRFA was restricted to neural tissues, while GN-19 expression was additionally found in the longitudinal muscle and intestinal tissues. In conclusion, we have obtained new insights into the neuropeptide signaling systems of holothurians, which will facilitate physiological studies that may enable advances in the aquaculture of sea cucumbers.

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The neuropeptidome of the Crown-of-Thorns Starfish, Acanthaster planci

Cited by 48 publications

References 42 publications

Functional characterization of a second pedal peptide/orcokinin‐type neuropeptide signaling system in the starfish Asterias rubens

Functional characterization of a second pedal peptide/orcokinin‐type neuropeptide signaling system in the starfish Asterias rubens

Evolution and Comparative Physiology of Luqin-Type Neuropeptide Signaling

Transcriptomic discovery and comparative analysis of neuropeptide precursors in sea cucumbers (Holothuroidea)

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