Neuropeptide precursors and neuropeptides in the sea cucumber Apostichopus japonicus: a genomic, transcriptomic and proteomic analysis

Scientific Reports, Journal Year: 2019, Volume and Issue: 9(1)

Published: June 20, 2019

The sea cucumber Apostichopus japonicus is a foodstuff with very high economic value in China, Japan and other countries south-east Asia. It at the heart of multibillion-dollar industry to meet demand for this product, aquaculture methods facilities have been established. However, there are challenges associated optimization reproduction, feeding growth non-natural environments. Therefore, we need learn more about biology A. japonicus, including processes such as aestivation, evisceration, regeneration albinism. One major classes molecules that regulate physiology behaviour animals neuropeptides, few bioactive peptides already identified japonicus. To facilitate comprehensive investigations neuropeptide function here analysed genomic transcriptomic sequence data proteomic identify precursors neuropeptides species. We 44 transcripts encoding or putative precursors, some instances derived from these were confirmed by mass spectrometry. Furthermore, analysis enabled identification location precursor genes on scaffolds linkage groups (chromosomes) determination gene structure. Many contain homologs bilaterian animals. Precursors thus far only echinoderms identified, L- F-type SALMFamides, AN others. several act modulators neuromuscular activity also identified. discovery large repertoire provides basis experimental studies investigate physiological roles signaling systems Looking ahead, may effects could be harnessed enable improvements economically important

Language: Английский

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Ancient role of sulfakinin/cholecystokinin-type signalling in inhibitory regulation of feeding processes revealed in an echinoderm

eLife, Journal Year: 2021, Volume and Issue: 10

Published: Sept. 7, 2021

Sulfakinin (SK)/cholecystokinin (CCK)-type neuropeptides regulate feeding and digestion in protostomes (e.g. insects) chordates. Here, we characterised SK/CCK-type signalling for the first time a non-chordate deuterostome – starfish Asterias rubens (phylum Echinodermata). In this species, two (ArSK/CCK1, ArSK/CCK2) derived from precursor protein ArSK/CCKP act as ligands an receptor (ArSK/CCKR) these peptides/proteins are expressed nervous system, digestive tube feet, body wall. Furthermore, ArSK/CCK1 ArSK/CCK2 cause dose-dependent contraction of cardiac stomach, foot, apical muscle preparations vitro, injection vivo triggers stomach retraction inhibition onset A. . Thus, evolutionarily ancient role inhibitory regulators feeding-related processes Bilateria has been conserved unusual unique context extra-oral behaviour pentaradial plan echinoderm.

Language: Английский

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The complex simplicity of the brittle star nervous system

Frontiers in Zoology, Journal Year: 2018, Volume and Issue: 15(1)

Published: Feb. 1, 2018

Brittle stars (Ophiuroidea, Echinodermata) have been increasingly used in studies of animal behavior, locomotion, regeneration, physiology, and bioluminescence. The success these directly depends on good working knowledge the ophiuroid nervous system.Here, we describe arm system at different levels organization, including microanatomy radial nerve cord peripheral nerves, ultrastructure neural tissue, localization cell types using specific antibody markers. We standardize nomenclature nerves ganglia, provide an anatomically accurate digital 3D model as a reference for future studies. Our results helped identify several general features characteristic to adult echinoderm system, extensive anatomical interconnections between ectoneural hyponeural components, neuroepithelial organization central supporting scaffold neuroepithelium formed by glial cells. In addition, further support notion that glia is complex diverse population. also tested suitability range cell-type markers brittle star established cells are reliably labeled with ERG1 antibodies, whereas best neuronal acetylated tubulin, ELAV, synaptotagmin B. transcription factor Brn1/2/4 - marker progenitors expressed not only neurons, but subpopulation glia. For first time, putative proprioceptors associated part system.Together, our data help establish both principles architecture common phylum Echinodermata features.

Language: Английский

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Functional Characterization of Paralogous Gonadotropin-Releasing Hormone-Type and Corazonin-Type Neuropeptides in an Echinoderm

Frontiers in Endocrinology, Journal Year: 2017, Volume and Issue: 8

Published: Sept. 29, 2017

Homologs of the vertebrate neuropeptide gonadotropin-releasing hormone (GnRH) have been identified in invertebrates, including insect corazonin (CRZ). Recently, we reported discovery GnRH-type and CRZ-type signaling systems an echinoderm, starfish Asterias rubens, demonstrating that evolutionary origin paralogous neuropeptides can be traced back to common ancestor protostomes deuterostomes. Here, investigated physiological roles (ArGnRH) (ArCRZ) A. using mRNA situ hybridization, immunohistochemistry vitro pharmacology. ArGnRH precursor (ArGnRHP)-expressing cells ArGnRH-immunoreactive and/or processes are present radial nerve cords, circumoral ring, digestive system (e.g., cardiac stomach pyloric stomach), body wall-associated muscle (apical muscle), appendages (tube feet, terminal tentacle). The general distribution ArCRZ (ArCRZP)-expressing is similar ArGnRHP, but with specific local differences. For example, expressing ArGnRHP both ectoneural hyponeural regions cords whereas ArCRZP were only observed region. In pharmacological experiments revealed cause contraction stomach, apical muscle, tube foot preparations. However, was more potent/effective than as a contractant muscle. These findings demonstrate myoexcitatory starfish, differences their expression patterns activities indicative distinct roles. This first study investigate deuterostome, providing new insights into evolution comparative physiology these Bilateria.

Language: Английский

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Comparative and Evolutionary Physiology of Vasopressin/ Oxytocin-Type Neuropeptide Signaling in Invertebrates

Frontiers in Endocrinology, Journal Year: 2020, Volume and Issue: 11

Published: April 17, 2020

The identification of structurally related hypothalamic hormones that regulate blood pressure and diuresis (vasopressin, VP; CYFQNCPRG-NH2) or lactation uterine contraction (oxytocin, OT; CYIQNCPLG-NH2) was a major advance in neuroendocrinology, recognised the award Nobel Prize for Chemistry 1955. Furthermore, discovery central actions VP OT as regulators reproductive social behaviour humans other mammals has broadened interest these neuropeptides beyond physiology into psychology. VP/OT-type their G-protein coupled receptors originated common ancestor Bilateria (Urbilateria), with invertebrates typically having single neuropeptide cognate receptor. Gene/genome duplications followed by gene loss gave rise to variety number different vertebrate lineages. Recent advances comparative transcriptomics/genomics have enabled an ever-growing diversity invertebrate taxa, providing new opportunities gain insights evolution function Bilateria. Here we review invertebrates, roles regulation reproduction, feeding water/salt homeostasis emerging themes. For example, highlight recent reports oocyte maturation sea-squirt Ciona intestinalis, extraoral starfish Asterias rubens energy status dessication resistance ants. Thus, are pleiotropic physiological processes, evolutionarily conserved can be traced back Urbilateria. To deeper understanding it may necessary not only determine peptides but also characterise transcriptomic/proteomic/metabolomic profiles cells expressing precursors and/or within framework anatomically functionally identified neuronal networks. investigation wider range species is now needed if how when this ancient signalling system recruited diverse behavioural processes branches animal phylogeny contrasting environmental contexts.

Language: Английский

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Echinoderms provide missing link in the evolution of PrRP/sNPF-type neuropeptide signalling

eLife, Journal Year: 2020, Volume and Issue: 9

Published: June 24, 2020

Neuropeptide signalling systems comprising peptide ligands and cognate receptors are evolutionarily ancient regulators of physiology behaviour. However, there challenges associated with determination orthology between neuropeptides in different taxa. Orthologs vertebrate neuropeptide-Y (NPY) known as neuropeptide-F (NPF) have been identified protostome invertebrates, whilst prolactin-releasing (PrRP) short (sNPF) paralogs NPY/NPF vertebrates protostomes, respectively. Here we investigated the occurrence NPY/NPF/PrRP/sNPF-related a deuterostome invertebrate phylum - Echinodermata. Analysis transcriptome/genome sequence data revealed loss NPY/NPF-type signalling, but orthologs PrRP-type sNPF/PrRP-type were echinoderms. Furthermore, experimental studies that neuropeptide pQDRSKAMQAERTGQLRRLNPRF-NH2 is potent ligand for receptor starfish Asterias rubens. Our findings indicate sNPF-type orthologous originated paralog Urbilateria.

Language: Английский

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Somatostatin-type and allatostatin-C–type neuropeptides are paralogous and have opposing myoregulatory roles in an echinoderm

Proceedings of the National Academy of Sciences, Journal Year: 2022, Volume and Issue: 119(7)

Published: Feb. 10, 2022

Somatostatin (SS) and allatostatin-C (ASTC) are inhibitory neuropeptides in chordates protostomes, respectively, which hitherto were identified as orthologs. However, echinoderms have two SS/ASTC-type (SS1 SS2), here, our analysis of sequence data indicates that SS1 is an ortholog ASTC SS2 SS. The occurrence both SS-type ASTC-type provides a unique context to compare their physiological roles. Investigation the expression actions neuropeptide ArSS1 starfish Asterias rubens revealed it causes muscle contraction (myoexcitation), contrasting with myoinhibitory effects ArSS2. Our findings suggest paralogous originated by gene duplication common ancestor Bilateria, only one type being retained protostomes but types echinoderms. Loss may been due functional redundancy regulators processes. Conversely, retention be consequence evolution myoexcitatory role for mediated yet unknown signaling mechanisms.

Language: Английский

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Biochemical, Anatomical, and Pharmacological Characterization of Calcitonin-Type Neuropeptides in Starfish: Discovery of an Ancient Role as Muscle Relaxants

Frontiers in Neuroscience, Journal Year: 2018, Volume and Issue: 12

Published: June 8, 2018

Calcitonin (CT) is a peptide hormone released by the thyroid gland that regulates blood Ca2+ levels in mammals. The CT gene alternatively spliced, with one transcript encoding and another CT-like neuropeptide calcitonin-gene related (α-CGRP), which powerful vasodilator. Other CT-related peptides vertebrates include adrenomedullin, amylin intermedin, also act as smooth muscle relaxants. evolutionary origin of CT-type has been traced to bilaterian common ancestor protostomes deuterostomes (DH31) identified diuretic some insect species. However, little known about physiological roles other invertebrates. Here we characterized deuterostomian invertebrate – starfish Asterias rubens (Phylum Echinodermata). A precursor cDNA (ArCTP) was sequenced predicted structure (ArCT) derived from ArCTP confirmed using mass spectrometry. distribution mRNA ArCT investigated situ hybridization immunohistochemistry, respectively, revealing stained cells/processes nervous system, digestive system muscular organs, including apical tube feet. Investigation effects synthetic on vitro preparations feet revealed it acts relaxant, causing dose-dependent reversal acetylcholine-induced contraction. Furthermore, relaxant present whole-animal extracts species, Patiria pectinifera, an ortholog named PpCT. Consistent expression pattern A. rubens, RT-qPCR P. pectinifera PpCT more abundant radial nerve cords than tissues/organs analyzed. In conclusion, our findings indicate action relaxants may reflect evolutionarily ancient role neuropeptides can be back deuterostomes.

Language: Английский

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Pedal peptide/orcokinin-type neuropeptide signaling in a deuterostome: The anatomy and pharmacology of starfish myorelaxant peptide inAsterias rubens

The Journal of Comparative Neurology, Journal Year: 2017, Volume and Issue: 525(18), P. 3890 - 3917

Published: Aug. 28, 2017

Abstract Pedal peptide (PP) and orcokinin (OK) are related neuropeptides that were discovered in protostomian invertebrates (mollusks, arthropods). However, analysis of genome/transcriptome sequence data has revealed PP/OK‐type also occur a deuterostomian phylum—the echinoderms. Furthermore, neuropeptide (starfish myorelaxant peptide, SMP) was recently identified as muscle relaxant the starfish Patiria pectinifera . Here mass spectrometry used to identify five (ArPPLN1a‐e) derived from SMP precursor (PP‐like 1; ArPPLNP1) Asterias rubens Analysis expression ArPPLNP1 this A. using mRNA situ hybridization immunohistochemistry widespread pattern expression, with labeled cells and/or processes present radial nerve cords, circumoral ring, digestive system (e.g., cardiac stomach) body wall‐associated muscles apical muscle) appendages tube feet papulae). our provide first evidence lateral motor nerves innervating interossicular muscles. In vitro pharmacological tests (ArPPLN1b) it causes dose‐dependent relaxation muscle, foot stomach preparations Collectively, these anatomical indicate act inhibitory neuromuscular transmitters starfish, which contrasts myoexcitatory actions invertebrates. Thus, divergence deuterostomes protostomes may have been accompanied by an inhibitory–excitatory transition roles regulators activity.

Language: Английский

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Discovery and functional characterisation of a luqin-type neuropeptide signalling system in a deuterostome

Scientific Reports, Journal Year: 2018, Volume and Issue: 8(1)

Published: May 2, 2018

Neuropeptides are diverse and evolutionarily ancient regulators of physiological/behavioural processes in animals. Here we have investigated the evolution comparative physiology luqin-type neuropeptide signalling, which has been characterised previously protostomian invertebrates. Phylogenetic analysis indicates that receptors tachykinin-type paralogous probably originated a common ancestor Bilateria. In deuterostomian lineage, signalling lost chordates but interestingly it retained ambulacrarians. Therefore, here for first time an ambulacrarian - starfish Asterias rubens (phylum Echinodermata). A luqin-like with C-terminal RWamide motif (ArLQ; EEKTRFPKFMRW-NH

Language: Английский

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