Tachykinins: Neuropeptides That Are Ancient, Diverse, Widespread and Functionally Pleiotropic

Frontiers in Neuroscience, Journal Year: 2019, Volume and Issue: 13

Published: Nov. 20, 2019

Tachykinins (TKs) are ancient neuropeptides present throughout the bilaterians and are, with some exceptions, characterized by a conserved FX1GX2Ramide carboxy terminus among protostomes FXGLMamide in deuterostomes. The best-known TK is vertebrate substance P, which mammals, together other TKs, has been implicated health disease important roles pain, inflammation, cancer, depressive disorder, immune system, gut function, hematopoiesis, sensory processing, hormone regulation. invertebrate TKs also known to have multiple functions central nervous system intestine these investigated more detail fly Drosophila arthropods. Here, we review protostome deuterostome organization evolution of precursors, peptides their receptors, as well functions, appear be partly across Bilateria. We outline distribution brains representative organisms. In Drosophila, recent studies revealed early olfactory neuromodulation circuits controlling locomotion food search, nociception, aggression, metabolic stress, release. signaling regulates lipid metabolism intestine. crustaceans, an neuromodulator rhythm-generating motor stomatogastric presynaptic modulator photoreceptor cells. Several additional functional can inferred from various brain circuits. addition, there few interesting cases where injected into prey animals vasodilators salivary glands or paralyzing agents venom glands. cases, produced predator sequences mimicking TKs. Lastly, TK-signaling appears duplicated Panarthropoda (comprising arthropods, onychophores, tardigrades) give rise novel type peptides, natalisins, distinct receptor. natalisins general, it that widely distributed act at short range neuromodulators cotransmitters.

Language: Английский

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The chemical brain hypothesis for the origin of nervous systems

Philosophical Transactions of the Royal Society B Biological Sciences, Journal Year: 2021, Volume and Issue: 376(1821), P. 20190761 - 20190761

Published: Feb. 8, 2021

In nervous systems, there are two main modes of transmission for the propagation activity between cells. Synaptic relies on close contact at chemical or electrical synapses while volume is mediated by diffusible signals and does not require direct contact. It possible to wire complex neuronal networks both synaptic transmission. Both types ubiquitous in leading question which appeared first evolution. This paper explores a scenario where chemically organized cellular before evolution, possibility supported presence peptidergic signalling all animals except sponges. Small peptides ideally suited link up cells into networks. They have unlimited diversity, high diffusivity copy numbers derived from repetitive precursors. But diffusion limited becomes inefficient larger bodies. To overcome this, may developed projections formed synaptically connected tiling body surfaces displaying synchronized with pulsatile peptide release. The advent circulatory systems neurohemal organs further reduced constraint imposed diffusion. could contributed explosive radiation stem bilaterians. Neurosecretory centres extant still predominantly wired coexist brain. article part theme issue ‘Basal cognition: multicellularity, neurons cognitive lens’.

Language: Английский

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Conservative route to genome compaction in a miniature annelid

Nature Ecology & Evolution, Journal Year: 2020, Volume and Issue: 5(2), P. 231 - 242

Published: Nov. 16, 2020

Abstract The causes and consequences of genome reduction in animals are unclear because our understanding this process mostly relies on lineages with often exceptionally high rates evolution. Here, we decode the compact 73.8-megabase Dimorphilus gyrociliatus , a meiobenthic segmented worm. D. retains traits classically associated larger slower-evolving genomes, such as an ordered, intact Hox cluster, generally conserved developmental toolkit traces ancestral bilaterian linkage. Unlike some other small analysis epigenome revealed canonical features regulation, excluding presence operons trans -splicing. Instead, gene-dense presents divergent Myc pathway, key physiological regulator growth, proliferation stability animals. Altogether, results uncover conservative route to compaction annelids, reminiscent that observed vertebrate Takifugu rubripes .

Language: Английский

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Cholecystokinin/sulfakinin peptide signaling: conserved roles at the intersection between feeding, mating and aggression

Cellular and Molecular Life Sciences, Journal Year: 2022, Volume and Issue: 79(3)

Published: March 1, 2022

Neuropeptides are the most diverse messenger molecules in metazoans and involved regulation of daily physiology a wide array behaviors. Some neuropeptides their cognate receptors structurally functionally well conserved over evolution bilaterian animals. Among these peptides related to gastrin cholecystokinin (CCK). In mammals, CCK is produced by intestinal endocrine cells brain neurons, regulates gall bladder contractions, pancreatic enzyme secretion, gut functions, satiety food intake. Additionally, plays important roles neuromodulation several circuits that regulate reward, anxiety, aggression sexual behavior. invertebrates, CCK-type (sulfakinins, SKs) are, with few exceptions, neurons only. Common among invertebrates SKs mediate ingestion variety mechanisms. Also secretion digestive enzymes has been reported. Studies genetically tractable fly Drosophila have advanced our understanding SK signaling mechanisms feeding, but also gustatory sensitivity, locomotor activity, reproductive A set eight SK-expressing competing males, they integrate internal state external stimuli diminish sex drive increase aggression. The same sugar gustation, induce reduce feeding. Although functional CCK/SK appear between available data suggest underlying differ.

Language: Английский

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A G protein–coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia

PLoS Biology, Journal Year: 2020, Volume and Issue: 18(3), P. e3000614 - e3000614

Published: March 3, 2020

The reproductive hormones that trigger oocyte meiotic maturation and release from the ovary vary greatly between animal species. Identification of receptors for these maturation-inducing (MIHs) understanding how they initiate largely conserved process remain important challenges. In hydrozoan cnidarians including jellyfish Clytia hemisphaerica, MIH comprises neuropeptides released somatic cells gonad. We identified receptor (MIHR) in using cell culture–based "deorphanization" candidate oocyte-expressed G protein–coupled (GPCRs). MIHR mutant generated CRISPR-Cas9 editing had severe defects gamete development or spawning both males females. Female gonads, oocytes isolated mutants, failed to respond synthetic MIH. Treatment with cAMP analogue Br-cAMP mimic rise at onset rescued spawning. Injection inhibitory antibodies alpha subunit Gs heterodimeric protein (GαS) into wild-type phenocopied mutants. These results provide molecular links stimulation initiation oocytes. Molecular phylogeny grouped a subset bilaterian neuropeptide receptors, Y, gonadotropin hormone (GnIH), pyroglutamylated RFamide, luqin, all upstream regulators sexual reproduction. This identification functional characterization cnidarian peptide GPCR advances our sheds light on evolution neuropeptide-hormone systems.

Language: Английский

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Ancient origins of arthropod moulting pathway components

eLife, Journal Year: 2019, Volume and Issue: 8

Published: July 3, 2019

Ecdysis (moulting) is the defining character of Ecdysoza (arthropods, nematodes and related phyla). Despite superficial similarities, signalling cascade underlying moulting differs between Panarthropoda remaining ecdysozoans. Here, we reconstruct evolution major components ecdysis pathway. Its key elements evolved much earlier than previously thought are present in non-moulting lophotrochozoans deuterostomes. Eclosion hormone (EH) bursicon originated prior to cnidarian-bilaterian split, whereas ecdysis-triggering (ETH) crustacean cardioactive peptide (CCAP) bilaterian last common ancestor (LCA). Identification EH, CCAP Onychophora ETH Tardigrada suggests that pathway was panarthropod LCA. Trunk, an ancient extracellular molecule a well-established paralog insect prothoracicotropic (PTTH), non-bilaterian ctenophore Mnemiopsis leidyi. This constitutes first case with homology neuropeptide.

Language: Английский

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Nemertean, Brachiopod, and Phoronid Neuropeptidomics Reveals Ancestral Spiralian Signaling Systems

Molecular Biology and Evolution, Journal Year: 2021, Volume and Issue: 38(11), P. 4847 - 4866

Published: July 16, 2021

Neuropeptides are diverse signaling molecules in animals commonly acting through G-protein coupled receptors (GPCRs). and their underwent extensive diversification bilaterians the relationships of many peptide-receptor systems have been clarified. However, we lack a detailed picture neuropeptide evolution lophotrochozoans as in-depth studies only exist for mollusks annelids. Here, analyze peptidergic Nemertea, Brachiopoda, Phoronida. We screened transcriptomes from 13 nemertean, 6 brachiopod, 4 phoronid species proneuropeptides GPCRs. With mass spectrometry nemertean Lineus longissimus, validated several predicted peptides identified novel ones. Molecular phylogeny combined with peptide-sequence gene-structure comparisons allowed us to comprehensively map spiralian evolution. found most mollusk annelid also nemerteans, brachiopods, phoronids. uncovered previously hidden including orthologies CCWamides arthropod agatoxin-like APGWamides RGWamides annelids, ortholog that pleurin neuropeptides present nemerteans brachiopods. cases gene family duplications losses. These include protostome-specific expansion RFamide/Wamide signaling, GnRH-related peptides, vasopressin/oxytocin before divergence phoronids, nemerteans. This analysis expands our knowledge spiralians other protostomes. Our annotated data set nearly 1,300 proneuropeptide sequences 600 GPCRs presents useful resource further signaling.

Language: Английский

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Single-cell atlases of two lophotrochozoan larvae highlight their complex evolutionary histories

Science Advances, Journal Year: 2023, Volume and Issue: 9(31)

Published: Aug. 2, 2023

Pelagic larval stages are widespread across animals, yet it is unclear whether larvae were present in the last common ancestor of animals or they evolved multiple times due to selective pressures. Many marine at least superficially similar; small, swim through beating bands cilia, and sense environment with an apical organ. To understand these similarities, we have generated single-cell atlases for from two animal phyla compared their cell types. We found clear similarities among ciliary band cells between neurons organ pointing possible homology structures, suggesting a single origin within Spiralia. also find several clade-specific innovations each larva, including distinct myocytes shell gland oyster larva. Oyster express many recently genes that made previous gene age estimates trochophore too young.

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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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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