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

Tinoco, Ana B.; Barreiro‐Iglesias, Antón; Yáñez-Guerra, Luis Alfonso; Delroisse, Jérôme; Zhang, Ya; Gunner, Elizabeth F; Zampronio, Cleidiane G.; Jones, Alexandra M. E.; Egertová, Michaela; Elphick, Maurice R.

doi:10.7554/elife.65667

Cited by 26 publications

(42 citation statements)

References 139 publications

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“…The first invertebrate gene encoding a SK precursor was cloned in Drosophila in 1988, and can give rise to the peptides DSK1, DSK2 and DSK0 [70] and later two DSK receptors (CCKLR1 and CCKLR2) were identified and characterized [42,43]. Now CCK-type peptides have been identified in numerous invertebrate species of several bilaterian phyla, including the protostome phyla nematodes, mollusks, nemerteans, brachiopods, phoronids, annelids, tardigrades and arthropods [13-15, 24-31, 71-73], as well as in deuterostome invertebrates such as echinoderms and invertebrate chordates [32,33]. Examples of SK sequences from different taxa are shown in Fig.…”

Section: Structure Of Invertebrate Sk Precursors and Peptidesmentioning

confidence: 99%

“…Peptide injection Inhibits feeding and triggers stomach retraction [32] Crassostrea gigas (oyster) In vitro assay Inhibits contractions in hindgut f [71] Pecten maximus (scallop) Peptide injection Stimulates release of α-amylase [136] C. elegans Genetic manipulation Modulates food-related behavior [27] In general, the cellular SK peptide expression in the nervous system is conserved among studied insects, but the distribution in other arthropods has not been described in detail. Thus, it is hard to make wide comparisons even among the arthropod taxa.…”

Section: Homarus Americanus (Lobster)mentioning

confidence: 99%

“…CCK signaling components have been identified in vertebrates and in several bilaterian invertebrate phyla [13][14][15][24][25][26][27][28][29][30][31], as well as in deuterostome invertebrates such as echinoderms and invertebrate chordates (the latter also known as protochordates) [32,33]. In mammals, CCK activity was first discovered in tissue already in 1906 [34] and CCK was isolated as a gut hormone in 1928 [35].…”

Section: Introductionmentioning

confidence: 99%

“…However, CCK-type peptides have not been found in non-bilaterians such as Porifera, Placozoa, Cnidaria, or Ctenophora (see [13][14][15]). After the identification of two SK receptors in Drosophila [42,43], numerous invertebrate SK receptors are now known that display homologies to those of gastrin and CCK receptors in vertebrates (see [20,32]). Signaling with CCK-type peptides has been assayed in multiple invertebrates and in this review we highlight the structure, distribution and functions of these peptides and their receptors, with some more detailed analysis in Drosophila and with comparisons to mammals.…”

Section: Introductionmentioning

confidence: 99%

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

Nässel

2022

Cell. Mol. Life Sci.

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

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Section: Structure Of Invertebrate Sk Precursors and Peptidesmentioning

confidence: 99%

Section: Homarus Americanus (Lobster)mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Nässel

2022

Cell. Mol. Life Sci.

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“…In humans, CCK signaling has been implicated in nocebo hyperalgesia, mediated by the descending nociceptive control system 15 . The CCK system is very well-conserved and has been implicated in several common physiological functions among bilaterian species [16][17][18][19][20] . However, whether CCK is functionally involved in regulating nociception outside of mammals remains unknown.…”

Section: Introductionmentioning

confidence: 99%

A descending inhibitory mechanism of nociception mediated by an evolutionarily conserved neuropeptide system inDrosophila

Oikawa

Kondo

Hashimoto

et al. 2022

Preprint

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Nociception is a neural process that animals have developed to avoid potentially tissue-damaging stimuli. While nociception is triggered in the peripheral nervous system, its modulation by the central nervous system is a critical process in mammals, whose dysfunction has been extensively implicated in chronic pain pathogenesis. The peripheral mechanisms of nociception are largely conserved across the animal kingdom. However, it is unclear whether the brain-mediated modulation is also conserved in non-mammalian species. Here, we show that Drosophila has a descending inhibitory mechanism of nociception from the brain, mediated by the neuropeptide Drosulfakinin (DSK), a homolog of cholecystokinin (CCK) that plays an important role in the descending control of nociception in mammals. We found that mutants lacking dsk or its receptors are hypersensitive to noxious heat. Through a combination of genetic, behavioral, histological, and Ca2+ imaging analyses, we subsequently revealed neurons involved in DSK-mediated nociceptive regulation at a single-cell resolution and identified a DSKergic descending pathway that inhibits nociception. This study provides the first evidence for a descending modulatory mechanism of nociception from the brain in a non-mammalian species that is mediated by the evolutionarily conserved CCK system, raising the possibility that the descending inhibition is an ancient mechanism to regulate nociception.

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Localization of relaxin‐like gonad‐stimulating peptide expression in starfish reveals the gonoducts as a source for its role as a regulator of spawning

González

Lin

et al. 2023

J of Comparative Neurology

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Oocyte maturation and gamete release (spawning) in starfish are triggered by relaxin‐like gonad‐stimulating peptide (RGP), a neuropeptide that was first isolated from the radial nerve cords of these animals. Hitherto, it has generally been assumed that the radial nerve cords are the source of RGP that triggers spawning physiologically. To investigate other sources of RGP, here we report the first comprehensive anatomical analysis of its expression, using both in situ hybridization and immunohistochemistry to map RGP precursor transcripts and RGP, respectively, in the starfish Asterias rubens. Cells expressing RGP precursor transcripts were revealed in the ectoneural epithelium of the radial nerve cords and circumoral nerve ring, arm tips, tube feet, cardiac stomach, pyloric stomach, and, most notably, gonoducts. Using specific antibodies to A. rubens RGP, immunostaining was revealed in cells and/or fibers in the ectoneural region of the radial nerve cords and circumoral nerve ring, tube feet, terminal tentacle and other arm tip‐associated structures, body wall, peristomial membrane, esophagus, cardiac stomach, pyloric stomach, pyloric caeca, and gonoducts. Our discovery that RGP is expressed in the gonoducts of A. rubens proximal to its gonadotropic site of action in the gonads is important because it provides a new perspective on how RGP may act as a gonadotropin in starfish. Thus, we hypothesize that it is the release of RGP from the gonoducts that triggers gamete maturation and spawning in starfish, while RGP produced in other parts of the body may regulate other physiological/behavioral processes.

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

Cited by 26 publications

References 139 publications

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

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

A descending inhibitory mechanism of nociception mediated by an evolutionarily conserved neuropeptide system inDrosophila

Localization of relaxin‐like gonad‐stimulating peptide expression in starfish reveals the gonoducts as a source for its role as a regulator of spawning

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