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Evolution and comparative physiology of luqin-type neuropeptide signaling

Evolution and comparative physiology of luqin-type neuropeptide signaling
Evolution and comparative physiology of luqin-type neuropeptide signaling

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.

cardio-excitatory peptide, G-protein coupled receptors, luqin, neuropeptide evolution, RWamides, RYamides
1662-4548
Yañez-Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Elphick, Maurice R.
b4c8b4f9-bb5c-4a0a-bc9d-e941857d4800
Yañez-Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Elphick, Maurice R.
b4c8b4f9-bb5c-4a0a-bc9d-e941857d4800

Yañez-Guerra, Luis Alfonso and Elphick, Maurice R. (2020) Evolution and comparative physiology of luqin-type neuropeptide signaling. Frontiers in Neuroscience, 14, [130]. (doi:10.3389/fnins.2020.00130).

Record type: Review

Abstract

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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Accepted/In Press date: 31 January 2020
e-pub ahead of print date: 18 February 2020
Additional Information: Funding Information: we thank Michael Crossley (University of Sussex, United Kingdom), Marycruz Flores-Flores (Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Mexico), Marina Ezcurra (University of Kent, United Kingdom), and Ray Crundwell (Queen Mary University of London, United Kingdom) for providing copyright free photographs of Lymnaea stagnalis, Drosophila melanogaster, Caenorhabditis elegans, and Asterias rubens, respectively. Funding. LY-G was supported by a Leverhulme Trust grant (RPG-2016-353) and by a Ph.D. studentship awarded by the Mexican Council of Science and Technology (CONACyT studentship No. 418612) and Queen Mary University of London. ME was supported by grants from the Biotechnology and Biological Sciences Research Council (BB/M001644/1) and the Leverhulme Trust (RPG-2016-353).
Keywords: cardio-excitatory peptide, G-protein coupled receptors, luqin, neuropeptide evolution, RWamides, RYamides

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Local EPrints ID: 483984
URI: http://eprints.soton.ac.uk/id/eprint/483984
ISSN: 1662-4548
PURE UUID: a6495ff7-7b16-4254-af63-433c41f06087
ORCID for Luis Alfonso Yañez-Guerra: ORCID iD orcid.org/0000-0002-2523-1310

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Date deposited: 08 Nov 2023 18:14
Last modified: 18 Mar 2024 04:15

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Author: Luis Alfonso Yañez-Guerra ORCID iD
Author: Maurice R. Elphick

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