Cargando…

The Caenorhabditis elegans DEG-3/DES-2 Channel Is a Betaine-Gated Receptor Insensitive to Monepantel

Natural plant compounds, such as betaine, are described to have nematocidal properties. Betaine also acts as a neurotransmitter in the free-living model nematode Caenorhabditis elegans, where it is required for normal motility. Worm motility is mediated by nicotinic acetylcholine receptors (nAChRs),...

Descripción completa

Detalles Bibliográficos
Autores principales: Hansen, Tina V. A., Sager, Heinz, Toutain, Céline E., Courtot, Elise, Neveu, Cédric, Charvet, Claude L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8747062/
https://www.ncbi.nlm.nih.gov/pubmed/35011544
http://dx.doi.org/10.3390/molecules27010312
_version_ 1784630740014596096
author Hansen, Tina V. A.
Sager, Heinz
Toutain, Céline E.
Courtot, Elise
Neveu, Cédric
Charvet, Claude L.
author_facet Hansen, Tina V. A.
Sager, Heinz
Toutain, Céline E.
Courtot, Elise
Neveu, Cédric
Charvet, Claude L.
author_sort Hansen, Tina V. A.
collection PubMed
description Natural plant compounds, such as betaine, are described to have nematocidal properties. Betaine also acts as a neurotransmitter in the free-living model nematode Caenorhabditis elegans, where it is required for normal motility. Worm motility is mediated by nicotinic acetylcholine receptors (nAChRs), including subunits from the nematode-specific DEG-3 group. Not all types of nAChRs in this group are associated with motility, and one of these is the DEG-3/DES-2 channel from C. elegans, which is involved in nociception and possibly chemotaxis. Interestingly, the activity of DEG-3/DES-2 channel from the parasitic nematode of ruminants, Haemonchus contortus, is modulated by monepantel and its sulfone metabolite, which belong to the amino-acetonitrile derivative anthelmintic drug class. Here, our aim was to advance the pharmacological knowledge of the DEG-3/DES-2 channel from C. elegans by functionally expressing the DEG-3/DES-2 channel in Xenopus laevis oocytes and using two-electrode voltage-clamp electrophysiology. We found that the DEG-3/DES-2 channel was more sensitive to betaine than ACh and choline, but insensitive to monepantel and monepantel sulfone when used as direct agonists and as allosteric modulators in co-application with betaine. These findings provide important insight into the pharmacology of DEG-3/DES-2 from C. elegans and highlight the pharmacological differences between non-parasitic and parasitic nematode species.
format Online
Article
Text
id pubmed-8747062
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-87470622022-01-11 The Caenorhabditis elegans DEG-3/DES-2 Channel Is a Betaine-Gated Receptor Insensitive to Monepantel Hansen, Tina V. A. Sager, Heinz Toutain, Céline E. Courtot, Elise Neveu, Cédric Charvet, Claude L. Molecules Communication Natural plant compounds, such as betaine, are described to have nematocidal properties. Betaine also acts as a neurotransmitter in the free-living model nematode Caenorhabditis elegans, where it is required for normal motility. Worm motility is mediated by nicotinic acetylcholine receptors (nAChRs), including subunits from the nematode-specific DEG-3 group. Not all types of nAChRs in this group are associated with motility, and one of these is the DEG-3/DES-2 channel from C. elegans, which is involved in nociception and possibly chemotaxis. Interestingly, the activity of DEG-3/DES-2 channel from the parasitic nematode of ruminants, Haemonchus contortus, is modulated by monepantel and its sulfone metabolite, which belong to the amino-acetonitrile derivative anthelmintic drug class. Here, our aim was to advance the pharmacological knowledge of the DEG-3/DES-2 channel from C. elegans by functionally expressing the DEG-3/DES-2 channel in Xenopus laevis oocytes and using two-electrode voltage-clamp electrophysiology. We found that the DEG-3/DES-2 channel was more sensitive to betaine than ACh and choline, but insensitive to monepantel and monepantel sulfone when used as direct agonists and as allosteric modulators in co-application with betaine. These findings provide important insight into the pharmacology of DEG-3/DES-2 from C. elegans and highlight the pharmacological differences between non-parasitic and parasitic nematode species. MDPI 2022-01-05 /pmc/articles/PMC8747062/ /pubmed/35011544 http://dx.doi.org/10.3390/molecules27010312 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Communication
Hansen, Tina V. A.
Sager, Heinz
Toutain, Céline E.
Courtot, Elise
Neveu, Cédric
Charvet, Claude L.
The Caenorhabditis elegans DEG-3/DES-2 Channel Is a Betaine-Gated Receptor Insensitive to Monepantel
title The Caenorhabditis elegans DEG-3/DES-2 Channel Is a Betaine-Gated Receptor Insensitive to Monepantel
title_full The Caenorhabditis elegans DEG-3/DES-2 Channel Is a Betaine-Gated Receptor Insensitive to Monepantel
title_fullStr The Caenorhabditis elegans DEG-3/DES-2 Channel Is a Betaine-Gated Receptor Insensitive to Monepantel
title_full_unstemmed The Caenorhabditis elegans DEG-3/DES-2 Channel Is a Betaine-Gated Receptor Insensitive to Monepantel
title_short The Caenorhabditis elegans DEG-3/DES-2 Channel Is a Betaine-Gated Receptor Insensitive to Monepantel
title_sort caenorhabditis elegans deg-3/des-2 channel is a betaine-gated receptor insensitive to monepantel
topic Communication
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8747062/
https://www.ncbi.nlm.nih.gov/pubmed/35011544
http://dx.doi.org/10.3390/molecules27010312
work_keys_str_mv AT hansentinava thecaenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel
AT sagerheinz thecaenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel
AT toutaincelinee thecaenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel
AT courtotelise thecaenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel
AT neveucedric thecaenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel
AT charvetclaudel thecaenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel
AT hansentinava caenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel
AT sagerheinz caenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel
AT toutaincelinee caenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel
AT courtotelise caenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel
AT neveucedric caenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel
AT charvetclaudel caenorhabditiselegansdeg3des2channelisabetainegatedreceptorinsensitivetomonepantel