Release of neuropeptides from a neuro-cutaneous co-culture model: A novel in vitro model for studying sensory effects of ciguatoxins.
Identifieur interne : 001826 ( Main/Exploration ); précédent : 001825; suivant : 001827Release of neuropeptides from a neuro-cutaneous co-culture model: A novel in vitro model for studying sensory effects of ciguatoxins.
Auteurs : Raphaele Le Garrec [France] ; Killian L'Herondelle [France] ; Christelle Le Gall-Ianotto [France] ; Nicolas Lebonvallet [France] ; Raphael Leschiera [France] ; Virginie Buhe [France] ; Matthieu Talagas [France] ; Irina Vetter [Australie] ; Richard J. Lewis [Australie] ; Laurent Misery [France]Source :
- Toxicon : official journal of the International Society on Toxinology [ 1879-3150 ] ; 2016.
Descripteurs français
- KwdFr :
- Animaux, Calcium (métabolisme), Cellules réceptrices sensorielles (), Cellules réceptrices sensorielles (cytologie), Ciguatera, Ciguatoxines (), Ciguatoxines (pharmacologie), Humains, Immunohistochimie, Kératinocytes (), Kératinocytes (cytologie), Modèles biologiques, Neuropeptide CGRP (métabolisme), Neuropeptides (métabolisme), Rats, Techniques de coculture.
- MESH :
- cytologie : Cellules réceptrices sensorielles, Kératinocytes.
- métabolisme : Calcium, Neuropeptide CGRP, Neuropeptides.
- pharmacologie : Ciguatoxines.
- Animaux, Cellules réceptrices sensorielles, Ciguatera, Ciguatoxines, Humains, Immunohistochimie, Kératinocytes, Modèles biologiques, Rats, Techniques de coculture.
English descriptors
- KwdEn :
- Animals, Calcitonin Gene-Related Peptide (metabolism), Calcium (metabolism), Ciguatera Poisoning, Ciguatoxins (chemistry), Ciguatoxins (pharmacology), Coculture Techniques, Humans, Immunohistochemistry, Keratinocytes (cytology), Keratinocytes (drug effects), Models, Biological, Neuropeptides (metabolism), Rats, Sensory Receptor Cells (cytology), Sensory Receptor Cells (drug effects).
- MESH :
- chemical , chemistry : Ciguatoxins.
- chemical , metabolism : Calcitonin Gene-Related Peptide, Calcium, Neuropeptides.
- chemical , pharmacology : Ciguatoxins.
- cytology : Keratinocytes, Sensory Receptor Cells.
- drug effects : Keratinocytes, Sensory Receptor Cells.
- Animals, Ciguatera Poisoning, Coculture Techniques, Humans, Immunohistochemistry, Models, Biological, Rats.
Abstract
Ciguatoxins are the major toxins responsible for ciguatera fish poisoning, a disease dominated by muco-cutaneous sensory disorders including paresthesiae, cold dysesthesia and pruritus. While the ciguatoxins are well known to target voltage-gated sodium channels (VGSCs), the ensuing molecular mechanisms underlying these sensory disorders remain poorly understood. In this study, we propose a primary sensory neuron-keratinocyte co-culture as an appropriate model to study the neuro-cutaneous effects of ciguatoxins. Using this model, we show for the first time that nanomolar concentrations of Pacific ciguatoxin-2 (P-CTX-2) induced a VGSC-dependent release of substance P (SP) and calcitonin gene-related peptide (CGRP). As these neuropeptides are known mediators of pain and itch sensations, the ciguatoxin-induced sensory disturbances in ciguatera fish poisoning may involve the release of these neuropeptides. We further determined time- and P-CTX-2 concentration-dependence of the release of SP and CGRP from the co-culture model. Moreover, we highlighted the influence of extracellular calcium on the release of neuropeptides elicited by P-CTX-2. These findings underline the usefulness of this novel in vitro model for studying the cellular and molecular mechanisms of the neuro-cutaneous effects of ciguatoxins, which may assist with identifying potential therapeutics for ciguatera fish poisoning.
DOI: 10.1016/j.toxicon.2015.11.004
PubMed: 26562445
Affiliations:
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Electronic address: rlegarrec@univ-brest.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Brest</settlement></placeName></affiliation></author><author><name sortKey="L Herondelle, Killian" sort="L Herondelle, Killian" uniqKey="L Herondelle K" first="Killian" last="L'Herondelle">Killian L'Herondelle</name><affiliation wicri:level="3"><nlm:affiliation>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Brest</settlement></placeName></affiliation></author><author><name sortKey="Le Gall Ianotto, Christelle" sort="Le Gall Ianotto, Christelle" uniqKey="Le Gall Ianotto C" first="Christelle" last="Le Gall-Ianotto">Christelle Le Gall-Ianotto</name><affiliation wicri:level="3"><nlm:affiliation>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Brest</settlement></placeName></affiliation></author><author><name sortKey="Lebonvallet, Nicolas" sort="Lebonvallet, Nicolas" uniqKey="Lebonvallet N" first="Nicolas" last="Lebonvallet">Nicolas Lebonvallet</name><affiliation wicri:level="3"><nlm:affiliation>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Brest</settlement></placeName></affiliation></author><author><name sortKey="Leschiera, Raphael" sort="Leschiera, Raphael" uniqKey="Leschiera R" first="Raphael" last="Leschiera">Raphael Leschiera</name><affiliation wicri:level="3"><nlm:affiliation>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Brest</settlement></placeName></affiliation></author><author><name sortKey="Buhe, Virginie" sort="Buhe, Virginie" uniqKey="Buhe V" first="Virginie" last="Buhe">Virginie Buhe</name><affiliation wicri:level="3"><nlm:affiliation>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Brest</settlement></placeName></affiliation></author><author><name sortKey="Talagas, Matthieu" sort="Talagas, Matthieu" uniqKey="Talagas M" first="Matthieu" last="Talagas">Matthieu Talagas</name><affiliation wicri:level="3"><nlm:affiliation>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest, France; Department of Pathology, University Hospital of Brest, 2 avenue Foch, 29200 Brest, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest, France; Department of Pathology, University Hospital of Brest, 2 avenue Foch, 29200 Brest</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Brest</settlement></placeName></affiliation></author><author><name sortKey="Vetter, Irina" sort="Vetter, Irina" uniqKey="Vetter I" first="Irina" last="Vetter">Irina Vetter</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Queensland 4072, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Queensland 4072</wicri:regionArea><wicri:noRegion>Queensland 4072</wicri:noRegion></affiliation></author><author><name sortKey="Lewis, Richard J" sort="Lewis, Richard J" uniqKey="Lewis R" first="Richard J" last="Lewis">Richard J. Lewis</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Queensland 4072, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Queensland 4072</wicri:regionArea><wicri:noRegion>Queensland 4072</wicri:noRegion></affiliation></author><author><name sortKey="Misery, Laurent" sort="Misery, Laurent" uniqKey="Misery L" first="Laurent" last="Misery">Laurent Misery</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest, France; Department of Dermatology, University Hospital of Brest, 2 avenue Foch, 29200 Brest, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratory of Neurosciences of Brest (EA4685), University of Western Brittany, 22 avenue Camille Desmoulins, 29200 Brest, France; Department of Dermatology, University Hospital of Brest, 2 avenue Foch, 29200 Brest</wicri:regionArea><wicri:noRegion>29200 Brest</wicri:noRegion><wicri:noRegion>29200 Brest</wicri:noRegion></affiliation></author></analytic><series><title level="j">Toxicon : official journal of the International Society on Toxinology</title><idno type="eISSN">1879-3150</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Calcitonin Gene-Related Peptide (metabolism)</term><term>Calcium (metabolism)</term><term>Ciguatera Poisoning</term><term>Ciguatoxins (chemistry)</term><term>Ciguatoxins (pharmacology)</term><term>Coculture Techniques</term><term>Humans</term><term>Immunohistochemistry</term><term>Keratinocytes (cytology)</term><term>Keratinocytes (drug effects)</term><term>Models, Biological</term><term>Neuropeptides (metabolism)</term><term>Rats</term><term>Sensory Receptor Cells (cytology)</term><term>Sensory Receptor Cells (drug effects)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animaux</term><term>Calcium (métabolisme)</term><term>Cellules réceptrices sensorielles ()</term><term>Cellules réceptrices sensorielles (cytologie)</term><term>Ciguatera</term><term>Ciguatoxines ()</term><term>Ciguatoxines (pharmacologie)</term><term>Humains</term><term>Immunohistochimie</term><term>Kératinocytes ()</term><term>Kératinocytes (cytologie)</term><term>Modèles biologiques</term><term>Neuropeptide CGRP (métabolisme)</term><term>Neuropeptides (métabolisme)</term><term>Rats</term><term>Techniques de coculture</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Ciguatoxins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Calcitonin Gene-Related Peptide</term><term>Calcium</term><term>Neuropeptides</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Ciguatoxins</term></keywords><keywords scheme="MESH" qualifier="cytologie" xml:lang="fr"><term>Cellules réceptrices sensorielles</term><term>Kératinocytes</term></keywords><keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Keratinocytes</term><term>Sensory Receptor Cells</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Keratinocytes</term><term>Sensory Receptor Cells</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Calcium</term><term>Neuropeptide CGRP</term><term>Neuropeptides</term></keywords><keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr"><term>Ciguatoxines</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Ciguatera Poisoning</term><term>Coculture Techniques</term><term>Humans</term><term>Immunohistochemistry</term><term>Models, Biological</term><term>Rats</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Cellules réceptrices sensorielles</term><term>Ciguatera</term><term>Ciguatoxines</term><term>Humains</term><term>Immunohistochimie</term><term>Kératinocytes</term><term>Modèles biologiques</term><term>Rats</term><term>Techniques de coculture</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Ciguatoxins are the major toxins responsible for ciguatera fish poisoning, a disease dominated by muco-cutaneous sensory disorders including paresthesiae, cold dysesthesia and pruritus. While the ciguatoxins are well known to target voltage-gated sodium channels (VGSCs), the ensuing molecular mechanisms underlying these sensory disorders remain poorly understood. In this study, we propose a primary sensory neuron-keratinocyte co-culture as an appropriate model to study the neuro-cutaneous effects of ciguatoxins. Using this model, we show for the first time that nanomolar concentrations of Pacific ciguatoxin-2 (P-CTX-2) induced a VGSC-dependent release of substance P (SP) and calcitonin gene-related peptide (CGRP). As these neuropeptides are known mediators of pain and itch sensations, the ciguatoxin-induced sensory disturbances in ciguatera fish poisoning may involve the release of these neuropeptides. We further determined time- and P-CTX-2 concentration-dependence of the release of SP and CGRP from the co-culture model. Moreover, we highlighted the influence of extracellular calcium on the release of neuropeptides elicited by P-CTX-2. These findings underline the usefulness of this novel in vitro model for studying the cellular and molecular mechanisms of the neuro-cutaneous effects of ciguatoxins, which may assist with identifying potential therapeutics for ciguatera fish poisoning.</div></front></TEI><affiliations><list><country><li>Australie</li><li>France</li></country><region><li>Région Bretagne</li></region><settlement><li>Brest</li></settlement></list><tree><country name="France"><region name="Région Bretagne"><name sortKey="Le Garrec, Raphaele" sort="Le Garrec, Raphaele" uniqKey="Le Garrec R" first="Raphaele" last="Le Garrec">Raphaele Le Garrec</name></region><name sortKey="Buhe, Virginie" sort="Buhe, Virginie" uniqKey="Buhe V" first="Virginie" last="Buhe">Virginie Buhe</name><name sortKey="L Herondelle, Killian" sort="L Herondelle, Killian" uniqKey="L Herondelle K" first="Killian" last="L'Herondelle">Killian L'Herondelle</name><name sortKey="Le Gall Ianotto, Christelle" sort="Le Gall Ianotto, Christelle" uniqKey="Le Gall Ianotto C" first="Christelle" last="Le Gall-Ianotto">Christelle Le Gall-Ianotto</name><name sortKey="Lebonvallet, Nicolas" sort="Lebonvallet, Nicolas" uniqKey="Lebonvallet N" first="Nicolas" last="Lebonvallet">Nicolas Lebonvallet</name><name sortKey="Leschiera, Raphael" sort="Leschiera, Raphael" uniqKey="Leschiera R" first="Raphael" last="Leschiera">Raphael Leschiera</name><name sortKey="Misery, Laurent" sort="Misery, Laurent" uniqKey="Misery L" first="Laurent" last="Misery">Laurent Misery</name><name sortKey="Talagas, Matthieu" sort="Talagas, Matthieu" uniqKey="Talagas M" first="Matthieu" last="Talagas">Matthieu Talagas</name></country><country name="Australie"><noRegion><name sortKey="Vetter, Irina" sort="Vetter, Irina" uniqKey="Vetter I" first="Irina" last="Vetter">Irina Vetter</name></noRegion><name sortKey="Lewis, Richard J" sort="Lewis, Richard J" uniqKey="Lewis R" first="Richard J" last="Lewis">Richard J. 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