Pacific-Ciguatoxin-2 and Brevetoxin-1 Induce the Sensitization of Sensory Receptors Mediating Pain and Pruritus in Sensory Neurons
Ciguatera fish poisoning (CFP) and neurotoxic shellfish poisoning syndromes are induced by the consumption of seafood contaminated by ciguatoxins and brevetoxins. Both toxins cause sensory symptoms such as paresthesia, cold dysesthesia and painful disorders. An intense pruritus, which may become chr...
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MDPI AG
2021-07-01
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author | Ophélie Pierre Maxime Fouchard Nelig Le Goux Paul Buscaglia Raphaël Leschiera Richard J. Lewis Olivier Mignen Joachim W. Fluhr Laurent Misery Raphaële Le Garrec |
author_facet | Ophélie Pierre Maxime Fouchard Nelig Le Goux Paul Buscaglia Raphaël Leschiera Richard J. Lewis Olivier Mignen Joachim W. Fluhr Laurent Misery Raphaële Le Garrec |
author_sort | Ophélie Pierre |
collection | DOAJ |
description | Ciguatera fish poisoning (CFP) and neurotoxic shellfish poisoning syndromes are induced by the consumption of seafood contaminated by ciguatoxins and brevetoxins. Both toxins cause sensory symptoms such as paresthesia, cold dysesthesia and painful disorders. An intense pruritus, which may become chronic, occurs also in CFP. No curative treatment is available and the pathophysiology is not fully elucidated. Here we conducted single-cell calcium video-imaging experiments in sensory neurons from newborn rats to study in vitro the ability of Pacific-ciguatoxin-2 (P-CTX-2) and brevetoxin-1 (PbTx-1) to sensitize receptors and ion channels, (i.e., to increase the percentage of responding cells and/or the response amplitude to their pharmacological agonists). In addition, we studied the neurotrophin release in sensory neurons co-cultured with keratinocytes after exposure to P-CTX-2. Our results show that P-CTX-2 induced the sensitization of TRPA1, TRPV4, PAR2, MrgprC, MrgprA and TTX-r NaV channels in sensory neurons. P-CTX-2 increased the release of nerve growth factor and brain-derived neurotrophic factor in the co-culture supernatant, suggesting that those neurotrophins could contribute to the sensitization of the aforementioned receptors and channels. Our results suggest the potential role of sensitization of sensory receptors/ion channels in the induction or persistence of sensory disturbances in CFP syndrome. |
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publishDate | 2021-07-01 |
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series | Marine Drugs |
spelling | doaj.art-35ee68cc76944ba0b2951f546916e3c72023-11-22T04:14:11ZengMDPI AGMarine Drugs1660-33972021-07-0119738710.3390/md19070387Pacific-Ciguatoxin-2 and Brevetoxin-1 Induce the Sensitization of Sensory Receptors Mediating Pain and Pruritus in Sensory NeuronsOphélie Pierre0Maxime Fouchard1Nelig Le Goux2Paul Buscaglia3Raphaël Leschiera4Richard J. Lewis5Olivier Mignen6Joachim W. Fluhr7Laurent Misery8Raphaële Le Garrec9Laboratoire Interactions Epithéliums-Neurones (LIEN), University of Brest, EA4685, F-29200 Brest, FranceLaboratoire Interactions Epithéliums-Neurones (LIEN), University of Brest, EA4685, F-29200 Brest, FranceLymphocytes B et Autoimmunité, Faculty of Medicine and Health Sciences, University of Brest, Inserm, UMR1227, F-29200 Brest, FranceLymphocytes B et Autoimmunité, Faculty of Medicine and Health Sciences, University of Brest, Inserm, UMR1227, F-29200 Brest, FranceLaboratoire Interactions Epithéliums-Neurones (LIEN), University of Brest, EA4685, F-29200 Brest, FranceInstitute for Molecular Bioscience, The University of Queensland, St. Lucia, QLD 4072, AustraliaLymphocytes B et Autoimmunité, Faculty of Medicine and Health Sciences, University of Brest, Inserm, UMR1227, F-29200 Brest, FranceLaboratoire Interactions Epithéliums-Neurones (LIEN), University of Brest, EA4685, F-29200 Brest, FranceLaboratoire Interactions Epithéliums-Neurones (LIEN), University of Brest, EA4685, F-29200 Brest, FranceLaboratoire Interactions Epithéliums-Neurones (LIEN), University of Brest, EA4685, F-29200 Brest, FranceCiguatera fish poisoning (CFP) and neurotoxic shellfish poisoning syndromes are induced by the consumption of seafood contaminated by ciguatoxins and brevetoxins. Both toxins cause sensory symptoms such as paresthesia, cold dysesthesia and painful disorders. An intense pruritus, which may become chronic, occurs also in CFP. No curative treatment is available and the pathophysiology is not fully elucidated. Here we conducted single-cell calcium video-imaging experiments in sensory neurons from newborn rats to study in vitro the ability of Pacific-ciguatoxin-2 (P-CTX-2) and brevetoxin-1 (PbTx-1) to sensitize receptors and ion channels, (i.e., to increase the percentage of responding cells and/or the response amplitude to their pharmacological agonists). In addition, we studied the neurotrophin release in sensory neurons co-cultured with keratinocytes after exposure to P-CTX-2. Our results show that P-CTX-2 induced the sensitization of TRPA1, TRPV4, PAR2, MrgprC, MrgprA and TTX-r NaV channels in sensory neurons. P-CTX-2 increased the release of nerve growth factor and brain-derived neurotrophic factor in the co-culture supernatant, suggesting that those neurotrophins could contribute to the sensitization of the aforementioned receptors and channels. Our results suggest the potential role of sensitization of sensory receptors/ion channels in the induction or persistence of sensory disturbances in CFP syndrome.https://www.mdpi.com/1660-3397/19/7/387ciguatoxinciguatera fish poisoningbrevetoxinneurotoxic shellfish poisoningsensory disorderspruritus |
spellingShingle | Ophélie Pierre Maxime Fouchard Nelig Le Goux Paul Buscaglia Raphaël Leschiera Richard J. Lewis Olivier Mignen Joachim W. Fluhr Laurent Misery Raphaële Le Garrec Pacific-Ciguatoxin-2 and Brevetoxin-1 Induce the Sensitization of Sensory Receptors Mediating Pain and Pruritus in Sensory Neurons Marine Drugs ciguatoxin ciguatera fish poisoning brevetoxin neurotoxic shellfish poisoning sensory disorders pruritus |
title | Pacific-Ciguatoxin-2 and Brevetoxin-1 Induce the Sensitization of Sensory Receptors Mediating Pain and Pruritus in Sensory Neurons |
title_full | Pacific-Ciguatoxin-2 and Brevetoxin-1 Induce the Sensitization of Sensory Receptors Mediating Pain and Pruritus in Sensory Neurons |
title_fullStr | Pacific-Ciguatoxin-2 and Brevetoxin-1 Induce the Sensitization of Sensory Receptors Mediating Pain and Pruritus in Sensory Neurons |
title_full_unstemmed | Pacific-Ciguatoxin-2 and Brevetoxin-1 Induce the Sensitization of Sensory Receptors Mediating Pain and Pruritus in Sensory Neurons |
title_short | Pacific-Ciguatoxin-2 and Brevetoxin-1 Induce the Sensitization of Sensory Receptors Mediating Pain and Pruritus in Sensory Neurons |
title_sort | pacific ciguatoxin 2 and brevetoxin 1 induce the sensitization of sensory receptors mediating pain and pruritus in sensory neurons |
topic | ciguatoxin ciguatera fish poisoning brevetoxin neurotoxic shellfish poisoning sensory disorders pruritus |
url | https://www.mdpi.com/1660-3397/19/7/387 |
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