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...

Full description

Bibliographic Details
Main Authors: Ophélie Pierre, Maxime Fouchard, Nelig Le Goux, Paul Buscaglia, Raphaël Leschiera, Richard J. Lewis, Olivier Mignen, Joachim W. Fluhr, Laurent Misery, Raphaële Le Garrec
Format: Article
Language:English
Published: MDPI AG 2021-07-01
Series:Marine Drugs
Subjects:
Online Access:https://www.mdpi.com/1660-3397/19/7/387
_version_ 1797526709473378304
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.
first_indexed 2024-03-10T09:34:10Z
format Article
id doaj.art-35ee68cc76944ba0b2951f546916e3c7
institution Directory Open Access Journal
issn 1660-3397
language English
last_indexed 2024-03-10T09:34:10Z
publishDate 2021-07-01
publisher MDPI AG
record_format Article
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
work_keys_str_mv AT opheliepierre pacificciguatoxin2andbrevetoxin1inducethesensitizationofsensoryreceptorsmediatingpainandpruritusinsensoryneurons
AT maximefouchard pacificciguatoxin2andbrevetoxin1inducethesensitizationofsensoryreceptorsmediatingpainandpruritusinsensoryneurons
AT neliglegoux pacificciguatoxin2andbrevetoxin1inducethesensitizationofsensoryreceptorsmediatingpainandpruritusinsensoryneurons
AT paulbuscaglia pacificciguatoxin2andbrevetoxin1inducethesensitizationofsensoryreceptorsmediatingpainandpruritusinsensoryneurons
AT raphaelleschiera pacificciguatoxin2andbrevetoxin1inducethesensitizationofsensoryreceptorsmediatingpainandpruritusinsensoryneurons
AT richardjlewis pacificciguatoxin2andbrevetoxin1inducethesensitizationofsensoryreceptorsmediatingpainandpruritusinsensoryneurons
AT oliviermignen pacificciguatoxin2andbrevetoxin1inducethesensitizationofsensoryreceptorsmediatingpainandpruritusinsensoryneurons
AT joachimwfluhr pacificciguatoxin2andbrevetoxin1inducethesensitizationofsensoryreceptorsmediatingpainandpruritusinsensoryneurons
AT laurentmisery pacificciguatoxin2andbrevetoxin1inducethesensitizationofsensoryreceptorsmediatingpainandpruritusinsensoryneurons
AT raphaelelegarrec pacificciguatoxin2andbrevetoxin1inducethesensitizationofsensoryreceptorsmediatingpainandpruritusinsensoryneurons