Nicotinic acetylcholine receptors in the synganglion of the tick Ixodes ricinus: Functional characterization using membrane microtransplantation

Nicotinic acetylcholine receptors are an important class of excitatory receptors in the central nervous system of arthropods. In the ticks Ixodes ricinus, the functional and pharmacological properties of nicotinic receptors located in their neurons are still unknown. The objective of this study was...

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Main Authors: Anaïs Le Mauff, Hamza Chouikh, Alison Cartereau, Claude L. Charvet, Cédric Neveu, Claude Rispe, Olivier Plantard, Emiliane Taillebois, Steeve H. Thany
Format: Article
Language:English
Published: Elsevier 2020-12-01
Series:International Journal for Parasitology: Drugs and Drug Resistance
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211320720300361
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spelling doaj-467d949aa231486faaf26ec095558c7f2020-12-17T04:48:09ZengElsevierInternational Journal for Parasitology: Drugs and Drug Resistance2211-32072020-12-0114144151Nicotinic acetylcholine receptors in the synganglion of the tick Ixodes ricinus: Functional characterization using membrane microtransplantationAnaïs Le Mauff0Hamza Chouikh1Alison Cartereau2Claude L. Charvet3Cédric Neveu4Claude Rispe5Olivier Plantard6Emiliane Taillebois7Steeve H. Thany8LBLGC USC INRAE 1328, Université d'Orléans, 1 rue de Chartres, 45067, Orléans, FranceLBLGC USC INRAE 1328, Université d'Orléans, 1 rue de Chartres, 45067, Orléans, FranceLBLGC USC INRAE 1328, Université d'Orléans, 1 rue de Chartres, 45067, Orléans, FranceINRAE, Oniris, BIOEPAR, 44307, Nantes, FranceINRAE, Oniris, BIOEPAR, 44307, Nantes, FranceINRAE, ISP, 37380, Nouzilly, FranceINRAE, ISP, 37380, Nouzilly, FranceLBLGC USC INRAE 1328, Université d'Orléans, 1 rue de Chartres, 45067, Orléans, FranceLBLGC USC INRAE 1328, Université d'Orléans, 1 rue de Chartres, 45067, Orléans, France; Corresponding author.Nicotinic acetylcholine receptors are an important class of excitatory receptors in the central nervous system of arthropods. In the ticks Ixodes ricinus, the functional and pharmacological properties of nicotinic receptors located in their neurons are still unknown. The objective of this study was to characterize the pharmacological properties of tick nicotinic receptors using membrane microtransplantation in Xenopus laevis oocytes and two-electrodes voltage clamp method. The membranes microtransplanted were extracted from the tick synganglion. We found that oocytes microtransplanted with tick synganglion membranes expressed nicotinic acetylcholine receptor subtypes which were activated by acetylcholine (1 mM) and nicotine (1 mM). Currents induced by pressure application of acetylcholine and nicotine were diminished by 10 nM α-bungarotoxin and methyllycaconitine, suggesting that they expressed two subtypes of nicotinic receptors, α-bungarotoxin-sensitive and -insensitive, respectively. In addition, we found that nicotine receptors expressed in the synganglion membranes were poorly sensitive to the neonicotinoid insecticides clothianidin (CLT), imidacloprid (IMI), acetamiprid (ACE) and thiamethoxam (TMX), in agreement with their lack of activity as acaricides. Interestingly, current amplitudes were strongly potentialized in the presence of 1 μM PNU-120596. CLT was more active as an agonist than IMI, TMX and ACE. Finally, we demonstrated that microtransplantation of purified membrane from the tick synganglion can be a valuable tool for the development and screening of compounds targeting tick nicotinic acetylcholine receptor subtypes.http://www.sciencedirect.com/science/article/pii/S2211320720300361TickIxodes ricinusSynganglion membraneMicrotransplantationNicotinic acetylcholine receptors
collection DOAJ
language English
format Article
sources DOAJ
author Anaïs Le Mauff
Hamza Chouikh
Alison Cartereau
Claude L. Charvet
Cédric Neveu
Claude Rispe
Olivier Plantard
Emiliane Taillebois
Steeve H. Thany
spellingShingle Anaïs Le Mauff
Hamza Chouikh
Alison Cartereau
Claude L. Charvet
Cédric Neveu
Claude Rispe
Olivier Plantard
Emiliane Taillebois
Steeve H. Thany
Nicotinic acetylcholine receptors in the synganglion of the tick Ixodes ricinus: Functional characterization using membrane microtransplantation
International Journal for Parasitology: Drugs and Drug Resistance
Tick
Ixodes ricinus
Synganglion membrane
Microtransplantation
Nicotinic acetylcholine receptors
author_facet Anaïs Le Mauff
Hamza Chouikh
Alison Cartereau
Claude L. Charvet
Cédric Neveu
Claude Rispe
Olivier Plantard
Emiliane Taillebois
Steeve H. Thany
author_sort Anaïs Le Mauff
title Nicotinic acetylcholine receptors in the synganglion of the tick Ixodes ricinus: Functional characterization using membrane microtransplantation
title_short Nicotinic acetylcholine receptors in the synganglion of the tick Ixodes ricinus: Functional characterization using membrane microtransplantation
title_full Nicotinic acetylcholine receptors in the synganglion of the tick Ixodes ricinus: Functional characterization using membrane microtransplantation
title_fullStr Nicotinic acetylcholine receptors in the synganglion of the tick Ixodes ricinus: Functional characterization using membrane microtransplantation
title_full_unstemmed Nicotinic acetylcholine receptors in the synganglion of the tick Ixodes ricinus: Functional characterization using membrane microtransplantation
title_sort nicotinic acetylcholine receptors in the synganglion of the tick ixodes ricinus: functional characterization using membrane microtransplantation
publisher Elsevier
series International Journal for Parasitology: Drugs and Drug Resistance
issn 2211-3207
publishDate 2020-12-01
description Nicotinic acetylcholine receptors are an important class of excitatory receptors in the central nervous system of arthropods. In the ticks Ixodes ricinus, the functional and pharmacological properties of nicotinic receptors located in their neurons are still unknown. The objective of this study was to characterize the pharmacological properties of tick nicotinic receptors using membrane microtransplantation in Xenopus laevis oocytes and two-electrodes voltage clamp method. The membranes microtransplanted were extracted from the tick synganglion. We found that oocytes microtransplanted with tick synganglion membranes expressed nicotinic acetylcholine receptor subtypes which were activated by acetylcholine (1 mM) and nicotine (1 mM). Currents induced by pressure application of acetylcholine and nicotine were diminished by 10 nM α-bungarotoxin and methyllycaconitine, suggesting that they expressed two subtypes of nicotinic receptors, α-bungarotoxin-sensitive and -insensitive, respectively. In addition, we found that nicotine receptors expressed in the synganglion membranes were poorly sensitive to the neonicotinoid insecticides clothianidin (CLT), imidacloprid (IMI), acetamiprid (ACE) and thiamethoxam (TMX), in agreement with their lack of activity as acaricides. Interestingly, current amplitudes were strongly potentialized in the presence of 1 μM PNU-120596. CLT was more active as an agonist than IMI, TMX and ACE. Finally, we demonstrated that microtransplantation of purified membrane from the tick synganglion can be a valuable tool for the development and screening of compounds targeting tick nicotinic acetylcholine receptor subtypes.
topic Tick
Ixodes ricinus
Synganglion membrane
Microtransplantation
Nicotinic acetylcholine receptors
url http://www.sciencedirect.com/science/article/pii/S2211320720300361
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