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TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons

The transient receptor potential vanilloid 1 (TRPV1) channel is highly expressed in a subset of sensory neurons in the dorsal root ganglia (DRG) and trigeminal ganglia of experimental animals, responsible for nociception. Many researches have revealed that some TRPV1-positive neurons co-express the...

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Autores principales: Masuoka, Takayoshi, Kudo, Makiko, Yamashita, Yuka, Yoshida, Junko, Imaizumi, Noriko, Muramatsu, Ikunobu, Nishio, Matomo, Ishibashi, Takaharu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5413491/
https://www.ncbi.nlm.nih.gov/pubmed/28515697
http://dx.doi.org/10.3389/fphys.2017.00272
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author Masuoka, Takayoshi
Kudo, Makiko
Yamashita, Yuka
Yoshida, Junko
Imaizumi, Noriko
Muramatsu, Ikunobu
Nishio, Matomo
Ishibashi, Takaharu
author_facet Masuoka, Takayoshi
Kudo, Makiko
Yamashita, Yuka
Yoshida, Junko
Imaizumi, Noriko
Muramatsu, Ikunobu
Nishio, Matomo
Ishibashi, Takaharu
author_sort Masuoka, Takayoshi
collection PubMed
description The transient receptor potential vanilloid 1 (TRPV1) channel is highly expressed in a subset of sensory neurons in the dorsal root ganglia (DRG) and trigeminal ganglia of experimental animals, responsible for nociception. Many researches have revealed that some TRPV1-positive neurons co-express the transient receptor potential ankyrin 1 (TRPA1) channel whose activities are closely modulated by TRPV1 channel. However, it is less investigated whether the activities of TRPV1 channel are modulated by the presence of TRPA1 channel in primary sensory neurons. This study clarified the difference in electrophysiological responses induced by TRPV1 channel activation between TRPA1-positive and TRPA1-negative DRG. TRPV1 and TRPA1 channel activations were evoked by capsaicin (1 μM), a TRPV1 agonist, and allyl isothiocyanate (AITC; 500 μM), a TRPA1 agonist, respectively. Capsaicin perfusion for 15 s caused a large inward current without a desensitization phase at a membrane potential of −70 mV in AITC-insensitive DRG (current density; 29.6 ± 5.6 pA/pF, time constant of decay; 12.8 ± 1.8 s). The capsaicin-induced currents in AITC-sensitive DRG had a small current density (12.7 ± 2.9 pA/pF) with a large time constant of decay (24.3 ± 5.4 s). In calcium imaging with Fura-2, the peak response by capsaicin was small and duration reaching the peak response was long in AITC-sensitive neurons. These electrophysiological differences were completely eliminated by HC-030031, a TRPA1 antagonist, in an extracellular solution or 10 mM EGTA, a Ca(2+) chelator, in an internal solution. Capsaicin perfusion for 120 s desensitized the inward currents after a transient peak. The decay during capsaicin perfusion was notably slow in AITC-sensitive DRG; ratio of capsaicin-induced current 60 s after the treatment per the peak current in AITC-sensitive neurons (78 ± 9%) was larger than that in AITC-insensitive neurons (48 ± 5%). The capsaicin-induced current in the desensitization phase was attenuated by HC-030031 in AITC-insensitive DRG. These results indicate that (1) TRPV1-mediated currents in TRPA1-positive neurons characterize small current densities with slow decay, which is caused by TRPA1 channel activities and intracellular Ca(2+) mobilization and (2) desensitization of TRPV1-mediated current in TRPA1-positive neurons is apparently slow, due to appending TRPA1-mediated current.
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spelling pubmed-54134912017-05-17 TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons Masuoka, Takayoshi Kudo, Makiko Yamashita, Yuka Yoshida, Junko Imaizumi, Noriko Muramatsu, Ikunobu Nishio, Matomo Ishibashi, Takaharu Front Physiol Physiology The transient receptor potential vanilloid 1 (TRPV1) channel is highly expressed in a subset of sensory neurons in the dorsal root ganglia (DRG) and trigeminal ganglia of experimental animals, responsible for nociception. Many researches have revealed that some TRPV1-positive neurons co-express the transient receptor potential ankyrin 1 (TRPA1) channel whose activities are closely modulated by TRPV1 channel. However, it is less investigated whether the activities of TRPV1 channel are modulated by the presence of TRPA1 channel in primary sensory neurons. This study clarified the difference in electrophysiological responses induced by TRPV1 channel activation between TRPA1-positive and TRPA1-negative DRG. TRPV1 and TRPA1 channel activations were evoked by capsaicin (1 μM), a TRPV1 agonist, and allyl isothiocyanate (AITC; 500 μM), a TRPA1 agonist, respectively. Capsaicin perfusion for 15 s caused a large inward current without a desensitization phase at a membrane potential of −70 mV in AITC-insensitive DRG (current density; 29.6 ± 5.6 pA/pF, time constant of decay; 12.8 ± 1.8 s). The capsaicin-induced currents in AITC-sensitive DRG had a small current density (12.7 ± 2.9 pA/pF) with a large time constant of decay (24.3 ± 5.4 s). In calcium imaging with Fura-2, the peak response by capsaicin was small and duration reaching the peak response was long in AITC-sensitive neurons. These electrophysiological differences were completely eliminated by HC-030031, a TRPA1 antagonist, in an extracellular solution or 10 mM EGTA, a Ca(2+) chelator, in an internal solution. Capsaicin perfusion for 120 s desensitized the inward currents after a transient peak. The decay during capsaicin perfusion was notably slow in AITC-sensitive DRG; ratio of capsaicin-induced current 60 s after the treatment per the peak current in AITC-sensitive neurons (78 ± 9%) was larger than that in AITC-insensitive neurons (48 ± 5%). The capsaicin-induced current in the desensitization phase was attenuated by HC-030031 in AITC-insensitive DRG. These results indicate that (1) TRPV1-mediated currents in TRPA1-positive neurons characterize small current densities with slow decay, which is caused by TRPA1 channel activities and intracellular Ca(2+) mobilization and (2) desensitization of TRPV1-mediated current in TRPA1-positive neurons is apparently slow, due to appending TRPA1-mediated current. Frontiers Media S.A. 2017-05-03 /pmc/articles/PMC5413491/ /pubmed/28515697 http://dx.doi.org/10.3389/fphys.2017.00272 Text en Copyright © 2017 Masuoka, Kudo, Yamashita, Yoshida, Imaizumi, Muramatsu, Nishio and Ishibashi. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Masuoka, Takayoshi
Kudo, Makiko
Yamashita, Yuka
Yoshida, Junko
Imaizumi, Noriko
Muramatsu, Ikunobu
Nishio, Matomo
Ishibashi, Takaharu
TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons
title TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons
title_full TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons
title_fullStr TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons
title_full_unstemmed TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons
title_short TRPA1 Channels Modify TRPV1-Mediated Current Responses in Dorsal Root Ganglion Neurons
title_sort trpa1 channels modify trpv1-mediated current responses in dorsal root ganglion neurons
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5413491/
https://www.ncbi.nlm.nih.gov/pubmed/28515697
http://dx.doi.org/10.3389/fphys.2017.00272
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