TRPA1 as a O2 sensor detects microenvironmental hypoxia in the mice anterior cingulate cortex

Abstract Transient receptor potential ankyrin 1 (TRPA1) is a member of the TRP channel family and is expressed in peripheral and central nervous systems. In the periphery, TRPA1 senses cold and pain. However, the functions of TRPA1 in the CNS are unclear. Here, we examined the roles of TRPA1 on neur...

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Main Authors: Ryo Kawabata, Shuji Shimoyama, Shinya Ueno, Ikuko Yao, Akiko Arata, Kohei Koga
Format: Article
Language:English
Published: Nature Portfolio 2023-02-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-29140-8
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author Ryo Kawabata
Shuji Shimoyama
Shinya Ueno
Ikuko Yao
Akiko Arata
Kohei Koga
author_facet Ryo Kawabata
Shuji Shimoyama
Shinya Ueno
Ikuko Yao
Akiko Arata
Kohei Koga
author_sort Ryo Kawabata
collection DOAJ
description Abstract Transient receptor potential ankyrin 1 (TRPA1) is a member of the TRP channel family and is expressed in peripheral and central nervous systems. In the periphery, TRPA1 senses cold and pain. However, the functions of TRPA1 in the CNS are unclear. Here, we examined the roles of TRPA1 on neural activity and synaptic transmission in layer II/III pyramidal neurons from mice anterior cingulate cortex (ACC) by whole-cell patch-clamp recordings. The activation of Cinnamaldehyde (CA), which is TRPA1 agonist produced inward currents and these were blocked by the TRPA1 antagonists. Furthermore, activating TRPA1 changed the properties of action potentials such as the firing rate, rise time and decay time. In contrast, stimulating TRPA1 did not alter the spontaneous synaptic transmission. Finally, we examined the functional role of TRPA1 on neurons in a hypoxic environment. We induced an acute hypoxia by substituting nitrogen (N2) gas for oxygen (O2) in the external solution. N2 produced biphasic effects that consisting of inward currents in the early phase and outward currents in the late phase. Importantly, blocking TRPA1 reduced inward currents, but not outward currents. In contrast, a KATP channel blocker completely inhibited outward currents. These results suggest that TRPA1 acts on postsynaptic neurons in the ACC as an acute O2 sensor.
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spelling doaj.art-99f0224416494579bb9d905765977a882023-03-22T11:06:46ZengNature PortfolioScientific Reports2045-23222023-02-0113111110.1038/s41598-023-29140-8TRPA1 as a O2 sensor detects microenvironmental hypoxia in the mice anterior cingulate cortexRyo Kawabata0Shuji Shimoyama1Shinya Ueno2Ikuko Yao3Akiko Arata4Kohei Koga5Department of Biomedical Chemistry major, Graduate School of Science and Technology, Kwansei Gakuin UniversityDepartment of Neurophysiology, Hirosaki University Graduate School of MedicineDepartment of Neurophysiology, Hirosaki University Graduate School of MedicineDepartment of Biomedical Chemistry major, Graduate School of Science and Technology, Kwansei Gakuin UniversityDepartment of Physiology, Hyogo Medical UniversityDepartment of Neurophysiology, Hyogo Medical UniversityAbstract Transient receptor potential ankyrin 1 (TRPA1) is a member of the TRP channel family and is expressed in peripheral and central nervous systems. In the periphery, TRPA1 senses cold and pain. However, the functions of TRPA1 in the CNS are unclear. Here, we examined the roles of TRPA1 on neural activity and synaptic transmission in layer II/III pyramidal neurons from mice anterior cingulate cortex (ACC) by whole-cell patch-clamp recordings. The activation of Cinnamaldehyde (CA), which is TRPA1 agonist produced inward currents and these were blocked by the TRPA1 antagonists. Furthermore, activating TRPA1 changed the properties of action potentials such as the firing rate, rise time and decay time. In contrast, stimulating TRPA1 did not alter the spontaneous synaptic transmission. Finally, we examined the functional role of TRPA1 on neurons in a hypoxic environment. We induced an acute hypoxia by substituting nitrogen (N2) gas for oxygen (O2) in the external solution. N2 produced biphasic effects that consisting of inward currents in the early phase and outward currents in the late phase. Importantly, blocking TRPA1 reduced inward currents, but not outward currents. In contrast, a KATP channel blocker completely inhibited outward currents. These results suggest that TRPA1 acts on postsynaptic neurons in the ACC as an acute O2 sensor.https://doi.org/10.1038/s41598-023-29140-8
spellingShingle Ryo Kawabata
Shuji Shimoyama
Shinya Ueno
Ikuko Yao
Akiko Arata
Kohei Koga
TRPA1 as a O2 sensor detects microenvironmental hypoxia in the mice anterior cingulate cortex
Scientific Reports
title TRPA1 as a O2 sensor detects microenvironmental hypoxia in the mice anterior cingulate cortex
title_full TRPA1 as a O2 sensor detects microenvironmental hypoxia in the mice anterior cingulate cortex
title_fullStr TRPA1 as a O2 sensor detects microenvironmental hypoxia in the mice anterior cingulate cortex
title_full_unstemmed TRPA1 as a O2 sensor detects microenvironmental hypoxia in the mice anterior cingulate cortex
title_short TRPA1 as a O2 sensor detects microenvironmental hypoxia in the mice anterior cingulate cortex
title_sort trpa1 as a o2 sensor detects microenvironmental hypoxia in the mice anterior cingulate cortex
url https://doi.org/10.1038/s41598-023-29140-8
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