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Circadian rhythm of PERIOD2::LUCIFERASE expression in the trigeminal ganglion of mice

INTRODUCTION: The trigeminal nerve conveys delicate sensations such as warmth, pain, and tactile pressure in the oral and facial regions, and most trigeminal afferent cell bodies are located in the trigeminal ganglion. Our previous study has shown that sensations in trigeminal nerve innervated areas...

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Autores principales: Shirakawa, Yukie, Ohno, Sachi N., Yamagata, Kanae A., Kuramoto, Eriko, Oda, Yoshiaki, Nakamura, Takahiro J., Nakamura, Wataru, Sugimura, Mitsutaka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10086191/
https://www.ncbi.nlm.nih.gov/pubmed/37056311
http://dx.doi.org/10.3389/fnins.2023.1142785
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author Shirakawa, Yukie
Ohno, Sachi N.
Yamagata, Kanae A.
Kuramoto, Eriko
Oda, Yoshiaki
Nakamura, Takahiro J.
Nakamura, Wataru
Sugimura, Mitsutaka
author_facet Shirakawa, Yukie
Ohno, Sachi N.
Yamagata, Kanae A.
Kuramoto, Eriko
Oda, Yoshiaki
Nakamura, Takahiro J.
Nakamura, Wataru
Sugimura, Mitsutaka
author_sort Shirakawa, Yukie
collection PubMed
description INTRODUCTION: The trigeminal nerve conveys delicate sensations such as warmth, pain, and tactile pressure in the oral and facial regions, and most trigeminal afferent cell bodies are located in the trigeminal ganglion. Our previous study has shown that sensations in trigeminal nerve innervated areas, specifically in the maxillofacial region, exhibit diurnal variation and that sensitivity changes time-dependently. In this study, we aimed to clarify the rhythm of expression of clock gene in the trigeminal ganglion of mice to elucidate the mechanism of circadian regulation in the same area. METHODS: Immunohistochemistry examined the expression of the PER2 protein in the suprachiasmatic nucleus and trigeminal ganglion of wild-type mice. To measure gene expression as bioluminescence, PERIOD2::LUCIFERASE knock-in (PER2::LUC) mice were used. Unilateral trigeminal ganglion and brain sections including the suprachiasmatic nucleus were incubated ex vivo. Bioluminescence levels were then measured using a highly sensitive photodetector. The same experiments were then conducted with Cry1 gene-deficient (Cry1(−/−)) or Cry2 gene-deficient (Cry2(−/−)) mice. RESULTS: In the trigeminal ganglion, immunohistochemistry localized PER2 protein expression within the neuronal cell body. Mouse trigeminal ganglion ex vivo tissues showed distinct circadian oscillations in PER2::LUC levels in all genotypes, wild-type, Cry1(−/−), and Cry2(−/−). The period was shorter in the trigeminal ganglion than in the suprachiasmatic nucleus; it was shorter in Cry1(−/−) and longer in Cry2(−/−) mice than in the wild-type mice. CONCLUSION: The expression of Per2 in neurons of the trigeminal ganglion in ex vivo culture and the oscillation in a distinct circadian rhythm suggests that the trigeminal ganglion is responsible for the relay of sensory inputs and temporal gating through autonomous circadian oscillations.
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spelling pubmed-100861912023-04-12 Circadian rhythm of PERIOD2::LUCIFERASE expression in the trigeminal ganglion of mice Shirakawa, Yukie Ohno, Sachi N. Yamagata, Kanae A. Kuramoto, Eriko Oda, Yoshiaki Nakamura, Takahiro J. Nakamura, Wataru Sugimura, Mitsutaka Front Neurosci Neuroscience INTRODUCTION: The trigeminal nerve conveys delicate sensations such as warmth, pain, and tactile pressure in the oral and facial regions, and most trigeminal afferent cell bodies are located in the trigeminal ganglion. Our previous study has shown that sensations in trigeminal nerve innervated areas, specifically in the maxillofacial region, exhibit diurnal variation and that sensitivity changes time-dependently. In this study, we aimed to clarify the rhythm of expression of clock gene in the trigeminal ganglion of mice to elucidate the mechanism of circadian regulation in the same area. METHODS: Immunohistochemistry examined the expression of the PER2 protein in the suprachiasmatic nucleus and trigeminal ganglion of wild-type mice. To measure gene expression as bioluminescence, PERIOD2::LUCIFERASE knock-in (PER2::LUC) mice were used. Unilateral trigeminal ganglion and brain sections including the suprachiasmatic nucleus were incubated ex vivo. Bioluminescence levels were then measured using a highly sensitive photodetector. The same experiments were then conducted with Cry1 gene-deficient (Cry1(−/−)) or Cry2 gene-deficient (Cry2(−/−)) mice. RESULTS: In the trigeminal ganglion, immunohistochemistry localized PER2 protein expression within the neuronal cell body. Mouse trigeminal ganglion ex vivo tissues showed distinct circadian oscillations in PER2::LUC levels in all genotypes, wild-type, Cry1(−/−), and Cry2(−/−). The period was shorter in the trigeminal ganglion than in the suprachiasmatic nucleus; it was shorter in Cry1(−/−) and longer in Cry2(−/−) mice than in the wild-type mice. CONCLUSION: The expression of Per2 in neurons of the trigeminal ganglion in ex vivo culture and the oscillation in a distinct circadian rhythm suggests that the trigeminal ganglion is responsible for the relay of sensory inputs and temporal gating through autonomous circadian oscillations. Frontiers Media S.A. 2023-03-28 /pmc/articles/PMC10086191/ /pubmed/37056311 http://dx.doi.org/10.3389/fnins.2023.1142785 Text en Copyright © 2023 Shirakawa, Ohno, Yamagata, Kuramoto, Oda, Nakamura, Nakamura and Sugimura. https://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) and the copyright owner(s) 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 Neuroscience
Shirakawa, Yukie
Ohno, Sachi N.
Yamagata, Kanae A.
Kuramoto, Eriko
Oda, Yoshiaki
Nakamura, Takahiro J.
Nakamura, Wataru
Sugimura, Mitsutaka
Circadian rhythm of PERIOD2::LUCIFERASE expression in the trigeminal ganglion of mice
title Circadian rhythm of PERIOD2::LUCIFERASE expression in the trigeminal ganglion of mice
title_full Circadian rhythm of PERIOD2::LUCIFERASE expression in the trigeminal ganglion of mice
title_fullStr Circadian rhythm of PERIOD2::LUCIFERASE expression in the trigeminal ganglion of mice
title_full_unstemmed Circadian rhythm of PERIOD2::LUCIFERASE expression in the trigeminal ganglion of mice
title_short Circadian rhythm of PERIOD2::LUCIFERASE expression in the trigeminal ganglion of mice
title_sort circadian rhythm of period2::luciferase expression in the trigeminal ganglion of mice
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10086191/
https://www.ncbi.nlm.nih.gov/pubmed/37056311
http://dx.doi.org/10.3389/fnins.2023.1142785
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