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Effects of Cooling Temperatures via Thermal K2P Channels on Regeneration of High-Frequency Action Potentials at Nodes of Ranvier of Rat Aβ-Afferent Nerves
Temperature-sensitive two-pore domain potassium channels (thermal K2P) are recently shown to cluster at nodes of Ranvier (NRs) and play a key role in action potential (AP) regeneration and conduction on Aβ-afferent nerves. Cooling temperatures affect AP regeneration and conduction on Aβ-afferent ner...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Society for Neuroscience
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8445039/ https://www.ncbi.nlm.nih.gov/pubmed/34462308 http://dx.doi.org/10.1523/ENEURO.0308-21.2021 |
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author | Kanda, Hirosato Tonomura, Sotatsu Gu, Jianguo G. |
author_facet | Kanda, Hirosato Tonomura, Sotatsu Gu, Jianguo G. |
author_sort | Kanda, Hirosato |
collection | PubMed |
description | Temperature-sensitive two-pore domain potassium channels (thermal K2P) are recently shown to cluster at nodes of Ranvier (NRs) and play a key role in action potential (AP) regeneration and conduction on Aβ-afferent nerves. Cooling temperatures affect AP regeneration and conduction on Aβ-afferent nerves but the underlying mechanisms are not completely understood. Here, we have performed patch-clamp recordings directly at the NR in an ex vivo trigeminal nerve preparation. We have characterized the effects of cooling temperatures on intrinsic electrophysiological properties and AP regeneration at the NR on rat Aβ-afferent nerves, and determined whether and how thermal K2P channels may be involved in the effects of cooling temperatures. We show that cooling temperatures from 35°C to 15°C decrease outward leak currents, increase input resistance, depolarize resting membrane potential (RMP), broaden AP width and increase latency of AP threshold at the NR. We further demonstrate that cooling temperatures impair regeneration of high-frequency AP trains at the NR. The effects of cooling temperatures on the intrinsic electrophysiological properties and regeneration of high-frequency AP trains at the NR can be partially reversed by BL-1249 (BL), arachidonic acid (AA), and intra-axonal protons, three thermal K2P activators, indicating the involvement of thermal K2P channels. Moreover, we show that at cooling temperatures there are interplays among thermal K2P channels, RMPs, and voltage-gated Na(+) channels, which together limit regeneration of high-frequency AP trains at the NR. Our findings demonstrate a new role of thermal K2P channels in temperature-dependent conduction of high-frequency sensory signals. |
format | Online Article Text |
id | pubmed-8445039 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Society for Neuroscience |
record_format | MEDLINE/PubMed |
spelling | pubmed-84450392021-09-20 Effects of Cooling Temperatures via Thermal K2P Channels on Regeneration of High-Frequency Action Potentials at Nodes of Ranvier of Rat Aβ-Afferent Nerves Kanda, Hirosato Tonomura, Sotatsu Gu, Jianguo G. eNeuro Research Article: New Research Temperature-sensitive two-pore domain potassium channels (thermal K2P) are recently shown to cluster at nodes of Ranvier (NRs) and play a key role in action potential (AP) regeneration and conduction on Aβ-afferent nerves. Cooling temperatures affect AP regeneration and conduction on Aβ-afferent nerves but the underlying mechanisms are not completely understood. Here, we have performed patch-clamp recordings directly at the NR in an ex vivo trigeminal nerve preparation. We have characterized the effects of cooling temperatures on intrinsic electrophysiological properties and AP regeneration at the NR on rat Aβ-afferent nerves, and determined whether and how thermal K2P channels may be involved in the effects of cooling temperatures. We show that cooling temperatures from 35°C to 15°C decrease outward leak currents, increase input resistance, depolarize resting membrane potential (RMP), broaden AP width and increase latency of AP threshold at the NR. We further demonstrate that cooling temperatures impair regeneration of high-frequency AP trains at the NR. The effects of cooling temperatures on the intrinsic electrophysiological properties and regeneration of high-frequency AP trains at the NR can be partially reversed by BL-1249 (BL), arachidonic acid (AA), and intra-axonal protons, three thermal K2P activators, indicating the involvement of thermal K2P channels. Moreover, we show that at cooling temperatures there are interplays among thermal K2P channels, RMPs, and voltage-gated Na(+) channels, which together limit regeneration of high-frequency AP trains at the NR. Our findings demonstrate a new role of thermal K2P channels in temperature-dependent conduction of high-frequency sensory signals. Society for Neuroscience 2021-09-15 /pmc/articles/PMC8445039/ /pubmed/34462308 http://dx.doi.org/10.1523/ENEURO.0308-21.2021 Text en Copyright © 2021 Kanda et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. |
spellingShingle | Research Article: New Research Kanda, Hirosato Tonomura, Sotatsu Gu, Jianguo G. Effects of Cooling Temperatures via Thermal K2P Channels on Regeneration of High-Frequency Action Potentials at Nodes of Ranvier of Rat Aβ-Afferent Nerves |
title | Effects of Cooling Temperatures via Thermal K2P Channels on Regeneration of High-Frequency Action Potentials at Nodes of Ranvier of Rat Aβ-Afferent Nerves |
title_full | Effects of Cooling Temperatures via Thermal K2P Channels on Regeneration of High-Frequency Action Potentials at Nodes of Ranvier of Rat Aβ-Afferent Nerves |
title_fullStr | Effects of Cooling Temperatures via Thermal K2P Channels on Regeneration of High-Frequency Action Potentials at Nodes of Ranvier of Rat Aβ-Afferent Nerves |
title_full_unstemmed | Effects of Cooling Temperatures via Thermal K2P Channels on Regeneration of High-Frequency Action Potentials at Nodes of Ranvier of Rat Aβ-Afferent Nerves |
title_short | Effects of Cooling Temperatures via Thermal K2P Channels on Regeneration of High-Frequency Action Potentials at Nodes of Ranvier of Rat Aβ-Afferent Nerves |
title_sort | effects of cooling temperatures via thermal k2p channels on regeneration of high-frequency action potentials at nodes of ranvier of rat aβ-afferent nerves |
topic | Research Article: New Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8445039/ https://www.ncbi.nlm.nih.gov/pubmed/34462308 http://dx.doi.org/10.1523/ENEURO.0308-21.2021 |
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