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Tension Sensor Based on Fluorescence Resonance Energy Transfer Reveals Fiber Diameter-Dependent Mechanical Factors During Myelination

Oligodendrocytes (OLs) form a myelin sheath around neuronal axons to increase conduction velocity of action potential. Although both large and small diameter axons are intermingled in the central nervous system (CNS), the number of myelin wrapping is related to the axon diameter, such that the ratio...

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Autores principales: Shimizu, Takeshi, Murakoshi, Hideji, Matsumoto, Hidetoshi, Ichino, Kota, Hattori, Atsunori, Ueno, Shinya, Ishida, Akimasa, Tajiri, Naoki, Hida, Hideki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8364977/
https://www.ncbi.nlm.nih.gov/pubmed/34408628
http://dx.doi.org/10.3389/fncel.2021.685044
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author Shimizu, Takeshi
Murakoshi, Hideji
Matsumoto, Hidetoshi
Ichino, Kota
Hattori, Atsunori
Ueno, Shinya
Ishida, Akimasa
Tajiri, Naoki
Hida, Hideki
author_facet Shimizu, Takeshi
Murakoshi, Hideji
Matsumoto, Hidetoshi
Ichino, Kota
Hattori, Atsunori
Ueno, Shinya
Ishida, Akimasa
Tajiri, Naoki
Hida, Hideki
author_sort Shimizu, Takeshi
collection PubMed
description Oligodendrocytes (OLs) form a myelin sheath around neuronal axons to increase conduction velocity of action potential. Although both large and small diameter axons are intermingled in the central nervous system (CNS), the number of myelin wrapping is related to the axon diameter, such that the ratio of the diameter of the axon to that of the entire myelinated-axon unit is optimal for each axon, which is required for exerting higher brain functions. This indicates there are unknown axon diameter-dependent factors that control myelination. We tried to investigate physical factors to clarify the mechanisms underlying axon diameter-dependent myelination. To visualize OL-generating forces during myelination, a tension sensor based on fluorescence resonance energy transfer (FRET) was used. Polystyrene nanofibers with varying diameters similar to neuronal axons were prepared to investigate biophysical factors regulating the OL-axon interactions. We found that higher tension was generated at OL processes contacting larger diameter fibers compared with smaller diameter fibers. Additionally, OLs formed longer focal adhesions (FAs) on larger diameter axons and shorter FAs on smaller diameter axons. These results suggest that OLs respond to the fiber diameter and activate mechanotransduction initiated at FAs, which controls their cytoskeletal organization and myelin formation. This study leads to the novel and interesting idea that physical factors are involved in myelin formation in response to axon diameter.
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spelling pubmed-83649772021-08-17 Tension Sensor Based on Fluorescence Resonance Energy Transfer Reveals Fiber Diameter-Dependent Mechanical Factors During Myelination Shimizu, Takeshi Murakoshi, Hideji Matsumoto, Hidetoshi Ichino, Kota Hattori, Atsunori Ueno, Shinya Ishida, Akimasa Tajiri, Naoki Hida, Hideki Front Cell Neurosci Neuroscience Oligodendrocytes (OLs) form a myelin sheath around neuronal axons to increase conduction velocity of action potential. Although both large and small diameter axons are intermingled in the central nervous system (CNS), the number of myelin wrapping is related to the axon diameter, such that the ratio of the diameter of the axon to that of the entire myelinated-axon unit is optimal for each axon, which is required for exerting higher brain functions. This indicates there are unknown axon diameter-dependent factors that control myelination. We tried to investigate physical factors to clarify the mechanisms underlying axon diameter-dependent myelination. To visualize OL-generating forces during myelination, a tension sensor based on fluorescence resonance energy transfer (FRET) was used. Polystyrene nanofibers with varying diameters similar to neuronal axons were prepared to investigate biophysical factors regulating the OL-axon interactions. We found that higher tension was generated at OL processes contacting larger diameter fibers compared with smaller diameter fibers. Additionally, OLs formed longer focal adhesions (FAs) on larger diameter axons and shorter FAs on smaller diameter axons. These results suggest that OLs respond to the fiber diameter and activate mechanotransduction initiated at FAs, which controls their cytoskeletal organization and myelin formation. This study leads to the novel and interesting idea that physical factors are involved in myelin formation in response to axon diameter. Frontiers Media S.A. 2021-08-02 /pmc/articles/PMC8364977/ /pubmed/34408628 http://dx.doi.org/10.3389/fncel.2021.685044 Text en Copyright © 2021 Shimizu, Murakoshi, Matsumoto, Ichino, Hattori, Ueno, Ishida, Tajiri and Hida. 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
Shimizu, Takeshi
Murakoshi, Hideji
Matsumoto, Hidetoshi
Ichino, Kota
Hattori, Atsunori
Ueno, Shinya
Ishida, Akimasa
Tajiri, Naoki
Hida, Hideki
Tension Sensor Based on Fluorescence Resonance Energy Transfer Reveals Fiber Diameter-Dependent Mechanical Factors During Myelination
title Tension Sensor Based on Fluorescence Resonance Energy Transfer Reveals Fiber Diameter-Dependent Mechanical Factors During Myelination
title_full Tension Sensor Based on Fluorescence Resonance Energy Transfer Reveals Fiber Diameter-Dependent Mechanical Factors During Myelination
title_fullStr Tension Sensor Based on Fluorescence Resonance Energy Transfer Reveals Fiber Diameter-Dependent Mechanical Factors During Myelination
title_full_unstemmed Tension Sensor Based on Fluorescence Resonance Energy Transfer Reveals Fiber Diameter-Dependent Mechanical Factors During Myelination
title_short Tension Sensor Based on Fluorescence Resonance Energy Transfer Reveals Fiber Diameter-Dependent Mechanical Factors During Myelination
title_sort tension sensor based on fluorescence resonance energy transfer reveals fiber diameter-dependent mechanical factors during myelination
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8364977/
https://www.ncbi.nlm.nih.gov/pubmed/34408628
http://dx.doi.org/10.3389/fncel.2021.685044
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