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Micromotion Derived Fluid Shear Stress Mediates Peri‐Electrode Gliosis through Mechanosensitive Ion Channels

The development of bioelectronic neural implant technologies has advanced significantly over the past 5 years, particularly in brain–machine interfaces and electronic medicine. However, neuroelectrode‐based therapies require invasive neurosurgery and can subject neural tissues to micromotion‐induced...

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Autores principales: Trotier, Alexandre, Bagnoli, Enrico, Walski, Tomasz, Evers, Judith, Pugliese, Eugenia, Lowery, Madeleine, Kilcoyne, Michelle, Fitzgerald, Una, Biggs, Manus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10520674/
https://www.ncbi.nlm.nih.gov/pubmed/37518828
http://dx.doi.org/10.1002/advs.202301352
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author Trotier, Alexandre
Bagnoli, Enrico
Walski, Tomasz
Evers, Judith
Pugliese, Eugenia
Lowery, Madeleine
Kilcoyne, Michelle
Fitzgerald, Una
Biggs, Manus
author_facet Trotier, Alexandre
Bagnoli, Enrico
Walski, Tomasz
Evers, Judith
Pugliese, Eugenia
Lowery, Madeleine
Kilcoyne, Michelle
Fitzgerald, Una
Biggs, Manus
author_sort Trotier, Alexandre
collection PubMed
description The development of bioelectronic neural implant technologies has advanced significantly over the past 5 years, particularly in brain–machine interfaces and electronic medicine. However, neuroelectrode‐based therapies require invasive neurosurgery and can subject neural tissues to micromotion‐induced mechanical shear, leading to chronic inflammation, the formation of a peri‐electrode void and the deposition of reactive glial scar tissue. These structures act as physical barriers, hindering electrical signal propagation and reducing neural implant functionality. Although well documented, the mechanisms behind the initiation and progression of these processes are poorly understood. Herein, in silico analysis of micromotion‐induced peri‐electrode void progression and gliosis is described. Subsequently, ventral mesencephalic cells exposed to milliscale fluid shear stress in vitro exhibited increased expression of gliosis‐associated proteins and overexpression of mechanosensitive ion channels PIEZO1 (piezo‐type mechanosensitive ion channel component 1) and TRPA1 (transient receptor potential ankyrin 1), effects further confirmed in vivo in a rat model of peri‐electrode gliosis. Furthermore, in vitro analysis indicates that chemical inhibition/activation of PIEZO1 affects fluid shear stress mediated astrocyte reactivity in a mitochondrial‐dependent manner. Together, the results suggest that mechanosensitive ion channels play a major role in the development of a peri‐electrode void and micromotion‐induced glial scarring at the peri‐electrode region.
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spelling pubmed-105206742023-09-27 Micromotion Derived Fluid Shear Stress Mediates Peri‐Electrode Gliosis through Mechanosensitive Ion Channels Trotier, Alexandre Bagnoli, Enrico Walski, Tomasz Evers, Judith Pugliese, Eugenia Lowery, Madeleine Kilcoyne, Michelle Fitzgerald, Una Biggs, Manus Adv Sci (Weinh) Research Articles The development of bioelectronic neural implant technologies has advanced significantly over the past 5 years, particularly in brain–machine interfaces and electronic medicine. However, neuroelectrode‐based therapies require invasive neurosurgery and can subject neural tissues to micromotion‐induced mechanical shear, leading to chronic inflammation, the formation of a peri‐electrode void and the deposition of reactive glial scar tissue. These structures act as physical barriers, hindering electrical signal propagation and reducing neural implant functionality. Although well documented, the mechanisms behind the initiation and progression of these processes are poorly understood. Herein, in silico analysis of micromotion‐induced peri‐electrode void progression and gliosis is described. Subsequently, ventral mesencephalic cells exposed to milliscale fluid shear stress in vitro exhibited increased expression of gliosis‐associated proteins and overexpression of mechanosensitive ion channels PIEZO1 (piezo‐type mechanosensitive ion channel component 1) and TRPA1 (transient receptor potential ankyrin 1), effects further confirmed in vivo in a rat model of peri‐electrode gliosis. Furthermore, in vitro analysis indicates that chemical inhibition/activation of PIEZO1 affects fluid shear stress mediated astrocyte reactivity in a mitochondrial‐dependent manner. Together, the results suggest that mechanosensitive ion channels play a major role in the development of a peri‐electrode void and micromotion‐induced glial scarring at the peri‐electrode region. John Wiley and Sons Inc. 2023-07-30 /pmc/articles/PMC10520674/ /pubmed/37518828 http://dx.doi.org/10.1002/advs.202301352 Text en © 2023 The Authors. Advanced Science published by Wiley‐VCH GmbH https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Trotier, Alexandre
Bagnoli, Enrico
Walski, Tomasz
Evers, Judith
Pugliese, Eugenia
Lowery, Madeleine
Kilcoyne, Michelle
Fitzgerald, Una
Biggs, Manus
Micromotion Derived Fluid Shear Stress Mediates Peri‐Electrode Gliosis through Mechanosensitive Ion Channels
title Micromotion Derived Fluid Shear Stress Mediates Peri‐Electrode Gliosis through Mechanosensitive Ion Channels
title_full Micromotion Derived Fluid Shear Stress Mediates Peri‐Electrode Gliosis through Mechanosensitive Ion Channels
title_fullStr Micromotion Derived Fluid Shear Stress Mediates Peri‐Electrode Gliosis through Mechanosensitive Ion Channels
title_full_unstemmed Micromotion Derived Fluid Shear Stress Mediates Peri‐Electrode Gliosis through Mechanosensitive Ion Channels
title_short Micromotion Derived Fluid Shear Stress Mediates Peri‐Electrode Gliosis through Mechanosensitive Ion Channels
title_sort micromotion derived fluid shear stress mediates peri‐electrode gliosis through mechanosensitive ion channels
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10520674/
https://www.ncbi.nlm.nih.gov/pubmed/37518828
http://dx.doi.org/10.1002/advs.202301352
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