Ion current and action potential alterations in peripheral neurons subject to uniaxial strain
Peripheral nerves, subject to continuous elongation and compression during everyday movement, contain neuron fibers vital for movement and sensation. At supraphysiological strains resulting from trauma, chronic conditions, aberrant limb positioning, or surgery, conduction blocks occur which may resu...
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Veröffentlicht in: | Journal of neuroscience research 2019-07, Vol.97 (7), p.744-751 |
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description | Peripheral nerves, subject to continuous elongation and compression during everyday movement, contain neuron fibers vital for movement and sensation. At supraphysiological strains resulting from trauma, chronic conditions, aberrant limb positioning, or surgery, conduction blocks occur which may result in chronic or temporary loss of function. Previous in vitro stretch models, mainly focused on traumatic brain injury modelling, have demonstrated altered electrophysiological behavior during localized deformation applied by pipette suction. Our aim was to evaluate the changes in voltage‐activated ion channel function during uniaxial straining of neurons applied by whole‐cell deformation, more physiologically relevant model of peripheral nerve trauma. Here, we quantified experimentally the changes in inwards and outwards ion currents and action potential (AP) firing in dorsal root ganglion‐derived neurons subject to uniaxial strains, using a custom‐built device allowing simultaneous cell deformation and patch clamp recording. Peak inwards sodium currents and rectifying potassium current magnitudes were found to decrease in cells under stretch, channel reversal potentials were found to be left‐shifted, and half‐maximum activation potentials right‐shifted. The threshold for AP firing was increased in stretched cells, although neurons retained the ability to fire induced APs. Overall, these results point to ion channels being damaged directly and immediately by uniaxial strain, affecting cell electrophysiological activity, and can help develop prevention and treatment strategies for peripheral neuropathies caused by mechanical trauma.
We apply uniaxial tensile loading to F11 neurons while simultaneously recording patch‐clamp current and voltage to investigate how physiologically relevant cell stretch alters neural electrophysiology. |
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We apply uniaxial tensile loading to F11 neurons while simultaneously recording patch‐clamp current and voltage to investigate how physiologically relevant cell stretch alters neural electrophysiology.</description><identifier>ISSN: 0360-4012</identifier><identifier>EISSN: 1097-4547</identifier><identifier>DOI: 10.1002/jnr.24408</identifier><identifier>PMID: 30927386</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Action potential ; Action Potentials - physiology ; Animals ; Brain ; Cell Line, Tumor ; Chronic conditions ; Chronic illnesses ; Compression ; Deformation ; Deformation mechanisms ; Dorsal root ganglia ; Electrophysiology ; Elongation ; Fibers ; Fire damage ; Ganglia, Spinal ; Head injuries ; Ion Channel Gating - physiology ; Ion channels ; ion current ; Ion currents ; Membrane Potentials - physiology ; Neuroblastoma ; Neurons ; Neurons - physiology ; Patch-Clamp Techniques ; peripheral nerve ; Peripheral Nerve Injuries - physiopathology ; Peripheral nerves ; Potassium ; Rats ; Recording ; Sodium ; Sodium currents ; Suction ; Surgery ; Trauma ; Traumatic brain injury ; whole‐cell patch clamping</subject><ispartof>Journal of neuroscience research, 2019-07, Vol.97 (7), p.744-751</ispartof><rights>2019 The Authors. Published by Wiley Periodicals, Inc.</rights><rights>2019 The Authors. Journal of Neuroscience Research Published by Wiley Periodicals, Inc.</rights><rights>2019 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4438-1d3e8f8ec1c948b22d6f8488bdc45c742847adeabc18c4833bd3ccd41425f64c3</citedby><cites>FETCH-LOGICAL-c4438-1d3e8f8ec1c948b22d6f8488bdc45c742847adeabc18c4833bd3ccd41425f64c3</cites><orcidid>0000-0001-9025-1708 ; 0000-0001-7613-6041 ; 0000-0001-8958-0336</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fjnr.24408$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fjnr.24408$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30927386$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bianchi, Fabio</creatorcontrib><creatorcontrib>Malboubi, Majid</creatorcontrib><creatorcontrib>George, Julian H.</creatorcontrib><creatorcontrib>Jerusalem, Antoine</creatorcontrib><creatorcontrib>Thompson, Mark S.</creatorcontrib><creatorcontrib>Ye, Hua</creatorcontrib><title>Ion current and action potential alterations in peripheral neurons subject to uniaxial strain</title><title>Journal of neuroscience research</title><addtitle>J Neurosci Res</addtitle><description>Peripheral nerves, subject to continuous elongation and compression during everyday movement, contain neuron fibers vital for movement and sensation. At supraphysiological strains resulting from trauma, chronic conditions, aberrant limb positioning, or surgery, conduction blocks occur which may result in chronic or temporary loss of function. Previous in vitro stretch models, mainly focused on traumatic brain injury modelling, have demonstrated altered electrophysiological behavior during localized deformation applied by pipette suction. Our aim was to evaluate the changes in voltage‐activated ion channel function during uniaxial straining of neurons applied by whole‐cell deformation, more physiologically relevant model of peripheral nerve trauma. Here, we quantified experimentally the changes in inwards and outwards ion currents and action potential (AP) firing in dorsal root ganglion‐derived neurons subject to uniaxial strains, using a custom‐built device allowing simultaneous cell deformation and patch clamp recording. Peak inwards sodium currents and rectifying potassium current magnitudes were found to decrease in cells under stretch, channel reversal potentials were found to be left‐shifted, and half‐maximum activation potentials right‐shifted. The threshold for AP firing was increased in stretched cells, although neurons retained the ability to fire induced APs. Overall, these results point to ion channels being damaged directly and immediately by uniaxial strain, affecting cell electrophysiological activity, and can help develop prevention and treatment strategies for peripheral neuropathies caused by mechanical trauma.
We apply uniaxial tensile loading to F11 neurons while simultaneously recording patch‐clamp current and voltage to investigate how physiologically relevant cell stretch alters neural electrophysiology.</description><subject>Action potential</subject><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>Brain</subject><subject>Cell Line, Tumor</subject><subject>Chronic conditions</subject><subject>Chronic illnesses</subject><subject>Compression</subject><subject>Deformation</subject><subject>Deformation mechanisms</subject><subject>Dorsal root ganglia</subject><subject>Electrophysiology</subject><subject>Elongation</subject><subject>Fibers</subject><subject>Fire damage</subject><subject>Ganglia, Spinal</subject><subject>Head injuries</subject><subject>Ion Channel Gating - physiology</subject><subject>Ion channels</subject><subject>ion current</subject><subject>Ion currents</subject><subject>Membrane Potentials - physiology</subject><subject>Neuroblastoma</subject><subject>Neurons</subject><subject>Neurons - physiology</subject><subject>Patch-Clamp Techniques</subject><subject>peripheral nerve</subject><subject>Peripheral Nerve Injuries - physiopathology</subject><subject>Peripheral nerves</subject><subject>Potassium</subject><subject>Rats</subject><subject>Recording</subject><subject>Sodium</subject><subject>Sodium currents</subject><subject>Suction</subject><subject>Surgery</subject><subject>Trauma</subject><subject>Traumatic brain injury</subject><subject>whole‐cell patch clamping</subject><issn>0360-4012</issn><issn>1097-4547</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kc1LJDEQxYMoOroe_AekwYseWitJdXf6Ioj4tcgKsntcQjqd1gw9yZh0-_Hfm3FcUWFPBa9-9XjFI2SHwiEFYEdTFw4ZIogVMqFQVzkWWK2SCfAScgTKNshmjFMAqOuCr5MNDjWruCgn5O-Vd5keQzBuyJRrM6UHm6S5H5JiVZ-pfjBBLcSY2bQwwc7vk9JnzoxhocaxmRo9ZIPPRmfV8-IqDkFZ94OsdaqPZvt9bpE_52e_Ty_z65uLq9OT61wjcpHTlhvRCaOprlE0jLVlJ1CIptVY6AqZwEq1RjWaCo2C86blWrdIkRVdiZpvkeOl73xsZqbVKXoKKOfBzlR4kV5Z-XXj7L2884-yLGjNC5oM9t8Ngn8YTRzkzEZt-l4548coGQOoBGBdJ3TvGzr1Y3DpvURRISgwyhN1sKR08DEG032EoSAXpclUmnwrLbG7n9N_kP9aSsDREniyvXn5v5P8-et2afkKxA-jRQ</recordid><startdate>201907</startdate><enddate>201907</enddate><creator>Bianchi, Fabio</creator><creator>Malboubi, Majid</creator><creator>George, Julian H.</creator><creator>Jerusalem, Antoine</creator><creator>Thompson, Mark S.</creator><creator>Ye, Hua</creator><general>Wiley Subscription Services, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9025-1708</orcidid><orcidid>https://orcid.org/0000-0001-7613-6041</orcidid><orcidid>https://orcid.org/0000-0001-8958-0336</orcidid></search><sort><creationdate>201907</creationdate><title>Ion current and action potential alterations in peripheral neurons subject to uniaxial strain</title><author>Bianchi, Fabio ; Malboubi, Majid ; George, Julian H. ; Jerusalem, Antoine ; Thompson, Mark S. ; Ye, Hua</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4438-1d3e8f8ec1c948b22d6f8488bdc45c742847adeabc18c4833bd3ccd41425f64c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Action potential</topic><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>Brain</topic><topic>Cell Line, Tumor</topic><topic>Chronic conditions</topic><topic>Chronic illnesses</topic><topic>Compression</topic><topic>Deformation</topic><topic>Deformation mechanisms</topic><topic>Dorsal root ganglia</topic><topic>Electrophysiology</topic><topic>Elongation</topic><topic>Fibers</topic><topic>Fire damage</topic><topic>Ganglia, Spinal</topic><topic>Head injuries</topic><topic>Ion Channel Gating - physiology</topic><topic>Ion channels</topic><topic>ion current</topic><topic>Ion currents</topic><topic>Membrane Potentials - physiology</topic><topic>Neuroblastoma</topic><topic>Neurons</topic><topic>Neurons - physiology</topic><topic>Patch-Clamp Techniques</topic><topic>peripheral nerve</topic><topic>Peripheral Nerve Injuries - physiopathology</topic><topic>Peripheral nerves</topic><topic>Potassium</topic><topic>Rats</topic><topic>Recording</topic><topic>Sodium</topic><topic>Sodium currents</topic><topic>Suction</topic><topic>Surgery</topic><topic>Trauma</topic><topic>Traumatic brain injury</topic><topic>whole‐cell patch clamping</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bianchi, Fabio</creatorcontrib><creatorcontrib>Malboubi, Majid</creatorcontrib><creatorcontrib>George, Julian H.</creatorcontrib><creatorcontrib>Jerusalem, Antoine</creatorcontrib><creatorcontrib>Thompson, Mark S.</creatorcontrib><creatorcontrib>Ye, Hua</creatorcontrib><collection>Wiley Online Library (Open Access Collection)</collection><collection>Wiley Online Library (Open Access Collection)</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of neuroscience research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bianchi, Fabio</au><au>Malboubi, Majid</au><au>George, Julian H.</au><au>Jerusalem, Antoine</au><au>Thompson, Mark S.</au><au>Ye, Hua</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ion current and action potential alterations in peripheral neurons subject to uniaxial strain</atitle><jtitle>Journal of neuroscience research</jtitle><addtitle>J Neurosci Res</addtitle><date>2019-07</date><risdate>2019</risdate><volume>97</volume><issue>7</issue><spage>744</spage><epage>751</epage><pages>744-751</pages><issn>0360-4012</issn><eissn>1097-4547</eissn><abstract>Peripheral nerves, subject to continuous elongation and compression during everyday movement, contain neuron fibers vital for movement and sensation. At supraphysiological strains resulting from trauma, chronic conditions, aberrant limb positioning, or surgery, conduction blocks occur which may result in chronic or temporary loss of function. Previous in vitro stretch models, mainly focused on traumatic brain injury modelling, have demonstrated altered electrophysiological behavior during localized deformation applied by pipette suction. Our aim was to evaluate the changes in voltage‐activated ion channel function during uniaxial straining of neurons applied by whole‐cell deformation, more physiologically relevant model of peripheral nerve trauma. Here, we quantified experimentally the changes in inwards and outwards ion currents and action potential (AP) firing in dorsal root ganglion‐derived neurons subject to uniaxial strains, using a custom‐built device allowing simultaneous cell deformation and patch clamp recording. Peak inwards sodium currents and rectifying potassium current magnitudes were found to decrease in cells under stretch, channel reversal potentials were found to be left‐shifted, and half‐maximum activation potentials right‐shifted. The threshold for AP firing was increased in stretched cells, although neurons retained the ability to fire induced APs. Overall, these results point to ion channels being damaged directly and immediately by uniaxial strain, affecting cell electrophysiological activity, and can help develop prevention and treatment strategies for peripheral neuropathies caused by mechanical trauma.
We apply uniaxial tensile loading to F11 neurons while simultaneously recording patch‐clamp current and voltage to investigate how physiologically relevant cell stretch alters neural electrophysiology.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>30927386</pmid><doi>10.1002/jnr.24408</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0001-9025-1708</orcidid><orcidid>https://orcid.org/0000-0001-7613-6041</orcidid><orcidid>https://orcid.org/0000-0001-8958-0336</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Action potential Action Potentials - physiology Animals Brain Cell Line, Tumor Chronic conditions Chronic illnesses Compression Deformation Deformation mechanisms Dorsal root ganglia Electrophysiology Elongation Fibers Fire damage Ganglia, Spinal Head injuries Ion Channel Gating - physiology Ion channels ion current Ion currents Membrane Potentials - physiology Neuroblastoma Neurons Neurons - physiology Patch-Clamp Techniques peripheral nerve Peripheral Nerve Injuries - physiopathology Peripheral nerves Potassium Rats Recording Sodium Sodium currents Suction Surgery Trauma Traumatic brain injury whole‐cell patch clamping |
title | Ion current and action potential alterations in peripheral neurons subject to uniaxial strain |
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