Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations
Autor(a) principal: | |
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Data de Publicação: | 2016 |
Outros Autores: | , , , , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
Texto Completo: | http://hdl.handle.net/10316/108898 https://doi.org/10.1126/sciadv.1600516 |
Resumo: | Glioma patients often suffer from epileptic seizures because of the tumor's impact on the brain physiology. Using the rat glioma cell line C6 as a model system, we performed long-term live recordings of the electrical activity of glioma populations in an ultrasensitive detection method. The transducer exploits large-area electrodes that maximize double-layer capacitance, thus increasing the sensitivity. This strategy allowed us to record glioma electrical activity. We show that although glioma cells are nonelectrogenic, they display a remarkable electrical burst activity in time. The low-frequency current noise after cell adhesion is dominated by the flow of Na+ ions through voltage-gated ion channels. However, after an incubation period of many hours, the current noise markedly increased. This electric bursting phenomenon was not associated with apoptosis because the cells were viable and proliferative during the period of increased electric activity. We detected a rapid cell culture medium acidification accompanying this event. By using specific inhibitors, we showed that the electrical bursting activity was prompted by extracellular pH changes, which enhanced Na+ ion flux through the psalmotoxin 1-sensitive acid-sensing ion channels. Our model of pH-triggered bursting was unambiguously supported by deliberate, external acidification of the cell culture medium. This unexpected, acidosis-driven electrical activity is likely to directly perturb, in vivo, the functionality of the healthy neuronal network in the vicinity of the tumor bulk and may contribute to seizures in glioma patients. |
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Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populationsASICsAcid-sensing ion channelsC6 GliomaElectrical recordingLow frequency current noisePcTX-1bioelectronicsgliaGlioma patients often suffer from epileptic seizures because of the tumor's impact on the brain physiology. Using the rat glioma cell line C6 as a model system, we performed long-term live recordings of the electrical activity of glioma populations in an ultrasensitive detection method. The transducer exploits large-area electrodes that maximize double-layer capacitance, thus increasing the sensitivity. This strategy allowed us to record glioma electrical activity. We show that although glioma cells are nonelectrogenic, they display a remarkable electrical burst activity in time. The low-frequency current noise after cell adhesion is dominated by the flow of Na+ ions through voltage-gated ion channels. However, after an incubation period of many hours, the current noise markedly increased. This electric bursting phenomenon was not associated with apoptosis because the cells were viable and proliferative during the period of increased electric activity. We detected a rapid cell culture medium acidification accompanying this event. By using specific inhibitors, we showed that the electrical bursting activity was prompted by extracellular pH changes, which enhanced Na+ ion flux through the psalmotoxin 1-sensitive acid-sensing ion channels. Our model of pH-triggered bursting was unambiguously supported by deliberate, external acidification of the cell culture medium. This unexpected, acidosis-driven electrical activity is likely to directly perturb, in vivo, the functionality of the healthy neuronal network in the vicinity of the tumor bulk and may contribute to seizures in glioma patients.American Association for the Advancement of Science2016-12info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://hdl.handle.net/10316/108898http://hdl.handle.net/10316/108898https://doi.org/10.1126/sciadv.1600516eng2375-2548280285332375-2548Rocha, Paulo R. F.Medeiros, Maria C. R.Kintzel, UlrikeVogt, JohannesAraújo, Inês M.Mestre, Ana L. G.Mailänder, VolkerSchlett, PaulDröge, MelanieSchneider, LeonidBiscarini, Fabiode Leeuw, Dago M.Gomes, Henrique L.info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-09-22T11:20:50Zoai:estudogeral.uc.pt:10316/108898Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T21:25:08.204744Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse |
dc.title.none.fl_str_mv |
Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations |
title |
Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations |
spellingShingle |
Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations Rocha, Paulo R. F. ASICs Acid-sensing ion channels C6 Glioma Electrical recording Low frequency current noise PcTX-1 bioelectronics glia |
title_short |
Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations |
title_full |
Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations |
title_fullStr |
Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations |
title_full_unstemmed |
Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations |
title_sort |
Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations |
author |
Rocha, Paulo R. F. |
author_facet |
Rocha, Paulo R. F. Medeiros, Maria C. R. Kintzel, Ulrike Vogt, Johannes Araújo, Inês M. Mestre, Ana L. G. Mailänder, Volker Schlett, Paul Dröge, Melanie Schneider, Leonid Biscarini, Fabio de Leeuw, Dago M. Gomes, Henrique L. |
author_role |
author |
author2 |
Medeiros, Maria C. R. Kintzel, Ulrike Vogt, Johannes Araújo, Inês M. Mestre, Ana L. G. Mailänder, Volker Schlett, Paul Dröge, Melanie Schneider, Leonid Biscarini, Fabio de Leeuw, Dago M. Gomes, Henrique L. |
author2_role |
author author author author author author author author author author author author |
dc.contributor.author.fl_str_mv |
Rocha, Paulo R. F. Medeiros, Maria C. R. Kintzel, Ulrike Vogt, Johannes Araújo, Inês M. Mestre, Ana L. G. Mailänder, Volker Schlett, Paul Dröge, Melanie Schneider, Leonid Biscarini, Fabio de Leeuw, Dago M. Gomes, Henrique L. |
dc.subject.por.fl_str_mv |
ASICs Acid-sensing ion channels C6 Glioma Electrical recording Low frequency current noise PcTX-1 bioelectronics glia |
topic |
ASICs Acid-sensing ion channels C6 Glioma Electrical recording Low frequency current noise PcTX-1 bioelectronics glia |
description |
Glioma patients often suffer from epileptic seizures because of the tumor's impact on the brain physiology. Using the rat glioma cell line C6 as a model system, we performed long-term live recordings of the electrical activity of glioma populations in an ultrasensitive detection method. The transducer exploits large-area electrodes that maximize double-layer capacitance, thus increasing the sensitivity. This strategy allowed us to record glioma electrical activity. We show that although glioma cells are nonelectrogenic, they display a remarkable electrical burst activity in time. The low-frequency current noise after cell adhesion is dominated by the flow of Na+ ions through voltage-gated ion channels. However, after an incubation period of many hours, the current noise markedly increased. This electric bursting phenomenon was not associated with apoptosis because the cells were viable and proliferative during the period of increased electric activity. We detected a rapid cell culture medium acidification accompanying this event. By using specific inhibitors, we showed that the electrical bursting activity was prompted by extracellular pH changes, which enhanced Na+ ion flux through the psalmotoxin 1-sensitive acid-sensing ion channels. Our model of pH-triggered bursting was unambiguously supported by deliberate, external acidification of the cell culture medium. This unexpected, acidosis-driven electrical activity is likely to directly perturb, in vivo, the functionality of the healthy neuronal network in the vicinity of the tumor bulk and may contribute to seizures in glioma patients. |
publishDate |
2016 |
dc.date.none.fl_str_mv |
2016-12 |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://hdl.handle.net/10316/108898 http://hdl.handle.net/10316/108898 https://doi.org/10.1126/sciadv.1600516 |
url |
http://hdl.handle.net/10316/108898 https://doi.org/10.1126/sciadv.1600516 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
2375-2548 28028533 2375-2548 |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.publisher.none.fl_str_mv |
American Association for the Advancement of Science |
publisher.none.fl_str_mv |
American Association for the Advancement of Science |
dc.source.none.fl_str_mv |
reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação instacron:RCAAP |
instname_str |
Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
instacron_str |
RCAAP |
institution |
RCAAP |
reponame_str |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
collection |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
repository.name.fl_str_mv |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
repository.mail.fl_str_mv |
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_version_ |
1799134134431383552 |