Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations

Paulo R. F. Rocha, Maria C R Medeiros, Ulrike Kintzel, Johannes Vogt, Inês M. Araújo, Ana L. G. Mestre, Volker Mailänder, Paul Schlett, Melanie Dröge, Leonid Schneider, Fabio Biscarini, Dago M. De Leeuw, Henrique L. Gomes

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

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.
Original languageEnglish
Article numbere1600516
Pages (from-to)1 - 8
Number of pages8
JournalScience Advances
Volume2
Issue number12
Early online date23 Dec 2016
DOIs
Publication statusPublished - 23 Dec 2016

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Glioma
Population
Culture Media
Noise
Cell Culture Techniques
Acid Sensing Ion Channels
Ions
Acidosis
Transducers
Ion Channels
Cell Adhesion
Epilepsy
Neoplasms
Electrodes
Seizures
Apoptosis
Cell Line
Brain

Cite this

Rocha, P. R. F., Medeiros, M. C. R., Kintzel, U., Vogt, J., Araújo, I. M., Mestre, A. L. G., ... Gomes, H. L. (2016). Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations. Science Advances, 2(12), 1 - 8. [e1600516]. https://doi.org/10.1126/sciadv.1600516

Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations. / 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.

In: Science Advances, Vol. 2, No. 12, e1600516, 23.12.2016, p. 1 - 8.

Research output: Contribution to journalArticle

Rocha, PRF, Medeiros, MCR, Kintzel, U, Vogt, J, Araújo, IM, Mestre, ALG, Mailänder, V, Schlett, P, Dröge, M, Schneider, L, Biscarini, F, De Leeuw, DM & Gomes, HL 2016, 'Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations', Science Advances, vol. 2, no. 12, e1600516, pp. 1 - 8. https://doi.org/10.1126/sciadv.1600516
Rocha PRF, Medeiros MCR, Kintzel U, Vogt J, Araújo IM, Mestre ALG et al. Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations. Science Advances. 2016 Dec 23;2(12):1 - 8. e1600516. https://doi.org/10.1126/sciadv.1600516
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. / Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations. In: Science Advances. 2016 ; Vol. 2, No. 12. pp. 1 - 8.
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