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Volume 23
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Article

Changes in Astroglial K+ upon Brief Periods of Energy Deprivation in the Mouse Neocortex

by
Sara Eitelmann
†,
Jonathan Stephan
†,
Katharina Everaerts
,
Simone Durry
,
Nils Pape
,
Niklas J. Gerkau
and
Christine R. Rose
*
Institute of Neurobiology, Heinrich Heine University Düsseldorf, Universitätsstraße 1, D-40225 Düsseldorf, Germany
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2022, 23(9), 4836; https://doi.org/10.3390/ijms23094836
Submission received: 30 March 2022 / Revised: 21 April 2022 / Accepted: 24 April 2022 / Published: 27 April 2022
(This article belongs to the Special Issue Role of Astrocytes in Neurological Diseases)
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Abstract

Malfunction of astrocytic K+ regulation contributes to the breakdown of extracellular K+ homeostasis during ischemia and spreading depolarization events. Studying astroglial K+ changes is, however, hampered by a lack of suitable techniques. Here, we combined results from fluorescence imaging, ion-selective microelectrodes, and patch-clamp recordings in murine neocortical slices with the calculation of astrocytic [K+]. Brief chemical ischemia caused a reversible ATP reduction and a transient depolarization of astrocytes. Moreover, astrocytic [Na+] increased by 24 mM and extracellular [Na+] decreased. Extracellular [K+] increased, followed by an undershoot during recovery. Feeding these data into the Goldman–Hodgkin–Katz equation revealed a baseline astroglial [K+] of 146 mM, an initial K+ loss by 43 mM upon chemical ischemia, and a transient K+ overshoot of 16 mM during recovery. It also disclosed a biphasic mismatch in astrocytic Na+/K+ balance, which was initially ameliorated, but later aggravated by accompanying changes in pH and bicarbonate, respectively. Altogether, our study predicts a loss of K+ from astrocytes upon chemical ischemia followed by a net gain. The overshooting K+ uptake will promote low extracellular K+ during recovery, likely exerting a neuroprotective effect. The resulting late cation/anion imbalance requires additional efflux of cations and/or influx of anions, the latter eventually driving delayed astrocyte swelling.
Keywords: astrocyte; potassium; sodium; pH; extracellular space; ischemia; imaging; ATeam; ion-sensitive microelectrodes; patch-clamp astrocyte; potassium; sodium; pH; extracellular space; ischemia; imaging; ATeam; ion-sensitive microelectrodes; patch-clamp

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MDPI and ACS Style

Eitelmann, S.; Stephan, J.; Everaerts, K.; Durry, S.; Pape, N.; Gerkau, N.J.; Rose, C.R. Changes in Astroglial K+ upon Brief Periods of Energy Deprivation in the Mouse Neocortex. Int. J. Mol. Sci. 2022, 23, 4836. https://doi.org/10.3390/ijms23094836

AMA Style

Eitelmann S, Stephan J, Everaerts K, Durry S, Pape N, Gerkau NJ, Rose CR. Changes in Astroglial K+ upon Brief Periods of Energy Deprivation in the Mouse Neocortex. International Journal of Molecular Sciences. 2022; 23(9):4836. https://doi.org/10.3390/ijms23094836

Chicago/Turabian Style

Eitelmann, Sara, Jonathan Stephan, Katharina Everaerts, Simone Durry, Nils Pape, Niklas J. Gerkau, and Christine R. Rose. 2022. "Changes in Astroglial K+ upon Brief Periods of Energy Deprivation in the Mouse Neocortex" International Journal of Molecular Sciences 23, no. 9: 4836. https://doi.org/10.3390/ijms23094836

APA Style

Eitelmann, S., Stephan, J., Everaerts, K., Durry, S., Pape, N., Gerkau, N. J., & Rose, C. R. (2022). Changes in Astroglial K+ upon Brief Periods of Energy Deprivation in the Mouse Neocortex. International Journal of Molecular Sciences, 23(9), 4836. https://doi.org/10.3390/ijms23094836

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