Effect of elevated potassium on the ion content of mouse astrocytes and neurons

Abstract

Potassium is tightly regulated within the extracellular compartment of the brain. Nonetheless, it can increase 3- to 4-fold during periods of intense seizure activity and 10- to 20-fold under certain pathological conditions such as spreading depression. Within the central nervous system, neurons and astrocytes are both affected by shifts in the extracellular concentration of potassium. Elevated potassium can lead to a redistribution of other ions (e.g., calcium, sodium, chloride, hydrogen, etc.) within the cellular compartment of the brain. Small shifts in the extracellular potassium concentration can markedly affect acid-based homeostasis, energy metabolism, and volume regulation of these two brain cells. Since normal neuronal function is tightly coupled to the ability of the surrounding glial cells to regulate ionic shifts within the brain and since both cell types can be affected by shifts in the extracellular potassium, it is important to characterize their individual response to an elevation of this ion. This review describes the results of side-by-side studies conducted on cortical neurons and astrocytes, which assessed the effect of elevated potassium on their resting membrane potential, intracellular volume, and their intracellular concentration of potassium, sodium, and chloride. The results obtained from these studies suggest that there exists a marked cellular heterogeneity between neurons and astrocytes in their response to an elevation in the extracellular potassium concentration.

Blood Levels of Trace Elements, Electrolytes, and Oxidative Stress/Antioxidant Systems in Epileptic Patients

“…We reported hypokalemia with unaltered Mg 2+ and Ca 2+ levels in untreated epileptics (P<0.01) (Tables 2 and 4) which agrees with many studies (42,58,61,62). While we found no difference in the serum K + levels in different treated groups (Tables 2 and 4), White et al (58) reported elevation of K + levels during periods of intense seizure activity.…”

“…While we found no difference in the serum K + levels in different treated groups (Tables 2 and 4), White et al (58) reported elevation of K + levels during periods of intense seizure activity. Generally, the deficiency in K + is correlated to hypomagnesaemia and hypocalcaemia (42).…”

“…Biochonski et al (57) reported hypernatremia and hypokalemia in epileptic children. White et al (58) reported elevation of Na + levels during periods of intense seizure activity. In contrast, Natelson et al (59) and Shah et al (42) reported unaffected serum Na + during and after seizure activity in their untreated patients.…”

Neurologic Defects and Selective Disruption of Basement Membranes in Mice Lacking Entactin-1/Nidogen-1

“…Decreased glucose uptake and hypometabolism have been observed in seizure foci (Janigro, 1999). Also, astrocytes and endothelial cells play important roles in regulating intercellular levels of potassium and other ions that are important in brain electrophysiology (MacVicar, 1989;O'Donnell et al, 1995;Walz, 2000;White et al, 1992). Lost functions of astrocytes have also been linked to epileptic seizure (Heinemann et al, 1999).…”

Signalling Effect of Elevated Potassium Concentrations and Monoamines on Brain Energy Metabolism at the Cellular Level (Part 2 of 2)

“…The furosemidesensitive cotransport system appears to require some what higher concentrations of K + for maximum stimula tion than the ouabain-sensitive N a+/K + exchange but the exact correlation between the extracellular K + concentra tion and the activity of this system is disputed, since Walz and Hertz [42] and Chen et al [40] report maxi mum activity al higher [K+]0 concentrations than Walz and Hinks [36], A possible explanation for this discrep ancy might be that the latter authors compensated for the increase in K+ in the incubation medium by a corre sponding decrease in Na+ which may have become ratelimiting for the uptake. Jameson et al [61J concur in the conclusion that oxidative metabolism in astrocytes can be considerably increased above its resting level, in their studies by uncoupling with dinitrophenol [61], but they did not report any effects of exposure to excess K+.A moderate increase in the extracellular K+ concen tration beyond its resting level does not stimulate Na+,K+-ATPase activity in neurons obtained by gradient centrifugation [59], and there is no elevation in intracel lular K + concentration in cerebral cortical cultures highly enriched in GABAergic neurons when the extracellular K+ concentration is raised from 5 to 10 mM [53]. In the glutamatergic cerebellar granule cell neurons, the rate of both glucose ( fig.…”