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Larsen, Brian Roland; Assentoft, Mette; Cotrina, Maria L; Hua, Susan Z; Nedergaard, Maiken; Kaila, Kai; Voipio, Juha; MacAulay, Nanna
Glia, 04/2014, Volume: 62, Issue: 4Journal Article
Network activity in the brain is associated with a transient increase in extracellular K super(+) concentration. The excess K super(+) is removed from the extracellular space by mechanisms proposed to involve Kir4.1-mediated spatial buffering, the Na super(+)/K super(+)/2Cl super(-) cotransporter 1 (NKCC1), and/or Na super(+)/K super(+)-ATPase activity. Their individual contribution to K super(+) sub(o) management has been of extended controversy. This study aimed, by several complementary approaches, to delineate the transport characteristics of Kir4.1, NKCC1, and Na super(+)/K super(+)-ATPase and to resolve their involvement in clearance of extracellular K super(+) transients. Primary cultures of rat astrocytes displayed robust NKCC1 activity with K super(+) sub(o) increases above basal levels. Increased K super(+) sub(o) produced NKCC1-mediated swelling of cultured astrocytes and NKCC1 could thereby potentially act as a mechanism of K super(+) clearance while concomitantly mediate the associated shrinkage of the extracellular space. In rat hippocampal slices, inhibition of NKCC1 failed to affect the rate of K super(+) removal from the extracellular space while Kir4.1 enacted its spatial buffering only during a local K super(+) sub(o) increase. In contrast, inhibition of the different isoforms of Na super(+)/K super(+)-ATPase reduced post-stimulus clearance of K super(+) transients. The astrocyte-characteristic alpha2beta2 subunit composition of Na super(+)/K super(+)-ATPase , when expressed in Xenopus oocytes, displayed a K super(+) affinity and voltage-sensitivity that would render this subunit composition specifically geared for controlling K super(+) sub(o) during neuronal activity. In rat hippocampal slices, simultaneous measurements of the extracellular space volume revealed that neither Kir4.1, NKCC1, nor Na super(+)/K super(+)-ATPase accounted for the stimulus-induced shrinkage of the extracellular space. Thus, NKCC1 plays no role in activity-induced extracellular K super(+) recovery in native hippocampal tissue while Kir4.1 and Na super(+)/K super(+)-ATPase serve temporally distinct roles. GLIA 2014; 62:608-622 Main Points * Kir4.1 and Na super(+)/K super(+)-ATPase serve distinct roles in recovery of activity-induced K super(+) sub(o) in hippocampus. * The alpha2beta2 Na super(+)/K super(+)-ATPase is specifically geared for controlling K super(+) sub(o). * NKCC1 is not involved in stimulus-induced shrinkage of the extracellular space.
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