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Journal of Neuroscience, Vol 13, 2638-2650, Copyright © 1993 by Society for Neuroscience
Role of calcium in astrocyte volume regulation and in the release of ions and amino acids
ER O'Connor and HK Kimelberg
Department of Pharmacology and Toxicology, Albany Medical College, New York 12208.
Primary astrocyte cultures exposed to hypotonic media undergo a rapid
initial swelling followed by a regulatory volume decrease (RVD), which is
associated with the release of ions and amino acids. The Ca2+ dependence of
RVD was investigated. Using a method that measures extracellular electrical
resistance to measure cell volume changes in substratum-attached cells, we
found that when astrocytes were exposed to hypotonic media without calcium,
RVD was abolished. The addition of CaCl2 to astrocytes swollen in hypotonic
media without calcium caused an almost immediate initiation of volume
regulation, with an EC50 of approximately 0.1 mM CaCl2. Swelling of
astrocytes in hypotonic medium caused an increased influx of 45Ca2+, which
was partially blocked (60%) by 1 microM nimodipine, suggesting that
voltage-gated L-type calcium channels were being opened. Previous work had
shown that hypotonic media-induced swelling of astrocytes caused membrane
potential depolarizations sufficient to open such channels (Kimelberg and
O'Connor, 1988). By measuring intracellular free calcium with fura-2, we
found that astrocytes swollen in hypotonic medium showed a rapid increase
in [Ca2+]i, reaching a peak of approximately 600 nM, followed by a decrease
to a sustained plateau (approximately 250 nM) mirroring the time course of
volume regulation. The removal of extracellular calcium totally abolished,
and the addition of 1 microM nimodipine partially abolished the elevated
plateau, while neither affected the initial [Ca2+]i peak. These data
suggest that the initial peak of the hypotonic-induced rise in [Ca2+]i is
caused by release from intracellular stores and that the sustained elevated
plateau is due to extracellular calcium influx. The removal of
extracellular calcium also abolished swelling-induced K+(86Rb) and 36Cl-
efflux, but did not affect the swelling-induced release of 3H-D-aspartate,
or 3H-taurine (data not shown). These data indicate that hypotonic-induced
aspartate and taurine release is not necessary for RVD in astrocytes
swollen by exposure to hypotonic media, since RVD is completely inhibited
by the omission of external Ca2+. The addition of 1 mM quinine HCl, which
is known to block Ca(2+)-activated K+ channels, also abolished both volume
regulation and 86Rb+ efflux in hypotonic media-swollen astrocytes in the
presence of medium calcium, but did not affect 3H-D-aspartate efflux. We
suggest that the swelling of astrocytes in hypotonic media which leads to a
rapid membrane depolarization first opens voltage- gated calcium
channels.(ABSTRACT TRUNCATED AT 400 WORDS)
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