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Journal of Neuroscience, Vol 14, 5590-5602, Copyright © 1994 by Society for Neuroscience
Oxygen deprivation activates an ATP-inhibitable K+ channel in substantia nigra neurons
C Jiang, FJ Sigworth and GG Haddad
Department of Pediatrics (Section of Respiratory Medicine), Yale University School of Medicine, New Haven, Connecticut 06520-0864.
Depending on its severity and duration, O2 deprivation activates mechanisms
that can lead to profound deleterious changes in neuronal structure and
function. Hypoxia also evokes inherent adaptive mechanisms that can
possibly delay injury and increase neuronal survival. One of these neuronal
adaptive mechanisms is believed to be the activation of K+ channels, but
direct evidence for their activation is lacking. We performed experiments
to test the hypothesis that hypoxia induces activation of K+ channels via
changes in cytosolic and membrane factors such as ATP, Ca2+, and membrane
potential. The effect of hypoxia on single-channel currents was studied in
rat substantia nigra neurons, since these have a high density of
glibenclamide binding sites. In cell-attached patches, hypoxia or cyanide
reversibly activated an outward current. This hypoxia-activated current in
excised inside-out patches was K+ selective and voltage dependent, and had
a high sensitivity to internal ATP, ADP, and AMP-PNP, a nonhydrolyzable ATP
analog. Activation of this channel required the presence of free Ca2+ on
the cytosolic side, but charybdotoxin or apamin did not have any effect on
this channel. The effect of ATP on channel activity was not a result of
Ca2+ chelation because Mg.ATP in high Mg2+ background and K2.ATP in high
Ca2+ environment inhibited the channel. These results suggest that although
this hypoxia-activated K+ channel shares properties with ATP-sensitive K+
(KATP) channels in other tissues, substantia nigra neurons seem to have a
different subtype or isoform of KATP channels. Gating this channel by
multiple factors simultaneously would allow this channel to be particularly
suitable for activation during metabolic stress.
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