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Journal of Neuroscience, Vol 10, 1-10, Copyright © 1990 by Society for Neuroscience
ATP-activated channels in rat and bullfrog sensory neurons: concentration dependence and kinetics
BP Bean
Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115.
The concentration dependence and kinetics of ionic currents activated by
extracellular adenosine 5'-triphosphate (ATP) were studied in
voltage-clamped dorsal root ganglion neurons from rats and bullfrogs. About
40% of neurons of both species responded to ATP with an increase in
membrane conductance. The ATP-activated currents were similar in the 2
species, except that currents in rat neurons desensitized faster. In
bullfrog neurons, the conductance was half-maximally activated by about 3
microM ATP; at low concentrations, the conductance increased 3- to 7- fold
for a doubling in [ATP], suggesting that several ATP molecules must bind in
order to activate the current. A steeper concentration- response
relationship than expected from 1:1 binding was also seen in rat neurons.
The current activated quickly upon application of ATP and decayed quickly
when ATP was removed. Activation kinetics were faster at higher [ATP], with
time constants decreasing from about 200 msec at 0.3 microM ATP to about 10
msec at 100 microM ATP. Deactivation kinetics (tau approximately 100-200
msec) were independent of the ATP concentration. The rapid activation and
deactivation make it seem likely that the ATP-activated current is mediated
by direct ligand binding rather than by a second-messenger system. The
experimental observations can be mimicked by a simple model in which ATP
must bind to 3 identical, noninteracting sites in order to activate a
channel. The potency and kinetics of ATP action were voltage-dependent,
with hyperpolarization slowing deactivation and increasing ATP's potency.
Deactivation kinetics were also sensitive to the concentration of external
Ca, becoming faster in higher Ca.
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