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The Journal of Neuroscience, July 15, 2001, 21(14):4958-4968
Negative Cross Talk between Anionic GABAA and
Cationic P2X Ionotropic Receptors of Rat Dorsal Root Ganglion
Neurons
Elena
Sokolova1,
Andrea
Nistri1, and
Rashid
Giniatullin1, 2
1 Biophysics Sector and National Institute for Physics
of Matter Unit, International School for Advanced Studies
(SISSA), 34014 Trieste, Italy, and 2 Kazan Medical
University, 420012 Kazan, Russia
Using whole-cell patch-clamp recording and intracellular
Ca2+ imaging of rat cultured DRG neurons, we studied
the cross talk between GABAA and P2X receptors. A rapidly
fading current was the main response to ATP, whereas GABA elicited
slowly desensitizing inward currents. Coapplication of these agonists
produced a total current much smaller than the linear summation of
individual responses (68 ± 5% with 10 µM ATP plus
100 µM GABA). Occlusion was observed regardless of ATP
response type. Neurons without functional P2X receptors manifested no
effect of ATP on GABA currents (and vice versa). Occlusion was also
absent in the presence of the P2X blocker trinitrophenyl-ATP (TNP-ATP)
or of the GABA blocker picrotoxin, indicating a lack of involvement by
metabotropic ATP or GABA receptors. Less occlusion was obtained when
ATP was applied 2 sec after GABA than when GABA was applied after ATP.
Changing the polarity of GABA currents by using intracellular
SO42 instead of
Cl significantly reduced the occlusion of ATP
currents by GABA, suggesting an important role for
Cl efflux in this phenomenon. Occlusion was
enhanced whenever intracellular Ca2+
([Ca2+]i) was not buffered,
indicating the cross talk-facilitating role of this divalent cation.
Ca2+ imaging showed that ATP (but not GABA)
increased [Ca2+]i in voltage-clamped
or intact neurons. Our data demonstrated a novel
Cl and Ca2+-dependent
interaction between cationic P2X and anionic GABAA receptors of DRG neurons. Such negative cross talk might represent a
model for a new mechanism to inhibit afferent excitation to the spinal
cord as GABA and ATP are coreleased within the dorsal horn.
Key words:
ATP; GABA; occlusion; calcium imaging; chloride channels; DRG
Copyright © 2001 Society for Neuroscience 0270-6474/01/21144958-11$05.00/0
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