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The Journal of Neurophysiology Vol. 83 No. 1 January 2000, pp. 198-206
Copyright ©2000 by the American Physiological Society
1Departments of Physiology and Biophysics and Ophthalmology, Dalhousie University, Halifax, Nova Scotia B3H 4H7, Canada; and 2Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio 44106
Hirooka, Kazuyuki,
Dmitri E. Kourennyi, and
Steven Barnes.
Calcium Channel Activation Facilitated by Nitric Oxide in Retinal
Ganglion Cells. J. Neurophysiol. 83: 198-206, 2000. We investigated the modulation of voltage-gated
Ca channels by nitric oxide (NO) in isolated salamander retinal
ganglion cells with the goals of determining the type of Ca channel
affected and the signaling pathway by which modulation might occur. The NO donors, S-nitroso-N-acetyl-penicillamine (SNAP,
1 mM) and S-nitroso-cysteine (1 mM) induced modest
increases in the amplitude of Ca channel currents recorded with
ruptured- and permeabilized-patch techniques by causing a subpopulation
of the Ca channels to activate at more negative potentials. The Ca
channel antagonists 
-conotoxin GVIA and nisoldipine each reduced the
Ca channel current partially, but only -conotoxin GVIA blocked the
enhancement by SNAP. The SNAP-induced increase was blocked by
oxadiazolo-quinoxaline (50 µM), suggesting that the NO generated by
SNAP acts via a soluble guanylyl cyclase to raise levels of cGMP. The
membrane-permeant cGMP analog 8-(4-chlorophenylthio) guanosine cyclic
monophosphate also enhanced Ca channel currents and 8-bromo guanosine
cyclic monophosphate (1 mM) occluded enhancement by SNAP. Consistent with these results, isobutyl-methyl-xanthine (IBMX, 10 µM), which can
raise cGMP levels by inhibiting phosphodiesterase activity, increased
Ca channel current by the same amount as SNAP and occluded subsequent
enhancement by SNAP. Neither IBMX, the cGMP analogs, nor SNAP itself,
led to activation of cGMP-gated channels.
N-[2-(methylamino)ethyl]
5-isoquinoline-sulfonamide (2 µM), a broad spectrum inhibitor of protein kinase activity, KT5823
(1 µM), a specific protein kinase G (PKG) inhibitor, and a peptide
inhibitor of PKG (200 µM) blocked SNAP enhancement, as did
5'-adenylylimidophosphate (1.5 mM), a nonhydrolyzable ATP analog that
prevents protein phosphorylation. A peptide inhibitor of protein kinase
A (10 nM) did not block the facilitory effects of SNAP. Okadaic acid (1 µM), a phosphatase inhibitor, had no effect by itself but increased
the enhancement of Ca channel current by SNAP. These results suggest
that NO modulates retinal ganglion cell N-type Ca channels by
facilitating their voltage-dependent activation via a mechanism
involving guanylyl cyclase/PKG-dependent phosphorylation. This effect
could fine-tune neural integration in ganglion cells or play a role in
ganglion cell disease by modulating intracellular calcium signaling.
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