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The Journal of Neurophysiology Vol. 81 No. 4 April 1999, pp. 1449-1457
Copyright ©1999 by the American Physiological Society
Department of Physiology and Biophysics, School of Medicine, Case Western Reserve University, Cleveland, Ohio 44106-4970
Summers, Beth A.,
Jeffrey L. Overholt, and
Nanduri R. Prabhakar.
Nitric oxide inhibits L-type Ca2+ current in glomus cells
of the rabbit carotid body via a cGMP-independent mechanism.
Previous studies have shown that nitric oxide (NO) inhibits carotid
body sensory activity. To begin to understand the cellular mechanisms associated with the actions of NO in the carotid body, we monitored the
effects of NO donors on the macroscopic Ca2+ current in
glomus cells isolated from rabbit carotid bodies. Experiments were
performed on freshly dissociated glomus cells from adult rabbit carotid
bodies using the whole cell configuration of the patch-clamp technique.
The NO donors sodium nitroprusside (SNP; 600 µM, n = 7) and spermine nitric oxide (SNO; 100 µM, n = 7)
inhibited the Ca2+ current in glomus cells in a
voltage-independent manner. These effects of NO donors were rapid in
onset and peaked within 1 or 2 min. In contrast, the outward
K+ current was unaffected by SNP (600 µM,
n = 6), indicating that the inhibition by SNP was not a
nonspecific membrane effect.
2-(4-carboxyphenyl)-4,4,5,5-tetramethyl-imidazoline-1-oxyl-3-oxide (carboxy-PTIO; 500 µM), an NO scavenger, prevented inhibition of the
Ca2+ current by SNP (n = 7), whereas
neither superoxide dismutase (SOD; 2,000 U/ml, n = 4),
a superoxide scavenger, nor sodium hydrosulfite (SHS; 1 mM,
n = 7), a reducing agent, prevented inhibition of the
Ca2+ current by SNP. However, SNP inhibition of the
Ca2+ current was reversible in the presence of either SOD
or SHS. These results suggest that NO itself inhibits Ca2+
current in a reversible manner and that subsequent
formation of peroxynitrites results in irreversible inhibition. SNP
inhibition of the Ca2+ current was not affected by 30 µM
LY 83,583 (n = 7) nor was it mimicked by 600 µM
8-bromoguanosine 3':5'-cyclic monophosphate (8-Br-cGMP;
n = 6), suggesting that the effects of NO on the
Ca2+ current are mediated, in part, via a cGMP-independent
mechanism. N-ethylmaleimide (NEM; 2.5 mM, n = 6) prevented the inhibition of the Ca2+ current by SNP,
indicating that SNP is acting via a modification of sulfhydryl groups
on Ca2+ channel proteins. Norepinephrine (NE; 10 µM)
further inhibited the Ca2+ current in the presence of NEM
(n = 7), implying that NEM did not nonspecifically
eliminate Ca2+ current modulation. Nisoldipine, an L-type
Ca2+ channel blocker (2 µM, n = 6),
prevented the inhibition of Ca2+ current by SNP, whereas
-conotoxin GVIA, an N-type Ca2+ channel blocker (1 µM,
n = 9), did not prevent the inhibition of
Ca2+ current by SNP. These results demonstrate that NO
inhibits L-type Ca2+ channels in adult rabbit glomus cells,
in part, due to a modification of calcium channel proteins. The
inhibition might provide one plausible mechanism for efferent
inhibition of carotid body activity by NO.
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