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Departments of 1 Pediatrics and 2 Physiology and 3 Center for Cell and Molecular Signaling, Emory University School of Medicine, Atlanta, Georgia 30322
We used the patch-clamp technique to study the
effect of nitric oxide (NO) on a cation channel in rat type II
pneumocytes [alveolar type II (AT II) cells].
Single-channel recordings from the apical surface of AT II cells in
primary culture showed a predominant cation channel with a conductance
of 20.6 ± 1.1 (SE) pS (n = 9 cell-attached patches) and
Na+-to-K+
selectivity of 0.97 ± 0.07 (n = 7 cell-attached patches). An NO donor,
S-nitrosoglutathione (GSNO; 100 µM),
inhibited the basal cation-channel activity by 43% [open
probability (Po), control 0.28 ± 0.05 vs. GSNO 0.16 ± 0.03;
P < 0.001;
n = 16 cell-attached patches],
with no significant change in the conductance. GSNO reduced the
Po by reducing
channel mean open and increasing mean closed times. GSNO inhibition was
reversed by washout. The inhibitory effect of NO was confirmed by using
a second donor of NO,
S-nitroso-N-acetylpenicillamine (100 µM; Po,
control 0.53 ± 0.05 vs.
S-nitroso-N-acetylpenicillamine 0.31 ± 0.04;
42%; P < 0.05;
n = 5 cell-attached patches). The GSNO
effect was blocked by methylene blue (a blocker of guanylyl cyclase;
100 µM), suggesting a role for cGMP. The permeable analog of cGMP,
8-bromo-cGMP (8-BrcGMP; 1 mM), inhibited the cation channel in a manner
similar to GSNO
(Po, control 0.38 ± 0.06 vs. 8-BrcGMP 0.09 ± 0.02;
P < 0.05;
n = 7 cell-attached patches).
Pretreatment of cells with 1 µM KT-5823 (a blocker of protein kinase
G) abolished the inhibitory effect of GSNO. The NO inhibition of
channels was not due to changes in cell viability. Intracellular cGMP
was found to be elevated in AT II cells treated with NO (control 13.4 ± 3.6 vs. GSNO 25.4 ± 4.1 fmol/ml;
P < 0.05;
n = 6 cell-attached patches). We
conclude that NO suppresses the activity of an
Na+-permeant cation channel on the
apical surface of AT II cells. This action appears to be mediated by a
cGMP-dependent protein kinase.
guanosine 3',5'-cyclic monophosphate; nonselective cation channel; alveolar type II cells; S-nitrosoglutathione; sodium channel; single-channel recording; amiloride
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