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J Biol Chem, Vol. 273, Issue 46, 30249-30254, November 13, 1998
,
From the Cardiovascular Division, Department of Medicine, Brigham
and Women's Hospital, Harvard Medical School, Boston, Massachusetts
02115 and the The endothelial isoform of nitric oxide synthase
(eNOS) is dually acylated and thereby targeted to signal-transducing
microdomains termed caveolae. In endothelial cells, eNOS interacts with
caveolin-1, which represses eNOS enzyme activity. In cardiac myocytes,
eNOS associates with the muscle-specific caveolin-3 isoform, but
whether this interaction affects NO production and regulates myocyte
function is unknown. We isolated neonatal cardiac myocytes from mutant mice with targeted disruption of the eNOS gene and transfected them
with wild-type (WT) eNOS or myristoylation-deficient
(myr Boston Biomedical Research Institute, Harvard
Medical School, Boston, Massachusetts 02114
) eNOS mutant cDNA. In myocytes expressing
WT eNOS, the muscarinic cholinergic agonist carbachol completely
abrogated the spontaneous beating rate and induced a 4-fold elevation
of the cGMP level. By contrast, in the myr eNOS myocytes,
carbachol failed to exert its negative chronotropic effect and to
increase cGMP levels. We then used a reversible permeabilization
protocol to load intact neonatal rat myocytes with an oligopeptide
corresponding to the caveolin-3 scaffolding domain. This peptide
completely and specifically inhibited the carbachol-induced negative
chronotropic effect and the accompanying cGMP elevation. Thus, our
results suggest that acylated eNOS may couple muscarinic receptor
activation to heart rate control and indicate a key role for
eNOS/caveolin interactions in the cholinergic modulation of cardiac
myocyte function.
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