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Am J Physiol Heart Circ Physiol 276: H194-H204, 1999;
0363-6135/99 $5.00
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Vol. 276, Issue 1, H194-H204, January 1999

Mechanism of prejunctional muscarinic receptor-mediated inhibition of neurogenic vasodilation in cerebral arteries

J. Liu and T. J. F. Lee

Department of Pharmacology, Southern Illinois University School of Medicine, Springfield, Illinois 62794-9629

Nitric oxide (NO) is a major transmitter in mediating cerebral neurogenic vasodilation in several species. Recent findings have suggested that acetylcholine, which is costored with NO in cerebral perivascular nerves, plays a role in modulating NO release, presumably by acting on muscarinic (M) receptors on nitric oxidergic nerve terminals. The present study was designed using an in vitro tissue bath technique to pharmacologically characterize the presynaptic muscarinic-receptor subtype(s) that mediate modulation of NO release and therefore neurogenic vasodilation and to investigate further the possible mechanisms involved in this presynaptic modulation in porcine basilar arteries. Transmural nerve stimulation (TNS) elicited a frequency-dependent, tetrodotoxin-sensitive relaxation. The relaxation was abolished by nitro-L-arginine (30 µM) and was completely reversed by L-arginine and L-citrulline, but not by their D-enantiomers. Atropine (0.01-1 µM), pirenzepine (an M1-receptor antagonist, 0.01-1 µM), and methoctramine (an M2-receptor antagonist, 0.01-1 µM), but not 4-DAMP (an M3-receptor antagonist) or tropicamide (an M4-receptor antagonist) at concentrations as high as 10 mM, significantly increased the TNS-elicited relaxation. This relaxation, on the other hand, was significantly attenuated by arecaidine but-2-ynyl ester tosylate (an M2-receptor agonist, 0.1 µM) but was not affected by McN-A-343 (an M1-receptor agonist, 1 µM). Double-labeling immunohistochemical study demonstrated that perivascular M2 receptor-immunoreactive fibers were completely coincident with NADPH diaphorase fibers. Furthermore, the muscarinic receptor-mediated modulation of TNS-elicited relaxation was completely prevented by omega -conotoxin GVIA (0.1 µM), a specific N-type Ca2+ channel inhibitor, but was still observed in the presence of tetraethylammonium (1 mM), 8-bromo-cAMP (0.5 mM), and pertussis toxin. It is concluded that the presynaptic M2 receptors on porcine cerebral perivascular nitric oxidergic nerves mediate inhibition of NO release. The inhibition is due primarily to a decreased Ca2+ influx through N-type Ca2+ channels.

nitric oxide; presynaptic muscarinic receptor; transmural nerve stimulation; M2 receptor-immunoreactive fibers; N-type calcium channel; cerebral blood vessels; porcine


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