Electrical activation of endothelium evokes vasodilation and hyperpolarization along hamster feed arteries.
Endothelial cells are considered electrically unexcitable. However, endothelium-dependent vasodilators (e.g., acetylcholine) often evoke hyperpolarization. We hypothesized that electrical stimulation of endothelial cells could evoke hyperpolarization and vasodilation. Feed artery segments (resting diameter: 63 +/- 1 microm; length 3-4 mm) of the hamster retractor muscle were isolated and pressurized to 75 mmHg, and focal stimulation was performed via microelectrodes positioned across one end of the vessel. Stimulation at 16 Hz (30-50 V, 1-ms pulses, 5 s) evoked constriction (-20 +/- 2 microm) that spread along the entire vessel via perivascular sympathetic nerves, as shown by inhibition with tetrodotoxin, omega-conotoxin, or phentolamine. In contrast, stimulation with direct current (30 V, 5 s) evoked vasodilation (16 +/- 2 microm) and hyperpolarization (11 +/- 1 mV) of endothelial and smooth muscle cells that conducted along the entire vessel. Conducted responses were insensitive to preceding treatments, atropine, or N(omega)-nitro-L-arginine, yet were abolished by endothelial cell damage (with air). Injection of negative current (</=1.6 nA) into a single endothelial cell reproduced vasodilator responses along the entire vessel. We conclude that, independent of ligand-receptor interactions, endothelial cell hyperpolarization evokes vasodilation that is readily conducted along the vessel wall. Moreover, electrical events originating within a single endothelial cell can drive the relaxation of smooth muscle cells throughout the entire vessel.
Emerson
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The John B. Pierce Laboratory and Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut 06519, USA.
Segal
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D000317:Adrenergic alpha-Antagonists / Q000494:pharmacology; D000818:Animals; D001158:Arteries / Q000502:physiology*; D006224:Cricetinae; D004558:Electric Stimulation; D004594:Electrophysiology; D004730:Endothelium, Vascular / Q000166:cytology / Q000502:physiology*; D004791:Enzyme Inhibitors / Q000494:pharmacology; D066298:In Vitro Techniques; D008297:Male; D008647:Mesocricetus; D008839:Microelectrodes; D018482:Muscle, Skeletal / Q000098:blood supply; D010646:Phentolamine / Q000494:pharmacology; D013779:Tetrodotoxin / Q000494:pharmacology; D014655:Vascular Resistance; D014664:Vasodilation / Q000502:physiology*; D020960:omega-Conotoxins / Q000494:pharmacology; D019323:omega-N-Methylarginine / Q000494:pharmacology
D000317:Adrenergic alpha-Antagonists; D004791:Enzyme Inhibitors; D020960:omega-Conotoxins; D019323:omega-N-Methylarginine; D013779:Tetrodotoxin; D010646:Phentolamine