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(Circulation Research. 1996;78:431-442.)
© 1996 American Heart Association, Inc.

Articles

Differential Distribution of Electrophysiologically Distinct Myocytes in Conduit and Resistance Arteries Determines Their Response to Nitric Oxide and Hypoxia

Stephen L. Archer, James M.C. Huang, Helen L. Reeve, Václav Hampl, Simona Tolarová, Evangelos Michelakis, E. Kenneth Weir

From the Cardiovascular Section (111C), VA Medical Center and University of Minnesota, Minneapolis.

Correspondence to Dr Stephen L. Archer (111C), Associate Professor of Medicine, Minneapolis VA Medical Center, One Veterans Dr, Minneapolis, MN 55417. E-mail arche002@maroon.tc.umn.edu.

Abstract The cellular mechanisms that determine differences in reactivity of arteries of varying size and origin are unknown. We evaluated the hypothesis that there is diversity in the distribution of K⁺ channels between vascular smooth muscle (VSM) cells within a single segment of the pulmonary arteries (PAs) and that there are differences in the prevalence of these cell types between conduit and resistance arteries, which contribute to segmental differences in the vascular response to NO and hypoxia. Three types of VSM cells can be identified in rat PAs on the basis of their whole-cell electrophysiological properties—current density and the pharmacological dissection of whole-cell K⁺ current (I_K)—and morphology. Cells are referred to as "K_Ca, K_DR, or mixed," acknowledging the type of K⁺ channel that dominates the I_K: the Ca²⁺-sensitive (K_Ca) channel, delayed rectifier (K_DR) channel, or a mixture of both. The three cell types were identified by light and electron microscopy. K_Ca cells are large and elongated, and they have low current density and currents that are inhibited by tetraethylammonium (5 mmol/L) or charybdotoxin (100 nmol/L). K_DR cells are smaller, with a perinuclear bulge, but have high current density and currents that are inhibited by 4-aminopyridine (5 mmol/L). Conduit arteries contain significant numbers of K_Ca cells, whereas resistance arteries have a majority of K_DR cells and few K_Ca cells. NO rapidly and reversibly increases I_K and hyperpolarizes K_Ca cells because of an increase in open probability of a 170-pS K_Ca channel. Hypoxia depolarizes K_DR cells by rapidly and reversibly inhibiting one or more of the tonically active K_DR channels (including a 37-pS channel) that control resting membrane potential. The effects of both hypoxia and NO on K⁺ channels are evident at negative membrane potentials, supporting their physiological relevance. The functional correlate of this electrophysiological diversity is that K_DR-enriched resistance vessels constrict to hypoxia, whereas conduit arteries have a biphasic response predominated by relaxation. Although effective in both segments, NO relaxes conduit more than resistance rings, in both cases by a cGMP-dependent mechanism. We conclude that regional electrophysiological diversity among smooth muscle cells is a major determinant of segmental differences in vascular reactivity.

Key Words: nitric oxide • hypoxia • pulmonary circulation • vascular smooth muscle • K⁺ channels

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				O. Clement-Chomienne, K. Ishii, M. P Walsh, and W. C Cole Identification, cloning and expression of rabbit vascular smooth muscle Kv1.5 and comparison with native delayed rectifier K+ current J. Physiol., March 15, 1999; 515(3): 653 - 667. [Abstract] [Full Text] [PDF]

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				S. O Brij and A. J Peacock Cellular responses to hypoxia in the pulmonary circulation Thorax, December 1, 1998; 53(12): 1075 - 1079. [Full Text]

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				A. M. Evans, O. N. Osipenko, S. G. Haworth, and A. M. Gurney Resting potentials and potassium currents during development of pulmonary artery smooth muscle cells Am J Physiol Heart Circ Physiol, September 1, 1998; 275(3): H887 - H899. [Abstract] [Full Text] [PDF]

				H M Prior, M S Yates, and D J Beech Functions of large conductance Ca2+-activated (BKCa), delayed rectifier (KV) and background K+ channels in the control of membrane potential in rabbit renal arcuate artery J. Physiol., August 15, 1998; 511(1): 159 - 169. [Abstract] [Full Text] [PDF]

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				G. J. Waldron, S. B. Sigurdsson, E. A. Aiello, A. J. Halayko, N. L. Stephens, and W. C. Cole Delayed rectifier K+ current of dog bronchial myocytes: effect of pollen sensitization and PKC activation Am J Physiol Lung Cell Mol Physiol, August 1, 1998; 275(2): L336 - L347. [Abstract] [Full Text] [PDF]

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				A. J. Halayko, E. Rector, and N. L. Stephens Airway smooth muscle cell proliferation: characterization of subpopulations by sensitivity to heparin inhibition Am J Physiol Lung Cell Mol Physiol, January 1, 1998; 274(1): L17 - L25. [Abstract] [Full Text] [PDF]

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				S. V. Smirnov, R. Beck, P. Tammaro, T. Ishii, and P. I Aaronson Electrophysiologically distinct smooth muscle cell subtypes in rat conduit and resistance pulmonary arteries J. Physiol., December 19, 2001; (2001) 200101300. [Abstract] [PDF]