© 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
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 (IK)—and morphology. Cells are referred to as "KCa, KDR, or mixed," acknowledging the type of K+ channel that dominates the IK: the Ca2+-sensitive (KCa) channel, delayed rectifier (KDR) channel, or a mixture of both. The three cell types were identified by light and electron microscopy. KCa 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). KDR 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 KCa cells, whereas resistance arteries have a majority of KDR cells and few KCa cells. NO rapidly and reversibly increases IK and hyperpolarizes KCa cells because of an increase in open probability of a 170-pS KCa channel. Hypoxia depolarizes KDR cells by rapidly and reversibly inhibiting one or more of the tonically active KDR 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 KDR-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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K. Sato, Y. Morio, K. G. Morris, D. M. Rodman, and I. F. McMurtry Mechanism of hypoxic pulmonary vasoconstriction involves ETA receptor-mediated inhibition of KATP channel Am J Physiol Lung Cell Mol Physiol, March 1, 2000; 278(3): L434 - L442. [Abstract] [Full Text] [PDF]
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C. Austin and S. Wray Interactions Between Ca2+ and H+ and Functional Consequences in Vascular Smooth Muscle Circ. Res., February 18, 2000; 86(3): 355 - 363. [Abstract] [Full Text] [PDF]
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P. Ghisdal, J.-P. Gomez, and N. Morel Action of a NO donor on the excitation-contraction pathway activated by noradrenaline in rat superior mesenteric artery J. Physiol., January 1, 2000; 522(1): 83 - 96. [Abstract] [Full Text] [PDF]
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 E. D. Michelakis, E. K. Weir, D. P. Nelson, H. L. Reeve, S. Tolarova, and S. L. Archer Dexfenfluramine Elevates Systemic Blood Pressure by Inhibiting Potassium Currents in Vascular Smooth Muscle Cells J. Pharmacol. Exp. Ther., December 1, 1999; 291(3): 1143 - 1149. [Abstract] [Full Text]
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P.J. Boels, J. Deutsch, B. Gao, and S.G. Haworth Maturation of the response to bradykinin in resistance and conduit pulmonary arteries Cardiovasc Res, November 1, 1999; 44(2): 416 - 428. [Abstract] [Full Text] [PDF]
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C. B. Neylon, R. J. Lang, Y. Fu, A. Bobik, and P. H. Reinhart Molecular Cloning and Characterization of the Intermediate-Conductance Ca2+-Activated K+ Channel in Vascular Smooth Muscle : Relationship Between KCa Channel Diversity and Smooth Muscle Cell Function Circ. Res., October 29, 1999; 85 (9): e33 - e43. [Abstract] [Full Text] [PDF]
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J. T. Hulme, E. A. Coppock, A. Felipe, J. R. Martens, and M. M. Tamkun Oxygen Sensitivity of Cloned Voltage-Gated K+ Channels Expressed in the Pulmonary Vasculature Circ. Res., September 17, 1999; 85(6): 489 - 497. [Abstract] [Full Text] [PDF]
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L. A. Shimoda, J. T. Sylvester, and J. S. K. Sham Chronic hypoxia alters effects of endothelin and angiotensin on K+ currents in pulmonary arterial myocytes Am J Physiol Lung Cell Mol Physiol, September 1, 1999; 277(3): L431 - L439. [Abstract] [Full Text] [PDF]
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 S. L. Archer, H. L. Reeve, E. Michelakis, L. Puttagunta, R. Waite, D. P. Nelson, M. C. Dinauer, and E. K. Weir O2 sensing is preserved in mice lacking the gp91 phox subunit of NADPH oxidase PNAS, July 6, 1999; 96(14): 7944 - 7949. [Abstract] [Full Text] [PDF]
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K.-X. Li, B. Fouty, I. F. McMurtry, and D. M. Rodman Enhanced ETA-receptor-mediated inhibition of Kv channels in hypoxic hypertensive rat pulmonary artery myocytes Am J Physiol Heart Circ Physiol, July 1, 1999; 277(1): H363 - H370. [Abstract] [Full Text] [PDF]
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N. F. Voelkel, J. D. Allard, S. M. Anderson, and T. J. Burke cGMP and cAMP cause pulmonary vasoconstriction in the presence of hemolysate J Appl Physiol, May 1, 1999; 86(5): 1715 - 1720. [Abstract] [Full Text] [PDF]
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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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H. L. Reeve, D. P. Nelson, S. L. Archer, and E. K. Weir Effects of fluoxetine, phentermine, and venlafaxine on pulmonary arterial pressure and electrophysiology Am J Physiol Lung Cell Mol Physiol, February 1, 1999; 276(2): L213 - L219. [Abstract] [Full Text] [PDF]
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H. L. Reeve, E. K. Weir, S. L. Archer, and D. N. Cornfield A maturational shift in pulmonary K+ channels, from Ca2+ sensitive to voltage dependent Am J Physiol Lung Cell Mol Physiol, December 1, 1998; 275(6): L1019 - L1025. [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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I. S. Anand, B. A. K. Prasad, S. S. Chugh, K. R. M. Rao, D. N. Cornfield, C. E. Milla, N. Singh, S. Singh, and W. Selvamurthy Effects of Inhaled Nitric Oxide and Oxygen in High-Altitude Pulmonary Edema Circulation, December 1, 1998; 98(22): 2441 - 2445. [Abstract] [Full Text] [PDF]
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M. G. Berger, C. Vandier, P. Bonnet, W. F. Jackson, and N. J. Rusch Intracellular acidosis differentially regulates KV channels in coronary and pulmonary vascular muscle Am J Physiol Heart Circ Physiol, October 1, 1998; 275(4): H1351 - H1359. [Abstract] [Full Text] [PDF]
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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]
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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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J.-M. Hyvelin, C. Guibert, R. Marthan, and J.-P. Savineau Cellular mechanisms and role of endothelin-1-induced calcium oscillations in pulmonary arterial myocytes Am J Physiol Lung Cell Mol Physiol, August 1, 1998; 275(2): L269 - L282. [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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E. A. Aiello, A. T. Malcolm, M. P. Walsh, and W. C. Cole beta -Adrenoceptor activation and PKA regulate delayed rectifier K+ channels of vascular smooth muscle cells Am J Physiol Heart Circ Physiol, August 1, 1998; 275(2): H448 - H459. [Abstract] [Full Text] [PDF]
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C. Vandier, M. Delpech, and P. Bonnet Spontaneous transient outward currents and delayed rectifier K+ current: effects of hypoxia Am J Physiol Lung Cell Mol Physiol, July 1, 1998; 275(1): L145 - L154. [Abstract] [Full Text] [PDF]
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A. D. Giulumian, D. M. Pollock, N. Clarke, and L. C. Fuchs Coronary vascular reactivity is improved by endothelin A receptor blockade in DOCA-salt hypertensive rats Am J Physiol Regulatory Integrative Comp Physiol, June 1, 1998; 274(6): R1613 - R1618. [Abstract] [Full Text] [PDF]
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L. A. Shimoda, J. T. Sylvester, and J. S. K. Sham Inhibition of voltage-gated K+ current in rat intrapulmonary arterial myocytes by endothelin-1 Am J Physiol Lung Cell Mol Physiol, May 1, 1998; 274(5): L842 - L853. [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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C. H. Gelband and H. Gelband Ca2+ Release From Intracellular Stores Is an Initial Step in Hypoxic Pulmonary Vasoconstriction of Rat Pulmonary Artery Resistance Vessels Circulation, November 18, 1997; 96(10): 3647 - 3654. [Abstract] [Full Text]
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S. G. Clark and L. C. Fuchs Role of Nitric Oxide and Ca++-Dependent K+ Channels in Mediating Heterogeneous Microvascular Responses to Acetylcholine in Different Vascular Beds J. Pharmacol. Exp. Ther., September 1, 1997; 282(3): 1473 - 1479. [Abstract] [Full Text]
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