Excitation-contraction coupling and electrical events in two types of vascular smooth muscle

Somlyo, Avril V.; Vinall, P.; Somlyo, Andrew P.

doi:10.1016/0026-2862(69)90014-4

Cited by 93 publications

(38 citation statements)

References 25 publications

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“…In trachealis smooth muscle, phosphatidylinositol turnover is increased by cholinergic stimulation but not by sustained depolarization with high K alone, suggesting that pharmacomechanical coupling is mediated through some step ih phospholipid metabolism (15). The effect of InsP3 on rabbit MPA, a tonic smooth muscle that responds in a graded fashion to stimulation (8,28) similar to the trachealis (35) and is readily activated by pharmacomechanical coupling (6), provides further support for such a mechanism. Ca can be released from the central SR in this tissue (1); thus, if InsP3 is a messenger, it may have to diffuse to the central SR from the surface membrane where it is produced in response to the action of agonists on plasmalemmal receptors.…”

mentioning

confidence: 86%

Inositol trisphosphate-induced calcium release and contraction in vascular smooth muscle.

Somlyo¹,

Bond²,

Somlyo³

et al. 1985

Proc. Natl. Acad. Sci. U.S.A.

359

142

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Inositol 1,4,5-trisphosphate (InsP3) caused Ca release and tension development in rabbit main pulmonary artery smooth muscle permeabilized with saponin or digitonin. Both of these responses to single additions of uM) were repeatable and occurred in the presence of 0.0-1.9 mM free Mg +. Sustained contractions were induced by InsP3. The amount of Ca released by InsP3, measured with a Ca21-selective electrode, was also estimated to be sufficient to stimulate contraction in intact smooth muscle. Ca release was not influenced by inhibitors of mitochondrial oxidative phosphorylation. The uptake of Ca21 from the medium into the InsP3-sensitive pool was ATP-dependent. The present results support the hypothesis that, in smooth muscle, InsP3 is the messenger, or one of the messengers, involved in transmitterinduced (pharmacomechanical) Ca release from the sarcoplasmic reticulum, which is the intracellular Ca store identified previously as the source of Ca released by norepinephrine in main pulmonary artery.Activation of smooth muscle by transmitters and drugs involves, at least in part, the release of intracellular Ca (1-3), followed by Ca activation ofthe calmodulin-regulated myosin light chain kinase (4). The release of intracellular Ca does not require influx of extracellular Ca (5-7) and can be triggered by pharmacomechanical coupling, a process independent of changes in surface membrane potential (8). Recent electron probe analytic studies have directly demonstrated that the sarcoplasmic reticulum (SR) is the source of intracellular Ca released by norepinephrine in rabbit main pulmonary artery (MPA) (1), portal vein (7), and, probably, other smooth muscles. However, until very recently, the mechanism through which drugs and transmitters released Ca from the SR remained unknown.The recognition, in nonmuscle cells, that stimulation of phosphatidylinositol turnover, stimulated by cholinergic agents and other secretogogues (9, 10), is associated with the production of a metabolite, inositol 1,4,5-trisphosphate (Ins-P3), that can release Ca from the endoplasmic reticulum (11, 12) indicated that InsP3 may also function as an excitatory messenger in smooth muscle. In this study, we demonstrate that InsP3 can, indeed, release Ca from smooth muscle cells of the rabbit MPA, as indicated by Ca2+-selective electrode measurements and by InsP3-induced contraction of vascular strips permeabilized with saponin or digitonin. The quantity of Ca2' released by InsP3, like that released from the SR by norepinephrine in this tissue (1), is sufficient for the activation of contraction. These and other recent studies of phosphatidylinositol turnover (including its stimulation by norepinephrine) and of the effects of InsP3 in smooth muscle (13)(14)(15)(16)(17) provide further evidence for the possibility that InsP3 is a physiological messenger mediating agonist-induced Ca release in smooth muscle. MATERIALS AND METHODSTissue Preparation. Male New Zealand rabbits (1-2 kg of body weight) were killed by a blow on the back of the head...

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mentioning

confidence: 86%

Inositol trisphosphate-induced calcium release and contraction in vascular smooth muscle.

Somlyo¹,

Bond²,

Somlyo³

et al. 1985

Proc. Natl. Acad. Sci. U.S.A.

359

142

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“…In all three conditions, activation with high extracellular K + is used. It is wellestablished that activation of vascular smooth muscle (VSM) contraction by high-K + solution occurs through membrane depolarization (Burnstock and Straub, 1958;Somlyo et al, 1969), yielding increased transmembrane permeability to extracellular Ca ++ (Briggs, 1962;Hudgins and Weiss, 1968) as well as an exchange/release of some loosely bound fraction of intraceliular Ca ++ (Hinke, 1965;Weiss, 1975). An inward flux of extracellular Ca ++ maintains an elevated cytoplasmic free-Ca ++ level (Van Breeman et al, 1973;Karaki and Weiss, 1980), thus activating a stable contracture (Bohr, 1963;Bohr et al, 1978) as well as, undoubtedly, other Ca ++ -sensitive processes.…”

Section: Energy Cost Of Membrane Depolarization In Hogmentioning

confidence: 99%

Energy cost of membrane depolarization in hog carotid artery.

Peterson¹,

Glück²

1982

Circulation Research

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] and varying Ca ++ by less than 2.5% at all levels of activation, which was not statistically significant (P > 0.70). We conclude therefore that the steady state metabolic energy cost of membrane depolarization per se during contractile activity in vascular smooth muscle from a tonic conducting vessel (hog carotid artery) is negligible. Although the possibility cannot be excluded, we find no metabolic evidence that increased cytoplamic free-Ca ++ itself activates an ATPase associated with Ca ++ sequestration and/or extrusion beyond that present in the relaxed state. Activation of hog carotid artery with an isosmotic K + -for-Na + -substituted medium fails to stimulate aerobic glycolysis at all levels of K + substitution. Experiments were performed at the muscle length optimal for isometric tension generation and at 37°C. (Ore Res 50: 839-847, 1982) \N THIS and a subsequent report (Peterson 1982), we compare the metabolic energy cost of isometric tension maintenance in the isolated hog carotid artery under three sets of activating conditions by which the level of isometric tension development may be altered in a stable graded fashion. In all three conditions, activation with high extracellular K + is used. It is wellestablished that activation of vascular smooth muscle (VSM) contraction by high-K + solution occurs through membrane depolarization (Burnstock and Straub, 1958;Somlyo et al., 1969), yielding increased transmembrane permeability to extracellular Ca ++ (Briggs, 1962;Hudgins and Weiss, 1968) as well as an exchange/release of some loosely bound fraction of intraceliular Ca ++ (Hinke, 1965;Weiss, 1975). An inward flux of extracellular Ca ++ maintains an elevated cytoplasmic free-Ca ++ level (Van Breeman et al., 1973;Karaki and Weiss, 1980), thus activating a stable contracture (Bohr, 1963;Bohr et al., 1978) as well as, undoubtedly, other Ca ++ -sensitive processes. In previous studies on intact isolated arteries and veins, we have investigated the energy metabolism of VSM contractility and identified quantitatively those components of overall energy metabolism associated with the d'rect maintenence of isometric tension (i.e., actomyosin ATPase) and those associated with tension-development processes or "activation" per se (Peterson and Paul, 1974a;Paul and Peterson, 1975 1977). Activation energy metabolism was measured as that part of overall suprabasal energy metabolism that remains when tension-dependent metabolism in a fully activated smooth muscle preparation is abolished, and represents the metabolic energy requirements of processes such as increased transmembrane ion pumping, phosphorylation/dephosphoryiation cycles, and energy-dependent intraceliular Ca + "* translocation.The studies described below were undertaken to examine in more detail the energetics of particular processes which constitute some part of the "activation energy." In this report, we focus on the metabolic energy cost due to membrane depolarization per se, whereas a subsequent report (Peterson 1982) examines the excess metabol...

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“…In the course of investigations on excitation-contraction coupling in the rabbit main pulmonary artery, a vascular smooth muscle which does not generate action potentials (Somlyo & Somlyo, 1968;Somlyo, Vinall & Somlyo, 1969), we observed that TEA produced slow tonic contractions of rapid onset associated with an increase in intracellular calcium concentration and with an enhancement of the contractile responses to noradrenaline and high potassium. Long-lasting exposure of the rabbit main pulmonary artery to TEA led to the induction of spontaneous mechanical activity.…”

mentioning

confidence: 99%

Effects of tetraethylammonium chloride on contractile, membrane and cable properties of rabbit artery muscle.

Haeusler¹,

Thorens²

1980

The Journal of Physiology

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SUMMARY1. Two types of effects of tetraethylammonium chloride (TEA) have been found in the smooth muscle cells of the rabbit main pulmonary artery. (a) With rapid onset of action TEA depolarizes the cell membrane, increases the membrane resistance, causes anomalous rectification and occasionally spike potentials in response to externally applied depolarizing current pulses and produces tonic contractions.(b) During prolonged (> 30 min) incubation in TEA phasic contractions develop progressively and the vascular strips respond to electrical stimulation with synchronized and powerful contractions.2. There is a linear relationship between log concentration TEA and depolarization over the range of 10-100 mM-TEA. TEA (10 and 30 mM) raises the membrane resistance and decreases the core resistance. The latter effect appeared to develop more slowly than the former.3. During short exposure to TEA part of the smooth muscle cells respond to depolarizing current pulses with spike potentials of variable amplitude and duration. These spikes are very sensitive to inhibition by verapamil or nickel chloride but are not affected by tetrodotoxin. The amplitude of electrotonic potentials, increased by TEA, is slightly further elevated by verapamil or nickel chloride.4. TEA (10 mM) increases the mechanical response to low and intermediate potassium concentrations but has no effect on maximal contractions to high potassium. The slope of the line relating log potassium concentration to membrane potential is decreased by TEA.5. TEA (10 mM) shifts the concentration response curve for the contractile effect of noradrenaline to the left and increases the maximum of noradrenaline-induced contractions. In the presence of TEA, noradrenaline reduces the membrane potential to markedly lower values than under control conditions. 6. It is concluded that the rapidly occurring effects of TEA on the vascular smooth muscle cells of the rabbit main pulmonary artery are a decrease in potassium and an increase in calcium conductance. The latter effect may be related to a blockade of potassium channels; however, we cannot rule out the possibility that TEA affects calcium conductance independent of its presumed action on potassium channels. The slowly developing effects of TEA may be ascribed to the formation of gap junctions and/or (less likely) to an intracellular accumulation of TEA.

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Excitation-contraction coupling and electrical events in two types of vascular smooth muscle

Cited by 93 publications

References 25 publications

Inositol trisphosphate-induced calcium release and contraction in vascular smooth muscle.

Inositol trisphosphate-induced calcium release and contraction in vascular smooth muscle.

Energy cost of membrane depolarization in hog carotid artery.

Effects of tetraethylammonium chloride on contractile, membrane and cable properties of rabbit artery muscle.

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