Energy cost of membrane depolarization in hog carotid artery.

Abstract

] 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...

Effect of histamine on the energy metabolism of K+-depolarized hog carotid artery.

“…The apparatus, mechanical and metabolic measurements, artery preparation, solutions, and pre-equilibration procedures are identical to those previously described (Peterson and Gliick, 1982). Experimental protocol was altered, however, as required by the observation that a Ca ++ -depletionrestoration cycle in the histamine-activated artery had a large effect on basal metabolic rates.…”

Contractile Protein Interactions in Smooth Muscle

“…This would be related to fg/f + g. As shown previously, the rate of energy expen diture or the total ATPase activity of mus cles may be linearly related to force [13]. Therefore, tension cost, that is the ratio of ATPase/force, is constant.…”

Energetics of crossbridge phosphorylation and contraction in vascular smooth muscle.

“…Other than the brief description of basal metabolism, all measurements of energy consumption are given as suprabasal values. Estimates of active energy expenditure are usually based on measurements of oxygen consumption (Jo 2 ), lactate production (J, ac ), phosphagen utilization in metabolically poisoned preparations, 31 P nuclear magnetic resonance, or heat production. Steady-state measurements are usually based on Jo 2 and J| ac measurements, whereas high-time resolution is provided by measurements of muscle heat production.…”

“…30 Resting J| ac is approximately 0.14 /umol/min • g. 31 Estimates of basal Jo 2 in swine carotid artery at 37°C range from 0.07 to 0.09 /xmol/min • g (wet weight). Basal metabolism is largely unaffected by changes in resting tension, 16 changes in extracellular calcium concentration, anoxia, or the level of hypertrophy (at least in visceral smooth muscle) 32 and shows little dependence on contraction history after a sufficient rest period between contractile events.…”

“…Basal metabolism is largely unaffected by changes in resting tension, 16 changes in extracellular calcium concentration, anoxia, or the level of hypertrophy (at least in visceral smooth muscle) 32 and shows little dependence on contraction history after a sufficient rest period between contractile events. 31 The biochemical basis for basal metabolism is far from clear. 33 However, it is likely that Na + -K + pumping and protein metabolism are major contributors.…”