Department of Physiological Sciences, Biomedical Centre, University of Lund, S-221 84 Lund, Sweden
Submitted 31 October 2003 ; accepted in final form 25 February 2004
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ABSTRACT |
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muscle contraction; pH
The influence of intracellular pH on the kinetic properties of the contractile system has previously been explored in considerable detail during tetanic activity of frog single muscle fibers, i.e., under conditions where the myofilament system has been fully activated (14, 15, 2022, 54). Results from such studies show that a drop in pH from 7.0 to 6.5 leads to lowered capacity to produce force but only to a minor change in fiber stiffness (Ref. 20; see also Ref. 44 for frog whole sartorius muscle), suggesting that the decrease in active force is mainly due to reduced force output of the individual cross bridges with little change in the actual number of attached bridges. Lowered intracellular pH also leads to a decrease in the maximum speed of shortening, as originally demonstrated by Edman and Mattiazzi (22) using the slack-test method (17). The latter observation provides evidence that the turnover rate of the myosin cross bridges is reduced by acidification, which is in line with the finding that a drop in pH inhibits the rate of ATP breakdown by myofibrils in suspension (see above). The contractile changes induced by lowered pH are strikingly similar to those recorded during fatigue of isolated muscle, indicating that intracellular acidification might play a significant part during development of muscle fatigue in amphibian muscle.
The depressant effects of lowered pH on force and speed of shortening also appear in isolated mammalian muscle (e.g., Ref. 53) and accord well with the effects observed in frog muscle when tested at relatively low (1520°C) temperatures. However, there is evidence from studies of both intact (43, 53, 55) and skinned (40) mammalian muscles that the contractile effects of acidification diminish with increasing temperature and virtually disappear as the temperature is raised toward physiological levels (3035°C). The latter observations make it seem unlikely that intracellular acidification is a principal cause of fatigue of mammalian muscle in vivo.
So far, there has been no systematic study that enables a quantitative comparison of the contractile effects of acidification at different temperatures in frog muscle, the preparation often employed in previous studies of muscle function. The present investigation has been performed to fill this gap. To this end, measurements of force, instantaneous stiffness, and force-velocity relationships were performed on single frog muscle fibers, both at normal and lowered intracellular pH, while the fibers were exposed to different temperatures between 0 and 22°C, i.e., temperatures normally encountered by these animals. Our results show that, in maximally activated fibers, intracellular acidification, like moderate fatigue, depresses the tetanic force to the same degree at the different temperatures studied. The onset of activation, on the other hand, being markedly delayed by lowered pH and fatiguing stimulation at low temperature, becomes substantially faster by these two interventions as the temperature is raised. Some of these results have been described in a preliminary form (42).
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METHODS |
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The fiber was mounted horizontally in a Perspex chamber between a force transducer and an electromagnetic puller. The fiber tendons were held by aluminium clips as described previously (20, 23). The muscle chamber was covered to provide a constant environment around the fiber. The experiments were carried out at a resting sarcomere length of 2.1 µm. Fiber length, cross-sectional area, and sarcomere length were measured as described by Edman and Reggiani (23).
Solutions. The dissection of the muscle fibers was carried out in a standard Ringer solution containing (in mM) 115.5 NaCl, 2.0 KCl, 1.8 CaCl2, 2.0 Na2HPO4 + NaH2PO4, pH 7.0, at 2.0°C. For the actual experiments, a bicarbonate Ringer solution of the following composition was used (in mM): 108.0 NaCl, 2.0 KCl, 1.8 CaCl2, 10.0 NaHCO3. The solution was bubbled with mixtures of CO2 and O2 to give a pH of 7.0 or 6.26.3 at the temperature used in the muscle chamber (14). The bathing solution, which was thermostatically controlled to within 0.2°C, was continuously perfused through the muscle chamber (volume ca. 2.5 ml) at a speed of 2 ml/min. The experiments were performed at a given temperature within the range of 222°C as stated in RESULTS. Both temperature and pH of bathing solution in the chamber were measured periodically during the experiment.
Stimulation.
Fibers were stimulated by passing rectangular current pulses between two platinum-plate electrodes placed symmetrically on either side of the fiber 2 mm from it. The pulse duration was 0.2 ms, and the frequency used for tetanic stimulation (1622 Hz at low temperature and 6580 Hz at high temperature) was adjusted to give a fused tetanus of 600- to 1,000-ms duration. The interval between tetani was 3 min, except in some experiments where the interval was reduced from 180 to 15 or 30 s to induce fatigue of the fiber (fatiguing stimulation; Ref. 22). The strength of the electrical stimulus was set
15% above the twitch threshold and was adjusted, if required, during the experiment as the stimulation threshold changes with both temperature and pH.
Force transducer.
The principal unit of the transducer was a semiconductor strain-gauge element (AE 801, Aksjeselskapet Mikroelectronikk, Horten, Norway). To make the transducer suitable for stiffness measurements, a distal portion (2 mm in length) of the silicon bar was removed. The force transducer so modified had a resonant frequency of 19 kHz when submerged in the bathing fluid. There was no detectable "creep" of the transducer signal after a sudden unloading of the transducer (see Ref. 20).
Electromagnetic puller. Two different electromagnetic pullers were used in this study. Motor number 1 allowed relatively large semifast movements and was employed in experiments for force-velocity measurements and slack tests (for description, see Ref. 23). Motor number 2 had the capacity to produce fast, low-amplitude length changes and was used in experiments that involved stiffness measurements. A description of motor number 2 has been given by Edman and Lou (20).
Measurement of fiber stiffness. Stiffness was measured by recording the changes in force that occurred in response to an imposed sinusoidal length oscillation as fully described previously (20). The frequency of the length oscillation was 2 kHz, and the peak-to-peak amplitude was 1011 µm, corresponding to 1.61.8 nm per half sarcomere. This means that the fiber underwent alternating stretches and releases of <1 nm/half sarcormere in amplitude, about the unperturbed length of the fiber. The stiffness measurement was thus performed within the straight portion of the stress-strain relationship of the sarcomere elasticity located above and below the isometric force (see Refs. 25, 37). The stretch and release movements produced during the stiffness measurement were completed in 0.250 ms. The cyclic length changes may thus be considered rapid enough to provide a useful index of the instantaneous stiffness of active muscle (25, 31).
The oscillation was initiated just before the onset of stimulation and usually continued until the shoulder of the relaxation phase had been passed. A stiffness signal was formed by passing the signal from the force transducer through a narrow band-pass filter (Q value of 5.5), the optimum frequency of which was set to the actual frequency of the length oscillation used. By rectifying the filtered signal, a direct read-out of the fiber stiffness could be obtained during the course of the tetanus (see Fig. 1 in Ref. 20). The bandwidth of the rectified signal was DC-1.3 kHz. The force signal without the superimposed force oscillation was recorded simultaneously by using a notch filter, which produced maximum attenuation at the frequency (2 kHz) used for the length oscillation. The signal from the position transducer of the puller producing the fast length oscillation was treated in the same way as described for the force transducer to provide a measurement of the peak-to-peak amplitude of the length oscillation.
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Recording of signals. Force, puller position, and in some experiments stiffness measurements were recorded on a digital oscilloscope and stored on disk.
Velocity of unloaded shortening. The speed of unloaded shortening was measured with the slack-test method (17). To this end, the fiber was quickly released by an amount great enough to bring the force to zero. Three different amplitudes of release were produced, and each one was repeated three times in separate runs. The releases were carried out on the plateau of the isometric tetanus 500 ms after the onset of stimulation. A plot of the release amplitude against the time from release to the onset of force development (slack time) forms a straight line (determined by linear regression), the slope of which represents the shortening velocity under zero load (V0) (17). The results of a representative slack-test experiment are shown in Fig. 6.
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RESULTS |
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Example records of tetanic force and instantaneous stiffness derived at 2.4 and 19.4°C are illustrated in Fig. 1. Figure 1A shows two superimposed records of the tetanic force recorded at low and high temperature, and Fig. 1B illustrates the corresponding stiffness myograms. It can be seen, in accordance with earlier observations (see Ref. 56), that raising the temperature led to a steeper rise of force, a greater amplitude of force, and a faster relaxation phase. In 30 fibers investigated, the maximal tetanic force increased by 38.4 ± 2.4% as the temperature changed from 2.9 ± 0.1 to 20.5 ± 0.2°C. Stiffness, on the other hand, was found to decrease by 10.6 ± 2.9% as the temperature was raised over the same interval (see below for further details).
In accordance with previous observations at low temperature in frog muscle (3, 8, 20, 26, 29), Fig. 1, C and D, demonstrates that stiffness was in the lead of tension during the rising phase of the tetanus, and this applies to both low and high temperatures. The stiffness remained constant during the plateau phase of the tetanus and lagged behind tension during the relaxation phase.
In three experiments, simultaneous measurements of tetanic force and tetanic stiffness were performed at four to five different temperatures within the range 2.420.1°C. The results show (Fig. 2A) that force and stiffness do not undergo proportional changes as the temperature is altered. Thus, by raising the temperature from a range of 2.43.5°C to 8.2, 8.4, and 9.0°C in the three different experiments, the stiffness increased by merely 1.2, 2.4, and 6.5%, respectively. At the same time, tetanic force increased by 17.7, 45.9, and 24.1% of the value recorded at 2.43.5°C. By stepwise increasing the temperature from 9 to 20°C, there was a slight further increase in tetanic force (Fig. 2A) while, at the same time, the stiffness decreased to a value below that derived at 2.43.5°C (Fig. 2A, also see Fig. 1B). The unequal temperature dependence of force and stiffness depicted in Fig. 2A results in a rectilinear increase of the force-to-stiffness ratio (Q10 = 1.41) as the temperature is raised from
3 to 20°C (Fig. 2B). A similar observation was reported by Galler and Hilber (27) in studies on skinned rat skeletal muscle fibers. Assuming that the measured stiffness reflects the number of attached cross bridges (31), the results provide evidence that the average force produced by a cross bridge during a working cycle steadily increases as the temperature is raised within the temperature range considered.
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The dotted curves in Fig. 2B illustrate the estimated force-stiffness relationship of the cross bridges at different temperatures when account is made of the presence of thin-filament compliance amounting to 50% of the total sarcomere compliance. It is reasonable to assume that the elasticity of the free portion of thin filament has a low temperature dependence (see Ref. 38). The closed squares in Fig. 2B show the calculated force-to-stiffness ratio when the series compliance is assumed to be independent of temperature, whereas the closed triangles show the situation when the series compliance varies with temperature with a Q10 of 1.20. It can be seen that, even in the latter case, there is a substantial increase (40%) of the force-to-stiffness ratio as the temperature is raised from 3 to 20°C.
Effects of intracellular acidification on tetanic force and tetanic stiffness: influence of temperature.
The fibers, immersed in bicarbonate-CO2-buffered bathing solution at 23°C, were stimulated to produce a fused tetanus at regular 3-min intervals with recording of force and, in some experiments, with simultaneous measurements of fiber stiffness. After constant responses had been attained at pH 7.0, the pH of the bathing fluid was reduced to 6.3 by raising the CO2 concentration of the medium, and the fiber was tetanized at 3-min intervals as before. By reducing the pH, the tetanic force declined, reaching a constant level within 30 min. The above sequence of events was thereafter carried out at a temperature close to 20°C. In other experiments, the order of temperature changes was the opposite, i.e., measurements at normal and reduced pH were first carried out at the high temperature level (
20°C) and were followed by similar measurements near 2°C.
Figure 3 illustrates typical records of force and stiffness during isometric tetani at normal pH and during acidification at 2.4 and 19.4°C. At both high and low temperatures, the maximum tetanic force was moderately reduced by lowering the pH. In 10 fibers investigated, the reduction of force by acidification was 13.5 ± 1.2% at low temperature, whereas the corresponding decrease recorded at the high temperature was 11.5 ± 1.4% (Table 1). The difference between these two values was not statistically significant (P > 0.1, n = 10). As illustrated in Fig. 3B, stiffness was reduced less by acidosis than force was, and this applies to measurements at both high and low temperature. In five fibers, the decrease in stiffness during acidification was merely 5.6 ± 2.8% (P < 0.08) and 4.0 ± 2.6% (P < 0.16) at low and high temperature, respectively; these changes were not statistically significant.
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It was of interest to learn whether the increase in speed of force development induced by acidification at high temperature also occurred in response to fatiguing stimulation. Figure 5 shows an experiment to test this point, and Table 1 summarizes the results from a whole series of similar experiments at 20°C. The fiber, initially equilibrated at pH 7.0 (control 1, Fig. 5), was subjected to acidosis at pH 6.27. This caused a substantial increase in the rate of rise of force (acidification in Fig. 5), in accordance with the results presented in Fig. 4. After return to the control medium of pH 7.0, which restored the rate of force development to its original value (control 2, Fig. 5), the fiber was subjected to a period of fatiguing stimulation at pH 7.0 by reducing the intervals between tetani from 3 min to 15 s. This led to a steepening of the rising phase of the tetanus (fatigue in Fig. 5), which agreed well with the effects induced by acidification at the high temperature. The mean values of the effects produced by acidification and fatiguing stimulation are presented for comparison in Table 1. The results show that, as maximum tetanic force was depressed by 12% by acidification and fatiguing stimulation, the time to 70% of maximum force was reduced by 2025% by the two interventions. These findings provide yet another example of the striking similarities between the contractile effects of fatiguing stimulation and acidification that have previously been demonstrated in frog muscle fibers (22).
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DISCUSSION |
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Temperature dependence of the contractile effects of intracellular acidification.
Previous studies have demonstrated that frog muscle fibers that are brought to fatigue by frequent activation at low (23°C) temperature lose part of their capacity to produce force at the same time as their maximum speed of shortening is substantially reduced (15, 22). These changes were found to accord remarkably well with the effects induced by intracellular acidification (20, 22), supporting the view that lowered intracellular pH is an important factor in the development of fatigue induced by frequent stimulation of amphibian muscle. Similar to the observation in frog muscle, lowered intracellular pH does have a depressant effect on both force and shortening velocity also in mammalian muscle at relatively low (15°C) temperature. Surprisingly, however, lowered pH has been found to exert virtually no effect on the contractile performance at higher, more physiological temperatures, 2830°C (40, 43). This finding would seem to imply that pH, contrary to previous assumptions, plays an insignificant role in the development of fatigue of mammalian muscle in vivo.
The present study provides evidence that the temperature dependence of the pH effects observed in mammalian muscle does not apply to amphibian muscle fibers. The experiments, performed on isolated single muscle fibers of the frog, included measurements of maximum speed of shortening, force, and instantaneous stiffness during fused tetani, and the effects of intracellular acidification were tested over a temperature range (022°C) that is normally encountered by the frogs used. The intracellular pH changes were achieved by varying the CO2 concentration of the extracellular medium at constant bicarbonate concentration to give pH 7.0 and 6.3 at the different temperatures tested. According to measurements presented by Curtin et al. (16), these changes in pH of the extracellular medium can be presumed to be associated with quite similar intracellular changes at the temperatures studied.
The results show that acidification reduces the maximum tetanic force and also markedly prolongs the relaxation phase, effects that are characteristic of muscle fatigue. The tetanic force was reduced by 1214% by lowering the pH from 7.0 to 6.3, and this effect, like the slowing of relaxation, was unaffected by temperature within the range investigated. Similar to the situation during moderate fatigue (21), the force depression produced by acidification was associated with only a minor reduction in fiber stiffness, suggesting that lowered pH makes the cross bridges less capable of producing force without causing a proportional decrease in the number of active cross bridges. The results furthermore demonstrate that this effect is not significantly dependent on temperature. The experimental results obtained so far would thus seem to make clear that intracellular acidification puts the muscle in a state that is virtually indistinguishable from moderate fatigue, i.e., the milder form of fatigue (18, 21), in which the tetanic force is depressed by not more than 30% of the rested-state value. This by no means excludes that accumulation of other products of the ATP hydrolysis, such as Mg-ADP and Pi, also affects the cross-bridge function during moderate fatigue. The actions of ADP and Pi on force and shortening velocity have been reported in several studies on skinned muscle fibers (1, 10, 13, 28, 34, 48, 49), and a summary of these effects has been presented earlier (15, 22). It is clear, however, that the combined actions of the two hydrolysis products do not eliminate the close relationship that exists between the contractile changes recorded during intracellular acidification and moderate fatigue in frog muscle.
It is well known from previous studies of both amphibian and mammalian muscles that the decrease in tetanic force during fatigue and intracellular acidification is associated with a lower rate of force development. This is regularly observed in frog muscle preparations at the low temperatures generally used (e.g., Refs. 20, 22, 44). The reduced speed of force development is at least partly attributable to the change of the force-velocity relationship that occurs under these conditions leading to a lower speed of shortening at low and intermediate loads (15, 22). The present results demonstrate that fatigue and acidification of frog muscle fibers at high temperature (20°C) affect the rising phase of the tetanus in a way that is opposite to that observed at low temperature. That is, whereas the maximum tetanic force is depressed to the same extent at low and high temperature (Table 1), the rate of rise of force is increased by fatigue and acidification at the high temperature. These patterns of effects were fully reversible when the temperature was changed intermittently in each individual fiber tested.
The mechanism underlying the increased rate of rise of force during fatigue and acidification at high temperature is unclear and requires further investigation. As pointed out above, the basic effect of the two interventions can be presumed to be a slowing of the tension rise during tetanic stimulation at both low and high temperature in view of the fact that the speed of shortening is depressed in both cases. It is, therefore, logical to presume that the two interventions, fatigue and acidification, in addition to their depressant effect on cross-bridge function (20, 21), also increase the rate of activation of the contractile system, an effect that may become predominant at high temperatures. The possibility that the faster rise of force at high temperature might reflect an increased rate of attachment of the myosin cross bridges during fatigue and acidification can probably be excluded, because this would enhance the maximum tetanic force as well above the control level.
Variation in force output of attached cross bridges with altered temperature. According to the cross-bridge model of muscle contraction, the measured isometric force is a function of the number of attached cross bridges and the average force generated per cross bridge. A change in either of these two variables may be evaluated by simultaneously recording the force output of the muscle fiber and the instantaneous stiffness of the fiber, the latter measurement being used as an index of the number of attached cross bridges. Results from several previous studies on both frog and mammalian muscle preparations have shown that an increase in temperature results in a smaller rise in stiffness than in force, suggesting that the force output per bridge is enhanced with increasing temperature (7, 25, 27). The present study extends earlier work by providing a detailed account of the simultaneous changes in force and stiffness that occur as the temperature is altered in discrete steps between 2 and 22°C. By using the ratio between force and stiffness, it has been possible to derive an approximate index of the average force output per cross bridge and its variation with temperature. For the following discussion, it is essential to point out that the frog muscle fibers used are likely to be maximally, or supramaximally, activated over the entire range of temperatures investigated. This follows from the fact that the tetanic force is not enhanced by addition of caffeine or other twitch-potentiating agents at either low (13°C; Refs. 20, 35) or high (1530°C; Refs. 9, 33, 45; see also Ref. 6) temperatures.
Our results show that the average force generated per cross bridge, as indicated by the force-to-stiffness ratio, increases steadily as the temperature is raised between 3 and 20°C. This conclusion remains after account has been made of the possibility that 50% of the fiber compliance resides in the free portions of the thin filaments and, furthermore, that the filament compliance increases moderately with temperature (see Fig. 2B). In contrast to the force-to-stiffness ratio, the tetanic stiffness by itself changes in a more complex manner with temperature. Thus, as the temperature was raised from 3 to 20°C, the fiber stiffness increased to a maximum near 9°C. However, the tetanic stiffness decreased to a level below that recorded at 3°C by further increasing the temperature to 20°C. These findings suggest that the relatively steep rise in maximum tetanic force that occurs as the temperature is raised from 3 to 10°C is due to an increased number of active cross bridges in combination with increased force output per bridge. By raising the temperature beyond this level, however, the steady increase in force production of the active cross bridges will be counterbalanced by a decrease in the number of attached bridges, resulting in a flat maximum of the tetanic force between 15 and 20°C, as observed in the present study.
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GRANTS |
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DISCLOSURES |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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REFERENCES |
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