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Am J Physiol Cell Physiol 294: C1113-C1117, 2008. First published February 27, 2008; doi:10.1152/ajpcell.00063.2008
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MEMBRANE TRANSPORTERS, ION CHANNELS, AND PUMPS

Effect of temperature on cross-bridge properties in intact frog muscle fibers

Barbara Colombini, Marta Nocella, Giulia Benelli, Giovanni Cecchi, and M. Angela Bagni

Dipartimento di Scienze Fisiologiche and Istituto Interuniversitario di Miologia, Università degli Studi di Firenze, Firenze, Italy

Submitted 6 February 2008 ; accepted in final form 20 February 2008


   ABSTRACT
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 ABSTRACT
METHODS
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It is well known that the force developed by skeletal muscles increases with temperature. Despite the work done on this subject, the mechanism of force potentiation is still debated. Most of the published papers suggest that force enhancement is due to the increase of the individual cross-bridge force. However, reports on skinned fibers and single-molecule experiments suggest that cross-bridge force is temperature independent. The effects of temperature on cross-bridge properties in intact frog fibers were investigated in this study by applying fast stretches at various tension levels (P) on the tetanus rise at 5°C and 14°C to induce cross-bridge detachment. Cross-bridge number was measured from the force (critical force, Pc) needed to detach the cross-bridge ensemble, and the average cross-bridge strain was calculated from the sarcomere elongation needed to reach Pc (critical length, Lc). Our results show that Pc increased linearly with the force developed at both temperatures, but the Pc/P ratio was considerably smaller at 14°C. This means that the average force per cross bridge is greater at high temperature. This mechanism accounts for all the tetanic force enhancement. The critical length Lc was independent of the tension developed at both temperatures but was significantly lower at high temperature suggesting that cross bridges at 14°C are more strained. The increased cross-bridge strain accounts for the greater average force developed.

force enhancement; fast stretches

IT IS WELL KNOWN that tetanic tension in skeletal frog and mammalian muscle increases with temperature in the range 0°C to 20°C (5, 8, 9, 16–19, 23). Most of the data in the literature indicate that the force enhancement is due to an increase of the mean force developed by the individual cross bridge without a significant change in the total number of attached bridges. It has been also reported that increase of cross-bridge force with temperature occurs at the expense of the power stroke extent, which suggests a common mechanism with force development after electrical stimulation (17). A few reports in skinned fibers (14) and single-molecule experiments (15), however, suggest that temperature increases the number of cross bridges without altering the individual cross-bridge force. From the importance of these findings for the understanding of the mechanism of force generation, we have investigated the effect of temperature on cross-bridge properties in single frog muscle fibers by using a technique recently introduced by our group (1) following Flitney and Hirst (7). This technique measures the cross-bridge number from the measurements of the critical tension (Pc) needed to forcibly detach the cross-bridge ensemble by a fast stretch. Mean sarcomere length extension is obtained from measurements of the sarcomere elongation (critical length, Lc) needed to induce the rupture of the cross-bridge ensemble. In contrast to stiffness measurements traditionally used to measure the number of cross bridges, our measurements do not need to assume any particular value for filament and cross-bridge compliances as Pc is independent of these parameters. Our experiments at 5°C and 14°C show that the average cross-bridge force increased with temperature while the cross-bridge number remained unaltered. In agreement with this finding, critical length decreased at high temperature, indicating that cross bridges have a greater average length and are thus more strained than at low temperature. This mechanism accounts for the entire tetanic force enhancement occurring when temperature is raised from 5°C to 14°C.


   METHODS
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Frogs (Rana esculenta) were killed by decapitation followed by destruction of the spinal cord according to the procedure indicated by the Animal Care and Use Committee of the University of Florence and to the official regulation of the European Community Council (Directive 86/609/EEC). Single intact fibers, dissected from the tibialis anterior muscle (4–6 mm long, 60–120 µm diameter), were mounted by means of aluminium foil clips between the lever arms of a force transducer (natural frequency 30–50 kHz) and a fast electromagnetic motor (minimum stretch time 100 µs) in a thermostatically controlled chamber provided with a glass floor for both ordinary and laser light illumination. Stimuli of alternate polarity, 0.5-ms duration, and 1.5 times threshold strength, were applied transversely to the fiber by means of platinum-plate electrodes. Frequency of stimulation was adjusted at both temperatures (around 50 Hz at 14°C and 18 Hz at 5°C) to the minimum value needed to obtain fused tetanic contractions. Sarcomere length was measured using the striation follower device (11) in a fiber segment (1.2–2.5 mm long) selected for striation uniformity in a region as close as possible to the force transducer. This eliminated the effects of tendon compliance on sarcomere length measurements. To measure the cross-bridge rupture force, fast ramp test stretches of 0.25–0.70 ms duration and 16–25 nm per half sarcomere (nm/hs) amplitude [corresponding to stretching velocity between 23 and 95 sarcomere length per second (l0/s)] were applied to one end of the activated fiber while force response was measured at the other end. Since fibers developing the maximum tetanic tension (P0) were quickly damaged by the stretches used here, our experiments were mostly performed on the tetanus rise at a tension level between about 0.2 and 0.8 P0 at which fiber damage was much reduced. Measurements at 5°C and 14°C were made on the same fiber in a group of 12 fibers at resting sarcomere length of about 2.1 µm. Given the relative small stretches used, no change in effective overlap between myofilaments occurred during the experiments. Further details of measurements, including the correction for the first fast phase of the force response due to fiber inertia, can be found in our previous papers (1, 3).

Ringer solution had the following composition (mM): 115 NaCl, 2.5 KCl, 1.8 CaCl2, 0.85 NaH2PO4, and 2.15 Na2HPO4. Force and sarcomere length signals were measured with 1-ms and 10-µs time resolution with a digital oscilloscope (4094 Nicolet) and transferred to a personal computer for further analysis.


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Figure 1A shows the well-known potentiating effect of temperature on tetanic tension. In this fiber, tension increased by 27% as the temperature was raised from 5°C to 14°C. The average tension increase in a group of 12 fibers for the same temperature increase was 37 ± 3% (means ± SE) in agreement with previous data (16).


Figure 1
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  		Fig. 1. A: effect of temperature on isometric tetanic force (bottom traces) and sarcomere length (top traces) in the same single muscle fiber. Tetanic tension at 14°C (dashed line) is greater than at 5°C (solid line). B: effect of a fast stretch applied during the tetanus rise (at maximum tension of about 0.5 P0 and 5°C) on the force response. The vertical dashed line indicates the tension peak (Pc) at which the cross bridges are forcibly detached and the sarcomere elongation at tension peak Lc. Stretch amplitude, 24 nm/hs; stretch duration at Pc, 620 µs.

 
Figure 1B shows the force response of a single fiber to a fast stretch applied on the tetanus rise, at tension of about 0.5 P0 at 5°C. The tension rises almost linearly during the stretch up to a peak and then falls quickly toward the isometric level despite the continued stretching of the fiber. This means that at tension peak fiber compliance increases suddenly due to the forced cross-bridge detachment imposed by the stretch. The tension peak, representing the critical tension Pc, is directly proportional to cross-bridge number under a variety of conditions so that Pc can be used as a measure of cross-bridge number (1). Lc indicates the stretch amplitude needed to detach the cross bridges. Figure 1B shows that tension after the stretch does not fall below the isometric value. This could be due to a fast cross-bridge reattachment, which very likely follows the rupture imposed by the stretch.

To examine the effect of temperature on cross-bridge properties, Pc and Lc were measured by applying stretches at various isometric tensions during the tetanus rise at both 5°C and 14°C. An example of the effect obtained when the stretch is applied on a fiber developing the same absolute tension at high and low temperature is shown in Fig. 2.


Figure 2
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  		Fig. 2. Force responses (bottom traces) to a fast sarcomere elongation (top traces) of the same fiber developing the same absolute tension at 5°C (continuous trace) and 14°C (dashed trace) at fast time base. Note that both peak tension Pc and critical length Lc (indicated by the vertical dashed line) are greater at low temperature. Pc/P0 was 0.37 at 5°C and 0.29 at 14°C. Stretch duration at Pc, 290 µs.

 
It can be seen that peak tension at low temperature is greater than at high temperature, suggesting that at 5°C a greater number of cross bridges is necessary to develop the same isometric tension than at 14°C. The overall results obtained on the same group of 12 fibers used to determine the effect of temperature on tetanic tension are shown in Fig. 3.


Figure 3
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  		Fig. 3. Relative Pc/P0 relationships measured at 14°C (closed circles) and at 5°C (open circles) during the tetanus rise. Values at P0, indicated by open and closed triangles, are obtained by extrapolation from the fitting of the data points at 5°C and 14°C (continuous lines), respectively. It can be seen that for any given tension P, Pc is much greater at low temperature. Both Pc and P are expressed relatively to their P0.

 
Critical tension increases linearly with the isometric tension at both temperatures however, the slope of the relationship, represented by the Pc/P ratio, is considerably greater at 5°C. The fittings of the experimental data (straight lines) show that Pc/P rises from 2.26 ± 0.04 at 14°C to 3.08 ± 0.09 at 5°C (t-test for paired values, P < 0.01). This means that at any given isometric tension, the force needed to forcibly detach the cross-bridge ensemble is 36% greater at low temperature.

If the mechanism of cross-bridge force increase by temperature is the same of that occurring during force generation, cross bridges developing greater force should be more strained and therefore a smaller external elongation would suffice to stretch them up to the rupture force. This idea was tested by measuring the effect of temperature on the sarcomere elongation (Lc) needed to reach the critical force on the same fibers of Fig. 3. The results are shown in Fig. 4.


Figure 4
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  		Fig. 4. Critical length measured at various tensions during the tetanus rise at 5°C (open squares) and 14°C (closed squares). Individual points represent the mean values (means ± SE) for 0.20 P/P0 class averaging from 10 experiments. Same fibers of Fig. 3 minus 2 fibers in which it was not possible to record reliable sarcomere length data.

 
It can be seen that Lc is almost independent of tension at both 5°C and 14°C, but it depends on temperature. Its value (measured as a mean of all the points in Fig. 4) decreased by 1.97 nm/hs going from 13.14 ± 0.28 nm/hs at 5°C to 11.17 ± 0.19 nm/hs at 14°C. This suggests that cross bridges at 14°C are more strained in agreement with the prevision above.


   DISCUSSION
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One important characteristic of skeletal frog and mammalian skeletal muscle, either intact or skinned, is that the force developed depends markedly on temperature (5, 8, 9, 16–19, 23). Most of the experimental reports in the literature indicate that force potentiation by temperature in the range of 0–20°C is due mainly to the increase of the mean force developed by the individual cross bridge with no significant changes in cross-bridge number. However, recent reports on skinned fibers (14) or single-molecule experiments (15) attributed to a change in cross-bridge number, the greater force developed at higher temperatures. The experiments reported here were aimed to investigate the effect of temperature on cross-bridges properties by using a technique introduced recently by our group (1) in which very fast test stretches were applied to the fiber to induce the forced rupture of the cross-bridge ensemble. The tension Pc at which the rupture occurred was taken as a measure of cross-bridge number. In contrast to stiffness measurements, this way to measure cross-bridge number is independent of the properties of both myofilaments and cross-bridge compliances, which have no effect on Pc. At the same time, through Lc measurements we obtained information on the average cross-bridges strain (1).

It is known that a force applied to a noncovalent chemical bond increases the detachment rate constant leading to a rapid rupture of the bond. The most probable rupture force of the single bond F* follows the equation (2, 6):

Formula 1(1)
where kB is the Boltzmann constant, T is the absolute temperature, k0 is the detachment rate constant at zero tension, r is the loading rate of the bond, and xβ is the distance between the stable state to the transition state. In a previous paper (3), we showed that Eq. 1 can be applied to the cross bridges in the overlap region of the half sarcomere, and this allowed calculation of the total rupture force of the parallel cross-bridge ensemble Pc with the simple equation:

Formula 2(2)
where N is the total number of cross bridges. Thus by knowing the effect of temperature on F* it is possible to calculate cross-bridge number from critical tension measurements.

Our data show that Pc/P ratio is 3.08 at 5°C and 2.26 at 14°C. Hence, Pc, measured at the same isometric tension, is 27% smaller at 14°C than at 5°C. To calculate the influence of cross-bridge number on this reduction, it is necessary to correct Pc for the effect of the absolute temperature on F* (Eq. 1). When this correction is made, Pc/P ratio at 14°C reduces to 2.19, and cross-bridge number is 0.71 times the number at 5°C. Thus the development of the same isometric tension at 14°C requires 29% fewer bridges than at 5°C, which means that at 14°C cross bridges develop a 40% greater individual force. Considering that for the same temperature range tetanic force increased on average by 37%, we can conclude that, within the experimental error, the tetanic force enhancement by temperature is entirely accounted by the increase of the average cross-bridge force, with no significant change in cross-bridge number. This also means that the increase in Pc/P ratio at low temperature is almost entirely due to the reduction of tetanic tension.

If the mechanism underlying force enhancement by temperature is the same as that of the myosin power stroke leading to force generation and filament sliding, it is expected that cross bridges developing a greater individual force (at higher temperature) are more strained and have a mean position shifted further along the power stroke compared with bridges at low temperature. Then a smaller external elongation would suffice to rise the tension of these cross bridges up to the rupture force. Therefore, critical length should be reduced at high temperature. This is exactly what we found: mean Lc decreased by 1.97 nm/hs, from 13.14 nm/hs at 5°C to 11.17 nm/hs at 14°C in agreement with the expectation.

It may be asked whether this change is in quantitative agreement with the idea that increase of the average cross-bridge force justifies the whole force potentiation. This question can be answered if both cross-bridge and myofilament compliances are assumed to be linear in the following way: at 5°C Pc is 3.08 times P and Lc = 13.14 nm/hs, consequently, the mean half-sarcomere extension (y0) at isometric plateau is 13.14/2.08 = 6.32 nm/hs. To account for the 37% potentiation occurring when temperature was raised from 5°C to 14°C, with the sole change in individual cross-bridge force, y0 should also increase by 37%. Therefore, at 14°C, y0 should be 6.32 x 1.37 = 8.66 nm/hs, 2.34 nm/hs greater than at 5°C. This predicted value can be compared with the value calculated directly: at 14°C Pc/P ratio is 2.26 and Lc is 11.17 nm/hs; therefore, y0 = 11.17/1.26 = 8.86 nm/hs, close to the expected value. Although the agreement is good, this prediction is subjected to some uncertainties since, in contrast to critical tension, critical length measurements are affected by several factors. In addition to linearity and amount of cross-bridge and filament compliances, Lc is in fact influenced by the speed of the quick force recovery and velocity of the applied stretches (1).

The value of 6.32 nm/hs for cross-bridge mean extension (y0) at 5°C is relatively high compared with that in previous data (8). This is mostly due to the use of a relatively slow stretching speed and to the procedure above which calculated y0 directly and not through the extrapolation from force data obtained with very small step-length changes.

Experiments on rabbit psoas skinned fibers showed that the effect of temperature on force development in the range 5–30°C was attenuated by inorganic phosphate (5). Interestingly, the effect of phosphate on force, which is attributed to the shift of cross-bridge population toward a low force-generating state, is accompanied by an increase of the sarcomere elongation needed to reach the break point on the force record during a stretch (21), similarly to the effect of low temperature in our experiments.

Our analysis rely on the assumption that for a given isometric tension the increase of Pc at low temperature is due to an increased number of cross bridges (Eq. 2) while F* remains constant (except for the dependence on T shown in Eq. 1). Alternatively, it could be argued that Pc increase is due to the increase of F* occurring at low temperature (in contrast to the prediction of Eq. 1) with no change in cross-bridge number. However, if F* increases, the elongation needed to rupture the cross-bridge Lc should also increase by a corresponding amount. This is in contrast with our data showing that Lc at low temperature increased by <18% (13.14/11.17) while Pc increased by 36% making unlikely the above alternative hypothesis.

Our data were mostly obtained on the tetanus rise; however, Fig. 3 shows that the relationships between Pc/P at low and high temperature are both linear, hence, the conclusion above are applicable for any isometric tension including the plateau.

According to our results at 14°C the half-sarcomeres are more strained by about 1.97 nm (13.14–11.17 nm/hs) compared with 5°C. Since cross-bridge and myofilament compliances are about equal (13, 22), mean cross-bridge strain at 14°C is about 0.99 nm greater than that at 5°C. This value is in good quantitative agreement with the shift of the myosin head position of 0.73 nm toward the end of the power stroke, measured for 28% of force potentiation with X-ray diffraction technique (10) and gives further support to the idea that force generation and temperature potentiation occurs through the same molecular mechanism. A similar shift of the myosin head mean position occurred when muscle force was potentiated by lowering the ionic strength of the Ringer solution (4).

It has been shown recently (20) that force potentiation by a temperature jump is strongly reduced when the t-jump is applied to a fiber during stretching. This is consistent with the observation reported here showing that the absolute value of critical tension is independent of temperature.

The increment of the mean cross-bridge force and extension occurring when temperature is raised can be interpreted according to the Huxley and Simmons model (12) as a temperature-sensitive endothermic shift of the equilibrium between cross-bridge states, which increases the cross-bridge population generating high force at expenses of that generating low force.

In conclusion our results, being obtained with a technique independent of those used previously, strengthen significantly the predominant hypothesis that force potentiation by temperature is due to the increase of the average cross-bridge force and strain with no change in cross-bridge number.


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This study was supported by the Università di Firenze, Ministero della Ricerca Scientifica (PRIN) and Ente Cassa di Risparmio di Firenze (2004.1671).


   FOOTNOTES
 

Address for reprint requests and other correspondence: G. Cecchi, Dipartimento di Scienze Fisiologiche, Viale G. B. Morgagni 63, I-50134 Firenze, Italy (e-mail: giovanni.cecchi{at}unifi.it)

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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1. Bagni MA, Cecchi G, Colombini B. Crossbridges properties investigated by fast ramp stretching of activated frog muscle fibres. J Physiol 565: 261–268, 2005.[Abstract/Free Full Text]

2. Bell GI. Models for the specific adhesion of cells to cells. Science 200: 618–627, 1978.[Abstract/Free Full Text]

3. Colombini B, Bagni MA, Romano G, Cecchi G. Characterization of actomyosin bond properties in intact skeletal muscle by force spectroscopy. Proc Natl Acad Sci USA 104: 9284–9289, 2007.[Abstract/Free Full Text]

4. Colombini B, Bagni MA, Cecchi G, Griffiths PJ. Effect of solution tonicity on crossbridge properties and myosin lever arm disposition in intact frog muscle fibres. J Physiol 578.1: 337–346, 2007.

5. Coupland ME, Puchert E, Ranatunga KW. Temperature dependence of active tension in mammalian (rabbit psoas) muscle fibres: effect of inorganic phosphate. J Physiol 536: 879–891, 2001.[Abstract/Free Full Text]

6. Evans E, Ritchie K. Dynamic strength of molecular adhesion bonds. Biophys J 72: 1541–1555, 1997.[Web of Science][Medline]

7. Flitney FW, Hirst DG. Cross-bridge detachment and sarcomere "give" during stretch of active frog's muscle. J Physiol 276: 449–465, 1978.[Abstract/Free Full Text]

8. Ford LE, Huxley AF, Simmons RM. Tension responses to sudden length changes in stimulated frog muscle fibres near slack length. J Physiol 269: 441–515, 1977.[Abstract/Free Full Text]

9. Goldman YE, McCray JA, Ranatunga KW. Transient tension changes initiated by laser temperature jumps in rabbit psoas muscle fibres. J Physiol 392: 71–95, 1987.[Abstract/Free Full Text]

10. Griffiths PJ, Bagni MA, Colombini B, Amenitsch H, Bernstorff S, Ashley CC, Cecchi G. Changes in myosin S1 orientation and force induced by a temperature increase. Proc Natl Acad Sci USA 99: 5384–5389, 2002.[Abstract/Free Full Text]

11. Huxley AF, Lombardi V, Peachey LD. A system for fast recording of longitudinal displacement of a striated muscle fibre. J Physiol 317: 12–13, 1981.

12. Huxley AF, Simmons RM. Proposed mechanism of force generation in striated muscle. Nature 233: 533–538, 1971.[CrossRef][Medline]

13. Huxley HE, Stewart A, Sosa H, Irving CT. X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys J 67: 2411–2421, 1994.[Web of Science][Medline]

14. Kawai M. What do we learn by studying the temperature effect on isometric tension and tension transients in mammalian striated muscle fibres? J Muscle Res Cell Motil 24: 127–138, 2003.[CrossRef][Web of Science][Medline]

15. Kawai M, Kido T, Vogel M, Fink RHA, Ishiwata S. Temperature changes does not affect force between regulated actin filaments and heavy meromyosin in single-molecule experiments. J Physiol 574.3: 877–887, 2006.

16. Linari M, Brunello E, Reconditi M, Sun YB, Panini P, Narayanan T, Piazzesi G, Lombardi V, Irving M. The structural basis of the increase in isometric force production with temperature in frog skeletal muscle. J Physiol 567.2: 459–469, 2005.

17. Piazzesi G, Reconditi M, Koubassova N, Decostre V, Linari M, Lucii L, Lombardi V. Temperature dependence of the force-generating process in single fibres from frog skeletal muscle. J Physiol 549.1: 93–106, 2003.

18. Rall JA, Woledge RC. Influence of temperature on mechanics and energetics of muscle contraction. Am J Physiol Regul Integr Comp Physiol 259: R197–R203, 1990.[Abstract/Free Full Text]

19. Ranatunga KW. Endothermic force generation in fast and slow mammalian (rabbit) muscle fibers. Biophys J 71: 1905–1913, 1996.[Web of Science][Medline]

20. Ranatunga KW, Coupland ME, Pinniger GJ, Roots H, Offer GW. Force generation examined by laser temperature-jumps in shortening and lengthening mammalian (rabbit psoas) muscle fibres. J Physiol 585: 263–277, 2007.[Abstract/Free Full Text]

21. Stienen GJM, Versteeg PGA, Papp Z, Elzinga G. Mechanical properties of skinned rabbit psoas and soleus muscle fibres during lengthening: effects of phosphate and Ca2+. J Physiol 222: 237–253, 1992.

22. Wakabayashi K, Sugimoto Y, Tanaka H, Hueno Y, Takezaw Y, Amemiya Y. X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J 67: 2422–2435, 1994.[Web of Science][Medline]

23. Zhao Y, Kawai M. Kinetic and thermodynamic studies of the cross-bridge cycle in rabbit psoas muscle fibers. Biophys J 67: 1655–1668, 1994.[Web of Science][Medline]




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