Changes in myosin S1 orientation and force induced by a temperature increase

Griffiths, Peter; Bagni, Maria Angela; Colombini, Barbara; Amenitsch, Heinz; Bernstorff, Sigrid; Ashley, Christopher; Cecchi, Giovanni

doi:10.1073/pnas.082482599

Cited by 23 publications

(43 citation statements)

References 27 publications

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“…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).…”

Section: Discussionsupporting

confidence: 75%

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

Colombini

Nocella²,

Benelli³

et al. 2008

American Journal of Physiology-Cell Physiology

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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 (P c ) 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, L c ) 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...

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Section: Discussionsupporting

confidence: 75%

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

Colombini

Nocella²,

Benelli³

et al. 2008

American Journal of Physiology-Cell Physiology

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“…The comparison shown in Fig. 4 indicates that the shape of this function was similar in both cases, in agreement with an earlier study (22) and was also similar to that obtained from our simulations of S1 structure by overlapping spheres (2,12). I M3,max was reduced to 72% by disordering whereas the filament displacement required to reduce I M3,max intensity by 20% was slightly reduced from 2.93 to 2.81 nm.…”

Section: Mechanical Properties Of Dorsal Interossei Bundlessupporting

confidence: 80%

“…However, larger oscillation amplitudes (peak to peak, 5-7 nm per HS, producing force oscillations of 1.3-1.6 times isometric tension) gave rise to a clear secondary minimum in I M3 at maximum shortening (Fig. 2, B and C), producing a double peak in intensity at this point similar to that seen previously at lower frequencies (2) or higher temperatures (12).…”

Section: Mechanical Properties Of Dorsal Interossei Bundlessupporting

confidence: 56%

“…8 and 15): their effects on I M3 are cumulative (28). Passive tilting is thought to account for most of the compliance associated with the cross-bridges (12).…”

mentioning

confidence: 99%

“…To achieve this, the I M3 response was simulated by a model, in which we varied the mean tilt of the lever arm domain, until a good fit to the corresponding, experimentally observed I M3 distortion was obtained (12).…”

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confidence: 99%

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Myosin lever disposition during length oscillations when power stroke tilting is reduced

Griffiths

Bagni²,

Colombini³

et al. 2005

American Journal of Physiology-Cell Physiology

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(I M3) from tetanized, intact skeletal muscle fiber bundles was measured during sinusoidal length oscillations at 2.8 kHz, a frequency at which the myosin motor's power stroke is greatly reduced. I M3 signals were approximately sinusoidal, but showed a "double peak" distortion previously observed only at lower oscillation frequencies. A tilting lever arm model simulated this distortion, where I M3 was calculated from the molecular structure of myosin subfragment 1 (S1). Simulations showed an isometric lever arm disposition close to normal to the filament axis at isometric tension, similar to that found using lower oscillation frequencies, where the power stroke contributes more toward total S1 movement. Inclusion of a second detached S1 in each actin-bound myosin dimer increased simulated I M3 signal amplitude and improved agreement with the experimental data. The best agreement was obtained when detached heads have a fixed orientation, insensitive to length changes, and similar to that of attached heads at tetanus plateau. This configuration also accounts for the variations in relative intensity of the two main peaks of the M3 reflection substructure after a length change. This evidence of an I M3 signal distortion when power stroke tilting is suppressed, provided that a large enough amplitude of length oscillation is used, is consistent with the tilting lever arm model of the power stroke. skeletal muscle; X-ray diffraction; muscle mechanics; molecular motors; subfragment 1 structure MYOSIN MOTORS are intracellular protein macromolecules, which function as actin-dependent transducers of ATP hydrolysis free energy into mechanical work. At least 17 classes of myosin exist, fulfilling many important motile roles in cell physiology, including cell division, cytokinesis, exo-, endo-, and pinocytosis, acuity adjustment of sensory receptors, and the contraction of all forms of muscle tissue (34). Their mechanism is thought to involve the active tilting (power stroke) of the myosin lever arm domain [a 9-nm-long projection from the actin-and ATP-binding motor domain of myosin subfragment 1 (S1)] during ATP cleavage at the motor domain's catalytic site (17, 31). Tilting displaces the arm's tip, producing a ϳ4-to 10-nm translational movement or 2-4 pN of force (7,27). A feature unique among myosin motors is that striated muscle myosin (myosin II) aggregates into highly structured filaments aligned within a quasicrystalline lattice, which yield a characteristic X-ray diffraction pattern (18) and the intensity of the 14.55 nm meridional X-ray reflection (I M3 ) is thought to be sensitive to lever arm tilting (21). This is because I M3 depends on the density of the S1 mass projected onto the filament axis, which changes with lever arm tilting. The maximum I M3 (I M3,max ) is reached when the lever is roughly perpendicular to the filament because at this point the axially projected mass distribution is at its most concentrated. In isometrically activated muscle, I M3 increases to a maximum for a small filament displacement ...

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Cross-Bridge Properties in Single Intact Frog Fibers Studied by Fast Stretches

Colombini¹,

Nocella²,

Benelli³

et al. 2010

Advances in Experimental Medicine and Biology

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Cross-bridges properties were measured under different experimental conditions by applying fast stretches to activated skeletal frog muscle fiber to -forcibly detach the cross-bridge ensemble. This allowed to measure the tension needed to detach the cross-bridges, P(c), and the sarcomere elongation at the rupture force, L(c). These two parameters are expected to be correlated with cross-bridges number (P(c)) and their mean extension (L(c)). Conditions investigated were: tetanus rise and plateau under normal Ringer and Ringer containing different BDM -concentrations, hyper (1.4T) and hypotonic (0.8T) solutions, 5 and 14 degrees C temperature. P(c) was linearly correlated with the tension (P) developed by the fibers under all the conditions examined, however the ratio P(c)/P changed depending on conditions being greater at low temperature and higher tonicity. These results indicate that, (a) P(c) can be used as a measure of attached cross-bridge number and (b) the force developed by the individual cross-bridge increases at high temperature and low tonicity. L(c) was not affected by tension developed, however it changed under different conditions, being greater at low temperature and high tonicity. These findings, suggests, in agreement with P(c) data, that cross-bridge extension is smaller at low temperature and high tonicity. By comparing these data with tetanic tension we concluded that potentiation or depression induced on tetanic force by tonicity or temperature changes are entirely accounted for by changes of the force developed by the individual cross-bridge.

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Changes in myosin S1 orientation and force induced by a temperature increase

Abstract: CorrectionsMEDICAL SCIENCES. For the article ''Initiating oncogenic event determines gene-expression patterns of human breast cancer models,''

Cited by 23 publications

References 27 publications

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

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

Myosin lever disposition during length oscillations when power stroke tilting is reduced

Cross-Bridge Properties in Single Intact Frog Fibers Studied by Fast Stretches

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