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Force generation examined by laser temperature-jumps in shortening and lengthening mammalian (rabbit psoas) muscle fibres.

Ranatunga KW, Coupland ME, Pinniger GJ, Roots H, Offer GW - J. Physiol. (Lond.) (2007)

Bottom Line: At a given shortening velocity and over the temperature range of 8-30 degrees C, the rate of T-jump tension rise increased with warming (Q10 approximately 2.7), similar to phase 2b (endothermic force generation) in isometric muscle.Results are discussed in relation to the previous findings in isometric muscle fibres which showed that a T-jump promotes an early step in the crossbridge-ATPase cycle that generates force.In general, the finding that the T-jump effect on active muscle tension is pronounced during shortening, but is depressed/inhibited during lengthening, is consistent with the expectations from the Fenn effect that energy liberation (and acto-myosin ATPase rate) in muscle are increased during shortening and depressed/inhibited during lengthening.

View Article: PubMed Central - PubMed

Affiliation: Muscle Contraction Group, Department of Physiology, School of Medical Sciences, University of Bristol, Bristol BS8 1TD, UK. k.w.ranatunga@bristol.ac.uk

ABSTRACT
We examined the tension change induced by a rapid temperature jump (T-jump) in shortening and lengthening active muscle fibres. Experiments were done on segments of permeabilized single fibres (length (L0) approximately 2 mm, sarcomere length 2.5 microm) from rabbit psoas muscle; [MgATP] was 4.6 mm, pH 7.1, ionic strength 200 mm and temperature approximately 9 degrees C. A fibre was maximally Ca2+-activated in the isometric state and a approximately 3 degrees C, rapid (< 0.2 ms), laser T-jump applied when the tension was approximately steady in the isometric state, or during ramp shortening or ramp lengthening at a limited range of velocities (0-0.2 L0 s(-1)). The tension increased to 2- to 3 x P0 (isometric force) during ramp lengthening at velocities > 0.05 L0 s(-1), whereas the tension decreased to about < 0.5 x P0 during shortening at 0.1-0.2 L0 s(-1); the unloaded shortening velocity was approximately 1 L0 s(-1) and the curvature of the force-shortening velocity relation was high (a/P0 ratio from Hill's equation of approximately 0.05). In isometric state, a T-jump induced a tension rise of 15-20% to a new steady state; by curve fitting, the tension rise could be resolved into a fast (phase 2b, 40-50 s(-1)) and a slow (phase 3, 5-10 s(-1)) exponential component (as previously reported). During steady lengthening, a T-jump induced a small instantaneous drop in tension, followed by recovery, so that the final tension recorded with and without a T-jump was not significantly different; thus, a T-jump did not lead to a net increase of tension. During steady shortening, the T-jump induced a pronounced tension rise and both its amplitude and the rate (from a single exponential fit) increased with shortening velocity; at 0.1-0.2 L0 s(-1), the extent of fibre shortening during the T-jump tension rise was estimated to be approximately 1.2% L(0) and it was shorter at lower velocities. At a given shortening velocity and over the temperature range of 8-30 degrees C, the rate of T-jump tension rise increased with warming (Q10 approximately 2.7), similar to phase 2b (endothermic force generation) in isometric muscle. Results are discussed in relation to the previous findings in isometric muscle fibres which showed that a T-jump promotes an early step in the crossbridge-ATPase cycle that generates force. In general, the finding that the T-jump effect on active muscle tension is pronounced during shortening, but is depressed/inhibited during lengthening, is consistent with the expectations from the Fenn effect that energy liberation (and acto-myosin ATPase rate) in muscle are increased during shortening and depressed/inhibited during lengthening.

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T-jumps during steady shortening at different temperatures A, superimposed tension (upper panel) and length (lower panel) records from an experiment in which the response to a 3°C T-jump (upward arrow), during same ramp shortening (velocity ∼0.06 V0), was recorded at a number of different temperatures; the post-T-jump temperature is given to the right of each trace. The isometric tension (i.e. tension before the downward arrow) and the tension during steady shortening are higher and the T-jump-induced tension rise, while shortening, becomes faster at the higher temperatures. B, the temperature dependence of the isometric tension (filled symbols) and of the tension during steady shortening (open symbols). Mean (± s.e.m.) data are from 4 fibres in each of which tensions are plotted as a percentage of its isometric tension at the low temperature (7–9°C); the abscissa is reciprocal absolute temperature (103× 1/T) and is also labelled in °C. The total number of measurements was 42 for isometric (n = 2–5 per data point) and 72 for shortening (n = 8 per data point). The shortening (velocity range 0.05–0.08 V0 in different experiments) decreased the tension during steady shortening to ∼50% P0 at ∼9°C. Note that in warming over this temperature range, the isometric tension increases ∼2-fold (as shown in previous studies, see references in Coupland et al. 2005) and the tension during steady shortening, within this velocity range, also shows a similar increase with warming.
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fig07: T-jumps during steady shortening at different temperatures A, superimposed tension (upper panel) and length (lower panel) records from an experiment in which the response to a 3°C T-jump (upward arrow), during same ramp shortening (velocity ∼0.06 V0), was recorded at a number of different temperatures; the post-T-jump temperature is given to the right of each trace. The isometric tension (i.e. tension before the downward arrow) and the tension during steady shortening are higher and the T-jump-induced tension rise, while shortening, becomes faster at the higher temperatures. B, the temperature dependence of the isometric tension (filled symbols) and of the tension during steady shortening (open symbols). Mean (± s.e.m.) data are from 4 fibres in each of which tensions are plotted as a percentage of its isometric tension at the low temperature (7–9°C); the abscissa is reciprocal absolute temperature (103× 1/T) and is also labelled in °C. The total number of measurements was 42 for isometric (n = 2–5 per data point) and 72 for shortening (n = 8 per data point). The shortening (velocity range 0.05–0.08 V0 in different experiments) decreased the tension during steady shortening to ∼50% P0 at ∼9°C. Note that in warming over this temperature range, the isometric tension increases ∼2-fold (as shown in previous studies, see references in Coupland et al. 2005) and the tension during steady shortening, within this velocity range, also shows a similar increase with warming.

Mentions: Figure 7A shows tension responses recorded from a fibre at four different temperatures; the fibre was first activated at 7–8°C, and the temperature raised (and clamped) by the Peltier, thermo-electric module system in the trough. At each temperature, it was shortened at the same ramp velocity and a T-jump of 3°C applied when tension during shortening was nearly steady. It is seen that the tension before the ramp (isometric) as well as the tension during shortening, before and after the T-jump, rise with increase of temperature. Figure 7B shows the pooled data (mean ± s.e.m.) for isometric tension (filled symbols) and for steady-shortening tension (open symbols), plotted against the reciprocal absolute temperature; the temperature dependence of isometric tension is essentially similar to previous findings, and the data also show that the tension during shortening, at about the same velocity, shows a similar temperature dependence.


Force generation examined by laser temperature-jumps in shortening and lengthening mammalian (rabbit psoas) muscle fibres.

Ranatunga KW, Coupland ME, Pinniger GJ, Roots H, Offer GW - J. Physiol. (Lond.) (2007)

T-jumps during steady shortening at different temperatures A, superimposed tension (upper panel) and length (lower panel) records from an experiment in which the response to a 3°C T-jump (upward arrow), during same ramp shortening (velocity ∼0.06 V0), was recorded at a number of different temperatures; the post-T-jump temperature is given to the right of each trace. The isometric tension (i.e. tension before the downward arrow) and the tension during steady shortening are higher and the T-jump-induced tension rise, while shortening, becomes faster at the higher temperatures. B, the temperature dependence of the isometric tension (filled symbols) and of the tension during steady shortening (open symbols). Mean (± s.e.m.) data are from 4 fibres in each of which tensions are plotted as a percentage of its isometric tension at the low temperature (7–9°C); the abscissa is reciprocal absolute temperature (103× 1/T) and is also labelled in °C. The total number of measurements was 42 for isometric (n = 2–5 per data point) and 72 for shortening (n = 8 per data point). The shortening (velocity range 0.05–0.08 V0 in different experiments) decreased the tension during steady shortening to ∼50% P0 at ∼9°C. Note that in warming over this temperature range, the isometric tension increases ∼2-fold (as shown in previous studies, see references in Coupland et al. 2005) and the tension during steady shortening, within this velocity range, also shows a similar increase with warming.
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Related In: Results  -  Collection

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fig07: T-jumps during steady shortening at different temperatures A, superimposed tension (upper panel) and length (lower panel) records from an experiment in which the response to a 3°C T-jump (upward arrow), during same ramp shortening (velocity ∼0.06 V0), was recorded at a number of different temperatures; the post-T-jump temperature is given to the right of each trace. The isometric tension (i.e. tension before the downward arrow) and the tension during steady shortening are higher and the T-jump-induced tension rise, while shortening, becomes faster at the higher temperatures. B, the temperature dependence of the isometric tension (filled symbols) and of the tension during steady shortening (open symbols). Mean (± s.e.m.) data are from 4 fibres in each of which tensions are plotted as a percentage of its isometric tension at the low temperature (7–9°C); the abscissa is reciprocal absolute temperature (103× 1/T) and is also labelled in °C. The total number of measurements was 42 for isometric (n = 2–5 per data point) and 72 for shortening (n = 8 per data point). The shortening (velocity range 0.05–0.08 V0 in different experiments) decreased the tension during steady shortening to ∼50% P0 at ∼9°C. Note that in warming over this temperature range, the isometric tension increases ∼2-fold (as shown in previous studies, see references in Coupland et al. 2005) and the tension during steady shortening, within this velocity range, also shows a similar increase with warming.
Mentions: Figure 7A shows tension responses recorded from a fibre at four different temperatures; the fibre was first activated at 7–8°C, and the temperature raised (and clamped) by the Peltier, thermo-electric module system in the trough. At each temperature, it was shortened at the same ramp velocity and a T-jump of 3°C applied when tension during shortening was nearly steady. It is seen that the tension before the ramp (isometric) as well as the tension during shortening, before and after the T-jump, rise with increase of temperature. Figure 7B shows the pooled data (mean ± s.e.m.) for isometric tension (filled symbols) and for steady-shortening tension (open symbols), plotted against the reciprocal absolute temperature; the temperature dependence of isometric tension is essentially similar to previous findings, and the data also show that the tension during shortening, at about the same velocity, shows a similar temperature dependence.

Bottom Line: At a given shortening velocity and over the temperature range of 8-30 degrees C, the rate of T-jump tension rise increased with warming (Q10 approximately 2.7), similar to phase 2b (endothermic force generation) in isometric muscle.Results are discussed in relation to the previous findings in isometric muscle fibres which showed that a T-jump promotes an early step in the crossbridge-ATPase cycle that generates force.In general, the finding that the T-jump effect on active muscle tension is pronounced during shortening, but is depressed/inhibited during lengthening, is consistent with the expectations from the Fenn effect that energy liberation (and acto-myosin ATPase rate) in muscle are increased during shortening and depressed/inhibited during lengthening.

View Article: PubMed Central - PubMed

Affiliation: Muscle Contraction Group, Department of Physiology, School of Medical Sciences, University of Bristol, Bristol BS8 1TD, UK. k.w.ranatunga@bristol.ac.uk

ABSTRACT
We examined the tension change induced by a rapid temperature jump (T-jump) in shortening and lengthening active muscle fibres. Experiments were done on segments of permeabilized single fibres (length (L0) approximately 2 mm, sarcomere length 2.5 microm) from rabbit psoas muscle; [MgATP] was 4.6 mm, pH 7.1, ionic strength 200 mm and temperature approximately 9 degrees C. A fibre was maximally Ca2+-activated in the isometric state and a approximately 3 degrees C, rapid (< 0.2 ms), laser T-jump applied when the tension was approximately steady in the isometric state, or during ramp shortening or ramp lengthening at a limited range of velocities (0-0.2 L0 s(-1)). The tension increased to 2- to 3 x P0 (isometric force) during ramp lengthening at velocities > 0.05 L0 s(-1), whereas the tension decreased to about < 0.5 x P0 during shortening at 0.1-0.2 L0 s(-1); the unloaded shortening velocity was approximately 1 L0 s(-1) and the curvature of the force-shortening velocity relation was high (a/P0 ratio from Hill's equation of approximately 0.05). In isometric state, a T-jump induced a tension rise of 15-20% to a new steady state; by curve fitting, the tension rise could be resolved into a fast (phase 2b, 40-50 s(-1)) and a slow (phase 3, 5-10 s(-1)) exponential component (as previously reported). During steady lengthening, a T-jump induced a small instantaneous drop in tension, followed by recovery, so that the final tension recorded with and without a T-jump was not significantly different; thus, a T-jump did not lead to a net increase of tension. During steady shortening, the T-jump induced a pronounced tension rise and both its amplitude and the rate (from a single exponential fit) increased with shortening velocity; at 0.1-0.2 L0 s(-1), the extent of fibre shortening during the T-jump tension rise was estimated to be approximately 1.2% L(0) and it was shorter at lower velocities. At a given shortening velocity and over the temperature range of 8-30 degrees C, the rate of T-jump tension rise increased with warming (Q10 approximately 2.7), similar to phase 2b (endothermic force generation) in isometric muscle. Results are discussed in relation to the previous findings in isometric muscle fibres which showed that a T-jump promotes an early step in the crossbridge-ATPase cycle that generates force. In general, the finding that the T-jump effect on active muscle tension is pronounced during shortening, but is depressed/inhibited during lengthening, is consistent with the expectations from the Fenn effect that energy liberation (and acto-myosin ATPase rate) in muscle are increased during shortening and depressed/inhibited during lengthening.

Show MeSH
Related in: MedlinePlus