The stiffness of slow-twitch muscle lags behind twitch tension: Implications for contractile mechanisms and behavior

Small, square stretches were applied during contractions of soleus and plantaris muscles in the cat to measure muscle stiffness. The stiffness of the slow-twitch soleus muscle (but not of the fast plantaris muscle) reaches a maximum after the peak in twitch tension. Since the number of active bonds should be maximum before the peak in tension, we suggest that many bonds are in the rigor state during the falling phase of the twitch. The stiffness of the bonds in this state may be useful for prolonging the twitch in slow-twitch muscles and for maintaining a posture.

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Nonlinear summation of contractions in cat muscles. II. Later facilitation and stiffness changes.

The Journal of General Physiology ◽

10.1085/jgp.78.3.295 ◽

1981 ◽

Vol 78 (3) ◽

pp. 295-311 ◽

Cited By ~ 153

Author(s):

F Parmiggiani ◽

R B Stein

Keyword(s):

Soleus Muscle ◽

Time Course ◽

Short Interval ◽

Force Production ◽

Muscle Stiffness ◽

Contraction Time ◽

Plantaris Muscle ◽

Twitch Contraction ◽

Slow Twitch ◽

Fast Twitch

The force produced by cat muscles over time with two stimuli separated by a short interval is approximately three times that produced by a twitch of cat muscles. This facilitation of force production by a second stimulus involves both increases in magnitude and duration of the contraction. Increased magnitude is relatively more important in the fast-twitch plantaris muscle, whereas increased duration is more important in the slow-twitch soleus muscle. The facilitation decays in an approximately exponential manner with the interval between stimuli, having a time constant between one and two times the twitch contraction time in different muscles. If a third stimulus is added, the greatest facilitation is seen at intervals longer than the twitch contraction time. The drug Dantrolene, which specifically reduces Ca++ release from the sarcoplasmic reticulum, eliminates the delayed peak in facilitation with three stimuli. Associated with the increases in force with one or more stimuli are increases in muscle stiffness, which can be measured with small, brief stretches and releases that do not alter the time-course of contraction. The stiffness of soleus muscle reaches a peak after the peak in force. The increasing stiffness of the muscle can considerably facilitate transmission of force generated internally, in addition to any facilitation arising from Ca++-release mechanisms.

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ATP-sensitive potassium channels mediate hyperosmotic stimulation of NKCC in slow-twitch muscle

AJP Cell Physiology ◽

10.1152/ajpcell.00247.2003 ◽

2004 ◽

Vol 286 (3) ◽

pp. C586-C595 ◽

Cited By ~ 4

Author(s):

Aidar R. Gosmanov ◽

Zheng Fan ◽

Xianqiang Mi ◽

Edward G. Schneider ◽

Donald B. Thomason

Keyword(s):

Skeletal Muscle ◽

Soleus Muscle ◽

Potassium Current ◽

Plantaris Muscle ◽

Channel Inhibition ◽

Slow Twitch Muscle ◽

Inhibition Of Glycolysis ◽

Slow Twitch ◽

Mapk Inhibitors ◽

Fast Twitch

In mildly hyperosmotic medium, activation of the Na+-K+-2Cl- cotransporter (NKCC) counteracts skeletal muscle cell water loss, and compounds that stimulate protein kinase A (PKA) activity inhibit the activation of the NKCC. The aim of this study was to determine the mechanism for PKA inhibition of NKCC activity in resting skeletal muscle. Incubation of rat slow-twitch soleus and fast-twitch plantaris muscles in isosmotic medium with the PKA inhibitors H-89 and KT-5720 caused activation of the NKCC only in the soleus muscle. NKCC activation caused by PKA inhibition was insensitive to MEK MAPK inhibitors and to insulin but was abolished by the PKA stimulators isoproterenol and forskolin. Furthermore, pinacidil [an ATP-sensitive potassium (KATP) channel opener] or inhibition of glycolysis increased NKCC activity in the soleus muscle but not in the plantaris muscle. Preincubation of the soleus muscle with glibenclamide (a KATP channel inhibitor) prevented the NKCC activation by hyperosmolarity, PKA inhibition, pinacidil, and glycolysis inhibitors. In contrast, glibenclamide stimulated NKCC activity in the plantaris muscle. In cells stably transfected with the Kir6.2 subunit of the of KATP channel, inhibition of glycolysis activated potassium current and NKCC activity. We conclude that activation of KATP channels in slow-twitch muscle is necessary for activation of the NKCC and cell volume restoration in hyperosmotic conditions.

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Temperature-dependent skeletal muscle dysfunction in rats with congestive heart failure

Journal of Applied Physiology ◽

10.1152/japplphysiol.00807.2004 ◽

2005 ◽

Vol 99 (4) ◽

pp. 1500-1507 ◽

Cited By ~ 4

Author(s):

H.-M. Schiøtz Thorud ◽

E. Verburg ◽

P. K. Lunde ◽

T. A. Strømme ◽

I. Sjaastad ◽

...

Keyword(s):

Soleus Muscle ◽

Temperature Sensitivity ◽

Muscle Dysfunction ◽

Temperature Sensitive ◽

Relaxation Rates ◽

Intracellular Ca ◽

Slow Twitch Muscle ◽

Slow Twitch ◽

The Difference ◽

Contraction And Relaxation

Abnormalities in the excitation-contraction coupling of slow-twitch muscle seem to explain the slowing and increased fatigue observed in congestive heart failure (CHF). However, it is not known which elements of the excitation-contraction coupling might be affected. We hypothesize that the temperature sensitivity of contractile properties of the soleus muscle might be altered in CHF possibly because of alterations of the temperature sensitivity of intracellular Ca2+ handling. We electrically stimulated the in situ soleus muscle of anesthetised rats that had 6-wk postinfarction CHF using 1 and 50 Hz and using a fatigue protocol (5-Hz stimulation for 30 min) at 35, 37, and 40°C. Ca2+ uptake and release were measured in sarcoplasmic reticulum vesicles at various temperatures. Contraction and relaxation rates of the soleus muscle were slower in CHF than in sham at 35°C, but the difference was almost absent at 40°C. The fatigue protocol revealed that force development was more temperature sensitive in CHF, whereas contraction and relaxation rates were less temperature sensitive in CHF than in sham. The Ca2+ uptake and release rates did not correlate to the difference between CHF and sham regarding contractile properties or temperature sensitivity. In conclusion, the discrepant results regarding altered temperature sensitivity of contraction and relaxation rates in the soleus muscle of CHF rats compared with Ca2+ release and uptake rates in vesicles indicate that the molecular cause of slow-twitch muscle dysfunction in CHF is not linked to the intracellular Ca2+ cycling.

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Calcium binding protein changes of sarcoplasmic reticulum from rat denervated skeletal muscle

Bioscience Reports ◽

10.1007/bf01115228 ◽

1988 ◽

Vol 8 (4) ◽

pp. 369-378 ◽

Cited By ~ 9

Author(s):

Marie-Jeanne Loirat ◽

Brigitte Lucas-Heron ◽

Béatrice Ollivier ◽

Claude Leoty

Keyword(s):

Skeletal Muscle ◽

Sarcoplasmic Reticulum ◽

Atpase Activity ◽

Soleus Muscle ◽

Calcium Binding ◽

Neural Control ◽

Calcium Binding Protein ◽

Slow Twitch Muscle ◽

Slow Twitch ◽

Fast Twitch

Two Ca2+ sequestering proteins were studied in fast-twitch (EDL) and slow-twitch (soleus) muscle sarcoplasmic reticulum (SR) as a function of denervation time. Ca2+-ATPase activity measured in SR fractions of normal soleus represented 5% of that measure in SR fractions of normal EDL. Denervation caused a severe decrease in activity only in fast-twich muscle. Ca2+-ATPase and calsequestrin contents were affected differently by denervation. In EDL SR, Ca2+-ATPase content decreased progressively, whereas in soleus SR, no variation was observed. Calsequestrin showed a slight increase in both muscles as a function of denervation time correlated with increased45Ca-binding. These results indicate first that Ca2+-ATPase activity in EDL was under neural control, and that because of low Ca2+-ATPase activity and content in slow-twitch muscle no variation could be detected, and secondly that greater calsequestrin content might represent a relative increasing of heavy vesicles or decreasing of light vesicles as a function of denervation time in the whole SR fraction isolated in both types of muscles.

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Centrifugal intensity and duration as countermeasures to soleus muscle atrophy

Journal of Applied Physiology ◽

10.1152/jappl.1990.69.4.1387 ◽

1990 ◽

Vol 69 (4) ◽

pp. 1387-1389 ◽

Cited By ~ 14

Author(s):

D. S. D'Aunno ◽

D. B. Thomason ◽

F. W. Booth

Keyword(s):

Muscle Atrophy ◽

Soleus Muscle ◽

Weight Bearing ◽

Slow Twitch Muscle ◽

Wet Weight ◽

Slow Twitch

Mechanical acceleration is a countermeasure that may be employed to prevent atrophy of slow-twitch muscle during non-weight bearing. In the present study, daily centrifugation of rats for different durations (1 or 2 h) and at different gravitational intensities (1.5 or 2.6 G) was used to test whether mechanical acceleration could ameliorate the atrophy of the soleus muscle induced by non-weight bearing (tail-traction model). The soleus muscle atrophied 32% during 7 days of non-weight bearing without countermeasures. Centrifugation treatment did not completely prevent atrophy relative to precontrol wet weight of the soleus muscle. Non-weight-bearing groups receiving 2-h daily treatments of 1, 1.5, or 2.6 G had 48, 56, and 65%, respectively, of the atrophy observed in the non-weight-bearing-only group compared with the precontrol group. No evidence was obtained that centrifugation at 2.6 G was more effective than exposure to 1 or 1.5 G as a countermeasure to non-weight-bearing-induced atrophy of the soleus muscle.

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Atrophy of the soleus muscle by hindlimb unweighting

Journal of Applied Physiology ◽

10.1152/jappl.1990.68.1.1 ◽

1990 ◽

Vol 68 (1) ◽

pp. 1-12 ◽

Cited By ~ 354

Author(s):

D. B. Thomason ◽

F. W. Booth

Keyword(s):

Soleus Muscle ◽

Oxidative Capacity ◽

Glycolytic Enzyme ◽

Hindlimb Unweighting ◽

Degradation Rates ◽

Applied Physiology ◽

Slow Twitch Muscle ◽

Specific Mrnas ◽

Slow Twitch ◽

Fast Twitch

The unweighting model is a unique whole animal model that will permit the future delineation of the mechanism(s) by which gravity maintains contractile mass in postural (slow-twitch) skeletal muscle. Since the origination of the model of rodent hindlimb unweighting almost one decade ago, about half of the 59 refereed articles in which this model was utilized have been published in the Journal of Applied Physiology. Thus the purpose of this review is to provide, for those researchers with an interest in the hindlimb unweighting model, a summation of the data derived from this model to data and hopefully to stimulate research interest in aspects of the model for which data are lacking. The stress response of the animal to hindlimb unweighting is transient, minimal in magnitude, and somewhat variable. After 1 wk of unweighting, the animal exhibits no chronic signs of stress. The atrophy of the soleus muscle, a predominantly slow-twitch muscle, is emphasized because unweighting preferentially affects it compared with other calf muscles, which are mainly fast-twitch muscles. The review considers the following information about the unweighted soleus muscle: electromyogram activity, amount and type of protein lost, capillarization, oxidative capacity, glycolytic enzyme activities, fiber cross section, contractile properties, glucose uptake, sensitivity to insulin, protein synthesis and degradation rates, glucocorticoid receptor numbers, responses of specific mRNAs, and changes in metabolite concentrations.

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Akt kinases and 2-deoxyglucose uptake in rat skeletal muscles in vivo: study with insulin and exercise

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1999.276.1.r277 ◽

1999 ◽

Vol 276 (1) ◽

pp. R277-R282 ◽

Cited By ~ 23

Author(s):

Jiri Turinsky ◽

Alice Damrau-Abney

Keyword(s):

Glucose Uptake ◽

Soleus Muscle ◽

Insulin Injection ◽

Plantaris Muscle ◽

Hindlimb Muscles ◽

Slow Twitch Muscle ◽

Fast Twitch Muscle ◽

Exercise Induced ◽

Calf Muscles

Activities of Akt1, Akt2, and Akt3 kinases and glucose uptake in hindlimb muscles of the rat in vivo were investigated. The rats were studied either after intravenous injection of 0.1 U of insulin or during exercise induced by stimulating calf muscles electrically at 1 contraction/s. Akt kinases were immunoprecipitated from supernatants of muscle homogenates. Glucose uptake by muscles in vivo was assessed by cellular accumulation of 2-deoxy-d-[1,2-3H(N)]glucose. Administration of insulin resulted in rapid activation of Akt1 kinase, with peak activity observed 5 min after insulin injection. Soleus muscle, a slow-twitch muscle, and plantaris muscle, a fast-twitch muscle, differed in their content of Akt1 kinase and in their response to insulin. Soleus muscle exhibited a 105% higher abundance of Akt1 kinase, a 101% higher insulin-stimulated activity of Akt1 kinase, and 83% higher insulin-stimulated 2-deoxyglucose uptake compared with plantaris muscle. Additionally, insulin administration increased the activities of Akt1, Akt2, and Akt3 kinases in calf muscles and caused a sevenfold augmentation in 2-deoxyglucose uptake by these muscles. In contrast, the exercised calf muscles exhibited an increase in Akt1 kinase activity at 5, 15, and 25 min of exercise but no change in activities of Akt2 and Akt3 isoforms, and the 2-deoxyglucose uptake by calf muscles exercised for 25 min was 11-fold higher compared with muscles of resting rats. The data demonstrate that 1) there is a close, direct correlation between the magnitude of insulin-stimulated activity of Akt1 kinase and the level of glucose uptake in muscles with different fiber populations, 2) insulin activates three isoforms of Akt kinase in skeletal muscle, and 3) exercise in vivo is associated with activation of Akt1 but not Akt2 and Akt3 kinases in contracting muscles.

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Differences in histone modifications between slow- and fast-twitch muscle of adult rats and following overload, denervation, or valproic acid administration

Journal of Applied Physiology ◽

10.1152/japplphysiol.00289.2015 ◽

2015 ◽

Vol 119 (10) ◽

pp. 1042-1052 ◽

Cited By ~ 11

Author(s):

Fuminori Kawano ◽

Keisuke Nimura ◽

Saki Ishino ◽

Naoya Nakai ◽

Ken Nakata ◽

...

Keyword(s):

Valproic Acid ◽

Rna Polymerase Ii ◽

Histone Modifications ◽

Soleus Muscle ◽

Plantaris Muscle ◽

Adult Rats ◽

Muscle Properties ◽

Pol Ii ◽

Slow Twitch ◽

Fast Twitch

Numerous studies have reported alterations in skeletal muscle properties and phenotypes in response to various stimuli such as exercise, unloading, and gene mutation. However, a shift in muscle fiber phenotype from fast twitch to slow twitch is not completely induced by stimuli. This limitation is hypothesized to result from the epigenetic differences between muscle types. The main purpose of the present study was to identify the differences in histone modification for the plantaris (fast) and soleus (slow) muscles of adult rats. Genome-wide analysis by chromatin immunoprecipitation followed by DNA sequencing revealed that trimethylation at lysine 4 and acetylation of histone 3, which occurs at transcriptionally active gene loci, was less prevalent in the genes specific to the slow-twitch soleus muscle. Conversely, gene loci specific to the fast-twitch plantaris muscle were associated with the aforementioned histone modifications. We also found that upregulation of slow genes in the plantaris muscle, which are related to enhanced muscular activity, is not associated with activating histone modifications. Furthermore, silencing of muscle activity by denervation caused the displacement of acetylated histone and RNA polymerase II (Pol II) in 5′ ends of genes in plantaris, but minor effects were observed in soleus. Increased recruitment of Pol II induced by forced acetylation of histone was also suppressed in valproic acid-treated soleus. Our present data indicate that the slow-twitch soleus muscle has a unique set of histone modifications, which may relate to the preservation of the genetic backbone against physiological stimuli.

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