Sarcomere Lengths Become More Uniform Over Time in Intact Muscle-Tendon Unit During Isometric Contractions

Moo, Eng Kuan; Herzog, Walter

doi:10.3389/fphys.2020.00448

Cited by 6 publications

(5 citation statements)

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“…A4B) and this is greater than the value previously reported for rat SOL muscle (Mutungi & Ranatunga, 2000). However, the changes in SL in both muscles are smaller compared to tibialis anterior muscle in mice (Moo & Herzog, 2020).…”

Section: Structural Changes During Fixed-end Tetanic Contractions In ...mentioning

confidence: 80%

Thick filament activation is different in fast‐ and slow‐twitch skeletal muscle

Gong

Regnier

et al. 2022

The Journal of Physiology

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The contractile properties of fast‐twitch and slow‐twitch skeletal muscles are primarily determined by the myosin isoform content and modulated by a variety of sarcomere proteins. X‐ray diffraction studies of regulatory mechanisms in muscle contraction have focused predominately on fast‐ or mixed‐fibre muscle with slow muscle being much less studied. Here, we used time‐resolved X‐ray diffraction to investigate the dynamic behaviour of the myofilament proteins in relatively pure slow‐twitch‐fibre rat soleus (SOL) and pure fast‐twitch‐fibre rat extensor digitorum longus (EDL) muscle during twitch and tetanic contractions at optimal length. During twitch contractions the diffraction signatures indicating a transition in the myosin heads from ordered OFF states, where heads are held close to the thick filament backbone, to disordered ON states, where heads are free to bind to thin filaments, were found in EDL and not in SOL muscle. During tetanic contraction, changes in the disposition of myosin heads as active tension develops is a quasi‐stepwise process in EDL muscle whereas in SOL muscle this relationship appears to be linear. The observed reduced extensibility of the thick filaments in SOL muscle as compared to EDL muscles indicates a molecular basis for this behaviour. These data indicate that for the EDL, thick filament activation is a cooperative strain‐induced mechano‐sensing mechanism, whereas for the SOL, thick filament activation has a more graded response. These different approaches to thick filament regulation in fast‐ and slow‐twitch muscles may be adaptations for short‐duration, strong contractions versus sustained, finely controlled contractions, respectively. Key points Fast‐twitch muscle and slow‐twitch muscle are optimized for strong, short‐duration contractions and for tonic postural activity, respectively. Structural events (OFF to ON transitions) in the myosin‐containing thick filaments in fast muscle help determine the timing and strength of contractions, but these have not been studied in slow‐twitch muscle. The X‐ray diffraction signatures of structural OFF to ON transitions are different in fast extensor digitorum longus (EDL) and slow soleus (SOL) muscle, being completely absent during twitches in soleus muscle and blunted during tetanic contractions SOL as compared to EDL Quasi‐stepwise thick filament structural OFF to ON transitions in fast twitch muscle may be an adaptation for rapid, ballistic movements, whereas more graded OFF to ON structural transitions in slow‐twitch muscle may be an adaptation for slower, finer motions.

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Section: Structural Changes During Fixed-end Tetanic Contractions In ...mentioning

confidence: 80%

Thick filament activation is different in fast‐ and slow‐twitch skeletal muscle

Gong

Regnier

et al. 2022

The Journal of Physiology

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“… Moo et al (2016) found that sarcomere strains are not uniform across different regions of intact muscle, and that the greatest sarcomere strains occur close to the myotendinous junction where external loads are applied. These strains become less uniform when muscle is activated during fixed-end contractions ( Moo et al, 2017 ), but this non-uniformity in sarcomere strains decreases over time ( Moo and Herzog, 2020 ). This pattern of sarcomere non-uniformity may be in part due to muscle mass and may vary depending on the size of the muscle, much like the response of the spring with mass and 1D and 3D muscle models that account for muscle mass.…”

Section: Discussionmentioning

confidence: 99%

The Energy of Muscle Contraction. III. Kinetic Energy During Cyclic Contractions

et al. 2021

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During muscle contraction, chemical energy is converted to mechanical energy when ATP is hydrolysed during cross-bridge cycling. This mechanical energy is then distributed and stored in the tissue as the muscle deforms or is used to perform external work. We previously showed how energy is distributed through contracting muscle during fixed-end contractions; however, it is not clear how the distribution of tissue energy is altered by the kinetic energy of muscle mass during dynamic contractions. In this study we conducted simulations of a 3D continuum muscle model that accounts for tissue mass, as well as force-velocity effects, in which the muscle underwent sinusoidal work-loop contractions coupled with bursts of excitation. We found that increasing muscle size, and therefore mass, increased the kinetic energy per unit volume of the muscle. In addition to greater relative kinetic energy per cycle, relatively more energy was also stored in the aponeurosis, and less was stored in the base material, which represented the intra and extracellular tissue components apart from the myofibrils. These energy changes in larger muscles due to greater mass were associated lower mass-specific mechanical work output per cycle, and this reduction in mass-specific work was greatest for smaller initial pennation angles. When we compared the effects of mass on the model tissue behaviour to that of in situ muscle with added mass during comparable work-loop trials, we found that greater mass led to lower maximum and higher minimum acceleration in the longitudinal (x) direction near the middle of the muscle compared to at the non-fixed end, which indicates that greater mass contributes to tissue non-uniformity in whole muscle. These comparable results for the simulated and in situ muscle also show that this modelling framework behaves in ways that are consistent with experimental muscle. Overall, the results of this study highlight that muscle mass is an important determinant of whole muscle behaviour.

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“…The mechanical communication between in-series sarcomeres is also affected by the passive properties of myofibrils and intracellular matrix ( de Souza Leite et al, 2017 ). On the other hand, SL heterogeneity presents at the level of a single myofibril, whole isolated muscle and in situ in living animals ( Moo et al, 2017 ; Moo and Herzog, 2018 ; Moo and Herzog, 2020 ), i.e. under highly different mechanical conditions.…”

Section: Discussionmentioning

confidence: 99%

“…This supports the notion that intracellular SL dispersion has a specific physiological role rather than that it simply follows the pattern of passive stress/strain. Moreover, the intracellular mechanisms of SL variability may differ between rest and active states of a myocyte ( Moo and Herzog, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

“…It remains poorly studied whether the dispersion of individual SL is linked somehow to the contractile activation of a myocyte and what physiological role this dispersion may represent. In intact skeletal muscle, it has been shown that the in situ activation of the myofibrils is accompanied by elevation of SL dispersion ( Pavlov et al, 2009 ; Moo and Herzog, 2018 ; Moo and Herzog, 2020 ) which then, however, either remains constant or only slightly decreases during a subsequent period of steady-state activation ( Pavlov et al, 2009 ; Moo and Herzog, 2020 ). The SL dispersion is higher in a stretched myofibril, but the activation-induced elevation in this dispersion seems to be stretch-independent ( Pavlov et al, 2009 ).…”

Section: Discussionmentioning

confidence: 99%

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Contractile State Dependent Sarcomere Length Variability in Isolated Guinea-Pig Cardiomyocytes

et al. 2022

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Cardiomyocytes contract keeping their sarcomere length (SL) close to optimal values for force generation. Transmural heterogeneity in SL across the ventricular wall coordinates the contractility of the whole-ventricle. SL heterogeneity (variability) exists not only at the tissue (macroscale) level, but also presents at the level of a single cardiomyocyte (microscale level). However, transmural differences in intracellular SL variability and its possible dependence on the state of contraction (e.g. end-diastole or end-systole) have not been previously reported. In the present study, we studied three aspects of sarcomere-to-sarcomere variability in intact cardiomyocytes isolated from the left ventricle of healthy guinea-pig: 1) transmural differences in SL distribution between subepi- (EPI) and subendocardial (ENDO) cardiomyocytes; 2) the dependence of intracellular variability in SL upon the state of contraction; 3) local differences in SL variability, comparing SL distributions between central and peripheral regions within the cardiomyocyte. To characterize the intracellular variability of SL, we used different normality tests for the assessment of SL distributions, as well as nonparametric coefficients to quantify the variability. We found that individual SL values in the end-systolic state of contraction followed a normal distribution to a lesser extent as compared to the end-diastolic state of contraction (∼1.3-fold and ∼1.6-fold in ENDO and EPI, respectively). The relative and absolute coefficients of sarcomere-to-sarcomere variability in end-systolic SL were significantly greater (∼1.3-fold) as compared to end-diastolic SL. This was independent of both the transmural region across the left ventricle and the intracellular region within the cardiomyocyte. We conclude that the intracellular variability in SL, which exists in normal intact guinea-pig cardiomyocytes, is affected by the contractile state of the myocyte. This phenomenon may play a role in inter-sarcomere communication in the beating heart.

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Sarcomere Lengths Become More Uniform Over Time in Intact Muscle-Tendon Unit During Isometric Contractions

Cited by 6 publications

References 50 publications

Thick filament activation is different in fast‐ and slow‐twitch skeletal muscle

Thick filament activation is different in fast‐ and slow‐twitch skeletal muscle

The Energy of Muscle Contraction. III. Kinetic Energy During Cyclic Contractions

Contractile State Dependent Sarcomere Length Variability in Isolated Guinea-Pig Cardiomyocytes

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