Abstract:Passive skeletal muscle derives its structural response from the combination of the titin filaments in the muscle fibres, the collagen fibres in the connective tissue and incompressibility due to the high fluid content. Experiments have shown that skeletal muscle tissue presents a highly asymmetrical three-dimensional behaviour when passively loaded in tension or compression, but structural models predicting this are not available. The objective of this paper is to develop a mathematical model to study the int… Show more
“…Recent models based on passive material properties of porcine muscle suggest that the contribution of stretched parallel elastic elements to passive stiffness becomes significant only at sarcomere lengths longer than those used in our study (Gindre et al, 2013). As a consequence of constant volume, muscles also expand radially during shortening or compression.…”
Section: Contribution Of Elastic Elements To Active and Passive Musclmentioning
confidence: 61%
“…Radial expansion will also load collagen fibers in the extracellular matrix. However, the increase in stress of collagen fibers due to radial expansion becomes significant only at sarcomere lengths much shorter than the ones used in this study (Gindre et al, 2013).…”
Section: Contribution Of Elastic Elements To Active and Passive Musclmentioning
confidence: 70%
“…Intact skeletal muscles are composed of a variety of elastic elements, both inside and outside muscle sarcomeres (Gindre et al, 2013;Roberts, 2016). Owing to the complexity and integration of these structures, it is difficult to differentiate their roles at the level of intact muscles.…”
Titin has long been known to contribute to muscle passive tension. Recently, it was also demonstrated that titin-based stiffness increases upon Ca 2+ activation of wild-type mouse psoas myofibrils stretched beyond overlap of the thick and thin filaments. In addition, this increase in titin-based stiffness was impaired in single psoas myofibrils from mdm mice, characterized by a deletion in the N2A region of the Ttn gene. Here, we investigated the effects of activation on elastic properties of intact soleus muscles from wild-type and mdm mice to determine whether titin contributes to active muscle stiffness. Using load-clamp experiments, we compared the stress-strain relationships of elastic elements in active and passive muscles during unloading, and quantified the change in stiffness upon activation. Results from wild-type muscles show that upon activation, the elastic modulus increases, elastic elements develop force at 15% shorter lengths, and there was a 2.9-fold increase in the slope of the stress-strain relationship. These results are qualitatively and quantitatively similar to results from single wild-type psoas myofibrils. In contrast, mdm soleus showed no effect of activation on the slope or intercept of the stress-strain relationship, which is consistent with impaired titin activation observed in single mdm psoas myofibrils. Therefore, it is likely that titin plays a role in the increase of active muscle stiffness during rapid unloading. These results are consistent with the idea that, in addition to the thin filaments, titin is activated upon Ca 2+ influx in skeletal muscle.
“…Recent models based on passive material properties of porcine muscle suggest that the contribution of stretched parallel elastic elements to passive stiffness becomes significant only at sarcomere lengths longer than those used in our study (Gindre et al, 2013). As a consequence of constant volume, muscles also expand radially during shortening or compression.…”
Section: Contribution Of Elastic Elements To Active and Passive Musclmentioning
confidence: 61%
“…Radial expansion will also load collagen fibers in the extracellular matrix. However, the increase in stress of collagen fibers due to radial expansion becomes significant only at sarcomere lengths much shorter than the ones used in this study (Gindre et al, 2013).…”
Section: Contribution Of Elastic Elements To Active and Passive Musclmentioning
confidence: 70%
“…Intact skeletal muscles are composed of a variety of elastic elements, both inside and outside muscle sarcomeres (Gindre et al, 2013;Roberts, 2016). Owing to the complexity and integration of these structures, it is difficult to differentiate their roles at the level of intact muscles.…”
Titin has long been known to contribute to muscle passive tension. Recently, it was also demonstrated that titin-based stiffness increases upon Ca 2+ activation of wild-type mouse psoas myofibrils stretched beyond overlap of the thick and thin filaments. In addition, this increase in titin-based stiffness was impaired in single psoas myofibrils from mdm mice, characterized by a deletion in the N2A region of the Ttn gene. Here, we investigated the effects of activation on elastic properties of intact soleus muscles from wild-type and mdm mice to determine whether titin contributes to active muscle stiffness. Using load-clamp experiments, we compared the stress-strain relationships of elastic elements in active and passive muscles during unloading, and quantified the change in stiffness upon activation. Results from wild-type muscles show that upon activation, the elastic modulus increases, elastic elements develop force at 15% shorter lengths, and there was a 2.9-fold increase in the slope of the stress-strain relationship. These results are qualitatively and quantitatively similar to results from single wild-type psoas myofibrils. In contrast, mdm soleus showed no effect of activation on the slope or intercept of the stress-strain relationship, which is consistent with impaired titin activation observed in single mdm psoas myofibrils. Therefore, it is likely that titin plays a role in the increase of active muscle stiffness during rapid unloading. These results are consistent with the idea that, in addition to the thin filaments, titin is activated upon Ca 2+ influx in skeletal muscle.
“…Titin is purported to be the primary contributor to intracellular skeletal muscle passive mechanics, with mechanical stiffness dependent on alternative splicing (48). However, there is evidence that extracellular components bear most of the passive load in whole mammalian muscle, particularly at 10% strain (13,15). It is currently unknown how titin splice variants are affected in mdx skeletal muscle and how titin alteration might affect mdx muscle stiffness.…”
Many skeletal muscle diseases are associated with progressive fibrosis leading to impaired muscle function. Collagen within the extracellular matrix is the primary structural protein providing a mechanical scaffold for cells within tissues. During fibrosis collagen not only increases in amount but also undergoes posttranslational changes that alter its organization that is thought to contribute to tissue stiffness. Little, however, is known about collagen organization in fibrotic muscle and its consequences for function. To investigate the relationship between collagen content and organization with muscle mechanical properties, we studied mdx mice, a model for Duchenne muscular dystrophy (DMD) that undergoes skeletal muscle fibrosis, and age-matched control mice. We determined collagen content both histologically, with picosirius red staining, and biochemically, with hydroxyproline quantification. Collagen content increased in the mdx soleus and diaphragm muscles, which was exacerbated by age in the diaphragm. Collagen packing density, a parameter of collagen organization, was determined using circularly polarized light microscopy of picosirius red-stained sections. Extensor digitorum longus (EDL) and soleus muscle had proportionally less dense collagen in mdx muscle, while the diaphragm did not change packing density. The mdx muscles had compromised strength as expected, yet only the EDL had a significantly increased elastic stiffness. The EDL and diaphragm had increased dynamic stiffness and a change in relative viscosity. Unexpectedly, passive stiffness did not correlate with collagen content and only weakly correlated with collagen organization. We conclude that muscle fibrosis does not lead to increased passive stiffness and that collagen content is not predictive of muscle stiffness.
“…Collagen is very resilient; thus, the collagen fibers responsible for passive force production in the ECM would be expected to be efficiently elastic. Viscoelastic behavior in whole muscle may result from the complex interaction of collagen fibers and muscle fluid pressure that occurs as fibers reorient and generate force (Gindre et al, 2013). At the level of both whole muscles and single fibers, the viscoelastic behavior of passive muscle is strain rate dependent (Rehorn et al, 2014); thus, the potential spring-like function of these elements may be variable depending upon the speed of movement.…”
Section: Energy Storage Capacity Of Tendonmentioning
Muscle force production occurs within an environment of tissues that exhibit spring-like behavior, and this elasticity is a critical determinant of muscle performance during locomotion. Muscle force and power output both depend on the speed of contraction, as described by the isotonic force-velocity curve. By influencing the speed of contractile elements, elastic structures can have a profound effect on muscle force, power and work. In very rapid movements, elastic mechanisms can amplify muscle power by storing the work of muscle contraction slowly and releasing it rapidly. When energy must be dissipated rapidly, such as in landing from a jump, energy stored rapidly in elastic elements can be released more slowly to stretch muscle contractile elements, reducing the power input to muscle and possibly protecting it from damage. Elastic mechanisms identified so far rely primarily on in-series tendons, but many structures within muscles exhibit springlike properties. Actomyosin cross-bridges, actin and myosin filaments, titin, and the connective tissue scaffolding of the extracellular matrix all have the potential to store and recover elastic energy during muscle contraction. The potential contribution of these elements can be assessed from their stiffness and estimates of the strain they undergo during muscle function. Such calculations provide boundaries for the possible roles these springs might play in locomotion, and may help to direct future studies of the uses of elastic elements in muscle.
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