Human skeletal muscle biochemical diversity

Tirrell, Timothy F.; Cook, Mark S.; Carr, J. Austin; Lin, Evie; Ward, Samuel R.; Lieber, Richard L.

doi:10.1242/jeb.069385

Cited by 56 publications

(49 citation statements)

References 42 publications

(60 reference statements)

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“…2 and SI Appendix, Table S3). This is in marked contrast to humans, who exhibit a significant bias toward MHC I fibers in these same muscles and throughout the limbs and trunk overall (14,15). Although the genetic basis of skeletal muscle MHC isoform specification is an active area of research (e.g., ref.…”

Section: Resultsmentioning

confidence: 93%

“…Longer muscle fibers have a broader force-length relation that may enhance the dynamic force, work, and power capabilities of a muscle-tendon unit (20). Therefore, to estimate the net interacting effects of P o , V o , MHC distribution, and muscle fiber length on maximum dynamic muscle force and power output in vivo, we designed Hilltype "chimpanzee muscle" and "human muscle" models that reflected the parameter differences measured herein and elsewhere (14,15,19). Using computer simulations, we determined the maximum dynamic force and power-producing capabilities of these models at the whole-muscle level.…”

Section: Resultsmentioning

confidence: 99%

“…The curvature of the force-velocity relationship (A rel ) and activation-deactivation time constants (τ act , τ deact ) were calculated based on the average fraction of MHC II (fast-twitch) fibers determined for each species (C: 67%, H: 40%) (39). The distribution of fast-twitch fibers in humans represents an average of recent MHC measurements (i.e., MHC IIa+IIx) (14) and older immunohistochemistry measurements [i.e., fast oxidative glycolytic (FOG) + fast glycolytic (FG)] (15). To isolate the effects of muscle on performance, the simulations were conducted using rigid tendons with fiber pennation angles set to 0°.…”

Section: Methodsmentioning

confidence: 99%

“…Independent sample t tests were used to conduct pairwise comparisons between the average fraction of MHC I or slow-twitch fibers in chimpanzees and humans, as well as between the relative muscle fiber length in chimpanzees and humans. For the MHC I content and relative fiber-length comparisons, the same 35 muscles were compiled for the chimpanzee and human samples, with the exceptions that m. gluteus minimus MHC content was not reported in Tirrell et al (14) and m. obturator externus fiber length was not included in Arnold et al (24). Exclusion of these muscles from the chimpanzee samples did not alter the statistical significance of the t-test results.…”

Section: Methodsmentioning

confidence: 99%

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Chimpanzee super strength and human skeletal muscle evolution

O’Neill

Umberger

Holowka

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Since at least the 1920s, it has been reported that common chimpanzees (Pan troglodytes) differ from humans in being capable of exceptional feats of "super strength," both in the wild and in captive environments. A mix of anecdotal and more controlled studies provides some support for this view; however, a critical review of available data suggests that chimpanzee mass-specific muscular performance is a more modest 1.5 times greater than humans on average. Hypotheses for the muscular basis of this performance differential have included greater isometric force-generating capabilities, faster maximum shortening velocities, and/or a difference in myosin heavy chain (MHC) isoform content in chimpanzee relative to human skeletal muscle. Here, we show that chimpanzee muscle is similar to human muscle in its single-fiber contractile properties, but exhibits a much higher fraction of MHC II isoforms. Unlike humans, chimpanzee muscle is composed of ∼67% fast-twitch fibers (MHC IIa+IId). Computer simulations of species-specific whole-muscle models indicate that maximum dynamic force and power output is 1.35 times higher in a chimpanzee muscle than a human muscle of similar size. Thus, the superior mass-specific muscular performance of chimpanzees does not stem from differences in isometric force-generating capabilities or maximum shortening velocities-as has long been suggested-but rather is due in part to differences in MHC isoform content and fiber length. We propose that the hominin lineage experienced a decline in maximum dynamic force and power output during the past 7-8 million years in response to selection for repetitive, low-cost contractile behavior.chimpanzee | human | muscle | myosin heavy chain | muscle modeling M odern humans-with some exceptions-are often characterized as a weak and unathletic species compared with our closest living relatives, the chimpanzees. Whereas chimpanzees are proficient tree climbers and arborealists (1), our hominin ancestors gave up a reliance on the forest canopy after the emergence of the genus Homo (2). Subsequent evolution in brain size (3) and cognition as well as advancements in tools and other material culture (4, 5) have reduced our strict dependence on muscular strength for survival and fitness.Since at least the 1920s, both anecdotal reports and more controlled experiments have indicated that the strength of a chimpanzee can exceed that of a human (6-12). This has led to the now long-standing proposal that chimpanzees are "super strong" compared with humans. A critical review of experiments (i.e., pulling and jumping tasks) carried out between 1923 and 2014 suggests that chimpanzee mass-specific muscular performance consistently exceeds that of humans, with a differential of about 1.5 times, on average (SI Appendix, SI Discussion). Hypotheses for the muscular basis of the chimpanzee-human performance differential have included higher isometric force-producing capabilities (6-8, 11), faster maximum shortening velocities (7, 11), and/or a different distribution of myosin ...

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Section: Resultsmentioning

confidence: 93%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Chimpanzee super strength and human skeletal muscle evolution

O’Neill

Umberger

Holowka

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Biochemical quantification of collagen is often performed with a hydroxyproline assay to assess the degree of fibrosis within a whole muscle (43,45). These methods provide quantitative data on the amount of collagen in skeletal muscle tissue; however, they do not provide information on how collagen is organized.…”

mentioning

confidence: 99%

Collagen content does not alter the passive mechanical properties of fibrotic skeletal muscle in mdx mice

Smith

Barton

2014

American Journal of Physiology-Cell Physiology

112

159

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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.

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Why does strength training improve endurance performance?

Best

2020

American J Hum Biol

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Objective: The specificity of training principle holds that adaptations to exercise training closely match capacity to the specific demands of the stimulus. Improvements in endurance sport performance gained through strength training are a notable exception to this principle. While the proximate mechanisms for how strength training produces muscular adaptations beneficial to endurance sports are increasingly well understood, the ultimate causes of this phenomenon remain unexplored. Methods: Using a holistic approach tying together exercise physiology and evolution, I argue that we can reconcile the apparent "endurance training specificity paradox."Results and Conclusions: Competing selective pressures, inherited mammalian biology, and millennia of living in energy-scarce environments constrained our evolution as endurance athletes, but also imparted high muscular plasticity which can be exploited to improve endurance performance beyond what was useful in our evolutionary past.

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Human skeletal muscle biochemical diversity

Cited by 56 publications

References 42 publications

Chimpanzee super strength and human skeletal muscle evolution

Chimpanzee super strength and human skeletal muscle evolution

Collagen content does not alter the passive mechanical properties of fibrotic skeletal muscle in mdx mice

Why does strength training improve endurance performance?

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