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Mechanisms Modulating Skeletal Muscle Phenotype

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Abstract

Mammalian skeletal muscles are composed of a variety of highly specialized fibers whose selective recruitment allows muscles to fulfill their diverse functional tasks. In addition, skeletal muscle fibers can change their structural and functional properties to perform new tasks or respond to new conditions. The adaptive changes of muscle fibers can occur in response to variations in the pattern of neural stimulation, loading conditions, availability of substrates, and hormonal signals. The new conditions can be detected by multiple sensors, from membrane receptors for hormones and cytokines, to metabolic sensors, which detect high‐energy phosphate concentration, oxygen and oxygen free radicals, to calcium binding proteins, which sense variations in intracellular calcium induced by nerve activity, to load sensors located in the sarcomeric and sarcolemmal cytoskeleton. These sensors trigger cascades of signaling pathways which may ultimately lead to changes in fiber size and fiber type. Changes in fiber size reflect an imbalance in protein turnover with either protein accumulation, leading to muscle hypertrophy, or protein loss, with consequent muscle atrophy. Changes in fiber type reflect a reprogramming of gene transcription leading to a remodeling of fiber contractile properties (slow‐fast transitions) or metabolic profile (glycolytic‐oxidative transitions). While myonuclei are in postmitotic state, satellite cells represent a reserve of new nuclei and can be involved in the adaptive response. © 2013 American Physiological Society. Compr Physiol 3:1645‐1687, 2013.

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Figure 1. Figure 1. The complete panel of sarcomeric MYH genes in mammals with the corresponding protein products and their expression pattern. The evolutionary relationship between MYH genes is indicated in the phylogenetic tree on the left. Spacing and length of the branches do not reflect actual scale in this simplified scheme. Only extrafusal muscle fibers are considered for the expression pattern. §Expression only in some mammalian species. *MYH7b, also referred to as MYH14, is expressed in both slow muscles and heart at the transcript level, but only in extraocular muscles at the protein level (). Scheme, with permission, from ().
Figure 2. Figure 2. Myosin heavy chain isoforms are the determinants of ATPase activity and maximum shortening velocity (Vo) of single muscle fibers and of filament sliding speed (Vf) on purified myosin in vitro motility assay. Fibers expressing specific myosin isoforms (1 or slow, 2A, 2X, and 2B) have been isolated from muscles of five mammalian species: in all species a progressive increase in ATPase rate, shortening velocity and sliding filament velocity from slow () to 2A, 2X, and 2B is detectable. Comparing different species the kinetics parameters vary in inverse proportion to body size. Note that (i) 2B myosin is not expressed in human and (ii) for experimental reasons determinations of ATPase and Vf were not performed for all myosin isoform in each species. Data, with permission, from ().
Figure 3. Figure 3. Cytosolic calcium transients (A) and myofibrillar response to calcium (B) vary among fiber types. Panel A: calcium transients in four different murine fiber types (1 or slow, 2A, 2X, 2B): the amplitude has been normalized to better show the difference in the decline rate. Adapted, with permission, from (). Panel B: pCa‐force curves in four fiber types from the rat diaphragm: note the greater steepness of the curves of the fast fibers and the greater sensitivity to low calcium concentration of slow fibers. Adapted, with permission, from ()
Figure 4. Figure 4. Myogenic and neurogenic control of fiber‐type specification in skeletal muscles. The scheme illustrates the adaptive range of MyHC transformations observed in different muscle systems after experimental interventions aimed at dissecting the relative contribution of neurogenic factors that induce muscle plasticity and intrinsic myogenic constraints that limit the range of possible adaptations. Based on results from () for electrically stimulated fast and slow rat limb muscles (pink and green, respectively), from () and () for reinnervated rat laryngeal (thyroarytenoid, pale blue) muscle, and from () for reinnervated cat jaw muscle (violet). Scheme, with permission, from ().
Figure 5. Figure 5. Summary of some conditions and factors able to induce skeletal muscle hypertrophy and atrophy. Overload: functional overload imposed by elimination of synergistic muscles; unload: muscle unloading induced by hindlimb suspension or in conditions of microgravity.
Figure 6. Figure 6. Summary of some conditions and factors able to modulate the muscle fiber‐type phenotype. CLFS: chronic electrical stimulation applied continuously either via nerve or directly to denervated muscles; overload: functional overload imposed by elimination of synergistic muscles; unload: muscle unloading induced by hindlimb suspension or in conditions of microgravity.
Figure 7. Figure 7. Adaptive response to chronic electrical stimulation of rat fast muscles, underlining the effects of frequency and amount of stimuli delivered to muscles. Force‐frequency curve and twitch time to peak are taken as read out of muscle adaptation. Panel A shows that prolongation of time to peak (i.e., fast to slow transformation) is only induced by low‐frequency stimulation (<20 Hz). Panel B shows that the effect of the amount of stimuli delivered in 24 h is not effective if the frequency of stimulation is not adequately low. Panel C shows the shift to the left (i.e., toward lower fusion frequency) of the force‐frequency curve and the increase of the twitch/tetanus ratio in relation to the frequency of chronic. Those effects are significant only when stimulation rate is below 50 Hz. Modified, with permission, from ()
Figure 8. Figure 8. The role of intracellular calcium in the regulation of muscle size and function. As can be seen, changes in the level of intracellular calcium can have pronounced effects on the size and function of adult skeletal muscle.
Figure 9. Figure 9. Signaling pathways involved in skeletal muscle hypertrophy. The scheme highlights two major pathways, the IGF/Akt and the myostatin/Smad pathways, which converge on mTOR and protein synthesis.
Figure 10. Figure 10. Overview of the different major pathways involved in the transcriptional regulation of muscle plasticity, focusing on the role of PGC‐1α, AMPK, mTOR, and Cn‐NFAT.


Figure 1. The complete panel of sarcomeric MYH genes in mammals with the corresponding protein products and their expression pattern. The evolutionary relationship between MYH genes is indicated in the phylogenetic tree on the left. Spacing and length of the branches do not reflect actual scale in this simplified scheme. Only extrafusal muscle fibers are considered for the expression pattern. §Expression only in some mammalian species. *MYH7b, also referred to as MYH14, is expressed in both slow muscles and heart at the transcript level, but only in extraocular muscles at the protein level (). Scheme, with permission, from ().


Figure 2. Myosin heavy chain isoforms are the determinants of ATPase activity and maximum shortening velocity (Vo) of single muscle fibers and of filament sliding speed (Vf) on purified myosin in vitro motility assay. Fibers expressing specific myosin isoforms (1 or slow, 2A, 2X, and 2B) have been isolated from muscles of five mammalian species: in all species a progressive increase in ATPase rate, shortening velocity and sliding filament velocity from slow () to 2A, 2X, and 2B is detectable. Comparing different species the kinetics parameters vary in inverse proportion to body size. Note that (i) 2B myosin is not expressed in human and (ii) for experimental reasons determinations of ATPase and Vf were not performed for all myosin isoform in each species. Data, with permission, from ().


Figure 3. Cytosolic calcium transients (A) and myofibrillar response to calcium (B) vary among fiber types. Panel A: calcium transients in four different murine fiber types (1 or slow, 2A, 2X, 2B): the amplitude has been normalized to better show the difference in the decline rate. Adapted, with permission, from (). Panel B: pCa‐force curves in four fiber types from the rat diaphragm: note the greater steepness of the curves of the fast fibers and the greater sensitivity to low calcium concentration of slow fibers. Adapted, with permission, from ()


Figure 4. Myogenic and neurogenic control of fiber‐type specification in skeletal muscles. The scheme illustrates the adaptive range of MyHC transformations observed in different muscle systems after experimental interventions aimed at dissecting the relative contribution of neurogenic factors that induce muscle plasticity and intrinsic myogenic constraints that limit the range of possible adaptations. Based on results from () for electrically stimulated fast and slow rat limb muscles (pink and green, respectively), from () and () for reinnervated rat laryngeal (thyroarytenoid, pale blue) muscle, and from () for reinnervated cat jaw muscle (violet). Scheme, with permission, from ().


Figure 5. Summary of some conditions and factors able to induce skeletal muscle hypertrophy and atrophy. Overload: functional overload imposed by elimination of synergistic muscles; unload: muscle unloading induced by hindlimb suspension or in conditions of microgravity.


Figure 6. Summary of some conditions and factors able to modulate the muscle fiber‐type phenotype. CLFS: chronic electrical stimulation applied continuously either via nerve or directly to denervated muscles; overload: functional overload imposed by elimination of synergistic muscles; unload: muscle unloading induced by hindlimb suspension or in conditions of microgravity.


Figure 7. Adaptive response to chronic electrical stimulation of rat fast muscles, underlining the effects of frequency and amount of stimuli delivered to muscles. Force‐frequency curve and twitch time to peak are taken as read out of muscle adaptation. Panel A shows that prolongation of time to peak (i.e., fast to slow transformation) is only induced by low‐frequency stimulation (<20 Hz). Panel B shows that the effect of the amount of stimuli delivered in 24 h is not effective if the frequency of stimulation is not adequately low. Panel C shows the shift to the left (i.e., toward lower fusion frequency) of the force‐frequency curve and the increase of the twitch/tetanus ratio in relation to the frequency of chronic. Those effects are significant only when stimulation rate is below 50 Hz. Modified, with permission, from ()


Figure 8. The role of intracellular calcium in the regulation of muscle size and function. As can be seen, changes in the level of intracellular calcium can have pronounced effects on the size and function of adult skeletal muscle.


Figure 9. Signaling pathways involved in skeletal muscle hypertrophy. The scheme highlights two major pathways, the IGF/Akt and the myostatin/Smad pathways, which converge on mTOR and protein synthesis.


Figure 10. Overview of the different major pathways involved in the transcriptional regulation of muscle plasticity, focusing on the role of PGC‐1α, AMPK, mTOR, and Cn‐NFAT.
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Bert Blaauw, Stefano Schiaffino, Carlo Reggiani. Mechanisms Modulating Skeletal Muscle Phenotype. Compr Physiol 2013, 3: 1645-1687. doi: 10.1002/cphy.c130009