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Characterization and Regulation of Mechanical Loading‐Induced Compensatory Muscle Hypertrophy

Gregory R. Adams, Marcas M. Bamman

10.1002/cphy.c110066

Source: Volume 2, Issue 4, October 2012

Published online: October 2012

Full Article on Wiley Online Library



Abstract

In mammalian systems, skeletal muscle exists in a dynamic state that monitors and regulates the physiological investment in muscle size to meet the current level of functional demand. This review attempts to consolidate current knowledge concerning development of the compensatory hypertrophy that occurs in response to a sustained increase in the mechanical loading of skeletal muscle. Topics covered include: defining and measuring compensatory hypertrophy, experimental models, loading stimulus parameters, acute responses to increased loading, hyperplasia, myofiber‐type adaptations, the involvement of satellite cells, mRNA translational control, mechanotransduction, and endocrinology. The authors conclude with their impressions of current knowledge gaps in the field that are ripe for future study. © 2012 American Physiological Society. Compr Physiol 2:2829‐2870, 2012.

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Figure 1. Figure 1.

Satellite cells and muscle hypertrophy. (A) The initial hypertrophy adaptation to a chronic increase in the loading state of myofibers is accomplished by accretion of cellular protein via upregulated protein synthesis. This would be expected to result in the recruitment of all intrinsic myonuclei for transcriptional activity. Over time, some threshold is thought to be reached at which all myonuclei are maximally involved in transcription and diffusion/localization of mRNA becomes limiting for further expansion of myofiber size. The activation of satellite cells and the incorporation of some of their progeny into myofibers would relieve this restriction. The addition of new myonuclei would facilitate continued protein synthesis to fill out new myonuclear domains. (B) The myonuclear domains of small myofibers may not reach a critical threshold with regard to the distribution of mRNA; and thus may not demand nuclear addition even in cases of extreme hypertrophy (e.g., via compensatory overload). However, human myofibers are much larger in size and appear to manifest domain size limitations.
Figure 2. Figure 2.

Translational signaling intracellular mechanisms converge to regulate the translational activity necessary to initiate hypertrophic responses. These (and other) pathways and effectors are known to be sensitive to a number of stimuli including mechanical forces on the cytoskeleton and cell membrane, growth factor receptor activity, and nutritional (primarily amino acid) status. Abbreviations: ECM, extracellular matrix; DGC, dystrophin‐associated glycoprotein complex; MEK, MAP kinase; ERK, extracellular response kinase; PI3‐kinase, phosphoinositide 3‐kinase; Akt, cellular homolog of the v‐Akt oncogene; mTOR, mammalian target of rapamycin; S6K1, ribosomal S6 kinase; 4E‐BP, eukaryotic initiation factor (eIF) 4E binding protein; GSK3, glycogen synthase kinase 3; FOXO, forkhead box O3 transcription factor; eIF2Bɛ, eukaryotic initiation factor 2Bɛ; eIF2, eukaryotic initiation factor 2.
Figure 3. Figure 3.

Elements of mechanotransduction. A number of components of the dystrophin‐associated glycoprotein complex (DGC), as well as transmembrane integrins, have been posited to contribute to the transduction of loading into biochemical and biological processes, that is, mechanotransduction. In particular, DGC‐associated nitric oxide synthase may be critical to the hypertrophic process.


Figure 1.

Satellite cells and muscle hypertrophy. (A) The initial hypertrophy adaptation to a chronic increase in the loading state of myofibers is accomplished by accretion of cellular protein via upregulated protein synthesis. This would be expected to result in the recruitment of all intrinsic myonuclei for transcriptional activity. Over time, some threshold is thought to be reached at which all myonuclei are maximally involved in transcription and diffusion/localization of mRNA becomes limiting for further expansion of myofiber size. The activation of satellite cells and the incorporation of some of their progeny into myofibers would relieve this restriction. The addition of new myonuclei would facilitate continued protein synthesis to fill out new myonuclear domains. (B) The myonuclear domains of small myofibers may not reach a critical threshold with regard to the distribution of mRNA; and thus may not demand nuclear addition even in cases of extreme hypertrophy (e.g., via compensatory overload). However, human myofibers are much larger in size and appear to manifest domain size limitations.



Figure 2.

Translational signaling intracellular mechanisms converge to regulate the translational activity necessary to initiate hypertrophic responses. These (and other) pathways and effectors are known to be sensitive to a number of stimuli including mechanical forces on the cytoskeleton and cell membrane, growth factor receptor activity, and nutritional (primarily amino acid) status. Abbreviations: ECM, extracellular matrix; DGC, dystrophin‐associated glycoprotein complex; MEK, MAP kinase; ERK, extracellular response kinase; PI3‐kinase, phosphoinositide 3‐kinase; Akt, cellular homolog of the v‐Akt oncogene; mTOR, mammalian target of rapamycin; S6K1, ribosomal S6 kinase; 4E‐BP, eukaryotic initiation factor (eIF) 4E binding protein; GSK3, glycogen synthase kinase 3; FOXO, forkhead box O3 transcription factor; eIF2Bɛ, eukaryotic initiation factor 2Bɛ; eIF2, eukaryotic initiation factor 2.



Figure 3.

Elements of mechanotransduction. A number of components of the dystrophin‐associated glycoprotein complex (DGC), as well as transmembrane integrins, have been posited to contribute to the transduction of loading into biochemical and biological processes, that is, mechanotransduction. In particular, DGC‐associated nitric oxide synthase may be critical to the hypertrophic process.

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Article Title: Characterization and Regulation of Mechanical Loading‐Induced Compensatory Muscle Hypertrophy
 

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Gregory R. Adams, Marcas M. Bamman. Characterization and Regulation of Mechanical Loading‐Induced Compensatory Muscle Hypertrophy. Compr Physiol 2012, 2: 2829-2870. doi: 10.1002/cphy.c110066