Skeletal Muscle Cell Mass and Growth: The Concept of the Deoxyribonucleic Acid Unit

Cheek, Donald B.; Holt, A B; Hill, Donald E.; Talbert, James L.

doi:10.1203/00006450-197107000-00004

Cited by 150 publications

(99 citation statements)

References 35 publications

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“…The view that only satellite cells are myogenic has recently changed through the demonstration that cells expressing myogenic markers lie within the interstitial cell compartment (Asakura et al, 2002;Polesskaya et al, 2003), but the relationship between myogenic interstitial cells and satellite cells is presently unknown. It is currently thought that only satellite cells are responsible for the increase in myonuclei during normal growth through mitotic division and fusion of one or both of the daughter cells with their myofiber (Moss and Leblond, 1971;Cheek et al, 1971;Mozdziak et al, 1997;Anderson, 2006). Furthermore, it currently appears that myogenic interstitial cells are not necessary for muscle regeneration (Zammit et al, 2002;Collins et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Satellite cells express distinct patterns of myogenic proteins in immature skeletal muscle

Schultz

Chamberlain

McCormick

et al. 2006

Developmental Dynamics

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Satellite cells are the myogenic cells lying between the myofiber sarcolemma and basal lamina. The objective of this study was to determine the expression patterns of MyoD, myogenin, and Pax7 within the satellite cell population in the growing rat soleus and extensor digitorum longus (EDL) muscles. Secondly, the expression of the myogenic markers was also studied within the interstitial cell compartment and myonuclei. It was discovered that the soleus contained a higher number of Pax7, MyoD, or myogeninpositive nuclei compared with the EDL. Similarly, myogenin was expressed at a lower level in the myonuclei of the soleus compared with the EDL, and myogenin was expressed at a higher level in the interstitial compartment of the soleus compared with the EDL. When interstitial nuclei, myonuclei, and double-labeled nuclei were used in the estimate of the satellite cell population, it was discovered that approximately of 13% of the myofibers in a transverse section of the soleus muscle and 4.1% of EDL myofibers exhibit a labeled satellite cell nucleus. Overall, results from this study suggest that expression patterns of these markers vary predictably among muscles with different growth dynamics and phenotypic characteristics. Developmental Dynamics 235:3230 -3239, 2006.

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Section: Introductionmentioning

confidence: 99%

Satellite cells express distinct patterns of myogenic proteins in immature skeletal muscle

Schultz

Chamberlain

McCormick

et al. 2006

Developmental Dynamics

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“…Individuals with a greater basal presence of SCs demonstrated, with training, a remarkable ability to expand the SC pool, incorporate new nuclei, and achieve robust growth. strength training; skeletal muscle; neural cell adhesion molecule; myonucleus; myogenesis EACH MYONUCLEUS WITHIN THE multinucleated skeletal myofiber regulates gene transcription and subsequent protein synthesis over a finite volume of cytoplasm (6,7,23). This volume per nucleus, or myonuclear domain, is not a fixed quantity as evidenced during atrophy due to disuse (3, 24) or aging (25) as loss of cell volume exceeds nuclear shedding.…”

mentioning

confidence: 99%

Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis

Petrella¹,

Kim²,

Mayhew³

et al. 2008

Journal of Applied Physiology

371

380

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Petrella JK, Kim J, Mayhew DL, Cross JM, Bamman MM. Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis. J Appl Physiol 104: 1736-1742, 2008. First published April 24, 2008 doi:10.1152/japplphysiol.01215.2007.-A present debate in muscle biology is whether myonuclear addition is required during skeletal muscle hypertrophy. We utilized K-means cluster analysis to classify 66 humans after 16 wk of knee extensor resistance training as extreme (Xtr, n ϭ 17), modest (Mod, n ϭ 32), or nonresponders (Non, n ϭ 17) based on myofiber hypertrophy, which averaged 58, 28, and 0%, respectively (Bamman MM, Petrella JK, Kim JS, Mayhew DL, Cross JM. J Appl Physiol 102: [2232][2233][2234][2235][2236][2237][2238][2239] 2007). We hypothesized that robust hypertrophy seen in Xtr was driven by superior satellite cell (SC) activation and myonuclear addition. Vastus lateralis biopsies were obtained at baseline and week 16. SCs were identified immunohistochemically by surface expression of neural cell adhesion molecule. At baseline, myofiber size did not differ among clusters; however, the SC population was greater in Xtr (P Ͻ 0.01) than both Mod and Non, suggesting superior basal myogenic potential. SC number increased robustly during training in Xtr only (117%; P Ͻ 0.001). Myonuclear addition occurred in Mod (9%; P Ͻ 0.05) and was most effectively accomplished in Xtr (26%; P Ͻ 0.001). After training, Xtr had more myonuclei per fiber than Non (23%; P Ͻ 0.05) and tended to have more than Mod (19%; P ϭ 0.056). Both Xtr and Mod expanded the myonuclear domain to meet (Mod) or exceed (Xtr) 2,000 m 2 per nucleus, possibly driving demand for myonuclear addition to support myofiber expansion. These findings strongly suggest myonuclear addition via SC recruitment may be required to achieve substantial myofiber hypertrophy in humans. Individuals with a greater basal presence of SCs demonstrated, with training, a remarkable ability to expand the SC pool, incorporate new nuclei, and achieve robust growth. strength training; skeletal muscle; neural cell adhesion molecule; myonucleus; myogenesis EACH MYONUCLEUS WITHIN THE multinucleated skeletal myofiber regulates gene transcription and subsequent protein synthesis over a finite volume of cytoplasm (6,7,23). This volume per nucleus, or myonuclear domain, is not a fixed quantity as evidenced during atrophy due to disuse (3, 24) or aging (25) as loss of cell volume exceeds nuclear shedding. Similarly, our laboratory and others have shown that some initial myofiber hypertrophy can expand the cytoplasmic volume associated with each myonucleus (17,25). This has led some to debate whether the addition of nuclei is required for skeletal myofiber hypertrophy (23). However, a ceiling size on the domain has been suggested (17, 23, 25) based on the concept that sufficient expansion of the myonuclear domain likely puts each nucleus under greater strain to supply the necessary gene products, driving a demand for the a...

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“…and Leblond (1962) also observed that, up to 17 days of age, accretion of DNA was quite rapid and there was little or no change in mass weight of muscle per nucleus. This supports the evi dence that the total number of nuclei increases in each muscle cell during growth as has been reported by Winick and Noble (1965) and Cheek et al (1971).…”

Section: Dna and Rna -Indicators Of Cellular Growthsupporting

confidence: 77%

“…Cheek et al (1971) also found growth hormone to be necessary for cell multiplication. Kostyo (1968) and Young (1970) suggested that the major effects of growth hormone is on amino acid incorporation into protein with somewhat limited effects on amino acid transport.…”

Section: Growth Hormonementioning

confidence: 99%

“…Likewise the ratio of protein to DNA is regarded as an indication of cell size. Cheek et al (1971) suggested that a particular nucleus within a muscle fiber exerts control over only a small portion of cytoplasm and referred to this as a "physiological cell" even though muscle fibers are multinucleated. Cheek et al (1965) re ported an eight fold increase in cell size and a five fold increase in cell number (physiological cell) in skeletal muscles of rats from 1 to 8 weeks in age.…”

Section: Dna and Rna -Indicators Of Cellular Growthmentioning

confidence: 99%

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Growth, cellular development of skeletal muscle and body composition of rats selected for post weaning gain

Woodward

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Skeletal Muscle Cell Mass and Growth: The Concept of the Deoxyribonucleic Acid Unit

Cited by 150 publications

References 35 publications

Satellite cells express distinct patterns of myogenic proteins in immature skeletal muscle

Satellite cells express distinct patterns of myogenic proteins in immature skeletal muscle

Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis

Growth, cellular development of skeletal muscle and body composition of rats selected for post weaning gain

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