Skeletal muscle satellite cells: Changes in proliferation potential as a function of age

doi:10.1016/0047-6374(82)90105-1

Mechanisms of Ageing and Development

Volume 20, Issue 4, December 1982, Pages 377-383

https://doi.org/10.1016/0047-6374(82)90105-1 Get rights and content

Abstract

Skeletal muscle satellite cells were isolated from soleus and extensor digitorum longus muscles of Sprague-Dawley rats at selected ages between 6 days and 30 months and grown in cell culture. Cells at each donor age were monitored individually to determine the number of progeny they were capable of producing. Under identical in vitro conditions, the average number of progeny produced was inversely proportional to donor age. Hence, the proliferation potential of satellite cells decreases with age.

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Muscle tissue engineering is a promising therapeutic strategy for volumetric muscle loss (VML). Among them, decellularized extracellular matrix (dECM) biological scaffolds have shown certain effects in restoring muscle function. However, researchers have inconsistent or even contradictory results on whether dECM biological scaffolds can efficiently regenerate muscle fibers and restore muscle function. This suggests that therapeutic strategies based on dECM biological scaffolds need to be further optimized and developed. In this study, we used a recellularization method of perfusing adipose-derived stem cells (ASCs) and L6 into adipose dECM (adECM) through vascular pedicles. On one hand, this strategy ensures sufficient quantity and uniform distribution of seeded cells inside scaffold. On the other hand, auxiliary L6 cells addresses the issue of low myogenic differentiation efficiency of ASCs. Subsequently, the treatment of VML animal experiments showed that the combined recellularization strategy can improve muscle regeneration and angiogenesis than the single ASCs recellularization strategy, and the TA of former had greater muscle contraction strength. Further single-nucleus RNA sequencing (snRNA-seq) analysis found that L6 cells induced ASCs transform into a new subpopulation of cells highly expressing Mki67, CD34 and CDK1 genes, which had stronger ability of oriented myogenic differentiation. This study demonstrates that co-seeding ASCs and L6 cells through vascular pedicles is a promising recellularization strategy for adECM biological scaffolds, and the engineered muscle tissue constructed based on this has significant therapeutic effects on VML. Overall, this study provides a new paradigm for optimizing and developing dECM-based therapeutic strategies.
Effects of thermal stress and mechanistic target of rapamycin and wingless-type mouse mammary tumor virus integration site family pathways on the proliferation and differentiation of satellite cells derived from the breast muscle of different chicken lines
2023, Poultry Science
Satellite cells (SCs) are muscle stem cells responsible for muscle hypertrophic growth and the regeneration of damaged muscle. Proliferation and differentiation of the pectoralis major (p. major) muscle SCs are responsive to thermal stress in turkeys, which are, in part, regulated by mechanistic target of rapamycin (mTOR) and Frizzled7 (Fzd7)-mediated wingless-type mouse mammary tumor virus integration site family/planar cell polarity (Wnt/PCP) pathways in a growth dependent-manner. It is not known if chicken p. major SCs respond to thermal stress in a manner similar to that of turkey p. major SCs. The objective of the current study was to investigate the effects of thermal stress and mTOR and Wnt/PCP pathways on the proliferation, differentiation, and expression of myogenic transcriptional regulatory factors in SCs isolated from the p. major muscle of a current modern commercial (MC) broiler line as compared to that of a Cornish Rock (BPM8) and Randombred (RBch) chicken line in the 1990s. The MC line SCs had lower proliferation and differentiation rates and decreased expression of myoblast determination factor 1 (MyoD) and myogenin (MyoG) compared to the BPM8 and RBch lines. Heat stress (43°C) increased proliferation and MyoD expression in all the cell lines, while cold stress (33°C) showed a suppressive effect compared to the control temperature (38°C). Satellite cell differentiation was altered with heat and cold stress in a cell line-specific manner. In general, the differentiation of the MC SCs was less responsive to both heat and cold stress compared to the BPM8 and RBch lines. Knockdown of the expression of either mTOR or Fzd7 decreased the proliferation, differentiation, and the expression of MyoD and MyoG in all the cell lines. The MC line during proliferation was more dependent on the expression of mTOR and Fzd7 than during differentiation. Thus, modern commercial meat-type chickens have decreased myogenic activity and temperature sensitivity of SCs in an mTOR- and Fzd7-dependent manner. The decrease in muscle regeneration will make modern commercial broilers more susceptible to the negative effects of myopathies with muscle fiber necrosis requiring satellite cell-mediated repair.
Bovine muscle satellite cells in calves and cattle: A comparative study of cellular and genetic characteristics for cultivated meat production
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This study compared the cellular and genetic characteristics of bovine skeletal muscle satellite cells (SMSCs) from Hanwoo (a Korean native cattle breed), including calves and mature cattle. SMSCs were isolated using magnetic-activated cell sorting (MACS) from tissue samples of six Hanwoo (three calves and three mature cattle) using the CD29 antibody. Calves’ SMSCs exhibited significantly faster growth rates than did those from cattle (P < 0.01), with a doubling time of 2.43 days. Genetic analysis revealed higher MyoD and Pax7 expression in SMSCs from calves during proliferation than in those from mature cattle (P < 0.001). However, FASN and PLAG1 expression levels were higher in mature cattle than in calves during both proliferation and differentiation (P < 0.001). These findings highlight the need for strategies to improve bovine muscle cell growth to produce competitive cultivated meat at a competitive price.
Aging of the immune system and impaired muscle regeneration: A failure of immunomodulation of adult myogenesis
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Skeletal muscle regeneration that follows acute injury is strongly influenced by interactions with immune cells that invade and proliferate in the damaged tissue. Discoveries over the past 20 years have identified many of the key mechanisms through which myeloid cells, especially macrophages, regulate muscle regeneration. In addition, lymphoid cells that include CD8+ T-cells and regulatory T-cells also significantly affect the course of muscle regeneration. During aging, the regenerative capacity of skeletal muscle declines, which can contribute to progressive loss of muscle mass and function. Those age-related reductions in muscle regeneration are accompanied by systemic, age-related changes in the immune system, that affect many of the myeloid and lymphoid cell populations that can influence muscle regeneration. In this review, we present recent discoveries that indicate that aging of the immune system contributes to the diminished regenerative capacity of aging muscle. Intrinsic, age-related changes in immune cells modify their expression of factors that affect the function of a population of muscle stem cells, called satellite cells, that are necessary for normal muscle regeneration. For example, age-related reductions in the expression of growth differentiation factor-3 (GDF3) or CXCL10 by macrophages negatively affect adult myogenesis, by disrupting regulatory interactions between macrophages and satellite cells. Those changes contribute to a reduction in the numbers and myogenic capacity of satellite cells in old muscle, which reduces their ability to restore damaged muscle. In addition, aging produces changes in the expression of molecules that regulate the inflammatory response to injured muscle, which also contributes to age-related defects in muscle regeneration. For example, age-related increases in the production of osteopontin by macrophages disrupts the normal inflammatory response to muscle injury, resulting in regenerative defects. These nascent findings represent the beginning of a newly-developing field of investigation into mechanisms through which aging of the immune system affects muscle regeneration.
Myogenic marker expression as a function of age and exercise-based therapy in the tongue
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Degeneration of tongue muscles with aging may contribute to swallowing deficits observed in elderly people. However, the capacity for tongue muscle stem cells (SCs) to regenerate and repair the aged tongue and improve tongue strength following tongue exercise (a current clinical treatment) has never been examined. We found that the expression of regenerative, myogenic markers were impaired with age and may be related to increased expression of senescent marker p16^INK4a. Tongue strength increased in young adult and old rats following exercise and was related to the expression of Pax7, MyoD, myogenin, and p16^INK4a. Our study also suggests that strengthening of tongue muscles via clinical rehabilitation strategies also increased the expression of SC regenerative markers in the tongue throughout the exercise duration.
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2024, Aging and Disease

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Mechanisms of Ageing and Development

Abstract

References (24)

Satellite cells and myofiber growth in the rat soleus and extensor digitorum longus muscles

Dev. Biol.

Myogenic potential of satellite cells in skeletal muscle of old rats: a brief note

Mech. Ageing Dev.

Influence of age on accumulation of α-actinin satellite-cell-derived myotubes in vitro

Mech. Ageing Dev.

A fine structured analysis of normal and modulated cells in myogenic cultures

Dev. Biol.

The latent period of explanted organs of newborn adult and senile rats

Exp. Cell Res.

Basic mechanisms of aging in the neuromuscular system

Mech. Ageing Dev.

Regeneration and transplantation of muscles in old rats and between young and old rats

Life Sci.

Origin of regenerating myoblasts in mammalian skeletal muscle

Satellite cells as a source of nuclei in muscles of growing rats

Anat. Rec.

The fate of newly formed satellite cells during compensatory muscle hypertrophy

Virchows Arch. B. Cell Pathol.

The distribution of satellite cells and their relationship to specific fiber types in soleus and extensor digitorum longus muscles

Anat. Rec.

Activation of muscle nuclei in denervation and hypertrophy

Basic Res. Myol.

Cited by (276)

Perfusable adipose decellularized extracellular matrix biological scaffold co-recellularized with adipose-derived stem cells and L6 promotes functional skeletal muscle regeneration following volumetric muscle loss

Effects of thermal stress and mechanistic target of rapamycin and wingless-type mouse mammary tumor virus integration site family pathways on the proliferation and differentiation of satellite cells derived from the breast muscle of different chicken lines

Bovine muscle satellite cells in calves and cattle: A comparative study of cellular and genetic characteristics for cultivated meat production

Aging of the immune system and impaired muscle regeneration: A failure of immunomodulation of adult myogenesis

Myogenic marker expression as a function of age and exercise-based therapy in the tongue

Semaphorins: Missing Signals in Age-dependent Alteration of Neuromuscular Junctions and Skeletal Muscle Regeneration