Satellite cells in human skeletal muscle plasticity

Tim Snijders, Joshua P Nederveen, Bryon R McKay, Sophie Joanisse, Lex B Verdijk, Luc J C van Loon, Gianni Parise, Tim Snijders, Joshua P Nederveen, Bryon R McKay, Sophie Joanisse, Lex B Verdijk, Luc J C van Loon, Gianni Parise

Abstract

Skeletal muscle satellite cells are considered to play a crucial role in muscle fiber maintenance, repair and remodeling. Our knowledge of the role of satellite cells in muscle fiber adaptation has traditionally relied on in vitro cell and in vivo animal models. Over the past decade, a genuine effort has been made to translate these results to humans under physiological conditions. Findings from in vivo human studies suggest that satellite cells play a key role in skeletal muscle fiber repair/remodeling in response to exercise. Mounting evidence indicates that aging has a profound impact on the regulation of satellite cells in human skeletal muscle. Yet, the precise role of satellite cells in the development of muscle fiber atrophy with age remains unresolved. This review seeks to integrate recent results from in vivo human studies on satellite cell function in muscle fiber repair/remodeling in the wider context of satellite cell biology whose literature is largely based on animal and cell models.

Keywords: IGF-1; Pax7; aging; exercise; interleukin-6; muscle fiber hypertrophy; muscle satellite cells; myostatin.

Figures

Figure 1
Figure 1
Proportion (±SEM) of satellite cell pool positive for interleukin-6 (IL-6), myostatin (MSTN), phosphorylated signal transducer and activator of transcription 3 (pSTAT3), cMyc, Myogenic Differentiation (MyoD), Delta Like 1 (DLK1), Proliferating cell nuclear antigen (PCNA), Ki-67, determined by immunohistochemistry, and “active” (G2/M phase) and “quiescent” (G0/G1 phase) satellite cells assessed by flow cytometric in resting vastus lateralis muscle from healthy young men (combined data from O'Reilly et al., ; McKay et al., , , , , ; Toth et al., ; Snijders et al., , ,; Cermak et al., ; Bellamy et al., 2014).
Figure 2
Figure 2
Mean (±SEM) number of satellite cells (mixed muscle) expressed as a percentage of total myonuclei before and 1, 3, 4, 24, 72, and 120 h after a single bout of eccentric exercise in healthy young men (n = 52; combined data from McKay et al., , , ; Toth et al., 2011).
Figure 3
Figure 3
Schematic representation of normal (A) and aged (B) myogenic program in response to an anabolic stimulus. In adult skeletal muscle, satellite cells are typically in a quiescent state and reside in a niche between the sarcolemma and basal lamina of their associated muscle fiber. Upon stimulation, i.e., following exercise, satellite cells become activated, and start to proliferate. Following proliferation, satellite cells differentiate, and either fuse with each other forming new myofibers, fuse to an existing muscle fiber donating their nucleus to the fiber thereby allowing muscle fiber hypertrophy, or return back to their quiescent state (self-renewal). The progression of the satellite cell through the myogenic program is orchestrated by the up- or down-regulation of the paired box transcription factor Pax7 and the myogenic regulatory factors (e.g., Myf5, MyoD, MRF4, and Myogenin). A number of factors [e.g., hepatocyte growth factor (HGF), myostatin (Mstn), Notch/Delta1, interleukin-6 (IL-6), mechano growth factor (MGF), and insulin like growth factor-1 (IGF-1)] have been identified to have a positive/negative influence on the different stages of the myogenic program. In aged skeletal muscle the number of muscle satellite cells is reduced and the microstructure of the niche is altered. An increased subclinical level of inflammation and increased Mstn in the circulation has been suggested to impair or delay the proliferative drive of satellite cells in response to anabolic stimuli. Alternatively, it has been hypothesized that in aged muscle the activated satellite cells may also commit directly to differentiation, i.e., skipping the proliferation phase. Studies suggest that aged satellite cells are more likely to differentiate to an alternative cell fate (e.g., adipocytes, fibroblasts) or are directed toward apoptosis, thereby reducing the number of myonuclei formed to allow adequate repair and/or hypertrophy of the muscle fiber. Increased systemic levels of Mstn reduces the fusion of newly formed myonuclei, impairing muscle repair and regeneration, and impairs fusion of myonuclei to existing muscle fibers, limiting muscle fiber growth in aged skeletal muscle.

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