Consistent expression pattern of myogenic regulatory factors in whole muscle and isolated human muscle satellite cells after eccentric contractions in humans

Nederveen, Joshua P.; Fortino, Stephen A.; Baker, Jeff; Snijders, Tim; Joanisse, Sophie; McGlory, Chris; McKay, Bryon R.; Kumbhare, Dinesh; Parise, Gianni

doi:10.1152/japplphysiol.01123.2018

Cited by 16 publications

(5 citation statements)

References 56 publications

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“…In skeletal muscle, ∼10 mg was used for total RNA extraction, as previously described, using the TRIzol method (Nederveen et al., 2019). Similarly, for cell culture experiments, cells were lysed in TRIzol and a similar extraction protocol was followed.…”

Section: Methodsmentioning

confidence: 99%

Circulating exosome‐like vesicle and skeletal muscle microRNAs are altered with age and resistance training

Xhuti

Nilsson

Manta

et al. 2023

The Journal of Physiology

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The age‐related loss of skeletal muscle mass and functionality, known as sarcopenia, is a critical risk factor for morbidity and all‐cause mortality. Resistance exercise training (RET) is the primary countermeasure to fight sarcopenia and ageing. Altered intercellular communication is a hallmark of ageing, which is not well elucidated. Circulating extracellular vesicles (EVs), including exosomes, contribute to intercellular communication by delivering microRNAs (miRNAs), which modulate post‐translational modifications, and have been shown to be released following exercise. There is little evidence regarding how EVs or EV‐miRNAs are altered with age or RET. Therefore, we sought to characterize circulating EVs in young and older individuals, prior to and following a 12‐week resistance exercise programme. Plasma EVs were isolated using size exclusion chromatography and ultracentrifugation. We found that ageing reduced circulating expression markers of CD9, and CD81. Using late‐passage human myotubes as a model for ageing in vitro, we show significantly lower secreted exosome‐like vesicles (ELVs). Further, levels of circulating ELV‐miRNAs associated with muscle health were lower in older individuals at baseline but increased following RET to levels comparable to young. Muscle biopsies show similar age‐related reductions in miRNA expressions, with largely no effect of training. This is reflected in vitro, where aged myotubes show significantly reduced expression of endogenous and secreted muscle‐specific miRNAs (myomiRs). Lastly, proteins associated with ELV and miRNA biogenesis were significantly higher in both older skeletal muscle tissues and aged human myotubes. Together we show that ageing significantly affects ELV and miRNA cargo biogenesis, and release. RET can partially normalize this altered intercellular communication. imageKey points We show that ageing reduces circulating expression of exosome‐like vesicle (ELV) markers, CD9 and CD81. Using late‐passage human skeletal myotubes as a model of ageing, we show that secreted ELV markers are significantly reduced in vitro. We find circulating ELV miRNAs associated with skeletal muscle health are lower in older individuals but can increase following resistance exercise training (RET). In skeletal muscle, we find altered expression of miRNAs in older individuals, with no effect of RET. Late‐passage myotubes also appear to have aberrant production of endogenous myomiRs with lower abundance than youthful counterparts In older skeletal muscle and late‐passage myotubes, proteins involved with ELV‐ and miRNA biogenesis are upregulated

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Section: Methodsmentioning

confidence: 99%

Circulating exosome‐like vesicle and skeletal muscle microRNAs are altered with age and resistance training

Xhuti

Nilsson

Manta

et al. 2023

The Journal of Physiology

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“…Participants underwent resting (Pre) skeletal muscle biopsies from the vastus lateralis of both the AC and CTL legs according to Tarnopolsky et al, (2011) at least 1 week following the last AC bout. Participants then underwent 300 isokinetic, eccentric contractions of the quadriceps muscles at 180 degrees/second using a Biodex dynamometer (Biodex-System 4, Biodex Medical Systems, Shirley, NY, USA) with each leg, a protocol used frequently in our laboratory to elicit skeletal muscle damage (8,(30)(31)(32). Participants returned to the laboratory 24 and 48 hours following eccentric contractions and underwent biopsies from both the CTL and AC legs.…”

Section: Methodsmentioning

confidence: 99%

Aerobic conditioning alters the satellite cell and ribosome response to acute eccentric contractions in young men and women

Brown

Thomas

Hatt

et al. 2022

American Journal of Physiology-Cell Physiology

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Satellite cells (SC) and ribosomes are key determinants of the skeletal muscle adaptive response. Both are thought to increase acutely after resistance exercise and chronically with resistance training. However, the acute SC and ribosome exercise response with prior aerobic conditioning is unknown. Fourteen young men and women underwent 6 weeks of single-legged aerobic conditioning followed by an acute bout of 300 eccentric contractions. Muscle biopsies were taken from the vastus lateralis of the aerobically conditioned (AC) and the control (CTL) legs before (Pre), 24 (24h) and 48 (48h) hours post-contractions. SC pool expansion (PAX7+ cells/100 fibres) was greater in type-I (1.3-fold) and mixed-fibres (1.2-fold) in the AC leg compared to the CTL. Pax7 (1.2-fold) and MyoD1 (1.4-fold) mRNA expression was also greater in the AC leg compared to the CTL. AC had greater RNA concentration (1.2-fold) and mRNA expression of Ubf (1.2-fold) and Tif-1a (1.3-fold) compared to CTL. Only the AC leg increased (Pre-48h) c-Myc (3.0-fold), (Pre-24h) 45S pre-rRNA (2.6-fold), 5.8S ITS (2.1-fold) and 28S ITS (2.0-fold) following eccentric contractions. We discovered that aerobic conditioning augmented type-I SC pool expansion and ribosome content following an acute bout of eccentric contractions.

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“…Animal studies suggest that although muscle growth can occur in satellite cell ablated conditions (2 weeks overload) (McCarthy et al, 2011), satellite cells may be necessary to support more extensive muscle fiber hypertrophy (8 weeks overload) (Fry et al, 2014). Work in humans showing the upregulation of MRFs following resistance exercise (McKay et al, 2008;Nederveen et al, 2019), and positive correlations between muscle growth and increased satellite cell content during prolonged resistance exercise training (Petrella et al, 2006;Verdijk et al, 2010;Bellamy et al, 2014), has contributed to the idea that satellite cells play a role in human muscle fiber hypertrophy (Snijders et al, 2015;Brook et al, 2019). The MuIS (+) phenotype and age-related impairments in satellite cell function may therefore limit hypertrophy of skeletal muscle after an atrophy-inducing event.…”

Section: Variability In Muscle Regenerative Capacitymentioning

confidence: 99%

Divergent Roles of Inflammation in Skeletal Muscle Recovery From Injury

et al. 2020

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A transient increase in local pro-inflammatory cytokine expression following skeletal muscle injury mediates the repair and regeneration of damaged myofibers through myogenesis. Regenerative capacity is diminished and muscle wasting occurs, however, when intramuscular inflammatory signaling is exceedingly high or persists chronically. An excessive and persistent inflammatory response to muscle injury may therefore impair recovery by limiting the repair of damaged tissue and triggering muscle atrophy. The concentration-dependent activation of different downstream signaling pathways by several pro-inflammatory cytokines in cell and animal models support these opposing roles of post-injury inflammation. Understanding these molecular pathways is essential in developing therapeutic strategies to attenuate excessive inflammation and accelerate functional recovery and muscle mass accretion following muscle damage. This is especially relevant given the observation that basal levels of intramuscular inflammation and the inflammatory response to muscle damage are not uniform across all populations, suggesting certain individuals may be more susceptible to an excessive inflammatory response to injury that limits recovery. This narrative review explores the opposing roles of intramuscular inflammation in muscle regeneration and muscle protein turnover. Factors contributing to an exceedingly high inflammatory response to damage and age-related impairments in regenerative capacity are also considered.

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Consistent expression pattern of myogenic regulatory factors in whole muscle and isolated human muscle satellite cells after eccentric contractions in humans

Cited by 16 publications

References 56 publications

Circulating exosome‐like vesicle and skeletal muscle microRNAs are altered with age and resistance training

Circulating exosome‐like vesicle and skeletal muscle microRNAs are altered with age and resistance training

Aerobic conditioning alters the satellite cell and ribosome response to acute eccentric contractions in young men and women

Divergent Roles of Inflammation in Skeletal Muscle Recovery From Injury

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