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Abstract
Optimal repair and adaptation of skeletal muscle is facilitated by resident stem cells (satellite cells). To understand how different exercise modes influence satellite cell dynamics, we measured satellite cell activity in conjunction with markers of muscle damage and inflammation in human skeletal muscle following a single work- and intensity-matched bout of eccentric (ECC) or concentric contractions (CON). Participants completed a single bout of ECC (n = 7) or CON (n = 7) of the knee extensors. A muscle biopsy was obtained before and 24 h after exercise. Functional measures and immunohistochemical analyses were used to determine the extent of muscle damage and indices of satellite cell activity. Cytokine concentrations were measured using a multiplexed magnetic bead assay. Isokinetic peak torque decreased following ECC (p < 0.05) but not CON. Greater histological staining of the damage marker Xin was observed in muscle samples of ECC vs. CON. Tenasin C immunoreactivity increased 15 fold (p < 0.01) following ECC and was unchanged following CON. The inflammatory cytokines interferon gamma-induced protein 10 (IP-10) and monocyte chemotactic protein 1 (MCP-1) increased pre- to post-ECC (4.26 ± 1.4 vs. 10.49 ± 5.8 pg/ml, and 3.06 ± 0.7 vs. 6.25 ± 4.6 pg/ml, respectively; p < 0.05). There was no change in any cytokine post-CON. Satellite cell content increased 27% pre- to post-ECC (0.10 ± 0.031 vs. 0.127 ± 0.041, respectively; p < 0.05). There was no change in satellite cell number in CON (0.099 ± 0.027 vs. 0.102 ± 0.029, respectively). There was no fiber type-specific satellite cell response following either exercise mode. ECC but not CON resulted in an increase in MyoD positive nuclei per myofiber pre- to post-exercise (p < 0.05), but there was no change in MyoD DNA binding activity in either condition. In conclusion, ECC but not CON results in functional and histological evidence of muscle damage that is accompanied by increased satellite cell activity 24 h post-exercise.
Highlights
The unique regenerative and adaptive properties of skeletal muscle are largely under-lied by the action of muscle stem cells called satellite cells
Our primary findings were that a single bout of maximal eccentric (ECC), but not concentric (CON) muscle contractions induced: (1) muscle damage and evidence of extracellular matrix (ECM) de-adhesion, and (2) an acute increase in the activation and quantity of mixed muscle fiber satellite cells 24 h post-exercise
This study confirms the longstanding notion that muscle damage primarily occurs due to ECC, but not CON (Friden et al, 1986; Faulkner et al, 1993), and is, to our knowledge, the first to show that exercise contraction mode influences satellite cell proliferation in human skeletal muscle following a single exercise bout
Summary
The unique regenerative and adaptive properties of skeletal muscle are largely under-lied by the action of muscle stem cells called satellite cells. In response to a sufficient stimulus (i.e., muscle injury or exercise), satellite cells exit their quiescent state (activation), proliferate, migrate to areas of damage, and fuse to the surrounding post-mitotic skeletal muscle (Yin et al, 2013). Studies suggest that optimal repair of injured skeletal muscle is dependent on a healthy and active pool of satellite cells (McCarthy et al, 2011; Murphy et al, 2011). Growth of mechanically overloaded muscle is limited in satellite cell depleted animals (Fry et al, 2014), and it appears that in humans, individuals with a large satellite cell pool have a greater propensity for hypertrophic adaptations following exercise (Petrella et al, 2008). Investigations of the mechanisms that underlie satellite cell responsiveness to exercise are important
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