Regulation of myogenesis and skeletal muscle regeneration: effects of oxygen levels on satellite cell activity

Chaillou, Thomas; Lanner, Johanna T.

doi:10.1096/fj.201600757r

Cited by 66 publications

(67 citation statements)

References 84 publications

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“…MyoD remains expressed at early stages of differentiation and myogenin, followed by Mrf4 at a later stage (40). In vitro, low oxygen levels (3-6%) seem to favor myoblast proliferation, whereas very low oxygen levels (,1%) tend to alter myogenic differentiation and myotube formation (41). Murine myoblasts cultured in a severe hypoxic environment (1% O 2 ) have been shown to upregulate the expression of genes related to cell cycle and metabolic processes and to down-regulate the expression of genes associated with catabolic processes and muscle development (42).…”

Section: Discussionmentioning

confidence: 99%

Environmental hypoxia favors myoblast differentiation and fast phenotype but blunts activation of protein synthesis after resistance exercise in human skeletal muscle

et al. 2018

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We hypothesized that a single session of resistance exercise performed in moderate hypoxic (FiO: 14%) environmental conditions would potentiate the anabolic response during the recovery period spent in normoxia. Twenty subjects performed a 1-leg knee extension session in normoxic or hypoxic conditions. Muscle biopsies were taken 15 min and 4 h after exercise in the vastus lateralis of the exercised and the nonexercised legs. Blood and saliva samples were taken at regular intervals before, during, and after the exercise session. The muscle fractional-protein synthetic rate was determined by deuterium incorporation into proteins, and the protein-degradation rate was determined by methylhistidine release from skeletal muscle. We found that: 1) hypoxia blunted the activation of protein synthesis after resistance exercise; 2) hypoxia down-regulated the transcriptional program of autophagy; 3) hypoxia regulated the expression of genes involved in glucose metabolism at rest and the genes involved in myoblast differentiation and fusion and in muscle contraction machinery after exercise; and 4) the hypoxia-inducible factor-1α pathway was not activated at the time points studied. Contrary to our hypothesis, environmental hypoxia did not potentiate the short-term anabolic response after resistance exercise, but it initiated transcriptional regulations that could potentially translate into satellite cell incorporation and higher force production in the long term.-Gnimassou, O., Fernández-Verdejo, R., Brook, M., Naslain, D., Balan, E., Sayda, M., Cegielski, J., Nielens, H., Decottignies, A., Demoulin, J.-B., Smith, K., Atherton, P. J., Fancaux, M., Deldicque, L. Environmental hypoxia favors myoblast differentiation and fast phenotype but blunts activation of protein synthesis after resistance exercise in human skeletal muscle.

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Section: Discussionmentioning

confidence: 99%

Environmental hypoxia favors myoblast differentiation and fast phenotype but blunts activation of protein synthesis after resistance exercise in human skeletal muscle

et al. 2018

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“…22 Exercise increased cyclin D1, myogenin, and MRF4 mRNA levels only in the hypoxic group. 23 On the one hand, severe hypoxia (≤1%O 2 ) seems to inhibit mouse and human myoblast differentiation. 23 On the one hand, severe hypoxia (≤1%O 2 ) seems to inhibit mouse and human myoblast differentiation.…”

Section: Acute Hypoxia Fosters Myogenesis In Response To Resistancementioning

confidence: 99%

“…23 In addition, the role of hypoxia-inducible factor-1 alpha (HIF-1α) in those events is still unclear. 23 In addition, the role of hypoxia-inducible factor-1 alpha (HIF-1α) in those events is still unclear.…”

Section: Introductionmentioning

confidence: 99%

Acute environmental hypoxia potentiates satellite cell‐dependent myogenesis in response to resistance exercise through the inflammation pathway in human

et al. 2019

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Abbreviations: ADAMTS5, ADAM metallopeptidase with thrombospondin type 1 motif 5; BHLHE40, basic helix-loop-helix family member E40; CTGF, connective tissue growth factor; Cyr61, cysteine-rich angiogenic inducer 61; FiO 2 , fraction of inspired oxygen; GM-CSF, granulocyte macrophage colony stimulating factor; Gulp1, GULP PTB domain containing engulfment adaptor 1; HIF-1, hypoxia-inducible factor-1; IFNγ, interferon gamma; IGF, insulin-like growth factor; Il, interleukin; IKzf2, IKAROS family zinc finger 2; MRF, myogenic regulatory factors; Myf5, myogenic factor 5; MyoD, myogenic differentiation; NF-κB, nuclear factor kappa B; Pax7, paired box 7; Pmp22, peripheral myelin protein 22; STAT3, signal transducer and activator of transcription 3; TAZ, Taffazin; TNFα, tumor necrosis factor alpha; YAP, yes associated protein. AbstractAcute environmental hypoxia may potentiate muscle hypertrophy in response to resistance training but the mechanisms are still unknown. To this end, twenty subjects performed a 1-leg knee extension session (8 sets of 8 repetitions at 80% 1 repetition maximum, 2-min rest between sets) in normoxic or normobaric hypoxic conditions (FiO2 14%). Muscle biopsies were taken 15 min and 4 hours after exercise in the vastus lateralis of the exercised and the non-exercised legs. Blood samples were taken immediately, 2h and 4h after exercise. In vivo, hypoxic exercise fostered acute inflammation mediated by the TNFα/NF-κB/IL-6/STAT3 (+333%, +194%, + 163% and +50% respectively) pathway, which has been shown to contribute to satellite cells myogenesis. Inflammation activation was followed by skeletal muscle invasion by CD68 (+63%) and CD197 (+152%) positive immune cells, both known to regulate muscle regeneration. The role of hypoxia-induced activation of inflammation in myogenesis was confirmed in vitro. Acute hypoxia promoted myogenesis through increased Myf5 (+300%), MyoD (+88%), myogenin (+1816%) and MRF4 (+489%) mRNA levels in primary myotubes and this response was blunted by siRNA targeting STAT3. In conclusion, our results suggest that hypoxia could improve muscle hypertrophic response following resistance exercise through IL-6/STAT3-dependent myogenesis and immune cells-dependent muscle regeneration. K E Y W O R D Sexercise, hypoxia, inflammation, muscle, myogenesis 1886 | BRITTO eT al.

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“…[17]. In a recent review, the authors discuss the fact that O 2 levels actually controls myogenesis and muscle regeneration, showing that hypoxia (3–6% O 2 levels) could in fact promote myogenesis, while anoxia (oxygen levels below 1% O 2 ) appears damaging to cell differentiation [18]. To achieve anoxic conditions, an enzymatic oxygen scavenger (EC-Oxyrase) was added to differentiated muscle cells.…”

Section: Resultsmentioning

confidence: 99%

Primary bovine skeletal muscle cells enters apoptosis rapidly via the intrinsic pathway when available oxygen is removed

et al. 2017

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Muscle cells undergo changes post-mortem during the process of converting muscle into meat, and this complex process is far from revealed. Recent reports have suggested programmed cell death (apoptosis) to be important in the very early period of converting muscle into meat. The dynamic balance that occurs between anti-apoptotic members, such as Bcl-2, and pro-apoptotic members (Bid, Bim) helps determine whether the cell initiates apoptosis. In this study, we used primary bovine skeletal muscle cells, cultured in monolayers in vitro, to investigate if apoptosis is induced when oxygen is removed from the growth medium. Primary bovine muscle cells were differentiated to form myotubes, and anoxia was induced for 6h. The anoxic conditions significantly increased (P<0.05) the relative gene expression of anti- and pro-apoptotic markers (Aif, Bcl-2, Bid and Bim), and the PARK7 (P<0.05) and Grp75 (Hsp70) protein expressions were transiently increased. The anoxic conditions also led to a loss of mitochondrial membrane potential, which is an early apoptotic event, as well as cytochrome c release from the mitochondria. Finally, reorganization and degradation of cytoskeletal filaments occurred. These results suggest that muscle cells enters apoptosis via the intrinsic pathway rapidly when available oxygen in the muscle diminishes post-mortem.

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Regulation of myogenesis and skeletal muscle regeneration: effects of oxygen levels on satellite cell activity

Cited by 66 publications

References 84 publications

Environmental hypoxia favors myoblast differentiation and fast phenotype but blunts activation of protein synthesis after resistance exercise in human skeletal muscle

Environmental hypoxia favors myoblast differentiation and fast phenotype but blunts activation of protein synthesis after resistance exercise in human skeletal muscle

Acute environmental hypoxia potentiates satellite cell‐dependent myogenesis in response to resistance exercise through the inflammation pathway in human

Primary bovine skeletal muscle cells enters apoptosis rapidly via the intrinsic pathway when available oxygen is removed

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