Cited by 61Muscle Physiology and DisordersChronic Obstructive Pulmonary Disease (COPD) ResearchMeat and Animal Product Quality

Reduced myotube diameter, atrophic signalling and elevated oxidative stress in cultured satellite cells from COPD patients

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Pomiès, Pascal, Rodriguez, Julie, Blaquière, Marine, Sedraoui, Sami, Gouzi, Fares, Carnac, Gilles, Laoudj‐Chenivesse, Dalila, Mercier, Jacques +2 more·2015·Journal of Cellular and Molecular Medicine

Abstract

The mechanisms leading to skeletal limb muscle dysfunction in chronic obstructive pulmonary disease ( COPD ) have not been fully elucidated. Exhausted muscle regenerative capacity of satellite cells has been evocated, but the capacity of satellite cells to proliferate and differentiate properly remains unknown. Our objectives were to compare the characteristics of satellite cells derived from COPD patients and healthy individuals, in terms of proliferative and differentiation capacities, morphological phenotype and atrophy/hypertrophy signalling, and oxidative stress status. Therefore, we purified and cultivated satellite cells from progressively frozen vastus lateralis biopsies of eight COPD patients and eight healthy individuals. We examined proliferation parameters, differentiation capacities, myotube diameter, expression of atrophy/hypertrophy markers, oxidative stress damages, antioxidant enzyme expression and cell susceptibility to H 2 O 2 in cultured myoblasts and/or myotubes. Proliferation characteristics and commitment to terminal differentiation were similar in COPD patients and healthy individuals, despite impaired fusion capacities of COPD myotubes. Myotube diameter was smaller in COPD patients ( P = 0.015), and was associated with a higher expression of myostatin (myoblasts: P = 0.083; myotubes: P = 0.050) and atrogin‐1 (myoblasts: P = 0.050), and a decreased phospho‐ AKT / AKT ratio (myoblasts: P = 0.022). Protein carbonylation (myoblasts: P = 0.028; myotubes: P = 0.002) and lipid peroxidation (myotubes: P = 0.065) were higher in COPD cells, and COPD myoblasts were significantly more susceptible to oxidative stress. Thus, cultured satellite cells from COPD patients display characteristics of morphology, atrophic signalling and oxidative stress similar to those described in in vivo COPD skeletal limb muscles. We have therefore demonstrated that muscle alteration in COPD can be studied by classical in vitro cellular models.

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  • Increased Mn-superoxide dismutase (SOD) and Cu-Zn-SOD protein levels have been demonstrated in COPD quadriceps, whereas unchanged SOD content and decreased SOD activity have been reported in another study, and unchanged MnSOD, Cu/ZnSOD, and catalase expressions have been found in cultured COPD myoblasts and myotubes.

    “For example, increased Mn-superoxide dismutase (SOD) and Cu-Zn-SOD protein levels have been demonstrated in the quadriceps [118,127], whereas unchanged SOD content and decreased SOD activity have been reported in another study [122], and unchanged MnSOD, Cu/ZnSOD, and catalase expressions in cultured COPD myoblasts and myotubes have been found [128].”

    From Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting (2023) · cites this paper as [128]

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  • Several studies have found increased lipofuscin accumulation in COPD quadriceps and higher levels of 4-HNE in quadriceps tissue, as well as in cultured myotubes from COPD patients.

    “For example, several studies have found an increased lipofuscin accumulation in COPD quadriceps [126] and higher levels of hydroxy-2-nonenal (4-HNE) in quadriceps tissue [87,127], as well as in cultured myotubes from COPD patients [128].”

    From Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting (2023) · cites this paper as [128]

    The Results section reports higher measured 4-HNE levels in cultured myotubes from COPD patients than in controls, which supports the portion attributed to this paper. It describes the difference as a tendency (P = 0.065), however, so the unqualified claim of higher levels overstates the evidence. The lipofuscin and quadriceps-tissue claims have other citations. (LLM, conf=0.87)

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  • Glutathione peroxidase 1 is increased in cultured COPD myoblasts.

    “Of note, we have shown an increase in glutathione peroxidase 1 in cultured COPD myoblasts [128].”

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  1. [1]Gosselink R Troosters T Decramer M Peripheral muscle weakness contributes to exercise limitation in COPD Am J Respir Crit Care Med 1996 153 976 80 8630582
  2. [2]Marquis K Debigare R Lacasse Y Midthigh muscle cross-sectional area is a better predictor of mortality than body mass index in patients with chronic obstructive pulmonary disease Am J Respir Crit Care Med 2002 166 809 13 12231489
  3. [3]Swallow EB Reyes D Hopkinson NS Quadriceps strength predicts mortality in patients with moderate to severe chronic obstructive pulmonary disease Thorax 2007 62 115 20 17090575 PMC2111256
  4. [4]Barreiro E Gea J Corominas JM Nitric oxide synthases and protein oxidation in the quadriceps femoris of patients with chronic obstructive pulmonary disease Am J Respir Cell Mol Biol 2003 29 771 8 12816735
  5. [5]Barreiro E Rabinovich R Marin-Corral J Chronic endurance exercise induces quadriceps nitrosative stress in patients with severe COPD Thorax 2009 64 13 9 18835959
  6. [6]Barreiro E Schols AM Polkey MI Cytokine profile in quadriceps muscles of patients with severe COPD Thorax 2008 63 100 7 17875568
  7. [7]Couillard A Maltais F Saey D Exercise-induced quadriceps oxidative stress and peripheral muscle dysfunction in patients with chronic obstructive pulmonary disease Am J Respir Crit Care Med 2003 167 1664 9 12672647
  8. [8]Fermoselle C Rabinovich R Ausin P Does oxidative stress modulate limb muscle atrophy in severe COPD patients? Eur Respir J 2012 40 851 62 22408199
  9. [9]Koechlin C Couillard A Simar D Does oxidative stress alter quadriceps endurance in chronic obstructive pulmonary disease? Am J Respir Crit Care Med 2004 169 1022 7 15001462
  10. [10]Hansen MJ Gualano RC Bozinovski S Therapeutic prospects to treat skeletal muscle wasting in COPD (chronic obstructive lung disease) Pharmacol Ther 2006 109 162 72 16154635
  11. [11]Theriault ME Pare ME Maltais F Satellite cells senescence in limb muscle of severe patients with COPD PLoS ONE 2012 7 e39124 22720047 PMC3374758
  12. [12]Wang YX Rudnicki MA Satellite cells, the engines of muscle repair Nat Rev Mol Cell Biol 2012 13 127 33 22186952
  13. [13]Eliason G Abdel-Halim S Arvidsson B Physical performance and muscular characteristics in different stages of COPD Scand J Med Sci Sports 2009 19 865 70 18980606
  14. [14]Menon MK Houchen L Singh SJ Inflammatory and satellite cells in the quadriceps of patients with COPD and the response to resistance training Chest 2012 142 1134 42 22459782
  15. [15]Barro M Carnac G Flavier S Myoblasts from affected and non-affected FSHD muscles exhibit morphological differentiation defects J Cell Mol Med 2010 14 275 89 18505476 PMC2910739
  16. [16]Winokur ST Barrett K Martin JH Facioscapulohumeral muscular dystrophy (FSHD) myoblasts demonstrate increased susceptibility to oxidative stress Neuromuscul Disord 2003 13 322 33 12868502
  17. [17]Gaster M Petersen I Hojlund K The diabetic phenotype is conserved in myotubes established from diabetic subjects: evidence for primary defects in glucose transport and glycogen synthase activity Diabetes 2002 51 921 7 11916908
  18. [18]Jackson S Bagstaff SM Lynn S Decreased insulin responsiveness of glucose uptake in cultured human skeletal muscle cells from insulin-resistant nondiabetic relatives of type 2 diabetic families Diabetes 2000 49 1169 77 10909975
  19. [19]Rabe KF Hurd S Anzueto A Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary Am J Respir Crit Care Med 2007 176 532 55 17507545
  20. [20]Hayot M Michaud A Koechlin C Skeletal muscle microbiopsy: a validation study of a minimally invasive technique Eur Respir J 2005 25 431 40 15738285
  21. [21]Kitzmann M Bonnieu A Duret C Inhibition of Notch signaling induces myotube hypertrophy by recruiting a subpopulation of reserve cells J Cell Physiol 2006 208 538 48 16741964
  22. [22]Celli BR Cote CG Marin JM The body-mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease N Engl J Med 2004 350 1005 12 14999112
  23. [23]Gaster M Kristensen SR Beck-Nielsen H A cellular model system of differentiated human myotubes APMIS 2001 109 735 44 11900052
  24. [24]Carlson ME Suetta C Conboy MJ Molecular aging and rejuvenation of human muscle stem cells EMBO Mol Med 2009 1 381 91 20049743 PMC2875071
  25. [25]Aguer C Mercier J Kitzmann M Lipid content and response to insulin are not invariably linked in human muscle cells Mol Cell Endocrinol 2010 315 225 32 19897010
  26. [26]Minet AD Gaster M ATP synthesis is impaired in isolated mitochondria from myotubes established from type 2 diabetic subjects Biochem Biophys Res Commun 2010 402 70 4 20920472
  27. [27]Gosker HR Kubat B Schaart G Myopathological features in skeletal muscle of patients with chronic obstructive pulmonary disease Eur Respir J 2003 22 280 5 12952261
  28. [28]Bernard S LeBlanc P Whittom F Peripheral muscle weakness in patients with chronic obstructive pulmonary disease Am J Respir Crit Care Med 1998 158 629 34 9700144
  29. [29]Morissette MR Cook SA Buranasombati C Myostatin inhibits IGF-I-induced myotube hypertrophy through Akt Am J Physiol Cell Physiol 2009 297 C1124 32 19759331 PMC2777401
  30. [30]Lokireddy S Mouly V Butler-Browne G Myostatin promotes the wasting of human myoblast cultures through promoting ubiquitin-proteasome pathway-mediated loss of sarcomeric proteins Am J Physiol Cell Physiol 2011 301 C1316 24 21900687
  31. [31]Constantin D Menon MK Houchen-Wolloff L Skeletal muscle molecular responses to resistance training and dietary supplementation in COPD Thorax 2013 68 625 33 23535211
  32. [32]Doucet M Russell AP Leger B Muscle atrophy and hypertrophy signaling in patients with chronic obstructive pulmonary disease Am J Respir Crit Care Med 2007 176 261 9 17478621
  33. [33]Plant PJ Brooks D Faughnan M Cellular markers of muscle atrophy in chronic obstructive pulmonary disease Am J Respir Cell Mol Biol 2010 42 461 71 19520920
  34. [34]Pillai SG Ge D Zhu G A genome-wide association study in chronic obstructive pulmonary disease (COPD): identification of two major susceptibility loci PLoS Genet 2009 5 e1000421 19300482 PMC2650282
  35. [35]Soler Artigas M Wain LV Repapi E Effect of five genetic variants associated with lung function on the risk of chronic obstructive lung disease, and their joint effects on lung function Am J Respir Crit Care Med 2011 184 786 95 21965014 PMC3398416
  36. [36]Sorheim IC DeMeo DL Washko G Polymorphisms in the superoxide dismutase-3 gene are associated with emphysema in COPD COPD 2010 7 262 8 20673035 PMC2923920
  37. [37]Puente-Maestu L Perez-Parra J Godoy R Abnormal mitochondrial function in locomotor and respiratory muscles of COPD patients Eur Respir J 2009 33 1045 52 19129279
  38. [38]Puente-Maestu L Lazaro A Tejedor A Effects of exercise on mitochondrial DNA content in skeletal muscle of patients with COPD Thorax 2011 66 121 7 21097816
  39. [39]He J Xu Q Jing Y Reactive oxygen species regulate ERBB2 and ERBB3 expression via miR-199a/125b and DNA methylation EMBO Rep 2012 13 1116 22 23146892 PMC3512405
  40. [40]Kang KA Zhang R Kim GY Epigenetic changes induced by oxidative stress in colorectal cancer cells: methylation of tumor suppressor RUNX3 Tumour Biol 2012 33 403 12 22274925

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Authors
Pomiès, P., Rodriguez, J., Blaquière, M., Sedraoui, S., Gouzi, F., Carnac, G., Laoudj‐Chenivesse, D., Mercier, J., Préfaut, C., & Hayot, M.
Affiliations
  • Inserm (FR)
  • INSERM U‐1046 University Montpellier I University Montpellier II Montpellier France
Corresponding author
Pomiès, Pascal
Venue
Journal of Cellular and Molecular Medicine
Publisher
Wiley
Published
2014-10-22
Volume
19
Issue
1
Pages
175-186
ISSN
  • 1582-1838 (ISSN-L)
  • 1582-4934
OpenAlex
W1988850834
Cited by
61
References
0
Citations by year
2026: 5 · 2025: 2 · 2024: 5 · 2023: 5 · 2022: 6 · 2021: 7 · 2020: 6 · 2019: 5 · 2018: 8 · 2017: 4 · 2016: 6 · 2015: 2
FWCI
1.64
Type
journal article
Language
en
Open access
Locations
  • Journal of Cellular and Molecular Medicine (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
  • Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Chronic Obstructive Pulmonary Disease (COPD) Research
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Meat and Animal Product Quality
Keywords
chronic obstructive pulmonary disease, satellite cells, skeletal muscle atrophy, myotube diameter, oxidative stress, myostatin, atrogin-1, Akt signaling, protein carbonylation, lipid peroxidation, myoblast fusion, muscle regeneration, vastus lateralis
MeSH terms
Aged, Cell Differentiation, Cell Fusion, Cells, Cultured, Female, Humans, Hydrogen Peroxide, Male, Middle Aged, Muscle Proteins, Muscular Atrophy, RNA, Messenger, Protein Biosynthesis, Lipid Peroxidation, Signal Transduction, Biomarkers, Case-Control Studies, Oxidative Stress, Muscle Fibers, Skeletal, Pulmonary Disease, Chronic Obstructive, Myoblasts, Satellite Cells, Skeletal Muscle, Cell Size, Cell Proliferation, Protein Carbonylation

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