Cited by 9Muscle Physiology and DisordersChronic Obstructive Pulmonary Disease (COPD) ResearchMuscle metabolism and nutrition

Response to Electrostimulation Is Impaired in Muscle Cells from Patients with Chronic Obstructive Pulmonary Disease

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Catteau, Matthias, Passerieux, Emilie, Blervaque, Léo, Gouzi, Farés, Ayoub, Bronia, Hayot, Maurice, Pomiès, Pascal·2021·Cells

Abstract

Among the comorbidities associated with chronic obstructive pulmonary disease (COPD), skeletal muscle weakness and atrophy are known to affect patient survival rate. In addition to muscle deconditioning, various systemic and intrinsic factors have been implicated in COPD muscle dysfunction but an impaired COPD muscle adaptation to contraction has never been extensively studied. We submitted cultured myotubes from nine healthy subjects and nine patients with COPD to an endurance-type protocol of electrical pulse stimulation (EPS). EPS induced a decrease in the diameter, covered surface and expression of MHC1 in COPD myotubes. Although the expression of protein degradation markers was not affected, expression of the protein synthesis marker mTOR was not induced in COPD compared to healthy myotubes after EPS. The expression of the differentiation markers p16INK4a and p21 was impaired, while expression of Myf5 and MyoD tended to be affected in COPD muscle cells in response to EPS. The expression of mitochondrial biogenesis markers PGC1α and MFN2 was affected and expression of TFAM and COX1 tended to be reduced in COPD compared to healthy myotubes upon EPS. Lipid peroxidation was increased and the expression of the antioxidant enzymes SOD2 and GPx4 was affected in COPD compared to healthy myotubes in response to EPS. Thus, we provide evidence of an impaired response of COPD muscle cells to contraction, which might be involved in the muscle weakness observed in patients with COPD.

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  • In vitro, mitochondrial biogenesis markers PGC1α (and to a lesser extent TFAM and COX1) and MFN2 have been shown to be reduced in cultured myotubes from COPD patients compared to healthy subjects upon electrical stimulation.

    “mitochondrial biogenesis markers PGC1α (and to a lesser extent TFAM and COX1) and MFN2 have been shown to be reduced in cultured myotubes from COPD patients compared to healthy subjects upon electrical stimulation [92].”

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  1. [1]Mostert R. Goris A. Weling-Scheepers C. Wouters E. Schols A. Tissue depletion and health related quality of life in patients with chronic obstructive pulmonary disease Respir. Med. 2000 94 859 867 10.1053/rmed.2000.0829 11001077 · DOI
  2. [2]Swallow E.B. Reyes D. Hopkinson N. Man W.D.-C. Porcher R. Cetti E.J. Moore A.J. Moxham J. Polkey M.I. Quadriceps strength predicts mortality in patients with moderate to severe chronic obstructive pulmonary disease Thorax 2007 62 115 120 10.1136/thx.2006.062026 17090575 PMC2111256 · DOI · Paper page
  3. [3]Agustí A. Edwards L.D. Rennard S.I. MacNee W. Tal-Singer R. Miller B.E. Vestbo J. Lomas D.A. Calverley P.M.A. Wouters E. Persistent Systemic Inflammation is Associated with Poor Clinical Outcomes in COPD: A Novel Phenotype PLoS ONE 2012 7 e37483 10.1371/journal.pone.0037483 22624038 PMC3356313 · DOI
  4. [4]Couillard A. Maltais F. Saey D. Debigaré R. Michaud A. Koechlin C. LeBlanc P. Préfaut C. 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 1669 10.1164/rccm.200209-1028OC 12672647 · DOI
  5. [5]Blervaque L. Passerieux E. Pomiès P. Catteau M. Héraud N. Blaquière M. Bughin F. Ayoub B. Molinari N. Cristol J.-P. Impaired training-induced angiogenesis process with loss of pericyte-endothelium interactions is associated with an abnormal capillary remodelling in the skeletal muscle of COPD patients Respir. Res. 2019 20 278 10.1186/s12931-019-1240-6 31806021 PMC6896673 · DOI
  6. [6]Alexandre F. Héraud N. Tremey E. Oliver N. Bourgouin D. Varray A. Specific motor cortex hypoexcitability and hypoactivation in COPD patients with peripheral muscle weakness BMC Pulm. Med. 2020 20 1 10.1186/s12890-019-1042-0 31900129 PMC6942311 · DOI
  7. [7]Gundersen K. Excitation-transcription coupling in skeletal muscle: The molecular pathways of exercise Biol. Rev. 2010 86 564 600 10.1111/j.1469-185X.2010.00161.x 21040371 PMC3170710 · DOI
  8. [8]Ge Y. Chen J. Mammalian Target of Rapamycin (mTOR) Signaling Network in Skeletal Myogenesis J. Biol. Chem. 2012 287 43928 43935 10.1074/jbc.R112.406942 23115234 PMC3527976 · DOI
  9. [9]Zanou B.N. Gailly P. Skeletal muscle hypertrophy and regeneration: Interplay between the myogenic regulatory factors (MRFs) and insulin-like growth factors (IGFs) pathways Cell. Mol. Life Sci. 2013 70 4117 4130 10.1007/s00018-013-1330-4 23552962 PMC11113627 · DOI
  10. [10]Casuso R.A. Huertas J.R. The emerging role of skeletal muscle mitochondrial dynamics in exercise and ageing Ageing Res. Rev. 2020 58 101025 10.1016/j.arr.2020.101025 32018055 · DOI
  11. [11]Vargas-Mendoza N. Morales-González Á. Madrigal-Santillán E.O. Madrigal-Bujaidar E. Álvarez-González I. García-Melo L.F. Anguiano-Robledo L. Fregoso-Aguilar T. Morales-Gonzalez J.A. Antioxidant and Adaptative Response Mediated by Nrf2 during Physical Exercise Antioxidants 2019 8 196 10.3390/antiox8060196 PMC6617290 31242588 · DOI
  12. [12]Nikolić N. Bakke S.S. Kase E.T. Rudberg I. Halle I.F. Rustan A.C. Thoresen G.H. Aas V. Electrical Pulse Stimulation of Cultured Human Skeletal Muscle Cells as an In Vitro Model of Exercise PLoS ONE 2012 7 e33203 10.1371/journal.pone.0033203 22457744 PMC3310863 · DOI
  13. [13]Burch N. Arnold A.-S. Item F. Summermatter S. Santos G.B.S. Christe M. Boutellier U. Toigo M. Handschin C. Electric Pulse Stimulation of Cultured Murine Muscle Cells Reproduces Gene Expression Changes of Trained Mouse Muscle PLoS ONE 2010 5 e10970 10.1371/journal.pone.0010970 20532042 PMC2881042 · DOI
  14. [14]Christensen C.S. Christensen D.P. Lundh M. Dahllöf M.S. Haase T.N. Velasquez J.M. Laye M.J. Mandrup-Poulsen T. Solomon T.P.J. Skeletal Muscle to Pancreatic β-Cell Cross-talk: The Effect of Humoral Mediators Liberated by Muscle Contraction and Acute Exercise on β-Cell Apoptosis J. Clin. Endocrinol. Metab. 2015 100 E1289 E1298 10.1210/jc.2014-4506 26218753 · DOI
  15. [15]Scheler M. Irmler M. Lehr S. Hartwig S. Staiger H. Al-Hasani H. Beckers J. de Angelis M.H. Häring H.-U. Weigert C. Cytokine response of primary human myotubes in an in vitro exercise model Am. J. Physiol. Physiol. 2013 305 C877 C886 10.1152/ajpcell.00043.2013 23926130 · DOI · Paper page
  16. [16]Tarum J. Folkesson M. Atherton P.J. Kadi F. Electrical pulse stimulation: Anin vitroexercise model for the induction of human skeletal muscle cell hypertrophy. A proof-of-concept study Exp. Physiol. 2017 102 1405 1413 10.1113/EP086581 28861930 · DOI
  17. [17]Gouzi F. Blaquière M. Catteau M. Bughin F. Maury J. Passerieux E. Ayoub B. Mercier J. Hayot M. Pomiès P. Oxidative stress regulates autophagy in cultured muscle cells of patients with chronic obstructive pulmonary disease J. Cell. Physiol. 2018 233 9629 9639 10.1002/jcp.26868 29943813 · DOI · Paper page
  18. [18]Pomiès P. Rodriguez J. Blaquière M. Sedraoui S. Gouzi F. Carnac G. Laoudj-Chenivesse D. Mercier J. Préfaut C. Hayot M. Reduced myotube diameter, atrophic signalling and elevated oxidative stress in cultured satellite cells from COPD patients J. Cell. Mol. Med. 2014 19 175 186 10.1111/jcmm.12390 25339614 PMC4288361 · DOI · Paper page
  19. [19]Pomiès P. Blaquière M. Maury J. Mercier J. Gouzi F. Hayot M. Involvement of the FoxO1/MuRF1/Atrogin-1 Signaling Pathway in the Oxidative Stress-Induced Atrophy of Cultured Chronic Obstructive Pulmonary Disease Myotubes PLoS ONE 2016 11 e0160092 10.1371/journal.pone.0160092 27526027 PMC4987766 · DOI · Paper page
  20. [20]Maury J. Gouzi F. De Rigal P. Heraud N. Pincemail J. Molinari N. Pomiès P. Laoudj-Chenivesse D. Mercier J. Prefaut C. Heterogeneity of Systemic Oxidative Stress Profiles in COPD: A Potential Role of Gender Oxidative Med. Cell. Longev. 2015 2015 201843 10.1155/2015/201843 26167238 PMC4488160 · DOI
  21. [21]Blervaque L. Pomiès P. Rossi E. Catteau M. Blandinières A. Passerieux E. Blaquière M. Ayoub B. Molinari N. Mercier J. COPD is deleterious for pericytes: Implications during training-induced angiogenesis in skeletal muscle Am. J. Physiol. Circ. Physiol. 2020 319 H1142 H1151 10.1152/ajpheart.00306.2020 32986960 · DOI
  22. [22]ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories ATS Statement Am. J. Respir. Crit. Care Med. 2002 166 111 117 10.1164/ajrccm.166.1.at1102 12091180 · DOI · Paper page
  23. [23]Koechlin C. Couillard A. Simar D. Cristol J.P. Bellet H. Hayot M. Prefaut C. Does Oxidative Stress Alter Quadriceps Endurance in Chronic Obstructive Pulmonary Disease? Am. J. Respir. Crit. Care Med. 2004 169 1022 1027 10.1164/rccm.200310-1465OC 15001462 · DOI
  24. [24]Hayot M. Michaud A. Koechlin C. Caron M.-A. Leblanc P. Prefaut C. Maltais F. Skeletal muscle microbiopsy: A validation study of a minimally invasive technique Eur. Respir. J. 2005 25 431 440 10.1183/09031936.05.00053404 15738285 · DOI
  25. [25]Catteau M. Gouzi F. Blervaque L. Passerieux E. Blaquière M. Ayoub B. Bughin F. Mercier J. Hayot M. Pomiès P. Effects of a human microenvironment on the differentiation of human myoblasts Biochem. Biophys. Res. Commun. 2020 525 968 973 10.1016/j.bbrc.2020.03.020 32173533 · DOI
  26. [26]Hawke T.J. Meeson A.P. Jiang N. Graham S. Hutcheson K. DiMaio J.M. Garry D.J. p21 is essential for normal myogenic progenitor cell function in regenerating skeletal muscle Am. J. Physiol. Physiol. 2003 285 C1019 C1027 10.1152/ajpcell.00055.2003 12826599 · DOI
  27. [27]Urashima M. Teoh G. Akiyama M. Yuza Y. Anderson K.C. Maekawa K. Restoration of p16INK4A protein induces myogenic differentiation in RD rhabdomyosarcoma cells Br. J. Cancer 1999 79 1032 1036 10.1038/sj.bjc.6690165 10098732 PMC2362237 · DOI
  28. [28]Nikolić N. Görgens S.W. Thoresen G.H. Aas V. Eckel J. Eckardt K. Electrical pulse stimulation of cultured skeletal muscle cells as a model forin vitroexercise - possibilities and limitations Acta Physiol. 2016 220 310 331 10.1111/apha.12830 27863008 · DOI
  29. [29]Lambernd S. Taube A. Schober A. Platzbecker B. Görgens S.W. Schlich R. Jeruschke K. Weiss J. Eckardt K. Eckel J. Contractile activity of human skeletal muscle cells prevents insulin resistance by inhibiting pro-inflammatory signalling pathways Diabetologia 2012 55 1128 1139 10.1007/s00125-012-2454-z 22282161 · DOI
  30. [30]Son Y.H. Lee S.-M. Lee S.H. Yoon J.H. Kang J.S. Yang Y.R. Kwon K.-S. Comparative molecular analysis of endurance exercise in vivo with electrically stimulated in vitro myotube contraction J. Appl. Physiol. 2019 127 1742 1753 10.1152/japplphysiol.00091.2019 31622160 · DOI
  31. [31]Fujita H. Nedachi T. Kanzaki M. Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes Exp. Cell Res. 2007 313 1853 1865 10.1016/j.yexcr.2007.03.002 17425954 · DOI
  32. [32]Zhang P. Liang X. Shan T. Jiang Q. Deng C. Zheng R. Kuang S. mTOR is necessary for proper satellite cell activity and skeletal muscle regeneration Biochem. Biophys. Res. Commun. 2015 463 102 108 10.1016/j.bbrc.2015.05.032 25998386 PMC4484853 · DOI · Paper page
  33. [34]Yan Z. Exercise, PGC-1α, and metabolic adaptation in skeletal muscle. This paper article is one of a selection of papers published in this Special Issue, entitled 14th International Biochemistry of Exercise Conference—Muscles as Molecular and Metabolic Machines, and has undergone the Journal’s usual peer review process Appl. Physiol. Nutr. Metab. 2009 34 424 427 10.1139/h09-030 19448709 PMC3354917 · DOI
  34. [36]Whittom F. Jobin J. Simard P.M. Leblanc P. Simard C. Bernard S. Belleau R. Maltais F. Histochemical and morphological characteristics of the vastus lateralis muscle in patients with chronic obstructive pulmonary disease Med. Sci. Sports Exerc. 1998 30 1467 1474 10.1097/00005768-199810000-00001 9789845 · DOI · Paper page
  35. [37]Gouzi F. Préfaut C. Abdellaoui A. Roudier E. De Rigal P. Molinari N. Laoudj-Chenivesse D. Mercier J. Birot O. Hayot M. Blunted muscle angiogenic training-response in COPD patientsversussedentary controls Eur. Respir. J. 2012 41 806 814 10.1183/09031936.00053512 22790908 · DOI
  36. [38]Gifford J.R. Trinity J.D. Kwon O.-S. Layec G. Garten R.S. Park S.-Y. Nelson A.D. Richardson R.S. Altered skeletal muscle mitochondrial phenotype in COPD: Disease vs. disuse J. Appl. Physiol. 2018 124 1045 1053 10.1152/japplphysiol.00788.2017 29357496 PMC5972462 · DOI
  37. [39]Cole-Ezea P. Swan D. Shanley D. Hesketh J. Glutathione peroxidase 4 has a major role in protecting mitochondria from oxidative damage and maintaining oxidative phosphorylation complexes in gut epithelial cells Free. Radic. Biol. Med. 2012 53 488 497 10.1016/j.freeradbiomed.2012.05.029 22634395 · DOI
  38. [40]Lustgarten M.S. Jang Y.C. Liu Y. Muller F.L. Qi W. Steinhelper M. Brooks S.V. Larkin L. Shimizu T. Shirasawa T. Conditional knockout of Mn-SOD targeted to type IIB skeletal muscle fibers increases oxidative stress and is sufficient to alter aerobic exercise capacity Am. J. Physiol. Physiol. 2009 297 C1520 C1532 10.1152/ajpcell.00372.2009 19776389 PMC2793066 · DOI
  39. [41]Kneppers A. Verdijk L. De Theije C. Corten M. Gielen E. Van Loon L. Schols A. Langen R. A novel in vitro model for the assessment of postnatal myonuclear accretion Skelet. Muscle 2018 8 4 10.1186/s13395-018-0151-4 29444710 PMC5813369 · DOI
  40. [42]Orfanos Z. Gödderz M.P.O. Soroka E. Gödderz T. Rumyantseva A. van der Ven P. Hawke T.J. Fürst D.O. Breaking sarcomeres by in vitro exercise Sci. Rep. 2016 6 19614 10.1038/srep19614 26804343 PMC4726327 · DOI
  41. [43]Feng Y.Z. Nikolić N. Bakke S.S. Kase E.T. Guderud K. Hjelmesæth J. Aas V. Rustan A.C. Thoresen G.H. Myotubes from lean and severely obese subjects with and without type 2 diabetes respond differently to an in vitro model of exercise Am. J. Physiol. Physiol. 2015 308 C548 C556 10.1152/ajpcell.00314.2014 25608533 · DOI
  42. [44]Brown A.E. Jones D.E. Walker M. Newton J.L. Abnormalities of AMPK Activation and Glucose Uptake in Cultured Skeletal Muscle Cells from Individuals with Chronic Fatigue Syndrome PLoS ONE 2015 10 e0122982 10.1371/journal.pone.0122982 25836975 PMC4383615 · DOI

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Authors
Catteau, M., Passerieux, E., Blervaque, L., Gouzi, F., Ayoub, B., Hayot, M., & Pomiès, P.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • PhyMedExp, University of Montpellier—INSERM—CNRS—CHRU Montpellier, 34295 Montpellier, France
Corresponding author
Pomiès, Pascal
Venue
Cells
Publisher
MDPI AG
Published
2021-11-03
Volume
10
Issue
11
Pages
3002
ISSN
2073-4409 (ISSN-L)
OpenAlex
W3209880202
Cited by
9
References
2
Citations by year
2026: 1 · 2025: 2 · 2024: 1 · 2023: 2 · 2022: 3
FWCI
0.47
Type
journal article
Language
en
Open access
Locations
  • Cells (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
French Ministry of Public Health and Montpellier University Hospital (PHRCI)
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 › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
Keywords
chronic obstructive pulmonary disease, skeletal muscle weakness, muscle atrophy, electrical pulse stimulation, endurance training, myotubes, muscle fiber type shift, mTOR signaling, myogenesis, mitochondrial biogenesis, lipid peroxidation, oxidative stress, manganese superoxide dismutase, GPX4, PGC-1α, MyoD, Myf5
MeSH terms
Antioxidants, Organelle Biogenesis, Cell Differentiation, Electric Stimulation Therapy, Female, Humans, Male, Middle Aged, Lipid Peroxidation, Biomarkers, Case-Control Studies, Oxidative Stress, Muscle Fibers, Skeletal, Pulmonary Disease, Chronic Obstructive, Muscle Cells, Proteolysis

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