Respiratory Research | |
Regenerative defect in vastus lateralis muscle of patients with chronic obstructive pulmonary disease | |
Richard Debigaré1  François Maltais1  Bruno B Lemire1  Marie-Ève Paré1  Marie-Eve Thériault1  | |
[1] Centre de recherche Institut universitaire de cardiologie et de pneumologie de Québec, Université Laval, Québec, QC G1V 4G5, Canada | |
关键词: Atrophy; Regeneration; Muscle; COPD; Satellite cells; | |
Others : 790358 DOI : 10.1186/1465-9921-15-35 |
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received in 2013-11-01, accepted in 2014-03-10, 发布年份 2014 | |
【 摘 要 】
Background
Impaired skeletal muscle regeneration could contribute to the progression of muscle atrophy in patients with chronic obstructive pulmonary disease (COPD).
Methods
Satellite cells and myogenesis-related proteins were compared between healthy subjects and patients with COPD, with or without muscle atrophy. Satellite cells were isolated and cultured to assess their proliferative and differentiation aptitudes.
Results
Although satellite cell numbers in muscle samples were similar between groups, the proportion of muscle fibers with central nuclei was increased in COPD. In muscle homogenates, increased expression of MyoD and decreased expression of myogenin and MRF4 were observed in COPD. In cultured satellite cells of patients with COPD, increased protein content was observed for Pax7, Myf5 (proliferation phase) and myogenin (differentiation phase) while myosin heavy chain protein content was significantly lower during differentiation.
Conclusion
In COPD, the number of central nuclei was increased in muscle fibers suggesting a greater number of attempts to regenerate muscle tissue than in healthy subjects. Myogenesis signaling was also altered in muscle homogenates in patients with COPD and there was a profound reduction in the differentiation potential in this population as indicated by a reduced ability to incorporate myosin heavy chain into newly formed myotubes. Collectively, these results indicate that skeletal muscle regenerative capacity termination is impaired in COPD and could contribute to the progression of muscle atrophy progression in this population.
【 授权许可】
2014 Thériault et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Llovera M, Garcia-Martinez C, Agell N, Lopez-Soriano FJ, Authier FJ, Gherardi RK, Argiles JM: Ubiquitin and proteasome gene expression is increased in skeletal muscle of slim AIDS patients. Int J Mol Med 1998, 2:69-73.
- [2]Tisdale MJ: Cachexia in cancer patients. Nat Rev Cancer 2002, 2:862-871.
- [3]Price SR, Bailey JL, Wang X, Jurkovitz C, England BK, Ding X, Phillips LS, Mitch WE: Muscle wasting in insulinopenic rats results from activation of the ATP-dependent, ubiquitin-proteasome proteolytic pathway by a mechanism including gene transcription. J Clin Invest 1996, 98:1703-1708.
- [4]Brooks SV, Faulkner JA: Skeletal muscle weakness in old age: underlying mechanisms. Med Sci Sports Exerc 1994, 26:432-439.
- [5]Tiao G, Fagan JM, Samuels N, James JH, Hudson K, Lieberman M, Fischer JE, Hasselgren PO: Sepsis stimulates nonlysosomal, energy-dependent proteolysis and increases ubiquitin mRNA levels in rat skeletal muscle. J Clin Invest 1994, 94:2255-2264.
- [6]Debigare R, Marquis K, Cote CH, Tremblay RR, Michaud A, Leblanc P, Maltais F: Catabolic/anabolic balance and muscle wasting in patients with COPD. Chest 2003, 124:83-89.
- [7]Gosselink R, Troosters T, Decramer M: Peripheral muscle weakness contributes to exercise limitation in COPD. Am J Respir Crit Care Med 1996, 153:976-980.
- [8]Marquis K, Debigare R, Lacasse Y, LeBlanc P, Jobin J, Carrier G, Maltais F: 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, 166:809-813.
- [9]Wust RC, Degens H: Factors contributing to muscle wasting and dysfunction in COPD patients. Int J Chron Obstruct Pulmon Dis 2007, 2:289-300.
- [10]Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z: Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol 2006, 294:50-66.
- [11]Tidball JG: Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 2005, 288:R345-R353.
- [12]Charge SB, Rudnicki MA: Cellular and molecular regulation of muscle regeneration. Physiol Rev 2004, 84:209-238.
- [13]Hawke TJ, Garry DJ: Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 2001, 91:534-551.
- [14]Hyatt JP, McCall GE, Kander EM, Zhong H, Roy RR, Huey KA: PAX3/7 expression coincides with MyoD during chronic skeletal muscle overload. Muscle Nerve 2008, 38:861-866.
- [15]Snow MH: An autoradiographic study of satellite cell differentiation into regenerating myotubes following transplantation of muscles in young rats. Cell Tissue Res 1978, 186:535-540.
- [16]Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR: Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 2004, 166:347-357.
- [17]Collins CA, Partridge TA: Self-renewal of the adult skeletal muscle satellite cell. Cell Cycle 2005, 4:1338-1341.
- [18]Conboy IM, Rando TA: The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 2002, 3:397-409.
- [19]Nofziger D, Miyamoto A, Lyons KM, Weinmaster G: Notch signaling imposes two distinct blocks in the differentiation of C2C12 myoblasts. Development 1999, 126:1689-1702.
- [20]Brack AS, Conboy IM, Conboy MJ, Shen J, Rando TA: A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2008, 2:50-59.
- [21]Theriault ME, Pare ME, Maltais F, Debigare R: Satellite cells senescence in limb muscle of severe patients with COPD. PLoS ONE 2012, 7:e39124.
- [22]From the Global Strategy for the Diagnosis, Management and Prevention of COPD: Global Initiative for Chronic Obstructive Lung Disease (GOLD). 2014. Available from: http://www.goldcopd.org/ webcite
- [23]Anonymous: Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease (COPD) and asthma. This official statement of the American thoracic society was adopted by the ATS board of directors, November 1986. Am Rev Respir Dis 1987, 136:225-244.
- [24]Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault JC: Lung volumes and forced ventilatory flows. Report working party standardization of lung function tests, European community for steel and coal. Official statement of the European respiratory society. Eur Respir J Suppl 1993, 16:5-40.
- [25]Doucet M, Russell AP, Leger B, Debigare R, Joanisse DR, Caron MA, LeBlanc P, Maltais F: Muscle atrophy and hypertrophy signaling in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2007, 176:261-269.
- [26]Allen RE, Temm-Grove CJ, Sheehan SM, Rice G: Skeletal muscle satellite cell cultures. Methods Cell Biol 1997, 52:155-176.
- [27]Mostert R, Goris A, Weling-Scheepers C, Wouters EFM, Schols AMW: Tissue depletion and health related quality of life in patients with chronic obstructive pulmonary disease. Respir Med 2000, 94:859-867.
- [28]Fabbri LM, Hurd SS: Global strategy for the diagnosis, management and prevention of COPD: 2003 update. Eur Respir J 2003, 22:1-2.
- [29]Debigare R, Maltais F: The major limitation to exercise performance in COPD is lower limb muscle dysfunction. J Appl Physiol 2008, 105:751-753.
- [30]Bernard S, LeBlanc P, Whittom F, Carrier G, Jobin J, Belleau R, Maltais F: Peripheral muscle weakness in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1998, 158:629-634.
- [31]Saey D, Debigare R, LeBlanc P, Mador MJ, Cote CH, Jobin J, Maltais F: Contractile leg fatigue after cycle exercise: a factor limiting exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2003, 168:425-430.
- [32]Eliason G, Abdel-Halim S, Arvidsson B, Kadi F, Piehl-Aulin K: Physical performance and muscular characteristics in different stages of COPD. Scand J Med Sci Sports 2009, 19:865-870.
- [33]Maier A, Gambke B, Pette D: Degeneration-regeneration as a mechanism contributing to the fast to slow conversion of chronically stimulated fast-twitch rabbit muscle. Cell Tissue Res 1986, 244:635-643.
- [34]Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA: Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005, 433:760-764.
- [35]Moore BJ, Miller MJ, Feldman HA, Reid MB: Diaphragm atrophy and weakness in cortisone-treated rats. J Appl Physiol 1989, 67:2420-2426.
- [36]Reid WD, MacGowan NA: Respiratory muscle injury in animal models and humans. Mol Cell Biochem 1998, 179:63-80.
- [37]Orozco-Levi M: Structure and function of the respiratory muscles in patients with COPD: impairment or adaptation? Eur Respir J Suppl 2003, 46:41s-51s.
- [38]Wen Y, Bi P, Liu W, Asakura A, Keller C, Kuang S: Constitutive Notch activation upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells. Mol Cell Biol 2012, 32:2300-2311.
- [39]Plant PJ, Brooks D, Faughnan M, Bayley T, Bain J, Singer L, Correa J, Pearce D, Binnie M, Batt J: Cellular markers of muscle atrophy in chronic obstructive pulmonary disease (COPD). Am J Respir Cell Mol Biol 2010, 42:461-471.
- [40]Fermoselle C, Rabinovich R, Ausin P, Puig-Vilanova E, Coronell C, Sanchez F, Roca J, Gea J, Barreiro E: Does oxidative stress modulate limb muscle atrophy in severe COPD patients? Eur Respir J 2012, 40:851-862.
- [41]Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA: Pax7 is required for the specification of myogenic satellite cells. Cell 2000, 102:777-786.
- [42]Le GF, Rudnicki MA: Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol 2007, 19:628-633.
- [43]Dreyer HC, Blanco CE, Sattler FR, Schroeder ET, Wiswell RA: Satellite cell numbers in young and older men 24 hours after eccentric exercise. Muscle Nerve 2006, 33:242-253.
- [44]Goetsch SC, Hawke TJ, Gallardo TD, Richardson JA, Garry DJ: Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration. Physiol Genomics 2003, 14:261-271.
- [45]Caporossi D, Ciafre SA, Pittaluga M, Savini I, Farace MG: Cellular responses to H(2)O(2) and bleomycin-induced oxidative stress in L6C5 rat myoblasts. Free Radic Biol Med 2003, 35:1355-1364.
- [46]Barnes PJ, Celli BR: Systemic manifestations and comorbidities of COPD. Eur Respir J 2009, 33:1165-1185.
- [47]Crul T, Spruit MA, Gayan-Ramirez G, Quarck R, Gosselink R, Troosters T, Pitta F, Decramer M: Markers of inflammation and disuse in vastus lateralis of chronic obstructive pulmonary disease patients. Eur J Clin Invest 2007, 37:897-904.
- [48]Mitch WE, Price SR: Mechanisms activating proteolysis to cause muscle atrophy in catabolic conditions. J Ren Nutr 2003, 13:149-152.
- [49]Weintraub H, Davis R, Tapscott S, Thayer M, Krause M, Benezra R, Weintraub H, Davis R, Tapscott S, Thayer M, Krause M, Benezra R, Blackwell TK, Turner D, Rupp R, Hollenberg S: The myoD gene family: nodal point during specification of the muscle cell lineage. Science 1991, 251:761-766.
- [50]Rudnicki MA, Braun T, Hinuma S, Jaenisch R: Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 1992, 71:383-390.
- [51]Timchenko NA, Iakova P, Cai ZJ, Smith JR, Timchenko LT: Molecular basis for impaired muscle differentiation in myotonic dystrophy. Mol Cell Biol 2001, 21:6927-6938.
- [52]Oexle K, Kohlschutter A: Cause of progression in Duchenne muscular dystrophy: impaired differentiation more probable than replicative aging. Neuropediatrics 2001, 32:123-129.
- [53]Carlson ME, Hsu M, Conboy IM: Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 2008, 454:528-532.