Frontiers in Biology

, Volume 7, Issue 6, pp 506–513 | Cite as

Oxidative stress, respiratory muscle dysfunction, and potential therapeutics in chronic obstructive pulmonary disease

  • Li Zuo
  • Allison H. Hallman
  • Marvin K. Yousif
  • Michael T. Chien
Review

Abstract

Chronic obstructive pulmonary disease (COPD) is a highly relevant disorder that induces respiratory muscle dysfunction. One prevalent symptom of COPD is resistive breathing which causes respiratory muscle to significantly increase the magnitude of contractions, resulting in reactive oxygen species (ROS) formation and oxidative stress. Through cellular signaling cascades, ROS activate molecules such as mitogen-activated protein kinases and nuclear factor-κB. These signaling molecules stimulate the release of cytokines which in turn cause damage to the diaphragm, involving sarcomeric disruptions. In response to COPD induced fatigue, the diaphragm undergoes a beneficial fibertype shift to type I muscle fibers, which are more resistant to hypoxia than type II fibers. The lung hyperinflation that occurs in COPD also causes intercostal muscle dysfunction, thereby exacerbating COPD symptoms. In addition, COPD is known to have a connection with heart failure, diabetes, and aging, further decreasing respiratory function. Currently, there is no cure for this disorder. Nevertheless, various potential therapeutic strategies focusing on respiratory muscle have been identified including respiratory muscle training, β2-agonist therapy, and lung volume reduction surgery. In this review, we will outline the role of COPD, oxidative stress, and related complications in respiratory muscle dysfunction.

Keywords

COPD diaphragm ROS cytokine respiratory therapy 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. ACCP/AACVPR evidence-based guidelines (1997). Pulmonary rehabilitation: joint ACCP/AACVPR evidence-based guidelines. ACCP/AACVPR pulmonary rehabilitation guidelines panel. American College of Chest Physicians. American Association of Cardiovascular and Pulmonary Rehabilitation. Chest, 112: 1363–1396CrossRefGoogle Scholar
  2. Allen R G, Tresini M (2000). Oxidative stress and gene regulation. Free Radic Biol Med, 28(3): 463–499PubMedCrossRefGoogle Scholar
  3. Anthonisen N R, Connett J E, Kiley J P, Altose M D, Bailey W C, Buist A S, Conway W A Jr, Enright P L, Kanner R E, O’Hara P, Owens G R, Scanlon P D, Tashkin D P, Wise R A, Altose M D, Connors A F, Redline S, Deitz C, Rakos R F, Conway W A, DeHorn A, Ward J C, Hoppe-Ryan C S, Jentons R L, Reddick J A, Sawicki C, Wise R A, Permutt S, Rand C S, Scanlon P D, Davis L J, Hurt R D, Miller R D, Williams D E, Caron G M, Lauger G G, Toogood S M, Buist A S, Bjornson W M, Johnson L R, Bailey W C, Brooks C M, Dolce J J, Higgins D M, Johnson M A, Lorish C D, Martin B A, Tashkin D P, Coulson A H, Gong H, Harber P I, Li V C, Roth M, Nides M A, Simmons M S, Zuniga I, Anthonisen N R, Manfreda J, Murray R P, Rempel-Rossum S C, Stoyko J M, Connett J E, Kjelsberg M O, Cowles M K, Durkin D A, Enright P L, Kurnow K J, Lee W W, Lindgren P G, Mongin S J, O’Hara P, Voelker H T, Waller L A, Owens G R, Rogers R M, Johnston J J, Pope F P, Vitale F M, Kanner R E, Rigdon M A, Benton K C, Grant P M, Becklake M, Burrows B, Cleary P, Kimbel P, Nett L, Ockene J K, Senior R M, Snider G L, Spitzer W, Williams O D, Hurd S S, Kiley J P, Wu M C, Ayres S M, Hyatt R E, Mason B A (1994). Effects of smoking intervention and the use of an inhaled anticholinergic bronchodilator on the rate of decline of FEV1. The Lung Health Study. JAMA, 272(19): 1497–1505PubMedCrossRefGoogle Scholar
  4. Armstrong R B (1990). Initial events in exercise-induced muscular injury. Med Sci Sports Exerc, 22(4): 429–435PubMedGoogle Scholar
  5. Barreiro E, de la Puente B, Minguella J, Corominas J M, Serrano S, Hussain S N, Gea J (2005). Oxidative stress and respiratory muscle dysfunction in severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med, 171(10): 1116–1124PubMedCrossRefGoogle Scholar
  6. Barreiro E, Peinado V I, Galdiz J B, Ferrer E, Marin-Corral J, Sánchez F, Gea J, Barberà J A, the ENIGMA in COPD Project (2010). Cigarette smoke-induced oxidative stress: A role in chronic obstructive pulmonary disease skeletal muscle dysfunction. Am J Respir Crit Care Med, 182(4): 477–488PubMedCrossRefGoogle Scholar
  7. Begin P, Grassino A (1991). Inspiratory muscle dysfunction and chronic hypercapnia in chronic obstructive pulmonary disease. Am Rev Respir Dis, 143(5 Pt 1): 905–912PubMedGoogle Scholar
  8. Brochard L, Mancebo J, Wysocki M, Lofaso F, Conti G, Rauss A, Simonneau G, Benito S, Gasparetto A, Lemaire F, Isabey D, Harf A (1995). Noninvasive ventilation for acute exacerbations of chronic obstructive pulmonary disease. N Engl J Med, 333(13): 817–822PubMedCrossRefGoogle Scholar
  9. Burge P S, Calverley P M, Jones PW, Spencer S, Anderson J A, Maslen T K (2000). Randomised, double blind, placebo controlled study of fluticasone propionate in patients with moderate to severe chronic obstructive pulmonary disease: the ISOLDE trial. BMJ, 320(7245): 1297–1303PubMedCrossRefGoogle Scholar
  10. Cannon J G, St Pierre B A (1998). Cytokines in exertion-induced skeletal muscle injury. Mol Cell Biochem, 179(1–2): 159–167PubMedCrossRefGoogle Scholar
  11. Cavalcante A G, de Bruin P F (2009). The role of oxidative stress in COPD: current concepts and perspectives. J Bras Pneumol, 35(12): 1227–1237PubMedCrossRefGoogle Scholar
  12. Cooper J D, Trulock E P, Triantafillou A N, Patterson G A, Pohl M S, Deloney P A, Sundaresan R S, Roper C L (1995). Bilateral pneumectomy (volume reduction) for chronic obstructive pulmonary disease. J Thorac Cardiovasc Surg, 109: 106–116; discussion 116–119PubMedCrossRefGoogle Scholar
  13. Covey M K, Larson J L, Wirtz S E, Berry J K, Pogue N J, Alex C G, Patel M (2001). High-intensity inspiratory muscle training in patients with chronic obstructive pulmonary disease and severely reduced function. J Cardiopulm Rehabil, 21(4): 231–240PubMedCrossRefGoogle Scholar
  14. Crisafulli E, Costi S, Fabbri LM, Clini EM (2007). Respiratory muscles training in COPD patients. Int J Chron Obstruct Pulmon Dis, 2(1): 19–25PubMedCrossRefGoogle Scholar
  15. Curkendall S M, DeLuise C, Jones J K, Lanes S, Stang MR, Goehring E Jr, She D (2006). Cardiovascular disease in patients with chronic obstructive pulmonary disease, Saskatchewan Canada cardiovascular disease in COPD patients. Ann Epidemiol, 16(1): 63–70PubMedCrossRefGoogle Scholar
  16. Cutler R G (2005). Oxidative stress and aging: catalase is a longevity determinant enzyme. Rejuvenation Res, 8(3): 138–140PubMedCrossRefGoogle Scholar
  17. Dal Vecchio L, Polese G, Poggi R, Rossi A (1990). “Intrinsic” positive end-expiratory pressure in stable patients with chronic obstructive pulmonary disease. Eur Respir J, 3(1): 74–80Google Scholar
  18. De Troyer A, Kirkwood P A, Wilson T A (2005). Respiratory action of the intercostal muscles. Physiol Rev, 85(2): 717–756PubMedCrossRefGoogle Scholar
  19. De Troyer A, Wilson T A (2009). Effect of acute inflation on the mechanics of the inspiratory muscles. J Appl Physiol, 107(1): 315–323PubMedCrossRefGoogle Scholar
  20. Doucet M, Debigaré R, Joanisse D R, Côté C, Leblanc P, Grégoire J, Deslauriers J, Vaillancourt R, Maltais F (2004). Adaptation of the diaphragm and the vastus lateralis in mild-to-moderate COPD. Eur Respir J, 24(6): 971–979PubMedCrossRefGoogle Scholar
  21. Eid A A, Ionescu A A, Nixon L S, Lewis-Jenkins V, Matthews S B, Griffiths T L, Shale D J (2001). Inflammatory response and body composition in chronic obstructive pulmonary disease. Am J Respir Crit Care Med, 164(8 Pt 1): 1414–1418PubMedGoogle Scholar
  22. Ferguson G T (2006). Why does the lung hyperinflate? Proc Am Thorac Soc, 3(2): 176–179PubMedCrossRefGoogle Scholar
  23. Fessler H E, Permutt S (1998). Lung volume reduction surgery and airflow limitation. Am J Respir Crit Care Med, 157(3 Pt 1): 715–722PubMedGoogle Scholar
  24. Friden J, Sjöström M, Ekblom B (1983). Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med, 4(3): 170–176PubMedCrossRefGoogle Scholar
  25. Gea J, Barreiro E (2008). Update on the mechanisms of muscle dysfunction in COPD. Arch Bronconeumol, 44(6): 328–337PubMedCrossRefGoogle Scholar
  26. Groneberg D A, Chung K F (2004). Models of chronic obstructive pulmonary disease. Respir Res, 5(1): 18PubMedCrossRefGoogle Scholar
  27. Guerri R, Gayete A, Balcells E, Ramirez-Sarmiento A, Vollmer I, Garcia-Aymerich J, Gea J, Orozco-Levi M (2010). Mass of intercostal muscles associates with risk of multiple exacerbations in COPD. Respir Med, 104(3): 378–388PubMedCrossRefGoogle Scholar
  28. Haluszka J, Chartrand D A, Grassino A E, Milic-Emili J (1990). Intrinsic PEEP and arterial PCO2 in stable patients with chronic obstructive pulmonary disease. Am Rev Respir Dis, 141(5 Pt 1): 1194–1197PubMedGoogle Scholar
  29. Ito K, Barnes P J (2009). COPD as a disease of accelerated lung aging. Chest, 135(1): 173–180PubMedCrossRefGoogle Scholar
  30. Janssens J P, Pache J C, Nicod L P (1999). Physiological changes in respiratory function associated with ageing. Eur Respir J, 13(1): 197–205PubMedCrossRefGoogle Scholar
  31. Kang MJ, Lee C G, Lee J Y, Dela Cruz C S, Chen Z J, Enelow R, Elias J A (2008). Cigarette smoke selectively enhances viral PAMP- and virus-induced pulmonary innate immune and remodeling responses in mice. J Clin Invest, 118(8): 2771–2784PubMedGoogle Scholar
  32. Klimathianaki M, Vaporidi K, Georgopoulos D (2011). Respiratory muscle dysfunction in COPD: from muscles to cell. Curr Drug Targets, 12(4): 478–488PubMedCrossRefGoogle Scholar
  33. Kosmidou I, Vassilakopoulos T, Xagorari A, Zakynthinos S, Papapetropoulos A, Roussos C (2002). Production of interleukin-6 by skeletal myotubes: role of reactive oxygen species. Am J Respir Cell Mol Biol, 26(5): 587–593PubMedGoogle Scholar
  34. Lando Y, Boiselle P M, Shade D, Furukawa S, Kuzma A M, Travaline J M, Criner G J (1999). Effect of lung volume reduction surgery on diaphragm length in severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med, 159(3): 796–805PubMedGoogle Scholar
  35. Laoutaris I D, Adamopoulos S, Manginas A, Panagiotakos D B, Kallistratos M S, Doulaptsis C, Kouloubinis A, Voudris V, Pavlides G, Cokkinos D V, Dritsas A (2012). Benefits of combined aerobic/resistance/inspiratory training in patients with chronic heart failure. A complete exercise model? A prospective randomised study. Int J Cardiol, doi: 10.1016/j.ijcard.2012.05.019Google Scholar
  36. Laude E A, Duffy N C, Baveystock C, Dougill B, Campbell M J, Lawson R, Jones P W, Calverley P M (2006). The effect of helium and oxygen on exercise performance in chronic obstructive pulmonary disease: a randomized crossover trial. Am J Respir Crit Care Med, 173: 865–870PubMedCrossRefGoogle Scholar
  37. Levine S, Gregory C, Nguyen T, Shrager J, Kaiser L, Rubinstein N, Dudley G (2002). Bioenergetic adaptation of individual human diaphragmatic myofibers to severe COPD. J Appl Physiol, 92(3): 1205–1213PubMedGoogle Scholar
  38. Levine S, Kaiser L, Leferovich J, Tikunov B (1997). Cellular adaptations in the diaphragm in chronic obstructive pulmonary disease. N Engl J Med, 337(25): 1799–1806PubMedCrossRefGoogle Scholar
  39. Loring S H, Garcia-Jacques M, Malhotra A (2009). Pulmonary characteristics in COPD and mechanisms of increased work of breathing. J Appl Physiol, 107(1): 309–314PubMedCrossRefGoogle Scholar
  40. Lotters F, van Tol B, Kwakkel G, Gosselink R (2002). Effects of controlled inspiratory muscle training in patients with COPD: a metaanalysis. Eur Respir J, 20(3): 570–576PubMedCrossRefGoogle Scholar
  41. Louvaris Z, Zakynthinos S, Aliverti A, Habazettl H, Vasilopoulou M, Andrianopoulos V, Wagner H, Wagner P, Vogiatzis I (2012). Heliox increases quadriceps muscle oxygen delivery during exercise in COPD patients with and without dynamic hyperinflation. J Appl Physiol, 113(7): 1012–1023PubMedCrossRefGoogle Scholar
  42. Mador M J (2002). Muscle mass, not body weight, predicts outcome in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med, 166(6): 787–789PubMedCrossRefGoogle Scholar
  43. Mannino D M, Ford E S, Redd S C (2003). Obstructive and restrictive lung disease and markers of inflammation: data from the Third National Health and Nutrition Examination. Am J Med, 114(9): 758–762PubMedCrossRefGoogle Scholar
  44. Mascarenhas J, Azevedo A, Bettencourt P (2010). Coexisting chronic obstructive pulmonary disease and heart failure: implications for treatment, course and mortality. Curr Opin Pulm Med, 16(2): 106–111PubMedCrossRefGoogle Scholar
  45. McCullough P A, Hollander J E, Nowak R M, Storrow A B, Duc P, Omland T, McCord J, Herrmann H C, Steg P G, Westheim A, Knudsen C W, Abraham W T, Lamba S, Wu A H, Perez A, Clopton P, Krishnaswamy P, Kazanegra R, Maisel A S, Investigators B N PM S, the BNP Multinational Study Investigators (2003). Uncovering heart failure in patients with a history of pulmonary disease: rationale for the early use of B-type natriuretic peptide in the emergency department. Acad Emerg Med, 10(3): 198–204PubMedCrossRefGoogle Scholar
  46. Meecham Jones D J, Paul E A, Jones P W, Wedzicha J A (1995). Nasal pressure support ventilation plus oxygen compared with oxygen therapy alone in hypercapnic COPD. Am J Respir Crit Care Med, 152 (2): 538–544PubMedGoogle Scholar
  47. Mercadier J J, Schwartz K, Schiaffino S, Wisnewsky C, Ausoni S, Heimburger M, Marrash R, Pariente R, Aubier M (1998). Myosin heavy chain gene expression changes in the diaphragm of patients with chronic lung hyperinflation. Am J Physiol, 274(4 Pt 1): L527–L534PubMedGoogle Scholar
  48. Meyer T J, Hill N S (1994). Noninvasive positive pressure ventilation to treat respiratory failure. Ann Intern Med, 120(9): 760–770PubMedGoogle Scholar
  49. Mizuno M (1991). Human respiratory muscles: fibre morphology and capillary supply. Eur Respir J, 4(5): 587–601PubMedGoogle Scholar
  50. Mohanraj P, Merola A J, Wright V P, Clanton T L (1998). Antioxidants protect rat diaphragmatic muscle function under hypoxic conditions. J Appl Physiol, 84(6): 1960–1966PubMedGoogle Scholar
  51. Moon C, Lee Y J, Park H J, Chong Y H, Kang J L (2010). Nacetylcysteine inhibits RhoA and promotes apoptotic cell clearance during intense lung inflammation. Am J Respir Crit Care Med, 181 (4): 374–387PubMedCrossRefGoogle Scholar
  52. Mroz R M, Szulakowski P, Pierzchala W, Chyczewska E, MacNee W (2006). Pathogenesis of chronic obstructive pulmonary disease. Cellular mechanisms (part I). Wiad Lek, 59(1–2): 92–96PubMedGoogle Scholar
  53. Naunheim K S, Wood D E, Mohsenifar Z, Sternberg A L, Criner G J, DeCamp M M, Deschamps C C, Martinez F J, Sciurba F C, Tonascia J, Fishman A P, the National Emphysema Treatment Trial Research Group (2006). Long-term follow-up of patients receiving lungvolume-reduction surgery versus medical therapy for severe emphysema by the National Emphysema Treatment Trial Research Group. Ann Thorac Surg, 82(2): 431–443PubMedCrossRefGoogle Scholar
  54. Nava S, Crotti P, Gurrieri G, Fracchia C, Rampulla C (1992). Effect of a beta 2-agonist (broxaterol) on respiratory muscle strength and endurance in patients with COPD with irreversible airway obstruction. Chest, 101(1): 133–140PubMedCrossRefGoogle Scholar
  55. Orozco-Levi M, Lloreta J, Minguella J, Serrano S, Broquetas J M, Gea J (2001). Injury of the human diaphragm associated with exertion and chronic obstructive pulmonary disease. Am J Respir Crit Care Med, 164(9): 1734–1739PubMedGoogle Scholar
  56. Ottenheijm C A, Heunks L M, Dekhuijzen P N (2007). Diaphragm muscle fiber dysfunction in chronic obstructive pulmonary disease: toward a pathophysiological concept. Am J Respir Crit Care Med, 175(12): 1233–1240PubMedCrossRefGoogle Scholar
  57. Ottenheijm C A, Heunks L M, Dekhuijzen R P (2008). Diaphragm adaptations in patients with COPD. Respir Res, 9(1): 12PubMedCrossRefGoogle Scholar
  58. Ottenheijm C A, Heunks L M, Sieck G C, Zhan W Z, Jansen S M, Degens H, de Boo T, Dekhuijzen P N (2005). Diaphragm dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med, 172(2): 200–205PubMedCrossRefGoogle Scholar
  59. Pauwels R A, Löfdahl C G, Laitinen L A, Schouten J P, Postma D S, Pride N B, Ohlsson S V, the European Respiratory Society Study on Chronic Obstructive Pulmonary Disease (1999). Long-term treatment with inhaled budesonide in persons with mild chronic obstructive pulmonary disease who continue smoking. N Engl J Med, 340(25): 1948–1953PubMedCrossRefGoogle Scholar
  60. Pitsiou G, Kyriazis G, Hatzizisi O, Argyropoulou P, Mavrofridis E, Patakas D (2002). Tumor necrosis factor-alpha serum levels, weight loss and tissue oxygenation in chronic obstructive pulmonary disease. Respir Med, 96(8): 594–598PubMedCrossRefGoogle Scholar
  61. Puente-Maestu L, Pérez-Parra J, Godoy R, Moreno N, Tejedor A, González-Aragoneses F, Bravo J L, Alvarez F V, Camaño S, Agustí A (2009). Abnormal mitochondrial function in locomotor and respiratory muscles of COPD patients. Eur Respir J, 33(5): 1045–1052PubMedCrossRefGoogle Scholar
  62. Ramirez-Sarmiento A, Orozco-Levi M, Guell R, Barreiro E, Hernandez N, Mota S, Sangenis M, Broquetas J M, Casan P, Gea J (2002). Inspiratory muscle training in patients with chronic obstructive pulmonary disease: structural adaptation and physiologic outcomes. Am J Respir Crit Care Med, 166(11): 1491–1497PubMedCrossRefGoogle Scholar
  63. Rana J S, Mittleman M A, Sheikh J, Hu F B, Manson J E, Colditz G A, Speizer F E, Barr R G, Camargo C A Jr (2004). Chronic obstructive pulmonary disease, asthma, and risk of type 2 diabetes in women. Diabetes Care, 27(10): 2478–2484PubMedCrossRefGoogle Scholar
  64. Reid M B (2001). Invited Review: redox modulation of skeletal muscle contraction: what we know and what we don’t. J Appl Physiol, 90(2): 724–731PubMedCrossRefGoogle Scholar
  65. Reid MB, Haack K E, Franchek KM, Valberg P A, Kobzik L, West M S (1992). Reactive oxygen in skeletal muscle. I. Intracellular oxidant kinetics and fatigue in vitro. J Appl Physiol, 73(5): 1797–1804PubMedGoogle Scholar
  66. Rennard S I, Vestbo J (2008). Natural histories of chronic obstructive pulmonary disease. Proc Am Thorac Soc, 5(9): 878–883PubMedCrossRefGoogle Scholar
  67. Ribera F, N’Guessan B, Zoll J, Fortin D, Serrurier B, Mettauer B, Bigard X, Ventura-Clapier R, Lampert E (2003). Mitochondrial electron transport chain function is enhanced in inspiratory muscles of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med, 167(6): 873–879PubMedCrossRefGoogle Scholar
  68. Roisin R R, Vestbo J (2011). Global initiative for chronic obstructive lung disease. GOLD: 1-74Google Scholar
  69. Rutten F H, Cramer MJ, Grobbee D E, Sachs A P, Kirkels J H, Lammers JW, Hoes AW (2005). Unrecognized heart failure in elderly patients with stable chronic obstructive pulmonary disease. Eur Heart J, 26 (18): 1887–1894PubMedCrossRefGoogle Scholar
  70. Sanchez J, Bastien C, Medrano G, Riquet M, Derenne J P (1984). Metabolic enzymatic activities in the diaphragm of normal men and patients with moderate chronic obstructive pulmonary disease. Bull Eur Physiopathol Respir, 20(6): 535–540PubMedGoogle Scholar
  71. Schols A M (2003). Nutritional and metabolic modulation in chronic obstructive pulmonary disease management. Eur Respir J Suppl, 46: 81s–86sPubMedCrossRefGoogle Scholar
  72. Scott A, Wang X, Road J D, Reid W D (2006). Increased injury and intramuscular collagen of the diaphragm in COPD: autopsy observations. Eur Respir J, 27(1): 51–59PubMedCrossRefGoogle Scholar
  73. Shindoh C, DiMarco A, Thomas A, Manubay P, Supinski G (1990). Effect of N-acetylcysteine on diaphragm fatigue. J Appl Physiol, 68 (5): 2107–2113PubMedGoogle Scholar
  74. Sidney S, Sorel M, Quesenberry C P Jr, DeLuise C, Lanes S, Eisner MD (2005). COPD and incident cardiovascular disease hospitalizations and mortality: Kaiser Permanente Medical Care Program. Chest, 128 (4): 2068–2075PubMedCrossRefGoogle Scholar
  75. Sigala I, Zacharatos P, Toumpanakis D, Michailidou T, Noussia O, Theocharis S, Roussos C, Papapetropoulos A, Vassilakopoulos T (2011). MAPKs and NF-κB differentially regulate cytokine expression in the diaphragm in response to resistive breathing: the role of oxidative stress. Am J Physiol Regul Integr Comp Physiol, 300(5): R1152–R1162PubMedCrossRefGoogle Scholar
  76. Smith W N, Dirks A, Sugiura T, Muller S, Scarpace P, Powers S K (2002). Alteration of contractile force and mass in the senescent diaphragm with beta(2)-agonist treatment. J Appl Physiol, 92(3): 941–948PubMedGoogle Scholar
  77. Son Y O, Wang L, Poyil P, Budhraja A, Hitron J A, Zhang Z, Lee J C, Shi X (2012). Cadmium induces carcinogenesis in BEAS-2b cells through ROS-dependent activation of PI3K/AKT/GSK-3beta/betacatenin signaling. Toxicol Appl Pharmacol, doi: S0041-008X(12)00329-8 [pii] 10.1016/j.taap.2012.07.028Google Scholar
  78. Stauber W T, Smith C A, Miller G R, Stauber F D (2000). Recovery from 6 weeks of repeated strain injury to rat soleus muscles. Muscle Nerve, 23(12): 1819–1825PubMedCrossRefGoogle Scholar
  79. Stubbings A K, Moore A J, Dusmet M, Goldstraw P, West T G, Polkey M I, Ferenczi M A (2008). Physiological properties of human diaphragm muscle fibres and the effect of chronic obstructive pulmonary disease. J Physiol, 586(10): 2637–2650PubMedCrossRefGoogle Scholar
  80. Testelmans D, Crul T, Maes K, Agten A, Crombach M, Decramer M, Gayan-Ramirez G (2010). Atrophy and hypertrophy signalling in the diaphragm of patients with COPD. Eur Respir J, 35(3): 549–556PubMedCrossRefGoogle Scholar
  81. Tidball J G (2005). Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol, 288(2): R345–R353PubMedCrossRefGoogle Scholar
  82. Van Der Heijden H F, Dekhuijzen P N, Folgering H, Ginsel L A, Van Herwaarden C L (1998). Long-term effects of clenbuterol on diaphragm morphology and contractile properties in emphysematous hamsters. J Appl Physiol, 85(1): 215–222Google Scholar
  83. Vestbo J, Sørensen T, Lange P, Brix A, Torre P, Viskum K (1999). Longterm effect of inhaled budesonide in mild and moderate chronic obstructive pulmonary disease: a randomised controlled trial. Lancet, 353(9167): 1819–1823PubMedCrossRefGoogle Scholar
  84. Watz H, Waschki B, Meyer T, Kretschmar G, Kirsten A, Claussen M, Magnussen H (2010). Decreasing cardiac chamber sizes and associated heart dysfunction in COPD: role of hyperinflation. Chest, 138(1): 32–38PubMedGoogle Scholar
  85. Wijnhoven H J, Heunks L M, Geraedts M C, Hafmans T, Viña J R, Dekhuijzen P N (2006). Oxidative and nitrosative stress in the diaphragm of patients with COPD. Int J Chron Obstruct Pulmon Dis, 1(2): 173–179PubMedCrossRefGoogle Scholar
  86. Willems ME, Stauber WT (2001). Force deficits after repeated stretches of activated skeletal muscles in female and male rats. Acta Physiol Scand, 172(1): 63–67PubMedCrossRefGoogle Scholar
  87. Wouters E F (2000). Nutrition and metabolism in COPD. Chest, 117(5 Suppl 1): 274S–280SPubMedCrossRefGoogle Scholar
  88. Zuo L, Nogueira L, Hogan M C (2011a). Reactive oxygen species formation during tetanic contractions in single isolated Xenopus myofibers. J Appl Physiol, 111(3): 898–904PubMedCrossRefGoogle Scholar
  89. Zuo L, Roberts W J, Tolomello R C, Goins A T (2011b). Ischemic and hypoxic preconditioning protect cardiac muscles via intracellular ROS signaling. Front Biol, doi: 10.1007/s11515-012-1225-zGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Li Zuo
    • 1
  • Allison H. Hallman
    • 1
  • Marvin K. Yousif
    • 1
  • Michael T. Chien
    • 2
  1. 1.Molecular Physiology and Biophysics Laboratory, Department of Biological SciencesOakland UniversityRochesterUSA
  2. 2.Department of BiologyKalamazoo CollegeKalamazooUSA

Personalised recommendations