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

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: 1363–1396

Allen R G, Tresini M (2000). Oxidative stress and gene regulation. Free Radic Biol Med, 28(3): 463–499

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): 1497–1505

Armstrong R B (1990). Initial events in exercise-induced muscular injury. Med Sci Sports Exerc, 22(4): 429–435

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): 1116–1124

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): 477–488

Begin P, Grassino A (1991). Inspiratory muscle dysfunction and chronic hypercapnia in chronic obstructive pulmonary disease. Am Rev Respir Dis, 143(5 Pt 1): 905–912

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): 817–822

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): 1297–1303

Cannon J G, St Pierre B A (1998). Cytokines in exertion-induced skeletal muscle injury. Mol Cell Biochem, 179(1–2): 159–167

Cavalcante A G, de Bruin P F (2009). The role of oxidative stress in COPD: current concepts and perspectives. J Bras Pneumol, 35(12): 1227–1237

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 116–119

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): 231–240

Crisafulli E, Costi S, Fabbri LM, Clini EM (2007). Respiratory muscles training in COPD patients. Int J Chron Obstruct Pulmon Dis, 2(1): 19–25

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): 63–70

Cutler R G (2005). Oxidative stress and aging: catalase is a longevity determinant enzyme. Rejuvenation Res, 8(3): 138–140

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): 74–80

De Troyer A, Kirkwood P A, Wilson T A (2005). Respiratory action of the intercostal muscles. Physiol Rev, 85(2): 717–756

De Troyer A, Wilson T A (2009). Effect of acute inflation on the mechanics of the inspiratory muscles. J Appl Physiol, 107(1): 315–323

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): 971–979

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): 1414–1418

Ferguson G T (2006). Why does the lung hyperinflate? Proc Am Thorac Soc, 3(2): 176–179

Fessler H E, Permutt S (1998). Lung volume reduction surgery and airflow limitation. Am J Respir Crit Care Med, 157(3 Pt 1): 715–722

Friden J, Sjöström M, Ekblom B (1983). Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med, 4(3): 170–176

Gea J, Barreiro E (2008). Update on the mechanisms of muscle dysfunction in COPD. Arch Bronconeumol, 44(6): 328–337

Groneberg D A, Chung K F (2004). Models of chronic obstructive pulmonary disease. Respir Res, 5(1): 18

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): 378–388

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): 1194–1197

Ito K, Barnes P J (2009). COPD as a disease of accelerated lung aging. Chest, 135(1): 173–180

Janssens J P, Pache J C, Nicod L P (1999). Physiological changes in respiratory function associated with ageing. Eur Respir J, 13(1): 197–205

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): 2771–2784

Klimathianaki M, Vaporidi K, Georgopoulos D (2011). Respiratory muscle dysfunction in COPD: from muscles to cell. Curr Drug Targets, 12(4): 478–488

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): 587–593

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): 796–805

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.2012.05.019

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: 865–870

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): 1205–1213

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): 1799–1806

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): 309–314

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): 570–576

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): 1012–1023

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): 787–789

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): 758–762

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): 106–111

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): 198–204

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): 538–544

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–L534

Meyer T J, Hill N S (1994). Noninvasive positive pressure ventilation to treat respiratory failure. Ann Intern Med, 120(9): 760–770

Mizuno M (1991). Human respiratory muscles: fibre morphology and capillary supply. Eur Respir J, 4(5): 587–601

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): 1960–1966

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): 374–387

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): 92–96

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): 431–443

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): 133–140

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): 1734–1739

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): 1233–1240

Ottenheijm C A, Heunks L M, Dekhuijzen R P (2008). Diaphragm adaptations in patients with COPD. Respir Res, 9(1): 12

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): 200–205

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): 1948–1953

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): 594–598

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): 1045–1052

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): 1491–1497

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): 2478–2484

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): 724–731

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): 1797–1804

Rennard S I, Vestbo J (2008). Natural histories of chronic obstructive pulmonary disease. Proc Am Thorac Soc, 5(9): 878–883

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): 873–879

Roisin R R, Vestbo J (2011). Global initiative for chronic obstructive lung disease. GOLD: 1-74

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): 1887–1894

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): 535–540

Schols A M (2003). Nutritional and metabolic modulation in chronic obstructive pulmonary disease management. Eur Respir J Suppl, 46: 81s–86s

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): 51–59

Shindoh C, DiMarco A, Thomas A, Manubay P, Supinski G (1990). Effect of N-acetylcysteine on diaphragm fatigue. J Appl Physiol, 68 (5): 2107–2113

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): 2068–2075

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–R1162

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): 941–948

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.2012.07.028

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): 1819–1825

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): 2637–2650

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): 549–556

Tidball J G (2005). Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol, 288(2): R345–R353

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): 215–222

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): 1819–1823

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): 32–38

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): 173–179

Willems ME, Stauber WT (2001). Force deficits after repeated stretches of activated skeletal muscles in female and male rats. Acta Physiol Scand, 172(1): 63–67

Wouters E F (2000). Nutrition and metabolism in COPD. Chest, 117(5 Suppl 1): 274S–280S

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): 898–904

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-z