Cigarette Smoke–induced Oxidative Stress: A Role in Chronic Obstructive Pulmonary Disease Skeletal Muscle Dysfunction
Abstract
Rationale Inflammation and oxidative stress contribute to muscle dysfunction in patients with chronic obstructive pulmonary disease (COPD). Oxidants contained in cigarette smoke (CS) induce adverse effects on tissues through oxidative phenomena. Objectives To explore oxidative stress and inflammation in quadriceps of human smokers and in diaphragm and limb muscles of guinea pigs chronically exposed to CS. Methods Muscle function, protein oxidation and nitration, antioxidants, oxidized proteins, inflammation, creatine kinase activity, and lung and muscle structures were investigated in vastus lateralis of smokers, patients with COPD, and healthy control subjects and in diaphragm and gastrocnemius of CS-exposed guinea pigs at 3, 4, and 6 months. Measurements and main results Compared with control subjects, quadriceps muscle force was mildly but significantly reduced in smokers; protein oxidation levels were increased in quadriceps of smokers and patients with COPD, and in respiratory and limb muscles of CS-exposed animals; glycolytic enzymes, creatine kinase, carbonic anydrase-3, and contractile proteins were significantly more carbonylated in quadriceps of smokers and patients with COPD, and in respiratory and limb muscles of CS-exposed guinea pigs. Chronic CS exposure induced no significant rise in muscle inflammation in either smokers or rodents. Muscle creatine kinase activity was reduced only in patients with COPD and in both diaphragm and gastrocnemius of CS-exposed anima…
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Some studies report no difference in oxidative stress markers between COPD patients and healthy smokers, implying that oxidative stress could mainly be attributed to cigarette smoke extracts and not the specificity of systemic involvement of COPD.
“Of note, some studies report no difference in oxidative stress markers between COPD patients and healthy smokers [130], implying that oxidative stress could mainly be attributed to CS extracts and not the specificity of systemic involvement of COPD.”
From Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting (2023) · cites this paper as [130]
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InfluentialLocomotor Muscles in COPD: The Rationale for Rehabilitative Exercise Training
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Barreiro, E. (2013) · Mass Spectrometry Reviews · doi:10.1002/mas.21394 · Cited by 42 · see citing works
“Significant inflammatory events did not develop in any of the analyzed muscles (Barreiro et al., 2010).”
BackgroundInfluentialSelf-citationGouzi, F., Maury, J., Molinari, N., Pomiès, P., Mercier, J. G., PREFAUT, C. G., & Hayot, M. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01352.2012 · Cited by 39 · see citing works
Konokhova, Y., Spendiff, S., Jagoe, R. T., Aare, S., Kapchinsky, S., MacMillan, N. J., Rozakis, P., Picard, M., Aubertin-Leheudre, M., Pion, C. H., et al. (2016) · Skeletal Muscle · doi:10.1186/s13395-016-0083-9 · Cited by 46 · see citing works
“with oxidative damage to lipids and proteins having been measured most commonly [20, 48, 49].”
Darabseh, M., Maden-Wilkinson, T., Welbourne, G., Wüst, R., Ahmed, N., Aushah, H., Selfe, J., Morse, C., & Degens, H. (2021) · Scientific Reports · doi:10.1038/s41598-021-91510-x · Cited by 45
Konno, M., Asai, A., Kawamoto, K., Nishida, N., Satoh, T., Doki, Y., Mori, M., & Ishii, H. (2017) · International Journal of Oncology · doi:10.3892/ijo.2017.3885 · Cited by 47 · see citing works
“However, the induced pluripotent stem cell lines showed different pathological mtDNA point mutations (20,25,63-66).”
Salazar-Degracia, A., Busquets, S., Argiles, J., Bargalló-Gispert, N., López-Soriano, F., & Barreiro, E. (2018) · Biochimie · doi:10.1016/j.biochi.2018.04.009 · Cited by 43 · see citing works
Self-citationZuo, L., Hallman, A. H., Yousif, M. K., & Chien, M. T. (2012) · Frontiers in Biology · doi:10.1007/s11515-012-1251-x · Cited by 39 · see citing works
“Hypercapnic respiratory failure often accompanies COPD due to the declination of force per contraction of inspiratory muscle and the increase of intracellular CO2 (Begin and Grassino, 1991; Loring et al., 2009).”
BackgroundBarreiro, E., & Sznajder, J. I. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01027.2012 · Cited by 47 · see citing works
“Taken together, these biological mechanisms could, in part, account for the lesser fatigue-resistant phenotype encountered in the peripheral muscles of patients with severe COPD and muscle atrophy (13, 16, 18, 35, 56).”
BackgroundSelf-citationBarreiro, E., Salazar‐Degracia, A., Sancho‐Muñoz, A., & Gea, J. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27789 · Cited by 39 · see citing works
“In the present study, oxidative stress levels were significantly greater in the VL of both cancer cachectic and all groups of COPD patients, as also consistently demonstrated in previous studies (Barreiro et al., 2010, 2018; Puig‐Vilanova, Rodriguez, et al., 2014).”
BackgroundResultSelf-citationEvaluation of the pulmonary effects of short-term nose-only cigarette smoke exposure in mice
Nemmar, A., Raza, H., Subramaniyan, D., John, A., Elwasila, M., Ali, B., & Adeghate, E. (2012) · Experimental biology and medicine · doi:10.1258/ebm.2012.012103 · Cited by 40
Liu, F., You, F., Yang, L., Du, X., Li, C., Chen, G., & Xie, D. (2024) · Nutrition Journal · doi:10.1186/s12937-024-00953-1 · Cited by 38 · see citing works
“Besides dietary factors, the body’s oxidative stress status is also influenced by various lifestyle elements such as obesity, alcohol consumption, smoking, and physical activity [10–12].”
BackgroundGreising, S. M., Ottenheijm, C., O'Halloran, K., & Barreiro, E. (2018) · Journal of applied physiology · doi:10.1152/japplphysiol.01059.2017 · Cited by 39 · see citing works
Self-citationNemmar, A., Raza, H., Yuvaraju, P., Beegam, S., John, A., Yasin, J., Hameed, R., Adeghate, E., & Ali, B. (2013) · Journal of applied physiology · doi:10.1152/japplphysiol.00194.2013 · Cited by 39
Exercise training reverses inflammation and muscle wasting after tobacco smoke exposure.
Krüger, K., Seimetz, M., Ringseis, R., Wilhelm, J., Pichl, A., Couturier, A., Eder, K., Weissmann, N., & Mooren, F. (2018) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.00316.2017 · Cited by 38
Sreekumar, V., Aspera-Werz, R. H., Ehnert, S., Strobel, J., Tendulkar, G., Heid, D., Schreiner, A. J., Arnscheidt, C., & Nussler, A. K. (2017) · Archives of Toxicology · doi:10.1007/s00204-017-2149-9 · Cited by 37 · see citing works
“which has profound roles in impairing bone regeneration (Barreiro et al. 2010; Church and Pryor 1985; Patel et al. 2013; Staempfli and Anderson 2009).”
BackgroundExercise Capacity, Muscle Strength, and Fatigue in Sarcoidosis: A Follow-Up Study
Marcellis, R. G. J., Lenssen, A., Kleynen, S., de Vries, J., & Drent, M. (2013) · Lung · doi:10.1007/s00408-013-9456-6 · Cited by 36 · see citing works
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“The possibility of directly implicating chronic CS exposure to development of PCS in COPD is further supported by recent findings that CS induces direct oxidative damage of several important proteins involved in the regulation of muscle metabolism and bioenergetics and that these changes precede the respiratory change…”
BackgroundResultBin, Y., Xiao, Y., Huang, D., Ma, Z., Liang, Y., Bai, J., Zhang, W., Liang, Q., Zhang, J., Zhong, X., et al. (2019) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00005.2018 · Cited by 35 · see citing works
Wang, Y., Li, P., Cao, Y., Liu, C., Wang, J., & Wu, W. (2022) · Aging and Disease · doi:10.14336/ad.2022.0603 · Cited by 39 · see citing works
“Mitochondria are involved in the production of most ROS and are an important hub of OS [46].”
BackgroundAusín, P., Martínez-Llorens, J., Sabaté-Brescó, M., Casadevall, C., Barreiro, E., & Gea, J. (2017) · Chronic Respiratory Disease · doi:10.1177/1479972316674412 · Cited by 35 · see citing works
Self-citationThe Role of Physical Therapists in Smoking Cessation: Opportunities for Improving Treatment Outcomes
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Natural products and skeletal muscle health
Qu, Z., Zhou, S., Li, P., Liu, C., Yuan, B., Zhang, S., & Liu, A. (2021) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2021.108619 · Cited by 35 · see citing works
Ramos, C. M. D. O., Campos, K., Costa, G. D. P., Cangussú, S. D., Talvani, A., & Bezerra, F. (2018) · Regulatory toxicology and pharmacology : RTP · doi:10.1016/j.yrtph.2018.07.008 · Cited by 33 · see citing works
Foumani, A. A., Mehrdad, M., Jafarinezhad, A., Nokani, K., & Jafari, A. (2019) · International Journal of COPD · doi:10.2147/copd.s207400 · Cited by 39 · see citing works
“In other words, deficient vitamin D3 can also reduce actin and troponin, impair calcium uptake in the sarcoplasmic reticulum, adjust protein synthesis, and increase apoptosis.(20) Banerjee et al demonstrated that vitamin D3 stimulated the airway smooth-muscle cells to express vitamin D3 receptors and regulated inflamm…”
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Exercise Training Reverses Extrapulmonary Impairments in Smoke-exposed Mice
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Stasko, S. A., Hardin, B. J., Smith, J. D., Moylan, J. S., & Reid, M. B. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00871.2012 · Cited by 30 · see citing works
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- Authors
- Barreiro, E., Peinado, V. I., Galdiz, J. B., Ferrer, E., Marin-Corral, J., Sánchez, F., Gea, J., & Barberà, J. A.
- Affiliations
- Universitat Pompeu Fabra (ES)
- Instituto de Salud Carlos III (ES)
- Pulmonology Department and Research Unit, Hospital de Cruces, Basque Country University, Barakaldo, Basque Country, Spain
- Muscle and Respiratory System Research Unit, Pulmonology Department, Municipal Institute of Medical Research, Hospital del Mar, and Health and Experimental Sciences Department, Universitat Pompeu Fabra, Barcelona, Catalonia
- Venue
- American Journal of Respiratory and Critical Care Medicine
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-08
- Volume
- 182
- Issue
- 4
- Pages
- 477-488
- ISSN
- 1073-449X (ISSN-L)
- 1535-4970
- OpenAlex
- W1941094264
- Cited by
- 272
- References
- 0
- Citations by year
- 2026: 10 · 2025: 11 · 2024: 9 · 2023: 19 · 2022: 15 · 2021: 21 · 2020: 10 · 2019: 13 · 2018: 16 · 2017: 21 · 2016: 23 · 2015: 20 · 2014: 20 · 2013: 27 · 2012: 23
- FWCI
- 17.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Respiratory and Critical Care Medicine (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Chronic Obstructive Pulmonary Disease (COPD) Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Keywords
- cigarette smoke, oxidative stress, chronic obstructive pulmonary disease, skeletal muscle dysfunction, protein oxidation, nitration, muscle inflammation, creatine kinase, diaphragm, quadriceps, guinea pig model, muscle atrophy
- MeSH terms
- Animals, Creatine Kinase, Guinea Pigs, Humans, Lung, Male, Middle Aged, Smoking, Time Factors, Immunoblotting, Biomarkers, Cytokines, Reactive Oxygen Species, Oxidative Stress, Muscle, Skeletal, Muscle Weakness, Carbonic Anhydrase III, Reactive Nitrogen Species, Pulmonary Disease, Chronic Obstructive
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