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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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“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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Proteomic profiling of carbonic anhydrase CA3 in skeletal muscle
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“In addition, oxidative stress has been also known to be increased by smoking, suggesting that chronic exposure to cigarette smoke may induce muscle atrophy [32].”
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“Examples include oxidative modifications on muscle proteins [22], oxidative DNA damage in lung tissues [23] as well as in human tracheal smooth muscle cells [24].”
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“Inflammation generates mitochondrial dysfunction and oxidative stress and is the main cause that induces the degradation of muscle proteins [51,52].”
BackgroundThe Relevance of Limb Muscle Dysfunction in Chronic Obstructive Pulmonary Disease
Bui, K.-L., Nyberg, A., Rabinovich, R., Saey, D., & Maltais, F. (2019) · Clinics in Chest Medicine · doi:10.1016/j.ccm.2019.02.013 · Cited by 36
Oxidative stress and skeletal muscle dysfunction are present in healthy smokers
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“hemoglobin for carbon monoxide present in cigarette smoke (38), to the decline of the mitochondrial function because of the lower activity of cytochrome c oxidase (37), and to oxidative stress (8).”
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“Cytokine ELISA Protein levels of the inflammatory cytokines tumor necrosis factor (TNF)-α and interleukin (IL)-6 were quantified in the diaphragm and gastrocnemius muscles in all study groups of the 35-week cohort using specific sandwich ELISA kits (eBioscience, Bender MedSystems GmbH, Vienna, Austria), and specific m…”
MethodSelf-citationBarreiro, E., Puig‐Vilanova, E., Marín‐Corral, J., Chacon‐Cabrera, A., Salazar‐Degracia, A., Mateu, X., Puente‐Maestu, L., García‐Arumí, E., Andreu, A. L., & Molina, L. (2015) · Journal of Cellular Physiology · doi:10.1002/jcp.25241 · Cited by 29
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“Oxidative stress is increased in the quadriceps of smokers and COPD patients, in whom it relates to skeletal muscle dysfunction (36).”
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Red Blood Cells Protect Albumin from Cigarette Smoke–Induced Oxidation
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“Conversely, behaviors such as smoking and high iron intake can elevate the production of reactive oxygen and nitrogen species and hasten cellular damage related to oxidative stress [13–15].”
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“Further, in accordance with previous findings in COPD patients [6], guinea pigs demonstrate CS-induced oxidative stress in limb muscles within 3 months of exposure [6,16], potentially highlighting the relevance of the guinea pig model for studying extrapulmonary co-morbidities that characterise human COPD.”
BackgroundResultInfluentialSelf-citationIs vaping better than smoking for cardiorespiratory and muscle function?
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“Furthermore, smoking could promote skeletal muscle wasting via smoking-induced inflammation that increases protein breakdown and decreases protein synthesis [93,94] and results in a reduced maximal force-generating capacity of the muscles from smokers [95,96].”
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Self-citationOxidative Stress in Chronic Obstructive Pulmonary Disease
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Self-citationRedox Regulation in Aging Lungs and Therapeutic Implications of Antioxidants in COPD
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“Higher levels of oxidative stress are detected in the skeletal muscle of patients with COPD [106].”
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“As we did not observe diaphragm ECM remodeling in a mice model of COPD in trained group, it is possible to suggest that training did not lead to abnormal dynamic ventilatory and disadvantages of diaphragm, regarding force generation.”
InfluentialSalazar‐Degracia, A., Busquets, S., Argilés, J. M. A., López-Soriano, F. J., & Barreiro, E. (2017) · PeerJ · doi:10.7717/peerj.4109 · Cited by 23
“In order to evaluate the presence of inflammatory cells in diaphragm and gastrocnemius muscles, immunohistochemical analyses were conducted in eachmuscle of all study groups following previously published methodologies and specific antibodies (Barreiro et al., 2011; Barreiro et al., 2010).”
BackgroundMethodInfluentialSelf-citationRole of Nrf2 and exercise in alleviating COPD-induced skeletal muscle dysfunction
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“10 Skeletal muscle dysfunction is more pronounced in exacerbating patients, 11 suggesting that oxidative stress is aggravated with disease progression.”
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“We conducted exposure studies using the AqE of 3R4F smoke and inducers of oxidative stress, DNA damage, and inflammatory responses because these are considered the earliest key events for chronic inflammatory lung diseases [29 – 32].”
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“oxidative stress imposed by cigarette smoking together with systemic inflammation and hypoxia are important contributors to pathogenesis of skeletal muscle wasting and dysfunction and have been previously extensively reviewed (2-4).”
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SHP2 : The protein tyrosine phosphatase involved in chronic pulmonary inflammation and fibrosis
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“IL-8 secreted by alveolar epithelial cells and activated macrophages after CS exposure exerts an inflammatory mediator and chemoattractant for proinflammatory cells, including neutrophils and lymphocytes.(53,54) Studies indicate that the elevated expression of SHP2 in vitro and in vivo increases the release of IL-8 th…”
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“CS acts as a trigger of oxidative stress and inflammatory responses in the pathogenesis of such diseases (Barreiro et al., 2010; King, 2015; Oh & Sin, 2012; Rahman, Swarska, Henry, Stolk, & MacNee, 2000; Tavilani, Nadi, Karimi, & Goodarzi, 2012).”
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“1,5 It is thought that CS-induced inflammation, 6 apoptosis, 7 and oxidative stress 8,9 are the major drivers of emphysema.”
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“Furthermore, oxidative stress could be applied through personal behavior habits such as smoking or a high-fat diet [17,18].”
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“Whereas the levels of several classical cytokines associated with muscle wasting (such as TNF-a, insulin-like growth factor-1, hypoxia inducible factor 1, and mammalian target of rapamycin) are increased in COPD, the role of TWEAK in muscle mass loss during COPD remains unknown [1, 4, 7, 8].”
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“18,22 It is thought that CS-induced inflam-mation, 23 apoptosis, 24 and oxidative stress, 25,26 are the major drivers of emphysema.”
Sarcopenia in Chronic Illness and Rehabilitative Approaches
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“In addition, the effect of tobacco is associated with the [36] myopathy induced by corticosteroid use (especially systemic steroids) [37, 38], malnutrition that has a negative balance of energy [39], and reduction of physical activity leading sarcopenia [40].”
BackgroundCOPD: osteoporosis and sarcopenia
Majid, H., Kanbar-Agha, F., & Sharafkhaneh, A. (2016) · COPD Research and Practice · doi:10.1186/s40749-016-0019-0 · Cited by 14
“These include poor peripheral oxygenation (due to COPD related gas exchange abnormalities and anemia, leading to inflammation, oxidative stress, apoptosis and poor muscle repair) [190–192], systemic inflammatory state particularly during exacerbations (inhibits muscle contractions, activates catabolic systems such as…”
BackgroundGammal, A. E., O'Farrell, R., O'Mahony, L., Shanahan, F., Killian, K., & O'Connor, T. M. (2015) · Open Journal of Respiratory Diseases · doi:10.4236/ojrd.2015.51003 · Cited by 11
Muscle Dysfunction in Smokers and Patients With Mild COPD
Fonseca, J., Nellessen, A. G., & Pitta, F. D. O. (2019) · Journal of Cardiopulmonary Rehabilitation and Prevention · doi:10.1097/hcr.0000000000000400 · Cited by 9
Association between the oxidative balance score and low muscle mass in middle-aged US adults
Chen, K., Yin, Q., Guan, J.-G., Yang, J.-W., Ma, Y., Hu, Y., Chen, C., & Chen, W. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1358231 · Cited by 9
García-Lucio, J., Argemí, G., Tura-Ceide, O., Díez, M., Paul, T., Bonjoch, C., Coll-Bonfill, N., Blanco, I., Barberá, J. A., Musri, M., et al. (2016) · American Journal of Physiology - Lung cellular and Molecular Physiology · doi:10.1152/ajplung.00261.2015 · Cited by 9
Self-citationTomoda, K., Kubo, K., Hino, K., Kondoh, Y., Nishii, Y., Koyama, N., Yamamoto, Y., Yoshikawa, M., & Kimura, H. (2014) · Journal of Toxicological Sciences · doi:10.2131/jts.39.331 · Cited by 9
“Cigarette smoke induces skeletal muscle wasting (Barreiro et al., 2010; Liu et al., 2011; Nakatani et al., 2003; Rinaldi et al., 2012; Rom et al., 2012).”
Deng, Q., Guo, H., Dai, J., Yang, L., Wu, C. H., Wang, Q., Hu, Z., Yang, M., Liu, L., Yu, D., et al. (2013) · Carcinogenesis · doi:10.1093/carcin/bgt145 · Cited by 8
“Cigarette smoke is a complex mixture of numerous carcinogens and oxidants, which can induce multiple important cancer-related changes, such as cell cycle dysregulation (10,11), abnormal apoptosis (12), oxidative stress (13) and inflammation response (14,15), and further induce abnormal cell proliferation and death, ox…”
BackgroundAdvances in proteomic techniques for biomarker discovery in COPD
Casado, B., Luisetti, M., & Iadarola, P. (2010) · Expert Review of Clinical Immunology · doi:10.1586/eci.10.75 · Cited by 8
Oxidative Signaling in Chronic Obstructive Airway Diseases
Thimraj, T. A., George, L., Asrafuzzaman, S., Upadhyay, S., & Ganguly, K. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-805417-8.00007-x · Cited by 9
Arinc, S., Ağca, M., & Yaman, F. (2020) · European Journal of Clinical Nutrition · doi:10.1038/s41430-020-0663-y · Cited by 8
Martínez-González, C., Casanova, C., de Torres, J., Marin, J., de Lucas, P., Fuster, A., Cosío, B., Calle, M., Peces-Barba, G., Solanes, I., et al. (2018) · Chest · doi:10.1016/j.chest.2018.02.007 · Cited by 8
Self-citationAnalysis of Short-Term Smoking Effects in PBMC of Healthy Subjects—Preliminary Study
Wieczfińska, J., Kowalczyk, T., Sitarek, P., Skała, E., & Pawliczak, R. (2018) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph15051021 · Cited by 8
“These compounds are responsible for the recruitment of inflammatory agents and cells and the formation of oxidants, thus inducing oxidative stress and the oxidation of proteins and thiol groups [4].”
BackgroundMateu-Jiménez, M., Fermoselle, C., Rojo, F., Mateu, J., Peña, R., Urtreger, A., Diament, M., Joffé, E. B. D. D. K., Pijuan, L., de Herreros, A. G., et al. (2016) · Current pharmaceutical design · doi:10.2174/1381612822666160623065523 · Cited by 8
“Protein levels of the cytokines TNFalpha and IL-1beta were quantified in tumor homogenates of all mice groups using specific sandwich ELISA kits (RayBiotech, Norcross, GA, USA) as previously described[29-31].”
BackgroundMethodSelf-citationCigarette Smoke Inhibits Brain Mitochondrial Adaptations of Exercised Mice
Speck, A. E., Fraga, D. B., Soares, P., Scheffer, D., da Silva, L. A., Aguiar, A. S., Estreck, E. L., & Pinho, R. A. (2011) · Neurochemical Research · doi:10.1007/s11064-011-0447-9 · Cited by 8
The SIDS–critical diaphragm failure hypothesis revisited
Siren, P. M. (2013) · Upsala Journal of Medical Sciences · doi:10.3109/03009734.2012.744373 · Cited by 7
“The authors go on to note that CS ‘led to the significant increase in oxidative modifications of proteins involved in glycolysis, energy production and distribution, carbon dioxide hydration, and muscle contraction in both humans and guinea pigs [and] the reduction in creatine kinase activity in both respiratory and l…”
BackgroundZhu, Z., Bai, H., Li, Z., Fan, M., Li, G., & Chen, L. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1373709 · Cited by 7
Pérez-Peiró, M., Alvarado, M., Martín‐Ontiyuelo, C., Rodriguez, D. A., & Barreiro, E. (2023) · Nutrients · doi:10.3390/nu15061454 · Cited by 5
Self-citationCOPD: preclinical models and emerging therapeutic targets
Barreiro, E., Wang, X., & Tang, J. (2019) · Expert opinion on therapeutic targets · doi:10.1080/14728222.2019.1667976 · Cited by 6
Self-citationde Vasconcelos, T. B., de Araújo, F. Y. R., de Pinho, J. P. M., Soares, P., & Bastos, V. (2016) · Jornal Brasileiro de Pneumologia · doi:10.1590/s1806-37562015000000342 · Cited by 6
“In this sense, several studies support the relationship between cigarette smoke inhalation and the production of oxidative stress,(33-35) because cigarettes are known to be a potential inducer of adverse effects in biological structures and in tissues, as well as influencing weight loss, inflammatory cell increase, an…”
BackgroundDomínguez‐Álvarez, M., Bresco, M. S., Vilà-Ubach, M., Gáldiz, J. B., Alvarez, F. J., Casadevall, C., Gea, J., & Barreiro, E. (2013) · Translational research · doi:10.1016/j.trsl.2013.12.004 · Cited by 7
Self-citationDas, B., Ray, T., Panda, K., Maiti, A., Sarkar, S., & Sil, A. K. (2014) · Toxicology Reports · doi:10.1016/j.toxrep.2014.09.011 · Cited by 6
Targeting Multiple Pathophysiological Axes in COPD: Nanomaterial Advances
Zhang, Q., Xu, S., Yang, C., Wang, X., Liu, T., Zhang, X., Qu, C., Wu, J. ‐., Yang, J., & Xing, X. (2025) · International Journal of Nanomedicine · doi:10.2147/ijn.s542725 · Cited by 5
Jin, Y., Lin, H., Ye, Z., Wang, H., Liu, Y., Qiu, W., & Liu, C. (2025) · Journal of Alzheimer s Disease Reports · doi:10.1177/25424823241300354 · Cited by 3
“Compared to the lowest quartile, females in the highest OBS quartile scored 268 points higher (OR = 268, 95% CI [14.8, 4863], p = 0.001); males scored 12.7 points higher (OR = 12.7, 95% CI [1.90, 180], p = 0.048).”
InfluentialImpacts of Cigarette Smoke (CS) on Muscle Derangement in Rodents—A Systematic Review
He, W., Ngai, S. P. C., Cheung, K., Lau, B. W.-M., Sánchez-Vidaña, D. I., & Pang, M. Y. C. (2022) · Toxics · doi:10.3390/toxics10050262 · Cited by 6
“Characteristics of the Rodents Three species of rodents were used in the selected studies: Hartley guinea pig, [9] mouse, [23–26,28–30], and Wistar-Kyoto rats [31,32].”
BackgroundMethodResultInfluentialUpper Limb Extremity Muscle-Dysfunction in Chronic Obstructive Pulmonary Disease: A Narrative Review
Suhas, K. M., Alaparthi, G. K., Krishnan, S. K., & Bairapareddy, K. C. (2020) · Current Respiratory Medicine Reviews · doi:10.2174/1573398x16999200621201220 · Cited by 3
Ghosh, S., Acharyya, M., Majumder, T., & Bagchi, A. (2015) · North American Journal of Medicine and Science · doi:10.4103/1947-2714.172846 · Cited by 4
“, PEFR, further ensures these observations.[23]”
Monsó, E., Montuenga, L., de Cos, J. S., & Villena, C. (2015) · Archivos de Bronconeumologia · doi:10.1016/j.arbres.2014.11.010 · Cited by 4
The metabolic profiles of cancer stem cells
Tylichová, Z., Vojtěšek, B., & Coates, P. J. (2026) · Stem Cell Research & Therapy · doi:10.1186/s13287-026-05014-4 · Cited by 3
“Chemotherapy, radioactivity, drugs, toxins, and even smoking can increase ROS levels in the cell [165–167].”
Razat, L., Tamisier, R., Destors, M., Arbib, F., Lantuejoul, L. R., Loiodice, C., Pépin, J., & Degano, B. (2025) · ERJ Open Research · doi:10.1183/23120541.00380-2025 · Cited by 3
Metadata
- 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 › Physiology (medical) › 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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