Chronic exercise decreases cytokine production in healthy rat skeletal muscle
Abstract
Skeletal muscle is the source of pro- and anti-inflammatory cytokines, and recently, it has been recognized as an important source of interleukin-6 (IL-6). Acute physical exercise is known to induce a pro-inflammatory cytokine profile in the plasma. However, the effect of chronic physical exercise in the production of pro- and anti-inflammatory cytokines by the skeletal muscle has never been examined. We assessed IL-6, TNF-alpha, IL-1beta and IL-10 levels in the skeletal muscle of rats submitted to endurance training. Animals were randomly assigned to either a sedentary group (S, n = 7) or an endurance exercise trained group (T, n = 8). Trained rats ran on a treadmill for 5 days week(-1) for 8 weeks (60% VO(2max)). Detection of IL-6, TNF-alpha, IL-1beta and IL-10 protein expression was carried out by ELISA. We found decreased expression of IL-1beta, IL-6, TNF-alpha and IL-10 (28%, 27%, 32% and 37%, respectively, p < 0.05) in the extensor digital longus (EDL) from T, when compared with S. In the soleus, IL-1beta, TNF-alpha and IL-10 protein levels were similarly decreased (34%, 42% and 50%, respectively, p < 0.05) in T in relation to S, while IL-6 expression was not affected by the training protocol. In conclusion, exercise training induced decreased cytokine protein expression in the skeletal muscle. These data show that in healthy rats, 8-week moderate-intensity aerobic training down regulates skeletal muscle production of cytokines involved in the onset, maintenance and regulation of inflammation, and that the response is heterogeneous according to fibre composition.
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Regular physical exercise is directly related to reduced systemic inflammation.
“(5) reduced systemic inflammation (Lira et al., 2009; Rosa Neto et al., 2009; Batista et al., 2010)”
From Physical Exercise-Induced Myokines and Muscle-Adipose Tissue Crosstalk: A Review of Current Knowledge and the Implications for Health and Metabolic Diseases (2018) · cites this paper as Lira et al., 2009
Regular physical exercise, organized in an exercise training program (chronic effect), exerts an anti-inflammatory effect induced by the sessions (acute effect), which leads to improved protection against chronic inflammatory situations, levels of proinflammatory cytokines and C-reactive protein.
“Given this condition, the hypothesis that has been proposed is that the regular practice of physical exercise, organized in a exercise training program (chronic effect), exerts an anti-inflammatory effect induced by the sessions (acute effect), which leads to improved protection against chronic inflammatory situations, levels of proinflammatory cytokines and C-reactive protein (Petersen and Peders”
From Physical Exercise-Induced Myokines and Muscle-Adipose Tissue Crosstalk: A Review of Current Knowledge and the Implications for Health and Metabolic Diseases (2018) · cites this paper as Lira et al., 2009
Cites
The anti-inflammatory effect of exercise
Petersen, A. M. W., & Pedersen, B. K. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00164.2004 · Cited by 3,100 · see citing works
Muscle‐derived interleukin‐6: mechanisms for activation and possible biological roles
FEBBRAIO, M. A., & PEDERSEN, B. K. (2002) · The FASEB Journal · doi:10.1096/fj.01-0876rev · Cited by 875 · see citing works
Role of Myokines in Exercise and Metabolism
Pedersen, B. K., Åkerström, T. C. A., Nielsen, A. R., & Fischer, C. P. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00080.2007 · Cited by 841 · see citing works
Interleukin-6 in acute exercise and training: what is the biological relevance?
Fischer, C. P. (2026) · PubMed · doi:10.22029/eir.2006.1620 · Cited by 817 · see citing works
The Role of Inflammatory Cytokines in Diabetes and Its Complications
King, G. L. (2008) · Journal of Periodontology · doi:10.1902/jop.2008.080246 · Cited by 680 · see citing works
Interleukin-10 Signaling Blocks Inhibitor of κB Kinase Activity and Nuclear Factor κB DNA Binding
Schottelius, A. J. G., Mayo, M. W., Sartor, R. B., & Baldwin, A. S. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.45.31868 · Cited by 526 · see citing works
Hamburg, N. M., McMackin, C. J., Huang, A. L., Shenouda, S. M., Widlansky, M. E., Schulz, E., Gokce, N., Ruderman, N. B., Keaney, J. F., & Vita, J. A. (2007) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.107.153288 · Cited by 474 · see citing works
Interleukin-6 Is a Novel Factor Mediating Glucose Homeostasis During Skeletal Muscle Contraction
Febbraio, M. A., Hiscock, N., Sacchetti, M., Fischer, C. P., & Pedersen, B. K. (2004) · Diabetes · doi:10.2337/diabetes.53.7.1643 · Cited by 455 · see citing works
Mattusch, Dufaux, Heine, Mertens, & Rost (2000) · International Journal of Sports Medicine · doi:10.1055/s-2000-8852 · Cited by 389 · see citing works
The Cytokine Response to Physical Activity and Training
Moldoveanu, A., Shephard, R., & Shek, P. (2001) · Sports Medicine · doi:10.2165/00007256-200131020-00004 · Cited by 339 · see citing works
Bradley, R. L., Jeon, J. Y., Liu, F.-F., & Maratos–Flier, E. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00309.2007 · Cited by 317 · see citing works
Aerobic Exercise Decreases Chronic Allergic Lung Inflammation and Airway Remodeling in Mice
Vieira, R. P., Barbosa, R. C. C., Duarte, A. C. S., Santos, A. B. G., Perini, A., Neto, H. C. C.-F., Mauad, T., Martins, M. A., Dolhnikoff, M., & Carvalho, C. R. F. (2007) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200610-1567oc · Cited by 196 · see citing works
Zaldivar, F. P., Wang‐Rodriguez, J., Nemet, D., Schwindt, C. D., Galassetti, P. R., Mills, P. J., Wilson, L. D., & Cooper, D. M. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00562.2005 · Cited by 167 · see citing works
Neuroendocrine Regulation of IL‐12 and TNF‐α/IL‐10 Balance: Clinical Implications
ELENKOV, I. J., CHROUSOS, G. P., & WILDER, R. L. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb05374.x · Cited by 158 · see citing works
State of the Art Reviews: The Anti-Inflammatory Actions of Exercise Training
Flynn, M. G., McFarlin, B. K., & Markofski, M. M. (2007) · American Journal of Lifestyle Medicine · doi:10.1177/1559827607300283 · Cited by 154 · see citing works
Park, P., McMullen, M. R., Huang, H., Thakur, V., & Nagy, L. E. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701419200 · Cited by 148 · see citing works
Fiber type specific expression of TNF-alpha, IL-6 and IL-18 in human skeletal muscles.
Plomgaard, P., Penkowa, M., & Pedersen, B. K. (2005) · PubMed · Cited by 139 · see citing works
Skeletal muscle as an immunogenic organ
Nielsen, S. J., & Pedersen, B. K. (2008) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.02.005 · Cited by 114 · see citing works
Endurance training induces depot-specific changes in IL-10/TNF-alpha ratio in rat adipose tissue.
Lira, F. S., Neto, J. C. R., Yamashita, A. S., Koyama, C. H., Júnior, M. L. B., & Seelaender, M. C. L. (2009) · PubMed · doi:10.1016/j.cyto.2008.10.018 · Cited by 100 · see citing works
Endurance training in rats with chronic heart failure induced by myocardial infarction.
Musch, T. I., Moore, R. L., Leathers, D. J., Bruno, A., & ZELIS, R. F. (1986) · Circulation · doi:10.1161/01.cir.74.2.431 · Cited by 94 · see citing works
Regulation of inflammation in the adipose tissue in cancer cachexia: effect of exercise
Lira, F. S., Neto, J. C. R., Zanchi, N. E., Yamashita, A. S., Lópes, R. D., Lopes, A. C., Júnior, M. L. B., & Seelaender, M. C. L. (2009) · Cell Biochemistry and Function · doi:10.1002/cbf.1540 · Cited by 90 · see citing works
Gomez-Mérino, D., Drogou, C., Guezennec, C. Y., & Chennaoui, M. (2007) · Cytokine · doi:10.1016/j.cyto.2007.07.188 · Cited by 69 · see citing works
Effect of endurance training upon lipid metabolism in the liver of cachectic tumour‐bearing rats
Lira, F. S., Tavares, F. L., Yamashita, A. S., Koyama, C. H., Alves, M. J., Caperuto, É. C., Júnior, M. L. B., & Seelaender, M. C. L. (2008) · Cell Biochemistry and Function · doi:10.1002/cbf.1495 · Cited by 61 · see citing works
Rämson, R., Jürimäe, J., Jürimäe, T., & Mäestu, J. (2008) · European Journal of Applied Physiology · doi:10.1007/s00421-008-0839-y · Cited by 48 · see citing works
Endurance training restores peritoneal macrophage function in post-MI congestive heart failure rats
Júnior, M. L. B., dos Santos, R. V. T., de Oliveira, E. M., Seelaender, M. C. L., & Rosa, L. F. B. P. C. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00871.2006 · Cited by 41 · see citing works
Exercise as a Time‐conditioning Effector in Chronic Disease: a Complementary Treatment Strategy
Rosa, L. F. B. P. C. (2004) · Evidence-based Complementary and Alternative Medicine · doi:10.1093/ecam/neh018 · Cited by 41 · see citing works
Banzet, S., Koulmann, N., Sanchez, H., Serrurier, B., Peinnequin, A., Alonso, A., & Bigard, X. A. (2006) · Journal of Cellular Physiology · doi:10.1002/jcp.20854 · Cited by 31 · see citing works
Endurance training modulates lymphocyte function in rats with post-MI CHF
BATISTA, M. L., SANTOS, R. V. T., LOPES, R. D., LOPES, A. C., COSTA ROSA, L. F. B. P., & SEELAENDER, M. C. L. (2008) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31815ed6d2 · Cited by 19 · see citing works
Pedersen, B. K. (2007) · American Journal of Lifestyle Medicine · doi:10.1177/1559827607301410 · Cited by 14 · see citing works
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Leal, L. G., Lopes, M. A., & Batista, M. L. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01307 · Cited by 382 · see citing works
Muscle oxygen transport and utilization in heart failure: implications for exercise (in)tolerance
Poole, D. C., Hirai, D. M., Copp, S. W., & Musch, T. I. (2011) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00943.2011 · Cited by 284 · see citing works
Exercise training in chronic heart failure: improving skeletal muscle O2transport and utilization
Hirai, D. M., Musch, T. I., & Poole, D. C. (2015) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00469.2015 · Cited by 159 · see citing works
Exercise as an Anti-inflammatory Therapy for Cancer Cachexia: A Focus on Interleukin-6 Regulation.
Daou, H. (2019) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.00147.2019 · Cited by 74 · see citing works
Hoffman‐Goetz, L., Pervaiz, N., Packer, N. H., & Guan, J. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.05.001 · Cited by 80 · see citing works
“Treadmill training in rats reduced the expression of IL-1b and IL-12 in white adipose tissue, TNF-a, IL-1b, and IL-6 in skeletal muscle, and increased IL-10 in white adipose tissue (Gomez-Merino et al., 2007; Lira et al., 2009a; Lira et al., 2009b).”
Role of vitamin C and E supplementation on IL-6 in response to training
Yfanti, C., Fischer, C. P., Nielsen, S. J., Akerstrom, T. C. A., Nielsen, A. R., Veskoukis, A. S., Kouretas, D., Lykkesfeldt, J., Pilegaard, H., & Pedersen, B. K. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01027.2010 · Cited by 72 · see citing works
Inflammation in cancer cachexia: To resolve or not to resolve (is that the question?)
Seelaender, M. C. L., Júnior, M. L. B., Lira, F. S., Silvério, R., & Fanelli, F. R. (2012) · Clinical Nutrition · doi:10.1016/j.clnu.2012.01.011 · Cited by 65 · see citing works
Oxidative stress and inflammation: liver responses and adaptations to acute and regular exercise
Barcelos, R. P., Royes, L. F. F., González‐Gallego, J., & Bresciani, G. (2017) · Free Radical Research · doi:10.1080/10715762.2017.1291942 · Cited by 65 · see citing works
Skeletal muscle as a therapeutic target for delaying type 1 diabetic complications
Coleman, S. K. (2015) · World Journal of Diabetes · doi:10.4239/wjd.v6.i17.1323 · Cited by 64 · see citing works
Sedentary subjects have higher PAI-1 and lipoproteins levels than highly trained athletes
Lira, F. S., Neto, J. C. R., Lima‐Silva, A. E., Souza, H. A., Caperuto, É. C., Seelaender, M. C. L., Dâmaso, A. R., Oyama, L. M., & dos Santos, R. V. T. (2010) · Diabetology & Metabolic Syndrome · doi:10.1186/1758-5996-2-7 · Cited by 60 · see citing works
“These inflammatory process include increase in plasma the pro-inflammatory cytokines as tumor necrosis factor alpha (TNF-a), plasminogen activator inhibitor type-1 (PAI-1), C-reactive protein (CRP), interleukin 6 (IL-6) and reduction of anti-inflammatory cytokines as interleukin 10 (IL-10) and adiponectin [8-11].”
BackgroundExercise Training Reduces Inflammatory Mediators in the Intestinal Tract of Healthy Older Adult Mice
Packer, N., & Hoffman‐Goetz, L. (2012) · Canadian Journal on Aging / La Revue canadienne du vieillissement · doi:10.1017/s0714980812000104 · Cited by 60 · see citing works
“Moreover, Gomez-Merino et al. ( 2007 ) found that exercise training reduced IL-1 β in rat adipose tissue and skeletal muscle (Lira et al., 2009 ).”
RNA Sequencing of the Exercise Transcriptome in Equine Athletes
Capomaccio, S., Vitulo, N., Supplizi, A. V., Barcaccia, G., Albiero, A., D’Angelo, M., Campagna, D., Valle, G., Felicetti, M., Silvestrelli, M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083504 · Cited by 58 · see citing works
“Strenuous exercise leads to a transient inflammatory status in human athletes [46–49] and model animals [50,51], including the horse [4,7,8].”
BackgroundNicastro, H., Zanchi, N. E., da Luz, C. R., de Moraes, W. M. A. M., de Souza, P. R. M., Filho, M. A. D. S., Chaves, D. F. S., Medeiros, A., Brum, P. C., Dardevet, D. P., et al. (2011) · Nutrition · doi:10.1016/j.nut.2011.08.008 · Cited by 54 · see citing works
“our group [31–33].”
Shamsi, M. M., Hassan, Z. H., Gharakhanlou, R., Quinn, L. S., Azadmanesh, K., Baghersad, L., Isanejad, A., & Mahdavi, M. (2013) · Endocrine · doi:10.1007/s12020-013-0038-4 · Cited by 54 · see citing works
Lira, F. S., Neto, J. C. R., Antunes, B. M., & Fernandes, R. A. (2014) · Current Diabetes Reviews · doi:10.2174/1573399810666141122210135 · Cited by 50 · see citing works
“, obesity, cancer cachexia, diabetes, sleep deprivation] [35-38].”
Lavratti, C., Dorneles, G. P., Pochmann, D., Peres, A., Bard, A. L., Schipper, L. L., Lago, P. D., Wagner, L. C., & Elsner, V. R. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.10.021 · Cited by 48 · see citing works
James, G., Millecamps, M., Stone, L. S., & Hodges, P. W. (2018) · Spine · doi:10.1097/brs.0000000000002656 · Cited by 47 · see citing works
Lisio, M. D., Baker, J. M., & Parise, G. (2012) · Experimental Hematology · doi:10.1016/j.exphem.2012.10.003 · Cited by 46 · see citing works
Importance of exercise immunology in health promotion
Rosa, J. C., Lira, F., de Mello, M. D., & Santos, R. T. (2011) · Amino Acids · doi:10.1007/s00726-010-0786-x · Cited by 44 · see citing works
“In the soleus, IL-1b, TNF-a, and IL-10 protein levels were similarly decreased in trained in relation to sedentary rats, while IL-6 expression was not affected by the training protocol (Lira et al. 2009c).”
InfluentialCechella, J. L., Leite, M. R., Dobrachinski, F., da Rocha, J. T., de Carvalho, N. R., Duarte, M. M. M. F., Soares, F. A. A., Bresciani, G., Royes, L. F. F., & Zeni, G. R. (2014) · Amino Acids · doi:10.1007/s00726-014-1679-1 · Cited by 43 · see citing works
“In this context, the mechanisms by which a moderate-intensity exercise or caffeine exerts beneficial effects on cytokines have been reported (Pedersen and Hoffman-Goetz 2000; Lira et al. 2009; Petersen and Pedersen 2005; Lv et al. 2010; Yun et al. 2008).”
BackgroundBenatti, F. B. (2011) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s12143 · Cited by 39 · see citing works
Zanchi, N. E., Lira, F. S., Filho, M. A. D. S., Neto, J. C. R., Carvalho, C. R. D. O., Seelaender, M. C. L., dos Santos, R. V. T., & Lancha, A. H. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1456-0 · Cited by 37 · see citing works
“Regular physical activity, especially aerobic exercise, has been shown to decrease the production of pro-inXammatory cytokines in plasma and tissues (Pedersen and Saltin 2006; Lira et al. 2009a; Rosa Neto et al. 2009).”
BackgroundIsanejad, A., صراف, ز. ح., Mahdavi, M., Gharakhanlou, R., Shamsi, M. M., & Paulsen, G. (2015) · Cytokine · doi:10.1016/j.cyto.2015.03.013 · Cited by 36 · see citing works
“Moreover, exercise training may decrease resting levels of cytokines such as IL-1b, IL-6 and TNFa, but increase cytokines such as IL-1ra and IL-10 [14,15].”
BackgroundInfluentialCoelho‐Júnior, H. J., Gambassi, B. B., Diniz, T. A., Fernandes, I. M. D. C., Caperuto, É. C., Uchida, M. C., Lira, F. S., & Rodrigues, B. (2016) · Mediators of Inflammation · doi:10.1155/2016/3957958 · Cited by 36 · see citing works
Hovanloo, F., Arefirad, T., & Ahmadizad, S. (2013) · Journal of Diabetes & Metabolic Disorders · doi:10.1186/2251-6581-12-22 · Cited by 35 · see citing works
Caffeine Intake May Modulate Inflammation Markers in Trained Rats
Barcelos, R. P., Souza, M. A., Amaral, G. P., Stefanello, S. T., Bresciani, G., Fighera, M. R., Soares, F. A. A., & Barbosa, N. V. (2014) · Nutrients · doi:10.3390/nu6041678 · Cited by 33 · see citing works
“In animal models, chronic exercise has been attributed a key role in tissue homeostasis, associated with both increased antioxidant defenses and aerobic metabolism [7] and decreased liver inflammation [8], as well as the stimulation of tissue turnover [9,10].”
BackgroundResultCappelli, K., Felicetti, M., Capomaccio, S., Nocelli, C., Silvestrelli, M., & Supplizi, A. V. (2012) · The Veterinary Journal · doi:10.1016/j.tvjl.2012.07.021 · Cited by 32 · see citing works
“The beneficial effects of chronic training may be severely disrupted by major effort, although this effect is overcome in <24 h in well-trained subjects, suggesting that specific training may increase adaptive responses to exercise (Lira et al., 2009; Capomaccio et al., 2010).”
BackgroundVilela, T. C., Effting, P. S., Pedroso, G. S., Farias, H. R., Paganini, L., Sorato, H. R., Nesi, R. T., de Andrade, V. M., & Pinho, R. A. (2018) · Experimental Gerontology · doi:10.1016/j.exger.2018.02.014 · Cited by 30 · see citing works
Saitou, K., Tokunaga, M., Yoshino, D., Sakitani, N., Maekawa, T., Ryu, Y., Nagao, M., Nakamoto, H., Saito, T., Kawanishi, N., et al. (2018) · Clinical Science · doi:10.1042/cs20180432 · Cited by 30 · see citing works
Shamsi, M. M., Mahdavi, M., Quinn, L. S., Gharakhanlou, R., & Isanegad, A. (2016) · Cell Stress and Chaperones · doi:10.1007/s12192-016-0703-7 · Cited by 30 · see citing works
Leal, L. G., Lopes, M. A., Peres, S. B., & Júnior, M. L. B. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2020.570170 · Cited by 30 · see citing works
Al‐Nassan, S., Fujita, N., Kondo, H., Murakami, S., & Fujino, H. (2012) · ACTA HISTOCHEMICA ET CYTOCHEMICA · doi:10.1267/ahc.12023 · Cited by 28 · see citing works
“Exercise training in moderate intensity can have an influence on skeletal muscles to secrete cytokines in healthy rats [22].”
BackgroundResultInfluentialEffect of vitamin E succinate on inflammatory cytokines induced by high-intensity interval training
Sarir, H., Emdadifard, G., Farhangfar, H., & TaheriChadorneshin, H. (2015) · Journal of Research in Medical Sciences · doi:10.4103/1735-1995.172986 · Cited by 26 · see citing works
“[11] IL-6 IL-6 expressed more in fast twitch than in slow twitch.”
InfluentialCapomaccio, S., Cappelli, K., Barrey, É., Felicetti, M., Silvestrelli, M., & Verini‐Supplizi, A. (2010) · Animal Genetics · doi:10.1111/j.1365-2052.2010.02129.x · Cited by 25 · see citing works
“…the liver, muscles, and joints, but after chronic exercise training, the acute-phase reaction induced by a single exercise session is modified, and the acute inflammatory response at the systemic level is attenuated, inducing changes that favour an anti-inflammatory milieu (Lira et al. 2009).”
BackgroundRecovery of Damaged Skeletal Muscle in mdx Mice through Low-intensity Endurance Exercise
Frinchi, M., Macaluso, F., Licciardi, A., Perciavalle, V., Coco, M., Belluardo, N., Morici, G., & Mudò, G. (2013) · International Journal of Sports Medicine · doi:10.1055/s-0033-1343405 · Cited by 23 · see citing works
Ramos, L., Marcos, R. L., da Silva, R. T., Pallota, R. C., Magacho, T., Mafra, F. F. P., Macedo, M. M., Carvalho, R. L. D. P., Bjordal, J. M., & Lopes‐Martins, R. Á. B. (2018) · Photomedicine and Laser Surgery · doi:10.1089/pho.2018.4473 · Cited by 19 · see citing works
“22,24 In our study, we observed that laser irradiation was able to modulate the production of TNF-a to the basal level.”
Tunç-Ata, M., Turgut, G., Dalyanoğlu, M. M., & Turgut, S. (2017) · Journal of Exercise Rehabilitation · doi:10.12965/jer.1734920.490 · Cited by 16 · see citing works
“In addition other researcher show that IL-6 expression was not affected by the training protocol (Lira et al., 2009).”
BackgroundYeo, D., Zhang, T., Liu, T., Zhang, Y., Kang, C., & Ji, L. L. (2021) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2021.108902 · Cited by 16 · see citing works
Effects of exercise and antioxidant supplementation on endothelial gene expression
Matsumoto, A., Mason, S. R., Flatscher‐Bader, T., Ward, L. C., Marsh, S. A., Wilce, P. A., Fassett, R. G., de Haan, J. B., & Coombes, J. S. (2011) · International Journal of Cardiology · doi:10.1016/j.ijcard.2010.12.104 · Cited by 16 · see citing works
Cancer Cachexia: Underlying Mechanisms and Potential Therapeutic Interventions
Directo, D., & Lee, S.-R. (2023) · Metabolites · doi:10.3390/metabo13091024 · Cited by 12 · see citing works
“In exploring the link between inflammation and cachexia-induced muscle wasting, studies have shown that moderate-intensity endurance exercise can down-regulate TNF-α , which plays pivotal roles in inflammation onset and regulation [288].”
BackgroundT lymphocytes and muscle condition act like seeds and soil in a murine polymyositis model
Okiyama, N., Sugihara, T., Oida, T., Ohata, J., Yokozeki, H., Miyasaka, N., & Kohsaka, H. (2012) · Arthritis & Rheumatism · doi:10.1002/art.34629 · Cited by 15 · see citing works
Milton, L. K., Patton, T., O’Keeffe, M. A., Oldfield, B. J., & Foldi, C. J. (2022) · International Journal of Eating Disorders · doi:10.1002/eat.23705 · Cited by 14 · see citing works
“For example, 362 chronic or exhaustive exercise in rats both increases cytokine concentrations in skeletal muscle 363 and reduces concentrations in adipose tissue [73, 74], whereas moderate exercise reduces 364 expression of inflammatory cytokines in skeletal muscle [75] and in serum [76].”
BackgroundHucik, B., Lovell, A. J., Hoecht, E. M., Cervone, D. T., Mutch, D. M., & Dyck, D. J. (2021) · Adipocyte · doi:10.1080/21623945.2021.1945787 · Cited by 14 · see citing works
“Exercise acutely induces a stress response in activated muscle, such as increasing reactive oxygen species (ROS) production [32], triggering pathways that results in numerous physiological adaptations including increased mitochondrial biogenesis [33] and reduced inflammatory cytokine production [34].”
BackgroundAcute exercise activates myocardial nuclear factor kappa B
Balan, M., & Locke, M. (2010) · Cell Stress and Chaperones · doi:10.1007/s12192-010-0217-7 · Cited by 13 · see citing works
“In support of this, exercise training is known to provide systemic anti-inflammatory effects (Lira et al. 2009), although the mechanism for this remains unclear.”
BackgroundThe effects of exercise training and acute exercise duration on plasma folate and vitamin B12
Kim, Y., Hwang, J. H., & Cho, Y.-O. (2016) · Nutrition Research and Practice · doi:10.4162/nrp.2016.10.2.161 · Cited by 13 · see citing works
“Exercise training induces adaptations to stress during exercise and plays a key role in homeostasis related to an increase in aerobic metabolism [8-9].”
BackgroundStress biomarker responses to different protocols of forced exercise in chronically stressed rats
Radahmadi, M., Alaei, H., Sharifi, M. R., & Hosseini, N. (2016) · Journal of Bodywork and Movement Therapies · doi:10.1016/j.jbmt.2016.05.002 · Cited by 12 · see citing works
Khemraj, P., Kuznyetsova, A., & Hood, D. A. (2025) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2025.101049 · Cited by 11 · see citing works
Wunram, H. L., Oberste, M., Hamacher, S., Neufang, S., Grote, N., Krischer, M., Bloch, W., Schönaü, E., Bender, S., & Fricke, O. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18126527 · Cited by 11 · see citing works
“and Smart and colleagues also commented that regular exercise reduced TNF-α levels [44].”
BackgroundAcute Changes in Interleukin-6 Level During Four Days of Long-Distance Walking
Soares, V., de Avelar, I. S., Venâncio, P. E. M., Pires-Oliveira, D. A. D. A., Silva, P. H. D. A., Borges, A. R., Fonseca, G. P. E. F., & Noll, M. A. (2020) · Journal of Inflammation Research · doi:10.2147/jir.s281113 · Cited by 12 · see citing works
Regular moderate exercise training can alter the urinary excretion of thiamin and riboflavin
Kim, Y., Choi, J. Y., & Cho, Y.-O. (2015) · Nutrition Research and Practice · doi:10.4162/nrp.2015.9.1.43 · Cited by 9 · see citing works
“Exercise training also induces adaptations to stress during exercise and plays a key role in homeostasis associated with an increase in aerobic metabolism [8-10].”
BackgroundSumi, K., Ashida, K., & Nakazato, K. (2020) · Experimental Physiology · doi:10.1113/ep088622 · Cited by 7 · see citing works
“Also, intense endurance exercise, such as running, includes SSC-type contractions and was reported in a rat study to reduce intramuscular cytokines, including mIL-6 (Lira et al., 2009), and to increase plasma IL-10 (Nunes, Alves, Kessler, & Lago, 2013).”
BackgroundSilva, C. M. S., Vieira, R. C., Trombeta, J. C. D. S., Lima, T. R., Fraga, G. A., Sena, M. D. S., Ávila, E. T. P., Tibana, R. A., Prestes, J., Navalta, J. W., et al. (2016) · Revista Andaluza de Medicina del Deporte · doi:10.1016/j.ramd.2016.02.005 · Cited by 8 · see citing works
Vahdat, H., Mombini, H., Farsani, M. E., Abzadeh, S. A., & Barzegar, H. (2018) · Qom Univ Med Sci J · doi:10.29252/qums.12.2.35 · Cited by 6 · see citing works
Noura, M., Arshadi, S., Zafari, A., & Banaeyfar, A. (2020) · Middle East Journal of Rehabilitation and Health Studies · doi:10.5812/mejrh.99754 · Cited by 6 · see citing works
“In line with the present study, the researchers found that 8 weeks, 5 sessions per week of ET significantly reduced hs-CRP, creatine kinase and malondialdehyde in cardiac muscle of rats poisoned with lead acetate (21) and decreased IL-1β, IL-6, and TNF-α in skeletal muscle tissues of healthy rats (22).”
BackgroundResultBao, Z., Li, Z., Zhao, M., Wang, S., Liu, F., & Wang, H. (2025) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2025.2548009 · Cited by 4 · see citing works
“Notably, after long-term exercise, IL-1β levels decrease significantly, thereby relieving chronic inflammation and enhancing immune homeostasis (Lira et al. 2009; Behboudi and Eizadi 2017).”
Rakowska, A., Biazik, A. K., Sobuś, M., & Cywińska, A. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27052328 · Cited by 4 · see citing works
“This beneficial effect may be disrupted by intense effort; however, it should be overcome in less than 24 h in well-trained individuals, suggesting that specific training may increase adaptive response to exercise [72,73].”
Salomão, R., Neto, I. V. D. S., Ramos, G. V., Tibana, R. A., Durigan, J. L. Q., Pereira, G. B., Franco, O. L., Royer, C., Neves, F. D. A. R., de Carvalho, A. C. A., et al. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.706128 · Cited by 4 · see citing works
“Regarding possible physiological significance, decreased musclederived IL-6 production may work to inhibit the effects of pro-inflammatory cytokines, as well as contributing to glucose homeostasis maintenance and lipid metabolism (Lira et al., 2009; Munoz-Canoves et al., 2013).”
BackgroundZamani, A., Omidi, M., Hemmatfar, A., Salehi, I., & Bazmamoun, H. (2014) · Europe PMC (PubMed Central) · Cited by 4 · see citing works
Patterson, D. C., Birnbaum, A., Matthews, I., & Cortés, C. J. (2025) · Physiological Reports · doi:10.14814/phy2.70519 · Cited by 3 · see citing works
“…including tread-mill training or ladder-climbing, modify levels of pro-inflammatory cytokines (IL-1 β , IL-6, and TNF-α ) and anti-inflammatory factors (IL-10) in rodent hindlimb muscles such as the EDL, soleus, and gastrocnemius (Calegari et al., 2018; Isanejad et al., 2015; Lira et al., 2009).”
Trindade, K. L. G., da Silva, C. J. F. L., Cruz, R. K. S., Vilela, C. F., Simões, J., Coelho, C. S., Filho, J. D. R., Manso, H. E. C. D. C. C., & Filho, H. C. M. (2023) · Open Journal of Veterinary Medicine · doi:10.4236/ojvm.2023.138013 · Cited by 3 · see citing works
Effects of Physical Activity on DNA Methylation and Associations with Breast Cancer
Yu, H., & Irwin, M. L. (2016) · Energy balance and cancer · doi:10.1007/978-3-319-41610-6_11 · Cited by 2 · see citing works
Hoseini, M. A. S., Eizadi, M., Amini, A., & Mirakhori, Z. (2018) · International journal of basic science in medicine · doi:10.15171/ijbsm.2018.20 · Cited by 2 · see citing works
Liu, K., Wang, F., Cui, Z., Liu, S., & Han, X. (2015) · Cytokine · doi:10.1016/j.cyto.2014.12.018 · Cited by 1 · see citing works
The effect of resistance training on skeletal muscle inflammatory factors in diabetic rats
Shamsi, M. M., Fallah, M., & Mahdavi, M. (2014) · KAUMS Journal · Cited by 1 · see citing works
Exercise in the Maintenance of Muscle Mass
Dirks‐Naylor, A. J. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-397155-5.00020-9
Forced-Exercise Dependent Changes in Cellular Immunity: Effects on Experimental Autoimmune Neuritis
Calik, M. W. (2011) · Loyola eCommons (Loyola University of Chicago)
Kim, Y., Hwang, J. H., & Cho, Y.-O. (2016) · Nutrition Research and Practice
윤아람, 권순미, jang, H., 이위, Lee, S. K., Jun, J., Park, H., 이영란, & Lee, W.-L. (2012) · Exercise Science · doi:10.15857/ksep.2012.21.3.355
Yeom, M.-Y., & Cho, Y.-O. (2019) · Nutrition Research and Practice · doi:10.4162/nrp.2019.13.1.17
“Exercise training enables an animal to adapt to stress during exercise and induces a homeostasis that is associated with the increased aerobic metabolism [28,29].”
BackgroundThe Effects of Exercise and Massage on Disuse Muscle Atrophy in Special Focus on Mechanical Stress
(2018) · International Journal of Musculoskeletal Disorders · doi:10.29011/2690-0149.000015
Magalhães, A. J. B., Filho, J. C. S. C., Mariolani, J. R. L., Camargo, R. C. T., Oikawa, S. M., & Belangero, W. D. (2021) · Brazilian Journal of Health Review · doi:10.34119/bjhrv4n2-369
Tatebayashi, D., & Ono, R. (2022) · Springer eBooks · doi:10.1007/978-981-19-6710-8_10
Effects of High-Intensity Interval Exercise on Interleukin 6 Levels in Healthy Male Adolescents
Andiana, O., Yunus, M., Raharjo, S., Putra, U. A. A., & Azidin, R. M. F. R. (2023) · International Journal of Research Publications · doi:10.47119/ijrp10013611120235613
HEPATIC AND SKELETAL MUSCLE TISSUE IMMUNOMETABOLISM IN TRAINED RATS
Magalhães, A. J. B., Filho, J. C. S. C., Mariolani, J. R. L., Camargo, R. C. T., Oikawa, S. M., & Belangero, W. D. (2023) · Revista Brasileira de Medicina do Esporte · doi:10.1590/1517-8692202430022023_0219i
IMUNOMETABOLISMO TECIDUAL HEPÁTICO E MUSCULAR ESQUELÉTICO DE RATOS TREINADOS
Magalhães, A. J. B., Filho, J. C. S. C., Mariolani, J. R. L., Camargo, R. C. T., Oikawa, S. M., & Belangero, W. D. (2023) · Revista Brasileira de Medicina do Esporte · doi:10.1590/1517-8692202430022023_0219p
Cornish, S. M., & Peralta-Huertas, J. (2026) · Biomolecules · doi:10.3390/biom16060850
“…demonstrated skeletal muscle-specific adaptations where a significant decrease was noted in several myokines in the extensor digitorum longus muscle, including IL-6; however, in the soleus skeletal muscle, IL-6 was the only myokine to remain unchanged in response to the exercise training [103].”
- Authors
- Lira, F. S., Koyama, C. H., Yamashita, A. S., Rosa, J. C., Zanchi, N. E., Batista, M. L., & Seelaender, M. C.
- Affiliations
- Universidade de São Paulo (BR)
- Corresponding author
- Seelaender, Marília C.
- Venue
- Cell Biochemistry and Function
- Publisher
- Wiley
- Published
- 2009-08-13
- Volume
- 27
- Issue
- 7
- Pages
- 458-461
- ISSN
- 0263-6484 (ISSN-L)
- 1099-0844
- OpenAlex
- W2038134522
- Cited by
- 82
- References
- 29
- Citations by year
- 2026: 2 · 2025: 3 · 2023: 5 · 2022: 2 · 2021: 7 · 2020: 3 · 2019: 2 · 2018: 9 · 2017: 2 · 2016: 8 · 2015: 6 · 2014: 5 · 2013: 4 · 2012: 9
- FWCI
- 8.15
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cell Biochemistry and Function (publishedVersion)
- PubMed (publishedVersion)
- Scientific Electronic Library Online (São Paulo Research Foundation, Latin American and Caribbean Center on Health Sciences Information, Conselho Nacional de Desenvolvimento Científico e Tecnológico) (publishedVersion)
- Topics
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Keywords
- exercise training, skeletal muscle, cytokines, interleukin-6, TNF-α, IL-1β, IL-10, endurance training, muscle inflammation, muscle fiber composition, extensor digitorum longus, soleus muscle, aerobic exercise
- MeSH terms
- Animals, Health, Male, Physical Conditioning, Animal, Cytokines, Rats, Wistar, Muscle, Skeletal, Rats
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