The DOI matches its Crossref record; 53 of the 53 references it cites were found in a registry or an index.
Exhaustive exercise causes an anti-inflammatory effect in skeletal muscle and a pro-inflammatory effect in adipose tissue in rats
Abstract
It is well known that exhaustive exercise increases serum and skeletal muscle IL-6 concentrations. However, the effect of exhaustive exercise on the concentrations of other cytokines in the muscle and in the adipose tissue is controversial. The purpose of this study was to evaluate the effect of exhaustive exercise on mRNA and protein expression of IL-10, TNF-alpha and IL-6 in different types of skeletal muscle (EDL, soleus) and in two different depots of white adipose tissue (mesenteric-MEAT and retroperitoneal-RPAT). Rats were killed by decapitation immediately (E0 group, n = 6), 2 (E2 group, n = 6) and 6 (E6 group, n = 6) hours after the exhaustion protocol, which consisted of running on a treadmill (approximately 70% VO(2max) for 50 min and then subsequently at an elevated rate that increased at 1 m/min every minute, until exhaustion). The control group (C group, n = 6) was not subjected to exercise. Cytokine protein expression increased in EDL, soleus, MEAT and RPAT from all exercised groups, as detected by ELISA. EDL IL-10 and TNF-alpha expression was higher than that of the soleus. The IL-10/TNF-alpha ratio was increased in the skeletal muscle, especially in EDL, but it was found to be decreased in the adipose tissue. These results show that exhaustive exercise presents a different effect depending on the tissue which is analysed: in the muscle, it induces an anti-inflammatory effect, especially in type 2 fibres, while the pro-inflammatory effect prevails in adipose tissue, possibly contributing to increased lipolysis to provide energy for the exercising muscle.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“(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 Rosa Neto et al., 2009
Citations
Cites
1 retracted
Immunohistochemical detection of interleukin‐6 in human skeletal muscle fibers following exercise
Penkowa, M., Keller, C., Keller, P., Jauffred, S., & Pedersen, B. K. (2003) · The FASEB Journal · doi:10.1096/fj.03-0311fje · Cited by 157
RetractedIL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans
Steensberg, A., Fischer, C. P., Keller, C., Møller, K., & Pedersen, B. K. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00074.2003 · Cited by 1,135
Identity of tumour necrosis factor and the macrophage-secreted factor cachectin
Beutler, B., Greenwald, D., Hulmes, J. D., Chang, M., Pan, Y.-C. E., Mathison, J. C., Ulevitch, R. J., & Cerami, A. (1985) · Nature · doi:10.1038/316552a0 · Cited by 1,132
Pro‐ and anti‐inflammatory cytokine balance in strenuous exercise in humans
Ostrowski, K., Rohde, T., Asp, S., Schjerling, P., & Pedersen, B. K. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.287ad.x · Cited by 1,014
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
Cawthorn, W. P., & Sethi, J. K. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.11.051 · Cited by 833
Suganami, T., Tanimoto-Koyama, K., Nishida, J., Itoh, M., Yuan, X., Mizuarai, S., Kotani, H., Yamaoka, S., Miyake, K., Aoe, S., et al. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000251608.09329.9a · Cited by 820
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
Evidence for a role of developmental genes in the origin of obesity and body fat distribution.
Gesta, S., Blüher, M., Yamamoto, Y., Norris, A., Berndt, J., Kralisch, S., Boucher, J., Lewis, C., & Kahn, C. (2006) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0601752103 · Cited by 635
Insulin resistance in adipose tissue: direct and indirect effects of tumor necrosis factor-α
Ruan, H., & Lodish, H. F. (2003) · Cytokine & Growth Factor Reviews · doi:10.1016/s1359-6101(03)00052-2 · Cited by 541
Differential Effects of Interleukin-6 and -10 on Skeletal Muscle and Liver Insulin Action In Vivo
Kim, H.-J., Higashimori, T., Park, S.-Y., Choi, H., Dong, J., Kim, Y.-J., Noh, H.-L., Cho, Y.-R., Cline, G., Kim, Y.-B., et al. (2004) · Diabetes · doi:10.2337/diabetes.53.4.1060 · Cited by 534
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
A Macrophage Factor Inhibits Adipocyte Gene Expression: An in Vitro Model of Cachexia
Torti, F. M., Dieckmann, B. S., Beutler, B., Cerami, A., & RINGOLD, G. M. (1985) · Science · doi:10.1126/science.3839597 · Cited by 519
Exercise as a Mean to Control Low‐Grade Systemic Inflammation
Mathur, N., & Pedersen, B. K. (2008) · Mediators of Inflammation · doi:10.1155/2008/109502 · Cited by 514
Impact of a Competitive Marathon Race on Systemic Cytokine and Neutrophil Responses
Suzuki, K., Nakaji, S., Yamada, M., Liu, Q., Kurakake, S., Okamura, N., Kumae, T., Umeda, T., & Sugawara, K. (2003) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000048861.57899.04 · Cited by 366
A Survey of Genes Differentially Expressed in Subcutaneous and Visceral Adipose Tissue in Men*
Vohl, M., SLADEK, R. M., Robitaille, J., Gurd, S., Marceau, P., Richard, D., Hudson, T. J., & Tchernof, A. (2004) · Obesity Research · doi:10.1038/oby.2004.153 · Cited by 330
Suzuki, K., Yamada, M., Kurakake, S., Okamura, N., Yamaya, K., Liu, Q., Kudoh, S., Kowatari, K., Nakaji, S., & Sugawara, K. (2000) · European Journal of Applied Physiology · doi:10.1007/s004210050044 · Cited by 315
Schulz, K., Gold, S. M., Witte, J. A., Bartsch, K., Lang, U. E., Hellweg, R., Reer, R., Braumann, K.-M., & Heesen, C. (2004) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2004.06.009 · Cited by 313
Changes in inflammatory mediators following eccentric exercise of the elbow flexors
Hirose, L., Nosaka, K., Newton, M., Laveder, A., Kano, M., Peake, J. M., & Suzuki, K. (2026) · PubMed · doi:10.22029/eir.2004.1607 · Cited by 311
Do regional differences in adipocyte biology provide new pathophysiological insights?
Lafontan, M., & Berlan, M. (2003) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(03)00132-9 · Cited by 303
Hiscock, N. J., Chan, S. M. H., Bisucci, T., Darby, I. A., & Febbraio, M. A. (2004) · The FASEB Journal · doi:10.1096/fj.03-1259fje · Cited by 274
Interleukin-6 Regulates Human Adipose Tissue Lipid Metabolism and Leptin Productionin Vitro
Trujillo, M. E., Sullivan, S., Harten, I. A., Schneider, S. H., Greenberg, A. S., & Fried, S. K. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0603 · Cited by 259
Muscle contractions induce interleukin‐6 mRNA production in rat skeletal muscles
Jonsdottir, I. H., Schjerling, P., Ostrowski, S. R., Asp, S., Richter, E. A., & Pedersen, B. K. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00157.x · Cited by 251
Physiological roles of muscle-derived interleukin-6 in response to exercise
Pedersen, B. K., & Fischer, C. P. (2007) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/mco.0b013e3280ebb5b3 · Cited by 227
The effect of graded exercise on IL‐6 release and glucose uptake in human skeletal muscle
Helge, J. W., Stallknecht, B., Pedersen, B. K., Galbo, H., Kiens, B., & Richter, E. A. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.030437 · Cited by 212
Enhanced release of cytokines, interleukin-2 receptors, and neopterin after long-distance running
Sprenger, H., Jacobs, C., Nain, M., Gressner, A. M., Prinz, H., Wesemann, W., & Gemsa, D. (1992) · Clinical Immunology and Immunopathology · doi:10.1016/0090-1229(92)90012-d · Cited by 195
IL-6 signalling in exercise and disease
Pedersen, B. K. (2007) · Biochemical Society Transactions · doi:10.1042/bst0351295 · Cited by 193
Immunologic Mediators as Parameters of the Reaction to Strenuous Exercise
Northoff, H., & Berg, A. (1991) · International Journal of Sports Medicine · doi:10.1055/s-2007-1024743 · Cited by 186
Changes in markers of muscle damage, inflammation and HSP70 after an Ironman triathlon race
Suzuki, K., Peake, J. M., Nosaka, K., Okutsu, M., Abbiss, C. R., Suriano, R., Bishop, D. J., Quod, M. J., Lee, H., Martin, D. T., et al. (2006) · European Journal of Applied Physiology · doi:10.1007/s00421-006-0296-4 · Cited by 179
Raue, U., Slivka, D. R., Jemioło, B., Hollon, C. J., & Trappe, S. W. (2007) · The Journals of Gerontology Series A · doi:10.1093/gerona/62.12.1407 · Cited by 176
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
Chan, S. M. H., Carey, A. L., Watt, M. J., & Febbraio, M. A. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00030.2004 · Cited by 158
Mastorakos, G. P., & Pavlatou, M. G. (2005) · Hormone and Metabolic Research · doi:10.1055/s-2005-870426 · Cited by 151
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 138
Starkie, R. L., Angus, D. J., Rolland, J. M., Hargreaves, M., & Febbraio, M. A. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-1-00647.x · Cited by 131
Interleukin-10-mediated inhibition of free radical generation in macrophages
Dokka, S., Shi, X., Leonard, S. S., Wang, L., Castranova, V., & Rojanasakul, Y. (2001) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.2001.280.6.l1196 · Cited by 126
Interplay of TNF-α and IL-10 in regulating oxidative stress in isolated adult cardiac myocytes
Kaur, K., Sharma, A. K., Dhingra, S., & Singal, P. K. (2006) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2006.08.005 · Cited by 123
Muscle Cytokine mRNA Changes after 2.5 h of Cycling: Influence of Carbohydrate
NIEMAN, D. C., DAVIS, J. M., HENSON, D. A., GROSS, S. J., DUMKE, C. L., UTTER, A. C., VINCI, D. M., CARSON, J. A., BROWN, A., MCANULTY, S. R., et al. (2005) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000175054.99588.b1 · Cited by 122 · cited 1×
“Since the Wrst study in 1991 (NorthoV and Berg 1991), several studies have consistently reported that IL-6 concentration increases in response to acute exercise (Suzuki et al. 2000; Nieman et al. 2005 ).”
BackgroundCytokine production and hospital mortality in patients with sepsis-induced stress hyperglycemia
Λεωνίδου, Λ., Mouzaki, A., Michalaki, M. A., Delastic, A., Kyriazopoulou, V. E., Bassaris, H. P., & Gogos, C. A. (2007) · Journal of Infection · doi:10.1016/j.jinf.2007.05.177 · Cited by 116
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
Self-citationHepatosplanchnic clearance of interleukin-6 in humans during exercise
Febbraio, M. A., Ott, P., Nielsen, H. B., Steensberg, A., Keller, C., Krustrup, P., Secher, N. H., & Pedersen, B. K. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00134.2003 · Cited by 85
Physiological specialisation of adipose tissue
Pond, C. M. (1999) · Progress in Lipid Research · doi:10.1016/s0163-7827(99)00003-x · Cited by 84
Camus, G., Nys, M., Poortmans, J.-R., Venneman, I., Monfils, T., Deby-Dupont, G. P., Juchmès-Ferir, A., Deby, C. M. T., Lamy, M., & Duchateau, J. (1998) · European Journal of Applied Physiology · doi:10.1007/s004210050474 · Cited by 77
Tumor necrosis factor-α promotes the accumulation of neutrophils and macrophages in skeletal muscle
Peterson, J. M., Feeback, K. D., Baas, J. H., & Pizza, F. X. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01453.2005 · Cited by 74
Meador, B. M., Krzyszton, C. P., Johnson, R. W., & Huey, K. A. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01079.2007 · Cited by 72
Gomez-Mérino, D., Drogou, C., Guezennec, C. Y., & Chennaoui, M. (2007) · Cytokine · doi:10.1016/j.cyto.2007.07.188 · Cited by 69
Enevoldsen, L. H., Stallknecht, B. M., Langfort, J., Petersen, L. N., Holm, C., Ploug, T., & Galbo, H. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.t01-1-00871.x · Cited by 64
Banzet, S., Koulmann, N., Simler, N., Birot, O., Sanchez, H., Chapot, R., Peinnequin, A., & Bigard, X. A. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.089193 · Cited by 56
Park, P.-H., Huang, H., McMullen, M. R., Bryan, K., & Nagy, L. E. (2008) · Journal of Leukocyte Biology · doi:10.1189/jlb.0907631 · Cited by 53
Blood Mononudear Cells Mobilization and Cytokines Secretion During Prolonged Exercises
Bury, T., Louis, R. E., Radermecker, M., & Pirnay, F. (1996) · International Journal of Sports Medicine · doi:10.1055/s-2007-972825 · Cited by 47
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 33
Roher, N., Samokhvalov, V., Dı́az, M., MacKenzie, S. A., Klip, A., & Planas, J. V. (2007) · Endocrinology · doi:10.1210/en.2007-1045 · Cited by 28
IKEDA, M., Ohira, H., Toyama, Y., Katagiri, T., & Sakakibara, B. (2007) · Journal of Clinical Biochemistry and Nutrition · doi:10.3164/jcbn.2007023 · Cited by 4
Cited by
Sorted by citations
Leal, L. G., Lopes, M. A., & Batista, M. L. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01307 · Cited by 382
Role of Interleukin-6 in Vascular Health and Disease
Villar-Fincheira, P., Sanhueza-Olivares, F., Norambuena-Soto, I., Cancino-Arenas, N., Hernandez-Vargas, F., Troncoso, R., Gabrielli, L., & Chiong, M. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.641734 · Cited by 154
The search for exercise factors in humans
Catoire, M., & Kersten, S. (2015) · The FASEB Journal · doi:10.1096/fj.14-263699 · Cited by 137
Exercise training changes IL-10/TNF-α ratio in the skeletal muscle of post-MI rats
Batista Jr., M. L., Rosa, J. C., Lopes, R. D., Lira, F. S., Martins Jr., E., Yamashita, A. S., Brum, P. C., Lancha Jr., A. H., Lopes, A. C., & Seelaender, M. (2010) · Cytokine · doi:10.1016/j.cyto.2009.10.007 · Cited by 117
Self-citationExercise‐induced increases in inflammatory cytokines in muscle and blood of horses
Liburt, N. R., Adams, A. A., Betancourt, A., Horohov, D. W., & McKeever, K. H. (2010) · Equine Veterinary Journal · doi:10.1111/j.2042-3306.2010.00275.x · Cited by 104
Metadata
- Authors
- Rosa Neto, J. C., Lira, F. S., Oyama, L. M., Zanchi, N. E., Yamashita, A. S., Batista, M. L., Oller do Nascimento, C. M., & Seelaender, M.
- Affiliations
- Universidade de São Paulo (BR)
- Universidade Federal de São Paulo (BR)
- Venue
- European Journal of Applied Physiology
- Published
- 2009-05-08
- Volume
- 106
- Issue
- 5
- Pages
- 697-704
- ISSN
- 0020-9376 (ISSN-L)
- 1439-6319
- 1439-6327
- OpenAlex
- W2112842295
- Cited by
- 112
- References
- 53
- Citations by year
- 2025: 5 · 2024: 13 · 2023: 4 · 2022: 4 · 2021: 6 · 2020: 5 · 2019: 2 · 2018: 4 · 2017: 9 · 2016: 6 · 2015: 9 · 2014: 6 · 2013: 10 · 2012: 7
- FWCI
- 9.51
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- European Journal of Applied Physiology (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)
- UNIFESP Institutional Repository (Universidade Federal de São Paulo) (submittedVersion)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Physiology (medical) › Cardiovascular and exercise physiology
- Keywords
- exhaustive exercise, inflammation, skeletal muscle, adipose tissue, IL-10, TNF-α, interleukin-6, cytokine expression, soleus muscle, EDL muscle, mesenteric adipose tissue, retroperitoneal adipose tissue, lipolysis, treadmill running
- MeSH terms
- Adipose Tissue, Animals, Physical Exertion, Inflammation, Lipolysis, Male, Physical Conditioning, Animal, Tumor Necrosis Factor-alpha, Interleukin-6, Interleukin-10, Rats, Wistar, Muscle, Skeletal, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
