Muscle‐derived interleukin‐6: mechanisms for activation and possible biological roles

FEBBRAIO, MARK A.; PEDERSEN, BENTE KLARLUND

doi:10.1096/fj.01-0876rev

Cited by 875Exercise and Physiological ResponsesAdipokines, Inflammation, and Metabolic DiseasesMuscle Physiology and Disorders

Muscle‐derived interleukin‐6: mechanisms for activation and possible biological roles

FEBBRAIO, MARK A., PEDERSEN, BENTE KLARLUND·2002·The FASEB Journal

DOI 10.1096/fj.01-0876rev

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Abstract

It has recently been demonstrated that the marked increase in the systemic concentration of cytokine interleukin‐6 (IL‐6) seen with exercise originates from the contracting limb and that skeletal muscle cells per se are the likely source of the production. This review summarizes the possible mechanisms for activation and biological consequences of muscle‐derived IL‐6. It appears that intramuscular IL‐6 is stimulated by complex signaling cascades initiated by both calcium (Ca 2+ ) ‐dependent and ‐independent stimuli. It also seems likely that skeletal muscle produces IL‐6 to aid in maintaining metabolic homeostasis during periods of altered metabolic demand such as muscular exercise or insulin stimulation. It may do so via local and/or systemic effects. This review also explores the efficacy that IL‐6 may be used as a therapeutic drug in treating metabolic disorders such as obesity, type 2 diabetes, and atherosclerosis.—Febbraio, M. A., Pedersen, B. K. Muscle‐derived interleukin 6: mechanisms for activation and possible biological roles. FASEB J. 16, 1335–1347 (2002)

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Increased levels of IL-6 after exercise are followed by increased expression of IL-1ra and IL-10, constituting an anti-inflammatory component and a response to increased circulating IL-6 induced by exercise.
“Increased levels of IL-6 after exercise are followed by increased expression of the IL-1 receptor antagonist (IL-1ra) and IL-10, such adjustment chronically constitutes an anti-inflammatory component and a response to the increase in circulating IL-6 induced by exercise (Febbraio and Pedersen, 2002).”
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 Febbraio and Pedersen, 2002
Interleukin-6 is produced in, and subsequently released from, contracting muscle.
“However, there is also evidence that interleukin-6 is produced in, and subsequently released from, contracting muscle (61,62)”
From Expression of <i>Mfn2</i>, the Charcot-Marie-Tooth Neuropathy Type 2A Gene, in Human Skeletal Muscle (2005) · cites this paper as [62]
The magnitude by which plasma IL-6 increases is related to exercise duration, intensity, and muscle mass involved in the mechanical work.
“The magnitude by which plasma IL-6 increases is related to exercise duration, intensity, and muscle mass involved in the mechanical work [13, 18, 60, 62].”
From Exercise as a Mean to Control Low‐Grade Systemic Inflammation (2008) · cites this paper as [60]
Circulating IL-6 increases in an exponential fashion up to 100 fold in response to exercise and declines in the postexercise period.
“The level of circulating IL-6 increases in an exponential fashion (up to 100 fold) in response to exercise, and declines in the postexercise period [60–62].”
From Exercise as a Mean to Control Low‐Grade Systemic Inflammation (2008) · cites this paper as [60]

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A variety of cytokines and immunologically relevant surface molecules are expressed by normal human skeletal muscle cells under proinflammatory stimuli
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Strenuous exercise decreases the percentage of type 1 T cells in the circulation
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Immunologic Mediators as Parameters of the Reaction to Strenuous Exercise
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Signal transduction through gp130 that is shared among the receptors for the interleukin 6 related cytokine subfamily
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The Differential Effect of Food Intake and β-Adrenergic Stimulation on Adipose-Derived Hormones and Cytokines in Man
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Nitric oxide synthase inhibition reduces leg glucose uptake but not blood flow during dynamic exercise in humans.
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Elderly Humans Show Prolonged In Vivo Inflammatory Activity during Pneumococcal Infections
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The role of elevations in intracellular [Ca2+] in the development of low frequency fatigue in mouse single muscle fibres.
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Exercise-Induced Immunomodulation - Possible Roles of Neuroendocrine and Metabolic Factors
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IL-6 cytokine family and signal transduction: a model of the cytokine system
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Interleukin‐6 production in human subcutaneous abdominal adipose tissue: the effect of exercise
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Insulin stimulation of phosphatidylinositol 3-kinase activity maps to insulin receptor regions required for endogenous substrate phosphorylation.
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Chemokines are elevated in plasma after strenuous exercise in humans
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Phosphatidylinositol-3-kinase in isolated rat adipocytes. Activation by insulin and subcellular distribution.
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Extracellular-regulated kinase 1/2, Jun N-terminal kinase, and c-Jun are involved in NF-kappa B-dependent IL-6 expression in human monocytes.
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Induction of plasma interleukin-6 by circulating adrenaline in the rat
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Effect of carbohydrate ingestion on glucose kinetics during exercise
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Plasma interleukin-6 during strenuous exercise: role of epinephrine
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Anti-gamma interferon and anti-interleukin-6 antibodies affect staphylococcal enterotoxin B-induced weight loss, hypoglycemia, and cytokine release in D-galactosamine-sensitized and unsensitized mice
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Interleukin 1β and interleukin 6, but not tumor necrosis factor α, inhibit insulin-stimulated glycogen synthesis in rat hepatocytes
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Effect of prolonged, submaximal exercise and carbohydrate ingestion on monocyte intracellular cytokine production in humans
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Hypoxemia increases serum interleukin-6 in humans
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Effects of mode and carbohydrate on the granulocyte and monocyte response to intensive, prolonged exercise
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Extracellular-Regulated Kinase 1/2, Jun N-Terminal Kinase, and c-Jun Are Involved in NF-κB-Dependent IL-6 Expression in Human Monocytes
Tuyt, L., Dokter, W. H. A., Birkenkamp, K. U., Koopmans, S., Lummen, C., Kruijer, W., & Vellenga, E. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.8.4893 · Cited by 123 · see citing works
Modification of immune responses to exercise by carbohydrate, glutamine and anti‐oxidant supplements
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Impaired calcium pump function does not slow relaxation in human skeletal muscle after prolonged exercise
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Interleukin-6 Enhances Glucose Transport in 3T3-L1 Adipocytes
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Interleukins and exercise
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Intracellular monocyte and serum cytokine expression is modulated by exhausting exercise and cold exposure
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Interleukin-6 response to exercise and high-altitude exposure: influence of α-adrenergic blockade
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N-3 polyunsaturated fatty acids do not affect cytokine response to strenuous exercise
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Marathon running transiently increases c‐Jun NH2‐terminal kinase and p38γ activities in human skeletal muscle
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Muscle glycogen content affects insulin-stimulated glucose transport and protein kinase B activity
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Constitutive and cytokine-induced production of interleukin-6 by human myoblasts
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Effects of exercise of varying duration on sarcoplasmic reticulum function
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Role of epinephrine in TNF and IL-6 production from isolated perfused rat liver
Liao, J., Keiser, J. A., Scales, W. E., Kunkel, S. L., & Kluger, M. J. (1995) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1995.268.4.r896 · Cited by 98 · see citing works
Lymphocytes and NK cell activity during repeated bouts of maximal exercise
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Effects of Tumor Necrosis Factor-α on Insulin Action in Cultured Human Muscle Cells
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Overexpression of interleukin-6 aggravates viral myocarditis: impaired increase in tumor necrosis factor-alpha.
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Prolonged submaximal eccentric exercise is associated with increased levels of plasma IL-6
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Acute phase levels of C-reactive protein enhance IL-1 β and IL-1ra production by human blood monocytes but inhibit IL-1 β and IL-1ra production by alveolar macrophages
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Glycogen content and excitation‐contraction coupling in mechanically skinned muscle fibres of the cane toad
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Untitled work
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Effect of proinflammatory interleukins on jejunal nutrient transport
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Hepatic glucose production during exercise.
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Local production of human IL-6 promotes insulitis but retards the onset of insulin-dependent diabetes mellitus in non-obese diabetic mice
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The Differential Effect of Food Intake and -Adrenergic Stimulation on Adipose-Derived Hormones and Cytokines in Man
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Outcomes of Adjuvant Radiation Therapy for Breast Cancer in Women With Ataxia-Telangiectasia Mutations
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Interleukin 6 stimulates hepatic glucose release from prelabeled glycogen pools
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Necrotizing myopathy induced by overexpression of interferon-? in transgenic mice
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Blockade of the p38 Mitogen-activated Protein Kinase Pathway Inhibits Inducible Nitric Oxide Synthase and Interleukin-6 Expression in MC3T3E-1 Osteoblasts
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Stimulation of splanchnic glucose production during exercise in humans contains a glucagon-independent component
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Lack of IL-6 production during exercise in patients with mitochondrial myopathy
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Shifts in nuclear and cytoplasmic nucleic acid content in temperature‐synchronized Tetrahymena pyriformis (HSM)
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Exercise as medicine - evidence for prescribing exercise as therapy in 26 different chronic diseases
Pedersen, B. K., & Saltin, B. (2015) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1111/sms.12581 · Cited by 3,514 · see citing works
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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
Self-citation
Muscle as an Endocrine Organ: Focus on Muscle-Derived Interleukin-6
Pedersen, B. K., & Febbraio, M. A. (2008) · Physiological Reviews · doi:10.1152/physrev.90100.2007 · Cited by 2,388 · see citing works
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Inflammation in obesity, diabetes, and related disorders
Rohm, T. V., Meier, D. T., Olefsky, J. M., & Donath, M. Y. (2022) · Immunity · doi:10.1016/j.immuni.2021.12.013 · Cited by 2,066 · see citing works
So depression is an inflammatory disease, but where does the inflammation come from?
Berk, M., Williams, L. J., Jacka, F. N., O’Neil, A., Pasco, J. A., Moylan, S., Allen, N. B., Stuart, A. L., Hayley, A. C., Byrne, M. L., et al. (2013) · BMC Medicine · doi:10.1186/1741-7015-11-200 · Cited by 1,423 · see citing works
Evidence for prescribing exercise as therapy in chronic disease
Pedersen, B. K., & Saltin, B. (2006) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1111/j.1600-0838.2006.00520.x · Cited by 1,384 · see citing works
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Physical activity and depression: towards understanding the antidepressant mechanisms of physical activity
Kandola, A., Ashdown-Franks, G., Hendrikse, J., Sabiston, C. M., & Stubbs, B. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.040 · Cited by 1,309 · see citing works
The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis
Steptoe, A., Hamer, M., & Chida, Y. (2007) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.03.011 · Cited by 1,278 · see citing works
Muscle–Organ Crosstalk: The Emerging Roles of Myokines
Severinsen, M. C. K., & Pedersen, B. K. (2020) · Endocrine Reviews · doi:10.1210/endrev/bnaa016 · Cited by 1,226 · see citing works
“During muscle work, IL-6 is produced by human contracting skeletal muscle and released into the blood (114) in a TNF-independent fashion (115).”
BackgroundSelf-citation
The Effects of Physical Activity on Serum C-Reactive Protein and Inflammatory Markers
Kasapis, C., & Thompson, P. D. (2005) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2004.12.077 · Cited by 1,149 · see citing works
Interleukin-6 Increases Insulin-Stimulated Glucose Disposal in Humans and Glucose Uptake and Fatty Acid Oxidation In Vitro via AMP-Activated Protein Kinase
Carey, A. L., Steinberg, G. R., Macaulay, S. L., Thomas, W. G., Holmes, A. G., Ramm, G., Prelovsek, O., Hohnen-Behrens, C., Watt, M. J., James, D. E., et al. (2006) · Diabetes · doi:10.2337/db05-1404 · Cited by 898 · see citing works
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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
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Exercise and IL‐6 infusion inhibit endotoxin‐induced TNF‐α production in humans
Starkie, R., Ostrowski, S. R., Jauffred, S., Febbraio, M., & Pedersen, B. K. (2003) · The FASEB Journal · doi:10.1096/fj.02-0670fje · Cited by 790 · see citing works
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Physical activity and muscle-brain crosstalk
Pedersen, B. K. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0174-x · Cited by 772 · see citing works
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Brain-derived neurotrophic factor is produced by skeletal muscle cells in response to contraction and enhances fat oxidation via activation of AMP-activated protein kinase
Matthews, V. B., Åström, M.-B., Chan, M. H. S., Bruce, C. R., Krabbe, K. S., Prelovsek, O., Åkerström, T., Yfanti, C., Broholm, C., Mortensen, O. H., et al. (2009) · Diabetologia · doi:10.1007/s00125-009-1364-1 · Cited by 722 · see citing works
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Adipocytokines in Obesity and Metabolic Disease
Cao, H. (2014) · Journal of Endocrinology · doi:10.1530/joe-13-0339 · Cited by 705 · see citing works
FOXO/4E-BP Signaling in Drosophila Muscles Regulates Organism-wide Proteostasis during Aging
Demontis, F., & Perrimon, N. (2010) · Cell · doi:10.1016/j.cell.2010.10.007 · Cited by 656 · see citing works
Age-related inflammatory cytokines and disease
Brüünsgaard, H., & Pedersen, B. K. (2003) · Immunology and Allergy Clinics of North America · doi:10.1016/s0889-8561(02)00056-5 · Cited by 608 · see citing works
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IL-6-induced skeletal muscle atrophy
Haddad, F., Zaldivar, F., Cooper, D. M., & Adams, G. R. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01026.2004 · Cited by 612 · see citing works
Searching for the exercise factor: is IL-6 a candidate?
Pedersen (2003) · Journal of Muscle Research and Cell Motility · doi:10.1023/a:1026070911202 · Cited by 564 · see citing works
Muscle as a secretory organ
Pedersen, B. K. (2013) · Comprehensive physiology · doi:10.1002/cphy.c120033 · Cited by 516 · see citing works
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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 · see citing works
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AMPK and the biochemistry of exercise: implications for human health and disease
Richter, E. A., & Ruderman, N. B. (2009) · Biochemical Journal · doi:10.1042/bj20082055 · Cited by 481 · see citing works
Inflammation and cardiovascular disease: From mechanisms to therapeutics
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Authors: FEBBRAIO, M. A., & PEDERSEN, B. K.
Affiliations: University of Copenhagen (DK)
ORCID: FEBBRAIO, MARK A.
PEDERSEN, BENTE KLARLUND
Venue: The FASEB Journal
Publisher: Wiley
Published: 2002-09
Volume: 16
Issue: 11
Pages: 1335-1347
ISSN: 0892-6638 (ISSN-L)
1530-6860
DOI: 10.1096/fj.01-0876rev
OpenAlex: W2127647469
Cited by: 875
References: 143
Citations by year: 2026: 18 · 2025: 27 · 2024: 22 · 2023: 30 · 2022: 27 · 2021: 31 · 2020: 38 · 2019: 29 · 2018: 37 · 2017: 38 · 2016: 37 · 2015: 43 · 2014: 46 · 2013: 46 · 2012: 48
FWCI: 6.36
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The FASEB Journal (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Keywords: interleukin-6, skeletal muscle, physical activity, cytokine production, calcium signaling, insulin signaling, metabolic homeostasis, obesity, type 2 diabetes, atherosclerosis, therapeutic drug targets
MeSH terms: Animals, Anti-Inflammatory Agents, Diabetes Mellitus, Type 2, Glucose, Glycogen, Humans, Insulin Resistance, Models, Biological, Monocytes, Signal Transduction, Exercise, Interleukin-6, Muscle, Skeletal, Lipid Metabolism

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Muscle‐derived interleukin‐6: mechanisms for activation and possible biological roles

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