Dual Role of Interleukin-6 in Regulating Insulin Sensitivity in Murine Skeletal Muscle

Nieto-Vazquez, Iria; Fernández-Veledo, Sonia; de Alvaro, Cristina; Lorenzo, Margarita

doi:10.2337/db07-1062

Cited by 209Adipokines, Inflammation, and Metabolic DiseasesMetabolism, Diabetes, and CancerCytokine Signaling Pathways and Interactions

Dual Role of Interleukin-6 in Regulating Insulin Sensitivity in Murine Skeletal Muscle

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Nieto-Vazquez, Iria, Fernández-Veledo, Sonia, de Alvaro, Cristina, Lorenzo, Margarita·2008·Diabetes

DOI 10.2337/db07-1062PMC PMC2584126

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Abstract

OBJECTIVE—Cytokines are elevated in various insulin-resistant states, including type 2 diabetes and obesity, although the contribution of interleukin-6 (IL-6) in the induction of these diseases is controversial. RESEARCH DESIGN AND METHODS—We analyzed the impact of IL-6 on insulin action in murine primary myocytes, skeletal muscle cell lines, and mice (wild type and protein-tyrosine phosphatase 1B [PTP1B] deficient). RESULTS—IL-6 per se increased glucose uptake by activating serine/threonine protein kinase 11 (LKB1)/AMP-activated protein kinase/protein kinase B substrate of 160 kDa (AS160) pathway. A dual effect on insulin action was observed when myotubes and mice were exposed to this cytokine: additive with short-term insulin (increased glucose uptake and systemic insulin sensitivity) but chronic exposure produced insulin resistance (impaired GLUT4 translocation to plasma membrane and defects in insulin signaling at the insulin receptor substrate 1 [IRS-1] level). Three mechanisms seem to operate in IL-6–induced insulin resistance: activation of c-Jun NH2-terminal kinase 1/2 (JNK1/2), accumulation of suppressor of cytokine signaling 3 (socs3) mRNA, and an increase in PTP1B activity. Accordingly, silencing JNK1/2 with either small interfering RNA or chemical inhibitors impaired phosphorylation of IRS-1 (Ser307), restored insulin signaling, and normalized insulin-induced glucose uptake in myotubes. When using a pharmacological approach, liver X receptor agonists overcome IL-6–induced insulin resistance by producing downregulation of socs3 and ptp1b gene expression. Finally, the lack of PTP1B confers protection against IL-6–induced insulin resistance in skeletal muscle in vitro and in vivo, in agreement with the protection against the IL-6 hyperglycemic effect observed on glucose and insulin tolerance tests in adult male mice. CONCLUSIONS—These findings indicate the important role of IL-6 in the pathogenesis of insulin resistance and further implicate PTP1B as a potential therapeutic target in the treatment of type 2 diabetes.

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Chronic treatment with IL-6 induces insulin resistance via mechanisms involving protein-tyrosine phosphatase 1B, JNK activation and SOCS3-mediated inhibition of insulin signaling, while acute exposure enhances insulin-stimulated glucose uptake via the LKB1/AMPK/TBC1D4 pathway.
“The following year, Nieto-Vazquez et al. [166] found that the differential effects of IL-6 may be due to the amount of exposure to the cytokine, whereby, chronic treatment induces insulin resistance via mechanisms involving protein-tyrosine phosphatase 1B, JNK activation and SOCS3-mediated inhibition of insulin signaling, while acute exposure enhances insulin-stimulated glucose uptake via the LKB1”
From AMPK and Exercise: Glucose Uptake and Insulin Sensitivity (2013) · cites this paper as [166]

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Retracted
Protein–Tyrosine Phosphatase 1B–Deficient Myocytes Show Increased Insulin Sensitivity and Protection Against Tumor Necrosis Factor-α–Induced Insulin Resistance
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ORIGINAL ARTICLE Dual Role of Interleukin-6 in Regulating Insulin Sensitivity in Murine Skeletal Muscle
Nieto-vazquez, I., Fernández‐Veledo, S., Alvaro, C. D., & Lorenzo, M. (2013)
Self-citation
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 · see citing works
Direct Cross-talk of Interleukin-6 and Insulin Signal Transduction via Insulin Receptor Substrate-1 in Skeletal Muscle Cells
Weigert, C., Hennige, A. M., Lehmann, R., Brodbeck, K., Baumgärtner, F., Schaüble, M., Häring, H. U., & Schleicher, E. D. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m509782200 · Cited by 140 · see citing works
Mechanism of interleukin-6 induced insulin resistance in 3T3-L1 adipocytes
Lulu, C. (2007) · Zhongguo bingli shengli zazhi
Short-term infusion of interleukin-6 does not induce insulin resistance in vivo or impair insulin signalling in rats
Sopasakis, V. R., Larsson, B.-M., Johansson, A., Holm�ng, A., & Smith, U. (2004) · Diabetologia · doi:10.1007/s00125-004-1544-y · Cited by 39 · see citing works

Authors: Nieto-Vazquez, I., Fernández-Veledo, S., de Alvaro, C., & Lorenzo, M.
Affiliations: 1Department of Biochemistry and Molecular Biology II, Faculty of Pharmacy, Complutense University, Madrid, Spain
Universidad Complutense de Madrid (ES)
Corresponding author: Lorenzo, Margarita
Venue: Diabetes
Publisher: American Diabetes Association
Published: 2008-12-01
Volume: 57
Issue: 12
Pages: 3211-3221
ISSN: 0012-1797 (ISSN-L)
1939-327X
DOI: 10.2337/db07-1062
PMC: PMC2584126
OpenAlex: W2104603426
Cited by: 209
References: 52
Citations by year: 2026: 3 · 2024: 4 · 2023: 4 · 2022: 4 · 2021: 6 · 2020: 17 · 2019: 17 · 2018: 14 · 2017: 17 · 2016: 15 · 2015: 16 · 2014: 16 · 2013: 17 · 2012: 9
FWCI: 12.21
Type: journal article
Language: en
Status: Retracted
Update notices: retraction (2020-09-10)
retraction (2020-11-01)
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
Locations: Diabetes (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Funders: Comunidad de Madrid
European Commission
Universidad Rey Juan Carlos
Instituto de Salud Carlos III
Topics: Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Health Sciences › Medicine › Oncology › Cytokine Signaling Pathways and Interactions
Keywords: interleukin-6, insulin resistance, skeletal muscle, type 2 diabetes, PTP1B, JNK1/2, SOCS3, IRS-1 phosphorylation, GLUT4 translocation, liver X receptor agonist, glucose uptake, cytokines
MeSH terms: Adenylate Kinase, Animals, Animals, Newborn, Biological Transport, Extremities, Glucose, Insulin, Interleukin-6, Polymerase Chain Reaction, Muscle, Skeletal, Protein Transport, Muscle Cells, Myoblasts, RNA, Small Interfering, Proto-Oncogene Proteins c-akt, Glucose Transporter Type 4, Mice

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Dual Role of Interleukin-6 in Regulating Insulin Sensitivity in Murine Skeletal Muscle

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