CYTOKINE AND MATRIX METALLOPROTEINASE PROFILE IN THE SKELETAL MUSCLE OF RATS WITH DIET-INDUCED OBESITY

Tetiana Halenova, Oleksandr Rizun, Mariana Kuznietsova, Oksana Lynchak, Nataliia Raksha, Yuriy Prylutskyy


DOI: http://dx.doi.org/10.30970/sbi.2003.890

Abstract


Background. Our previous studies revealed impaired contractile performance of skeletal muscle in diet-induced obesity, accompanied by intramyocellular lipid accumulation and signs of fibrosis. These findings suggest that obesity-related muscle dysfunction may result from activation of pro-fibrotic pathways and imbalance in extracellular matrix turnover driven by chronic low-grade inflammation – a hallmark of obesity pathogenesis. This study aimed to evaluate the effects of long-term high-fat feeding on the cytokine profile and matrix remodeling markers in rat skeletal muscle and to identify possible biochemical mechanisms underlying obesity-related muscle dysfunction.
Materials and Methods. Adult male Wistar rats were fed either a standard chow (6.7 % fat; 15.27 kJ·g-1) or a high-fat diet (38.8 % fat; 28.71 kJ·g-1) for ten weeks. Serum biochemical parameters (total protein, glucose, cholesterol, bilirubin fractions, urea, creatinine, alanine and aspartate aminotransferases, α-amylase, alkaline phosphatase, γ-glutamyltransferase) were analyzed. Cytokines (TNF-α, IL-6, IL-1β, IL-10, IFN-γ), matrix metalloproteinases (MMP-2, MMP-9), and their inhibitor (TIMP-1) were quantified in skeletal muscle homogenates by ELISA.
Results. A high-fat diet produced pronounced alterations in serum biochemical parameters, reflecting profound metabolic dysregulation and systemic impairment of homeostatic control. In skeletal muscle, obesity induced a significant rise in pro-inflammatory cytokines (TNF-α, IL-6, IL-1β, IFN-γ) and a reduction in anti-inflammatory IL-10. These shifts were accompanied by increased MMP-2 and MMP-9 levels and a decline in TIMP-1, suggesting disturbed extracellular matrix turnover and early profibrotic remodeling.
Conclusion. Diet-induced obesity promotes a sustained pro-inflammatory state accompanied by enhanced extracellular matrix remodeling. The imbalance between cytokines, metalloproteinases, and their inhibitor may underlie structural stiffening and decreased contractile efficiency of muscle fibers. A deeper understanding of these cytokine-MMP/TIMP interactions may provide new insights into the mechanisms of obesity-related muscle dysfunction and identify potential targets for maintaining skeletal muscle performance.


Keywords


obesity, skeletal muscle, cytokines, matrix metalloproteinases, extracellular matrix, inflammation, metabolic dysfunction

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Alameddine, H. S., & Morgan, J. E. (2016). Matrix metalloproteinases and tissue inhibitor of metalloproteinases in inflammation and fibrosis of skeletal muscles. Journal of Neuromuscular Diseases, 3(4), 455-473. doi:10.3233/jnd-160183
CrossrefPubMedPMCGoogle Scholar

Babaeijandaghi, F., Paiero, A., Long, R., Tung, L. W., Smith, S. P., Cheng, R., Smandych, J., Kajabadi, N., Chang, C.-K., Ghassemi, A., Kennedy, W. D. M., Soliman, H., Schutz, P. W., & Rossi, F. M. V. (2022). TNFα and IFNγ cooperate for efficient pro- to anti-inflammatory transition of macrophages during muscle regeneration. Proceedings of the National Academy of Sciences, 119(44), e2209976119. doi:10.1073/pnas.2209976119
CrossrefPubMedPMCGoogle Scholar

Bach, D., Naon, D., Pich, S., Soriano, F. X., Vega, N., Rieusset, J., Laville, M., Guillet, C., Boirie, Y., Wallberg-Henriksson, H., Manco, M., Calvani, M., Castagneto, M., Palacín, M., Mingrone, G., Zierath, J. R., Vidal, H., & Zorzano, A. (2005). Expression of Mfn2, the Charcot–Marie–Tooth neuropathy type 2A gene, in human skeletal muscle: effects of type 2 diabetes, obesity, weight loss, and the regulatory role of tumor necrosis factor alpha and interleukin-6. Diabetes, 54(9), 2685-2693. doi:10.2337/diabetes.54.9.2685
CrossrefPubMedGoogle Scholar

Bollinger, L. M. (2017). Potential contributions of skeletal muscle contractile dysfunction to altered biomechanics in obesity. Gait & Posture, 56, 100-107. doi:10.1016/j.gaitpost.2017.05.003
CrossrefPubMedGoogle Scholar

Borovkov, S. B., Boiko, V. S., Paliy, A. P., Borovkova, V. M., Pavlichenko, O. V., & Gerilovich, I. O. (2024). Diagnostic significance of biochemical parameters of blood serum of ponies in obesity. Regulatory Mechanisms in Biosystems, 15(4), 856-861. doi:10.15421/0224123
CrossrefGoogle Scholar

Castillo, Í. M. P., Argilés, J. M., Rueda, R., Ramírez, M., & Pedrosa, J. M. L. (2025). Skeletal muscle atrophy and dysfunction in obesity and type-2 diabetes mellitus: myocellular mechanisms involved. Reviews in Endocrine and Metabolic Disorders, 26(5), 815-836. doi:10.1007/s11154-025-09954-9
CrossrefPubMedPMCGoogle Scholar

Catalán, V., Frühbeck, G., & Gómez-Ambrosi, J. (2018). Inflammatory and oxidative stress markers in skeletal muscle of obese subjects. In G. Frühbeck (Ed.), Obesity: a multidisciplinary approach (pp. 163-189). Elsevier. doi:10.1016/b978-0-12-812504-5.00008-8
CrossrefGoogle Scholar

Cavaliere, G., Cimmino, F., Trinchese, G., Catapano, A., Petrella, L., D'Angelo, M., Lucchin, L., & Mollica, M. P. (2023). From obesity-induced low-grade inflammation to lipotoxicity and mitochondrial dysfunction: altered multi-crosstalk between adipose tissue and metabolically active organs. Antioxidants, 12(6), 1172. doi:10.3390/antiox12061172
CrossrefPubMedPMCGoogle Scholar

Guo, L., Quan, M., Pang, W., Yin, Y., & Li, F. (2023). Cytokines and exosomal miRNAs in skeletal muscle-adipose crosstalk. Trends in Endocrinology & Metabolism, 34(10), 666-681. doi:10.1016/j.tem.2023.07.006
CrossrefPubMedGoogle Scholar

Halenova, T., Raksha, N., Vovk, T., Savchuk, O., Ostapchenko, L., Prylutskyy, Y., Kyzyma, O., Ritter, U., & Scharff, P. (2018). Effect of C60 fullerene nanoparticles on the diet-induced obesity in rats. International Journal of Obesity, 42(12), 1987-1998. doi:10.1038/s41366-018-0016-2
CrossrefPubMedGoogle Scholar

Jia, G., & Sowers, J. R. (2019). Increased fibro-adipogenic progenitors and intramyocellular lipid accumulation in obesity-related skeletal muscle dysfunction. Diabetes, 68(1), 18-20. doi:10.2337/dbi18-0047
CrossrefPubMedPMCGoogle Scholar

Kistner, T. M., Pedersen, B. K., & Lieberman, D. E. (2022). Interleukin 6 as an energy allocator in muscle tissue. Nature Metabolism, 4(2), 170-179. doi:10.1038/s42255-022-00538-4
CrossrefPubMedGoogle Scholar

Lee, H., Ha, T. Y., Jung, C. H., Nirmala, F. S., Park, S.-Y., Huh, Y. H., & Ahn, J. (2021). Mitochondrial dysfunction in skeletal muscle contributes to the development of acute insulin resistance in mice. Journal of Cachexia, Sarcopenia and Muscle, 12(6), 2123-2138. doi:10.1002/jcsm.12794
CrossrefPubMedPMCGoogle Scholar

Li, Y., Guo, W., Li, H., Wang, Y., Liu, X., & Kong, W. (2024). The change of skeletal muscle caused by inflammation in obesity as the key path to fibrosis: thoughts on mechanisms and intervention strategies. Biomolecules, 15(1), 20. doi:10.3390/biom15010020
CrossrefPubMedPMCGoogle Scholar

Lin, W., Song, H., Shen, J., Wang, J., Yang, Y., Yang, Y., Cao, J., Xue, L., Zhao, F., Xiao, T., & Lin, R. (2023). Functional role of skeletal muscle-derived interleukin-6 and its effects on lipid metabolism. Frontiers in Physiology, 14, 1110926. doi:10.3389/fphys.2023.1110926
CrossrefPubMedPMCGoogle Scholar

Mengeste, A. M., Rustan, A. C., & Lund, J. (2021). Skeletal muscle energy metabolism in obesity. Obesity, 29(10), 1582-1595. doi:10.1002/oby.23227
CrossrefPubMedGoogle Scholar

Mika, A., & Sledzinski, T. (2016). Alterations of specific lipid groups in serum of obese humans: a review. Obesity Reviews, 18(2), 247-272. doi:10.1111/obr.12475
CrossrefPubMedGoogle Scholar

Muñoz-Cánoves, P., Scheele, C., Pedersen, B. K., & Serrano, A. L. (2013). Interleukin-6 myokine signaling in skeletal muscle: a double-edged sword? The FEBS Journal, 280(17), 4131-4148. doi:10.1111/febs.12338
CrossrefPubMedPMCGoogle Scholar

Musale, V., Wasserman, D. H., & Kang, L. (2023). Extracellular matrix remodelling in obesity and metabolic disorders. Life Metabolism, 2(4), load021. doi:10.1093/lifemeta/load021
CrossrefPubMedPMCGoogle Scholar

Nozdrenko, D. M., Rizun, O. V., Kalmukova, O. O., Kuznietsova, M. Yu., Raksha, N. G., Halenova, T. I., Lynchak, O. V., & Prylutskyy, Yu. I. (2026). Indicators of musculus soleus contractility disorder in obese rats. The Ukrainian Biochemical Journal, 98(1), 88-97. doi:10.15407/ubj98.01.088
Crossref

Rahemi, H., Nigam, N., & Wakeling, J. M. (2015). The effect of intramuscular fat on skeletal muscle mechanics: implications for the elderly and obese. Journal of the Royal Society Interface, 12(109), 20150365. doi:10.1098/rsif.2015.0365
CrossrefPubMedPMCGoogle Scholar

Ruiz-Ojeda, F. J., Méndez-Gutiérrez, A., Aguilera, C. M., & Plaza-Díaz, J. (2019). Extracellular matrix remodeling of adipose tissue in obesity and metabolic diseases. International Journal of Molecular Sciences, 20(19), 4888. doi:10.3390/ijms20194888
CrossrefPubMedPMCGoogle Scholar

Soltis, A. R., Kennedy, N. J., Xin, X., Zhou, F., Ficarro, S. B., Yap, Y. S., Matthews, B. J., Lauffenburger, D. A., White, F. M., Marto, J. A., Davis, R. J., & Fraenkel, E. (2017). Hepatic dysfunction caused by consumption of a high-fat diet. Cell Reports, 21(11), 3317-3328. doi:10.1016/j.celrep.2017.11.059
CrossrefPubMedPMCGoogle Scholar

Shen, X.-H., Tang, Q.-Y., Huang, J., & Cai, W. (2010). Vitamin E regulates adipocytokine expression in a rat model of dietary-induced obesity. Experimental Biology and Medicine, 235(1), 47-51. doi:10.1258/ebm.2009.009122
CrossrefPubMedGoogle Scholar

Toita, R., Kawano, T., Murata, M., & Kang, J. H. (2016). Anti-obesity and anti-inflammatory effects of macrophage-targeted interleukin-10-conjugated liposomes in obese mice. Biomaterials, 110, 81-88. doi:10.1016/j.biomaterials.2016.09.018
CrossrefPubMedGoogle Scholar

Wang, L., Wang, Q., Xiong, Y., Shi, W., & Qi, X. (2025). Obesity and its comorbidities: current treatment options, emerging biological mechanisms, future perspectives and challenges. Diabetes, Metabolic Syndrome and Obesity, 18, 3427-3445. doi:10.2147/dmso.s540103
CrossrefPubMedPMCGoogle Scholar

Webster, J. M., Kempen, L. J. A. P., Hardy, R. S., & Langen, R. C. J. (2020). Inflammation and skeletal muscle wasting during cachexia. Frontiers in Physiology, 11, 597675. doi:10.3389/fphys.2020.597675
CrossrefPubMedPMCGoogle Scholar

Wiśniewski, K., Choromańska, B., Maciejczyk, M., Dadan, J., & Myśliwiec, P. (2025). Modulating matrix metalloproteinase activity in obesity: comparative effects of bariatric surgery and GLP-1/GIP-based pharmacotherapy. Journal of Clinical Medicine, 14(21), 7648. doi:10.3390/jcm14217648
CrossrefPubMedPMCGoogle Scholar

Žiberna, L., Jenko-Pražnikar, Z., & Petelin, A. (2021). Serum bilirubin levels in overweight and obese individuals: the importance of anti-inflammatory and antioxidant responses. Antioxidants, 10(9), 1352. doi:10.3390/antiox10091352
CrossrefPubMedPMCGoogle Scholar


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Copyright (c) 2026 Tetiana Halenova, Oleksandr Rizun, Mariana Kuznietsova, Oksana Lynchak, Nataliia Raksha, Yuriy Prylutskyy

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