Influence of organism stimulation with bacterial lipopolysaccharide on the metabolism of the extracellular matrix of the heart of rats under conditions of experimental metabolic syndrome

Authors

DOI:

https://doi.org/10.26641/2307-0404.2024.1.300443

Keywords:

metabolic syndrome, heart, bacterial lipopolysaccharide, extracellular matrix, glycosaminoglycans

Abstract

 Until recently, the extracellular matrix was considered only a structural component of the organ, which performs exclusively the function of the framework. However, recent studies provide insight into a much broader role of extracellular matrix in metabolic homeostasis, the transmission of intra-organ and tissue signals. Metabolic syndrome and chronic infectious diseases can change the extracellular matrix’s structure in the heart. However, the combined effect of bacterial lipopolysaccharide and metabolic syndrome on extracellular matrix of the heart remains insufficiently elucidated at present. The purpose of this work is to establish the effect of organism stimulation with bacterial lipopolysaccharide on the concentration of different fractions of glycosaminoglycans, the intensity of collagenolysis and the content of sialic acids in the heart of rats under conditions of experimental metabolic syndrome. The study was conducted on 24 sexually mature rats of the “Wistar” line weighing 200-260 g. Animals were divided into 4 groups with 6 animals in each group: control, metabolic syndrome group, lipopolysaccharide injection group and combination of lipopolysaccharide injection and metabolic syndrome group. Metabolic syndrome was modelled by using 20% fructose solution as the only water source. Lipopolysaccharide of S. typhi was administered according to the scheme: the first week, 0.4 μg/kg 3 times intraperitoneally, then once a week 0.4 μg/kg throughout the experiment. Experiment lasted for 60 days. The concentration of glycosaminoglycans, their separate fractions, the content of free L-hydroxyproline and sialic acids was studied in 10% rat heart homogenate. The combined effect of stimulation of the organism with bacterial lipopolysaccharide and metabolic syndrome modeling led to an increase in the total concentration of glycosaminoglycans in the heart of rats by 73.46% compared to the control group. Under these conditions, the concentration of the heparin-heparan fraction of glycosaminoglycans in the heart of rats increased by 188.64% compared to the control group. The content of the keratan-dermatan fraction of glycosaminoglycans increased by 75.34%, and the chondroitin fraction of glycosaminoglycans increased by 17.63%. The concentration of free L-hydroxyproline increased by 167.23%. The content of sialic acids increased by 66.95%. Metabolic syndrome, stimulation of the organism with bacterial lipopolysaccharide and their combination lead to intensification of degradation of the extracellular matrix of the heart of rats due to increased collagenolysis, destruction of proteoglycans and glycoproteins.

References

Karamanos NK, Theocharis AD, Piperigkou Z, et al. A guide to the composition and functions of the extracellular matrix. FEBS J. 2021;288(24):6850-912. doi: https://doi.org/10.1111/febs.15776

Liu C, Pei M, Li Q, Zhang Y. Decellularized ex-tracellular matrix mediates tissue construction and regeneration. Front Med. 2022;16(1):56-82. doi: https://doi.org/10.1007/s11684-021-0900-3

Frangogiannis NG. The Extracellular Matrix in Ischemic and Nonischemic Heart Failure. Circ Res. 2019;125(1):117-46. doi: https://doi.org/10.1161/CIRCRESAHA.119.311148

Park HJ, De Jesus Morales KJ, Bheri S, Kas-souf BP, Davis ME. Bidirectional relationship between cardiac extracellular matrix and cardiac cells in ischemic heart disease. Stem Cells. 2021;39(12):1650-9. doi: https://doi.org/10.1002/stem.3445

Frangogiannis NG. Cardiac fibrosis. Cardiovasc Res. 2021;117(6):1450-88. doi: https://doi.org/10.1093/cvr/cvaa324

Unamuno X, Gómez-Ambrosi J, Ramírez B, et al. NLRP3 inflammasome blockade reduces adipose tissue inflammation and extracellular matrix remodeling. Cell Mol Immunol. 2021;18(4):1045-57. doi: https://doi.org/10.1038/s41423-019-0296-z

Duan A, Shen K, Li B, et al. Extracellular vesicles derived from LPS-preconditioned human synovial me-senchymal stem cells inhibit extracellular matrix degradation and prevent osteoarthritis of the knee in a mouse model. Stem Cell Res Ther. 2021;12(1):427. doi: https://doi.org/10.1186/s13287-021-02507-2

Akimov OY, Mykytenko AO, Mischenko AV, Kostenko VO. Influence of bacterial lipopolysaccharide on the degradation of the components of the extracellular matrix of rat biceps femoris muscle during high fructose diet-induced metabolic syndrome. Fiziologichnyi Zhurnal. 2023;69(3):99-105. doi: https://doi.org/10.15407/fz69.03.099

Mamikutty N, Thent ZC, Sapri SR, Sahruddin NN, Mohd Yusof MR, Haji Suhaimi F. The estab-lishment of metabolic syndrome model by induction of fructose drinking water in male Wistar rats. Biomed Res Int. 2014;2014:263897. doi: https://doi.org/10.1155/2014/263897

Faizi N, Alvi Y. Biostatistics Manual for Health Research A Practical Guide to Data Analysis. Elsevier Science; 2023. 290 p.

doi: https://doi.org/10.1016/C2022-0-00374-3

Wang Q, Li H, Lu H, et al. SAA1 exacerbates pancreatic β-cell dysfunction through activation of NF-κB signaling in high-fat diet-induced type 2 diabetes mice. Mol Cell Endocrinol. 2023;576:112043. doi: https://doi.org/10.1016/j.mce.2023.112043

Al-Roub A, Akhter N, Al-Rashed F, et al. TNFα induces matrix metalloproteinase-9 expression in mono-cytic cells through ACSL1/JNK/ERK/NF-kB signaling pathways. Sci Rep. 2023;13(1):14351. doi: https://doi.org/10.1038/s41598-023-41514-6

Kirsten N, Ohmes J, Mikkelsen MD, et al. Impact of Enzymatically Extracted High Molecular Weight Fucoidan on Lipopolysaccharide-Induced Endothelial Activation and Leukocyte Adhesion. Mar Drugs. 2023;21(6):339. doi: https://doi.org/10.3390/md21060339

Feng C, Cross AS, Vasta GR. Galectin-1 mediates interactions between polymorphonuclear leukocytes and vascular endothelial cells, and promotes their extravasation during lipopolysaccharide-induced acute lung injury. Mol Immunol. 2023;156:127-35. doi: https://doi.org/10.1016/j.molimm.2023.02.011

Allendorf DH, Franssen EH, Brown GC. Lipopo-lysaccharide activates microglia via neuraminidase 1 desialylation of Toll-like Receptor 4. J Neurochem. 2020;155(4):403-16. doi: https://doi.org/10.1111/jnc.15024

Shahvali S, Shahesmaeili A, Sanjari M, Karami-Mohajeri S. The correlation between blood oxidative stress and sialic acid content in diabetic patients with nephro¬pathy, hypertension, and hyperlipidemia. Diabetol Int. 2019;11(1):19-26. doi: https://doi.org/10.1007/s13340-019-00395-9

Buijsers B, Maciej-Hulme M, Jacobs M, et al. Glycosaminoglycans and fucoidan have a protective effect on experimental glomerulonephritis. Front Mol Biosci. 2023;10:1223972. doi: https://doi.org/10.3389/fmolb.2023.1223972

Ying J, Zhang C, Wang Y, et al. Sulodexide im-proves vascular permeability via glycocalyx remodelling in endothelial cells during sepsis. Front Immunol. 2023;14:1172892. doi: https://doi.org/10.3389/fimmu.2023.1172892

Miguez PA, Bash E, Musskopf ML, et al. Control of tissue homeostasis by the extracellular matrix: Synthetic heparan sulfate as a promising therapeutic for periodontal health and bone regeneration. Periodontol 2000. 2023;00:1-22. doi: https://doi.org/10.1111/prd.12515

Klisic A, Patoulias D. The Role of Endocan in Cardiometabolic Disorders. Metabolites. 2023;13(5):640. doi: https://doi.org/10.3390/metabo13050640

Sullivan RC, Rockstrom MD, Schmidt EP, Hip-pensteel JA. Endothelial glycocalyx degradation during sepsis: Causes and consequences. Matrix Biol Plus. 2021;12:100094. doi: https://doi.org/10.1016/j.mbplus.2021.100094

Diaz-Salmeron R, Cailleau C, Denis S, Ponchel G, Bouchemal K. Hyaluronan nanoplatelets exert an intrinsic anti-inflammatory activity in a rat model of bladder painful syndrome/interstitial cystitis. J Control Release. 2023;356:434-47. doi: https://doi.org/10.1016/j.jconrel.2023.03.014

Wang X, Liu D, Li D, et al. Combined treatment with glucosamine and chondroitin sulfate improves rheumatoid arthritis in rats by regulating the gut microbiota. Nutr Metab (Lond). 2023;20(1):22. doi: https://doi.org/10.1186/s12986-023-00735-2

Zhang Y, Wang ZL, Deng ZP, Wang ZL, Song F, Zhu LL. An extracellular matrix-inspired self-healing composite hydrogel for enhanced platelet-rich plasma-mediated chronic diabetic wound treatment. Carbohydr Polym. 2023;315:120973. doi: https://doi.org/10.1016/j.carbpol.2023.120973

Matsytska YK, Akimov OY, Mykytenko AO. In-fluence of corvitin and metformin on biochemical changes in lacrimal glands of rats during water avoidance stress modeling. Oftalmologicheskii Zhurnal. 2022;97(3):39-44. doi: https://doi.org/10.31288/oftalmolzh202233944

Skrypnyk I, Maslova G, Lymanets T, Gusachenko I. L-arginine is an effective medication for pre-vention of endothelial dysfunction, a predictor of anthra-cycline cardiotoxicity in patients with acute leukemia. Exp Oncol. 2017;39(4):308-11. doi: https://doi.org/10.31768/2312-8852.2017.39(4):308-311

Chekalina NI, Kazakov YM, Mamontova TV, Vesnina LE, Kaidashev IP. Resveratrol more effectively than quercetin reduces endothelium degeneration and level of necrosis factor α in patients with coronary artery disease. Wiad Lek. 2016;69(3 pt 2):475-9.

Downloads

Published

2024-04-01

How to Cite

1.
Akimov O, Mykytenko A, Kostenko V. Influence of organism stimulation with bacterial lipopolysaccharide on the metabolism of the extracellular matrix of the heart of rats under conditions of experimental metabolic syndrome. Med. perspekt. [Internet]. 2024Apr.1 [cited 2024Jun.30];29(1):10-6. Available from: https://journals.uran.ua/index.php/2307-0404/article/view/300443

Issue

Section

THEORETICAL MEDICINE