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Brief Report

Role of TLR4 in the induction of inflammatory changes in adipocytes and macrophages

ORCID Icon, ORCID Icon, & ORCID Icon
Pages 212-222 | Received 20 Feb 2020, Accepted 21 Apr 2020, Published online: 13 May 2020

References

  • Stokes A, Preston SH. Deaths attributable to diabetes in the United States: comparison of data sources and estimation approaches. PLoS One. 2017;12(1):e0170219.
  • Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444(7121):860–867.
  • Schelbert KB. Comorbidities of obesity. Prim Care. 2009;36(2):271–285.
  • Fearon WF, Fearon DT. Inflammation and Cardiovascular Disease. Circulation. 2008;117(20):2577–2579.
  • Jiang SZ, Lu W, Zong XF, et al. Obesity and hypertension. Exp Ther Med. 2016;12(4):2395–2399.
  • Vucenik I, Stains JP. Obesity and cancer risk: evidence, mechanisms, and recommendations. Ann N Y Acad Sci. 2012;1271:37–43.
  • Hotamisligil GS. Inflammation, metaflammation and immunometabolic disorders. Nature. 2017;542(7640):177–185.
  • Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest. 2011;121(6):2111–2117.
  • Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol. 2011;29:415–445.
  • Saltiel AR, Olefsky JM. Inflammatory mechanisms linking obesity and metabolic disease. J Clin Invest. 2017;127(1):1–4.
  • Hammarstedt A, Gogg S, Hedjazifar S, et al. Impaired adipogenesis and dysfunctional adipose tissue in human hypertrophic obesity. Physiol Rev. 2018;98(4):1911–1941.
  • Gustafson B, Gogg S, Hedjazifar S, et al. Inflammation and impaired adipogenesis in hypertrophic obesity in man. Am J Physiol Endocrinol Metab. 2009;297(5):E999–E1003.
  • Gustafson B, Hedjazifar S, Gogg S, et al. Insulin resistance and impaired adipogenesis. Trends Endocrinol Metab. 2015;26(4):193–200.
  • Boden G. Obesity and Free Fatty Acids (FFA). Endocrinol Metab Clin North Am. 2008;37(3):635–ix.
  • Liu Z, Liu J, Jahn LA, et al. Infusing lipid raises plasma free fatty acids and induces insulin resistance in muscle microvasculature. J Clin Endocrinol Metab. 2009;94(9):3543–3549.
  • Wolever TM, Bentum-Williams A, Jenkins DJ. Physiological modulation of plasma free fatty acid concentrations by diet. Metabolic implications in nondiabetic subjects. Diabetes Care. 1995;18(7):962–970.
  • Reaven GM, Hollenbeck C, Jeng CY, et al. Measurement of plasma glucose, free fatty acid, lactate, and insulin for 24 h in patients with NIDDM. Diabetes. 1988;37(8):1020–1024.
  • Bouloumie A, Curat CA, Sengenes C, et al. Role of macrophage tissue infiltration in metabolic diseases. Curr Opin Clin Nutr Metab Care. 2005;8(4):347–354.
  • Bruun JM, Helge JW, Richelsen B, et al. Diet and exercise reduce low-grade inflammation and macrophage infiltration in adipose tissue but not in skeletal muscle in severely obese subjects. Am J Physiol Endocrinol Metab. 2006;290(5):E961–967.
  • Cancello R, Henegar C, Viguerie N, et al. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes. 2005;54(8):2277–2286.
  • Griffin C, Eter L, Lanzetta N, et al. TLR4, TRIF, and MyD88 are essential for myelopoiesis and CD11c(+) adipose tissue macrophage production in obese mice. J Biol Chem. 2018;293(23):8775–8786.
  • Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest. 2007;117(1):175–184.
  • Crewe C, An YA, Scherer PE. The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. J Clin Invest. 2017;127(1):74–82.
  • Strissel KJ, Stancheva Z, Miyoshi H, et al. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes. 2007;56(12):2910–2918.
  • Panee J. Monocyte chemoattractant protein 1 (MCP-1) in obesity and diabetes. Cytokine. 2012;60(1):1–12.
  • Cranford TL, Enos RT, Velázquez KT, et al. Role of MCP-1 on inflammatory processes and metabolic dysfunction following high-fat feedings in the FVB/N strain. Int J Obes (Lond). 2016;40(5):844–851.
  • Kanda H, Tateya S, Tamori Y, et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest. 2006;116(6):1494–1505.
  • Yu L, Wang L, Chen S. Endogenous toll-like receptor ligands and their biological significance. J Cell Mol Med. 2010;14(11):2592–2603.
  • Orr JS, Puglisi MJ, Ellacott KL, et al. Toll-like receptor 4 deficiency promotes the alternative activation of adipose tissue macrophages. Diabetes. 2012;61(11):2718–2727.
  • Vila IK, Badin PM, Marques MA, et al. Immune cell Toll-like receptor 4 mediates the development of obesity- and endotoxemia-associated adipose tissue fibrosis. Cell Rep. 2014;7(4):1116–1129.
  • Saberi M, Woods NB, de Luca C, et al. Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab. 2009;10(5):419–429.
  • Lin Y, Lee H, Berg AH, et al. The lipopolysaccharide-activated toll-like receptor (TLR)-4 induces synthesis of the closely related receptor TLR-2 in adipocytes. J Biol Chem. 2000;275(32):24255–24263.
  • Matsumura T, Ito A, Takii T. Endotoxin and cytokine regulation of toll-like receptor (TLR) 2 and TLR4 gene expression in murine liver and hepatocytes. J Interferon Cytokine Res. 2000;20(10):915–921.
  • Frantz S, Kobzik L, Kim YD, et al. Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. J Clin Invest. 1999;104(3):271–280.
  • Shi H, Kokoeva MV, Inouye K, et al. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest. 2006;116(11):3015–3025.
  • Lee JY, Ye J, Gao Z, et al. Reciprocal modulation of Toll-like receptor-4 signaling pathways involving MyD88 and phosphatidylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids. J Biol Chem. 2003;278(39):37041–37051.
  • Schaeffler A, Gross P, Buettner R, et al. Fatty acid-induced induction of Toll-like receptor-4/nuclear factor-kappaB pathway in adipocytes links nutritional signalling with innate immunity. Immunology. 2009;126(2):233–245.
  • Lancaster GI, Langley KG, Berglund NA, et al. Evidence that TLR4 Is not a receptor for saturated fatty acids but mediates lipid-induced inflammation by reprogramming macrophage metabolism. Cell Metab. 2018;27(5):1096–1110.e1095.
  • Galic S, Fullerton MD, Schertzer JD, et al. Hematopoietic AMPK beta1 reduces mouse adipose tissue macrophage inflammation and insulin resistance in obesity. J Clin Invest. 2011;121(12):4903–4915.
  • Hernandez ED, Lee SJ, Kim JY, et al. A macrophage NBR1-MEKK3 complex triggers JNK-mediated adipose tissue inflammation in obesity. Cell Metab. 2014;20(3):499–511.
  • Holzer RG, Park EJ, Li N, et al. Saturated fatty acids induce c-Src clustering within membrane subdomains, leading to JNK activation. Cell. 2011;147(1):173–184.
  • Tzeng HT, Chyuan IT, Chen WY. Shaping of innate immune response by fatty acid metabolite palmitate. Cells. 2019;8(12):12.
  • Gawronska-Kozak B. Preparation and differentiation of mesenchymal stem cells from ears of adult mice. Methods Enzymol. 2014;538:1–13.
  • Staszkiewicz J, Frazier T, Rowan B, et al. Cell growth characteristics, differentiation frequency, and immunophenotype of adult ear mesenchymal stem cells. Stem Cells Dev. 2010;19(1):83–92.
  • Erridge C, Samani NJ. Saturated fatty acids do not directly stimulate Toll-like receptor signaling. Arterioscler Thromb Vasc Biol. 2009;29(11):1944–1949.
  • Huang S, Rutkowsky JM, Snodgrass RG, et al. Saturated fatty acids activate TLR-mediated proinflammatory signaling pathways. J Lipid Res. 2012;53(9):2002–2013.
  • Singer K, DelProposto J, Morris DL, et al. Diet-induced obesity promotes myelopoiesis in hematopoietic stem cells. Mol Metab. 2014;3(6):664–675.
  • Rim JS, Mynatt RL, Gawronska-Kozak B. Mesenchymal stem cells from the outer ear: a novel adult stem cell model system for the study of adipogenesis. Faseb J. 2005;19(9):1205–1207.
  • Weatherill AR, Lee JY, Zhao L, et al. Saturated and polyunsaturated fatty acids reciprocally modulate dendritic cell functions mediated through TLR4. J Immunol. 2005;174(9):5390–5397.
  • Lee JY, Sohn KH, Rhee SH, et al. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J Biol Chem. 2001;276(20):16683–16689.
  • Wood IS, de Heredia FP, Wang B, et al. Cellular hypoxia and adipose tissue dysfunction in obesity. Proc Nutr Soc. 2009;68(4):370–377.
  • Suganami T, Tanimoto-Koyama K, Nishida J, et al. Role of the toll-like receptor 4/NF- B pathway in saturated fatty acid-induced inflammatory changes in the interaction between adipocytes and macrophages. Arterioscler Thromb Vasc Biol. 2007;27:84–91.
  • Kratz M, Coats B, Hisert K, et al. Metabolic dysfunction drives a mechanistically distinct proinflammatory phenotype in adipose tissue macrophages. Cell Metab. 2014;20:614–625.
  • Wang L, Li L, Ran X, et al. Lipopolysaccharides reduce adipogenesis in 3T3-L1 adipocytes through activation of NF-kappaB pathway and downregulation of AMPK expression. Cardiovasc Toxicol. 2013;13:338–346.
  • Chae G, Kwak S. NF-kappaB is involved in the TNF-alpha induced inhibition of the differentiation of 3T3-L1 cells by reducing PPARgamma expression. Exp Mol Med. 2003;431–437. DOI:10.1038/emm.2003.56
  • Lacasa D, Taleb S, Keophiphath M, et al. Macrophage- secreted factors impair human adipogenesis: involvement of proinflammatory state in preadipocytes. Endocrinology. 2007;148:868–877.
  • Liao F, Andalibi A, deBeer FC, et al. Genetic control of inflammatory gene induction and NF-kappa B-like transcription factor activation in response to an atherogenic diet in mice. J Clin Invest. 1993;91:2572–2579.
  • Nagareddy P, Kraakman M, Masters S, et al. Adipose tissue macrophages promote myelopoiesis and monocytosis in obesity. Cell Metab. 2014;19:821–835.
  • Nguyen MT, Favelyukis S, Nguyen AK, et al. A subpopulation of macrophages infiltrates hypertrophic adipose tissue and is activated by free fatty acids via Toll-like receptors 2 and 4 and JNK-dependent pathways. J Biol Chem. 2007;282:35279–35292.
  • Zhao M, Chen X. Effect of lipopolysaccharides on adipogenic potential and premature senescence of adipocyte progenitors. Am J Physiol Endocrinol Metab. 2015;309(4):E334–344.
  • Geric I, Tyurina Y, Krysko O, et al. Lipid homeostasis and inflammatory activation are disturbed in classically activated macrophages with peroxisomal beta‐oxidation deficiency. Immunology. 2018;153:342‐356.
  • Madsen L, Petersen RK, Kristiansen K. Regulation of adipocyte differentiation and function by polyunsaturated fatty acids. Biochim Biophys Acta. 2005;1740(2):266–286.
  • Guo W, Wong S, Xie W, et al. Palmitate modulates intracellular signaling, induces endoplasmic reticulum stress, and causes apoptosis in mouse 3T3-L1 and rat primary preadipocytes. Am J Physiol Endocrinol Metab. 2007;293(2):E576–586.
  • Listenberger LL, Ory DS, Schaffer JE. Palmitate-induced apoptosis can occur through a ceramide-independent pathway. J Biol Chem. 2001;276(18):14890–14895.
  • Lee JY, Plakidas A, Lee WH, et al. Differential modulation of Toll-like receptors by fatty acids: preferential inhibition by n-3 polyunsaturated fatty acids. J Lipid Res. 2003;44(3):479–486.
  • Pricola K, Kuhn N, Haleem-Smith H, et al. Interleukin-6 maintains bone marrow-derived mesenchymal stem cell stemness by an ERK1/2-dependent mechanism. J Cell Biochem. 2009;108(3):577–588.
  • van Hall G, Steensberg A, Sacchetti M, et al. Interleukin-6 stimulates lipolysis and fat oxidation in humans. J Clin Endocrinol Metab. 2003;88(7):3005–3010.
  • Carey A, Bruce C, Sacchetti M, et al. Interleukin-6 and tumor necrosis factor-α are not increased in patients with Type 2 diabetes: evidence that plasma interleukin-6 is related to fat mass and not insulin responsiveness. Diabetologia. 2004;47:1029–1037.
  • Mauer J, Denson JL, Brüning JC. Versatile functions for IL-6 in metabolism and cancer. Trends Immunol. 2015;36(2):92–101.
  • Han MS, White A, Perry RJ, et al. Regulation of adipose tissue inflammation by interleukin 6. Proc Natl Acad Sci U S A. 2020;24:pii: 201920004.