Metabolic Reprogramming of Macrophages in Atherosclerosis: Is It All about Cholesterol?
2
조회
0
다운로드
1
인용
0
참고문헌
키워드
초록
Hypercholesterolemia contributes to the chronic inflammatory response during the progression of atherosclerosis, in part by favoring cholesterol loading in macrophages and other immune cells. However, macrophages encounter a substantial amount of other lipids and nutrients after ingesting atherogenic lipoprotein particles or clearing apoptotic cells, increasing their metabolic load and impacting their behavior during atherosclerosis plaque progression. This review examines whether and how fatty acids and glucose shape the cellular metabolic reprogramming of macrophages in atherosclerosis to modulate the onset phase of inflammation and the later resolution stage, in which the balance is tipped toward tissue repair.
Abstract
Hypercholesterolemia contributes to the chronic inflammatory response during the progression of atherosclerosis, in part by favoring cholesterol loading in macrophages and other immune cells. However, macrophages encounter a substantial amount of other lipids and nutrients after ingesting atherogenic lipoprotein particles or clearing apoptotic cells, increasing their metabolic load and impacting their behavior during atherosclerosis plaque progression. This review examines whether and how fatty acids and glucose shape the cellular metabolic reprogramming of macrophages in atherosclerosis to modulate the onset phase of inflammation and the later resolution stage, in which the balance is tipped toward tissue repair.
참고문헌 (93)
- Anitschkow N, "Classics in arteriosclerosis research: on experimental cholesterin steatosis and its significance in the origin of some pathological processes", Arteriosclerosis, 3, pp.178~182 (1983)
- Han CZ, "Metabolic connections during apoptotic cell engulfment", Cell, 147, pp.1442~1445 (2011)
- Tabas I, "Macrophage death and defective inflammation resolution in atherosclerosis", Nat Rev Immunol, 10, pp.36~46 (2010)
- Koelwyn GJ, "Regulation of macrophage immunometabolism in atherosclerosis", Nat Immunol, 19, pp.526~537 (2018)
- Spann NJ, "Sterols and oxysterols in immune cell function", Nat Immunol, 14, pp.893~900 (2013)
- Tall AR, "Cholesterol, inflammation and innate immunity", Nat Rev Immunol, 15, pp.104~116 (2015)
- Yvan-Charvet L, "Immunometabolic function of cholesterol in cardiovascular disease and beyond", Cardiovasc Res, 115, pp.1393~1407 (2019)
- Giugliano RP, "Clinical efficacy and safety of achieving very low LDL-cholesterol concentrations with the PCSK9 inhibitor evolocumab : a prespecified secondary analysis of the FOURIER trial", Lancet, 390, pp.1962~1971 (2017)
- Ridker PM, "Residual inflammatory risk : addressing the obverse side of the atherosclerosis prevention coin", Eur Heart J, 37, pp.1720~1722 (2016)
- Benjamin EJ, "Heart disease and stroke statistics-2017 update : a report from the American Heart Association", Circulation, 135, pp.e146~e603 (2017)
- Christ A, "Western diet and the immune system : an inflammatory connection", Immunity, 51, pp.794~811 (2019)
- Linton MF, "Prevention of atherosclerosis in apolipoprotein E-deficient mice by bone marrow transplantation", Science, 267, pp.1034~1037 (1995)
- Yvan-Charvet L, "Poststatin era in atherosclerosis management : lessons from epidemiologic and genetic studies", Curr Opin Lipidol, 29, pp.246~258 (2018)
- Kim K, "Transcriptome analysis reveals nonfoamy rather than foamy plaque macrophages are proinflammatory in atherosclerotic murine models", Circ Res, 123, pp.1127~1142 (2018)
- Fernandez DM, "Single-cell immune landscape of human atherosclerotic plaques", Nat Med, 25, pp.1576~1588 (2019)
- Binder CJ, "Innate sensing of oxidation-specific epitopes in health and disease", Nat Rev Immunol, 16, pp.485~497 (2016)
- Grebe A, "NLRP3 inflammasome and the IL-1 pathway in atherosclerosis", Circ Res, 122, pp.1722~1740 (2018)
- Murphy AJ, "IL-18 production from the NLRP1 inflammasome prevents obesity and metabolic syndrome", Cell Metab, 23, pp.155~164 (2016)
- Jordan S, "Dietary intake regulates the circulating inflammatory monocyte pool", Cell, 178, pp.1102~1114 (2019)
- Flaherty SE 3rd, "A lipase-independent pathway of lipid release and immune modulation by adipocytes", Science, 363, pp.989~993 (2019)
- Brown RJ, "Lipases as modulators of atherosclerosis in murine models", Curr Drug Targets, 8, pp.1307~1319 (2007)
- Babaev VR, "Macrophage lipoprotein lipase promotes foam cell formation and atherosclerosis in low density lipoprotein receptor-deficient mice", J Biol Chem, 275, pp.26293~26299 (2000)
- Takahashi M, "Macrophage lipoprotein lipase modulates the development of atherosclerosis but not adiposity", J Lipid Res, 54, pp.1124~1134 (2013)
- Chang CL, "Lipoprotein lipase deficiency impairs bone marrow myelopoiesis and reduces circulating monocyte levels", Arterioscler Thromb Vasc Biol, 38, pp.509~519 (2018)
- Chang HR, "Role of LpL(lipoprotein lipase)in macrophage polarization in vitro and in vivo", Arterioscler Thromb Vasc Biol, 39, pp.1967~1985 (2019)
- Haemmerle G, "Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase", Science, 312, pp.734~737 (2006)
- Schoiswohl G, "Impact of reduced ATGL-mediated adipocyte lipolysis on obesity-associated insulin resistance and inflammation in male mice", Endocrinology, 156, pp.3610~3624 (2015)
- Kosteli A, "Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue", J Clin Invest, 120, pp.3466~3479 (2010)
- Lumeng CN, "Inflammatory links between obesity and metabolic disease", J Clin Invest, 121, pp.2111~2117 (2011)
- Osborn O, "The cellular and signaling networks linking the immune system and metabolism in disease", Nat Med, 18, pp.363~374 (2012)
- Ely BR, "Meeta-inflammation and cardiometabolic disease in obesity: can heat therapy help?", Temperature (Austin), 5, pp.9~21 (2017)
- Cooke AA, "Fatty acids and chronic low grade inflammation associated with obesity and the metabolic syndrome", Eur J Pharmacol, 785, pp.207~214 (2016)
- Perry RJ, "Hepatic acetyl CoA links adipose tissue inflammation to hepatic insulin resistance and type 2 diabetes", Cell, 160, pp.745~758 (2015)
- Schweiger M, "Pharmacological inhibition of adipose triglyceride lipase corrects high-fat diet-induced insulin resistance and hepatosteatosis in mice", Nat Commun, 8, pp.14859~ (2017)
- Lass A, "Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman Syndrome", Cell Metab, 3, pp.309~319 (2006)
- Yang X, "The G0", G1 switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase, 2010, pp.11, 194~205
- Zhang X, "Inhibition of intracellular lipolysis promotes human cancer cell adaptation to hypoxia", eLife, 6, pp.e31132~ (2017)
- Padmanabha Das KM, "Hypoxia-inducible lipid droplet-associated protein inhibits adipose triglyceride lipase", J Lipid Res, 59, pp.531~541 (2018)
- Heckmann BL, "Defective adipose lipolysis and altered global energy metabolism in mice with adipose overexpression of the lipolytic inhibitor G0", G1 switch gene 2(G0S2), 2014, pp.289, 1905~1916
- Shin H, "Lipolysis in brown adipocytes is not essential for cold-induced thermogenesis in mice", Cell Metab, 26, pp.764~777 (2017)
- van Dierendonck XA, "HILPDA uncouples lipid storage in adipose tissue macrophages from inflammation and metabolic dysregulation", bioRxiv, 566802~ (2019)
- Febbraio M, "Stem cell transplantation reveals that absence of macrophage CD36 is protective against atherosclerosis", Arterioscler Thromb Vasc Biol, 24, pp.2333~2338 (2004)
- Zhao L, "Lack of myeloid Fatp1 increases atherosclerotic lesion size in Ldlr-", -mice, 2017, pp.266, 182~189
- Huang SC, "Cell-intrinsic lysosomal lipolysis is essential for alternative activation of macrophages", Nat Immunol, 15, pp.846~855 (2014)
- Samovski D, "Regulation of AMPK activation by CD36 links fatty acid uptake to β-oxidation", Diabetes, 64, pp.353~359 (2015)
- Chen Y, "Mitochondrial metabolic reprogramming by CD36 signaling drives macrophage inflammatory responses", Circ Res, 125, pp.1087~1102 (2019)
- Johnson AR, "Metabolic reprogramming through fatty acid transport protein 1(FATP1)regulates macrophage inflammatory potential and adipose inflammation", Mol Metab, 5, pp.506~526 (2016)
- Makowski L, "Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis", Nat Med, 7, pp.699~705 (2001)
- Makowski L, "The fatty acid-binding protein, aP2, coordinates macrophage cholesterol trafficking and inflammatory activity. Macrophage expression of aP2 impacts peroxisome proliferator-activated receptor gamma and IkappaB kinase activities", J Biol Chem, 280, pp.12888~12895 (2005)
- Boord JB, "Adipocyte fatty acid-binding protein, aP2, alters late atherosclerotic lesion formation in severe hypercholesterolemia", Arterioscler Thromb Vasc Biol, 22, pp.1686~1691 (2002)
- Ménégaut L, "Macrophage fatty acid metabolism and atherosclerosis : the rise of PUFAs", Atherosclerosis, 291, pp.52~61 (2019)
- Chandak PG, "Efficient phagocytosis requires triacylglycerol hydrolysis by adipose triglyceride lipase", J Biol Chem, 285, pp.20192~20201 (2010)
- Aflaki E, "Impaired Rho GTPase activation abrogates cell polarization and migration in macrophages with defective lipolysis", Cell Mol Life Sci, 68, pp.3933~3947 (2011)
- Lammers B, "Macrophage adipose triglyceride lipase deficiency attenuates atherosclerotic lesion development in low-density lipoprotein receptor knockout mice", Arterioscler Thromb Vasc Biol, 31, pp.67~73 (2011)
- Goeritzer M, "Active autophagy but not lipophagy in macrophages with defective lipolysis", Biochim Biophys Acta, 1851, pp.1304~1316 (2015)
- Sekiya M, "Ablation of neutral cholesterol ester hydrolase 1 accelerates atherosclerosis", Cell Metab, 10, pp.219~228 (2009)
- Ghosh S, "Important considerations for evaluating the data presented by Igarashi et al", Circ Res, 108, pp.e6~e7 (2011)
- Kratky D, "Neutral cholesterol ester hydrolases in macrophages : still a matter of debate", Circ Res, 108, pp.e13~ (2011)
- Emanuel R, "Induction of lysosomal biogenesis in atherosclerotic macrophages can rescue lipid-induced lysosomal dysfunction and downstream sequelae", Arterioscler Thromb Vasc Biol, 34, pp.1942~1952 (2014)
- Sergin I, "Exploiting macrophage autophagy-lysosomal biogenesis as a therapy for atherosclerosis", Nat Commun, 8, pp.15750~ (2017)
- Zhang X, "Classical and alternative roles for autophagy in lipid metabolism", Curr Opin Lipidol, 29, pp.203~211 (2018)
- Zhang H, "CRISPR", Cas9-mediated gene editing in human iPSC-derived macrophage reveals lysosomal acid lipase function in human macrophages-brief report, 2017, pp.37, 2156~2160
- Razani B, "Autophagy links inflammasomes to atherosclerotic progression", Cell Metab, 15, pp.534~544 (2012)
- Viaud M, "Lysosomal cholesterol hydrolysis couples efferocytosis to anti-inflammatory oxysterol production", Circ Res, 122, pp.1369~1384 (2018)
- Schlager S, "Lysosomal lipid hydrolysis provides substrates for lipid mediator synthesis in murine macrophages", Oncotarget, 8, pp.40037~40051 (2017)
- Du H, "Lysosomal acid lipase and atherosclerosis", Curr Opin Lipidol, 15, pp.539~544 (2004)
- Yan C, "Macrophage-specific expression of human lysosomal acid lipase corrects inflammation and pathogenic phenotypes in lal-", -mice, 2006, pp.169, 916~926
- Serhan CN, "Discovery of specialized pro-resolving mediators marks the dawn of resolution physiology and pharmacology", Mol Aspects Med, 58, pp.1~11 (2017)
- Kasikara C, "The role of non-resolving inflammation in atherosclerosis", J Clin Invest, 128, pp.2713~2723 (2018)
- Bäck M, "Inflammation and its resolution in atherosclerosis : mediators and therapeutic opportunities", Nat Rev Cardiol, 16, pp.389~406 (2019)
- Serhan CN, "The resolution code of acute inflammation : Novel pro-resolving lipid mediators in resolution", Semin Immunol, 27, pp.200~215 (2015)
- Fredman G, "An imbalance between specialized pro-resolving lipid mediators and pro-inflammatory leukotrienes promotes instability of atherosclerotic plaques", Nat Commun, 7, pp.12859~ (2016)
- Viola JR, "Resolving lipid mediators Maresin 1 and Resolvin D2 prevent atheroprogression in mice", Circ Res, 119, pp.1030~1038 (2016)
- Kanter JE, "Diabetes promotes an inflammatory macrophage phenotype and atherosclerosis through acyl-CoA synthetase 1", Proc Natl Acad Sci U S A, 109, pp.E715~E724 (2012)
- Schneider JG, "Macrophage fatty-acid synthase deficiency decreases diet-induced atherosclerosis", J Biol Chem, 285, pp.23398~23409 (2010)
- Powell DR, "Fatty acid desaturase 1 knockout mice are lean with improved glycemic control and decreased development of atheromatous plaque", Diabetes Metab Syndr Obes, 9, pp.185~199 (2016)
- Saito R, "Macrophage Elovl6 deficiency ameliorates foam cell formation and reduces atherosclerosis in low-density lipoprotein receptor-deficient mice", Arterioscler Thromb Vasc Biol, 31, pp.1973~1979 (2011)
- Rogers IS, "Imaging of coronary inflammation with FDG-PET : feasibility and clinical hurdles", Curr Cardiol Rep, 13, pp.138~144 (2011)
- Hag AM, "18F-FDG PET imaging of murine atherosclerosis : association with gene expression of key molecular markers", PLoS One, 7, pp.e50908~ (2012)
- Lee SJ, "Oxidized low-density lipoprotein stimulates macrophage 18F-FDG uptake via hypoxia-inducible factor-1α activation through Nox2-dependent reactive oxygen species generation", J Nucl Med, 55, pp.1699~1705 (2014)
- Garcia-Garcia HM, "Imaging plaques to predict and better manage patients with acute coronary events", Circ Res, 114, pp.1904~1917 (2014)
- Kim EJ, "Metabolic activity of the spleen and bone marrow in patients with acute myocardial infarction evaluated by 18F-fluorodeoxyglucose positron emission tomograpic imaging", Circ Cardiovasc Imaging, 7, pp.454~460 (2014)
- Emami H, "Splenic metabolic activity predicts risk of future cardiovascular events : demonstration of a cardiosplenic axis in humans", JACC Cardiovasc Imaging, 8, pp.121~130 (2015)
- van der Valk FM, "Increased haematopoietic activity in patients with atherosclerosis", Eur Heart J, 38, pp.425~432 (2017)
- Robbins CS, "Extramedullary hematopoiesis generates Ly-6Chigh monocytes that infiltrate atherosclerotic lesions", Circulation, 125, pp.364~374 (2012)
- Roussel R, "Prevention of cardiovascular disease through reduction of glycaemic exposure in type 2 diabetes : a perspective on glucose-lowering interventions", Diabetes Obes Metab, 20, pp.238~244 (2018)
- Ross S, "Mendelian randomization analysis supports the causal role of dysglycaemia and diabetes in the risk of coronary artery disease", Eur Heart J, 36, pp.1454~1462 (2015)
- Ahmad OS, "A Mendelian randomization study of the effect of type-2 diabetes on coronary heart disease", Nat Commun, 6, pp.7060~ (2015)
- Sarrazy V, "Disruption of Glut1 in hematopoietic stem cells prevents myelopoiesis and enhanced glucose flux in atheromatous plaques of ApoE-", -mice, 2016, pp.118, 1062~1077
- Morioka S, "Efferocytosis induces a novel SLC program to promote glucose uptake and lactate release", Nature, 563, pp.714~718 (2018)
- Freemerman AJ, "Myeloid Slc2a1-deficient murine model revealed macrophage activation and metabolic phenotype are fueled by GLUT1", J Immunol, 202, pp.1265~1286 (2019)
- Haschemi A, "The sedoheptulose kinase CARKL directs macrophage polarization through control of glucose metabolism", Cell Metab, 15, pp.813~826 (2012)
- Sarrazy V, "Maintenance of macrophage redox status by ChREBP limits inflammation and apoptosis and protects against advanced atherosclerotic lesion formation", Cell Reports, 13, pp.132~144 (2015)
