Regulation of Macrophage Activation and Differentiation in Atherosclerosis
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Chronic inflammation is a hallmark of atherosclerosis and macrophages play a central role in controlling inflammation at all stages of atherosclerosis. In atherosclerosis, macrophages and monocyte-derived macrophages are continuously exposed to cholesterol, oxidized lipids, cell debris, cytokines, and chemokines. Not only do these stimuli induce a specific macrophage phenotype, but they also interact extensively, leading to macrophage heterogeneity in atherosclerotic plaques. Herein, we review the diverse phenotypes of macrophages, the mechanisms underlying macrophage activation, and the contributions of macrophages to atherosclerosis in this context. We also summarize recent studies on foamy macrophages and monocyte-derived macrophages in plaque during disease progression. We provide a comprehensive overview of transcriptional, epigenetic, and metabolic reprogramming of macrophages and discuss the emerging concepts of targeting cytokines and macrophages to modulate atherosclerosis.
Abstract
Chronic inflammation is a hallmark of atherosclerosis and macrophages play a central role in controlling inflammation at all stages of atherosclerosis. In atherosclerosis, macrophages and monocyte-derived macrophages are continuously exposed to cholesterol, oxidized lipids, cell debris, cytokines, and chemokines. Not only do these stimuli induce a specific macrophage phenotype, but they also interact extensively, leading to macrophage heterogeneity in atherosclerotic plaques. Herein, we review the diverse phenotypes of macrophages, the mechanisms underlying macrophage activation, and the contributions of macrophages to atherosclerosis in this context. We also summarize recent studies on foamy macrophages and monocyte-derived macrophages in plaque during disease progression. We provide a comprehensive overview of transcriptional, epigenetic, and metabolic reprogramming of macrophages and discuss the emerging concepts of targeting cytokines and macrophages to modulate atherosclerosis.
참고문헌 (106)
- Tall AR, "Cholesterol, inflammation and innate immunity", Nat Rev Immunol, 15, pp.104~116 (2015)
- Hansson GK, "The immune system in atherosclerosis", Nat Immunol, 12, pp.204~212 (2011)
- Moore KJ, "Macrophages in atherosclerosis : a dynamic balance", Nat Rev Immunol, 13, pp.709~721 (2013)
- Moore KJ, "Macrophages in the pathogenesis of atherosclerosis", Cell, 145, pp.341~355 (2011)
- Herrington W, "Epidemiology of atherosclerosis and the potential to reduce the global burden of atherothrombotic disease", Circ Res, 118, pp.535~546 (2016)
- Cheng AY, "Implications of recent clinical trials for the national cholesterol education program adult treatment panel III guidelines", Curr Opin Cardiol, 21, pp.400~404 (2006)
- Tabas I, "Monocyte-macrophages and T cells in atherosclerosis", Immunity, 47, pp.621~634 (2017)
- Libby P, "Progress and challenges in translating the biology of atherosclerosis", Nature, 473, pp.317~325 (2011)
- Gordon S, "Alternative activation of macrophages : mechanism and functions", Immunity, 32, pp.593~604 (2010)
- Murray PJ, "Macrophage activation and polarization : nomenclature and experimental guidelines", Immunity, 41, pp.14~20 (2014)
- Sica A, "Macrophage plasticity and polarization : in vivo veritas", J Clin Invest, 122, pp.787~795 (2012)
- Mosser DM, "Exploring the full spectrum of macrophage activation", Nat Rev Immunol, 8, pp.958~969 (2008)
- Glass CK, "Molecular control of activation and priming in macrophages", Nat Immunol, 17, pp.26~33 (2016)
- Kuznetsova T, "Transcriptional and epigenetic regulation of macrophages in atherosclerosis", Nat Rev Cardiol, 17, pp.216~228 (2020)
- Lawrence T, "Transcriptional regulation of macrophage polarization : enabling diversity with identity", Nat Rev Immunol, 11, pp.750~761 (2011)
- Koelwyn GJ, "Regulation of macrophage immunometabolism in atherosclerosis", Nat Immunol, 19, pp.526~537 (2018)
- Palsson-McDermott EM, "Pyruvate kinase M2 regulates Hif-1α activity and IL-1β induction and is a critical determinant of the warburg effect in LPS-activated macrophages", Cell Metab, 21, pp.65~80 (2015)
- Tannahill GM, "Succinate is an inflammatory signal that induces IL-1β through HIF-1α", Nature, 496, pp.238~242 (2013)
- Jha AK, "Network integration of parallel metabolic and transcriptional data reveals metabolic modules that regulate macrophage polarization", Immunity, 42, pp.419~430 (2015)
- Van den Bossche J, "Mitochondrial dysfunction prevents repolarization of inflammatory macrophages", Cell Reports, 17, pp.684~696 (2016)
- Tan Z, "Pyruvate dehydrogenase kinase 1participates in macrophage polarization via regulating glucose metabolism", J Immunol, 194, pp.6082~6089 (2015)
- Nomura M, "Fatty acid oxidation in macrophage polarization", Nat Immunol, 17, pp.216~217 (2016)
- Li B, "The role of chromatin during transcription", Cell, 128, pp.707~719 (2007)
- Kittan NA, "Cytokine induced phenotypic and epigenetic signatures are key to establishing specific macrophage phenotypes", PLoS One, 8, pp.e78045~ (2013)
- Kaikkonen MU, "Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription", Mol Cell, 51, pp.310~325 (2013)
- De Santa F, "Jmjd3 contributes to the control of gene expression in LPS-activated macrophages", EMBO J, 28, pp.3341~3352 (2009)
- Kruidenier L, "A selective jumonji H3K27demethylase inhibitor modulates the proinflammatory macrophage response", Nature, 488, pp.404~408 (2012)
- Ishii M, "Epigenetic regulation of the alternatively activated macrophage phenotype", Blood, 114, pp.3244~3254 (2009)
- Satoh T, "The Jmjd3-Irf4 axis regulates M2macrophage polarization and host responses against helminth infection", Nat Immunol, 11, pp.936~944 (2010)
- Mullican SE, "Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation", Genes Dev, 25, pp.2480~2488 (2011)
- Chen X, "Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages", Proc Natl Acad Sci U S A, 109, pp.E2865~ (2012)
- Cochain C, "Single-Cell RNA-Seq reveals the transcriptional landscape and heterogeneity of aortic macrophages in murine atherosclerosis", Circ Res, 122, pp.1661~1674 (2018)
- Stöger JL, "Distribution of macrophage polarization markers in human atherosclerosis", Atherosclerosis, 225, pp.461~468 (2012)
- Ginhoux F, "New insights into the multidimensional concept of macrophage ontogeny, activation and function", Nat Immunol, 17, pp.34~40 (2016)
- Benoit M, "Macrophage polarization in bacterial infections", J Immunol, 181, pp.3733~3739 (2008)
- Brånén L, "Inhibition of tumor necrosis factor-alpha reduces atherosclerosis in apolipoprotein E knockout mice", Arterioscler Thromb Vasc Biol, 24, pp.2137~2142 (2004)
- Ohta H, "Disruption of tumor necrosis factor-alpha gene diminishes the development of atherosclerosis in ApoE-deficient mice", Atherosclerosis, 180, pp.11~17 (2005)
- Oberoi R, "Anti-tumor necrosis factor-αtherapy increases plaque burden in a mouse model of experimental atherosclerosis", Atherosclerosis, 277, pp.80~89 (2018)
- Seino Y, "Interleukin 6 gene transcripts are expressed in human atherosclerotic lesions", Cytokine, 6, pp.87~91 (1994)
- Schieffer B, "Expression of angiotensin II and interleukin 6 in human coronary atherosclerotic plaques : potential implications for inflammation and plaque instability", Circulation, 101, pp.1372~1378 (2000)
- Sukovich DA, "Expression of interleukin-6 in atherosclerotic lesions of male ApoE-knockout mice : inhibition by 17beta-estradiol", Arterioscler Thromb Vasc Biol, 18, pp.1498~1505 (1998)
- Cardilo-Reis L, "Interleukin-13protects from atherosclerosis and modulates plaque composition by skewing the macrophage phenotype", EMBO Mol Med, 4, pp.1072~1086 (2012)
- Rahman K, "Inflammatory Ly6Chi monocytes and their conversion to M2 macrophages drive atherosclerosis regression", J Clin Invest, 127, pp.2904~2915 (2017)
- Lin JD, "Single-cell analysis of fate-mapped macrophages reveals heterogeneity, including stem-like properties, during atherosclerosis progression and regression", JCI Insight, 4, pp.e124574~ (2019)
- Guo L, "CD163+ macrophages promote angiogenesis and vascular permeability accompanied by inflammation in atherosclerosis", J Clin Invest, 128, pp.1106~1124 (2018)
- Kadl A, "Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2", Circ Res, 107, pp.737~746 (2010)
- Stewart CR, "CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer", Nat Immunol, 11, pp.155~161 (2010)
- Sheedy FJ, "CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation", Nat Immunol, 14, pp.812~820 (2013)
- Miller YI, "Toll-like receptor 4-dependent and-independent cytokine secretion induced by minimally oxidized low-density lipoprotein in macrophages", Arterioscler Thromb Vasc Biol, 25, pp.1213~1219 (2005)
- Duewell P, "NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals", Nature, 464, pp.1357~1361 (2010)
- Cyster JG, "25-Hydroxycholesterols in innate and adaptive immunity", Nat Rev Immunol, 14, pp.731~743 (2014)
- Chistiakov DA, "Mechanisms of foam cell formation in atherosclerosis", J Mol Med(Berl), 95, pp.1153~1165 (2017)
- Williams JW, "Cytokine circuits in cardiovascular disease", Immunity, 50, pp.941~954 (2019)
- Park YM, "CD36 modulates migration of mouse and human macrophages in response to oxidized LDL and may contribute to macrophage trapping in the arterial intima", J Clin Invest, 119, pp.136~145 (2009)
- van Gils JM, "The neuroimmune guidance cue netrin-1 promotes atherosclerosis by inhibiting the emigration of macrophages from plaques", Nat Immunol, 13, pp.136~143 (2012)
- Kim K, "Transcriptome analysis reveals nonfoamy rather than foamy plaque macrophages are proinflammatory in atherosclerotic murine models", Circ Res, 123, pp.1127~1142 (2018)
- Tangirala RK, "Identification of macrophage liver X receptors as inhibitors of atherosclerosis", Proc Natl Acad Sci U S A, 99, pp.11896~11901 (2002)
- Hamada M, "MafB promotes atherosclerosis by inhibiting foam-cell apoptosis", Nat Commun, 5, pp.3147~ (2014)
- Hasegawa H, "The role of macrophage transcription factor MafB in atherosclerotic plaque stability", Atherosclerosis, 250, pp.133~143 (2016)
- Li Z, "Krüppel-like factor 4 regulation of cholesterol-25-hydroxylase and liver x receptor mitigates atherosclerosis susceptibility", Circulation, 136, pp.1315~1330 (2017)
- Gold ES, "ATF3 protects against atherosclerosis by suppressing 25-hydroxycholesterol-induced lipid body formation", J Exp Med, 209, pp.807~817 (2012)
- De Nardo D, "High-density lipoprotein mediates anti-inflammatory reprogramming of macrophages via the transcriptional regulator ATF3", Nat Immunol, 15, pp.152~160 (2014)
- Bekkering S, "Oxidized low-density lipoprotein induces long-term proinflammatory cytokine production and foam cell formation via epigenetic reprogramming of monocytes", Arterioscler Thromb Vasc Biol, 34, pp.1731~1738 (2014)
- Christ A, "Western diet triggers NLRP3-dependent innate immune reprogramming", Cell, 172, pp.162~175 (2018)
- 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)
- van der Valk FM, "Oxidized phospholipids on lipoprotein(a)elicit arterial wall inflammation and an inflammatory monocyte response in humans", Circulation, 134, pp.611~624 (2016)
- Bekkering S, "Innate immune cell activation and epigenetic remodeling in symptomatic and asymptomatic atherosclerosis in humans in vivo", Atherosclerosis, 254, pp.228~236 (2016)
- Woollard KJ, "Monocytes in atherosclerosis : subsets and functions", Nat Rev Cardiol, 7, pp.77~86 (2010)
- Gautier EL, "Regulation of the migration and survival of monocyte subsets by chemokine receptors and its relevance to atherosclerosis", Arterioscler Thromb Vasc Biol, 29, pp.1412~1418 (2009)
- Tacke F, "Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques", J Clin Invest, 117, pp.185~194 (2007)
- Smith JD, "Decreased atherosclerosis in mice deficient in both macrophage colony-stimulating factor(op)and apolipoprotein E", Proc Natl Acad Sci U S A, 92, pp.8264~8268 (1995)
- Rajavashisth T, "Heterozygous osteopetrotic(op)mutation reduces atherosclerosis in LDL receptor-deficient mice", J Clin Invest, 101, pp.2702~2710 (1998)
- Sinha SK, "Local M-CSF(macrophage colony-stimulating factor)expression regulates macrophage proliferation and apoptosis in atherosclerosis", Arterioscler Thromb Vasc Biol, 41, pp.220~233 (2021)
- Carlin LM, "Nr4a1-dependent Ly6C(low)monocytes monitor endothelial cells and orchestrate their disposal", Cell, 153, pp.362~375 (2013)
- Auffray C, "Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior", Science, 317, pp.666~670 (2007)
- Hanna RN, "The transcription factor NR4A1(Nur77)controls bone marrow differentiation and the survival of Ly6C-monocytes", Nat Immunol, 12, pp.778~785 (2011)
- Hanna RN, "NR4A1(Nur77)deletion polarizes macrophages toward an inflammatory phenotype and increases atherosclerosis", Circ Res, 110, pp.416~427 (2012)
- Li P, "NR4A1 contributes to high-fat associated endothelial dysfunction by promoting CaMKII-Parkin-mitophagy pathways", Cell Stress Chaperones, 23, pp.749~761 (2018)
- Robbins CS, "Local proliferation dominates lesional macrophage accumulation in atherosclerosis", Nat Med, 19, pp.1166~1172 (2013)
- Schyns J, "Non-classical tissue monocytes and two functionally distinct populations of interstitial macrophages populate the mouse lung", Nat Commun, 10, pp.3964~ (2019)
- Feig JE, "Reversal of hyperlipidemia with a genetic switch favorably affects the content and inflammatory state of macrophages in atherosclerotic plaques", Circulation, 123, pp.989~998 (2011)
- Feig JE, "HDL promotes rapid atherosclerosis regression in mice and alters inflammatory properties of plaque monocyte-derived cells", Proc Natl Acad Sci U S A, 108, pp.7166~7171 (2011)
- Lieu HD, "Eliminating atherogenesis in mice by switching off hepatic lipoprotein secretion", Circulation, 107, pp.1315~1321 (2003)
- Llodrá J, "Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques", Proc Natl Acad Sci U S A, 101, pp.11779~11784 (2004)
- Dubland JA, "So Much Cholesterol : the unrecognized importance of smooth muscle cells in atherosclerotic foam cell formation", Curr Opin Lipidol, 27, pp.155~161 (2016)
- Cherepanova OA, "Activation of the pluripotency factor OCT4 in smooth muscle cells is atheroprotective", Nat Med, 22, pp.657~665 (2016)
- Rong JX, "Transdifferentiation of mouse aortic smooth muscle cells to a macrophage-like state after cholesterol loading", Proc Natl Acad Sci U S A, 100, pp.13531~13536 (2003)
- Shankman LS, "KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis", Nat Med, 21, pp.628~637 (2015)
- Holycross BJ, "Platelet-derived growth factor-BB-induced suppression of smooth muscle cell differentiation", Circ Res, 71, pp.1525~1532 (1992)
- Barrett TB, "Platelet-derived growth factor gene expression in human atherosclerotic plaques and normal artery wall", Proc Natl Acad Sci U S A, 85, pp.2810~2814 (1988)
- Owens GK, "Molecular regulation of vascular smooth muscle cell differentiation in development and disease", Physiol Rev, 84, pp.767~801 (2004)
- Williams KJ, "The response-to-retention hypothesis of early atherogenesis", Arterioscler Thromb Vasc Biol, 15, pp.551~561 (1995)
- Ma S, "Oleic acid induces smooth muscle foam cell formation and enhances atherosclerotic lesion development via CD36", Lipids Health Dis, 10, pp.53~ (2011)
- Costales P, "K domain CR9 of low density lipoprotein(LDL)receptor-related protein 1(LRP1)is critical for aggregated LDL-induced foam cell formation from human vascular smooth muscle cells", J Biol Chem, 290, pp.14852~14865 (2015)
- Rivera J, "Accumulation of serum lipids by vascular smooth muscle cells involves a macropinocytosis-like uptake pathway and is associated with the downregulation of the ATP-binding cassette transporter A1", Naunyn Schmiedebergs Arch Pharmacol, 386, pp.1081~1093 (2013)
- Allahverdian S, "Contribution of intimal smooth muscle cells to cholesterol accumulation and macrophage-like cells in human atherosclerosis", Circulation, 129, pp.1551~1559 (2014)
- Deaton RA, "Sp1-dependent activation of KLF4 is required for PDGF-BB-induced phenotypic modulation of smooth muscle", Am J Physiol Heart Circ Physiol, 296, pp.H1027~ (2009)
- Kapoor N, "Transcription factors STAT6 and KLF4implement macrophage polarization via the dual catalytic powers of MCPIP", J Immunol, 194, pp.6011~6023 (2015)
- Vengrenyuk Y, "Cholesterol loading reprograms the microRNA-143", 145-myocardin axis to convert aortic smooth muscle cells to a dysfunctional macrophage-like phenotype, 2015, pp.35, 535~546
- Feil S, "Transdifferentiation of vascular smooth muscle cells to macrophage-like cells during atherogenesis", Circ Res, 115, pp.662~667 (2014)
- Ridker PM, "Antiinflammatory therapy with canakinumab for atherosclerotic disease", N Engl J Med, 377, pp.1119~1131 (2017)
- Libby P, "Inducible interleukin-1 gene expression in human vascular smooth muscle cells", J Clin Invest, 78, pp.1432~1438 (1986)
- Libby P, "Endotoxin and tumor necrosis factor induce interleukin-1 gene expression in adult human vascular endothelial cells", Am J Pathol, 124, pp.179~185 (1986)
- Zhuang T, "Endothelial Foxp1 suppresses atherosclerosis via modulation of Nlrp3 inflammasome activation", Circ Res, 125, pp.590~605 (2019)
- Haneklaus M, "NLRP3 at the interface of metabolism and inflammation", Immunol Rev, 265, pp.53~62 (2015)
- Gomez D, "Interleukin-1β has atheroprotective effects in advanced atherosclerotic lesions of mice", Nat Med, 24, pp.1418~1429 (2018)
