Macrophages in the Pathogenesis of Atherosclerosis

A-Gonzalez, 2009, Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR, Immunity, 31, 245, 10.1016/j.immuni.2009.06.018 Abi-Younes, 2000, The stromal cell-derived factor-1 chemokine is a potent platelet agonist highly expressed in atherosclerotic plaques, Circ. Res., 86, 131, 10.1161/01.RES.86.2.131 Aouadi, 2009, Orally delivered siRNA targeting macrophage Map4k4 suppresses systemic inflammation, Nature, 458, 1180, 10.1038/nature07774 Arai, 2005, A role for the apoptosis inhibitory factor AIM/Spalpha/Api6 in atherosclerosis development, Cell Metab., 1, 201, 10.1016/j.cmet.2005.02.002 Arnold, 2007, Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis, J. Exp. Med., 204, 1057, 10.1084/jem.20070075 Babaev, 2008, Macrophage EP4 deficiency increases apoptosis and suppresses early atherosclerosis, Cell Metab., 8, 492, 10.1016/j.cmet.2008.09.005 Baetta, 2009, Role of polymorphonuclear neutrophils in atherosclerosis: Current state and future perspectives, Atherosclerosis, 210, 1, 10.1016/j.atherosclerosis.2009.10.028 Becker, 2010, A macrophage sterol-responsive network linked to atherogenesis, Cell Metab., 11, 125, 10.1016/j.cmet.2010.01.003 Bergmark, 2008, A novel function of lipoprotein [a] as a preferential carrier of oxidized phospholipids in human plasma, J. Lipid Res., 49, 2230, 10.1194/jlr.M800174-JLR200 Bobryshev, 2005, Dendritic cells in atherosclerosis: current status of the problem and clinical relevance, Eur. Heart J., 26, 1700, 10.1093/eurheartj/ehi282 Boyle, 2003, Tumor necrosis factor-alpha promotes macrophage-induced vascular smooth muscle cell apoptosis by direct and autocrine mechanisms, Arterioscler. Thromb. Vasc. Biol., 23, 1553, 10.1161/01.ATV.0000086961.44581.B7 Breslow, 1996, Mouse models of atherosclerosis, Science, 272, 685, 10.1126/science.272.5262.685 Brown, 1997, The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor, Cell, 89, 331, 10.1016/S0092-8674(00)80213-5 Brown, 1980, The cholesteryl ester cycle in macrophage foam cells. Continual hydrolysis and re-esterification of cytoplasmic cholesteryl esters, J. Biol. Chem., 255, 9344, 10.1016/S0021-9258(19)70568-7 Calkin, 2010, Liver x receptor signaling pathways and atherosclerosis, Arterioscler. Thromb. Vasc. Biol., 30, 1513, 10.1161/ATVBAHA.109.191197 Cannon, 2010, Safety of anacetrapib in patients with or at high risk for coronary heart disease, N. Engl. J. Med., 363, 2406, 10.1056/NEJMoa1009744 Chan, 2010, Spatiotemporal controlled delivery of nanoparticles to injured vasculature, Proc. Natl. Acad. Sci. USA, 107, 2213, 10.1073/pnas.0914585107 Chang, 2006, Cholesterol sensing, trafficking, and esterification, Annu. Rev. Cell Dev. Biol., 22, 129, 10.1146/annurev.cellbio.22.010305.104656 Choi, 2009, Identification of antigen-presenting dendritic cells in mouse aorta and cardiac valves, J. Exp. Med., 206, 497, 10.1084/jem.20082129 Coller, 2005, Leukocytosis and ischemic vascular disease morbidity and mortality: is it time to intervene?, Arterioscler. Thromb. Vasc. Biol., 25, 658, 10.1161/01.ATV.0000156877.94472.a5 Collins, 2009, Age-accelerated atherosclerosis correlates with failure to upregulate antioxidant genes, Circ. Res., 104, e42, 10.1161/CIRCRESAHA.108.188771 Curtiss, 2008, Emerging role of toll-like receptors in atherosclerosis, J. Lipid Res., 50 Suppl., S340 deGoma, 2008, Beyond high-density lipoprotein cholesterol levels evaluating high-density lipoprotein function as influenced by novel therapeutic approaches, J. Am. Coll. Cardiol., 51, 2199, 10.1016/j.jacc.2008.03.016 Deguchi, 2005, Matrix metalloproteinase-13/collagenase-3 deletion promotes collagen accumulation and organization in mouse atherosclerotic plaques, Circulation, 112, 2708, 10.1161/CIRCULATIONAHA.105.562041 Deguchi, 2006, Inflammation in atherosclerosis: visualizing matrix metalloproteinase action in macrophages in vivo, Circulation, 114, 55, 10.1161/CIRCULATIONAHA.106.619056 Duewell, 2010, NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals, Nature, 464, 1357, 10.1038/nature08938 Fadok, 1998, Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2, and PAF, J. Clin. Invest., 101, 890, 10.1172/JCI1112 Feig, 2010, LXR promotes the maximal egress of monocyte-derived cells from mouse aortic plaques during atherosclerosis regression, J. Clin. Invest., 120, 4415, 10.1172/JCI38911 Fryburg, 2011, Atherosclerosis drug development in jeopardy: the need for predictive biomarkers of treatment response, Sci. Transl. Med., 3, 72cm6, 10.1126/scitranslmed.3002029 Galis, 1994, Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques, J. Clin. Invest., 94, 2493, 10.1172/JCI117619 Gareus, 2008, Endothelial cell-specific NF-kappaB inhibition protects mice from atherosclerosis, Cell Metab., 8, 372, 10.1016/j.cmet.2008.08.016 Glass, 2001, Atherosclerosis. the road ahead, Cell, 104, 503, 10.1016/S0092-8674(01)00238-0 Goel, 2008, Site-specific effects of PECAM-1 on atherosclerosis in LDL receptor-deficient mice, Arterioscler. Thromb. Vasc. Biol., 28, 1996, 10.1161/ATVBAHA.108.172270 Goossens, 2010, Myeloid type I interferon signaling promotes atherosclerosis by stimulating macrophage recruitment to lesions, Cell Metab., 12, 142, 10.1016/j.cmet.2010.06.008 Gough, 2006, Macrophage expression of active MMP-9 induces acute plaque disruption in apoE-deficient mice, J. Clin. Invest., 116, 59, 10.1172/JCI25074 Han, 2006, Macrophage insulin receptor deficiency increases ER stress-induced apoptosis and necrotic core formation in advanced atherosclerotic lesions, Cell Metab., 3, 257, 10.1016/j.cmet.2006.02.008 Han, 2010, Interleukin-10 overexpression in macrophages suppresses atherosclerosis in hyperlipidemic mice, FASEB J., 24, 2869, 10.1096/fj.09-148155 Harry, 2008, Endothelial cell PECAM-1 promotes atherosclerotic lesions in areas of disturbed flow in ApoE-deficient mice, Arterioscler. Thromb. Vasc. Biol., 28, 2003, 10.1161/ATVBAHA.108.164707 Henson, 2001, Apoptotic cell removal, Curr. Biol., 11, R795, 10.1016/S0960-9822(01)00474-2 Jerome, 2006, Advanced atherosclerotic foam cell formation has features of an acquired lysosomal storage disorder, Rejuvenation Res., 9, 245, 10.1089/rej.2006.9.245 Johnson, 2009, Macrophage heterogeneity in atherosclerotic plaques, Curr. Opin. Lipidol., 20, 370, 10.1097/MOL.0b013e3283309848 Kadl, 2010, Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2, Circ. Res., 107, 737, 10.1161/CIRCRESAHA.109.215715 Kamei, 2010, New observations on the trafficking and diapedesis of monocytes, Curr. Opin. Hematol., 17, 43, 10.1097/MOH.0b013e3283333949 Kanters, 2003, Inhibition of NF-kappaB activation in macrophages increases atherosclerosis in LDL receptor-deficient mice, J. Clin. Invest., 112, 1176, 10.1172/JCI200318580 Koenen, 2009, Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice, Nat. Med., 15, 97, 10.1038/nm.1898 Kruth, 2005, Macropinocytosis is the endocytic pathway that mediates macrophage foam cell formation with native low density lipoprotein, J. Biol. Chem., 280, 2352, 10.1074/jbc.M407167200 Kunjathoor, 2002, Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages, J. Biol. Chem., 277, 49982, 10.1074/jbc.M209649200 León, 2005, Monocyte-derived dendritic cells, Semin. Immunol., 17, 313, 10.1016/j.smim.2005.05.013 Li, 2009, Defective phagocytosis of apoptotic cells by macrophages in atherosclerotic lesions of ob/ob mice and reversal by a fish oil diet, Circ. Res., 105, 1072, 10.1161/CIRCRESAHA.109.199570 Liu, 2004, Lysosomal cysteine proteases in atherosclerosis, Arterioscler. Thromb. Vasc. Biol., 24, 1359, 10.1161/01.ATV.0000134530.27208.41 Liu, 2005, Reduced macrophage apoptosis is associated with accelerated atherosclerosis in low-density lipoprotein receptor-null mice, Arterioscler. Thromb. Vasc. Biol., 25, 174, 10.1161/01.ATV.0000148548.47755.22 Lloyd-Jones, 2010, Executive summary: heart disease and stroke statistics—2010 update: a report from the American Heart Association, Circulation, 121, 948, 10.1161/CIRCULATIONAHA.109.192666 Lotta, 2010, Genome-wide association studies in atherothrombosis, Eur. J. Intern. Med., 21, 74, 10.1016/j.ejim.2009.11.003 Lusis, 2007, The problem of passenger genes in transgenic mice, Arterioscler. Thromb. Vasc. Biol., 27, 2100, 10.1161/ATVBAHA.107.147918 Lutgens, 2010, Deficient CD40-TRAF6 signaling in leukocytes prevents atherosclerosis by skewing the immune response toward an antiinflammatory profile, J. Exp. Med., 207, 391, 10.1084/jem.20091293 Manning-Tobin, 2009, Loss of SR-A and CD36 activity reduces atherosclerotic lesion complexity without abrogating foam cell formation in hyperlipidemic mice, Arterioscler. Thromb. Vasc. Biol., 29, 19, 10.1161/ATVBAHA.108.176644 Martinon, 2010, TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages, Nat. Immunol., 11, 411, 10.1038/ni.1857 Maxfield, 2005, Role of cholesterol and lipid organization in disease, Nature, 438, 612, 10.1038/nature04399 Mehta, 2011, The novel atherosclerosis locus at 10q11 regulates plasma CXCL12 levels, Eur. Heart J., 10.1093/eurheartj/ehr091 Mestas, 2008, Monocyte-endothelial cell interactions in the development of atherosclerosis, Trends Cardiovasc. Med., 18, 228, 10.1016/j.tcm.2008.11.004 Moore, 2005, Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice, J. Clin. Invest., 115, 2192, 10.1172/JCI24061 Mukundan, 2009, PPARδ senses and orchestrates clearance of apoptotic cells to promote tolerance, Nat. Med., 15, 1266, 10.1038/nm.2048 Mullick, 2005, Modulation of atherosclerosis in mice by Toll-like receptor 2, J. Clin. Invest., 115, 3149, 10.1172/JCI25482 Myoishi, 2007, Increased endoplasmic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome, Circulation, 116, 1226, 10.1161/CIRCULATIONAHA.106.682054 Nakano, 2007, Catheter-based adenovirus-mediated anti-monocyte chemoattractant gene therapy attenuates in-stent neointima formation in cynomolgus monkeys, Atherosclerosis, 194, 309, 10.1016/j.atherosclerosis.2006.10.029 Paulson, 2010, Resident intimal dendritic cells accumulate lipid and contribute to the initiation of atherosclerosis, Circ. Res., 106, 383, 10.1161/CIRCRESAHA.109.210781 Potteaux, 2011, Suppressed monocyte recruitment drives macrophage removal from atherosclerotic plaques of Apoe-/- mice during disease regression, J. Clin. Invest., 121, 10.1172/JCI43802 Rajamäki, 2010, Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation, PLoS ONE, 5, e11765, 10.1371/journal.pone.0011765 Ranalletta, 2006, Decreased atherosclerosis in low-density lipoprotein receptor knockout mice transplanted with Abcg1-/- bone marrow, Arterioscler. Thromb. Vasc. Biol., 26, 2308, 10.1161/01.ATV.0000242275.92915.43 Rigamonti, 2008, Regulation of macrophage functions by PPAR-alpha, PPAR-gamma, and LXRs in mice and men, Arterioscler. Thromb. Vasc. Biol., 28, 1050, 10.1161/ATVBAHA.107.158998 Rosenfeld, 2002, Animal models of spontaneous plaque rupture: the holy grail of experimental atherosclerosis research, Curr. Atheroscler. Rep., 4, 238, 10.1007/s11883-002-0025-3 Ross, 1986, The pathogenesis of atherosclerosis—an update, N. Engl. J. Med., 314, 488, 10.1056/NEJM198602203140806 Rothblat, 2010, High-density lipoprotein heterogeneity and function in reverse cholesterol transport, Curr. Opin. Lipidol., 21, 229, 10.1097/MOL.0b013e328338472d Sadeghi, 2010, Imaging atherosclerosis and vulnerable plaque, J. Nucl. Med., 51, 51S, 10.2967/jnumed.109.068163 Sather, 2007, A soluble form of the Mer receptor tyrosine kinase inhibits macrophage clearance of apoptotic cells and platelet aggregation, Blood, 109, 1026, 10.1182/blood-2006-05-021634 Schiller, 2001, Effect of gamma-irradiation and bone marrow transplantation on atherosclerosis in LDL receptor-deficient mice, Arterioscler. Thromb. Vasc. Biol., 21, 1674, 10.1161/hq1001.096724 Schneider, 2008, Matrix-metalloproteinase-14 deficiency in bone-marrow-derived cells promotes collagen accumulation in mouse atherosclerotic plaques, Circulation, 117, 931, 10.1161/CIRCULATIONAHA.107.707448 Schrijvers, 2005, Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis, Arterioscler. Thromb. Vasc. Biol., 25, 1256, 10.1161/01.ATV.0000166517.18801.a7 Schulte, 2008, Genetically programmed biases in Th1 and Th2 immune responses modulate atherogenesis, Am. J. Pathol., 172, 1500, 10.2353/ajpath.2008.070776 Seimon, 2010, Induction of ER stress in macrophages of tuberculosis granulomas, PLoS ONE, 5, e12772, 10.1371/journal.pone.0012772 Seimon, 2010, Atherogenic lipids and lipoproteins trigger CD36-TLR2-dependent apoptosis in macrophages undergoing endoplasmic reticulum stress, Cell Metab., 12, 467, 10.1016/j.cmet.2010.09.010 Serhan, 2008, Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators, Nat. Rev. Immunol., 8, 349, 10.1038/nri2294 Shaposhnik, 2007, Granulocyte macrophage colony-stimulating factor regulates dendritic cell content of atherosclerotic lesions, Arterioscler. Thromb. Vasc. Biol., 27, 621, 10.1161/01.ATV.0000254673.55431.e6 Shibata, 2009, Regulation of macrophage function in inflammation and atherosclerosis, J. Lipid Res., 50, S277, 10.1194/jlr.R800063-JLR200 Smith, 2001, Genetic modifiers of atherosclerosis in mice, Ann. N Y Acad. Sci., 947, 247, 10.1111/j.1749-6632.2001.tb03946.x Steinberg, 2008, Evidence mandating earlier and more aggressive treatment of hypercholesterolemia, Circulation, 118, 672, 10.1161/CIRCULATIONAHA.107.753152 Stewart, 2010, CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer, Nat. Immunol., 11, 155, 10.1038/ni.1836 Stone, 2011, A prospective natural-history study of coronary atherosclerosis, N. Engl. J. Med., 364, 226, 10.1056/NEJMoa1002358 Sun, 2002, Lipoprotein(a) enhances advanced atherosclerosis and vascular calcification in WHHL transgenic rabbits expressing human apolipoprotein(a), J. Biol. Chem., 277, 47486, 10.1074/jbc.M205814200 Tabas, 2010, Macrophage death and defective inflammation resolution in atherosclerosis, Nat. Rev. Immunol., 10, 36, 10.1038/nri2675 Tabas, 2010, The role of endoplasmic reticulum stress in the progression of atherosclerosis, Circ. Res., 107, 839, 10.1161/CIRCRESAHA.110.224766 Tabas, 2011, Molecular mechanisms integrating pathways of endoplasmic reticulum stress-induced apoptosis, Nat. Cell Biol., 13, 184, 10.1038/ncb0311-184 Tabas, 1993, J. Biol. Chem., 268, 20419, 10.1016/S0021-9258(20)80745-5 Tabas, 2010, The impact of macrophage insulin resistance on advanced atherosclerotic plaque progression, Circ. Res., 106, 58, 10.1161/CIRCRESAHA.109.208488 Tacke, 2007, Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques, J. Clin. Invest., 117, 185, 10.1172/JCI28549 Tall, 2008, HDL, ABC transporters, and cholesterol efflux: implications for the treatment of atherosclerosis, Cell Metab., 7, 365, 10.1016/j.cmet.2008.03.001 Tang, 2009, The macrophage cholesterol exporter ABCA1 functions as an anti-inflammatory receptor, J. Biol. Chem., 284, 32336, 10.1074/jbc.M109.047472 Tarling, 2010, Impaired development of atherosclerosis in Abcg1-/- Apoe-/- mice: identification of specific oxysterols that both accumulate in Abcg1-/- Apoe-/- tissues and induce apoptosis, Arterioscler. Thromb. Vasc. Biol., 30, 1174, 10.1161/ATVBAHA.110.205617 Tarr, 2008, ABCG1 and ABCG4 are coexpressed in neurons and astrocytes of the CNS and regulate cholesterol homeostasis through SREBP-2, J. Lipid Res., 49, 169, 10.1194/jlr.M700364-JLR200 Thorp, 2009, Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of Apoe-/- and Ldlr-/- mice lacking CHOP, Cell Metab., 9, 474, 10.1016/j.cmet.2009.03.003 Timmins, 2009, Calcium/calmodulin-dependent protein kinase II links endoplasmic reticulum stress with Fas and mitochondrial apoptosis pathways, J. Clin. Invest., 119, 2925, 10.1172/JCI38857 Trégouët, 2009, Genome-wide haplotype association study identifies the SLC22A3-LPAL2-LPA gene cluster as a risk locus for coronary artery disease, Nat. Genet., 41, 283, 10.1038/ng.314 Tsukano, 2010, The endoplasmic reticulum stress-C/EBP homologous protein pathway-mediated apoptosis in macrophages contributes to the instability of atherosclerotic plaques, Arterioscler. Thromb. Vasc. Biol., 30, 1925, 10.1161/ATVBAHA.110.206094 Virmani, 2002, Vulnerable plaque: the pathology of unstable coronary lesions, J. Interv. Cardiol., 15, 439, 10.1111/j.1540-8183.2002.tb01087.x Wilensky, 2009, Lipoprotein-associated phospholipase A(2) and atherosclerosis, Curr. Opin. Lipidol., 20, 415, 10.1097/MOL.0b013e3283307c16 Williams, 1995, The response-to-retention hypothesis of early atherogenesis, Arterioscler. Thromb. Vasc. Biol., 15, 551, 10.1161/01.ATV.15.5.551 Williams, 2005, Oxidation, lipoproteins, and atherosclerosis: which is wrong, the antioxidants or the theory?, Curr. Opin. Clin. Nutr. Metab. Care, 8, 139, 10.1097/00075197-200503000-00006 Witztum, 2001, The oxidative modification hypothesis of atherosclerosis: does it hold for humans?, Trends Cardiovasc. Med., 11, 93, 10.1016/S1050-1738(01)00111-6 Yancey, 2010, Macrophage LRP-1 controls plaque cellularity by regulating efferocytosis and AKT activation, Arterioscler. Thromb. Vasc. Biol., 30, 787, 10.1161/ATVBAHA.109.202051 Yvan-Charvet, 2007, Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice, J. Clin. Invest., 117, 3900 Yvan-Charvet, 2010, ATP-binding cassette transporters and HDL suppress hematopoietic stem cell proliferation, Science, 328, 1689, 10.1126/science.1189731 Yvan-Charvet, 2010, ABCA1 and ABCG1 protect against oxidative stress-induced macrophage apoptosis during efferocytosis, Circ. Res., 106, 1861, 10.1161/CIRCRESAHA.110.217281 Zhu, 2008, Increased cellular free cholesterol in macrophage-specific Abca1 knock-out mice enhances pro-inflammatory response of macrophages, J. Biol. Chem., 283, 22930, 10.1074/jbc.M801408200