The CD44-HA axis and inflammation in atherosclerosis: A temporal perspective

Matrix Biology - Tập 78 - Trang 201-218 - 2019
Mia Krolikoski1, James Monslow1, Ellen Puré1
1University of Pennsylvania, 380 S. University Avenue, Philadelphia, PA 19104, United States

Tài liệu tham khảo

Benjamin, 2017, Heart disease and stroke statistics—2017 update: a report from the American Heart Association, Circulation, 10.1161/CIR.0000000000000485 Kaperonis, 2006, Inflammation and atherosclerosis, Eur. J. Vasc. Endovasc. Surg., 31, 386, 10.1016/j.ejvs.2005.11.001 Galkina, 2009, Immune and inflammatory mechanisms of atherosclerosis, Annu. Rev. Immunol., 27, 165, 10.1146/annurev.immunol.021908.132620 Yash Prashar, 2017, Emerging role of various signaling pathways in the pathogenesis and therapeutics of atherosclerosis, Vasc. Med., 10–11, 1 Johnson, 2009, CD44 and its role in inflammation and inflammatory diseases, Inflamm. Allergy Drug Targets., 8, 208, 10.2174/187152809788680994 Puré, 2001, A crucial role for CD44 in inflammation, Trends Mol. Med., 7, 213, 10.1016/S1471-4914(01)01963-3 Cichy, 2004, Cytokines regulate the affinity of soluble CD44 for hyaluronan, FEBS Lett., 556, 69, 10.1016/S0014-5793(03)01370-X Goodison, 1999, CD44 cell adhesion molecules, Mol. Pathol., 52, 189, 10.1136/mp.52.4.189 Monslow, 2015, Hyaluronan - a functional and structural sweet spot in the tissue microenvironment, Front. Immunol., 6, 10.3389/fimmu.2015.00231 Wight, 2017, Provisional matrix: a role for versican and hyaluronan, Matrix Biol., 60–61, 38, 10.1016/j.matbio.2016.12.001 Hascall, 2014, The dynamic metabolism of hyaluronan regulates the cytosolic concentration of UDP-GlcNAc, Matrix Biol., 35, 14, 10.1016/j.matbio.2014.01.014 Vigetti, 2014, Hyaluronan: biosynthesis and signaling, Biochim. Biophys. Acta Gen. Subj., 1840, 2452, 10.1016/j.bbagen.2014.02.001 Viola, 2008, Molecular control of the hyaluronan biosynthesis, Connect. Tissue Res., 49, 111, 10.1080/03008200802148405 Siiskonen, 2015, Hyaluronan synthase 1: a mysterious enzyme with unexpected functions, Front. Immunol., 6, 10.3389/fimmu.2015.00043 Kiene, 2016, Deletion of hyaluronan synthase 3 inhibits neointimal hyperplasia in mice, Arterioscler. Thromb. Vasc. Biol., 36, e9, 10.1161/ATVBAHA.115.306607 Albright, 2014, Genetic network identifies novel pathways contributing to atherosclerosis susceptibility in the innominate artery, BMC Med. Genomics, 7, 10.1186/1755-8794-7-51 Zhao, 2008, CD44 expressed on both bone marrow-derived and non-bone marrow-derived cells promotes atherogenesis in ApoE-deficient mice, Arterioscler. Thromb. Vasc. Biol., 28, 1283, 10.1161/ATVBAHA.108.165753 Cuff, 2001, The adhesion receptor CD44 promotes atherosclerosis by mediating inflammatory cell recruitment and vascular cell activation, J. Clin. Invest., 108, 1031, 10.1172/JCI200112455 Hägg, 2007, Augmented levels of CD44 in macrophages from atherosclerotic subjects: a possible IL-6-CD44 feedback loop?, Atherosclerosis, 190, 291, 10.1016/j.atherosclerosis.2006.03.020 Zhao, 2007, CD44 regulates vascular gene expression in a proatherogenic environment, Arterioscler. Thromb. Vasc. Biol., 27, 886, 10.1161/01.ATV.0000259362.10882.c5 Dattilo, 1998, Hypercholesterolemia alters the gene expression of novel components of the extracellular matrix in experimental vein grafts, Ann. Vasc. Surg., 12, 168, 10.1007/s100169900136 Passerini, 2004, Coexisting proinflammatory and antioxidative endothelial transcription profiles in a disturbed flow region of the adult porcine aorta, Proc. Natl. Acad. Sci. U. S. A., 101, 2482, 10.1073/pnas.0305938101 Sjöberg, 2009, CD44-deficiency on hematopoietic cells limits T-cell number but does not protect against atherogenesis in LDL receptor-deficient mice, Atherosclerosis, 206, 369, 10.1016/j.atherosclerosis.2009.03.002 Getz, 2017, Animal Models of Atherosclerosis, 205 Lee, 2017, Mouse models of atherosclerosis: a historical perspective and recent advances, Lipids Health Dis., 16, 10.1186/s12944-016-0402-5 Vigetti, 2008, Vascular pathology and the role of hyaluronan, Sci. World J., 8, 1116, 10.1100/tsw.2008.145 Papakonstantinou, 1998, The differential distribution of hyaluronic acid in the layers of human atheromatic aortas is associated with vascular smooth muscle cell proliferation and migration, Atherosclerosis, 138, 79, 10.1016/S0021-9150(98)00006-9 Lévesque, 1994, Localization and solubilization of hyaluronan and of the hyaluronan-binding protein hyaluronectin in human normal and arteriosclerotic arterial walls, Atherosclerosis, 105, 51, 10.1016/0021-9150(94)90007-8 Bot, 2010, Hyaluronic acid metabolism is increased in unstable plaques, Eur. J. Clin. Investig., 40, 818, 10.1111/j.1365-2362.2010.02326.x Kolodgie, 2004, The accumulation of specific types of proteoglycans in eroded plaques: a role in coronary thrombosis in the absence of rupture, Curr. Opin. Lipidol., 15, 575, 10.1097/00041433-200410000-00012 Kolodgie, 2002, Differential accumulation of proteoglycans and hyaluronan in culprit lesions: insights into plaque erosion, Arterioscler. Thromb. Vasc. Biol., 22, 1642, 10.1161/01.ATV.0000034021.92658.4C Krupinski, 2007, 361 Chai, 2005, Overexpression of hyaluronan in the tunica media promotes the development of atherosclerosis, Circ. Res., 96, 583, 10.1161/01.RES.0000158963.37132.8b Kucur, 2009, Plasma hyaluronidase activity as an indicator of atherosclerosis in patients with coronary artery disease, Bratislava, Med. J., 110, 21 Krettek, 2009, CD44 - a new cardiovascular drug target or merely an innocent bystander?, Cardiovasc. Hematol. Disord. Drug Targets, 9, 293, 10.2174/1871529X10909040293 V., 2016, Extracellular matrix in atherosclerosis: hyaluronan and proteoglycan insights, Curr. Med. Chem., 23, 2958, 10.2174/0929867323666160607104602 Moretto, 2015, Regulation of hyaluronan synthesis in vascular diseases and diabetes, J. Diabetes Res., 2015, 10.1155/2015/167283 Sadowitz, 2012, The role of hyaluronic acid in atherosclerosis and intimal hyperplasia, J. Surg. Res., 173, 10.1016/j.jss.2011.09.025 Wight, 2008, Arterial remodeling in vascular disease: a key role for hyaluronan and versican, Front. Biosci., 13, 4933, 10.2741/3052 Karangelis, 2012, Glycosaminoglycans as key molecules in atherosclerosis: the role of versican and hyaluronan, Curr. Med. Chem., 17, 4018, 10.2174/092986710793205354 Riessen, 1996, Distribution of hyaluronan during extracellular matrix remodeling in human restenotic arteries and balloon-injured rat carotid arteries, Circulation, 93, 1141, 10.1161/01.CIR.93.6.1141 Bot, 2008, Hyaluronic acid: targeting immune modulatory components of the extracellular matrix in atherosclerosis, Curr. Med. Chem., 15, 786, 10.2174/092986708783955554 Slevin, 2007, Hyaluronan-mediated angiogenesis in vascular disease: uncovering RHAMM and CD44 receptor signaling pathways, Matrix Biol., 26, 58, 10.1016/j.matbio.2006.08.261 Sakr, 2008, Hyaluronan accumulation is elevated in cultures of low density lipoprotein receptor-deficient cells and is altered by manipulation of cell cholesterol content, J. Biol. Chem., 283, 36195, 10.1074/jbc.M807772200 Vendrov, 2010, NADPH oxidases regulate CD44 and hyaluronic acid expression in thrombin-treated vascular smooth muscle cells and in atherosclerosis, J. Biol. Chem., 285, 26545, 10.1074/jbc.M110.143917 Vendrov, 2006, Thrombin and NAD(P)H oxidase-mediated regulation of CD44 and BMP4-Id pathway in VSMC, restenosis, and atherosclerosis, Circ. Res., 98, 1254, 10.1161/01.RES.0000221214.37803.79 Wang, 2011, Hyaluronan matrices in pathobiological processes, FEBS J., 278, 1412, 10.1111/j.1742-4658.2011.08069.x Karousou, 2017, Roles and targeting of the HAS/hyaluronan/CD44 molecular system in cancer, Matrix Biol., 59, 3, 10.1016/j.matbio.2016.10.001 Hascall, 2011, Regulatory roles of hyaluronan in health and disease, FEBS J., 278, 1411, 10.1111/j.1742-4658.2011.08068.x Evanko, 2012, Hyaluronan and versican in the control of human T-lymphocyte adhesion and migration, Matrix Biol., 31, 90, 10.1016/j.matbio.2011.10.004 Hascall, 2004, Intracellular hyaluronan: a new frontier for inflammation?, Biochim. Biophys. Acta Gen. Subj., 1673, 3, 10.1016/j.bbagen.2004.02.013 Evanko, 1999, Formation of hyaluronan-and versican-rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells, Arterioscler. Thromb. Vasc. Biol., 19, 1004, 10.1161/01.ATV.19.4.1004 Day, 2005, Hyaluronan cross-linking: a protective mechanism in inflammation?, Trends Immunol., 26, 637, 10.1016/j.it.2005.09.009 Misra, 2015, Interactions between hyaluronan and its receptors (CD44, RHAMM) regulate the activities of inflammation and cancer, Front. Immunol., 6, 10.3389/fimmu.2015.00201 Jiang, 2011, Hyaluronan as an immune regulator in human diseases, Physiol. Rev., 91, 221, 10.1152/physrev.00052.2009 Theocharis, 2017, Proteoglycans remodeling in cancer: underlying molecular mechanisms, Matrix Biol. Vigetti, 2008, Hyaluronan-CD44-ERK1/2 regulate human aortic smooth muscle cell motility during aging, J. Biol. Chem., 283, 4448, 10.1074/jbc.M709051200 Toole, 2002, Hyaluronan-cell interactions in cancer and vascular disease, J. Biol. Chem., 277, 4593, 10.1074/jbc.R100039200 Misra, 2011, Hyaluronan-CD44 interactions as potential targets for cancer therapy, FEBS J., 278, 1429, 10.1111/j.1742-4658.2011.08071.x Vigetti, 2009, The effects of 4-methylumbelliferone on hyaluronan synthesis, MMP2 activity, proliferation, and motility of human aortic smooth muscle cells, Glycobiology, 19, 537, 10.1093/glycob/cwp022 Vigetti, 2008, Aortic smooth muscle cells migration and the role of metalloproteinases and hyaluronan, Connect. Tissue Res., 49, 189, 10.1080/03008200802143141 Bollyky, 2012, The role of hyaluronan and the extracellular matrix in islet inflammation and immune regulation, Curr. Diab. Rep., 12, 471, 10.1007/s11892-012-0297-0 Nagy, 2015, 4-Methylumbelliferone treatment and hyaluronan inhibition as a therapeutic strategy in inflammation, autoimmunity, and cancer, Front. Immunol., 6, 10.3389/fimmu.2015.00123 Wilkinson, 2006, Overexpression of hyaluronan synthases alters vascular smooth muscle cell phenotype and promotes monocyte adhesion, J. Cell. Physiol., 206, 378, 10.1002/jcp.20468 Lemire, 2002, Overexpression of the V3 variant of versican alters arterial smooth muscle cell adhesion, migration, and proliferation in vitro, J. Cell. Physiol., 190, 38, 10.1002/jcp.10043 Karousou, 2014, Collagen VI and hyaluronan: the common role in breast cancer, Biomed. Res. Int., 2014, 10.1155/2014/606458 Vigetti, 2014, Epigenetics in extracellular matrix remodeling and hyaluronan metabolism, FEBS J., 281, 4980, 10.1111/febs.12938 Vigetti, 2010, Proinflammatory cytokines induce hyaluronan synthesis and monocyte adhesion in human endothelial cells through hyaluronan synthase 2 (HAS2) and the nuclear factor-kappaB (NF-kappaB) pathway, J. Biol. Chem., 285, 24639, 10.1074/jbc.M110.134536 Liu, 2014, Oxidized low-density lipoprotein increases the proliferation and migration of human coronary artery smooth muscle cells through the upregulation of osteopontin, Int. J. Mol. Med., 33, 1341, 10.3892/ijmm.2014.1681 Chang, 2014, Reprint of: a rapid increase in macrophage-derived versican and hyaluronan in infectious lung disease, Matrix Biol., 35, 162, 10.1016/j.matbio.2014.04.003 Li, 2000, Antisense to LOX-1 inhibits oxidized LDL-mediated upregulation of monocyte chemoattractant protein-1 and monocyte adhesion to human coronary artery endothelial cells, Circulation, 101, 2889, 10.1161/01.CIR.101.25.2889 Li, 2003, LOX-1 mediates oxidized low-density lipoprotein-induced expression of matrix metalloproteinases in human coronary artery endothelial cells, Circulation, 107, 612, 10.1161/01.CIR.0000047276.52039.FB Magalhaes, 2016, LDL-cholesterol increases the transcytosis of molecules through endothelial monolayers, PLoS One, 11, 10.1371/journal.pone.0163988 Vink, 2000, Oxidized lipoproteins degrade the endothelia4 surface layer: implications for platelet-endothelial cell adhesion, Circulation, 101, 1500, 10.1161/01.CIR.101.13.1500 Kolářová, 2014, Modulation of endothelial glycocalyx structure under inflammatory conditions, Mediat. Inflamm., 2014, 10.1155/2014/694312 Nagy, 2010, Inhibition of hyaluronan synthesis accelerates murine atherosclerosis: novel insights into the role of hyaluronan synthesis, Circulation, 122, 2313, 10.1161/CIRCULATIONAHA.110.972653 Mambetsariev, 2010, Hyaluronic acid binding protein 2 is a novel regulator of vascular integrity, Arterioscler. Thromb. Vasc. Biol., 30, 483, 10.1161/ATVBAHA.109.200451 Singleton, 2010, High molecular weight hyaluronan is a novel inhibitor of pulmonary vascular leakiness, Am. J. Physiol. Lung Cell. Mol. Physiol., 299, L639, 10.1152/ajplung.00405.2009 Maroski, 2011, Shear stress increases endothelial hyaluronan synthase 2 and hyaluronan synthesis especially in regard to an atheroprotective flow profile, Exp. Physiol., 96, 977, 10.1113/expphysiol.2010.056051 Yu, 2015, Nuclear factor-κB activation as a pathological mechanism of lipid metabolism and atherosclerosis, Adv. Clin. Chem., 70, 1, 10.1016/bs.acc.2015.03.004 Oeckinghaus, 2009, The NF-κB family of transcription factors and its regulation, Cold Spring Harb. Perspect. Biol., 1, 10.1101/cshperspect.a000034 Gareus, 2008, Endothelial cell-specific NF-κB inhibition protects mice from atherosclerosis, Cell Metab., 8, 372, 10.1016/j.cmet.2008.08.016 Lockette, 1986, The loss of endothelium-dependent vascular relaxation in hypertension, Hypertension, 8, II61, 10.1161/01.HYP.8.6_Pt_2.II61 Anderson, 1995, Systemic nature of endothelial dysfunction in atherosclerosis, Am. J. Cardiol., 75, 10.1016/0002-9149(95)80017-M Napoli, 2006, Nitric oxide and atherosclerosis: an update, Nitric Oxide Biol. Chem., 15, 265, 10.1016/j.niox.2006.03.011 Singleton, 2004, CD44 interaction with ankyrin and IP3 receptor in lipid rafts promotes hyaluronan-mediated Ca2+ signaling leading to nitric oxide production and endothelial cell adhesion and proliferation, Exp. Cell Res., 295, 102, 10.1016/j.yexcr.2003.12.025 Virmani, 2002, Vulnerable plaque: the pathology of unstable coronary lesions, J. Interv. Cardiol., 15, 439, 10.1111/j.1540-8183.2002.tb01087.x Smith, 1995, Decreased atherosclerosis in mice deficient in both macrophage colony-stimulating factor (op) and apolipoprotein E, Proc. Natl. Acad. Sci. U. S. A., 92, 8264, 10.1073/pnas.92.18.8264 Mantovani, 2013, Tumor-associated macrophages as a paradigm of macrophage plasticity, diversity, and polarization lessons and open questions, Arterioscler. Thromb. Vasc. Biol., 33, 1478, 10.1161/ATVBAHA.113.300168 Khallou-Laschet, 2010, Macrophage plasticity in experimental atherosclerosis, PLoS ONE, 5, 10.1371/journal.pone.0008852 Moore, 2013, Macrophages in atherosclerosis: a dynamic balance, Nat. Rev. Immunol., 13, 709, 10.1038/nri3520 Hodge-Dufour, 1997, Induction of IL-12 and chemokines by hyaluronan requires adhesion-dependent priming of resident but not elicited macrophages, J. Immunol., 159, 2492, 10.4049/jimmunol.159.5.2492 Cybulsky, 2016, Macrophages and dendritic cells: partners in atherogenesis, Circ. Res., 118, 637, 10.1161/CIRCRESAHA.115.306542 Marques, 2016, Iron gene expression profile in atherogenic Mox macrophages, Biochim. Biophys. Acta Mol. Basis Dis., 1862, 1137, 10.1016/j.bbadis.2016.03.004 de Gaetano, 2016, M1- and M2-type macrophage responses are predictive of adverse outcomes in human atherosclerosis, Front. Immunol., 7, 10.3389/fimmu.2016.00275 Stöger, 2012, Distribution of macrophage polarization markers in human atherosclerosis, Atherosclerosis, 225, 461, 10.1016/j.atherosclerosis.2012.09.013 Hoeksema, 2012, Molecular pathways regulating macrophage polarization: implications for atherosclerosis, Curr Atheroscler Rep, 14, 254, 10.1007/s11883-012-0240-5 Chinetti-Gbaguidi, 2011, Human atherosclerotic plaque alternative macrophages display low cholesterol handling but high phagocytosis because of distinct activities of the PPARγ and LXRα pathways, Circ. Res., 108, 985, 10.1161/CIRCRESAHA.110.233775 Wang, 2014, Molecular mechanisms that influence the macrophage M1-M2 polarization balance, Front. Immunol., 5, 10.3389/fimmu.2014.00614 Park, 2012, Myeloid-specific IkappaB kinase beta deficiency decreases atherosclerosis in low-density lipoprotein receptor-deficient mice, Arter. Thromb. Vasc. Biol., 32, 2869, 10.1161/ATVBAHA.112.254573 Goossens, 2011, Myeloid IκBα deficiency promotes atherogenesis by enhancing leukocyte recruitment to the plaques, PLoS One, 6, 10.1371/journal.pone.0022327 Detmers, 2000, Deficiency in inducible nitric oxide synthase results in reduced atherosclerosis in apolipoprotein E-deficient mice, J. Immunol., 165, 3430, 10.4049/jimmunol.165.6.3430 Huang, 2014, Induction of inducible nitric oxide synthase (iNOS) expression by oxLDL inhibits macrophage derived foam cell migration, Atherosclerosis, 235, 213, 10.1016/j.atherosclerosis.2014.04.020 Janani, 2015, PPAR gamma gene – a review, Diabetes Metab. Syndr. Clin. Res. Rev., 9, 46, 10.1016/j.dsx.2014.09.015 Bouhlel, 2007, PPARγ activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties, Cell Metab., 6, 137, 10.1016/j.cmet.2007.06.010 Chinetti, 2001, PPAR-α and PPAR-γ activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway, Nat. Med., 7, 53, 10.1038/83348 Moore, 2001, The role of PPAR-gamma in macrophage differentiation and cholesterol uptake, Nat. Med., 7, 41, 10.1038/83328 Li, 2004, Differential inhibition of macrophage foam-cell formation and atherosclerosis in mice by PPARalpha, beta/delta, and gamma, J. Clin. Invest., 114, 1564, 10.1172/JCI18730 Mahamuni, 2012, Therapeutic approaches to drug targets in hyperlipidemia, Biomedicine, 2, 137, 10.1016/j.biomed.2012.08.002 Jiang, 1998, PPAR-γ agonists inhibit production of monocyte inflammatory cytokines, Nature, 391, 82, 10.1038/34184 Law, 1996, Troglitazone inhibits vascular smooth muscle cell growth and intimal hyperplasia, J. Clin. Invest., 98, 1897, 10.1172/JCI118991 Hollingsworth, 2007, CD44 regulates macrophage recruitment to the lung in lipopolysaccharide-induced airway disease, Am. J. Respir. Cell Mol. Biol., 37, 248, 10.1165/rcmb.2006-0363OC Leemans, 2003, CD44 is a macrophage binding site for Mycobacterium tuberculosis that mediates macrophage recruitment and protective immunity against tuberculosis, J. Clin. Invest., 111, 681, 10.1172/JCI200316936 Weiss, 1998, Activation-dependent modulation of hyaluronate-receptor expression and of hyaluronate-avidity by human monocytes, J. Invest. Dermatol., 111, 227, 10.1046/j.1523-1747.1998.00286.x Levesque, 1997, Cytokine induction of the ability of human monocyte CD44 to bind hyaluronan is mediated primarily by TNF-alpha and is inhibited by IL-4 and IL-13, J. Immunol., 159, 6184, 10.4049/jimmunol.159.12.6184 Levesque, 2001, Activated T lymphocytes regulate hyaluronan binding to monocyte CD44 via production of IL-2 and IFN-gamma, J. Immunol., 166, 188, 10.4049/jimmunol.166.1.188 Levesque, 1999, TNFalpha and IL-4 regulation of hyaluronan binding to monocyte CD44 involves posttranslational modification of CD44, Cell. Immunol., 193, 209, 10.1006/cimm.1999.1456 Ruffell, 2011, Differential use of chondroitin sulfate to regulate hyaluronan binding by receptor CD44 in inflammatory and interleukin 4-activated macrophages, J. Biol. Chem., 286, 19179, 10.1074/jbc.M110.200790 Brown, 2001, Role of sulfation in CD44-mediated hyaluronan binding induced by inflammatory mediators in human CD14(+) peripheral blood monocytes, J. Immunol., 167, 5367, 10.4049/jimmunol.167.9.5367 McKee, 1996, Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages: the role of HA size and CD44, J. Clin. Invest., 98, 2403, 10.1172/JCI119054 Rayahin, 2015, High and low molecular weight hyaluronic acid differentially influence macrophage activation, ACS Biomater. Sci. Eng., 1, 481, 10.1021/acsbiomaterials.5b00181 McKee, 1997, Hyaluronan fragments induce nitric-oxide synthase in murine macrophages through a nuclear factor κB-dependent mechanism, J. Biol. Chem., 272, 8013, 10.1074/jbc.272.12.8013 Yamawaki, 2009, Hyaluronan receptors involved in cytokine induction in monocytes, Glycobiology, 19, 83, 10.1093/glycob/cwn109 He, 2013, Immobilized heavy chain-hyaluronic acid polarizes lipopolysaccharide-activated macrophages toward m2 phenotype, J. Biol. Chem., 288, 25792, 10.1074/jbc.M113.479584 Noble, 1996, Hyaluronan fragments activate an NFKB/IKBa autoregulatory loop in murine macrophages, J. Exp. Med., 183, 2373, 10.1084/jem.183.5.2373 Steffan, 1995, Regulation of IkB alpha phosphorylation by PKC- and Ca(2+)-dependent signal transduction pathways, J. Immunol., 155, 4685, 10.4049/jimmunol.155.10.4685 Oertli, 1998, Mechanisms of hyaluronan-induced up-regulation of ICAM-1 and VCAM-1 expression by murine kidney tubullar epithelial cells: hyaluronan triggers cell adhesion molecule expression through a mechanism involving activation of nuclear factor-kappa B and activat, J. Immunol., 161, 3431, 10.4049/jimmunol.161.7.3431 Bollyky, 2009, CD44 costimulation promotes FoxP3+ regulatory T cell persistence and function via production of IL-2, IL-10, and TGF, J. Immunol., 183, 2232, 10.4049/jimmunol.0900191 Tse, 2013, T cells in atherosclerosis, Int. Immunol., 25, 615, 10.1093/intimm/dxt043 Baaten, 2010, Multifaceted regulation of T cells by CD44, Commun. Integr. Biol., 3, 508, 10.4161/cib.3.6.13495 Siegelman, 2000, The CD44-initiated pathway of T-cell extravasation uses VLA-4 but not LFA-1 for firm adhesion, J. Clin. Invest., 105, 683, 10.1172/JCI8692 Bonder, 2006, Use of CD44 by CD4+ Th1 and Th2 lymphocytes to roll and adhere, Blood, 107, 4798, 10.1182/blood-2005-09-3581 Homann, 2017, Hyaluronan synthase 3 promotes plaque inflammation and atheroprogression, Matrix Biol. Ait-Oufella, 2006, Natural regulatory T cells control the development of atherosclerosis in mice, Nat. Med., 12, 178, 10.1038/nm1343 Chistiakov, 2015, Vascular smooth muscle cell in atherosclerosis, Acta Physiol. (Oxf.), 214, 33, 10.1111/apha.12466 Foster, 1998, Regulation of CD44 gene expression by the proinflammatory cytokine interleukin-1 beta in vascular smooth muscle cells, J. Biol. Chem., 273, 20341, 10.1074/jbc.273.32.20341 Rudijanto, 2007, The role of vascular smooth muscle cells on the pathogenesis of atherosclerosis, Acta Med. Indones., 39, 86 Allahverdian, 2012, Contribution of monocyte-derived macrophages and smooth muscle cells to arterial foam cell formation, Cardiovasc. Res., 95, 165, 10.1093/cvr/cvs094 Lao, 2015, Endothelial and smooth muscle cell transformation in atherosclerosis, Curr. Opin. Lipidol., 26, 10.1097/MOL.0000000000000219 Cecchettini, 2011, Vascular smooth-muscle-cell activation. Proteomics point of view, Int. Rev. Cell Mol. Biol., 288, 43, 10.1016/B978-0-12-386041-5.00002-9 Lepidi, 2001, MMP9 production by human monocyte-derived macrophages is decreased on polymerized type I collagen, J. Vasc. Surg., 34, 1111, 10.1067/mva.2001.119401 Wesley, 1998, Extracellular matrix modulates macrophage functions characteristic to atheroma: collagen type I enhances acquisition of resident macrophage traits by human peripheral blood monocytes in vitro, Arterioscler. Thromb. Vasc. Biol., 18, 432, 10.1161/01.ATV.18.3.432 Kaplan, 1982, In vitro differentiation of human monocytes. Differences in monocyte phenotypes induced by cultivation on glass or on collagen, J. Exp. Med., 156, 1101, 10.1084/jem.156.4.1101 Rong, 2003, Transdifferentiation of mouse aortic smooth muscle cells to a macrophage-like state after cholesterol loading, Proc. Natl. Acad. Sci. U. S. A., 100, 13531, 10.1073/pnas.1735526100 Grandoch, 2013, Novel effects of adenosine receptors on pericellular hyaluronan matrix: implications for human smooth muscle cell phenotype and interactions with monocytes during atherosclerosis, Basic Res. Cardiol., 108, 10.1007/s00395-013-0340-6 Viola, 2013, Oxidized low density lipoprotein (LDL) affects hyaluronan synthesis in human aortic smooth muscle cells, J. Biol. Chem., 288, 29595, 10.1074/jbc.M113.508341 Bobryshev, 2006, Monocyte recruitment and foam cell formation in atherosclerosis, Micron, 37, 208, 10.1016/j.micron.2005.10.007 Yin, 2014, TLR4-mediated inflammation promotes foam cell formation of vascular smooth muscle cell by upregulating ACAT1 expression, Cell Death Dis., 5, 10.1038/cddis.2014.535 Chaabane, 2014, Smooth muscle cell phenotypic switch: implications for foam cell formation, Curr. Opin. Lipidol., 25, 374, 10.1097/MOL.0000000000000113 Chellan, 2016, Enzymatically modified low-density lipoprotein promotes foam cell formation in smooth muscle cells via macropinocytosis and enhances receptor-mediated uptake of oxidized low-density lipoprotein, Arterioscler. Thromb. Vasc. Biol., 36, 1101, 10.1161/ATVBAHA.116.307306 Feil, 2014, Transdifferentiation of vascular smooth muscle cells to macrophage-like cells during atherogenesis, Circ. Res., 115, 662, 10.1161/CIRCRESAHA.115.304634 Shankman, 2015, KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis, Nat. Med., 21, 628, 10.1038/nm.3866 Tabata, 2007, Low molecular weight hyaluronan increases the uptaking of oxidized LDL into monocytes, Endocr. J., 54, 685, 10.1507/endocrj.K05-120 Kishikawa, 2006, Glycated albumin and cross-linking of CD44 induce scavenger receptor expression and uptake of oxidized LDL in human monocytes, Biochem. Biophys. Res. Commun., 339, 846, 10.1016/j.bbrc.2005.11.091 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 Bauriedel, 1999, Role of smooth muscle cell death in advanced coronary primary lesions: implications for plaque instability, Cardiovasc. Res., 41, 480, 10.1016/S0008-6363(98)00318-6 Vigetti, 2011, Glycosaminoglycans and glucose prevent apoptosis in 4-methylumbelliferone-treated human aortic smooth muscle cells, J. Biol. Chem., 286, 34497, 10.1074/jbc.M111.266312 Kinscherf, 1997, Induction of mitochondrial manganese superoxide dismutase in macrophages by oxidized LDL: its relevance in atherosclerosis of humans and heritable hyperlipidemic rabbits, FASEB J., 11, 1317, 10.1096/fasebj.11.14.9409551 Kinscherf, 1999, Characterization of apoptotic macrophages in atheromatous tissue of humans and heritable hyperlipidemic rabbits, Atherosclerosis, 144, 33, 10.1016/S0021-9150(99)00037-4 Vivers, 2002, Role of macrophage CD44 in the disposal of inflammatory cell corpses, Clin. Sci. (Lond.), 103, 441, 10.1042/cs1030441 Hart, 1997, CD44 regulates phagocytosis of apoptotic neutrophil granulocytes, but not apoptotic lymphocytes, by human macrophages, J. Immunol., 159, 919, 10.4049/jimmunol.159.2.919 Hart, 2012, Characterization of the effects of cross-linking of macrophage CD44 associated with increased phagocytosis of apoptotic PMN, PLoS One, 7, 10.1371/journal.pone.0033142 Teder, 2002, Resolution of lung inflammation by CD44, Science (80-), 296, 155, 10.1126/science.1069659 Linton, 2016, Macrophage apoptosis and efferocytosis in the pathogenesis of atherosclerosis, Circ. J., 80, 2259, 10.1253/circj.CJ-16-0924 Feig, 2011, Reversal of hyperlipidemia with a genetic switch favorably affects the content and inflammatory state of macrophages in atherosclerotic plaques, Circulation, 123, 989, 10.1161/CIRCULATIONAHA.110.984146 Reis, 2001, Dramatic remodeling of advanced atherosclerotic plaques of the apolipoprotein e-deficient mouse in a novel transplantation model, J. Vasc. Surg., 34, 541, 10.1067/mva.2001.115963 Verschuren, 2009, LXR agonist suppresses atherosclerotic lesion growth and promotes lesion regression in apoE*3Leiden mice: time course and mechanisms, J. Lipid Res., 50, 301, 10.1194/jlr.M800374-JLR200 Lin, 2010, The role of CD4+CD25+ regulatory T cells in macrophage-derived foam-cell formation, J. Lipid Res., 51, 1208, 10.1194/jlr.D000497 Koltsova, 2012, Dynamic T cell-APC interactions sustain chronic inflammation in atherosclerosis, J. Clin. Invest., 122, 3114, 10.1172/JCI61758 Cho, 2007, Induction of dendritic cell-like phenotype in macrophages during foam cell formation, Physiol. Genomics, 29, 149, 10.1152/physiolgenomics.00051.2006 Hegde, 2008, CD44 mobilization in allogeneic dendritic cell-T cell immunological synapse plays a key role in T cell activation, J. Leukoc. Biol., 84, 134, 10.1189/jlb.1107752 Do, 2004, Role of CD44 and hyaluronic acid (HA) in activation of alloreactive and antigen-specific T cells by bone marrow-derived dendritic cells, J. Immunother., 27, 1, 10.1097/00002371-200401000-00001 Termeer, 2003, Targeting dendritic cells with CD44 monoclonal antibodies selectively inhibits the proliferation of naive CD4+ T-helper cells by induction of FAS-independent T-cell apoptosis, Immunology, 109, 32, 10.1046/j.1365-2567.2003.01617.x Hartwig, 2015, Neutrophils in atherosclerosis: a brief overview, Hamostaseologie, 35, 121, 10.5482/HAMO-14-09-0040 Krettek, 2004, Enhanced expression of CD44 variants in human atheroma and abdominal aortic aneurysm: possible role for a feedback loop in endothelial cells, Am. J. Pathol., 165, 1571, 10.1016/S0002-9440(10)63414-1 Watanabe, 2016, Atheroprotective effects of tumor necrosis factor–stimulated gene-6, JACC Basic Transl. Sci., 1, 494, 10.1016/j.jacbts.2016.07.008 Taher, 2016, Phenotypic transformation of intimal and adventitial lymphatics in atherosclerosis: a regulatory role for soluble VEGF receptor 2, FASEB J., 30, 2490, 10.1096/fj.201500112 Singh, 2007, Osteopontin: a novel inflammatory mediator of cardiovascular disease, Front. Biosci., 12, 214, 10.2741/2059 Ikeda, 1993, Osteopontin mRNA is expressed by smooth muscle-derived foam cells in human atherosclerotic lesions of the aorta, J. Clin. Invest., 92, 2814, 10.1172/JCI116901 Chung, 2016, Targeting and therapeutic peptides in nanomedicine for atherosclerosis, Exp. Biol. Med. (Maywood), 10.1177/1535370216640940