Immune-Inflammatory Responses in Atherosclerosis: The Role of Myeloid Cells
Abstract
1. Introduction
2. Myeloid Immune Cells Involved in Atherosclerosis
2.1. Monocytes
2.2. Macrophages
2.3. Dendritic Cells
3. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Ross, R. Atherosclerosis—An inflammatory disease. N. Engl. J. Med. 1999, 340, 115–126. [Google Scholar] [CrossRef] [PubMed]
- Alipov, V.I.; Sukhorukov, V.N.; Karagodin, V.P.; Grechko, A.V.; Orekhov, A.N. Chemical composition of circulating native and desialylated low density lipoprotein: What is the difference? Vessel Plus 2017, 1, 107–115. [Google Scholar] [CrossRef]
- Wong, B.W.; Meredith, A.; Lin, D.; McManus, B.M. The biological role of inflammation in atherosclerosis. Can. J. Cardiol. 2012, 28, 631–641. [Google Scholar] [CrossRef] [PubMed]
- Gimbrone, M.A., Jr.; García-Cardeña, G. Vascular endothelium, hemodynamics, and the pathobiology of atherosclerosis. Cardiovasc. Pathol. 2013, 22, 9–15. [Google Scholar] [CrossRef] [PubMed]
- Kasikara, C.; Doran, A.C.; Cai, B.; Tabas, I. The role of non-resolving inflammation in atherosclerosis. J. Clin. Investig. 2018, 128, 2713–2723. [Google Scholar] [CrossRef] [PubMed]
- Galkina, E.; Ley, K. Immune and inflammatory mechanisms of atherosclerosis. Annu. Rev. Immunol. 2009, 27, 165–197. [Google Scholar] [CrossRef]
- Gerrity, R.G.; Naito, H.K.; Richardson, M.; Schwartz, C.J. Dietary induced atherogenesis in swine. Morphology of the intima in prelesion stages. Am. J. Pathol. 1979, 95, 775–792. [Google Scholar]
- Galkina, E.; Ley, K. Leukocyte influx in atherosclerosis. Curr. Drug Targets 2007, 8, 1239–1248. [Google Scholar] [CrossRef]
- Jongstra-Bilen, J.; Haidari, M.; Zhu, S.N.; Chen, M.; Guha, D.; Cybulsky, M.I. Low-grade chronic inflammation in regions of the normal mouse arterial intima predisposed to atherosclerosis. J. Exp. Med. 2006, 203, 2073–2083. [Google Scholar] [CrossRef]
- Lessner, S.M.; Prado, H.L.; Waller, E.K.; Galis, Z.S. Atherosclerotic lesions grow through recruitment and proliferation of circulating monocytes in a murine model. Am. J. Pathol. 2002, 160, 2145–2155. [Google Scholar] [CrossRef]
- Lord, R.S.; Bobryshev, Y.V. Clustering of dendritic cells in athero-prone areas of the aorta. Atherosclerosis 1999, 146, 197–198. [Google Scholar] [PubMed]
- Strieter, R.M.; Wiggins, R.; Phan, S.H.; Wharram, B.L.; Showell, H.J.; Remich, D.G.; Chensue, S.W.; Kunkel, S.L. Monocyte chemotactic protein gene expression by cytokine-treated human fibroblasts and endothelial cells. Biochem. Biophys. Res. Commun. 1989, 162, 694–700. [Google Scholar] [CrossRef]
- Pober, J.S.; Gimbrone, M.A., Jr.; Collins, T.; Cotran, R.S.; Ault, K.A.; Fiers, W.; Krensky, A.M.; Clayberger, C.; Reiss, C.S.; Burakoff, S.J. Interactions of T lymphocytes with human vascular endothelial cells: Role of endothelial cells surface antigens. Immunobiology 1984, 168, 483–494. [Google Scholar] [CrossRef]
- Bobryshev, Y.V. Monocyte recruitment and foam cell formation in atherosclerosis. Micron 2006, 37, 208–222. [Google Scholar] [CrossRef]
- Huo, Y.; Xia, L. P-selectin glycoprotein ligand-1 plays a crucial role in the selective recruitment of leukocytes into the atherosclerotic arterial wall. Trends Cardiovasc. Med. 2009, 19, 140–145. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Randolph, G.J.; Jakubzick, C.; Qu, C. Antigen presentation by monocytes and monocyte-derived cells. Curr. Opin. Immunol. 2008, 20, 52–60. [Google Scholar] [CrossRef]
- Hatakeyama, S.; Iwabuchi, K.; Ogasawara, K.; Good, R.A.; Onoé, K. The murine c-fgr gene product associated with Ly6C and p70 integral membrane protein is expressed in cells of a monocyte/macrophage lineage. Proc. Natl. Acad. Sci. USA 1994, 91, 3458–3462. [Google Scholar] [CrossRef]
- Lauvau, G.; Chorro, L.; Spaulding, E.; Soudja, S.M. Inflammatory monocyte effector mechanisms. Cell. Immunol. 2014, 291, 32–40. [Google Scholar] [CrossRef]
- Fong, A.M.; Robinson, L.A.; Steeber, D.A.; Tedder, T.F.; Yoshie, O.; Imai, T.; Patel, D.D. Fractalkine and CX3CR1 mediate a novel mechanism of leukocyte capture, firm adhesion, and activation under physiologic flow. J. Exp. Med. 1998, 188, 1413–1419. [Google Scholar] [CrossRef]
- Tacke, F.; Alvarez, D.; Kaplan, T.J.; Jakubzick, C.; Spanbroek, R.; Llodra, J.; Garin, A.; Liu, J.; Mack, M.; van Rooijen, N.; et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Investig. 2007, 117, 185–194. [Google Scholar] [CrossRef]
- Auffray, C.; Fogg, D.; Garfa, M.; Elain, G.; Join-Lambert, O.; Kayal, S.; Sarnacki, S.; Cumano, A.; Lauvau, G.; Geissmann, F. Monitoring of blood vessels and tissues by a population of monocytes withpatrolling behavior. Science 2007, 317, 666–670. [Google Scholar] [CrossRef] [PubMed]
- Thomas, G.; Tacke, R.; Hedrick, C.C.; Hanna, R.N. Nonclassical patrolling monocyte function in the vasculature. Arterioscler. Thromb. Vasc. Biol. 2015, 35, 1306–1316. [Google Scholar] [CrossRef] [PubMed]
- Combadière, C.; Potteaux, S.; Rodero, M.; Simon, T.; Pezard, A.; Esposito, B.; Merval, R.; Proudfoot, A.; Tedgui, A.; Mallat, Z. Combined inhibition of CCL2, CX3CR1, and CCR5 abrogates Ly6Chi and Ly6Clo monocytosis and almost abolishes atherosclerosis in hypercholesterolemic mice. Circulation 2008, 117, 1649–1657. [Google Scholar] [CrossRef] [PubMed]
- Ilhan, F.; Kalkanli, S.T. Atherosclerosis and the role of immune cells. World J. Clin. Cases 2015, 3, 345–352. [Google Scholar] [CrossRef]
- Funk, J.L.; Feingold, K.R.; Moser, A.H.; Grunfeld, C. Lipopolysaccharide stimulation of RAW 264.7 macrophages induces lipid accumulation and foam cell formation. Atherosclerosis 1993, 98, 67–82. [Google Scholar] [CrossRef]
- Lee, J.G.; Lim, E.J.; Park, D.W.; Lee, S.H.; Kim, J.R.; Baek, S.H. A combination of Lox-1 and Nox1 regulates TLR9-mediated foam cell formation. Cell. Signal. 2008, 20, 2266–2275. [Google Scholar] [CrossRef]
- Higashimori, M.; Tatro, J.B.; Moore, K.J.; Mendelsohn, M.E.; Galper, J.B.; Beasley, D. Role of toll-like receptor 4 in intimal foam cell accumulation in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 50–57. [Google Scholar] [CrossRef]
- Cole, J.E.; Georgiou, E.; Monaco, C. The expression and functions of toll-like receptors in atherosclerosis. Mediat. Inflamm. 2010, 2010, 393946. [Google Scholar] [CrossRef]
- Seneviratne, A.N.; Sivagurunathan, B.; Monaco, C. Toll-like receptors and macrophage activation in atherosclerosis. Clin. Chim. Acta 2012, 413, 3–14. [Google Scholar] [CrossRef]
- Febbraio, M.; Podrez, E.A.; Smith, J.D.; Hajjar, D.P.; Hazen, S.L.; Hoff, H.F.; Sharma, K.; Silverstein, R.L. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J. Clin. Investig. 2000, 105, 1049–1056. [Google Scholar] [CrossRef]
- Moore, K.J.; Kunjathoor, V.V.; Koehn, S.L.; Manning, J.J.; Tseng, A.A.; Silver, J.M.; McKee, M.; Freeman, M.W. Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice. J. Clin. Investig. 2005, 115, 2192–2201. [Google Scholar] [CrossRef] [PubMed]
- Kuchibhotla, S.; Vanegas, D.; Kennedy, D.J.; Guy, E.; Nimako, G.; Morton, R.E.; Febbraio, M. Absence of CD36 protects against atherosclerosis in ApoE knock-out mice with no additional protection provided by absence of scavenger receptor A I/II. Cardiovasc. Res. 2008, 78, 185–196. [Google Scholar] [CrossRef] [PubMed]
- Kataoka, H.; Kume, N.; Miyamoto, S.; Minami, M.; Moriwaki, H.; Murase, T.; Sawamura, T.; Masaki, T.; Hashimoto, N.; Kita, T. Expression of lectinlike oxidized low-density lipoprotein receptor-1 in human atherosclerotic lesions. Circulation 1999, 99, 3110–3117. [Google Scholar] [CrossRef] [PubMed]
- Yoshida, H.; Kondratenko, N.; Green, S.; Steinberg, D.; Quehenberger, O. Identification of the lectin-like receptor for oxidized low-density lipoprotein in human macrophages and its potential role as a scavenger receptor. Biochem. J. 1998, 334, 9–13. [Google Scholar] [CrossRef] [PubMed]
- Kume, N.; Kita, T. Lectin-like oxidized low-density lipoprotein receptor-1 (LOX-1) in atherogenesis. Trends Cardiovasc. Med. 2001, 11, 22–25. [Google Scholar] [CrossRef]
- Schaeffer, D.F.; Riazy, M.; Parhar, K.S.; Chen, J.H.; Duronio, V.; Sawamura, T.; Steinbrecher, U.P. LOX-1 augments oxLDL uptake by lysoPC-stimulated murine macrophages but is not required for oxLDL clearance from plasma. J. Lipid. Res. 2009, 50, 1676–1684. [Google Scholar] [CrossRef]
- Inoue, K.; Arai, Y.; Kurihara, H.; Kita, T.; Sawamura, T. Overexpression of lectin-like oxidized low-density lipoprotein receptor-1 induces intramyocardial vasculopathy in apolipoprotein E-null mice. Circ. Res. 2005, 97, 176–184. [Google Scholar] [CrossRef]
- Mehta, J.L.; Sanada, N.; Hu, C.P.; Chen, J.; Dandapat, A.; Sugawara, F.; Satoh, H.; Inoue, K.; Kawase, Y.; Jishage, K.; et al. Deletion of LOX-1 reduces atherogenesis in LDLR knockout mice fed high cholesterol diet. Circ. Res. 2007, 100, 1634–1642. [Google Scholar] [CrossRef]
- Chistiakov, D.A.; Bobryshev, Y.V.; Nikiforov, N.G.; Elizova, N.V.; Sobenin, I.A.; Orekhov, A.N. Macrophage phenotypic plasticity in atherosclerosis: The associated features and the peculiarities of the expression of inflammatory genes. Int. J. Cardiol. 2015, 184, 436–445. [Google Scholar] [CrossRef]
- Taghavie-Moghadam, P.L.; Butcher, M.J.; Galkina, E.V. The dynamic lives of macrophage and dendritic cell subsets in atherosclerosis. Ann. N. Y. Acad. Sci. 2014, 1319, 19–37. [Google Scholar] [CrossRef]
- Zhang, S.; Kim, C.C.; Batra, S.; McKerrow, J.H.; Loke, P. Delineation of diverse macrophage activation programs in response to intracellular parasites and cytokines. PLoS Negl. Trop. Dis. 2010, 4, e648. [Google Scholar] [CrossRef] [PubMed]
- Lacavé-Lapalun, J.V.; Benderitter, M.; Linard, C. Flagellin or lipopolysaccharide treatment modified macrophage populations after colorectal radiation of rats. J. Pharmacol. Exp. Ther. 2013, 346, 75–85. [Google Scholar] [CrossRef] [PubMed]
- Mantovani, A.; Sica, A.; Sozzani, S.; Allavena, P.; Vecchi, A.; Locati, M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25, 677–686. [Google Scholar] [CrossRef] [PubMed]
- Martinez, F.O.; Sica, A.; Mantovani, A.; Locati, M. Macrophage activation and polarization. Front. Biosci. 2008, 13, 453–461. [Google Scholar] [CrossRef] [PubMed]
- Zizzo, G.; Hilliard, B.A.; Monestier, M.; Cohen, P.L. Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction. J. Immunol. 2012, 189, 3508–3520. [Google Scholar] [CrossRef]
- Pinhal-Enfield, G.; Ramanathan, M.; Hasko, G.; Vogel, S.N.; Salzman, A.L.; Boons, G.J.; Leibovich, S.J. An angiogenic switch in macrophages involving synergy between Toll-like receptors 2, 4, 7, and 9 and adenosine A(2A) receptors. Am. J. Pathol. 2003, 163, 711–721. [Google Scholar] [CrossRef]
- Ferrante, C.J.; Pinhal-Enfield, G.; Elson, G.; Cronstein, B.N.; Hasko, G.; Outram, S.; Leibovitch, S.J. The adenosine-dependent angiogenic switch of macrophages to an M2-like phenotype is independent of interleukin- 4 receptor alpha (IL-4Ralpha) signaling. Inflammation 2013, 36, 921–931. [Google Scholar] [CrossRef]
- Gleissner, C.A.; Shaked, I.; Little, K.M.; Ley, K. CXC chemokine ligand 4 induces a unique transcriptome in monocyte-derived macrophages. J. Immunol. 2010, 184, 4810–4818. [Google Scholar] [CrossRef]
- Erbel, C.; Tyka, M.; Helmes, C.M.; Akhavanpoor, M.; Rupp, G.; Domschke, G.; Linden, F.; Wolf, A.; Doesch, A.; Lasitschka, F.; et al. CXCL4-induced plaque macrophages can be specifically identified by co-expression of MMP7+S100A8+ in vitro and in vivo. Innate Immun. 2015, 21, 255–265. [Google Scholar] [CrossRef]
- Gleissner, C.A. Macrophage phenotype modulation by CXCL4 in atherosclerosis. Front. Physiol. 2012, 3, 1. [Google Scholar] [CrossRef]
- Kadl, A.; Meher, A.K.; Sharma, P.R.; Lee, M.Y.; Doran, A.C.; Johnstone, S.R.; Elliott, M.R.; Gruber, F.; Han, J.; Chen, W.; et al. Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ. Res. 2010, 107, 737–746. [Google Scholar] [CrossRef] [PubMed]
- Chinetti-Gbaguidi, G.; Colin, S.; Staels, B. Macrophage subsets in atherosclerosis. Nat. Rev. Cardiol. 2015, 12, 10–17. [Google Scholar] [CrossRef] [PubMed]
- Boyle, J.J.; Harrington, H.A.; Piper, E.; Elderfield, K.; Stark, J.; Landis, R.C.; Haskard, D.O. Coronary intraplaque hemorrhage evokes a novel atheroprotective macrophage phenotype. Am. J. Pathol. 2009, 174, 1097–1108. [Google Scholar] [CrossRef] [PubMed]
- Finn, A.V.; Nakano, M.; Polavarapu, R.; Karmali, V.; Saeed, O.; Zhao, X.; Yazdani, S.; Otsuka, F.; Davis, T.; Habib, A.; et al. Hemoglobin directs macrophage differentiation and prevents foam cell formation in human atherosclerotic plaques. J. Am. Coll. Cardiol. 2012, 59, 166–177. [Google Scholar] [CrossRef]
- Boyle, J.J.; Johns, M.; Kampfer, T.; Nguyen, A.T.; Game, L.; Schaer, D.J.; Mason, J.C.; Haskard, D.O. Activating transcription factor 1 directs Mhem atheroprotective macrophages through coordinated iron handling and foam cell protection. Circ. Res. 2012, 110, 20–33. [Google Scholar] [CrossRef]
- Philippidis, P.; Mason, J.C.; Evans, B.J.; Nadra, I.; Taylor, K.M.; Haskard, D.O.; Landis, R.C. Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme oxygenase-1 synthesis: Antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Circ. Res. 2004, 94, 119–126. [Google Scholar] [CrossRef]
- Groh, L.; Keating, S.T.; Joosten, L.A.B.; Netea, M.G.; Riksen, N.P. Monocyte and macropjhage immunometabolism in atherosclerosis. Semin. Immunopathol. 2018, 40, 203–214. [Google Scholar] [CrossRef]
- West, A.P.; Brodsky, I.E.; Rahner, C.; Woo, D.K.; Erdjument-Bromage, H.; Tempst, P.; Walsh, M.C.; Choi, Y.; Shadel, G.S.; Ghosh, S. TLR signaling augments macrophage bactericidal activity through mitochondrial ROS. Nature 2011, 472, 476–480. [Google Scholar] [CrossRef]
- Yvan-Charvet, L.; Bonacina, F.; Guinamard, R.R.; Norata, G.D. Immunometabolic function of cholesterol in cardiovascular disease and beyond. Cardiovasc. Res. 2019, 115, 1393–1407. [Google Scholar] [CrossRef]
- Van Tuijl, J.; Joosten, L.A.B.; Netea, M.G.; Bekkering, S.; Riksen, N.P. Immunometabolism orchestrates training of innate immunity in atherosclerosis. Cardiovasc. Res. 2019, 115, 1416–1424. [Google Scholar] [CrossRef]
- Siasos, G.; Tsigkou, V.; Kosmopoulos, M.; Theodosiadis, D.; Simantiris, S.; Tagkou, N.M.; Tsimpiktsioglou, A.; Stampouloglou, P.K.; Oikonomou, E.; Mourouzis, K.; et al. Mitochondria and cardiovascular diseases-from pathophysiology to treatment. Ann. Transl. Med. 2018, 6, 256. [Google Scholar] [CrossRef] [PubMed]
- Bobryshev, Y.V.; Lord, R.S. Ultrastructural recognition of cells with dendritic cell morphology in human aortic intima. Contacting interactions of Vascular Dendritic Cells in athero-resistant and athero-prone areas of the normal aorta. Arch. Histol. Cytol. 1995, 58, 307–322. [Google Scholar] [CrossRef] [PubMed]
- Wigren, M.; Nilsson, J.; Kolbus, D. Lymphocytes in atherosclerosis. Clin. Chim. Acta 2012, 413, 1562–1568. [Google Scholar] [CrossRef] [PubMed]
- Chistiakov, D.A.; Sobenin, I.A.; Orekhov, A.N.; Bobryshev, Y.V. Myeloid dendritic cells: Development, functions, and role in atherosclerotic inflammation. Immunobiology 2015, 220, 833–844. [Google Scholar] [CrossRef] [PubMed]
- Kadowaki, N.; Ho, S.; Antonenko, S.; Malefyt, R.W.; Kastelein, R.A.; Bazan, F.; Liu, Y.J. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J. Exp. Med. 2001, 194, 863–869. [Google Scholar] [CrossRef]
- Chistiakov, D.A.; Orekhov, A.N.; Sobenin, I.A.; Bobryshev, Y.V. Plasmacytoid dendritic cells: Development, functions, and role in atherosclerotic inflammation. Front. Physiol. 2014, 5, 279. [Google Scholar] [CrossRef] [PubMed]
- Penna, G.; Vulcano, M.; Sozzani, S.; Adorini, L. Differential migration behavior and chemokine production by myeloid and plasmacytoid dendritic cells. Hum. Immunol. 2002, 63, 1164–1171. [Google Scholar] [CrossRef]
- Dzionek, A.; Fuchs, A.; Schmidt, P.; Cremer, S.; Zysk, M.; Miltenyi, S.; Buck, D.W.; Schmitz, J. BDCA-2, BDCA-3, and BDCA-4: Three markers for distinct subsets of dendritic cells in human peripheral blood. J. Immunol. 2000, 165, 6037–6046. [Google Scholar] [CrossRef]
- Jongbloed, S.L.; Kassianos, A.J.; McDonald, K.J.; Clark, G.J.; Ju, X.; Angel, C.E.; Chen, C.J.; Dunbar, P.R.; Wadley, R.B.; Jeet, V.; et al. Human CD141+(BDCA-3) + dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J. Exp. Med. 2010, 207, 1247–1260. [Google Scholar] [CrossRef]
- Legein, B.; Temmerman, L.; Biessen, E.A.; Lutgens, E. Inflammation and immune system interactions in atherosclerosis. Cell. Mol. Life Sci. 2013, 70, 3847–3869. [Google Scholar] [CrossRef]
- Dopheide, J.F.; Sester, U.; Schlitt, A.; Horstick, G.; Rupprecht, H.J.; Munzel, T.; Blankenberg, S. Monocyte-derived dendritic cells of patients with coronary artery disease show an increased expression of costimulatory molecules CD40, CD80 and CD86 in vitro. Coron. Artery Dis. 2007, 18, 523–531. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Li, D.; Yang, K.; Hu, Y.; Zeng, Q. Toll-like receptor-4 and mitogen-activated protein kinase signal system are involved in activation of dendritic cells in patients with acute coronary syndrome. Immunology 2008, 125, 122–130. [Google Scholar] [CrossRef] [PubMed]
- Ghattas, A.; Griffiths, H.R.; Devitt, A.; Lip, G.Y.; Shantsila, E. Monocytes in coronary artery disease and atherosclerosis: Where are we now? J. Am. Coll. Cardiol. 2013, 62, 1541–1551. [Google Scholar] [CrossRef] [PubMed]
- Ait-Oufella, H.; Sage, A.P.; Mallat, Z.; Tedgui, A. Adaptive (T and B cells) immunity and control by dendritic cells in atherosclerosis. Circ. Res. 2014, 114, 1640–1660. [Google Scholar] [CrossRef]
- Döring, Y.; Manthey, H.D.; Drechsler, M.; Lievens, D.; Megens, R.T.; Soehnlein, O.; Busch, M.; Manca, M.; Koenen, R.R.; Pelisek, J.; et al. Auto-antigenic protein-DNA complexes stimulate plasmacytoid dendritic cells to promote atherosclerosis. Circulation 2012, 125, 1673–1683. [Google Scholar] [CrossRef]
- Niessner, A.; Sato, K.; Chaikof, E.L.; Colmegna, I.; Goronzy, J.J.; Weyand, C.M. Pathogen-sensing plasmacytoid dendritic cells stimulate cytotoxic T-cell function in the atherosclerotic plaque through interferon-alpha. Circulation 2006, 114, 2482–2489. [Google Scholar] [CrossRef]
- Anand, P.K.; Malireddi, R.K.; Kanneganti, T.D. Role of the nlrp3 inflammasome in microbial infection. Front. Microbiol. 2011, 2, 12. [Google Scholar] [CrossRef]
- Sozzani, S.; Vermi, W.; Del Prete, A.; Facchetti, F. Trafficking properties of plasmacytoid dendritic cells in health and disease. Trends Immunol. 2010, 31, 270–277. [Google Scholar] [CrossRef]
- Butcher, M.J.; Galkina, E.V. Phenotypic and functional heterogeneity of macrophages and dendritic cell subsets in the healthy and atherosclerosis-prone aorta. Front. Physiol. 2012, 3, 44. [Google Scholar] [CrossRef]
- Bobryshev, Y.V.; Lord, R.S.A. Mapping of vascular dendritic cells in atherosclerotic arteries suggests their involvement in local immune inflammatory reaction. Cardiovasc. Res. 1998, 37, 799–810. [Google Scholar] [CrossRef]
- Koltsova, E.K.; Garcia, Z.; Chodaczek, G.; Landau, M.; McArdle, S.; Scott, S.R.; von Vietinghoff, S.; Galkina, E.; Miller, Y.I.; Acton, S.T.; et al. Dynamic T cell-APC interactions sustain chronic inflammation in atherosclerosis. J. Clin. Investig. 2012, 122, 3114–3126. [Google Scholar] [CrossRef] [PubMed]
- Perrin-Cocon, L.; Coutant, F.; Agaugué, S.; Deforges, S.; André, P.; Lotteau, V. Oxidized low-density lipoprotein promotes mature dendritic cell transition from differentiating monocyte. J. Immunol. 2001, 167, 3785–3791. [Google Scholar] [CrossRef] [PubMed]
- Paulson, K.E.; Zhu, S.N.; Chen, M.; Nurmohamed, S.; Jongstra-Bilen, J.; Cybulsky, M.I. Resident intimal dendritic cells accumulate lipid and contribute to the initiation of atherosclerosis. Circ. Res. 2010, 106, 383–390. [Google Scholar] [CrossRef] [PubMed]
- Weber, C.; Meiler, S.; Döring, Y.; Koch, M.; Drechsler, M.; Megens, R.T.; Rowinska, Z.; Bidzhekov, K.; Fecher, C.; Ribechini, E.; et al. CCL17-expressing dendritic cells drive atherosclerosis by restraining regulatory T cell homeostasis in mice. J. Clin. Investig. 2011, 121, 2898–2910. [Google Scholar] [CrossRef]
- Maldonado, R.A.; von Andrian, U.H. How tolerogenic dendritic cells induce regulatory T cells. Adv. Immunol. 2010, 108, 111–165. [Google Scholar]
- Choi, J.H.; Cheong, C.; Dandamudi, D.B.; Park, C.G.; Rodriguez, A.; Mehandry, S.; Velinzon, K.; Jung, I.H.; Yoo, J.Y.; Oh, G.T.; et al. Flt3 signaling-dependent dendritic cells protect against atherosclerosis. Immunity 2011, 35, 819–831. [Google Scholar] [CrossRef]
- Chistiakov, D.A.; Sobenin, I.A.; Orekhov, A.N. Regulatory T cells in atherosclerosis and strategies to induce the endogenous atheroprotective immune response. Immunol Lett. 2013, 151, 10–22. [Google Scholar] [CrossRef]
- Lievens, D.; Habets, K.L.; Robertson, A.K.; Laouar, Y.; Winkels, H.; Rademakers, T.; Beckers, L.; Wijnands, E.; Boon, L.; Mosaheb, M.; et al. Abrogated transforming growth factor beta receptor II (TGFβRII) signalling in dendritic cells promotes immune reactivity of T cells resulting in enhanced atherosclerosis. Eur. Heart J. 2013, 34, 3717–3727. [Google Scholar] [CrossRef]
- Fife, B.T.; Pauken, K.E.; Eagar, T.N.; Obu, T.; Wu, J.; Tang, Q.; Azuma, M.; Krummel, M.F.; Bluestone, J.A. Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat. Immunol. 2009, 10, 1185–1192. [Google Scholar] [CrossRef]
- Heitger, A. Regulation of expression and function of IDO in human dendritic cells. Curr. Med. Chem. 2011, 18, 2222–2233. [Google Scholar] [CrossRef]
- Fallarino, F.; Orabona, C.; Vacca, C.; Bianchi, R.; Gizzi, S.; Asselin-Paturel, C.; Fioretti, M.C.; Trincheri, G.; Grohmann, U.; Puccetti, P. Ligand and cytokine dependence of the immunosuppressive pathway of tryptophan catabolism in plasmacytoid dendritic cells. Int. Immunol. 2005, 17, 1429–1438. [Google Scholar] [CrossRef] [PubMed]
- Daissormont, I.T.; Christ, A.; Temmerman, L.; Sampedro Millares, S.; Seijkens, T.; Manca, M.; Rousch, M.; Poggi, M.; Boon, L.; van der Loos, C.; et al. Plasmacytoid dendritic cells protect against atherosclerosis by tuning T-cell proliferation and activity. Circ. Res. 2011, 109, 1387–1395. [Google Scholar] [CrossRef] [PubMed]
- Ovchinnikova, O.A.; Berge, N.; Kang, C.; Urien, C.; Ketelhuth, D.F.; Pottier, J.; Drouet, L.; Hansson, G.K.; Marchal, G.; Back, M.; et al. Mycobacterium bovis BCG killed by extended freeze-drying induces an immunoregulatory profile and protects against atherosclerosis. J. Intern. Med. 2014, 275, 49–58. [Google Scholar] [CrossRef] [PubMed]
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Chistiakov, D.A.; Kashirskikh, D.A.; Khotina, V.A.; Grechko, A.V.; Orekhov, A.N. Immune-Inflammatory Responses in Atherosclerosis: The Role of Myeloid Cells. J. Clin. Med. 2019, 8, 1798. https://doi.org/10.3390/jcm8111798
Chistiakov DA, Kashirskikh DA, Khotina VA, Grechko AV, Orekhov AN. Immune-Inflammatory Responses in Atherosclerosis: The Role of Myeloid Cells. Journal of Clinical Medicine. 2019; 8(11):1798. https://doi.org/10.3390/jcm8111798
Chicago/Turabian StyleChistiakov, Dimitry A., Dmitry A. Kashirskikh, Victoriya A. Khotina, Andrey V. Grechko, and Alexander N. Orekhov. 2019. "Immune-Inflammatory Responses in Atherosclerosis: The Role of Myeloid Cells" Journal of Clinical Medicine 8, no. 11: 1798. https://doi.org/10.3390/jcm8111798
APA StyleChistiakov, D. A., Kashirskikh, D. A., Khotina, V. A., Grechko, A. V., & Orekhov, A. N. (2019). Immune-Inflammatory Responses in Atherosclerosis: The Role of Myeloid Cells. Journal of Clinical Medicine, 8(11), 1798. https://doi.org/10.3390/jcm8111798