The involvement of the monocytes/macrophages in chronic inflammation associated with atherosclerosis

Immunobiology

Volumn 218, Issue 11, 2013, Pages 1376-1384

  Fenyo, Ioana Madalina ^a   Gafencu, Anca Violeta ^a  

^a INSTITUTE OF CELLULAR BIOLOGY AND PATHOLOGY NICOLAE SIMIONESCU   (Romania)

Author keywords

Atherosclerotic plaque Inflammation Macrophages Monocytes Differentiation Polarization; Atherosclerotic plaque; Differentiation; Inflammation; Macrophages; Monocytes; Polarization

Indexed keywords

CD11B ANTIGEN; CD18 ANTIGEN; COLONY STIMULATING FACTOR 1; CYTOTOXIC FACTOR; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; LIPID; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MEMBRANE PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTERY WALL; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL WALL; CELL PROLIFERATION; CHRONIC INFLAMMATION; DISEASE ASSOCIATION; DISEASE COURSE; EXTRACELLULAR MATRIX; HUMAN; LIPID STORAGE; MACROPHAGE; MICROENVIRONMENT; MONOCYTE; PRIORITY JOURNAL; RISK FACTOR;

APOE; APOLIPOPROTEIN E; ATHEROSCLEROTIC PLAQUE; DIFFERENTIATION; ECS; ENDOTHELIAL CELLS; GM-CSF; GRANULOCYTE/MACROPHAGE COLONY STIMULATING FACTOR; ICAM-1; IL; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN; LDL; LOW DENSITY LIPOPROTEINS; M-CSF; MACROPHAGE COLONY STIMULATING FACTOR; MACROPHAGES; MCP-1; MONOCYTE CHEMOATTRACTANT PROTEIN-1; MONOCYTES; OXIDIZED LDL; OXLDL; PKC; POLARIZATION; PROTEIN KINASE C; REACTIVE OXYGEN SPECIES; ROS; SMCS; SMOOTH MUSCLE CELLS; TGF; TNF; TRANSFORMING GROWTH FACTOR; TUMOR NECROSIS FACTOR; VASCULAR CELL ADHESION MOLECULE 1; VCAM-1;

APOPTOSIS; ATHEROSCLEROSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MACROPHAGES; MONOCYTES; PLAQUE, ATHEROSCLEROTIC;

EID: 84884146185     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2013.06.005     Document Type: Article

References (138)

1. Andres V. Control of vascular cell proliferation and migration by cyclin-dependent kinase signalling: new perspectives and therapeutic potential. Cardiovasc. Res. 2004, 63(1):11-21.
2. Andres V., Pello O.M., Silvestre-Roig C. Macrophage proliferation and apoptosis in atherosclerosis. Curr. Opin. Lipidol. 2012, 23(5):429-438.
3. 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 with patrolling behavior. Science 2007, 317(5838):666-670.
4. Barks J.L., McQuillan J.J., Iademarco M.F. TNF-alpha and IL-4 synergistically increase vascular cell adhesion molecule-1 expression in cultured vascular smooth muscle cells. J. Immunol. 1997, 159(9):4532-4538.
5. Biwa T., Hakamata H., Sakai M., Miyazaki A., Suzuki H., Kodama T., Shichiri M., Horiuchi S. Induction of murine macrophage growth by oxidized low density lipoprotein is mediated by granulocyte macrophage colony-stimulating factor. J. Biol. Chem. 1998, 273(43):28305-28313.
6. Biwa T., Sakai M., Matsumura T., Kobori S., Kaneko K., Miyazaki A., Hakamata H., Horiuchi S., Shichiri M. Sites of action of protein kinase C and phosphatidylinositol 3-kinase are distinct in oxidized low density lipoprotein-induced macrophage proliferation. J. Biol. Chem. 2000, 275(8):5810-5816.
7. Bobryshev Y.V. Monocyte recruitment and foam cell formation in atherosclerosis. Micron 2006, 37(3):208-222.
8. 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(3):1097-1108.
9. Boyle J.J., Johns M., Lo J., Chiodini A., Ambrose N., Evans P.C., Mason J.C., Haskard D.O. Heme induces heme oxygenase 1 via Nrf2: role in the homeostatic macrophage response to intraplaque hemorrhage. Arterioscler. Thromb. Vasc. Biol. 2011, 31(11):2685-2691.
10. Braunersreuther V., Zernecke A., Arnaud C., Liehn E.A., Steffens S., Shagdarsuren E., Bidzhekov K., Burger F., Pelli G., Luckow B., Mach F., Weber C. Ccr5 but not Ccr1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 2007, 27(2):373-379.
11. Burgess A.W., Metcalf D. The nature and action of granulocyte-macrophage colony stimulating factors. Blood 1980, 56(6):947-958.
12. 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.
13. Calin M.V., Manduteanu I., Dragomir E., Dragan E., Nicolae M., Gan A.M., Simionescu M. Effect of depletion of monocytes/macrophages on early aortic valve lesion in experimental hyperlipidemia. Cell Tissue Res. 2009, 336(2):237-248.
14. Chang J.D., Sukhova G.K., Libby P., Schvartz E., Lichtenstein A.H., Field S.J., Kennedy C., Madhavarapu S., Luo J., Wu D., Cantley L.C. Deletion of the phosphoinositide 3-kinase p110gamma gene attenuates murine atherosclerosis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(19):8077-8082.
15. Chen J.H., Riazy M., Wang S.W., Dai J.M., Duronio V., Steinbrecher U.P. Sphingosine kinase regulates oxidized low density lipoprotein-mediated calcium oscillations and macrophage survival. J. Lipid Res. 2010, 51(5):991-998.
16. Chinetti-Gbaguidi G., Baron M., Bouhlel M.A., Vanhoutte J., Copin C., Sebti Y., Derudas B., Mayi T., Bories G., Tailleux A., Haulon S., Zawadzki C., Jude B., Staels B. Human atherosclerotic plaque alternative macrophages display low cholesterol handling but high phagocytosis because of distinct activities of the PPARgamma and LXRalpha pathways. Circ. Res. 2011, 108(8):985-995.
17. Croons V., Martinet W., De Meyer G.R. Selective removal of macrophages in atherosclerotic plaques as a pharmacological approach for plaque stabilization: benefits versus potential complications. Curr. Vasc. Pharmacol. 2010, 8(4):495-508.
18. Cuff C.A., Kothapalli D., Azonobi I., Chun S., Zhang Y., Belkin R., Yeh C., Secreto A., Assoian R.K., Rader D.J., Pure E. The adhesion receptor CD44 promotes atherosclerosis by mediating inflammatory cell recruitment and vascular cell activation. J. Clin. Invest. 2001, 108(7):1031-1040.
19. Cybulsky M.I., Iiyama K., Li H., Zhu S., Chen M., Iiyama M., Davis V., Gutierrez-Ramos J.C., Connelly P.W., Milstone D.S. A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J. Clin. Invest. 2001, 107(10):1255-1262.
20. de Villiers W.J., Smith J.D., Miyata M., Dansky H.M., Darley E., Gordon S. Macrophage phenotype in mice deficient in both macrophage-colony-stimulating factor (op) and apolipoprotein E. Arterioscler. Thromb. Vasc. Biol. 1998, 18(4):631-640.
21. Ditiatkovski M., Toh B.H., Bobik A. GM-CSF deficiency reduces macrophage PPAR-gamma expression and aggravates atherosclerosis in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 2006, 26(10):2337-2344.
22. Fenyo I.M., Florea I.C., Raicu M., Manea A. Tyrphostin AG490 reduces NAPDH oxidase activity and expression in the aorta of hypercholesterolemic apolipoprotein E-deficient mice. Vascul. Pharmacol. 2011, 54(3-6):100-106.
23. Fleetwood A.J., Lawrence T., Hamilton J.A., Cook A.D. Granulocyte-macrophage colony-stimulating factor (CSF) and macrophage CSF-dependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: implications for CSF blockade in inflammation. J. Immunol. 2007, 178(8):5245-5252.
24. Fuster J.J., Fernandez P., Gonzalez-Navarro H., Silvestre C., Nabah Y.N., Andres V. Control of cell proliferation in atherosclerosis: insights from animal models and human studies. Cardiovasc. Res. 2010, 86(2):254-264.
25. Gafencu A.V., Robciuc M.R., Fuior E., Zannis V.I., Kardassis D., Simionescu M. Inflammatory signaling pathways regulating ApoE gene expression in macrophages. J. Biol. Chem. 2007, 282(30):21776-21785.
26. Galkina E., Ley K. Leukocyte influx in atherosclerosis. Curr. Drug Targets 2007, 8(12):1239-1248.
27. Geissmann F., Jung S., Littman D.R. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003, 19(1):71-82.
28. Gengrinovitch S., Greenberg S.M., Cohen T., Gitay-Goren H., Rockwell P., Maione T.E., Levi B.Z., Neufeld G. Platelet factor-4 inhibits the mitogenic activity of VEGF121 and VEGF165 using several concurrent mechanisms. J. Biol. Chem. 1995, 270(25):15059-15065.
29. Gerszten R.E., Garcia-Zepeda E.A., Lim Y.C., Yoshida M., Ding H.A., Gimbrone M.A., Luster A.D., Luscinskas F.W., Rosenzweig A. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature 1999, 398(6729):718-723.
30. Gleissner C.A. Macrophage phenotype modulation by CXCL4 in atherosclerosis. Front. Physiol. 2012, 3:1.
31. Gleissner C.A., Leitinger N., Ley K. Effects of native and modified low-density lipoproteins on monocyte recruitment in atherosclerosis. Hypertension 2007, 50(2):276-283.
32. 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(9):4810-4818.
33. Gleissner C.A., von Hundelshausen P., Ley K. Platelet chemokines in vascular disease. Arterioscler. Thromb. Vasc. Biol. 2008, 28(11):1920-1927.
34. Gordon D., Reidy M.A., Benditt E.P., Schwartz S.M. Cell proliferation in human coronary arteries. Proc. Natl. Acad. Sci. U. S. A. 1990, 87(12):4600-4604.
35. Gordon S. Macrophage heterogeneity and tissue lipids. J. Clin. Invest. 2007, 117(1):89-93.
36. Gordon S., Taylor P.R. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 2005, 5(12):953-964.
37. Gui T., Shimokado A., Sun Y., Akasaka T., Muragaki Y. Diverse roles of macrophages in atherosclerosis: from inflammatory biology to biomarker discovery. Mediators Inflamm 2012, 2012:693083.
38. Haghighat A., Weiss D., Whalin M.K., Cowan D.P., Taylor W.R. Granulocyte colony-stimulating factor and granulocyte macrophage colony-stimulating factor exacerbate atherosclerosis in apolipoprotein E-deficient mice. Circulation 2007, 115(15):2049-2054.
39. Hajjar D.P., Haberland M.E. Lipoprotein trafficking in vascular cells. Molecular Trojan horses and cellular saboteurs. J. Biol. Chem. 1997, 272(37):22975-22978.
40. Hamilton J.A. Colony-stimulating factors in inflammation and autoimmunity. Nat. Rev. Immunol. 2008, 8(7):533-544.
41. Hamilton J.A., Dientsman S.R. Induction of macrophage DNA synthesis by phorbol esters. J. Cell. Physiol. 1981, 106(3):445-450.
42. Hamilton J.A., Myers D., Jessup W., Cochrane F., Byrne R., Whitty G., Moss S. Oxidized LDL can induce macrophage survival, DNA synthesis, and enhanced proliferative response to CSF-1 and GM-CSF. Arterioscler. Thromb. Vasc. Biol. 1999, 19(1):98-105.
43. Hamilton J.A., Whitty G., Jessup W. Oxidized LDL can promote human monocyte survival. Arterioscler. Thromb. Vasc. Biol. 2000, 20(10):2329-2331.
44. Han K.H., Chen Y., Chang M.K., Han Y.C., Park J.H., Green S.R., Boullier A., Quehenberger O. LDL activates signaling pathways leading to an increase in cytosolic free calcium and stimulation of CD11b expression in monocytes. J. Lipid Res. 2003, 44(7):1332-1340.
45. Han K.H., Tangirala R.K., Green S.R., Quehenberger O. Chemokine receptor CCR2 expression and monocyte chemoattractant protein-1-mediated chemotaxis in human monocytes. A regulatory role for plasma LDL. Arterioscler. Thromb. Vasc. Biol. 1998, 18(12):1983-1991.
46. Hansson G.K. Immune mechanisms in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2001, 21(12):1876-1890.
47. Hashimoto K., Kataoka N., Nakamura E., Hagihara K., Okamoto T., Kanouchi H., Mohri S., Tsujioka K., Kajiya F. Live-cell visualization of the trans-cellular mode of monocyte transmigration across the vascular endothelium, and its relationship with endothelial PECAM-1. J. Physiol. Sci. 2012, 62(1):63-69.
48. Hiasa M., Abe M., Nakano A., Oda A., Amou H., Kido S., Takeuchi K., Kagawa K., Yata K., Hashimoto T., Ozaki S., Asaoka K., Tanaka E., Moriyama K., Matsumoto T. GM-CSF and IL-4 induce dendritic cell differentiation and disrupt osteoclastogenesis through M-CSF receptor shedding by up-regulation of TNF-alpha converting enzyme (TACE). Blood 2009, 114(20):4517-4526.
49. Hoeksema M.A., Stoger J.L., de Winther M.P. Molecular pathways regulating macrophage polarization: implications for atherosclerosis. Curr. Atheroscler. Rep. 2012, 14(3):254-263.
50. Hu Z., Zhang J., Guan A., Gong H., Yang M., Zhang G., Jia J., Ma H., Yang C., Ge J., Zou Y. Granulocyte colony-stimulating factor promotes atherosclerosis in high-fat diet rabbits. Int. J. Mol. Sci. 2013, 14(3):4805-4816.
51. Huo Y., Hafezi-Moghadam A., Ley K. Role of vascular cell adhesion molecule-1 and fibronectin connecting segment-1 in monocyte rolling and adhesion on early atherosclerotic lesions. Circ. Res. 2000, 87(2):153-159.
52. Inoue I., Inaba T., Motoyoshi K., Harada K., Shimano H., Kawamura M., Gotoda T., Oka T., Shiomi M., Watanabe Y., et al. Macrophage colony stimulating factor prevents the progression of atherosclerosis in Watanabe heritable hyperlipidemic rabbits. Atherosclerosis 1992, 93(3):245-254.
53. Jenkins S.J., Ruckerl D., Cook P.C., Jones L.H., Finkelman F.D., van Rooijen N., MacDonald A.S., Allen J.E. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 2011, 332(6035):1284-1288.
54. Johnson P., Ruffell B. CD44 and its role in inflammation and inflammatory diseases. Inflamm. Allergy Drug Targets 2009, 8(3):208-220.
55. 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., Kensler T., Ravichandran K.S., Isakson B.E., Wamhoff B.R., Leitinger N. Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ. Res. 2010, 107(6):737-746.
56. Khallou-Laschet J., Varthaman A., Fornasa G., Compain C., Gaston A.T., Clement M., Dussiot M., Levillain O., Graff-Dubois S., Nicoletti A., Caligiuri G. Macrophage plasticity in experimental atherosclerosis. PLoS ONE 2010, 5(1):e8852.
57. Khoo J.C., Miller E., Pio F., Steinberg D., Witztum J.L. Monoclonal antibodies against LDL further enhance macrophage uptake of LDL aggregates. Arterioscler. Thromb. 1992, 12(11):1258-1266.
58. Koenen R.R., von Hundelshausen P., Nesmelova I.V., Zernecke A., Liehn E.A., Sarabi A., Kramp B.K., Piccinini A.M., Paludan S.R., Kowalska M.A., Kungl A.J., Hackeng T.M., Mayo K.H., Weber C. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat. Med. 2009, 15(1):97-103.
59. Koenen R.R., Weber C. Therapeutic targeting of chemokine interactions in atherosclerosis. Nat. Rev. Drug Discov. 2010, 9(2):141-153.
60. Lamharzi N., Renard C.B., Kramer F., Pennathur S., Heinecke J.W., Chait A., Bornfeldt K.E. Hyperlipidemia in concert with hyperglycemia stimulates the proliferation of macrophages in atherosclerotic lesions: potential role of glucose-oxidized LDL. Diabetes 2004, 53(12):3217-3225.
61. Lau E.K., Paavola C.D., Johnson Z., Gaudry J.P., Geretti E., Borlat F., Kungl A.J., Proudfoot A.E., Handel T.M. Identification of the glycosaminoglycan binding site of the CC chemokine, MCP-1: implications for structure and function in vivo. J. Biol. Chem. 2004, 279(21):22294-22305.
62. Leonard E.J., Yoshimura T. Human monocyte chemoattractant protein-1 (MCP-1). Immunol. Today 1990, 11(3):97-101.
63. Ley K., Laudanna C., Cybulsky M.I., Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 2007, 7(9):678-689.
64. Ley K., Miller Y.I., Hedrick C.C. Monocyte and macrophage dynamics during atherogenesis. Arterioscler. Thromb. Vasc. Biol. 2011, 31(7):1506-1516.
65. Libby P., Ridker P.M., Maseri A. Inflammation and atherosclerosis. Circulation 2002, 105(9):1135-1143.
66. Lusis A.J. Atherosclerosis. Nature 2000, 407(6801):233-241.
67. Lutgens E., Daemen M., Kockx M., Doevendans P., Hofker M., Havekes L., Wellens H., de Muinck E.D. Atherosclerosis in APOE*3-Leiden transgenic mice: from proliferative to atheromatous stage. Circulation 1999, 99(2):276-283.
68. Maderna P., Godson C. Phagocytosis of apoptotic cells and the resolution of inflammation. Biochim. Biophys. Acta 2003, 1639(3):141-151.
69. Mak P.A., Laffitte B.A., Desrumaux C., Joseph S.B., Curtiss L.K., Mangelsdorf D.J., Tontonoz P., Edwards P.A. Regulated expression of the apolipoprotein E/C-I/C-IV/C-II gene cluster in murine and human macrophages. A critical role for nuclear liver X receptors alpha and beta. J. Biol. Chem. 2002, 277(35):31900-31908.
70. Mallat Z., Gojova A., Marchiol-Fournigault C., Esposito B., Kamate C., Merval R., Fradelizi D., Tedgui A. Inhibition of transforming growth factor-beta signaling accelerates atherosclerosis and induces an unstable plaque phenotype in mice. Circ. Res. 2001, 89(10):930-934.
71. Manduteanu I., Pirvulescu M., Gan A.M., Stan D., Simion V., Dragomir E., Calin M., Manea A., Simionescu M. Similar effects of resistin and high glucose on P-selectin and fractalkine expression and monocyte adhesion in human endothelial cells. Biochem. Biophys. Res. Commun. 2010, 391(3):1443-1448.
72. Manduteanu I., Simionescu M. Inflammation in atherosclerosis: a cause or a result of vascular disorders?. J. Cell. Mol. Med. 2012, 16(9):1978-1990.
73. Manea A., Simionescu M. Nox enzymes and oxidative stress in atherosclerosis. Front. Biosci. (Schol. Ed.) 2012, 4:651-670.
74. Mantovani A., Garlanda C., Locati M. Macrophage diversity and polarization in atherosclerosis: a question of balance. Arterioscler. Thromb. Vasc. Biol. 2009, 29(10):1419-1423.
75. Martens J.S., Lougheed M., Gomez-Munoz A., Steinbrecher U.P. A modification of apolipoprotein B accounts for most of the induction of macrophage growth by oxidized low density lipoprotein. J. Biol. Chem. 1999, 274(16):10903-10910.
76. Martens J.S., Reiner N.E., Herrera-Velit P., Steinbrecher U.P. Phosphatidylinositol 3-kinase is involved in the induction of macrophage growth by oxidized low density lipoprotein. J. Biol. Chem. 1998, 273(9):4915-4920.
77. Martinez F.O., Gordon S., Locati M., Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 2006, 177(10):7303-7311.
78. Martinez F.O., Sica A., Mantovani A., Locati M. Macrophage activation and polarization. Front. Biosci. 2008, 13:453-461.
79. Matsumura T., Sakai M., Kobori S., Biwa T., Takemura T., Matsuda H., Hakamata H., Horiuchi S., Shichiri M. Two intracellular signaling pathways for activation of protein kinase C are involved in oxidized low-density lipoprotein-induced macrophage growth. Arterioscler. Thromb. Vasc. Biol. 1997, 17(11):3013-3020.
80. Moore K.J., Freeman M.W. Scavenger receptors in atherosclerosis: beyond lipid uptake. Arterioscler. Thromb. Vasc. Biol. 2006, 26(8):1702-1711.
81. Moore K.J., Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell 2011, 145(3):341-355.
82. Mosser D.M., Edwards J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8(12):958-969.
83. Muller W.A. The role of PECAM-1 (CD31) in leukocyte emigration: studies in vitro and in vivo. J. Leukoc. Biol. 1995, 57(4):523-528.
84. Naito M. Macrophage differentiation and function in health and disease. Pathol. Int. 2008, 58(3):143-155.
85. Osterud B., Bjorklid E. Role of monocytes in atherogenesis. Physiol. Rev. 2003, 83(4):1069-1112.
86. Packard R.R., Libby P. Inflammation in atherosclerosis: from vascular biology to biomarker discovery and risk prediction. Clin. Chem. 2008, 54(1):24-38.
87. Pello O.M., Silvestre C., De Pizzol M., Andres V. A glimpse on the phenomenon of macrophage polarization during atherosclerosis. Immunobiology 2011, 216(11):1172-1176.
88. Perollet C., Han Z.C., Savona C., Caen J.P., Bikfalvi A. Platelet factor 4 modulates fibroblast growth factor 2 (FGF-2) activity and inhibits FGF-2 dimerization. Blood 1998, 91(9):3289-3299.
89. Pitsilos S., Hunt J., Mohler E.R., Prabhakar A.M., Poncz M., Dawicki J., Khalapyan T.Z., Wolfe M.L., Fairman R., Mitchell M., Carpenter J., Golden M.A., Cines D.B., Sachais B.S. Platelet factor 4 localization in carotid atherosclerotic plaques: correlation with clinical parameters. Thromb. Haemost. 2003, 90(6):1112-1120.
90. Qiao J.H., Tripathi J., Mishra N.K., Cai Y., Tripathi S., Wang X.P., Imes S., Fishbein M.C., Clinton S.K., Libby P., Lusis A.J., Rajavashisth T.B. Role of macrophage colony-stimulating factor in atherosclerosis: studies of osteopetrotic mice. Am. J. Pathol. 1997, 150(5):1687-1699.
91. Quinn M.T., Parthasarathy S., Fong L.G., Steinberg D. Oxidatively modified low density lipoproteins: a potential role in recruitment and retention of monocyte/macrophages during atherogenesis. Proc. Natl. Acad. Sci. U. S. A. 1987, 84(9):2995-2998.
92. Rajavashisth T., Qiao J.H., Tripathi S., Tripathi J., Mishra N., Hua M., Wang X.P., Loussararian A., Clinton S., Libby P., Lusis A. Heterozygous osteopetrotic (op) mutation reduces atherosclerosis in LDL receptor-deficient mice. J. Clin. Invest. 1998, 101(12):2702-2710.
93. Rajavashisth T.B., Andalibi A., Territo M.C., Berliner J.A., Navab M., Fogelman A.M., Lusis A.J. Induction of endothelial cell expression of granulocyte and macrophage colony-stimulating factors by modified low-density lipoproteins. Nature 1990, 344(6263):254-257.
94. Ramos C.L., Huo Y., Jung U., Ghosh S., Manka D.R., Sarembock I.J., Ley K. Direct demonstration of P-selectin- and VCAM-1-dependent mononuclear cell rolling in early atherosclerotic lesions of apolipoprotein E-deficient mice. Circ. Res. 1999, 84(11):1237-1244.
95. Rekhter M.D., Gordon D. Active proliferation of different cell types, including lymphocytes, in human atherosclerotic plaques. Am. J. Pathol. 1995, 147(3):668-677.
96. Rosenfeld M.E., Ross R. Macrophage and smooth muscle cell proliferation in atherosclerotic lesions of WHHL and comparably hypercholesterolemic fat-fed rabbits. Arteriosclerosis 1990, 10(5):680-687.
97. Ross R. Atherosclerosis - an inflammatory disease. N. Engl. J. Med. 1999, 340(2):115-126.
98. Ross R., Glomset J.A. The pathogenesis of atherosclerosis (first of two parts). N. Engl. J. Med. 1976, 295(7):369-377.
99. Ross R., Glomset J.A. The pathogenesis of atherosclerosis (second of two parts). N. Engl. J. Med. 1976, 295(8):420-425.
100. Ruotsalainen A.K., Inkala M., Partanen M.E., Lappalainen J.P., Kansanen E., Makinen P.I., Heinonen S.E., Laitinen H.M., Heikkila J., Vatanen T., Horkko S., Yamamoto M., Yla-Herttuala S., Jauhiainen M., Levonen A.L. The absence of macrophage Nrf2 promotes early atherogenesis. Cardiovasc. Res. 2013, 98(1):107-115.
101. Sachais B.S., Turrentine T., Dawicki McKenna J.M., Rux A.H., Rader D., Kowalska M.A. Elimination of platelet factor 4 (PF4) from platelets reduces atherosclerosis in C57Bl/6 and apoE-/- mice. Thromb. Haemost. 2007, 98(5):1108-1113.
102. Sakai M., Kobori S., Miyazaki A., Horiuchi S. Macrophage proliferation in atherosclerosis. Curr. Opin. Lipidol. 2000, 11(5):503-509.
103. Sakai M., Miyazaki A., Hakamata H., Kodama T., Suzuki H., Kobori S., Shichiri M., Horiuchi S. The scavenger receptor serves as a route for internalization of lysophosphatidylcholine in oxidized low density lipoprotein-induced macrophage proliferation. J. Biol. Chem. 1996, 271(44):27346-27352.
104. Sakai M., Miyazaki A., Hakamata H., Sasaki T., Yui S., Yamazaki M., Shichiri M., Horiuchi S. Lysophosphatidylcholine plays an essential role in the mitogenic effect of oxidized low density lipoprotein on murine macrophages. J. Biol. Chem. 1994, 269(50):31430-31435.
105. Sakai M., Miyazaki A., Hakamata H., Sato Y., Matsumura T., Kobori S., Shichiri M., Horiuchi S. Lysophosphatidylcholine potentiates the mitogenic activity of modified LDL for human monocyte-derived macrophages. Arterioscler. Thromb. Vasc. Biol. 1996, 16(4):600-605.
106. Sarabi A., Kramp B.K., Drechsler M., Hackeng T.M., Soehnlein O., Weber C., Koenen R.R., Von Hundelshausen P. CXCL4L1 inhibits angiogenesis and induces undirected endothelial cell migration without affecting endothelial cell proliferation and monocyte recruitment. J. Thromb. Haemost. 2011, 9(1):209-219.
107. Schrijvers D.M., De Meyer G.R., Herman A.G., Martinet W. Phagocytosis in atherosclerosis: Molecular mechanisms and implications for plaque progression and stability. Cardiovasc. Res. 2007, 73(3):470-480.
108. Shackelford R.E., Misra U.K., Florine-Casteel K., Thai S.F., Pizzo S.V., Adams D.O. Oxidized low density lipoprotein suppresses activation of NFkB in macrophages via a pertussis toxin-sensitive signaling mechanism. J. Biol. Chem. 1995, 270(8):3475-3478.
109. Shi W., Wang X., Wang N.J., McBride W.H., Lusis A.J. Effect of macrophage-derived apolipoprotein E on established atherosclerosis in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 2000, 20(10):2261-2266.
110. Shindo J., Ishibashi T., Yokoyama K., Nakazato K., Ohwada T., Shiomi M., Maruyama Y. Granulocyte-macrophage colony-stimulating factor prevents the progression of atherosclerosis via changes in the cellular and extracellular composition of atherosclerotic lesions in watanabe heritable hyperlipidemic rabbits. Circulation 1999, 99(16):2150-2156.
111. Sima A.V., Stancu C.S., Simionescu M. Vascular endothelium in atherosclerosis. Cell Tissue Res. 2009, 335(1):191-203.
112. Simionescu M. Implications of early structural-functional changes in the endothelium for vascular disease. Arterioscler. Thromb. Vasc. Biol. 2007, 27(2):266-274.
113. Simionescu M. Cellular dysfunction in inflammatory-related vascular disorders' review series. The inflammatory process: a new dimension of a 19 century old story. J. Cell. Mol. Med. 2009, 13(11-12):4291-4292.
114. Smith J.D., Trogan E., Ginsberg M., Grigaux C., Tian J., Miyata M. Decreased atherosclerosis in mice deficient in both macrophage colony-stimulating factor (op) and apolipoprotein E. Proc. Natl. Acad. Sci. U. S. A. 1995, 92(18):8264-8268.
115. Soehnlein O. Multiple roles for neutrophils in atherosclerosis. Circ. Res. 2012, 110(6):875-888.
116. Soehnlein O., Weber C. Myeloid cells in atherosclerosis: initiators and decision shapers. Semin. Immunopathol. 2009, 31(1):35-47.
117. Spagnoli L.G., Orlandi A., Santeusanio G. Foam cells of the rabbit atherosclerotic plaque arrested in metaphase by colchicine show a macrophage phenotype. Atherosclerosis 1991, 88(1):87-92.
118. Stanley E.R., Chen D.M., Lin H.S. Induction of macrophage production and proliferation by a purified colony stimulating factor. Nature 1978, 274(5667):168-170.
119. Steinberg D. Low density lipoprotein oxidation and its pathobiological significance. J. Biol. Chem. 1997, 272(34):20963-20966.
120. Stoger J.L., Gijbels M.J., van der Velden S., Manca M., van der Loos C.M., Biessen E.A., Daemen M.J., Lutgens E., de Winther M.P. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis 2012, 225(2):461-468.
121. Stopeck A.T., Nicholson A.C., Mancini F.P., Hajjar D.P. Cytokine regulation of low density lipoprotein receptor gene transcription in HepG2 cells. J. Biol. Chem. 1993, 268(23):17489-17494.
122. Strauss-Ayali D., Conrad S.M., Mosser D.M. Monocyte subpopulations and their differentiation patterns during infection. J. Leukoc. Biol. 2007, 82(2):244-252.
123. Sussan T.E., Jun J., Thimmulappa R., Bedja D., Antero M., Gabrielson K.L., Polotsky V.Y., Biswal S. Disruption of Nrf2, a key inducer of antioxidant defenses, attenuates ApoE-mediated atherosclerosis in mice. PLoS ONE 2008, 3(11):e3791.
124. Swirski F.K., Libby P., Aikawa E., Alcaide P., Luscinskas F.W., Weissleder R., Pittet M.J. Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J. Clin. Invest. 2007, 117(1):195-205.
125. Tabas I. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency. Arterioscler. Thromb. Vasc. Biol. 2005, 25(11):2255-2264.
126. Tabas I. Apoptosis and efferocytosis in mouse models of atherosclerosis. Curr. Drug Targets 2007, 8(12):1288-1296.
127. Tabas I. Macrophage apoptosis in atherosclerosis: consequences on plaque progression and the role of endoplasmic reticulum stress. Antioxid. Redox Signal. 2009.
128. Tacke F., Alvarez D., Kaplan T.J., Jakubzick C., Spanbroek R., Llodra J., Garin A., Liu J., Mack M., van Rooijen N., Lira S.A., Habenicht A.J., Randolph G.J. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 2007, 117(1):185-194.
129. Tardif J.C., Gregoire J., L'Allier P.L., Ibrahim R., Anderson T.J., Reeves F., Title L.M., Schampaert E., LeMay M., Lesperance J., Scott R., Guertin M.C., Brennan M.L., Hazen S.L., Bertrand O.F. Effects of the antioxidant succinobucol (AGI-1067) on human atherosclerosis in a randomized clinical trial. Atherosclerosis 2008, 197(1):480-486.
130. Tardif J.C., Gregoire J., Schwartz L., Title L., Laramee L., Reeves F., Lesperance J., Bourassa M.G., L'Allier P.L., Glass M., Lambert J., Guertin M.C. Effects of AGI-1067 and probucol after percutaneous coronary interventions. Circulation 2003, 107(4):552-558.
131. Tedgui A., Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol. Rev. 2006, 86(2):515-581.
132. Trusca V.G., Fuior E.V., Florea I.C., Kardassis D., Simionescu M., Gafencu A.V. Macrophage-specific up-regulation of apolipoprotein E gene expression by STAT1 is achieved via long range genomic interactions. J. Biol. Chem. 2011, 286(16):13891-13904.
133. Wang S.C., Kanner S.B., Ledbetter J.A., Gupta S., Kumar G., Nel A.E. Evidence for LFA-1/ICAM-1 dependent stimulation of protein tyrosine phosphorylation in human B lymphoid cell lines during homotypic adhesion. J. Leukoc. Biol. 1995, 57(2):343-351.
134. Weber C., Zernecke A., Libby P. The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat. Rev. Immunol. 2008, 8(10):802-815.
135. Wolfs I.M., Donners M.M., de Winther M.P. Differentiation factors and cytokines in the atherosclerotic plaque micro-environment as a trigger for macrophage polarisation. Thromb. Haemost. 2011, 106(5):763-771.
136. Yui S., Sasaki T., Miyazaki A., Horiuchi S., Yamazaki M. Induction of murine macrophage growth by modified LDLs. Arterioscler. Thromb. 1993, 13(3):331-337.
137. Zannis V.I., Kan H.Y., Kritis A., Zanni E.E., Kardassis D. Transcriptional regulatory mechanisms of the human apolipoprotein genes in vitro and in vivo. Curr. Opin. Lipidol. 2001, 12(2):181-207.
138. Zhu S.N., Chen M., Jongstra-Bilen J., Cybulsky M.I. GM-CSF regulates intimal cell proliferation in nascent atherosclerotic lesions. J. Exp. Med. 2009, 206(10):2141-2149.