The specific role of chemokines in atherosclerosis

Vincent Braunersreuther; François Mach; Sabine Steffens

doi:10.1160/TH07-01-0036

Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 2007; 97(05): 714-721
DOI: 10.1160/TH07-01-0036

Theme Issue Article

Schattauer GmbH

The specific role of chemokines in atherosclerosis

Vincent Braunersreuther

¹Division of Cardiology, Foundation for Medical Researches, University Hospital, Geneva, Switzerland

,

François Mach

¹Division of Cardiology, Foundation for Medical Researches, University Hospital, Geneva, Switzerland

,

Sabine Steffens

¹Division of Cardiology, Foundation for Medical Researches, University Hospital, Geneva, Switzerland

› Institutsangaben

Abstract

Summary

Atherosclerosis is a chronic inflammatory disease that represents the primary cause of heart disease and stroke.The recruitment of inflammatory cells in the intima is an essential step in the development and progression of atherosclerosis.This process is triggered by local production of chemokines and chemokine receptors from activated endothelial cells and inflammatory cells. Various members of the CC chemokine family (e.g. MCP- 1/CCL2) as well as CXC family (e.g. IL-8/CCL8, IP-10/CXCL10, SDF-1/CXCL12) and, more recently, fractalkine/CX3CL1 have been implicated in atherosclerosis development. Latest findings in animal models suggest that blocking chemokine/chemokine receptor interactions may serve as a suitable approach to treat atherosclerosis. Likewise, chemokine antagonists that inhibit leukocyte recruitment could particularly be interesting to treat inflammation in response to myocardial infarction, the major consequence of atherosclerosis.

Keywords

Atherosclerosis - chemokines - inflammation - leukocyte recruitment - myocardial infarction

Volltext

Referenzen

References
1 Libby P. Inflammation in atherosclerosis. Nature 2002; 420: 868-874.
2 Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005; 352: 1685-1695.
3 Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 2006; 06: 508-519.
4 Glass CK, Witztum JL. Atherosclerosis. The road ahead. Cell 2001; 104: 503-516.
5 Newby AC. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev 2005; 85: 1-31.
6 Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 2006; 354: 610-621.
7 Proudfoot AE, Handel TM, Johnson Z. et al. Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc Natl Acad Sci USA 2003; 100: 1885-1890.
8 Proudfoot AE. The biological relevance of chemokine- proteoglycan interactions. Biochem Soc Trans 2006; 34: 422-426.
9 Lusis AJ. Atherosclerosis. Nature 2000; 407: 233-241.
10 Braunersreuther V, Mach F. Leukocyte recruitment in atherosclerosis: potential targets for therapeutic approaches?. Cell Mol Life Sci 2006; 63: 2079-2088.
11 Nelken NA, Coughlin SR, Gordon D. et al. Monocyte chemoattractant protein-1 in human atheromatous plaques. J Clin Invest 1991; 88: 1121-1127.
12 Yla-Herttuala S, Lipton BA, Rosenfeld ME. et al. Expression of monocyte chemoattractant protein 1 in macrophage- rich areas of human and rabbit atherosclerotic lesions. Proc Natl Acad Sci USA 1991; 88: 5252-5256.
13 Yu X, Dluz S, Graves DT. et al. Elevated expression of monocyte chemoattractant protein 1 by vascular smooth muscle cells in hypercholesterolemic primates. Proc Natl Acad Sci USA 1992; 89: 6953-6957.
14 Schecter AD, Calderon TM, Berman AB. et al. Human vascular smooth muscle cells possess functional CCR5. J Biol Chem 2000; 275: 5466-5471.
15 von Hundelshausen P, Weber KS, Huo Y. et al. RANTES deposition by platelets triggers monocyte arrest on inflamed and atherosclerotic endothelium. Circulation 2001; 103: 1772-1777.
16 Veillard NR, Steffens S, Burger F. et al. Differential expression patterns of proinflammatory and antiinflammatory mediators during atherogenesis in mice. Arterioscler Thromb Vasc Biol 2004; 24: 2339-2344.
17 Kowalska MA, Ratajczak MZ, Majka M. et al. Stromal cell-derived factor-1 and macrophage-derived chemokine: 2 chemokines that activate platelets. Blood 2000; 96: 50-57.
18 Abi-Younes S, Sauty A, Mach F. et al. The stromal cell-derived factor-1 chemokine is a potent platelet agonist highly expressed in atherosclerotic plaques. Circ Res 2000; 86: 131-138.
19 Nieswandt B, Aktas B, Moers A. et al. Platelets in atherothrombosis: lessons from mouse models. J Thromb Haemost 2005; 03: 1725-1736.
20 Gawaz M, Langer H, May AE. Platelets in inflammation and atherogenesis. J Clin Invest 2005; 115: 3378-3384.
21 Weber C. Platelets and chemokines in atherosclerosis: partners in crime. Circ Res 2005; 96: 612-616.
22 Scheuerer B, Ernst M, Durrbaum-Landmann I. et al. The CXC-chemokine platelet factor 4 promotes monocyte survival and induces monocyte differentiation into macrophages. Blood 2000; 95: 1158-1166.
23 Weber C, Schober A, Zernecke A. Chemokines: key regulators of mononuclear cell recruitment in atherosclerotic vascular disease. Arterioscler Thromb Vasc Biol 2004; 24: 1997-2008.
24 Boring L, Gosling J, Cleary M. et al. Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 1998; 394: 894-897.
25 Gu L, Okada Y, Clinton SK. et al. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell 1998; 02: 275-281.
26 Gosling J, Slaymaker S, Gu L. et al. MCP-1 deficiency reduces susceptibility to atherosclerosis in mice that overexpress human apolipoprotein B. J Clin Invest 1999; 103: 773-778.
27 Aiello RJ, Bourassa PA, Lindsey S. et al. Monocyte chemoattractant protein-1 accelerates atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 1999; 19: 1518-1525.
28 Ni W, Egashira K, Kitamoto S. et al. New antimonocyte chemoattractant protein-1 gene therapy attenuates atherosclerosis in apolipoprotein E-knockout mice. Circulation 2001; 103: 2096-2101.
29 Inoue S, Egashira K, Ni W. et al. Anti-monocyte chemoattractant protein-1 gene therapy limits progression and destabilization of established atherosclerosis in apolipoprotein E-knockout mice. Circulation 2002; 106: 2700-2706.
30 Martinovic I, Abegunewardene N, Seul M. et al. Elevated monocyte chemoattractant protein-1 serum levels in patients at risk for coronary artery disease. Circ J 2005; 69: 1484-1489.
31 Ortlepp JR, Vesper K, Mevissen V. et al. Chemokine receptor (CCR2) genotype is associated with myocardial infarction and heart failure in patients under 65 years of age. J Mol Med 2003; 81: 363-367.
32 Petrkova J, Cermakova Z, Drabek J. et al. CC chemokine receptor (CCR)2 polymorphism in Czech patients with myocardial infarction. Immunol Lett 2003; 88: 53-55.
33 Gonzalez P, Alvarez R, Batalla A. et al. Genetic variation at the chemokine receptors CCR5/CCR2 in myocardial infarction. Genes Immun 2001; 02: 191-195.
34 McDermott DH, Yang Q, Kathiresan S. et al. CCL2 polymorphisms are associated with serum monocyte chemoattractant protein-1 levels and myocardial infarction in the Framingham Heart Study. Circulation 2005; 112: 1113-1120.
35 Szalai C, Duba J, Prohaszka Z. et al. Involvement of polymorphisms in the chemokine system in the susceptibility for coronary artery disease (CAD). Coincidence of elevated Lp(a) and MCP-1 –2518 G/G genotype in CAD patients. Atherosclerosis 2001; 158: 233-239.
36 Veillard NR, Kwak B, Pelli G. et al. Antagonism of RANTES receptors reduces atherosclerotic plaque formation in mice. Circ Res 2004; 94: 253-261.
37 Kuziel WA, Dawson TC, Quinones M. et al. CCR5 deficiency is not protective in the early stages of atherogenesis in apoE knockout mice. Atherosclerosis 2003; 167: 25-32.
38 Potteaux S, Combadiere C, Esposito B. et al. Role of bone marrow-derived CC-chemokine receptor 5 in the development of atherosclerosis of low-density lipoprotein receptor knockout mice. Arterioscler Thromb Vasc Biol 2006; 26: 1858-1863.
39 Braunersreuther V, Zernecke A, Arnaud C. et al. Ccr5 but not Ccr1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler Thromb Vasc Biol 2007; 27: 373-379.
40 Zernecke A, Liehn EA, Gao JL. et al. Deficiency in CCR5 but not CCR1 protects against neointima formation in atherosclerosis-prone mice: involvement of IL-10. Blood 2006; 107: 4240-4243.
41 Braunersreuther V, Zernecke A, Steffens S. et al. Ccr5 but not Ccr1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler Thromb Vasc Biol 2006; 188: 51-58.
42 Flanagan K, Moroziewicz D, Kwak H. et al. The lymphoid chemokine CCL21 costimulates naive T cell expansion and Th1 polarization of non-regulatory CD4+ T cells. Cell Immunol 2004; 231: 75-84.
43 Marsland BJ, Battig P, Bauer M. et al. CCL19 and CCL21 induce a potent proinflammatory differentiation program in licensed dendritic cells. Immunity 2005; 22: 493-505.
44 Damas JK, Smith C, Oie E. et al. Enhanced expression of the homeostatic chemokines CCL19 and CCL21 in clinical and experimental atherosclerosis. Possible pathogenic role in plaque destabilization. Arterioscler Thromb Vasc Biol 2007; 27: 614-620.
45 Trogan E, Fayad ZA, Itskovich VV. et al. Serial studies of mouse atherosclerosis by in vivo magnetic resonance imaging detect lesion regression after correction of dyslipidemia. Arterioscler Thromb Vasc Biol 2004; 24: 1714-1719.
46 Llodra J, Angeli V, Liu J. et al. Emigration of monocyte- derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc Natl Acad Sci USA 2004; 101: 11779-11784.
47 Trogan E, Feig JE, Dogan S. et al. Gene expression changes in foam cells and the role of chemokine receptor CCR7 during atherosclerosis regression in ApoEdeficient mice. Proc Natl Acad Sci USA 2006; 103: 3781-3786.
48 Trogan E, Choudhury RP, Dansky HM. et al. Laser capture microdissection analysis of gene expression in macrophages from atherosclerotic lesions of apolipoprotein E-deficient mice. Proc Natl Acad Sci USA 2002; 99: 2234-2239.
49 Terkeltaub R, Banka CL, Solan J. et al. Oxidized LDL induces monocytic cell expression of interleukin- 8, a chemokine with T-lymphocyte chemotactic activity. Arterioscler Thromb 1994; 14: 47-53.
50 Apostolopoulos J, Davenport P, Tipping PG. Interleukin- 8 production by macrophages from atheromatous plaques. Arterioscler Thromb Vasc Biol 1996; 16: 1007-1012.
51 Boisvert WA, Santiago R, Curtiss LK. et al. A leukocyte homologue of the IL-8 receptor CXCR-2 mediates the accumulation of macrophages in atherosclerotic lesions of LDL receptor-deficient mice. J Clin Invest 1998; 101: 353-363.
52 Boisvert WA, Rose DM, Johnson KA. et al. Upregulated expression of the CXCR2 ligand KC/GROalpha in atherosclerotic lesions plays a central role in macrophage accumulation and lesion progression. Am J Pathol 2006; 168: 1385-1395.
53 Luster AD, Ravetch JV. Biochemical characterization of a gamma interferon-inducible cytokine (IP-10). J Exp Med 1987; 166: 1084-1097.
54 Mach F, Sauty A, Iarossi AS. et al. Differential expression of three T lymphocyte-activating CXC chemokines by human atheroma-associated cells. J Clin Invest 1999; 104: 1041-1050.
55 Veillard NR, Steffens S, Pelli G. et al. Differential influence of chemokine receptors CCR2 and CXCR3 in development of atherosclerosis in vivo. Circulation 2005; 112: 870-878.
56 Heller EA, Liu E, Tager AM. et al. Chemokine CXCL10 promotes atherogenesis by modulating the local balance of effector and regulatory T cells. Circu lation 2006; 113: 2301-2312.
57 Campbell JJ, Hedrick J, Zlotnik A. et al. Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 1998; 279: 381-384.
58 Kodali RB, Kim WJ, Galaria II. et al. CCL11 (Eotaxin) induces CCR3-dependent smooth muscle cell migration. Arterioscler Thromb Vasc Biol 2004; 24: 1211-1216.
59 Kodali R, Hajjou M, Berman AB. et al. Chemokines induce matrix metalloproteinase-2 through activation of epidermal growth factor receptor in arterial smooth muscle cells. Cardiovasc Res 2006; 69: 706-715.
60 Minami M, Kume N, Shimaoka T. et al. Expression of SR-PSOX, a novel cell-surface scavenger receptor for phosphatidylserine and oxidized LDL in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol 2001; 21: 1796-1800.
61 Wuttge DM, Zhou X, Sheikine Y. et al. CXCL16/SR-PSOX is an interferon-gamma-regulated chemokine and scavenger receptor expressed in atherosclerotic lesions. Arterioscler Thromb Vasc Biol 2004; 24: 750-755.
62 Sheikine Y, Bang CS, Nilsson L. et al. Decreased plasma CXCL16/SR-PSOX concentration is associated with coronary artery disease. Atherosclerosis 2006; 188: 462-466.
63 Aslanian AM, Charo IF. Targeted disruption of the scavenger receptor and chemokine CXCL16 accelerates atherosclerosis. Circulation 2006; 114: 583-590.
64 Bazan JF, Bacon KB, Hardiman G. et al. A new class of membrane-bound chemokine with a CX3C motif. Nature 1997; 385: 640-644.
65 McDermott DH, Halcox JP, Schenke WH. et al. Association between polymorphism in the chemokine receptor CX3CR1 and coronary vascular endothelial dysfunction and atherosclerosis. Circ Res 2001; 89: 401-407.
66 Moatti D, Faure S, Fumeron F. et al. Polymorphism in the fractalkine receptor CX3CR1 as a genetic risk factor for coronary artery disease. Blood 2001; 97: 1925-1928.
67 Niessner A, Marculescu R, Haschemi A. et al. Opposite effects of CX3CR1 receptor polymorphisms V249I and T280M on the development of acute coronary syndrome. A possible implication of fractalkine in inflammatory activation. Thromb Haemost 2005; 93: 949-954.
68 Greaves DR, Hakkinen T, Lucas AD. et al. Linked chromosome 16q13 chemokines, macrophage-derived chemokine, fractalkine, and thymus- and activationregulated chemokine, are expressed in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol 2001; 21: 923-929.
69 Wong BW, Wong D, McManus BM. Characterization of fractalkine (CX3CL1) and CX3CR1 in human coronary arteries with native atherosclerosis, diabetes mellitus, and transplant vascular disease. Cardiovasc Pathol 2002; 11: 332-338.
70 Lesnik P, Haskell CA, Charo IF. Decreased atherosclerosis in CX3CR1-/- mice reveals a role for fractalkine in atherogenesis. J Clin Invest 2003; 111: 333-340.
71 Combadiere C, Potteaux S, Gao JL. et al. Decreased atherosclerotic lesion formation in CX3CR1/apolipoprotein E double knockout mice. Circulation 2003; 107: 1009-1016.
72 Teupser D, Pavlides S, Tan M. et al. Major reduction of atherosclerosis in fractalkine (CX3CL1)-deficient mice is at the brachiocephalic artery, not the aortic root. Proc Natl Acad Sci USA 2004; 101: 17795-17800.
73 Niessner A, Marculescu R, Kvakan H. et al. Fractalkine receptor polymorphisms V2491 and T280M as genetic risk factors for restenosis. Thromb Haemost 2005; 94: 1251-1256.
74 Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003; 19: 71-82.
75 Tacke F, Alvarez D, Kaplan TJ. et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 2007; 117: 185-194.
76 Weber C, Belge KU, von Hundelshausen P. et al. Differential chemokine receptor expression and function in human monocyte subpopulations. J Leukoc Biol 2000; 67: 699-704.
77 van Wanrooij EJ, Happe H, Hauer AD. et al. HIV entry inhibitor TAK-779 attenuates atherogenesis in low-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol 2005; 25: 2642-2647.
78 Horvath C, Welt FG, Nedelman M. et al. Targeting CCR2 or CD18 inhibits experimental in-stent restenosis in primates: inhibitory potential depends on type of injury and leukocytes targeted. Circ Res 2002; 90: 488-494.
79 Usui M, Egashira K, Ohtani K. et al. Anti-monocyte chemoattractant protein-1 gene therapy inhibits restenotic changes (neointimal hyperplasia) after balloon injury in rats and monkeys. Faseb J 2002; 16: 1838-1840.
80 Schober A, Manka D, von Hundelshausen P. et al. Deposition of platelet RANTES triggering monocyte recruitment requires P-selectin and is involved in neointima formation after arterial injury. Circulation 2002; 106: 1523-1529.
81 Frangogiannis NG, Smith CW, Entman ML. The inflammatory response in myocardial infarction. Cardiovasc Res 2002; 53: 31-47.
82 Dewald O, Ren G, Duerr GD. et al. Of mice and dogs: species-specific differences in the inflammatory response following myocardial infarction. Am J Pathol 2004; 164: 665-677.
83 Frangogiannis N. Chemokines in ischemia-reperfusion injury. Thromb Haemost 2007; 97: 738-747.
84 Dewald O, Zymek P, Winkelmann K. et al. CCL2/Monocyte Chemoattractant Protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circ Res 2005; 96: 881-889.
85 Potteaux S, Combadiere C, Esposito B. et al. Chemokine receptor CCR1 disruption in bone marrow cells enhances atherosclerotic lesion development and inflammation in mice. Mol Med 2005; 11: 16-20.