Innate and acquired immunity in atherogenesis

Nature Medicine

Volumn 8, Issue 11, 2002, Pages 1218-1226

  Binder, Christoph J ^a   Chang, Mi Kyung ^a   Shaw, Peter X ^a   Miller, Yury I ^a   Hartvigsen, Karsten ^a   Dewan, Asheesh ^a   Witztum, Joseph L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; B LYMPHOCYTE RECEPTOR; C REACTIVE PROTEIN; CD14 ANTIGEN; CD36 ANTIGEN; CD40 LIGAND; CHEMOKINE RECEPTOR CCR2; CHOLESTEROL; COLONY STIMULATING FACTOR 1; CYTOKINE; GAMMA INTERFERON; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHORYLCHOLINE; PROTEOGLYCAN; RAG1 PROTEIN; RAG2 PROTEIN; SCAVENGER RECEPTOR; SERUM AMYLOID A; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG;

ATHEROGENESIS; ATHEROSCLEROSIS; B LYMPHOCYTE; CARDIOVASCULAR DISEASE; CYTOKINE RELEASE; HUMAN; HYPERCHOLESTEROLEMIA; IMMUNE RESPONSE; IMMUNITY; IMMUNOMODULATION; INFLAMMATION; LIPID OXIDATION; MOLECULAR MIMICRY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RISK FACTOR; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIGENS; ARTERIOSCLEROSIS; HUMANS; LIPOPROTEINS, LDL; MICE; MOLECULAR MIMICRY; PHOSPHATIDYLCHOLINES;

EID: 0036852824     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm1102-1218     Document Type: Review

References (98)

1. Tuzcu, E.M. et al. High prevalence of coronary atherosclerosis in asymptomatic teenagers and young adults: Evidence from intravascular ultrasound. Circulation 103, 2705-2710 (2001).
2. Leitersdorf, E., Tobin, E.J., Davignon, J. & Hobbs, H.H. Common low-density lipoprotein receptor mutations in the French Canadian population. J. Clin. Invest. 85, 1014-1023 (1990).
3. Glass, C.K. & Witztum, J.L. Atherosclerosis: The road ahead. Cell 104, 503-516 (2001).
4. Hansson, G.K., Libby, P., Schonbeck, U. & Yan, Z.Q. Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ. Res. 91, 281-291 (2002).
5. Hansson, G.K. Immune mechanisms in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 21, 1876-1890 (2001).
6. Hörkkö, S. et al. Immunological responses to oxidized LDL. Free Radic. Biol. Med. 28, 1771-1779 (2000).
7. Ross, R. Atherosclerosis - An inflammatory disease. N. Engl. J. Med. 340, 115-126 (1999).
8. Libby, P., Ridker, P.M. & Maseri, A. Inflammation and atherosclerosis. Circulation 105, 1135-1143 (2002).
9. Williams, K.J. & Tabas, I. The response-to-retention hypothesis of atherogenesis reinforced. Curr. Opin. Lipidol. 9, 471-474 (1998).
10. Skalen, K. et al. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature 417, 750-754 (2002).
11. Gaut, J.P. & Heinecke, J.W. Mechanisms for oxidizing low-density lipoprotein. Insights from patterns of oxidation products in the artery wall and from mouse models of atherosclerosis. Trends Cardiovasc. Med. 11, 103-112 (2001).
12. Pratico, D. Lipid peroxidation in mouse models of atherosclerosis. Trends Cardiovasc. Med. 11, 112-116 (2001).
13. Colles, S.M., Maxson, J.M., Carlson, S.G. & Chisolm, G.M. Oxidized LDL-induced injury and apoptosis in atherosclerosis. Potential roles for oxysterols. Trends Cordiovasc. Med. 11, 131-138 (2001).
14. Berliner, J.A., Subbanagounder, G., Leitinger, N., Watson, A.D. & Vora, D. Evidence for a role of phospholipid oxidation products in atherogenesis. Trends Cardiovasc. Med. 11, 142-147 (2001).
15. Marathe G.K., Prescott, S.M., Zimmerman G.A. & McIntyre T.M. Oxidized LDL contains inflammatory PAF-like phospholipids. Trends Cardiovasc. Med. 11, 139-142 (2001).
16. Witztum, J.L. & Steinberg, D. The oxidative modification hypothesis of atherosclerosis: Does it hold for humans? Trends Cardiovasc. Med. 11, 93-102 (2001).
17. Suzuki, H. et al. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 386, 292-296 (1997).
18. Febbraio, M. et al. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J. Clin. Invest. 105, 1049-1056 (2000).
19. Libby, P., Egan, D. & Skarlatos, S. Roles of infectious agents in atherosclerosis and restenosis: An assessment of the evidence and need for future research. Circulation 96, 4095-4103 (1997).
20. Landmesser, U. & Harrison, D.G. Oxidant stress as a marker for cardiovascular events - Ox marks the spot. Circulation 104, 2638-2640 (2001).
21. Dansky, H.M., Charlton, S.A., Harper, M.M. & Smith, J.D. T and B lymphocytes play a minor role in atherosclerotic plaque formation in the apolipoprotein Edeficient mouse. Proc. Natl. Acad. Sci. USA 94, 4642-4646 (1997).
22. -/- mice. J. Clin. Invest. 100, 1575-1580 (1997).
23. Song, L., Leung, C. & Schindler, C. Lymphocytes are important in early atherosclerosis. J. Clin. Invest. 108, 251-259 (2001).
24. Reardon, C.A. et al. Effect of immune deficiency on lipoproteins and atherosclerosis in male apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 21, 1011-1016 (2001).
25. + T cells aggravates atherosclerosis in immunodeficient apolipoprotein E knockout mice. Circulation 102, 2919-2922 (2000).
26. Palinski, W., Miller, E. & Witztum, J.L. Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis. Proc. Natl. Acad. Sci. USA 92, 821-825 (1995).
27. Ameli, S. et al. Effect of immunization with homologous LDL and oxidized LDL on early atherosclerosis in hypercholesterolemic rabbits. Arterioscler. Thromb. Vasc. Biol. 16, 1074-1079 (1996).
28. Freigang, S., Hörkkö, S., Miller, E., Witztum, J.L. & Palinski, W. Immunization of LDL receptor-deficient mice with homologous malondialdehyde-modified and native LDL reduces progression of atherosclerosis by mechanisms other than induction of high titers of antibodies to oxidative neoepitopes. Arterioscler. Thromb. Vasc. Biol. 18, 1972-1982 (1998).
29. George, J. et al. Hyperimmunization of apo-E-deficient mice with homologous malondialdehyde low-density lipoprotein suppresses early atherogenesis. Atherosclerosis 138, 147-152 (1998).
30. Zhou, X., Caligiuri, G., Hamsten, A., Lefvert, A.K. & Hansson, G.K. LDL immunization induces T-cell-dependent antibody formation and protection against atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 21, 108-114 (2001).
31. Nicoletti, A., Kaveri, S., Caligiuri, G., Bariaety, J. & Hansson, G.K. Immunoglobulin treatment reduces atherosclerosis in apo E knockout mice. J. Clin. Invest. 102, 910-918 (1998).
32. Medzhitov, R. & Janeway, C.A., Jr. Decoding the patterns of self and nonself by the innate immune system. Science 296, 298-300 (2002).
33. Medzhitov, R. Toll-like receptors and innate immunity. Nature Rev. Immunol. 1, 135-145 (2001).
34. Gosling, J. et al. MCP-1 deficiency reduces susceptibility to atherosclerosis in mice that overexpress human apolipoprotein 8. J. Clin. Invest. 103, 773-778 (1999).
35. -/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 394, 894-897 (1998).
36. Smith, J.D. et al. Decreased atherosclerosis in mice deficient in both macrophage colony-stimulating factor (op) and apolipoprotein E. Proc. Natl. Acad. Sci. USA 92, 8264-8268 (1995).
37. Cybulsky, M.I. & Gimbrone, M.A., Jr. Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis. Science 251, 788-791 (1991).
38. Witztum, J.L. & Berliner, J.A. Oxidized phospholipids and isoprostanes in atherosclerosis. Curr. Opin. Lipidol. 9, 441-448 (1998).
39. Edfeldt, K., Swedenborg, J., Hansson, G.K. & Yan Z.Q. Expression of toll-like receptors in human atherosclerotic lesions: A possible pathway for plaque activation. Circulation 105, 1158-1161 (2002).
40. Wright, S.D. et al. Infectious agents are not necessary for murine atherogenesis. J. Exp. Med. 191, 1437-1442 (2000).
41. Kiechl, S. et al. Toll-like receptor 4 polymorphisms and atherogenesis. N. Engl. J. Med. 347, 185-192 (2002).
42. Hubacek, J.A. et al. C(-260)→T polymorphism in the promoter of the CD14 monocyte receptor gene as a risk factor for myocardial infarction. Circulation 99, 3218-3220 (1999).
43. Li, A.C. & Glass, C.K. The macrophage foam cell as a target for therapeutic intervention. Nat. Med. 8, 1235-1242 (2002).
44. Vlaicu, R., Niculescu, F., Rus, H.G. & Cristea, A. Immunohistochemical localization of the terminal C5b-9 complement complex in human aortic fibrous plaque. Atherosclerosis 57, 163-177 (1985).
45. Buono, C. et al. Influence of C3 deficiency on atherosclerosis. Circulation 105, 3025-3031 (2002).
46. Volanakis, J.E. Human C-reactive protein: Expression, structure, and function. Mol. Immunol. 38, 189-197 (2001).
47. Yasojima, K., Schwab, C., McGeer, E.G. & McGeer, P.L. Generation of C-reactive protein and complement components in atherosclerotic plaques. Am. J. Pathol. 158, 1039-1051 (2001).
48. Shaw, P.X. et al. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J. Clin. Invest. 105, 1731-1740 (2000).
49. Vos, Q., Lees, A., Wu, Z.Q., Snapper, C.M. & Mond, J.J. B-cell activation by T-cell-independent type 2 antigens as an integral part of the humoral immune response to pathogenic microorganisms. Immunol. Rev. 176, 154-170 (2000).
50. Ochsenbein, A.F. et al. Correlation of T cell independence of antibody responses with antigen dose reaching secondary lymphoid organs: Implications for splenectomized patients and vaccine design. J. Immunol. 164, 6296-6302 (2000).
51. Millonig, G., Schwentner, C., Mueller, P., Mayerl, C. & Wick, G. The vascular-associated lymphoid tissue: A new site of local immunity. Curr. Opin. Lipidol. 12, 547-553 (2001).
52. beige mutations. Arterioscler. Thromb. Vasc. Biol. 22, 1341-1346 (2002).
53. Sohma, Y. et al. Accumulation of plasma cells in atherosclerotic lesions of Watanabe heritable hyperlipidemic rabbits. Proc. Natl. Acad. Sci. USA 92, 4937-4941 (1995).
54. Zhou, X. & Hansson, G.K. Detection of B cells and proinflammatory cytokines in atherosclerotic plaques of hypercholesterolaemic apolipoprotein E knockout mice. Scand. J. Immunol. 50, 25-30 (1999).
55. Mach, F. et al. Functional CD40 ligand is expressed on human vascular endothelial cells, smooth muscle cells, and macrophages: Implications for CD40-CD40 ligand signaling in atherosclerosis. Proc. Natl. Acad. Sci. USA 94, 1931-1936 (1997).
56. Lutgens, E. et al. Requirement for CD154 in the progression of atherosclerosis. Nature Med. 5, 1313-1316 (1999).
57. Mach, F., Schbnbeck, U., Sukhova, G.K., Atkinson, E. & Libby, P. Reduction of atherosclerosis in mice by inhibition of CD40 signalling. Nature 394, 200-203 (1998).
58. Schönbeck, U., Sukhova, G.K., Shimizu, K., Mach, F. & Libby, P. Inhibition of CD40 signaling limits evolution of established atherosclerosis in mice. Proc. Natl. Acad. Sci. USA 97, 7458-7463 (2000).
59. Lutgens, E. et al. Both early and deJayed anti-CD40L antibody treatment induces a stable plaque phenotype. Proc. Natl. Acad. Sci. USA 97, 7464-7469 (2000).
60. Uyemura, K. et al. Cross-regulatory roles of interleukin (IL)-12 and IL-10 in atherosclerosis. J. Clin. Invest. 97, 2130-2138 (1996).
61. Gerdes, N. et al. Expression of interleukin (IL)-18 and functional IL-18 receptor on human vascular endothelial cells, smooth muscle cells, and macrophages: Implications for atherogenesis. J. Exp. Med. 195, 245-257 (2002).
62. Gupta, S. et al. IFN-γ potentiates atherosclerosis in ApoE knock-out mice. J. Clin. Invest. 99, 2752-2761 (1997).
63. -/- mice. Am. J. Pathol. 157, 1819-1824 (2000).
64. Lee, T.S., Yen, H.C., Pan, C.C. & Chau, L.Y. The role of interleukin 12 in the development of atherosclerosis in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 19, 734-742 (1999).
65. -/- mice through release of interferon-γ. Circ. Res. 90, E34-E38 (2002).
66. Pinderski, L.J. et al. Overexpression of interleukin-10 by activated T lymphocytes inhibits atherosclerosis in LDL receptor-deficient mice by altering lymphocyte and macrophage phenotypes. Circ. Res. 90, 1064-1071 (2002).
67. Laurat, E. et al. In vivo downregulation of T helper cell 1 immune responses reduces atherogenesis in apolipoprotein E-knockout mice. Circulation 104, 197-202 (2001).
68. Huber, S.A., Sakkinen, P., David, C., Newell, M.K. & Tracy, R.P. T helper-cell phenotype regulates atherosclerosis in mice under conditions of mild hypercholesterolemia. Circulation 103, 2610-2616 (2001).
69. -/- mice. Arterioscler. Thromb. Vasc. Biol. 22, 456-461 (2002).
70. Mallat, Z. et al. Inhibition of transforming growth factor-β signaling accelerates atherosclerosis and induces an unstable plaque phenotype in mice. Circ. Res. 89, 930-934 (2001).
71. Lutgens, E. et al. Transforming growth factor-β mediates balance between inflammation and fibrosis during plaque progression. Arterioscler. Thromb. Vasc. Biol. 22, 975-982 (2002).
72. Caligiuri, G., Nicoletti, A., Poirier, B. & Hansson, G.K. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J. Clin. Invest. 109, 745-753 (2002).
73. Witztum, I.L. Splenic immunity and atherosclerosis: A glimpse into a novel paradigm? J. Clin. Invest. 109, 721-724 (2002).
74. Robinette, C.D. & Fraumeni, J.F., Jr. Splenectomy and subsequent mortality in veterans of the 1939-45 war. Lancet 2, 127-129 (1977).
75. Paulsson, G., Zhou, X., Tomquist, E. & Hansson, G.K. Oligoclonal T cell expansions in atherosclerotic lesions of apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 20, 10-17 (2000).
76. 2-glycoprotein I-reactive lymphocytes enhances early atherosclerosis in LDL receptor-deficient mice. Circulation 102, 1822-1827 (2000).
77. Beck, J.D., Pankow, J., Tyroler, H.A. & Offenbacher, S. Dental infections and atherosclerosis. Am. Heart J. 138, S528-S533 (1999).
78. Wick, G., Perschinka, H. & Millonig, G. Atherosclerosis as an autoimmune disease: An update. Trends Immunol. 22, 665-669 (2001).
79. Mayr, M., Kiechl, S., Willeit, J., Wick, G. & Xu, Q. Infections, immunity, and atherosclerosis: Associations of antibodies to Chlamydia pneumoniae, Helicobacter pylori, and cytomegalovirus with immune reactions to heat-shock protein 60 and carotid or femoral atherosclerosis. Circulation 102, 833-839 (2000).
80. Afek, A. et al. Immunization of low-density lipoprotein receptor deficient (LDLRD) mice with heat shock protein 65 (HSP-65) promotes early atherosclerosis. J. Autoimmun. 14, 115-121 (2000).
81. Maron, R. et al. Mucosal administration of heat shock protein-65 decreases atherosclerosis and inflammation in aortic arch of low-density lipoprotein receptor-deficient mice. Circulation 106, 1708-1715 (2002).
82. Palinski, W. & Witztum, J.L. Immune responses to oxidative neoepitopes on LDL and phospholipids modulate the development of atherosclerosis. J. Intern. Med. 247, 371-380 (2000).
83. Gillotte, K.L., Hörkkö, S., Witztum, J.L. & Steinberg, D. Oxidized phospholipids, linked to apolipoprotein B of oxidized LDL, are ligands for macrophage scavenger receptors. J. Lipid Res. 41, 824-833 (2000).
84. Friedman, P., Hörkkö, S., Steinberg, D., Witztum, J.L. & Dennis, E.A. Correlation of antiphospholipid antibody recognition with the structure of synthetic oxidized phospholipids. Importance of Schiff base formation and aldol concentration. J. Biol. Chem. 277, 7010-7020 (2002).
85. Ylä-Herttuala, S. et al. Rabbit and human atherosclerotic lesions contain IgG that recognizes epitopes of oxidized LDL. Arterioscler. Thromb. 14, 32-40 (1994).
86. Cyrus, T. et al. Absence of 12/15-lipoxygenase expression decreases lipid peroxidation and atherogenesis in apolipoprotein e-deficient mice. Circulation 103, 2277-2282 (2001).
87. Tsimikas, S., Palinski, W. & Witztum, J.L. Circulating autoantibodies to oxidized LDL correlate with arterial accumulation and depletion of oxidized LDL in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 21, 95-100 (2001).
88. Stemme, S. et al. T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc. Natl. Acad. Sci. USA 92, 3893-3897 (1995).
89. Palinski, W. et al. Cloning of monoclonal autoantibodies to epitopes of oxidized lipoproteins from apolipoprotein E-deficient mice. Demonstration of epitopes of oxidized low density lipoprotein in human plasma. J. Clin. Invest. 98, 800-814 (1996).
90. Hörkkö, S. et al. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J. Clin. Invest. 103, 117-128 (1999).
91. Gillotte-Taylor, K., Boullier, A., Witztum, J.L., Steinberg, D. & Quehenberger, O. Scavenger receptor class B type I as a receptor for oxidized low density lipoprotein. J. Lipid Res. 42, 1474-1482 (2001).
92. Boullier, A. et al. The binding of oxidized low density lipoprotein to mouse CD36 is mediated in part by oxidized phospholipids that are associated with both the lipid and protein moieties of the lipoprotein. J. Biol. Chem. 275, 9163-9169 (2000).
93. Podrez, E.A. et al. Identification of a novel family of oxidized phospholipids that serve as ligands for the macrophage scavenger receptor CD36. J. Biol. Chem. 277, 38503-38516 (2002).
94. Podrez, E.A. et al. A novel family of atherogenic oxidized phospholipids promotes macrophage foam cell formation via the scavenger receptor CD36 and is enriched in atherosclerotic lesions. J. Biol. Chem. 277, 38517-38523 (2002).
95. Chang, M.K. et al. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: Evidence that oxidation-specific epitopes mediate macrophage recognition. Proc. Natl. Acad. Sci. USA 96, 6353-6358 (1999).
96. Briles, D.E., Forman, C., Hudak, S. & Claflin, J.L. Anti-phosphorylcholine antibodies of the T15 idiotype are optimally protective against Streptococcus pneumoniae. J. Exp. Med. 156, 1177-1185 (1982).
97. Gershov, D., Kim, S., Brot, N. & Elkon, K.B. C-Reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: Implications for systemic autoimmunity. J. Exp. Med. 192, 1353-1364 (2000).
98. Chang, M.K., Binder, C.J., Torzewski, M. & Witztum, J.L. C-reactive protein binds to both oxidized LDL and apoptotic cells through recognition of a common ligand: Phosphorylcholine of oxidized phospholipids. Proc Natl. Acad. Sci. USA 99, 13043-13048 (2002).