The innate immune response to products of phospholipid peroxidation

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 10, 2012, Pages 2465-2475

  Weismann, David ^a,b   Binder, Christoph J ^a,b  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Apoptosis; Damage associated molecular pattern; Lipid peroxidation; Oxidation specific epitope; Oxidized LDL; Pattern recognition receptor

Indexed keywords

4 HYDROXYNONENAL; C REACTIVE PROTEIN; CARDIOLIPIN; COMPLEMENT FACTOR H; EPITOPE; HEAT SHOCK PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN M ANTIBODY; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MALONALDEHYDE; PATTERN RECOGNITION RECEPTOR; PHOSPHATIDYLSERINE; PHOSPHOLIPID; PHOSPHORYLCHOLINE; POLYSACCHARIDE; SCAVENGER RECEPTOR; THROMBOXANE SYNTHASE; TOLL LIKE RECEPTOR;

ADAPTIVE IMMUNITY; AMINO ACID SUBSTITUTION; ATHEROGENESIS; ATHEROSCLEROSIS; BINDING AFFINITY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; ELECTROPHILICITY; EPITOPE MAPPING; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; LIPID OXIDATION; LIPID PEROXIDATION; MACROPHAGE; MOLECULAR DYNAMICS; NONHUMAN; OPSONIZATION; OXIDATIVE STRESS; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN CONFORMATION; PROTEIN LIPID INTERACTION; PROTEIN POLYMORPHISM; PROTEIN PROTEIN INTERACTION; RETINA MACULA AGE RELATED DEGENERATION; REVIEW;

ANIMALS; EPITOPES; HUMANS; IMMUNITY, INNATE; LIPID PEROXIDATION; OXIDATION-REDUCTION; PHOSPHOLIPIDS; RECEPTORS, PATTERN RECOGNITION;

EID: 84863986254     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.01.018     Document Type: Review

References (124)

1. M.Y. Chou, K. Hartvigsen, L.F. Hansen, L. Fogelstrand, P.X. Shaw, A. Boullier, C.J. Binder, and J.L. Witztum Oxidation-specific epitopes are important targets of innate immunity J. Intern. Med. 263 2008 479 488
2. C. Janeway, P. Travers, M. Walport, and M. Shlomchik Immunobiology 5th edition 2001
3. G.Y. Chen, and G. Nunez Sterile inflammation: sensing and reacting to damage Nat. Rev. Immunol. 10 2010 826 837
4. P. Matzinger Tolerance, danger, and the extended family Annu. Rev. Immunol. 12 1994 991 1045
5. Y.I. Miller, S.H. Choi, P. Wiesner, L. Fang, R. Harkewicz, K. Hartvigsen, A. Boullier, A. Gonen, C.J. Diehl, X. Que, E. Montano, P.X. Shaw, S. Tsimikas, C.J. Binder, and J.L. Witztum Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity Circ. Res. 108 2011 235 248
6. M.K. Chang, C. Bergmark, A. Laurila, S. Horkko, K.H. Han, P. Friedman, E.A. Dennis, and J.L. Witztum 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. U. S. A. 96 1999 6353 6358
7. V.E. Kagan, G.G. Borisenko, Y.Y. Tyurina, V.A. Tyurin, J. Jiang, A.I. Potapovich, V. Kini, A.A. Amoscato, and Y. Fujii Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine Free Radic. Biol. Med. 37 2004 1963 1985
8. W. Palinski, S. Horkko, E. Miller, U.P. Steinbrecher, H.C. Powell, L.K. Curtiss, and J.L. Witztum 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 1996 800 814
9. Y. Imai, K. Kuba, G.G. Neely, R. Yaghubian-Malhami, T. Perkmann, G. van Loo, M. Ermolaeva, R. Veldhuizen, Y.H. Leung, H. Wang, H. Liu, Y. Sun, M. Pasparakis, M. Kopf, C. Mech, S. Bavari, J.S. Peiris, A.S. Slutsky, S. Akira, M. Hultqvist, R. Holmdahl, J. Nicholls, C. Jiang, C.J. Binder, and J.M. Penninger Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury Cell 133 2008 235 249
10. K. Horie, T. Miyata, K. Maeda, S. Miyata, S. Sugiyama, H. Sakai, C. van Ypersole, V.M. de Strihou, J.L. Monnier, and K. Kurokawa Witztum Immunohistochemical colocalization of glycoxidation products and lipid peroxidation products in diabetic renal glomerular lesions. Implication for glycoxidative stress in the pathogenesis of diabetic nephropathy J. Clin. Invest. 100 1997 2995 3004
11. M.J. Sanchez Perez, E. Gonzalez-Reimers, F. Santolaria-Fernandez, M.J. de la Vega-Prieto, A. Martinez-Riera, P.A. Gonzalez, E. Rodriguez Rodriguez, and M.C. Duran-Castellon Lipid peroxidation and serum cytokines in acute alcoholic hepatitis Alcohol Alcohol. 41 2006 593 597
12. L. Haider, M.T. Fischer, J.M. Frischer, J. Bauer, R. Hoftberger, G. Botond, H. Esterbauer, C.J. Binder, J.L. Witztum, and H. Lassmann Oxidative damage in multiple sclerosis lesions Brain 134 2011 1914 1924
13. R. Dei, A. Takeda, H. Niwa, M. Li, Y. Nakagomi, M. Watanabe, T. Inagaki, Y. Washimi, Y. Yasuda, K. Horie, T. Miyata, and G. Sobue Lipid peroxidation and advanced glycation end products in the brain in normal aging and in Alzheimer's disease Acta Neuropathol. 104 2002 113 122
14. T.J. Neale, P.P. Ojha, M. Exner, H. Poczewski, B. Ruger, J.L. Witztum, P. Davis, and D. Kerjaschki Proteinuria in passive Heymann nephritis is associated with lipid peroxidation and formation of adducts on type IV collagen J. Clin. Invest. 94 1994 1577 1584
15. J.A. Berliner, G. Subbanagounder, N. Leitinger, A.D. Watson, and D. Vora Evidence for a role of phospholipid oxidation products in atherogenesis Trends Cardiovasc. Med. 11 2001 142 147
16. D. Steinberg, and J.L. Witztum Oxidized low-density lipoprotein and atherosclerosis Arterioscler. Thromb. Vasc. Biol. 30 2010 2311 2316
17. Y.I. Miller, S.H. Choi, L. Fang, and S. Tsimikas Lipoprotein modification and macrophage uptake: role of pathologic cholesterol transport in atherogenesis Subcell. Biochem. 51 2010 229 251
18. E.A. Podrez, H.M. Abu-Soud, and S.L. Hazen Myeloperoxidase-generated oxidants and atherosclerosis Free Radic. Biol. Med. 28 2000 1717 1725
19. B. Shao, and J.W. Heinecke HDL, lipid peroxidation, and atherosclerosis J. Lipid Res. 50 2009 599 601
20. G.M. Chisolm, and D. Steinberg The oxidative modification hypothesis of atherogenesis: an overview Free Radic. Biol. Med. 28 2000 1815 1826
21. U.P. Steinbrecher, S. Parthasarathy, D.S. Leake, J.L. Witztum, and D. Steinberg Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids Proc. Natl. Acad. Sci. U. S. A. 81 1984 3883 3887
22. H. Esterbauer, R.J. Schaur, and H. Zollner Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes Free Radic. Biol. Med. 11 1991 81 128
23. C.J. Binder, M.K. Chang, P.X. Shaw, Y.I. Miller, K. Hartvigsen, A. Dewan, and J.L. Witztum Innate and acquired immunity in atherogenesis Nat. Med. 8 2002 1218 1226
24. A.J. Narkates, and J.E. Volanakis C-reactive protein binding specificities: artificial and natural phospholipid bilayers Ann. N. Y. Acad. Sci. 389 1982 172 182
25. Y.P. Li, C. Mold, and T.W. Du Clos Sublytic complement attack exposes C-reactive protein binding sites on cell membranes J. Immunol. 152 1994 2995 3005
26. W. Harnett, and M.M. Harnett Phosphorylcholine: friend or foe of the immune system? Immunol. Today 20 1999 125 129
27. M. Hecker, and V. Ullrich On the mechanism of prostacyclin and thromboxane A2 biosynthesis J. Biol. Chem. 264 1989 141 150
28. T. Ohya Formation of a new 1,1,1 adduct in the reaction of malondialdehyde, n-hexylamine and alkanal under neutral conditions Biol. Pharm. Bull. 16 1993 137 141
29. D.J. Tuma, G.M. Thiele, D. Xu, L.W. Klassen, and M.F. Sorrell Acetaldehyde and malondialdehyde react together to generate distinct protein adducts in the liver during long-term ethanol administration Hepatology 23 1996 872 880
30. D. Xu, G.M. Thiele, M.L. Kearley, M.D. Haugen, L.W. Klassen, M.F. Sorrell, and D.J. Tuma Epitope characterization of malondialdehyde-acetaldehyde adducts using an enzyme-linked immunosorbent assay Chem. Res. Toxicol. 10 1997 978 986
31. G.M. Thiele, M.J. Duryee, M.S. Willis, M.F. Sorrell, T.L. Freeman, D.J. Tuma, and L.W. Klassen Malondialdehyde-acetaldehyde (MAA) modified proteins induce pro-inflammatory and pro-fibrotic responses by liver endothelial cells Comp. Hepatol. 3 Suppl. 1 2004 S25
32. M.J. Duryee, L.W. Klassen, C.S. Schaffert, D.J. Tuma, C.D. Hunter, R.P. Garvin, D.R. Anderson, and G.M. Thiele Malondialdehyde-acetaldehyde adduct is the dominant epitope after MDA modification of proteins in atherosclerosis Free Radic. Biol. Med. 49 2010 1480 1486
33. R.J. Schaur Basic aspects of the biochemical reactivity of 4-hydroxynonenal Mol. Aspects Med. 24 2003 149 159
34. G. Jurgens, J. Lang, and H. Esterbauer Modification of human low-density lipoprotein by the lipid peroxidation product 4-hydroxynonenal Biochim. Biophys. Acta 875 1986 103 114
35. X. Gu, M. Sun, B. Gugiu, S. Hazen, J.W. Crabb, and R.G. Salomon Oxidatively truncated docosahexaenoate phospholipids: total synthesis, generation, and Peptide adduction chemistry J. Org. Chem. 68 2003 3749 3761
36. V.A. Fadok, D.L. Bratton, S.C. Frasch, M.L. Warner, and P.M. Henson The role of phosphatidylserine in recognition of apoptotic cells by phagocytes Cell Death Differ. 5 1998 551 562
37. Y.Y. Tyurina, V.A. Tyurin, Q. Zhao, M. Djukic, P.J. Quinn, B.R. Pitt, and V.E. Kagan Oxidation of phosphatidylserine: a mechanism for plasma membrane phospholipid scrambling during apoptosis? Biochem. Biophys. Res. Commun. 324 2004 1059 1064
38. V.A. Tyurin, Y.Y. Tyurina, W. Feng, A. Mnuskin, J. Jiang, M. Tang, X. Zhang, Q. Zhao, P.M. Kochanek, R.S. Clark, H. Bayir, and V.E. Kagan Mass-spectrometric characterization of phospholipids and their primary peroxidation products in rat cortical neurons during staurosporine-induced apoptosis J. Neurochem. 107 2008 1614 1633
39. H. Deguchi, J.A. Fernandez, T.M. Hackeng, C.L. Banka, and J.H. Griffin Cardiolipin is a normal component of human plasma lipoproteins Proc. Natl. Acad. Sci. U. S. A. 97 2000 1743 1748
40. V.E. Kagan, H.A. Bayir, N.A. Belikova, O. Kapralov, Y.Y. Tyurina, V.A. Tyurin, J. Jiang, D.A. Stoyanovsky, P. Wipf, P.M. Kochanek, J.S. Greenberger, B. Pitt, A.A. Shvedova, and G. Borisenko Cytochrome c/cardiolipin relations in mitochondria: a kiss of death Free Radic. Biol. Med. 46 2009 1439 1453
41. G.R. Sambrano, S. Parthasarathy, and D. Steinberg Recognition of oxidatively damaged erythrocytes by a macrophage receptor with specificity for oxidized low density lipoprotein Proc. Natl. Acad. Sci. U. S. A. 91 1994 3265 3269
42. D.R. Greaves, and S. Gordon The macrophage scavenger receptor at 30 years of age: current knowledge and future challenges J. Lipid Res. 50 Suppl. 2009 S282 S286
43. M. Krieger, and J. Herz Structures and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related protein (LRP) Annu. Rev. Biochem. 63 1994 601 637
44. G. Endemann, L.W. Stanton, K.S. Madden, C.M. Bryant, R.T. White, and A.A. Protter CD36 is a receptor for oxidized low density lipoprotein J. Biol. Chem. 268 1993 11811 11816
45. V.V. Kunjathoor, M. Febbraio, E.A. Podrez, K.J. Moore, L. Andersson, S. Koehn, J.S. Rhee, R. Silverstein, H.F. Hoff, and M.W. Freeman Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages J. Biol. Chem. 277 2002 49982 49988
46. A. Boullier, P. Friedman, R. Harkewicz, K. Hartvigsen, S.R. Green, F. Almazan, E.A. Dennis, D. Steinberg, J.L. Witztum, and O. Quehenberger Phosphocholine as a pattern recognition ligand for CD36 J. Lipid Res. 46 2005 969 976
47. K. Gillotte-Taylor, A. Boullier, J.L. Witztum, D. Steinberg, and O. Quehenberger Scavenger receptor class B type I as a receptor for oxidized low density lipoprotein J. Lipid Res. 42 2001 1474 1482
48. E.A. Podrez, T.V. Byzova, M. Febbraio, R.G. Salomon, Y. Ma, M. Valiyaveettil, E. Poliakov, M. Sun, P.J. Finton, B.R. Curtis, J. Chen, R. Zhang, R.L. Silverstein, and S.L. Hazen Platelet CD36 links hyperlipidemia, oxidant stress and a prothrombotic phenotype Nat. Med. 13 2007 1086 1095
49. E.A. Podrez, E. Poliakov, Z. Shen, R. Zhang, Y. Deng, M. Sun, P.J. Finton, L. Shan, M. Febbraio, D.P. Hajjar, R.L. Silverstein, H.F. Hoff, R.G. Salomon, and S.L. Hazen 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 2002 38517 38523
50. E.A. Podrez, E. Poliakov, Z. Shen, R. Zhang, Y. Deng, M. Sun, P.J. Finton, L. Shan, B. Gugiu, P.L. Fox, H.F. Hoff, R.G. Salomon, and S.L. Hazen Identification of a novel family of oxidized phospholipids that serve as ligands for the macrophage scavenger receptor CD36 J. Biol. Chem. 277 2002 38503 38516
51. S.L. Hazen Oxidized phospholipids as endogenous pattern recognition ligands in innate immunity J. Biol. Chem. 283 2008 15527 15531
52. R.L. Silverstein, and M. Febbraio CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior Sci. Signal. 2 2009 re3
53. S.W. Ryeom, R.L. Silverstein, A. Scotto, and J.R. Sparrow Binding of anionic phospholipids to retinal pigment epithelium may be mediated by the scavenger receptor CD36 J. Biol. Chem. 271 1996 20536 20539
54. V.A. Fadok, M.L. Warner, D.L. Bratton, and P.M. Henson CD36 is required for phagocytosis of apoptotic cells by human macrophages that use either a phosphatidylserine receptor or the vitronectin receptor (alpha v beta 3) J. Immunol. 161 1998 6250 6257
55. M.E. Greenberg, M. Sun, R. Zhang, M. Febbraio, R. Silverstein, and S.L. Hazen Oxidized phosphatidylserine-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells J. Exp. Med. 203 2006 2613 2625
56. M. Freeman, Y. Ekkel, L. Rohrer, M. Penman, N.J. Freedman, G.M. Chisolm, and M. Krieger Expression of type I and type II bovine scavenger receptors in Chinese hamster ovary cells: lipid droplet accumulation and nonreciprocal cross competition by acetylated and oxidized low density lipoprotein Proc. Natl. Acad. Sci. U. S. A. 88 1991 4931 4935
57. I. Shechter, A.M. Fogelman, M.E. Haberland, J. Seager, M. Hokom, and P.A. Edwards The metabolism of native and malondialdehyde-altered low density lipoproteins by human monocyte-macrophages J. Lipid Res. 22 1981 63 71
58. K.A. Walton, X. Hsieh, N. Gharavi, S. Wang, G. Wang, M. Yeh, A.L. Cole, and J.A. Berliner Receptors involved in the oxidized 1-palmitoyl-2-arachidonoyl- sn-glycero-3-phosphorylcholine-mediated synthesis of interleukin-8. A role for Toll-like receptor 4 and a glycosylphosphatidylinositol-anchored protein J. Biol. Chem. 278 2003 29661 29666
59. V.N. Bochkov, A. Kadl, J. Huber, F. Gruber, B.R. Binder, and N. Leitinger Protective role of phospholipid oxidation products in endotoxin-induced tissue damage Nature 419 2002 77 81
60. J.A. Berliner, and N.M. Gharavi Endothelial cell regulation by phospholipid oxidation products Free Radic. Biol. Med. 45 2008 119 123
61. V.N. Bochkov, O.V. Oskolkova, K.G. Birukov, A.L. Levonen, C.J. Binder, and J. Stockl Generation and biological activities of oxidized phospholipids Antioxid. Redox Signal. 12 2010 1009 1059
62. C.R. Stewart, L.M. Stuart, K. Wilkinson, J.M. van Gils, J. Deng, A. Halle, K.J. Rayner, L. Boyer, R. Zhong, W.A. Frazier, A. Lacy-Hulbert, J. El Khoury, D.T. Golenbock, and K.J. Moore CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer Nat. Immunol. 11 2010 155 161
63. X.Z. West, N.L. Malinin, A.A. Merkulova, M. Tischenko, B.A. Kerr, E.C. Borden, E.A. Podrez, R.G. Salomon, and T.V. Byzova Oxidative stress induces angiogenesis by activating TLR2 with novel endogenous ligands Nature 467 2010 972 976
64. J.E. Volanakis Human C-reactive protein: expression, structure, and function Mol. Immunol. 38 2001 189 197
65. S. Verma, P.E. Szmitko, and P.M. Ridker C-reactive protein comes of age Nat. Clin. Pract. Cardiovasc. Med. 2 2005 29 36 quiz 58
66. A.J. Szalai, D.E. Briles, and J.E. Volanakis Human C-reactive protein is protective against fatal Streptococcus pneumoniae infection in transgenic mice J. Immunol. 155 1995 2557 2563
67. C. Mold, S. Nakayama, T.J. Holzer, H. Gewurz, and T.W. Du Clos C-reactive protein is protective against Streptococcus pneumoniae infection in mice J. Exp. Med. 154 1981 1703 1708
68. A.J. Szalai, J.L. VanCott, J.R. McGhee, J.E. Volanakis, and W.H. Benjamin Jr. Human C-reactive protein is protective against fatal Salmonella enterica serovar typhimurium infection in transgenic mice Infect. Immun. 68 2000 5652 5656
69. E. Lysenko, J.C. Richards, A.D. Cox, A. Stewart, A. Martin, M. Kapoor, and J.N. Weiser The position of phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae affects binding and sensitivity to C-reactive protein-mediated killing Mol. Microbiol. 35 2000 234 245
70. M.K. Chang, C.J. Binder, M. Torzewski, and J.L. Witztum 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. U. S. A. 99 2002 13043 13048
71. D. Gershov, S. Kim, N. Brot, and K.B. Elkon 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 2000 1353 1364
72. L. van Tits, J. de Graaf, H. Toenhake, W. van Heerde, and A. Stalenhoef C-reactive protein and annexin A5 bind to distinct sites of negatively charged phospholipids present in oxidized low-density lipoprotein Arterioscler. Thromb. Vasc. Biol. 25 2005 717 722
73. U. Singh, M.R. Dasu, P.G. Yancey, A. Afify, S. Devaraj, and I. Jialal Human C-reactive protein promotes oxidized low density lipoprotein uptake and matrix metalloproteinase-9 release in Wistar rats J. Lipid Res. 49 2008 1015 1023
74. P.F. Zipfel, and C. Skerka Complement regulators and inhibitory proteins Nat. Rev. Immunol. 9 2009 729 740
75. D. Weismann, K. Hartvigsen, N. Lauer, K.L. Bennett, H.P. Scholl, P. Charbel Issa, M. Cano, H. Brandstatter, S. Tsimikas, C. Skerka, G. Superti-Furga, J.T. Handa, P.F. Zipfel, J.L. Witztum, and C.J. Binder Complement factor H binds malondialdehyde epitopes and protects from oxidative stress Nature 478 2011 76 81
76. M. Mihlan, S. Stippa, M. Jozsi, and P.F. Zipfel Monomeric CRP contributes to complement control in fluid phase and on cellular surfaces and increases phagocytosis by recruiting factor H Cell Death Differ. 16 2009 1630 1640
77. A.E. Hughes, N. Orr, H. Esfandiary, M. Diaz-Torres, T. Goodship, and U. Chakravarthy A common CFH haplotype, with deletion of CFHR1 and CFHR3, is associated with lower risk of age-related macular degeneration Nat. Genet. 38 2006 1173 1177
78. R. Berland, and H.H. Wortis Origins and functions of B-1 cells with notes on the role of CD5 Annu. Rev. Immunol. 20 2002 253 300
79. N. Baumgarth The double life of a B-1 cell: self-reactivity selects for protective effector functions Nat. Rev. Immunol. 11 2011 34 46
80. N. Baumgarth, J.W. Tung, and L.A. Herzenberg Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion Springer Semin. Immunopathol. 26 2005 347 362
81. M.Y. Chou, L. Fogelstrand, K. Hartvigsen, L.F. Hansen, D. Woelkers, P.X. Shaw, J. Choi, T. Perkmann, F. Backhed, Y.I. Miller, S. Horkko, M. Corr, J.L. Witztum, and C.J. Binder Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans J. Clin. Invest. 119 2009 1335 1349
82. P.X. Shaw, S. Horkko, M.K. Chang, L.K. Curtiss, W. Palinski, G.J. Silverman, and J.L. Witztum Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity J. Clin. Invest. 105 2000 1731 1740
83. D.E. Briles, C. Forman, S. Hudak, and J.L. Claflin Anti-phosphorylcholine antibodies of the T15 idiotype are optimally protective against Streptococcus pneumoniae J. Exp. Med. 156 1982 1177 1185
84. A. Tuominen, Y.I. Miller, L.F. Hansen, Y.A. Kesaniemi, J.L. Witztum, and S. Horkko A natural antibody to oxidized cardiolipin binds to oxidized low-density lipoprotein, apoptotic cells, and atherosclerotic lesions Arterioscler. Thromb. Vasc. Biol. 26 2006 2096 2102
85. G.G. Borisenko, S.L. Iverson, S. Ahlberg, V.E. Kagan, and B. Fadeel Milk fat globule epidermal growth factor 8 (MFG-E8) binds to oxidized phosphatidylserine: implications for macrophage clearance of apoptotic cells Cell Death Differ. 11 2004 943 945
86. S. Nozaki, H. Kashiwagi, S. Yamashita, T. Nakagawa, B. Kostner, Y. Tomiyama, A. Nakata, M. Ishigami, J. Miyagawa, and K. Kameda-Takemura Reduced uptake of oxidized low density lipoproteins in monocyte-derived macrophages from CD36-deficient subjects J. Clin. Invest. 96 1995 1859 1865
87. I. Tabas Macrophage death and defective inflammation resolution in atherosclerosis Nat. Rev. Immunol. 10 2010 36 46
88. K.J. Moore, V.V. Kunjathoor, S.L. Koehn, J.J. Manning, A.A. Tseng, J.M. Silver, M. McKee, and M.W. Freeman Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice J. Clin. Invest. 115 2005 2192 2201
89. H. Suzuki, Y. Kurihara, M. Takeya, N. Kamada, M. Kataoka, K. Jishage, O. Ueda, H. Sakaguchi, T. Higashi, T. Suzuki, Y. Takashima, Y. Kawabe, O. Cynshi, Y. Wada, M. Honda, H. Kurihara, H. Aburatani, T. Doi, A. Matsumoto, S. Azuma, T. Noda, Y. Toyoda, H. Itakura, Y. Yazaki, and T. Kodama A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection Nature 386 1997 292 296
90. S. Kuchibhotla, D. Vanegas, D.J. Kennedy, E. Guy, G. Nimako, R.E. Morton, and M. Febbraio 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. 78 2008 185 196
91. M.A. Ortiz, G.L. Campana, J.R. Woods, G. Boguslawski, M.J. Sosa, C.L. Walker, and C.A. Labarrere Continuously-infused human C-reactive protein is neither proatherosclerotic nor proinflammatory in apolipoprotein E-deficient mice Exp. Biol. Med. (Maywood) 234 2009 624 631
92. G.A. Tennent, W.L. Hutchinson, M.C. Kahan, G.M. Hirschfield, J.R. Gallimore, J. Lewin, C.A. Sabin, A.P. Dhillon, and M.B. Pepys Transgenic human CRP is not pro-atherogenic, pro-atherothrombotic or pro-inflammatory in apoE-/- mice Atherosclerosis 196 2008 248 255
93. S.B. Schwedler, K. Amann, K. Wernicke, A. Krebs, M. Nauck, C. Wanner, L.A. Potempa, and J. Galle Native C-reactive protein increases whereas modified C-reactive protein reduces atherosclerosis in apolipoprotein E-knockout mice Circulation 112 2005 1016 1023
94. A. Trion, M.P. de Maat, J.W. Jukema, A. van der Laarse, M.C. Maas, E.H. Offerman, L.M. Havekes, A.J. Szalai, H.M. Princen, and J.J. Emeis No effect of C-reactive protein on early atherosclerosis development in apolipoprotein E*3-leiden/human C-reactive protein transgenic mice Arterioscler. Thromb. Vasc. Biol. 25 2005 1635 1640
95. K. Reifenberg, H.A. Lehr, D. Baskal, E. Wiese, S.C. Schaefer, S. Black, D. Samols, M. Torzewski, K.J. Lackner, M. Husmann, M. Blettner, and S. Bhakdi Role of C-reactive protein in atherogenesis: can the apolipoprotein E knockout mouse provide the answer? Arterioscler. Thromb. Vasc. Biol. 25 2005 1641 1646
96. G.M. Hirschfield, J.R. Gallimore, M.C. Kahan, W.L. Hutchinson, C.A. Sabin, G.M. Benson, A.P. Dhillon, G.A. Tennent, and M.B. Pepys Transgenic human C-reactive protein is not proatherogenic in apolipoprotein E-deficient mice Proc. Natl. Acad. Sci. U. S. A. 102 2005 8309 8314
97. R. Oksjoki, H. Jarva, P.T. Kovanen, P. Laine, S. Meri, and M.O. Pentikainen Association between complement factor H and proteoglycans in early human coronary atherosclerotic lesions: implications for local regulation of complement activation Arterioscler. Thromb. Vasc. Biol. 23 2003 630 636
98. P.S. Seifert, and G.K. Hansson Complement receptors and regulatory proteins in human atherosclerotic lesions Arteriosclerosis 9 1989 802 811
99. I. Kardys, C.C. Klaver, D.D. Despriet, A.A. Bergen, A.G. Uitterlinden, A. Hofman, B.A. Oostra, C.M. Van Duijn, P.T. de Jong, and J.C. Witteman A common polymorphism in the complement factor H gene is associated with increased risk of myocardial infarction: the Rotterdam Study J. Am. Coll. Cardiol. 47 2006 1568 1575
100. S.V. Goverdhan, A.J. Lotery, A.J. Cree, and S. Ye Complement factor H Y402H gene polymorphism in coronary artery disease and atherosclerosis Atherosclerosis 188 2006 213 214
101. R.Y. Zee, K.A. Diehl, and P.M. Ridker Complement factor H Y402H gene polymorphism, C-reactive protein, and risk of incident myocardial infarction, ischaemic stroke, and venous thromboembolism: a nested case-control study Atherosclerosis 187 2006 332 335
102. E. Giannakis, T.S. Jokiranta, D.A. Male, S. Ranganathan, R.J. Ormsby, V.A. Fischetti, C. Mold, and D.L. Gordon A common site within factor H SCR 7 responsible for binding heparin, C-reactive protein and streptococcal M protein Eur. J. Immunol. 33 2003 962 969
103. K.A. Volcik, C.M. Ballantyne, M.C. Braun, J. Coresh, T.H. Mosley, and E. Boerwinkle Association of the complement factor H Y402H polymorphism with cardiovascular disease is dependent upon hypertension status: the ARIC study Am. J. Hypertens. 21 2008 533 538
104. R. Sofat, J.P. Casas, M. Kumari, P.J. Talmud, H. Ireland, M. Kivimaki, M. Marmot, A.D. Hughes, S. Thom, S. Ebrahim, J.C. Whittaker, L. Smeeth, D.A. Lawlor, S.E. Humphries, and A.D. Hingorani Genetic variation in complement factor H and risk of coronary heart disease: eight new studies and a meta-analysis of around 48,000 individuals Atherosclerosis 213 2010 184 190
105. M.J. Lewis, T.H. Malik, M.R. Ehrenstein, J.J. Boyle, M. Botto, and D.O. Haskard Immunoglobulin M is required for protection against atherosclerosis in low-density lipoprotein receptor-deficient mice Circulation 120 2009 417 426
106. T. Kyaw, C. Tay, S. Krishnamurthi, P. Kanellakis, A. Agrotis, P. Tipping, A. Bobik, and B.H. Toh B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions Circ. Res. 109 2011 830 840
107. C.A. Ogden, R. Kowalewski, Y. Peng, V. Montenegro, and K.B. Elkon IGM is required for efficient complement mediated phagocytosis of apoptotic cells in vivo Autoimmunity 38 2005 259 264
108. J. Huber, A. Vales, G. Mitulovic, M. Blumer, R. Schmid, J.L. Witztum, B.R. Binder, and N. Leitinger Oxidized membrane vesicles and blebs from apoptotic cells contain biologically active oxidized phospholipids that induce monocyte-endothelial interactions Arterioscler. Thromb. Vasc. Biol. 22 2002 101 107
109. M.K. Chang, C.J. Binder, Y.I. Miller, G. Subbanagounder, G.J. Silverman, J.A. Berliner, and J.L. Witztum Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory J. Exp. Med. 200 2004 1359 1370
110. C.J. Binder, S. Horkko, A. Dewan, M.K. Chang, E.P. Kieu, C.S. Goodyear, P.X. Shaw, W. Palinski, J.L. Witztum, and G.J. Silverman Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL Nat. Med. 9 2003 736 743
111. J.R. Faria-Neto, K.Y. Chyu, X. Li, P.C. Dimayuga, C. Ferreira, J. Yano, B. Cercek, and P.K. Shah Passive immunization with monoclonal IgM antibodies against phosphorylcholine reduces accelerated vein graft atherosclerosis in apolipoprotein E-null mice Atherosclerosis 189 2006 83 90
112. D. Pascolini, S.P. Mariotti, G.P. Pokharel, R. Pararajasegaram, D. Etya'ale, A.D. Negrel, and S. Resnikoff global update of available data on visual impairment: a compilation of population-based prevalence studies Ophthalmic Epidemiol. 11 2004 2002 67 115
113. N. Congdon, B. O'Colmain, C.C. Klaver, R. Klein, B. Munoz, D.S. Friedman, J. Kempen, H.R. Taylor, and P. Mitchell Causes and prevalence of visual impairment among adults in the United States Arch. Ophthalmol. 122 2004 477 485
114. J.G. Hollyfield, V.L. Bonilha, M.E. Rayborn, X. Yang, K.G. Shadrach, L. Lu, R.L. Ufret, R.G. Salomon, and V.L. Perez Oxidative damage-induced inflammation initiates age-related macular degeneration Nat. Med. 14 2008 194 198
115. M. Suzuki, M. Kamei, H. Itabe, K. Yoneda, H. Bando, N. Kume, and Y. Tano Oxidized phospholipids in the macula increase with age and in eyes with age-related macular degeneration Mol. Vis. 13 2007 772 778
116. M. Sun, S.C. Finnemann, M. Febbraio, L. Shan, S.P. Annangudi, E.A. Podrez, G. Hoppe, R. Darrow, D.T. Organisciak, R.G. Salomon, R.L. Silverstein, and S.L. Hazen Light-induced oxidation of photoreceptor outer segment phospholipids generates ligands for CD36-mediated phagocytosis by retinal pigment epithelium: a potential mechanism for modulating outer segment phagocytosis under oxidant stress conditions J. Biol. Chem. 281 2006 4222 4230
117. F. Schutt, M. Bergmann, F.G. Holz, and J. Kopitz Proteins modified by malondialdehyde, 4-hydroxynonenal, or advanced glycation end products in lipofuscin of human retinal pigment epithelium Invest. Ophthalmol. Vis. Sci. 44 2003 3663 3668
118. Q. Ebrahem, K. Renganathan, J. Sears, A. Vasanji, X. Gu, L. Lu, R.G. Salomon, J.W. Crabb, and B. Anand-Apte Carboxyethylpyrrole oxidative protein modifications stimulate neovascularization: implications for age-related macular degeneration Proc. Natl. Acad. Sci. U. S. A. 103 2006 13480 13484
119. J.L. Haines, M.A. Hauser, S. Schmidt, W.K. Scott, L.M. Olson, P. Gallins, K.L. Spencer, S.Y. Kwan, M. Noureddine, J.R. Gilbert, N. Schnetz-Boutaud, A. Agarwal, E.A. Postel, and M.A. Pericak-Vance Complement factor H variant increases the risk of age-related macular degeneration Science 308 2005 419 421
120. G.S. Hageman, D.H. Anderson, L.V. Johnson, L.S. Hancox, A.J. Taiber, L.I. Hardisty, J.L. Hageman, H.A. Stockman, J.D. Borchardt, K.M. Gehrs, R.J. Smith, G. Silvestri, S.R. Russell, C.C. Klaver, I. Barbazetto, S. Chang, L.A. Yannuzzi, G.R. Barile, J.C. Merriam, R.T. Smith, A.K. Olsh, J. Bergeron, J. Zernant, J.E. Merriam, B. Gold, M. Dean, and R. Allikmets A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration Proc. Natl. Acad. Sci. U. S. A. 102 2005 7227 7232
121. A.O. Edwards, R. Ritter III, K.J. Abel, A. Manning, C. Panhuysen, and L.A. Farrer Complement factor H polymorphism and age-related macular degeneration Science 308 2005 421 424
122. R.J. Klein, C. Zeiss, E.Y. Chew, J.Y. Tsai, R.S. Sackler, C. Haynes, A.K. Henning, J.P. SanGiovanni, S.M. Mane, S.T. Mayne, M.B. Bracken, F.L. Ferris, J. Ott, C. Barnstable, and J. Hoh Complement factor H polymorphism in age-related macular degeneration Science 308 2005 385 389
123. A. Thakkinstian, P. Han, M. McEvoy, W. Smith, J. Hoh, K. Magnusson, K. Zhang, and J. Attia Systematic review and meta-analysis of the association between complement factor H Y402H polymorphisms and age-related macular degeneration Hum. Mol. Genet. 15 2006 2784 2790
124. L.A. Donoso, T. Vrabec, and H. Kuivaniemi The role of complement Factor H in age-related macular degeneration: a review Surv. Ophthalmol. 55 2010 227 246