Oxidation-specific epitopes are major targets of innate immunity in atherothrombosis

Hamostaseologie

Volumn 36, Issue 2, 2016, Pages 89-96

  Gritti, Barbara Bartolini ^a   Binder, Christoph J ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Atherothrombosis; Innate immunity; Natural IgM antibodies; Oxidized LDL

Indexed keywords

EPITOPE; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M ANTIBODY; LIPOPROTEIN; MEMBRANE LIPID; OXIDIZED LOW DENSITY LIPOPROTEIN; PATTERN RECOGNITION RECEPTOR; CYTOKINE; IMMUNOLOGIC FACTOR; REACTIVE OXYGEN METABOLITE;

ATHEROSCLEROSIS; CARDIOVASCULAR RISK; HEART INFARCTION; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; INNATE IMMUNITY; MEMBRANE MICROPARTICLE; NONHUMAN; OXIDATION; OXIDATIVE STRESS; REVIEW; THROMBOSIS; ANIMAL; ARTERY; BIOLOGICAL MODEL; EVIDENCE BASED MEDICINE; IMMUNOLOGY; LIPID METABOLISM; PATHOLOGY;

ANIMALS; ARTERIES; ATHEROSCLEROSIS; CYTOKINES; EPITOPES; EVIDENCE-BASED MEDICINE; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC FACTORS; LIPID METABOLISM; MODELS, IMMUNOLOGICAL; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84971006571     PISSN: 07209355     EISSN: None     Source Type: Journal    
DOI: 10.5482/HAMO-14-11-0069     Document Type: Review

References (62)

1. Libby P, Lichtman AH, Hansson GK. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity 2013; 38: 1092-1104.
2. Lee RT, Libby P. The unstable atheroma. Arterioscler Thromb Vasc Biol 1997; 17: 1859-1867.
3. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 2006; 6: 508-519.
4. Ruggeri ZM. Platelets in atherothrombosis. Nat Med 2002; 8: 1227-1234.
5. Rautou PE, Vion AC, Amabile N et al. Microparticles, vascular function, and atherothrombosis. Circ Res 2011; 109: 593-606.
6. Badimon L, Storey RF, Vilahur G. Update on lipids, inflammation and atherothrombosis. Thromb Haemost 2011; 105 (Suppl 1): S34-S42.
7. Nakashima Y, Fujii H, Sumiyoshi S et al. Early human atherosclerosis: accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration. Arterioscler Thromb Vasc Biol 2007; 27: 1159-1165.
8. Steinberg D, Witztum JL. Oxidized low-density lipoprotein and atherosclerosis. Arterioscler Thromb Vasc Biol 2010; 30: 2311-2316.
9. Younis N, Sharma R, Soran H et al. Glycation as an atherogenic modification of LDL. Curr Opin Lipidol 2008; 19: 378-384.
10. Oorni K, Pentikainen MO, Ala-Korpela M, Kovanen PT. Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions. J Lipid Res 2000; 41: 1703-1714.
11. Weismann D, Binder CJ. The innate immune response to products of phospholipid peroxidation. Biochim Biophys Acta 2012; 1818: 2465-2475.
12. Miller YI, Choi SH, Wiesner P et al. Oxidationspecific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ Res 2011; 108: 235-248.
13. Moore KJ, Freeman MW. Scavenger receptors in atherosclerosis: beyond lipid uptake. Arterioscler Thromb Vasc Biol 2006; 26: 1702-1711.
14. Randolph GJ. Mechanisms that regulate macrophage burden in atherosclerosis. Circ Res 2014; 114: 1757-1771.
15. Canton J, Neculai D, Grinstein S. Scavenger receptors in homeostasis and immunity. Nat Rev Immunol 2013; 13: 621-634.
16. Tabas I, Williams KJ, Boren J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 2007; 116: 1832-1844.
17. Dei R, Takeda A, Niwa H et al. Lipid peroxidation and advanced glycation end products in the brain in normal aging and in Alzheimer's disease. Acta Neuropathol 2002; 104: 113-122.
18. Imai Y, Kuba K, Neely GG et al. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 2008; 133: 235-249.
19. Palinski W, Horkko S, Miller E 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 1996; 98: 800-814.
20. Weismann D, Hartvigsen K, Lauer N et al. Complement factor H binds malondialdehyde epitopes and protects from oxidative stress. Nature 2011; 478: 76-81.
21. Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol 2001; 1: 135-145.
22. Stewart CR, Stuart LM, Wilkinson K et al. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 2010; 11: 155-161.
23. Duewell P, Kono H, Rayner KJ et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010; 464: 1357-1361.
24. Chang MK, Bergmark C, Laurila A 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 1999; 96: 6353-6358.
25. Boisvert WA, Santiago R, Curtiss LK, Terkeltaub RA. A leukocyte homologue of the IL-8 receptor CXCR-2 mediates the accumulation of macrophages in atherosclerotic lesions of LDL receptordeficient mice. J Clin Invest 1998; 101: 353-363.
26. Chou MY, Fogelstrand L, Hartvigsen K et al. Oxidation- specific epitopes are dominant targets of innate natural antibodies in mice and humans. J Clin Invest 2009; 119: 1335-1349.
27. Ehrenstein MR, Notley CA. The importance of natural IgM: scavenger, protector and regulator. Nat Rev Immunol 2010; 10: 778-786.
28. Baumgarth N. The double life of a B-1 cell: selfreactivity selects for protective effector functions. Nat Rev Immunol 2011; 11: 34-46.
29. Griffin DO, Holodick NE, Rothstein TL. Human B1 cells are CD3-: A reply to "A human equivalent of mouse B-1 cells?" and "The nature of circulating CD27+CD43+ B cells". J Exp Med 2011; 208: 2566-2569.
30. Bochkov VN, Oskolkova OV, Birukov KG et al. Generation and biological activities of oxidized phospholipids. Antioxid Redox Signal 2010; 12: 1009-1059.
31. Lee S, Birukov KG, Romanoski CE et al. Role of phospholipid oxidation products in atherosclerosis. Circ Res 2012; 111: 778-799.
32. Annex BH, Denning SM, Channon KM et al. Differential expression of tissue factor protein in directional atherectomy specimens from patients with stable and unstable coronary syndromes. Circulation 1995; 91: 619-622.
33. Wilcox JN, Smith KM, Schwartz SM, Gordon D. Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque. Proc Natl Acad Sci USA 1989; 86: 2839-2843.
34. Pawlinski R, Wang JG, Owens AP et al. Hematopoietic and nonhematopoietic cell tissue factor activates the coagulation cascade in endotoxemic mice. Blood 2010; 116: 806-814.
35. Ferro D, Basili S, Alessandri C et al. Simvastatin reduces monocyte-tissue-factor expression type IIa hypercholesterolaemia. Lancet 1997;3 50: 1222.
36. Owens AP 3rd, Mackman N. Sources of tissue factor that contribute to thrombosis after rupture of an atherosclerotic plaque. Thromb Res 2012; 129 (Suppl 2): S30-S33.
37. Mallat Z, Hugel B, Ohan J et al. Shed membrane microparticles with procoagulant potential in human atherosclerotic plaques: a role for apoptosis in plaque thrombogenicity. Circulation 1999; 99: 348-353.
38. rd, Passam FH, Antoniak S et al. Monocyte tissue factor-dependent activation of coagulation in hypercholesterolemic mice and monkeys is inhibited by simvastatin. J Clin Invest 2012; 122: 558-568.
39. Ravandi A, Leibundgut G, Hung MY et al. Release and capture of bioactive oxidized phospholipids and oxidized cholesteryl esters during percutaneous coronary and peripheral arterial interventions in humans. J Am Coll Cardiol 2014; 63: 1961-1971.
40. Tsimikas S, Brilakis ES, Miller ER et al. Oxidized phospholipids, Lp(a) lipoprotein, and coronary artery disease. N Engl J Med 2005; 353: 46-57.
41. Podrez EA, Byzova TV, Febbraio M et al. Platelet CD36 links hyperlipidemia, oxidant stress and a prothrombotic phenotype. Nat Med 2007; 13: 1086-1095.
42. Morel O, Morel N, Jesel L et al. Microparticles: a critical component in the nexus between inflammation, immunity, and thrombosis. Semin Immunopathol 2011; 33: 469-486.
43. Leroyer AS, Isobe H, Leseche G, Castier Y, Wassef M, Mallat Z, et al. Cellular origins and thrombogenic activity of microparticles isolated from human atherosclerotic plaques. J Am Coll Cardiol 2007; 49: 772-777.
44. Barry OP, Pratico D, Lawson JA, FitzGerald GA. Transcellular activation of platelets and endothelial cells by bioactive lipids in platelet microparticles. J Clin Invest 1997; 99: 2118-2127.
45. Huber J, Vales A, Mitulovic G et al. Oxidized membrane vesicles and blebs from apoptotic cells contain biologically active oxidized phospholipids that induce monocyte-endothelial interactions. Arterioscler Thromb Vasc Biol 2002; 22: 101-107.
46. Chang MK, Binder CJ, Miller YI et al. Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory. J Exp Med 2004; 200: 1359-1370.
47. Tsiantoulas D, Perkmann T, Afonyushkin T et al. Circulating microparticles carry oxidation-specific epitopes and are recognized by natural IgM antibodies. J Lipid Res 2015; 56: 440-448.
48. Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med 1999; 340: 115-126.
49. Lichtman AH, Binder CJ, Tsimikas S, Witztum JL. Adaptive immunity in atherogenesis: new insights and therapeutic approaches. J Clin Invest 2013; 123: 27-36.
50. Stemme S, Faber B, Holm J et al. T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc Natl Acad Sci USA 1995; 92: 3893-3897.
51. Tsiantoulas D, Diehl CJ, Witztum JL, Binder CJ. B cells and humoral immunity in atherosclerosis. Circ Res 2014; 114: 1743-1756.
52. Boullier A, Gillotte KL, Horkko S 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 2000; 275: 9163-9169.
53. Horkko S, Bird DA, Miller E et al. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J Clin Invest 1999; 103: 117-128.
54. Chen Y, Park YB, Patel E, Silverman GJ. IgM antibodies to apoptosis-associated determinants recruit C1q and enhance dendritic cell phagocytosis of apoptotic cells. J Immunol 2009; 182: 6031-6043.
55. Binder CJ, Horkko S, Dewan A et al. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat Med 2003; 9: 736-743.
56. Faria-Neto JR, Chyu KY, Li X et al. Passive immunization with monoclonal IgM antibodies against phosphorylcholine reduces accelerated vein graft atherosclerosis in apolipoprotein E-null mice. Atherosclerosis 2006; 189: 83-90.
57. Puurunen M, Manttari M, Manninen V et al. Antibody against oxidized low-density lipoprotein predicting myocardial infarction. Arch Intern Med 1994; 154: 2605-2609.
58. Ahmed E, Trifunovic J, Stegmayr B et al. Autoantibodies against oxidatively modified LDL do not constitute a risk factor for stroke: a nested casecontrol study. Stroke 1999; 30: 2541-2546.
59. Tsimikas S, Brilakis ES, Lennon RJ et al. Relationship of IgG and IgM autoantibodies to oxidized low density lipoprotein with coronary artery disease and cardiovascular events. J Lipid Res 2007; 48: 425-433.
60. Sjoberg BG, Su J, Dahlbom I et al. Low levels of IgM antibodies against phosphorylcholine-A potential risk marker for ischemic stroke in men. Atherosclerosis 2009; 203: 528-532.
61. Gronlund H, Hallmans G, Jansson JH et al. Low levels of IgM antibodies against phosphorylcholine predict development of acute myocardial infarction in a population-based cohort from northern Sweden. Eur J Cardiovasc Prev Rehabil 2009; 16: 382-386.
62. Tsimikas S, Willeit P, Willeit J et al. Oxidation-specific biomarkers, prospective 15-year cardiovascular and stroke outcomes, and net reclassification of cardiovascular events. J Am Coll Cardiol 2012; 60: 2218-2229.