Oxidation-specific epitopes and immunological responses: Translational biotheranostic implications for atherosclerosis

Current Opinion in Pharmacology

Volumn 13, Issue 2, 2013, Pages 168-179

  Leibundgut, Gregor ^a   Witztum, Joseph L ^a   Tsimikas, Sotirios ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; APOLIPOPROTEIN B; BI 204; BIOLOGICAL MARKER; C REACTIVE PROTEIN; CHOLESTEROL; COMPLEMENT FACTOR H; EPITOPE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M ANTIBODY; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; LIPOPROTEIN A; LOW DENSITY LIPOPROTEIN; MALONALDEHYDE; MLDL 1278A; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY BI204; MONOCLONAL ANTIBODY IK17; OXIDIZED LOW DENSITY LIPOPROTEIN; PATTERN RECOGNITION RECEPTOR; PHOSPHOLIPID; PLACEBO; PLASMINOGEN; SCAVENGER RECEPTOR; SELECTIN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ADAPTIVE IMMUNITY; APOPTOSIS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; B LYMPHOCYTE; BLOOD VESSEL WALL; CARDIOVASCULAR RISK; CEREBROVASCULAR ACCIDENT; CHRONIC INFLAMMATION; DENDRITIC CELL; DRUG TARGETING; ENDOTHELIAL DYSFUNCTION; FIBRINOLYSIS; HEART INFARCTION; HUMAN; HYPERCHOLESTEROLEMIA; IMMUNE RESPONSE; IMMUNOTHERAPY; INNATE IMMUNITY; MACROPHAGE; MOLECULAR IMAGING; MONOCYTE; MORTALITY; MULTICENTER STUDY (TOPIC); NON INVASIVE MEASUREMENT; NONHUMAN; OXIDATION; PASSIVE IMMUNIZATION; PERCUTANEOUS CORONARY INTERVENTION; PHASE 2 CLINICAL TRIAL (TOPIC); PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; RANDOMIZED CONTROLLED TRIAL (TOPIC); T LYMPHOCYTE; VASCULAR ENDOTHELIUM; VIRAL GENE DELIVERY SYSTEM;

EID: 84879410282     PISSN: 14714892     EISSN: 14714973     Source Type: Journal    
DOI: 10.1016/j.coph.2013.02.005     Document Type: Review

References (72)

1. A.H. Lichtman, C.J. Binder, S. Tsimikas, and J.L. Witztum Adaptive immunity in atherogenesis: new insights and therapeutic approaches J Clin Invest 123 2013 27 36
2. K.J. Moore, and I. Tabas Macrophages in the pathogenesis of atherosclerosis Cell 145 2011 341 355
3. R.R.S. Packard, A.H. Lichtman, and P. Libby Innate and adaptive immunity in atherosclerosis Semin Immunopathol 31 2009 5 22
4. G.K. Hansson, and A. Hermansson The immune system in atherosclerosis Nat Immunol 12 2011 204 212
5. Y.I. Miller, S.-H. Choi, P. Wiesner, L. Fang, R. Harkewicz, K. Hartvigsen, A. Boullier, A. Gonen, C.J. Diehl, and X. Que Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity Circ Res 108 2011 235 248
6. P. Libby, P.M. Ridker, and G.K. Hansson Progress and challenges in translating the biology of atherosclerosis Nature 473 2011 317 325
7. S. Taleb, A. Tedgui, and Z. Mallat Adaptive T cell immune responses and atherogenesis Curr Opin Pharmacol 10 2010 197 202
8. I. Tabas, K.J. Williams, and J. Borén Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications Circulation 116 2007 1832 1844 (Pubitemid 350287108)
9. D. Steinberg, and J.L. Witztum Oxidized low-density lipoprotein and atherosclerosis Arterioscler Thromb Vasc Biol 30 2010 2311 2316
10. P. Libby Counterregulation rules in atherothrombosis J Am Coll Cardiol 59 2012 1438 1440
11. R.A. van Dijk, F. Kolodgie, A. Ravandi, G. Leibundgut, P.P. Hu, A. Prasad, E. Mahmud, E. Dennis, L.K. Curtiss, and J.L. Witztum Differential expression of oxidation-specific epitopes and apolipoprotein(a) in progressing and ruptured human coronary and carotid atherosclerotic lesions J Lipid Res 53 2012 2773 2790
12. S. Lee, K.G. Birukov, C.E. Romanoski, J.R. Springstead, A.J. Lusis, and J.A. Berliner Role of phospholipid oxidation products in atherosclerosis Circ Res 111 2012 778 799
13. K. Hartvigsen, M.-Y. Chou, L.F. Hansen, P.X. Shaw, S. Tsimikas, C.J. Binder, and J.L. Witztum The role of innate immunity in atherogenesis J Lipid Res 50 Suppl 2009 S388 S393
14. O. Quehenberger Thematic review series: the immune system and atherogenesis. Molecular mechanisms regulating monocyte recruitment in atherosclerosis J Lipid Res 46 2005 1582 1590 (Pubitemid 41099324)
15. Z.-Q. Yan, and G.K. Hansson Innate immunity, macrophage activation, and atherosclerosis Immunol Rev 219 2007 187 203 (Pubitemid 47390007)
16. E. Thorp, M. Subramanian, and I. Tabas The role of macrophages and dendritic cells in the clearance of apoptotic cells in advanced atherosclerosis Eur J Immunol 41 2011 2515 2518
17. I. Tabas Macrophage death and defective inflammation resolution in atherosclerosis Nat Rev Immunol 10 2010 36 46
18. N.J. Spann, L.X. Garmire, J.G. McDonald, D.S. Myers, S.B. Milne, N. Shibata, D. Reichart, J.N. Fox, I. Shaked, and D. Heudobler Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses Cell 151 2012 138 152
19. A. Plüddemann, C. Neyen, and S. Gordon Macrophage scavenger receptors and host-derived ligands Methods 43 2007 207 217 (Pubitemid 47499075)
20. J.L. Witztum You are right too! J Clin Invest 115 2005 2072 2075 (Pubitemid 41134146)
21. 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 (Pubitemid 41134161)
22. C. Erridge The roles of toll-like receptors in atherosclerosis J Innate Immun 1 2009 340 349
23. L.K. Curtiss, and P.S. Tobias Emerging role of Toll-like receptors in atherosclerosis J Lipid Res 50 Suppl 2009 S340 S345
24. A.E. Mullick, P.S. Tobias, and L.K. Curtiss Modulation of atherosclerosis in mice by Toll-like receptor 2 J Clin Invest 115 2005 3149 3156 (Pubitemid 41567579)
25. L.K. Curtiss, A.S. Black, D.J. Bonnet, and P.S. Tobias Atherosclerosis induced by endogenous and exogenous toll-like receptor (TLR)1 or TLR6 agonists J Lipid Res 53 2012 2126 2132
26. A. Kadl, A.K. Meher, P.R. Sharma, M.Y. Lee, A.C. Doran, S.R. Johnstone, M.R. Elliott, F. Gruber, J. Han, and W. Chen Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2 Circ Res 107 2010 737 746
27. A. Kadl, P.R. Sharma, W. Chen, R. Agrawal, A.K. Meher, S. Rudraiah, N. Grubbs, R. Sharma, and N. Leitinger Oxidized phospholipid-induced inflammation is mediated by Toll-like receptor 2 Free Radic Biol Med 51 2011 1903 1909
28. K.S. Michelsen, M.H. Wong, P.K. Shah, W. Zhang, J. Yano, T.M. Doherty, S. Akira, T.B. Rajavashisth, and M. Arditi Lack of Toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E Proc Natl Acad Sci USA 101 2004 10679 10684 (Pubitemid 38955802)
29. H. Björkbacka, V.V. Kunjathoor, K.J. Moore, S. Koehn, C.M. Ordija, M.A. Lee, T. Means, K. Halmen, A.D. Luster, and D.T. Golenbock Reduced atherosclerosis in MyD88-null mice links elevated serum cholesterol levels to activation of innate immunity signaling pathways Nat Med 10 2004 416 421 (Pubitemid 38508522)
30. M.K. Piya, A.L. Harte, and P.G. McTernan Metabolic endotoxaemia: is it more than just a gut feeling? Curr Opin Lipidol 24 2013 78 85
31. Y.I. Miller, S. Viriyakosol, D.S. Worrall, A. Boullier, S. Butler, and J.L. Witztum Toll-like receptor 4-dependent and -independent cytokine secretion induced by minimally oxidized low-density lipoprotein in macrophages Arterioscler Thromb Vasc Biol 25 2005 1213 1219 (Pubitemid 40776611)
32. S.-H. Choi, R. Harkewicz, J.H. Lee, A. Boullier, F. Almazan, A.C. Li, J.L. Witztum, Y.S. Bae, and Y.I. Miller Lipoprotein accumulation in macrophages via toll-like receptor-4-dependent fluid phase uptake Circ Res 104 2009 1355 1363
33. P. Wiesner, S.-H. Choi, F. Almazan, C. Benner, W. Huang, C.J. Diehl, A. Gonen, S. Butler, J.L. Witztum, and C.K. Glass Low doses of lipopolysaccharide and minimally oxidized low-density lipoprotein cooperatively activate macrophages via nuclear factor kappa B and activator protein-1: possible mechanism for acceleration of atherosclerosis by subclinical endotoxemia Circ Res 107 2010 56 65
34. D. Weismann, K. Hartvigsen, N. Lauer, K.L. Bennett, H.P.N. Scholl, P. Charbel Issa, M. Cano, H. Brandstätter, S. Tsimikas, and C. Skerka Complement factor H binds malondialdehyde epitopes and protects from oxidative stress Nature 478 2011 76 81
35. R. Oksjoki, H. Jarva, P.T. Kovanen, P. Laine, S. Meri, and M.O. Pentikäinen 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 (Pubitemid 36438076)
36. 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
37. M.-Y. Chou, L. Fogelstrand, K. Hartvigsen, L.F. Hansen, D. Woelkers, P.X. Shaw, J. Choi, T. Perkmann, F. Bäckhed, and Y.I. Miller Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans J Clin Invest 119 2009 1335 1349
38. 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 (Pubitemid 36749223)
39. 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
40. C.K. Glass, and J.L. Witztum Atherosclerosis. The road ahead Cell 104 2001 503 516
41. C. Bergmark, A. Dewan, A. Orsoni, E. Merki, E.R. Miller, M.-J. Shin, C.J. Binder, S. Horkko, R.M. Krauss, and M.J. Chapman A novel function of lipoprotein [a] as a preferential carrier of oxidized phospholipids in human plasma J Lipid Res 49 2008 2230 2239
42. B.G. Nordestgaard, M.J. Chapman, K. Ray, J. Borén, F. Andreotti, G.F. Watts, H. Ginsberg, P. Amarenco, A. Catapano, and O.S. Descamps Lipoprotein(a) as a cardiovascular risk factor: current status Eur Heart J 31 2010 2844 2853
43. B. Kolski, and S. Tsimikas Emerging therapeutic agents to lower lipoprotein (a) levels Curr Opin Lipidol 23 2012 560 568
44. A. Taleb, J.L. Witztum, and S. Tsimikas Oxidized phospholipids on apoB-100-containing lipoproteins: a biomarker predicting cardiovascular disease and cardiovascular events Biomark Med 5 2011 673 694
45. S. Tsimikas, P. Willeit, J. Willeit, P. Santer, M. Mayr, Q. Xu, A. Mayr, J.L. Witztum, and S. Kiechl Oxidation-specific biomarkers, prospective 15-year cardiovascular and stroke outcomes, and net reclassification of cardiovascular events J Am Coll Cardiol 60 2012 2218 2229
46. G. Leibundgut, K. Arai, A. Orsoni, H. Yin, C. Scipione, E.R. Miller, M.L. Koschinsky, M.J. Chapman, J.L. Witztum, and S. Tsimikas Oxidized phospholipids are present on plasminogen, affect fibrinolysis, and increase following acute myocardial infarction J Am Coll Cardiol 59 2012 1426 1437
47. K.C. Briley-Saebo, Y.S. Cho, P.X. Shaw, S.K. Ryu, V. Mani, S. Dickson, E. Izadmehr, S. Green, Z.A. Fayad, and S. Tsimikas Targeted iron oxide particles for in vivo magnetic resonance detection of atherosclerotic lesions with antibodies directed to oxidation-specific epitopes J Am Coll Cardiol 57 2011 337 347
48. K.C. Briley-Saebo, Y.S. Cho, and S. Tsimikas Imaging of oxidation-specific epitopes in atherosclerosis and macrophage-rich vulnerable plaques Curr Cardiovasc Imaging Rep 4 2011 4 16
49. K.C. Briley-Saebo, T.H. Nguyen, A.M. Saeboe, Y.S. Cho, S.K. Ryu, E. Volkava, S. Dickson, G. Leibundgut, P. Weisner, and S. Green In vivo detection of oxidation-specific epitopes in atherosclerotic lesions using biocompatible manganese molecular magnetic imaging probes J Am Coll Cardiol 59 2012 616 626
50. S. Amir, and C.J. Binder Experimental immunotherapeutic approaches for atherosclerosis Clin Immunol 134 2010 66 79
51. C.J. Binder, K. Hartvigsen, M.-K. Chang, M. Miller, D. Broide, W. Palinski, L.K. Curtiss, M. Corr, and J.L. Witztum IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis J Clin Invest 114 2004 427 437 (Pubitemid 39071615)
52. 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
53. A. Ravandi, S.M. Boekholdt, Z. Mallat, P.J. Talmud, J.J.P. Kastelein, N.J. Wareham, E.R. Miller, J. Benessiano, A. Tedgui, and J.L. Witztum Relationship of IgG and IgM autoantibodies and immune complexes to oxidized LDL with markers of oxidation and inflammation and cardiovascular events: results from the EPIC-Norfolk Study J Lipid Res 52 2011 1829 1836
54. 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 (Pubitemid 44468069)
55. A. Schiopu, J. Bengtsson, I. Söderberg, S. Janciauskiene, S. Lindgren, M.P.S. Ares, P.K. Shah, R. Carlsson, J. Nilsson, and G.N. Fredrikson Recombinant human antibodies against aldehyde-modified apolipoprotein B-100 peptide sequences inhibit atherosclerosis Circulation 110 2004 2047 2052 (Pubitemid 39331920)
56. A. Schiopu, B. Frendéus, B. Jansson, I. Söderberg, I. Ljungcrantz, Z. Araya, P.K. Shah, R. Carlsson, J. Nilsson, and G.N. Fredrikson Recombinant antibodies to an oxidized low-density lipoprotein epitope induce rapid regression of atherosclerosis in apobec-1(-/-)/low-density lipoprotein receptor(-/-) mice J Am Coll Cardiol 50 2007 2313 2318 (Pubitemid 350199611)
57. A. Ström, G.N. Fredrikson, A. Schiopu, I. Ljungcrantz, I. Söderberg, B. Jansson, R. Carlsson, A. Hultgårdh-Nilsson, and J. Nilsson Inhibition of injury-induced arterial remodelling and carotid atherosclerosis by recombinant human antibodies against aldehyde-modified apoB-100 Atherosclerosis 190 2007 298 305 (Pubitemid 46074045)
58. P.X. Shaw, S. Hörkkö, S. Tsimikas, M.K. Chang, W. Palinski, G.J. Silverman, P.P. Chen, and J.L. Witztum Human-derived anti-oxidized LDL autoantibody blocks uptake of oxidized LDL by macrophages and localizes to atherosclerotic lesions in vivo Arterioscler Thromb Vasc Biol 21 2001 1333 1339 (Pubitemid 34219841)
59. S. Tsimikas, A. Miyanohara, K. Hartvigsen, E. Merki, P.X. Shaw, M.-Y. Chou, J. Pattison, M. Torzewski, J. Sollors, and T. Friedmann Human oxidation-specific antibodies reduce foam cell formation and atherosclerosis progression J Am Coll Cardiol 58 2011 1715 1727
60. L. Fang, S.R. Green, J.S. Baek, S.-H. Lee, F. Ellett, E. Deer, G.J. Lieschke, J.L. Witztum, S. Tsimikas, and Y.I. Miller In vivo visualization and attenuation of oxidized lipid accumulation in hypercholesterolemic zebrafish J Clin Invest 2011 10.1172/JCI57755
61. W. Palinski, E. Miller, and J.L. Witztum Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis Proc Natl Acad Sci U S A 92 1995 821 825
62. C.J. Binder, P.X. Shaw, M.-K. Chang, A. Boullier, K. Hartvigsen, S. Hörkkö, Y.I. Miller, D.A. Woelkers, M. Corr, and J.L. Witztum The role of natural antibodies in atherogenesis J Lipid Res 46 2005 1353 1363 (Pubitemid 43109798)
63. J. Nilsson, H. Björkbacka, and G.N. Fredrikson Apolipoprotein B100 autoimmunity and atherosclerosis - disease mechanisms and therapeutic potential Curr Opin Lipidol 23 2012 422 428
64. S. Amir, K. Hartvigsen, A. Gonen, G. Leibundgut, X. Que, E. Jensen-Jarolim, O. Wagner, S. Tsimikas, J.L. Witztum, and C.J. Binder Peptide mimotopes of malondialdehyde epitopes for clinical applications in cardiovascular disease J Lipid Res 53 2012 1316 1326
65. A. Hermansson, D.F.J. Ketelhuth, D. Strodthoff, M. Wurm, E.M. Hansson, A. Nicoletti, G. Paulsson-Berne, and G.K. Hansson Inhibition of T cell response to native low-density lipoprotein reduces atherosclerosis J Exp Med 207 2010 1081 1093
66. A. Hermansson, D.K. Johansson, D.F.J. Ketelhuth, J. Andersson, X. Zhou, and G.K. Hansson Immunotherapy with tolerogenic apolipoprotein B-100-loaded dendritic cells attenuates atherosclerosis in hypercholesterolemic mice Circulation 123 2011 1083 1091
67. O. Herbin, H. Ait-Oufella, W. Yu, G.N. Fredrikson, B. Aubier, N. Perez, V. Barateau, J. Nilsson, A. Tedgui, and Z. Mallat Regulatory T-cell response to apolipoprotein B100-derived peptides reduces the development and progression of atherosclerosis in mice Arterioscler Thromb Vasc Biol 32 2012 605 612
68. S. Kiechl, J. Willeit, M. Mayr, B. Viehweider, M. Oberhollenzer, F. Kronenberg, C.J. Wiedermann, S. Oberthaler, Q. Xu, and J.L. Witztum Oxidized phospholipids, lipoprotein(a), lipoprotein-associated phospholipase A2 activity, and 10-year cardiovascular outcomes: prospective results from the Bruneck study Arterioscler Thromb Vasc Biol 27 2007 1788 1795 (Pubitemid 47207175)
69. S. Tsimikas, Z. Mallat, P.J. Talmud, J.J.P. Kastelein, N.J. Wareham, M.S. Sandhu, E.R. Miller, J. Benessiano, A. Tedgui, and J.L. Witztum Oxidation-specific biomarkers, lipoprotein(a), and risk of fatal and nonfatal coronary events J Am Coll Cardiol 56 2010 946 955
70. J.E. Murphy, P.R. Tedbury, S. Homer-Vanniasinkam, J.H. Walker, and S. Ponnambalam Biochemistry and cell biology of mammalian scavenger receptors Atherosclerosis 182 2005 1 15 (Pubitemid 41188365)
71. S.N. Shishido, S. Varahan, K. Yuan, X. Li, and S.D. Fleming Humoral innate immune response and disease Clin Immunol 144 2012 142 158
72. D. Weismann, and C.J. Binder The innate immune response to products of phospholipid peroxidation Cardiovasc Revasc Med 1818 2012 2465 2475