Circulating microparticles carry oxidation-specific epitopes and are recognized by natural IgM antibodies

Journal of Lipid Research

Volumn 56, Issue 2, 2015, Pages 440-448

  Tsiantoulas, Dimitrios ^a,b,c   Perkmann, Thomas ^a   Afonyushkin, Taras ^a,b   Mangold, Andreas ^a   Prohaska, Thomas A ^a,b   Papac Milicevic, Nikolina ^a,b   Millischer, Vincent ^a,b   Bartel, Caroline ^a   Hörkkö, Sohvi ^d   Boulanger, Chantal M ^e   Tsimikas, Sotirios ^f   Fischer, Michael B ^a,c   Witztum, Joseph L ^f   Lang, Irene M ^a   Binder, Christoph J ^a,b,c  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^c INSTITUTE FOR MICROELECTRONICS   (Austria)

^d UNIVERSITY OF OULU   (Finland)

^e PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Acute coronary syndrome; Immunoglobulin M antibodies; Malondialdehyde

Indexed keywords

EPITOPE; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 8; MALONALDEHYDE; OXIDIZED LOW DENSITY LIPOPROTEIN; IMMUNOGLOBULIN M;

ADULT; ANTIBODY COMBINING SITE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY REACTION; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORONARY ARTERY OCCLUSION; CYTOKINE PRODUCTION; FEMALE; FLOW CYTOMETRY; HEART PROTECTION; HUMAN; LEUKEMIA CELL LINE; MALE; MEMBRANE MICROPARTICLE; MONOCYTE; ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; THP 1 CELL LINE; ACUTE CORONARY SYNDROME; IMMUNOLOGY; METABOLISM; OXIDATION REDUCTION REACTION;

ACUTE CORONARY SYNDROME; ADULT; CELL-DERIVED MICROPARTICLES; EPITOPES; FEMALE; HUMANS; IMMUNOGLOBULIN M; MALE; MALONDIALDEHYDE; OXIDATION-REDUCTION;

EID: 84921898247     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.P054569     Document Type: Article

References (40)

1. Libby, P., A. H. Lichtman, and G. K. Hansson . 2013. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity . 38 : 1092-1104.
2. Tsiantoulas, D., C. J. Diehl, J. L. Witztum, and C. J. Binder . 2014. B cells and humoral immunity in atherosclerosis. Circ. Res. 114 : 1743-1756.
3. Karvonen, J., M. Paivansalo, Y. A. Kesaniemi, and S. Horkko . 2003. Immunoglobulin M type of autoantibodies to oxidized low-density lipoprotein has an inverse relation to carotid artery atherosclerosis. Circulation. 108 : 2107-2112.
4. Tsimikas, S., E. S. Brilakis, R. J. Lennon, E. R. Miller, J. L. Witztum, J. P. McConnell, K. S. Kornman, and P. B. Berger . 2007. Relationship of IgG and IgM autoantibodies to oxidized low density lipoprotein with coronary artery disease and cardiovascular events. J. Lipid Res. 48 : 425-433.
5. Fiskesund, R., B. Stegmayr, G. Hallmans, M. Vikstrom, L. Weinehall, U. de Faire, and J. Frostegard . 2010. Low levels of antibodies against phosphorylcholine predict development of stroke in a populationbased study from northern Sweden. Stroke . 41 : 607-612.
6. Grönlund, H., G. Hallmans, J. H. Jansson, K. Boman, M. Wikstrom, U. de Faire, and J. Frostegard . 2009. 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. 16 : 382-386.
7. Tsimikas, S., P. Willeit, J. Willeit, P. Santer, M. Mayr, Q. Xu, A. Mayr, J. L. Witztum, and S. Kiechl . 2012. Oxidation-specifi c biomarkers, prospective 15-year cardiovascular and stroke outcomes, and net reclassifi cation of cardiovascular events. J. Am. Coll. Cardiol. 60 : 2218-2229.
8. Binder, C. J., 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 . 2003. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat. Med. 9 : 736-743.
9. Kyaw, T., C. Tay, S. Krishnamurthi, P. Kanellakis, A. Agrotis, P. Tipping, A. Bobik, and B. H. Toh . 2011. B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions. Circ. Res. 109 : 830-840.
10. Lewis, M. J., T. H. Malik, M. R. Ehrenstein, J. J. Boyle, M. Botto, and D. O. Haskard . 2009. Immunoglobulin M is required for protection against atherosclerosis in low-density lipoprotein receptordefi cient mice. Circulation . 120 : 417-426.
11. Chou, M. Y., L. Fogelstrand, K. Hartvigsen, L. F. Hansen, D. Woelkers, P. X. Shaw, J. Choi, T. Perkmann, F. Backhed, Y. I. Miller, et al. 2009. Oxidation-specifi c epitopes are dominant targets of innate natural antibodies in mice and humans. J. Clin. Invest. 119 : 1335-1349.
12. Imai, Y., K. Kuba, G. G. Neely, R. Yaghubian-Malhami, T. Perkmann, G. van Loo, M. Ermolaeva, R. Veldhuizen, Y. H. Leung, H. Wang, et al. 2008. Identifi cation of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell. 133 : 235-249.
13. Haider, L., M. T. Fischer, J. M. Frischer, J. Bauer, R. Hoftberger, G. Botond, H. Esterbauer, C. J. Binder, J. L. Witztum, and H. Lassmann . 2011. Oxidative damage in multiple sclerosis lesions. Brain . 134 : 1914-1924.
14. Chang, M. K., C. Bergmark, A. Laurila, S. Horkko, K. H. Han, P. Friedman, E. A. Dennis, and J. L. Witztum . 1999. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specifi c epitopes mediate macrophage recognition. Proc. Natl. Acad. Sci. USA . 96 : 6353-6358.
15. Chang, M. K., C. J. Binder, Y. I. Miller, G. Subbanagounder, G. J. Silverman, J. A. Berliner, and J. L. Witztum . 2004. Apoptotic cells with oxidation-specifi c epitopes are immunogenic and proinfl ammatory. J. Exp. Med. 200 : 1359-1370.
16. Weismann, D., K. Hartvigsen, N. Lauer, K. L. Bennett, H. P. Scholl, P. Charbel Issa, M. Cano, H. Brandstatter, S. Tsimikas, C. Skerka, et al. 2011. Complement factor H binds malondialdehyde epitopes and protects from oxidative stress. Nature . 478 : 76-81.
17. Miller, Y. I., S. H. Choi, P. Wiesner, L. Fang, R. Harkewicz, K. Hartvigsen, A. Boullier, A. Gonen, C. J. Diehl, X. Que, et al. 2011. Oxidation-specifi c epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ. Res. 108 : 235-248.
18. Rautou, P. E., A. C. Vion, N. Amabile, G. Chironi, A. Simon, A. Tedgui, and C. M. Boulanger . 2011. Microparticles, vascular function, and atherothrombosis. Circ. Res. 109 : 593-606.
19. Owens III, A. P., and N. Mackman . 2011. Microparticles in hemostasis and thrombosis. Circ. Res. 108 : 1284-1297.
20. Morel, O., N. Morel, L. Jesel, J. M. Freyssinet, and F. Toti . 2011. Microparticles: a critical component in the nexus between infl ammation, immunity, and thrombosis. Semin. Immunopathol. 33 : 469-486.
21. Mallat, Z., H. Benamer, B. Hugel, J. Benessiano, P. G. Steg, J. M. Freyssinet, and A. Tedgui . 2000. Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation . 101 : 841-843.
22. Mause, S. F., and C. Weber . 2010. Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ. Res. 107 : 1047-1057.
23. Rautou, P. E., A. S. Leroyer, B. Ramkhelawon, C. Devue, D. Duflaut, A. C. Vion, G. Nalbone, Y. Castier, G. Leseche, S. Lehoux, et al. 2011. Microparticles from human atherosclerotic plaques promote endothelial ICAM-1-dependent monocyte adhesion and transendothelial migration. Circ. Res. 108 : 335-343.
24. Wang, J. G., J. C. Williams, B. K. Davis, K. Jacobson, C. M. Doerschuk, J. P. Ting, and N. Mackman . 2011. Monocytic microparticles activate endothelial cells in an IL-1beta-dependent manner. Blood . 118 : 2366-2374.
25. Barry, O. P., D. Pratico, J. A. Lawson, and G. A. FitzGerald . 1997. Transcellular activation of platelets and endothelial cells by bioactive lipids in platelet microparticles. J. Clin. Invest. 99 : 2118-2127.
26. Distelmaier, K., C. Adlbrecht, J. Jakowitsch, S. Winkler, D. Dunkler, C. Gerner, O. Wagner, I. M. Lang, and M. Kubicek . 2009. Local complement activation triggers neutrophil recruitment to the site of thrombus formation in acute myocardial infarction. Thromb. Haemost. 102 : 564-572.
27. Palinski, W., S. Horkko, E. Miller, U. P. Steinbrecher, H. C. Powell, L. K. Curtiss, and J. L. Witztum . 1996. Cloning of monoclonal autoantibodies to epitopes of oxidized lipoproteins from apolipoprotein E-defi cient mice. Demonstration of epitopes of oxidized low density lipoprotein in human plasma. J. Clin. Invest. 98 : 800-814.
28. Hörkkö, S., D. A. Bird, E. Miller, H. Itabe, N. Leitinger, G. Subbanagounder, J. A. Berliner, P. Friedman, E. A. Dennis, L. K. Curtiss, et al . 1999. Monoclonal autoantibodies specifi c for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J. Clin. Invest. 103 : 117-128.
29. Amir, S., K. Hartvigsen, A. Gonen, G. Leibundgut, X. Que, E. Jensen-Jarolim, O. Wagner, S. Tsimikas, J. L. Witztum, and C. J. Binder . 2012. Peptide mimotopes of malondialdehyde epitopes for clinical applications in cardiovascular disease. J. Lipid Res. 53 : 1316-1326.
30. Tuominen, A., Y. I. Miller, L. F. Hansen, Y. A. Kesaniemi, J. L. Witztum, and S. Horkko . 2006. A natural antibody to oxidized cardiolipin binds to oxidized low-density lipoprotein, apoptotic cells, and atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 26 : 2096-2102.
31. Huber, J., A. Vales, G. Mitulovic, M. Blumer, R. Schmid, J. L. Witztum, B. R. Binder, and N. Leitinger . 2002. Oxidized membrane vesicles and blebs from apoptotic cells contain biologically active oxidized phospholipids that induce monocyte-endothelial interactions. Arterioscler. Thromb. Vasc. Biol. 22 : 101-107.
32. Liu, M. L., R. Scalia, J. L. Mehta, and K. J. Williams . 2012. Cholesterolinduced membrane microvesicles as novel carriers of damageassociated molecular patterns: mechanisms of formation, action, and detoxifi cation. Arterioscler. Thromb. Vasc. Biol. 32 : 2113-2121.
33. Jialal, I., C. J. Fuller, and B. A. Huet . 1995. The effect of alphatocopherol supplementation on LDL oxidation. A dose-response study. Arterioscler. Thromb. Vasc. Biol. 15 : 190-198.
34. Thiele, G. M., M. J. Duryee, M. S. Willis, M. F. Sorrell, T. L. Freeman, D. J. Tuma, and L. W. Klassen . 2004. Malondialdehydeacetaldehyde (MAA) modifi ed proteins induce pro-infl ammatory and pro-fi brotic responses by liver endothelial cells. Comp. Hepatol. 3 (Suppl. 1) : S25.
35. Qin, Z. 2012. The use of THP-1 cells as a model for mimicking the function and regulation of monocytes and macrophages in the vasculature. Atherosclerosis . 221 : 2-11.
36. Min, P. K., J. Y. Kim, K. H. Chung, B. K. Lee, M. Cho, D. L. Lee, S. Y. Hong, E. Y. Choi, Y. W. Yoon, B. K. Hong, et al. 2013. Local increase in microparticles from the aspirate of culprit coronary arteries in patients with ST-segment elevation myocardial infarction. Atherosclerosis . 227 : 323-328.
37. Ravandi, A., G. Leibundgut, M. Y. Hung, M. Patel, P. M. Hutchins, R. C. Murphy, A. Prasad, E. Mahmud, Y. I. Miller, E. A. Dennis, et al. 2014. Release and capture of bioactive oxidized phospholipids and oxidized cholesteryl esters during percutaneous coronary and peripheral arterial interventions in humans. J. Am. Coll. Cardiol. 63 : 1961-1971.
38. Shanmugam, N., J. L. Figarola, Y. Li, P. M. Swiderski, S. Rahbar, and R. Natarajan . 2008. Proinfl ammatory effects of advanced lipoxidation end products in monocytes. Diabetes . 57 : 879-888.
39. Hammarström, S., and P. Falardeau . 1977. Resolution of prostaglandin endoperoxide synthase and thromboxane synthase of human platelets. Proc. Natl. Acad. Sci. USA . 74 : 3691-3695.
40. Fogelman, A. M., I. Shechter, J. Seager, M. Hokom, J. S. Child, and P. A. Edwards . 1980. Malondialdehyde alteration of low density lipoproteins leads to cholesteryl ester accumulation in human monocyte-macrophages. Proc. Natl. Acad. Sci. USA . 77 : 2214-2218.