Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans

Journal of Clinical Investigation

Volumn 119, Issue 5, 2009, Pages 1335-1349

  Chou, Meng Yun ^a   Fogelstrand, Linda ^a   Hartvigsen, Karsten ^a   Hansen, Lotte F ^a   Woelkers, Douglas ^a   Shaw, Peter X ^a   Choi, Jeomil ^a,b   Perkmann, Thomas ^c   Bäckhed, Fredrik ^d   Miller, Yury I ^a   Hörkkö, Sohvi ^a   Corr, Maripat ^a   Witztum, Joseph L ^a   Binder, Christoph J ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Pusan National University   (South Korea)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; EPITOPE; IMMUNOGLOBULIN M; BOVINE SERUM ALBUMIN; DRUG DERIVATIVE; HOMEODOMAIN PROTEIN; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MALONALDEHYDE; MALONDIALDEHYDE LOW DENSITY LIPOPROTEIN, MOUSE; MALONDIALDEHYDE-LOW DENSITY LIPOPROTEIN, MOUSE; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHORYLCHOLINE; PHOSPHORYLCHOLINE BOVINE SERUM ALBUMIN; PHOSPHORYLCHOLINE-BOVINE SERUM ALBUMIN; RAG 1 PROTEIN; RAG-1 PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CELL DEATH; CHRONIC INFLAMMATION; CONTROLLED STUDY; FEMALE; HOMEOSTASIS; HUMAN; HUMAN CELL; INFANT; INNATE IMMUNITY; MALE; MOUSE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; ADOPTIVE TRANSFER; ANIMAL; ANTIBODY AFFINITY; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; B LYMPHOCYTE; BLOOD; C57BL MOUSE; FETUS BLOOD; GENETICS; GERMFREE ANIMAL; IMMUNOLOGY; MOUSE MUTANT; OXIDATION REDUCTION REACTION; PATHOLOGY; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIBODY AFFINITY; ANTIBODY FORMATION; ANTIBODY SPECIFICITY; APOPTOSIS; ATHEROSCLEROSIS; B-LYMPHOCYTE SUBSETS; EPITOPES; FEMALE; FETAL BLOOD; GERM-FREE LIFE; HOMEODOMAIN PROTEINS; IMMUNITY, INNATE; IMMUNOGLOBULIN M; LIPOPROTEINS, LDL; MACROPHAGES, PERITONEAL; MALE; MALONDIALDEHYDE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDATION-REDUCTION; PHAGOCYTOSIS; PHOSPHORYLCHOLINE; RECEPTORS, LDL; SERUM ALBUMIN, BOVINE;

EID: 66449085101     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI36800     Document Type: Article

References (73)

1. Binder, C.J., et al. 2002. Innate and acquired immunity in atherogenesis. Nat. Med. 8:1218-1226.
2. Hansson, G.K., and Libby, P. 2006. The immune response in atherosclerosis: a double-edged sword. Nat. Rev. Immunol. 6:508-519.
3. Getz, G.S., Vanderlaan, P.A., and Reardon, C.A. 2007. The immune system and murine atherosclerosis. Curr. Drug Targets. 8:1297-1306.
4. Binder, C.J., et al. 2005. The role of natural antibodies in atherogenesis. J. Lipid Res. 46:1353-1363.
5. Boullier, A., et al. 2005. Phosphocholine as a pattern recognition ligand for CD36. J. Lipid Res. 46:969-976.
6. Gillotte-Taylor, K., Boullier, A., Witztum, J.L., Steinberg, D., and Quehenberger, O. 2001. Scavenger receptor class B type I as a receptor for oxidized low density lipoprotein. J. Lipid Res. 42:1474-1482.
7. Plüddemann, A., Neyen, C., and Gordon, S. 2007. Macrophage scavenger receptors and host-derived ligands. Methods. 43:207-217.
8. Palinski, W., et al. 1996. 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.
9. Hörkkö, S., Miller, E., Branch, D.W., Palinski, W., and Witztum, J.L. 1997. The epitopes for some antiphospholipid antibodies are adducts of oxidized phospholipid and beta2 glycoprotein 1 (and other proteins). Proc. Natl. Acad. Sci. U. S. A. 94:10356-10361.
10. Boullier, A., et al. 2000. 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.
11. Baumgarth, N., Tung, J.W., and Herzenberg, L.A. 2005. Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin. Immunopathol. 26:347-362.
12. Shaw, P.X., et al. 2000. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J. Clin. Invest. 105:1731-1740.
13. Briles, D.E., Forman, C., Hudak, S., and Claflin, J.L. 1982. Anti-phosphorylcholine antibodies of the T15 idiotype are optimally protective against Streptococcus pneumoniae. J. Exp. Med. 156:1177-1185.
14. Binder, C.J., et al. 2003. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat. Med. 9:736-743.
15. Kagan, V.E., et al. 2004. Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine. Free Radic. Biol. Med. 37:1963-1985.
16. Greenberg, M.E., et al. 2006. Oxidized phosphatidylserine-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. J. Exp. Med. 203:2613-2625.
17. Savill, J., Dransfield, I., Gregory, C., and Haslett, C. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2:965-975.
18. Chang, M.K., et al. 2004. Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory. J. Exp. Med. 200:1359-1370.
19. Chang, M.K., et al. 1999. 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. 96:6353-6358.
20. Chang, M.K., Binder, C.J., Torzewski, M., and Witztum, J.L. 2002. 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. 99:13043-13048.
21. Kawahara, T., Ohdan, H., Zhao, G., Yang, Y.G., and Sykes, M. 2003. Peritoneal cavity B cells are precursors of splenic IgM natural antibody-producing cells. J. Immunol. 171:5406-5414.
22. Hörkkö, S., et al. 1999. 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.
23. Friguet, B., et al. 1985. Measurements of the true affinity constant in solution of antigen-antibody complexes by enzyme-linked immunosorbent assay. J. Immunol. Methods. 77:305-319.
24. Masmoudi, H., Mota-Santos, T., Huetz, F., Coutinho, A., and Cazenave, P.A. 1990. All T15 Id-positive antibodies (but not the majority of VHT15+ antibodies) are produced by peritoneal CD5+ B lymphocytes. Int. Immunol. 2:515-520.
25. Binder, C.J., et al. 2004. IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis. J. Clin. Invest. 114:427-437.
26. Manz, R.A., Hauser, A.E., Hiepe, F., and Radbruch, A. 2005. Maintenance of serum antibody levels. Annu. Rev. Immunol. 23:367-386.
27. Shaw, P.X., et al. 2001. Human-derived anti-oxidized LDL autoantibody blocks uptake of oxidized LDL by macrophages and localizes to atherosclerotic lesions in vivo. Arterioscler. Thromb. Vasc. Biol. 21:1333-1339.
28. Tabas, I. 2005. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency. Arterioscler. Thromb. Vasc. Biol. 25:2255-2264.
29. Ylä-Herttuala, S., et al. 1989. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J. Clin. Invest. 84:1086-1095.
30. Palinski, W., et al. 1990. Antisera and monoclonal antibodies specific for epitopes generated during oxidative modification of low density lipoprotein. Arteriosclerosis. 10:325-335.
31. Merbl, Y., Zucker-Toledano, M., Quintana, F.J., and Cohen, I.R. 2007. Newborn humans manifest autoantibodies to defined self molecules detected by antigen microarray informatics. J. Clin. Invest. 117:712-718.
32. Taylor, P.R., et al. 2000. A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J. Exp. Med. 192:359-366.
33. Miller, Y.I., et al. 2005. Toll-like receptor 4-dependent and -independent cytokine secretion induced by minimally oxidized low-density lipoprotein in macrophages. Arterioscler. Thromb. Vasc. Biol. 25:1213-1219.
34. Miller, Y.I., Chang, M.K., Binder, C.J., Shaw, P.X., and Witztum, J.L. 2003. Oxidized low density lipoprotein and innate immune receptors. Curr. Opin. Lipidol. 14:437-445.
35. Haury, M., et al. 1997. The repertoire of serum IgM in normal mice is largely independent of external antigenic contact. Eur. J. Immunol. 27:1557-1563.
36. Vasconcellos, R., Nobrega, A., Haury, M., Viale, A.C., and Coutinho, A. 1998. Genetic control of natural antibody repertoires: I. IgH, MHC and TCR beta loci. Eur. J. Immunol. 28:1104-1115.
37. Mouthon, L., et al. 1995. Invariance and restriction toward a limited set of self-antigens characterize neonatal IgM antibody repertoires and prevail in autoreactive repertoires of healthy adults. Proc. Natl. Acad. Sci. U. S. A. 92:3839-3843.
38. Jayasekera, J.P., Moseman, E.A., and Carroll, M.C. 2007. Natural antibody and complement mediate neutralization of influenza virus in the absence of prior immunity. J. Virol. 81:3487-3494.
39. Hooijkaas, H., Benner, R., Pleasants, J.R., and Wostmann, B.S. 1984. Isotypes and specificities of immunoglobulins produced by germ-free mice fed chemically defined ultrafiltered "antigen-free" diet. Eur. J. Immunol. 14:1127-1130.
40. Avrameas, S. 1991. Natural autoantibodies: from "horror autotoxicus" to "gnothi seauton." Immunol. Today. 12:154-159.
41. Hardy, R.R., and Hayakawa, K. 2005. Development of B cells producing natural autoantibodies to thymocytes and senescent erythrocytes. Springer Semin. Immunopathol. 26:363-375.
42. Kearney, J.F. 2005. Innate-like B cells. Springer Semin. Immunopathol. 26:377-383.
43. Montecino-Rodriguez, E., Leathers, H., and Dorshkind, K. 2006. Identification of a B-1 B cell-specified progenitor. Nat. Immunol. 7:293-301.
44. Herzenberg, L.A., and Tung, J.W. 2006. B cell lineages: documented at last! Nat. Immunol. 7:225-226.
45. Tung, J.W., Mrazek, M.D., Yang, Y., Herzenberg, L.A., and Herzenberg, L.A. 2006. Phenotypically distinct B cell development pathways map to the three B cell lineages in the mouse. Proc. Natl. Acad. Sci. U. S. A. 103:6293-6298.
46. Dorshkind, K., and Montecino-Rodriguez, E. 2007. Fetal B-cell lymphopoiesis and the emergence of B-1-cell potential. Nat. Rev. Immunol. 7:213-219.
47. Hardy, R.R., Wei, C.J., and Hayakawa, K. 2004. Selection during development of VH11+ B cells: a model for natural autoantibody-producing CD5+ B cells. Immunol. Rev. 197:60-74.
48. Qian, Y., et al. 2006. Autoreactive MZ and B-1 B-cell activation by Faslpr is coincident with an increased frequency of apoptotic lymphocytes and a defect in macrophage clearance. Blood. 108:974-982.
49. Bos, N.A., et al. 1987. Early development of Ig-secreting cells in young of germ-free BALB/c mice fed a chemically defined ultrafiltered diet. Cell. Immunol. 105:235-245.
50. Thurnheer, M.C., Zuercher, A.W., Cebra, J.J., and Bos, N.A. 2003. B1 cells contribute to serum IgM, but not to intestinal IgA, production in gnotobiotic Ig allotype chimeric mice. J. Immunol. 170:4564-4571.
51. Kearney, J.F. 2000. Immune recognition of OxLDL in atherosclerosis. J. Clin. Invest. 105:1683-1685.
52. Huber, J., et al. 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.
53. Houglum, K., et al. 1997. Excess iron induces hepatic oxidative stress and transforming growth factor beta1 in genetic hemochromatosis. Hepatology. 26:605-610.
54. Horie, K., et al. 1997. 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. 100:2995-3004.
55. Imai, Y., et al. 2008. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell. 133:235-249.
56. Newcombe, J., Li, H., and Cuzner, M.L. 1994. Low density lipoprotein uptake by macrophages in multiple sclerosis plaques: implications for pathogenesis. Neuropathol. Appl. Neurobiol. 20:152-162.
57. Dei, R., et al. 2002. Lipid peroxidation and advanced glycation end products in the brain in normal aging and in Alzheimer's disease. Acta Neuropathol. (Berl.). 104:113-122.
58. Berland, R., and Wortis, H.H. 2002. Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 20:253-300.
59. Genestier, L., et al. 2007. TLR agonists selectively promote terminal plasma cell differentiation of B cell subsets specialized in thymus-independent responses. J. Immunol. 178:7779-7786.
60. Miller, Y.I., et al. 2003. Minimally modified LDL binds to CD14, induces macrophage spreading via TLR4/MD-2, and inhibits phagocytosis of apoptotic cells. J. Biol. Chem. 278:1561-1568.
61. Bae, Y.S., et al. 2009. Macrophages generate reactive oxygen species in response to minimally oxidized low-density lipoprotein. Toll-like receptor 4- and spleen tyrosine kinase-dependent activation of NADPH oxidase 2. Circ. Res. 104:210-218.
62. Bergmark, C., et al. 2008. A novel function of lipoprotein [a] as a preferential carrier of oxidized phospholipids in human plasma. J. Lipid Res. 49:2230-2239.
63. Blair, I.A. 2008. DNA-adducts with lipid peroxidation products. J. Biol. Chem. 283:15545-15549.
64. Esterbauer, H., Schaur, R.J., and Zollner, H. 1991. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11:81-128.
65. Ochsenbein, A.F., et al. 1999. Control of early viral and bacterial distribution and disease by natural antibodies. Science. 286:2156-2159.
66. Boes, M., Prodeus, A.P., Schmidt, T., Carroll, M.C., and Chen, J. 1998. A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J. Exp. Med. 188:2381-2386.
67. Baumgarth, N., et al. 1999. Innate and acquired humoral immunities to influenza virus are mediated by distinct arms of the immune system. Proc. Natl. Acad. Sci. U. S. A. 96:2250-2255.
68. Lutz, H.U. 2007. Homeostatic roles of naturally occurring antibodies: an overview. J. Autoimmun. 29:287-294.
69. Boes, M., et al. 2000. Accelerated development of IgG autoantibodies and autoimmune disease in the absence of secreted IgM. Proc. Natl. Acad. Sci. U. S. A. 97:1184-1189.
70. Quartier, P., Potter, P.K., Ehrenstein, M.R., Walport, M.J., and Botto, M. 2005. Predominant role of IgM-dependent activation of the classical pathway in the clearance of dying cells by murine bone marrow-derived macrophages in vitro. Eur. J. Immunol. 35:252-260.
71. Ogden, C.A., Kowalewski, R., Peng, Y., Montenegro, V., and Elkon, K.B. 2005. IGM is required for efficient complement mediated phagocytosis of apoptotic cells in vivo. Autoimmunity. 38:259-264.
72. Kearney, J.F., Barletta, R., Quan, Z.S., and Quintans, J. 1981. Monoclonal vs. heterogeneous anti-H-8 antibodies in the analysis of the anti-phosphorylcholine response in BALB/c mice. Eur. J. Immunol. 11:877-883.
73. Xu, D., et al. 1997. Epitope characterization of malondialdehyde- acetaldehyde adducts using an enzyme-linked immunosorbent assay. Chem. Res. Toxicol. 10:978-986.