Multispecificity of immunoglobulin M antibodies raised against advanced glycation end products: Involvement of electronegative potential of antigens

Journal of Biological Chemistry

Volumn 288, Issue 19, 2013, Pages 13204-13214

  Chikazawa, Miho ^a   Otaki, Natsuki ^a   Shibata, Takahiro ^a   Miyashita, Hiroaki ^a   Kawai, Yoshichika ^a   Maruyama, Shoichi ^d   Toyokuni, Shinya ^d   Kitaura, Yasuyuki ^b   Matsuda, Tsukasa ^c   Uchida, Koji ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b Laboratory of Nutritional Biochemistry   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

^d NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCTS; CHEMICALLY MODIFIED; CLOSE RELATIONSHIPS; ELECTRONEGATIVE POTENTIAL; IMMUNE RESPONSE; INNATE IMMUNE RESPONSE; MODIFIED PROTEINS;

IMMUNE SYSTEM;

ANTIBODIES;

ADVANCED GLYCATION END PRODUCT; AUTOANTIBODY; DEHYDROASCORBIC ACID; DOUBLE STRANDED DNA; IMMUNOGLOBULIN M ANTIBODY; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS REACTION; FEMALE; HUMAN; IMMUNIZATION; IMMUNOGLOBULIN A NEPHROPATHY; INNATE IMMUNITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SPLEEN CELL; SYSTEMIC LUPUS ERYTHEMATOSUS;

AGES; ANTIBODIES; ANTIGEN; GLYCATION; INNATE IMMUNITY; NATURAL ANTIBODIES; PROTEIN CHEMICAL MODIFICATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIBODY SPECIFICITY; ANTIGENS; DEHYDROASCORBIC ACID; FEMALE; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; IMMUNITY, INNATE; IMMUNOGLOBULIN M; ISOELECTRIC POINT; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED BALB C; MICE, INBRED MRL LPR; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, PROTEIN;

EID: 84877697551     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.452177     Document Type: Article

References (42)

1. Monnier, V. M., Sell, D. R., and Genuth, S. (2005) Glycation products as markers and predictors of the progression of diabetic complications. Ann. N.Y. Acad. Sci. 1043, 567-581
2. Brownlee, M., Cerami, A., and Vlassara, H. (1988) Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N. Engl. J. Med. 318, 1315-1321
3. Baynes, J. W., and Monnier, V. M. (1989) Prog. Clin. Biol. Res. 304, 1-41
4. Vlassara, H. (2001) The AGE-receptor in the pathogenesis of diabetic complications. Diabetes Metab. Res. Rev. 17, 436-443
5. ∈-(Carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J. Biol. Chem. 274, 31740-31749
6. Nemet, I., and Monnier, V. M. (2011) Vitamin Cdegradation products and pathways in the human lens. J. Biol. Chem. 286, 37128-37136
7. ∈- (carboxymethyl) lysine by reaction between lysine and products of autoxidation of ascorbate. Biochemistry 29, 10964-10970
8. Nagaraj, R. H., Sell, D. R., Prabhakaram, M., Ortwerth, B. J., and Monnier V. M. (1991) High correlation between pentosidine protein crosslinks and pigmentation implicates ascorbate oxidation in human lens senescence and cataractogenesis. Proc. Natl. Acad. Sci. U.S.A. 88, 10257-10261
9. Tessier, F., Obrenovich, M., and Monnier, V. M. (1999) Structure and mechanism of formation of human lens fluorophore LM-1. Relationship to vesperlysine A and the advanced Maillard reaction in aging, diabetes, and cataractogenesis. J. Biol. Chem. 274, 20796-20804
10. Witztum, J. L., Steinbrecher, U. P., Kesaniemi, Y. A., and Fisher, M. (1984) Autoantibodies to glucosylated proteins in the plasma of patients with diabetes mellitus. Proc. Natl. Acad. Sci. U.S.A. 81, 3204-3208
11. Shibayama, R., Araki, N., Nagai, R., and Horiuchi, S. (1999) Autoantibody against N∈-(carboxymethyl)lysine. An advanced glycation end product of the Maillard reaction. Diabetes 48, 1842-1849
12. Engelbertsen, D., Anand, D. V., Fredrikson, G. N., Hopkins, D., Corder, R., Shah, P. K., Lahiri, A., Nilsson, J., and Bengtsson, E. (2012) High levels of IgM against methylglyoxal-modified apolipoprotein B100 are associated with less coronary artery calcification in patients with type 2 diabetes. J. Intern. Med. 271, 82-89
13. ∈-(4- oxononanoyl)lysine as a pro-inflammatory ligand. J. Biol. Chem. 286, 19943-19957
14. Basu S. K., Goldstein J. L., Anderson G. W., and Brown M. S. (1976) Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 73, 3178-3182
15. Antone, S. M., Adderson, E. E., Mertens, N. M., and Cunningham, M. W. (1997) Molecular analysis of V gene sequences encoding cytotoxic antistreptococcal/anti-myosin monoclonal antibody 36.2.2 that recognizes the heart cell surface protein laminin. J. Immunol. 159, 5422-5430
16. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST. A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402
17. Wardemann, H., Boehm, T., Dear, N., and Carsetti, R. (2002) B-1a B cells that link the innate and adaptive immune responses are lacking in the absence of the spleen. J. Exp. Med. 195, 771-780
18. Hayakawa, K., and Hardy, R. R. (2000) Development and function of B-1 cells. Curr. Opin. Immunol. 12, 346-353
19. Kawasaki, T., Kawai, T., and Akira, S. (2011) Recognition of nucleic acids by pattern-recognition receptors and its relevance in autoimmunity. Immunol. Rev. 243, 61-73
20. Diaw, L., Magnac, C., Pritsch, O., Buckle, M., Alzari, P. M., and Dighiero, G. (1997) Structural and affinity studies of IgM polyreactive natural autoantibodies. J. Immunol. 158, 968-976
21. Holmberg, D. (1987) High connectivity, natural antibodies preferentially use 7183 and QUPC 52 VH families. Eur. J. Immunol. 17, 399-403
22. Pennell, C. A., Arnold, L. W., Haughton, G., and Clarke, S. H. (1988) Restricted Ig variable region gene expression among Ly-1+B cell lymphomas. J. Immunol. 141, 2788-2796
23. Lindemose, S., Nielsen, P. E., Hansen, M., and Møllegaard, N. E. (2011) A DNA minor groove electronegative potential genome map based on photo-chemical probing. Nucleic Acids Res. 39, 6269-6276
24. Miller, Y. I., Choi, S. H., Wiesner, P., Fang, L., Harkewicz, R., Hartvigsen, K., Boullier, A., Gonen, A., Diehl, C. J., Que, X., Montano, E., Shaw, P. X., Tsimikas, S., Binder, C. J., and Witztum, J. L. (2011) Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ. Res. 108, 235-248
25. Weismann, D., and Binder, C. J. (2012) The innate immune response to products of phospholipid peroxidation. Biochim. Biophys. Acta 1818, 2465-2475
26. Grönwall, C., Vas, J., and Silverman, G. J. (2012) Protective roles of natural IgM antibodies. Front. Immunol. 3, 66
27. Baumgarth, N. (2011) The double life of a B-1 cell. Self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 11, 34-46
28. Hartvigsen, K., Chou, M. Y., Hansen, L. F., Shaw, P. X., Tsimikas, S., Binder, C. J., and Witztum, J. L. (2009) The role of innate immunity in atherogenesis. J. Lipid Res. 50, S388-393
29. Spatz, L., Iliev, A., Saenko, V., Jones, L., Irigoyen, M., Manheimer-Lory, A., Gaynor, B., Putterman, C., Bynoe, M., Kowal, C., Kuo, P., Newman, J., and Diamond, B. (1997) Studies on the structure, regulation, and pathogenic potential of anti-dsDNA antibodies. Methods 11, 70-78
30. Kowal, C., Weinstein, A., and Diamond, B. (1999) Molecular mimicry between bacterial and self antigen in a patient with systemic lupus erythematosus. Eur. J. Immunol. 29, 1901-1911
31. Limpanasithikul, W., Ray, S., and Diamond, B. (1995) Cross-reactive antibodies have both protective and pathogenic potential. J. Immunol. 155, 967-973
32. Chan, T. M., Leung, J. K., Ho, S. K., and Yung, S. (2002) Mesangial cellbinding anti-DNA antibodies in patients with systemic lupus erythematosus. J. Am. Soc. Nephrol. 13, 1219-1229
33. Jacob, L., Lety, M. A., Choquette, D., Viard, J. P., Jacob, F., Louvard, D., and Bach, J. F. (1987) Presence of antibodies against a cell-surface protein, cross-reactive with DNA, in systemic lupus erythematosus. A marker of the disease. Proc. Natl. Acad. Sci. U.S.A. 84, 2956-2959
34. Thompson, K. M., Sutherland, J., Barden, G., Melamed, M. D., Wright, M. G., Bailey, S., and Thorpe, S. J. (1992) Human monoclonal antibodies specific for blood group antigens demonstrate multispecific properties characteristic of natural autoantibodies. Immunology 76, 146-157
35. Radic, M. Z., and Weigert, M. (1994) Genetic and structural evidence for antigen selection of anti-DNA antibodies. Annu. Rev. Immunol. 12, 487-520
36. Chang, M. K., Bergmark, C., Laurila, A., Hörkkö, S., Han, K. H., Friedman, P., Dennis, E. A., and Witztum, J. L. (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
37. Yeung T, Terebiznik M, Yu L, Silvius J, Abidi, W. M., Philips M, Levine T, Kapus A, and Grinstein S. (2006) Receptor activation alters inner surface potential during phagocytosis. Science 313, 347-351
38. Grönwall, C., Akhter, E., Oh, C., Burlingame, R. W., Petri, M., and Silverman, G. J. (2012) IgM autoantibodies to distinct apoptosis-associated antigens correlate with protection from cardiovascular events and renal disease in patients with SLE. Clin. Immunol. 142, 390-398
39. Witte, T. (2008) IgM antibodies against dsDNA in SLE. Clin. Rev. Allergy Immunol. 34, 345-347
40. Hahn, B. H. (1998) Antibodies to DNA. N. Engl. J. Med. 338, 1359-1368
41. Boes, M., Schmidt, T., Linkemann, K., Beaudette, B. C., Marshak-Rothstein, A., and Chen, J. (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
42. Shoenfeld, Y., and Toubi, E. (2005) Protective autoantibodies. Role in homeostasis, clinical importance, and therapeutic potential. Arthritis Rheum. 52, 2599-2606