Nephritogenic antibodies bind in glomeruli through interaction with exposed chromatin fragments and not with renal cross-reactive antigens

Autoimmunity

Volumn 44, Issue 5, 2011, Pages 373-383

  Mjelle, Janne Erikke ^a   Rekvig, Ole Petter ^a,b   Van Der Vlag, Johan ^c   Fenton, Kristin A ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Anti actinin antibodies; Anti dsDNA antibodies; Anti nucleosome antibodies; Lupus nephritis; Systemic lupus erythematosus

Indexed keywords

AGRIN; ALPHA ACTININ; ANTINUCLEAR ANTIBODY; CROSS REACTING ANTIGEN; DOUBLE STRANDED DNA; DOUBLE STRANDED DNA ANTIBODY; HEPARAN SULFATE; IMMUNOGLOBULIN G; LAMININ; MONOCLONAL ANTIBODY; NEPHRITOGENIC ANTIBODY; NUCLEOSOME ANTIBODY; PERLECAN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CHROMATIN STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; GLOMERULUS; GLOMERULUS BASEMENT MEMBRANE; IMMUNOELECTRON MICROSCOPY; LUPUS ERYTHEMATOSUS NEPHRITIS; MESANGIUM CELL; MOUSE; NONHUMAN; NUCLEOSOME; SURFACE PLASMON RESONANCE;

ACTININ; AGRIN; ANIMALS; ANTIBODIES, ANTINUCLEAR; ANTIGEN-ANTIBODY COMPLEX; BASEMENT MEMBRANE; CHROMATIN; DNA; IMMUNOGLOBULIN G; KIDNEY GLOMERULUS; LUPUS NEPHRITIS; MICE; MICE, INBRED NZB; NUCLEOSOMES; PROTEIN BINDING; SURFACE PLASMON RESONANCE;

EID: 79960143926     PISSN: 08916934     EISSN: 1607842X     Source Type: Journal    
DOI: 10.3109/08916934.2010.541170     Document Type: Article

References (52)

1. Hahn BH. Antibodies to DNA. N Engl J Med 1998;338: 1359-1368 (Pubitemid 28216666)
2. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271-1277 (Pubitemid 13221242)
3. Rekvig OP, Nossent JC. Anti-double-stranded DNA antibodies, nucleosomes, and systemic lupus erythematosus-A time for new paradigms? Arthritis Rheumat 2003;48: 300-312 (Pubitemid 36277996)
4. Mortensen ES, Fenton KA, Rekvig OP. Lupus nephritis: The central role of nucleosomes revealed. Am J Pathol 2008;172: 275-283 (Pubitemid 351282015)
5. Gilkeson GS, Bernstein K, Pippen AM, Clarke SH, Marion T, Pisetsky DS, Ruiz P, Lefkowith JB. The influence of variableregion somatic mutations on the specificity and pathogenicity of murine monoclonal anti-DNA antibodies. Clin Immunol Immunopathol 1995;76:59-67
6. Shlomchik MJ,Madaio MP. The role of antibodies and B cells in the pathogenesis of lupus nephritis. Springer Semin Immunopathol 2003;24:363-375
7. Mjelle JE, Kalaaji M, Rekvig OP. Exposure of chromatin and not high affinity for dsDNA determines the nephritogenic impact of anti-dsDNA antibodies in (NZB ? NZW)F1 mice. Autoimmunity 2009;42:104-111
8. Qureshi F, Yang Y, Jaques SM, Johnson MP, Naparstek Y, Ulmansky R, Schuger L. Anti-DNA antibodies cross-reacting with laminin inhibit trophoblast attachment and migration: Implications for recurrent pregnancy loss in SLE patients. Am J Reprod Immunol 2000;44:136-142
9. Sabbaga J, Line SR, Potocnjak P, Madaio MP. A murine nephritogenic monoclonal anti-DNA autoantibody binds directly to mouse laminin, the major non-collagenous protein component of the glomerular basement membrane. Eur J Immunol 1989;19:137-143 (Pubitemid 19069299)
10. Mageed RA, Zack DJ. Cross-reactivity and pathogenicity of anti-DNA autoantibodies in systemic lupus erythematosus. Lupus 2002;11:783-786 (Pubitemid 36069971)
11. Berden JH, Licht R, van Bruggen MC, Tax WJ. Role of nucleosomes for induction and glomerular binding of autoantibodies in lupus nephritis. Curr Opin Nephrol Hypertens 1999;8:299-306 (Pubitemid 29381618)
12. Lefkowith JB, Kiehl M, Rubenstein J, DiValerio R, Bernstein K, Kahl L, Rubin RL, Gourley M. Heterogeneity and clinical significance of glomerular-binding antibodies in systemic lupus erythematosus. J Clin Invest 1996;98: 1373-1380 (Pubitemid 26322062)
13. Rekvig OP, Kalaaji M, Nossent H. Anti-DNA antibody subpopulations and lupus nephritis. Autoimmun Rev 2004;3: 1-6 (Pubitemid 38293359)
14. van Bavel CC, Fenton KA, Rekvig OP, van der Vlag J, Berden JH. Glomerular targets of nephritogenic autoantibodies in systemic lupus erythematosus. Arthritis Rheum 2008;58:1892-1899 (Pubitemid 351988079)
15. Deocharan B, Qing X, Lichauco J, Putterman C. Alphaactinin is a cross-reactive renal target for pathogenic anti-DNA antibodies. J Immunol 2002;168:3072-3078 (Pubitemid 34211690)
16. Mason LJ, Ravirajan CT, Rahman A, Putterman C, Isenberg DA. Is alpha-actinin a target for pathogenic anti- DNA antibodies in lupus nephritis? Arthritis Rheum 2004;50: 866-870 (Pubitemid 38326187)
17. Renaudineau Y, Croquefer S, Jousse S, Renaudineau E, Devauchelle V, Gueguen P, Hanrotel C, Gilburd B, Saraux A, Shoenfeld Y, Putterman C, Youinou P. Association of alpha-actinin-binding anti-double-stranded DNA antibodies with lupus nephritis. Arthritis Rheum 2006;54: 2523-2532 (Pubitemid 44205013)
18. Zhao Z, Weinstein E, Tuzova M, Davidson A, Mundel P, Marambio P, Putterman C. Cross-reactivity of human lupus anti-DNA antibodies with alpha-actinin and nephritogenic potential. Arthritis Rheum 2005;52:522-530 (Pubitemid 40216316)
19. Manson JJ, Ma A, Rogers P, Mason LJ, Berden JH, van d V, D?Cruz DP, Isenberg DA, Rahman A. Relationship between anti-dsDNA, anti-nucleosome and anti-alpha-actinin antibodies and markers of renal disease in patients with lupus nephritis: A prospective longitudinal study. Arthritis Res Ther 2009;11:R154
20. Kalaaji M, Mortensen E, Jorgensen L, Olsen R, Rekvig OP. Nephritogenic lupus antibodies recognize glomerular basement membrane-associated chromatin fragments released from apoptotic intraglomerular cells. Am J Pathol 2006;168: 1779-1792 (Pubitemid 43825300)
21. Kalaaji M, Fenton KA, Mortensen ES, Olsen R, Sturfelt G, Alm P, Rekvig OP. Glomerular apoptotic nucleosomes are central target structures for nephritogenic antibodies in human SLE nephritis. Kidney Int 2007;71:664-672 (Pubitemid 46494570)
22. Mjelle JE, Rekvig OP, Fenton KA. Nucleosomes possess a high affinity for glomerular laminin and collagen IV and bind nephritogenic antibodies in murine lupus-like nephritis. Ann Rheum Dis 2007;66:1661-1668 (Pubitemid 350205458)
23. Ben-Bassat M, Rosenfeld J, Joshua H, Hazaz B, Gura V. Lupus nephritis. Electron-dense and immunofluorescent deposits and their correlation with proteinuria and renal function. Am J Clin Pathol 1979;72:186-193 (Pubitemid 10219894)
24. Comerford FR, Cohen AS, Desai RG. The evolution of the glomerular lesion in NZB mice. A light and electron microscopic study. Lab Invest 1968;19:643-651
25. Dillard MG, Tillman RL, Sampson CC. Lupus nephritis. Correlations between the clinical course and presence of electron-dense deposits. Lab Invest 1975;32:261-269
26. van Bruggen MCJ, Walgreen B, Rijke TPM, Tamboer W, Kramers K, Smeenk RJT, Monestier M, Fournie GJ, Berden JHM. Antigen specificity of anti-nuclear antibodies complexed to nucleosomes determines glomerular basement membrane binding in vivo. Euro J Immunol 1997;27: 1564-1569 (Pubitemid 27254851)
27. van Bruggen MC, Kramers K, Hylkema MN, van den Born J, Bakker MA, Assmann KJ, Smeenk RJ, Berden JH. Decrease of heparan sulfate staining in the glomerular basement membrane in murine lupus nephritis. Am J Pathol 1995;146: 753-763
28. van Bruggen MC, Walgreen B, Rijke TP, Corsius MJ, Assmann KJ, Smeenk RJ, van Dedem GW, Kramers K, Berden JH. Heparin and heparinoids prevent the binding of immune complexes containing nucleosomal antigens to the GBM and delay nephritis in MRL/lpr mice. Kidney Int 1996; 50:1555-1564 (Pubitemid 26364261)
29. Eilat D, Fischel R, Zlotnick A. A central anti-DNA idiotype in human and murine systemic lupus erythematosus. Eur J Immunol 1985;15:368-375 (Pubitemid 15068368)
30. Eilat D, Webster DM, Rees AR. V region sequences of anti-DNA and anti-RNA autoantibodies from NZB/NZW F1 mice. J Immunol 1988;141:1745-1753
31. Mostoslavsky G, Fischel R, Yachimovich N, Yarkoni Y, Rosenmann E, Monestier M, Baniyash M, Eilat D. Lupus anti-DNA autoantibodies cross-react with a glomerular structural protein: A case for tissue injury by molecular mimicry. Eur J Immunol 2001;31:1221-1227
32. Eilat D, Hochberg M, Pumphrey J, Rudikoff S. Monoclonal antibodies to DNA and RNA from NZB/NZW F1 mice: Antigenic specificities and NH2 terminal amino acid sequences. J Immunol 1984;133:489-494 (Pubitemid 14082079)
33. van den Born J, van den Heuvel LP, Bakker MA, Veerkamp JH, Assmann KJ, Berden JH. A monoclonal antibody against GBM heparan sulfate induces an acute selective proteinuria in rats. Kidney Int 1992;41:115-123
34. Kramers K, Stemmer C, Monestier M, van Bruggen MC, Rijke-Schilder TP, Hylkema MN, Smeenk RJ, Muller S, Berden JH. Specificity of monoclonal anti-nucleosome auto-antibodies derived from lupus mice. J Autoimmun 1996;9:723-729 (Pubitemid 27047021)
35. Smeenk RJ, Brinkman K, van den Brink HG, Westgeest AA. Reaction patterns of monoclonal antibodies to DNA. J Immunol 1988;140:3786-3792
36. Monestier M, Fasy TM, Losman MJ, Novick KE, Muller S. Structure and binding properties of monoclonal antibodies to core histones from autoimmune mice. Mol Immunol 1993; 30:1069-1075
37. Fenton KA, Tommeras B, Marion TN, Rekvig OP. Pure anti-dsDNA mAbs need chromatin structures to promote glomerular mesangial deposits in BALB/c mice. Autoimmunity 2010;43:179-188
38. Andreassen K, Bredholt G, Moens U, Bendiksen S, Kauric G, Rekvig OP. T cell lines specific for polyomavirus T-antigen recognize T-antigen complexed with nucleosomes: A molecular basis for anti-DNA antibody production. Eur J Immunol 1999;29:2715-2728 (Pubitemid 30098996)
39. Bredholt G, Olaussen E, Moens U, Rekvig OP. Linked production of antibodies to mammalian DNA and to human polyomavirus large T antigen-Footprints of a common molecular and cellular process? Arthritis Rheumat 1999;42: 2583-2592
40. Rekvig OP, Hannestad K. Lupus-erythematosus (Le) factors recognize both nucleosomes and viable human-leukocytes. Scand J Immunol 1981;13:597-604 (Pubitemid 11112502)
41. Kalaaji M, Sturfelt G, Mjelle JE, Nossent H, Rekvig OP. Critical comparative analyses of anti-alpha-actinin and glomerulus-bound antibodies in human and murine lupus nephritis. Arthritis Rheum 2006;54:914-926
42. Lafer EM, Rauch J, Andrzejewski C Jr, Mudd D, Furie B, Furie B, Schwartz RS, Stollar BD. Polyspecific monoclonal lupus autoantibodies reactive with both polynucleotides and phospholipids. J Exp Med 1981;153:897-909 (Pubitemid 11104738)
43. Madaio MP, Carlson J, Cataldo J, Ucci A, Migliorini P, Pankewycz O. Murine monoclonal anti-DNA antibodies bind directly to glomerular antigens and form immune deposits. J Immunol 1987;138:2883-2889 (Pubitemid 17072763)
44. Raz E, Ben-Bassat H, Davidi T, Shlomai Z, Eilat D. Crossreactions of anti-DNA autoantibodies with cell surface proteins. Eur J Immunol 1993;23:383-390 (Pubitemid 23075067)
45. Fournel S, Muller S. Peptides as DNA mimics: Crossreactivity and mimicry in systemic autoimmune diseases. Cell Mol Life Sci 2002;59:1280-1284
46. van Bruggen MC, Kramers C, Walgreen B, Elema JD, Kallenberg CG, van den Born J, Smeenk RJ, Assmann KJ, Muller S, Monestier M, Berden JH. Nucleosomes and histones are present in glomerular deposits in human lupus nephritis. Nephrol Dial Transplant 1997;12:57-66 (Pubitemid 27046202)
47. van Bruggen MCJ, Kramers C, Hylkema MN, Smeenk RJT, Berden JHM. Pathophysiology of lupus nephritis-The role of nucleosomes. Nether J Med 1994;45:273-279 (Pubitemid 24362333)
48. Amital H, Heilweil M, Ulmansky R, Szafer F, Bar-Tana R, Morel L, Foster MH, Mostoslavsky G, Eilat D, Pizov G, Naparstek Y. Treatment with a laminin-derived peptide suppresses lupus nephritis. J Immunol 2005;175: 5516-5523 (Pubitemid 41456439)
49. D?Andrea DM, Coupaye-Gerard B, Kleyman TR, Foster MH, Madaio MP. Lupus autoantibodies interact directly with distinct glomerular and vascular cell surface antigens. Kidney Int 1996;49:1214-1221 (Pubitemid 26167276)
50. Raz E, Brezis M, Rosenmann E, Eilat D. Anti-DNA antibodies bind directly to renal antigens and induce kidney dysfunction in the isolated perfused rat kidney. J Immunol 1989;142: 3076-3082 (Pubitemid 19129925)
51. Termaat RM, Brinkman K, van Gompel F, van den Heuvel LP, Veerkamp JH, Smeenk RJ, Berden JH. Cross-reactivity of monoclonal anti-DNA antibodies with heparan sulfate is mediated via bound DNA/histone complexes. J Autoimmun 1990;3:531-545 (Pubitemid 20358952)
52. Kramers C, Hylkema MN, van Bruggen MC, van de Lagemaat R, Dijkman HB, Assmann KJ, Smeenk RJ, Berden JH. Anti-nucleosome antibodies complexed to nucleosomal antigens show anti-DNA reactivity and bind to rat glomerular basement membrane in vivo. J Clin Invest 1994; 94:568-577