Immunization with a peptide surrogate for double-stranded DNA (dsDNA) induces autoantibody production and renal immunoglobulin deposition

Journal of Experimental Medicine

Volumn 188, Issue 1, 1998, Pages 29-38

  Putterman, Chaim ^a   Diamond, Betty ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Anti DNA; Autoantibodies; Inbred strains; Peptide library; Systemic lupus erythematosus

Indexed keywords

AUTOANTIBODY; DNA ANTIBODY; DOUBLE STRANDED DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; FEMALE; IMMUNOGLOBULIN DEPOSITION; IMMUNOMODULATION; IMMUNOPATHOGENESIS; INBRED STRAIN; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIBODIES, ANTINUCLEAR; AUTOANTIBODIES; AUTOANTIGENS; AUTOIMMUNITY; CARDIOLIPINS; DNA; HISTONES; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; KIDNEY; KIDNEY GLOMERULUS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED BALB C; PEPTIDE LIBRARY; PEPTIDES;

EID: 0032490679     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.1.29     Document Type: Article

References (44)

1. Diamond, B., J.B. Katz, E. Paul, C. Aranow, D. Lustgarten, and M.D. Scharff. 1992. The role of somatic mutation in the pathogenic anti-DNA response. Annu. Rev. Immunol. 10: 731-757.
2. Marion, T.N., D.M. Tillman, N.T. Jou, and R.J. Hill. 1992. Selection of immunoglobulin variable regions in autoimmunity to DNA. Immunol. Rev. 128:123-149.
3. Radic, M.Z., and M. Weigert. 1994. Genetic and structural evidence for antigen selection of anti-DNA antibodies. Annu. Rev. Immunol. 12:487-520.
4. Madaio, M.P., S. Hodder, R.S. Schwartz, and B.D. Stollar. 1984. Responsiveness of autoimmune and normal mice to nucleic acid antigens. J. Immunol. 132:872-876.
5. Pisetsky, D., J.P. Grudier, and G.S. Gilkeson. 1990. A role for immunogenic DNA in the pathogenesis of systemic lupus erythematosus. Arthritis Rheum. 33:153-159.
6. Gilkeson, G.S., A.M. Pippen, and D.S. Pisetsky. 1995. Induction of cross-reactive anti-dsDNA antibodies in preautoimniune NZB/NZW mice by immunization with bacterial DNA. J. Clin. Invest. 95:1398-1402.
7. Grayzel, A., A. Solomon, C. Aranow, and B. Diamond. 1991. Antibodies elicited by pneumococcal antigens bear an anti-DNA-associated idiotype. J. Clin. Invest. 87:842-846.
8. El-Roiey, A., O. Sela, D.A. Isenberg, R. Feldman, B.C. Colaco, R.C. Kennedy, and Y. Shoenfeld. 1987. The sera of patients with Klebsiella infections contain an anti-DNA idiotype (16/6) Id and anti-polynucleotide activity. Clin. Exp. Immunol. 67:507-515.
9. Izui, S., I.M. Zaldivar, I. Scher, and P.H. Lambert. 1977. Mechanisms of induction of anti-DNA antibodies by bacterial lipopolysaccharide in mice. I. Anti-DNA induction by LPS without significant release of DNA in circulating blood. J. Immunol. 119:2151-2156.
10. Shefner, R., G. Kleiner, A. Turken, L. Papazian, and B. Diamond. 1991. A novel class of anti-DNA antibodies identified in BALB/c mice. J. Exp. Med. 173:287-296.
11. Gaynor, B., C. Putterman, P. Valadon, L. Spatz, M.D. Scharff, and B. Diamond. 1997. Peptide inhibition of glomerular deposition of an anti-DNA antibody. Proc. Natl. Acad. Sci. USA. 94:1955-1960.
12. Tam, J.P. 1988. Synthetic peptide vaccine design: synthesis and properties of a high density, multiple antigenic peptide system. Proc. Natl. Acad. Sci. USA. 85:5409-5413.
13. Tam, J.P. 1996. Recent advances in multiple antigenic peptides. J. Immunol. Methods. 196:17-32.
14. Desaymard, C.A., M. Giusti, and M.D. Scharff. 1984. Rat anti-T15 monoclonal antibodies with specificity for VH and VH-VL epitopes. Mol. Immunol. 21:961-967.
15. Ginsberg, B., and H. Keiser. 1973. A Millipore filter assay for antibodies to native DNA in sera of patients with systemic lupus erythematosus. Arthritis Rheum. 16:199-207.
16. Putterman, C., W. Limpanasithikul, M. Edelman, and B. Diamond. 1996. The double edited sword of the immune response: mutational analysis of a murine anti-pneumococcal. anti-DNA antibody. J. Clin. Invest. 97:2251-2259.
17. Steward, M.W., and F.C. Hay. 1976. Changes in immunoglobulin class and subclass of anti-DNA antibodies with increasing age in NZB/NZW F1 hybrid mice. Clin. Exp. Immunol. 26:363-370.
18. Ohnishi, K., F.M. Ebling, B. Mitchell, R.R. Singh, B.H. Hahn, and B.P. Tasao. 1994. Comparison of pathogenic and non-pathogenic murine antibodies to DNA: antigen binding and structural characteristics. Int. Immunol. 6:817-830.
19. Foster, M.H., B. Cizman, and M.H. Madaio. 1993. Nephritogenic autoantibodies in systemic lupus erythematosus: immunochemical properties, mechanisms of immune deposition, and genetic origins. Lab. Invest. 69:494-507.
20. Raz, E., M. Brezis, E. Rosenmann, and D. Eilat. 1989. Anti-DNA antibodies bind directly to renal antigens and induce kidney dysfunction in the isolated perfused rat kidney. J. Immunol. 142:3076-3082.
21. Scott, J.K. 1992. Discovering peptide ligands using epitope libraries. Trends Biochem. Sci. 17:241-245.
22. Lundin, K., A. Samuelsson, M. Jansson, J. Hinkula, B. Wharen, H. Wigzell, and M.A. Persson. 1996. Peptides isolated from random peptide libraries on phage elicit a neutralizing anti-HIV-1 response: analysis of immunological mimicry. Immunology. 89:579-586.
23. Felici, F., A. Luzzago, A. Folgori, and R. Cortese. 1993. Mimicking of discontinuous epitopes by phage-displayed peptides. II. Selection of clones recognized by monoclonal antibody against the Bordetella pertussis toxin from phage peptide libraries. Gene. 128:21-27.
24. Westerink, M.A., P.C. Giardina, M.A. Apicella, and T. Kieber-Emmons. 1995. Peptide mimicry of the meningococcal group C capsular polysaccharide. Proc. Natl. Acad. Sci. USA. 92:4021-4025.
25. Valadon, P., G. Nussbaum, L.F. Boyd, D.H. Margulies, and M.D. Scharff. 1996. Peptide libraries define the fine specificity of anti-polysaccharide antibodies to Cryptococcus neaformans. J. Mol. Biol. 261:11-22.
26. Pisetsky, D.S., S.O. Hoch, S.L. Klatt, M.A. O'Donnell, and J.D. Keene. 1985. Specificity and idiotypic analysis of a monoclonal anti-Sm antibody with anti-DNA activity J. Immunol. 135:4080-4085.
27. Losman, M.J., T.M. Fasy, K.E. Novick, and M. Monestier. 1993. Relationship among antinuclear antibodies from autoimmune MRL mice reacting with histone H2A-H2B dimers and DNA. Int. Immunol. 5:513-523.
28. Ray, S.K., C. Putterman, and B. Diamond. 1996. Pathogenic antibodies are routinely generated during the response to foreign antigen: a paradigm for autoimmunity. Proc. Natl. Acad. Sci. USA. 93:2019-2024.
29. Limpanasithikul, W., S. Ray, and B. Diamond. 1995. Cross reactive antibodies have both protective and pathogenic potential. J. Immunol. 155:967-973.
30. James, J.A., T. Gross, R.H. Scofield, and J.B. Harley. 1995. Immunoglobulin epitope spreading and autoimmune disease after peptide immunization: Sm B/B′-derived PPPGMRPP and PPPGIRGP induce spliceosome autoimmunity. J. Exp. Med. 181:453-461.
31. Scofield, R.H., W.E. Henry, B.T. Kurien, J.A. James, and J.B. Harley. 1996. Immunization with short peptides from the sequence of the systemic lupus erythematosus-associated 60-kD Ro autoantigen results in anti-Ro ribonucleoprotein autoimmunity. J. Immunol. 156:4059-4066.
32. Topfer, F., T. Gordon, and J. McCluskey. 1995. Intra-and intermodular spreading of autoimmunity involving the nuclear self-antigens La (SS-B) and Ro (SS-A). Proc. Natl. Acad. Sci. USA. 92:875-879.
33. Mendelovic, S., S. Brocke, Y. Shoenfeld, M. Ben-Bassat, A. Meshorer, R. Bakimer, and E. Mozes. 1988. Induction of a systemic lupus erythematosus-like disease in mice by a common human anti-DNA idiotype. Proc. Natl. Acad. Sci. USA. 85:2260-2264.
34. McDevitt, H.O., and M.L. Tyan. 1968. Genetic control of the antibody response in inbred mice: transfer of the response by spleen cells and linkage to the major histocompatibility (H-2) locus. J. Exp. Med. 128:1-11.
35. Arnett, F.C., K. Goldstein, M. Duvic, and J.D. Reveille. 1988. Major histocompatibility complex genes in systemic lupus erythematosus, Sjogren's syndrome, and polymyositis. Am. J. Med. 85:38-41.
36. Fronek, Z., L.A. Timmerman, C.A. Alper, B.H. Hahn, K. Kalunian, B.M. Peterlin, and H.O. McDevitt. 1990. Major histocompatibility complex genes and susceptibility to systemic lupus erythematosus. Arthritis Rheum. 33:1542-1553.
37. James, J.A., and J.H. Harley. 1998. A model of peptide-induced lupus autoimmune B cell epitope spreading is strain specific and is not H-2 restricted in mice. J. Immunol. 160:502-508.
38. Izui, S., V.E. Kelley, K. Masuda, H. Yoshida, J.B. Roths, and E.D. Murphy. 1984. Induction of various autoantibodies by mutant gene lpr in several strains of mice. J. Immunol. 133: 227-233.
39. Strasser, A., A.W. Harris, and S. Cory. 1992. The role of bcl-2 in lymphoid differentiation and neoplastic transformation. Curr. Top. Microbiol. Immunol. 182:299-302.
40. Marchini, B., A. Puccetti, M.H. Dolcher, and M.P. Madaio. 1995. Induction of anti-DNA antibodies in non-autoimmune mice by immunization with a DNA-DNAse I complex. Clin. Exp. Rheumatol. 13:7-10.
41. Rekvig, O.P., U. Moens, A. Sundsfjord, G. Bredholt, A. Osei, H. Haaeim, E. Traavik-Arensen, and H.J. Haga. 1997. Experimental expression in mice and spontaneous expression in human SLE of polyomavirus T-antigen. A molecular basis for induction of antibodies to DNA and eukaryotic transcription factors. J. Clin. Invest. 99:2045-2054.
42. Rekvig, O.P., U. Moens, K. Fredrikson, and T. Traavik. 1997. Human polyomavirus and immunogenicty of mammalian DNA: a conceptual framework. Methods. 11:44-54.
43. Desai, D.D., M.K. Krishnan, J.T. Swindle, and T.N. Marion. 1993. Antigen-specific induction of antibodies against native mammalian DNA in nonautoimmune mice. J. Immunity. 151: 1614-1626.
44. Pisetsky, D.S. 1997. DNA and the immune system. Ann. Intern. Med. 126:169-171.