The epitopes targeted by the rheumatoid arthritis-associated antifilaggrin autoantibodies are posttranslationally generated on various sites of (pro)filaggrin by deimination of arginine residues

Journal of Immunology

Volumn 162, Issue 1, 1999, Pages 585-594

  Girbal Neuhauser, Elisabeth ^a   Durieux, Jean Jacques ^a   Arnaud, Michel ^b   Dalbon, Pascal ^b   Sebbag, Mireille ^a   Vincent, Christian ^a   Simon, Michel ^a   Senshu, Tatsuo ^c   Masson Bessière, Christine ^a   Jolivet Reynaud, Colette ^b   Jolivet, Michel ^b   Serre, Guy ^a,d  

^a INSERM   (France)

^b BioMérieux ^*  (France)

^c TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

^d CHU PURPAN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; EPITOPE;

ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; PRIORITY JOURNAL; PROTEIN PROCESSING; RHEUMATOID ARTHRITIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARGININE; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; CITRULLINE; EPIDERMIS; EPITHELIUM; EPITOPES; HUMANS; HYDROLASES; INTERMEDIATE FILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS;

EID: 0032960781     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (56)

1. Arnett, F. C., S. M. Edworthy, D. A. Bloch, D. J. McShane, J. F. Fries, N. S. Cooper, L. A. Healey, S. R. Kaplan, M. H. Liang, H. S. Luthra, et al. 1988. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 31:315.
2. Nienhuis, R. L. F., and E. Mandema. 1964. A new serum factor in patients with rheumatoid arthritis: the antiperinuclear factor. Ann. Rheum. Dis. 23:302.
3. Young, B. J. J., R. K. Mallya, R. D. G. Leslie, C. J. M. Clarck, and T. J. Hamblin. 1979. Anti-keratin antibodies in rheumatoid arthritis. Br. Med. J. 2:97.
4. Terato, K., Y. Shimozuru, K. Katayama, Y. Takemitsu, M. Yamashita, K. Miyatsu, K. Fujii, M. Sagara, S. Kobayashi, and M. Goto. 1990. Specificity of antibodies to type II collagen in rheumatoid arthritis. Arthritis Rheum. 33:1493.
5. Steiner, G., K. Harmuth, K. Skriner, I. Maurer-Fogy, A. Sinski, E. Thalmann, W. Hassfeld, A. Barta, and J. S. Smolen. 1992. Purification and partial sequencing of the nuclear autoantigen RA33 shows that it is indistinguishable from the A2 protein of the heterogeneous nuclear ribonucleoprolein complex. J. Clin. Invest. 90:1061.
6. Després, N., G. Boire, F. J. Lopez-Longo, and H.-A. Ménard. 1994. The Sa system: a novel antigen-antibody system specific for rheumatoid arthritis. J. Rheumatol. 21:1027.
7. Mimori, T., K. Suganuma, Y. Tanami, T. Nojima, M. Matsumura, T. Fujii, T. Yoshizawa, K. Suzuki, and M. Akizuki. 1995. Autoantibodies to calpastatin (an endogenous inhibitor for calcium-dependent neutral protease, calpain) in systemic rheumatic diseases. Proc. Natl. Acad. Sci. USA 92:7267.
8. Després. N., G. Talbot, B. PloufFe, G. Boire, and H.-A. Ménard. 1995. Detection and expression of a cDNA clone that encodes a polypeptide containing two inhibitory domains of human calpastatin and its recognition by rheumatoid arthritis sera. J. Clin Invest. 95:1891.
9. Bang, H., J. Mollenhauer, A. Schulmeister, C. Nager, W. van Eden, A. WandWürttenberger, S. H. E. Kaufmann, and K. Brune. 1994. Isolation and characterization of a cartilage-specific membrane antigen (CH65): comparison with cytokeratins and heat-shock proteins. Immunology 81:322.
10. Bläβ, S., C. Specker, H.-J. Lakomek, E. M. Schneider, and M. Schwochau. 1995. Novel 68 kD autoantigen detected by rheumatoid arthritis specific antibodies. Ann. Rheum. Dis. 54:355.
11. Hoet, R. M., and W. J. van Venrooij. 1992. The antiperinuclear factor (APF) and antikeratin antibodies (AKA) in rheumatoid arthritis. In Rheumatoid Arthritis. J.S. Smolen, J.R. Kalden, and R.N. Maini, eds. Springer-Verlag, Berlin/Heidelberg, p. 299.
12. Vincent, C., G. Serre, F. Lapeyre, B. Fournié, C. Ayrolles, A. Fournié, and J.-P. Soleilhavoup. 1989. High diagnostic value in rheumatoid arthritis of antibodies to the stratum corneum of rat œsophagus epithelium, so-called 'antikeratin antibodies'. Ann. Rheum. Dis. 48:712.
13. Gomès-Daudrix, V., M. Sebbag, E. Girbal, C. Vincent, M. Simon, J. Rakotoarivony, M. Abbal, B. Fournié, and G. Serre. 1994. Immunoblotting detection of so-called 'antikeratin antibodies': a new assay for the diagnosis of rheumatoid arthritis. Ann. Rheum. Dis. 53:735.
14. Vincent, C., M. Simon, M. Sebbag, E. Girbal-Neuhauser, J.-J. Durieux, A. Cantagrel, B. Fournié, B. Mazières, and G. Serre. 1998. Immunoblotting detection of autoantibodies to human epidermis filaggrin: a new diagnostic test for rheumatoid arthritis. J Rheumatol. 25:838.
15. Johnson, G. D., A. Carvalho, E. J. Holborow, D. H. Goddard, and G. Russel. 1981. Antiperinuclear factor and keratin antibodies in rheumatoid arthritis. Ann. Rheum. Dis. 40:263.
16. Quismorio, F. P. Jr., R. L. Kaufman, T. Beardmore, and E. S. Mongan. 1983. Reactivity of serum antibodies to the keratin layer of rat esophagus in patients with rheumatoid arthritis. Arthritis Rheum. 26:494.
17. Serre, G., C. Vincent, B. Fournié, F. Lapeyre, J.-P. Soleilhavoup, and A. Fournié. 1986. Anticorps anti-stratum corneum d'œsophage de rat, auto-anticorps anti-kératines épidermiques et anti-épiderme dans la polyarthrite rhumatoïde et différentes affections rhumatologiques. Intérêt diagnostique, aspects fondamentaux. Rev. Rhum. Mal. Osteoartic. 53:607.
18. Simon, M., C. Vincent, M. Haftek, E. Girbal, M. Sebbag, V. Gomès-Daudrix, and G. Serre. 1995. The rheumatoid arthritis-associated autoantibodies to filaggrin label the fibrous matrix of the cornified cells but not the profilaggrin-containing keratohyalin granules in human epidermis. Clin. Exp. Immunol. 100:90.
19. Kirstein, H., and F. K. Mathiesen. 1987. Antikeratin antibodies in rheumatoid arthritis. Scand. J. Rheumatol. 16:331.
20. Paimela, L., M. Gripenberg, P. Kurki, and M. Leirisalo-Repo. 1992. Antikeratin antibodies: diagnostic and prognostic markers for early rheumatoid arthritis. Ann. Rheum. Dis. 51:743.
21. Kurki, P., K. Aho, T. Palosuo, and M. Heliövaara. 1992. Immunopathology of rheumatoid arthritis: antikeratin antibodies precede the clinical disease. Arthritis Rheum. 35:914.
22. Girbal, E., and M. Sebbag, V. Gomès-Daudrix, M. Simon, C. Vincent, and G. Serre. 1993. Characterization of the rat œsophagus epithelium antigens defined by the so-called 'antikeratin antibodies', specific for rheumatoid arthritis. Ann. Rheum. Dis. 52:749.
23. Simon, M., E. Girbal, M. Sebbag, V. Gomès-Daudrix, C. Vincent, G. Salama, and G. Serre. 1993. The cytokeratin filament-aggregating protein filaggrin is the target of the so-called 'antikeratin antibodies', autoantibodies specific for rheumatoid arthritis. J. Clin. Invest. 92:1387.
24. Gan, S.-Q., W. O. McBride, W. W. Idler, N. Markova, and P. M. Steinert. 1990. Organization, structure, and polymorphisms of the human profilaggrin gene. Biochemistry, 29:9432.
25. Dale, B. A., K. A. Resing, and P. V. Haydock. 1990. Filaggrins. In Cellular and Molecular Biology of Intermediate filaments. R. D. Goldman and P. M. Steinert, eds. Plenum, New York/London, p. 393.
26. Harding, C. R., and I. R. Scott. 1983. Histidine-rich proteins (filaggrins): structural and functional heterogeneity during epidermal differentiation. J. Mol. Biol. 170:651.
27. Senshu, T., S. Kan, H. Ogawa, M. Manabe, and H. Asaga. 1996. Preferential deimination of keratin K1 and filaggrin during the terminal differentiation of human epidermis. Biochim. Biophys. Res. Commun. 225:712.
28. Girbal-Neuhauser, E., M. Montézin, F. Croute, M. Sebbag, M. Simon, J.-J. Durieux, and G. Serre. 1997. Normal human epidermal keratinocytes express in vitro specific molecular forms of (pro)filaggrin recognized by rheumatoid arthritis-associated antifilaggrin autoantibodies. Mol. Med. 3:145.
29. Sebbag, M., M. Simon, C. Vincent, C. Masson-Bessière, E. Girbal, J.-J. Durieux, and G. Serre. 1995. The antiperinuclear factor and the so-called antikeratin antibodies are the same rheumatoid arthritis-specific autoantibodies. J. Clin. Invest. 95:2672.
30. Lonsdale-Eccles, J. D., D. C. Teller, and B. A. Dale. 1982. Characterization of a phosphorylated form of the intermediate filament-aggregating protein filaggrin. Biochemistry 21:5940.
31. Scott, I. R., and C. R. Harding. 1981. Studies on the synthesis and degradation of a high molecular weight histidine-rich phosphoprotein from mammalian epidermis. Biochim. Biophys. Acta. 669:65.
32. Simon, M., M. Sebbag, M. Haftek, C. Vincent, E. Girbal-Neuhauser, J. Rakotoarivony, G. Sommé, D. Schmitt, and G. Serre. 1995. Monoclonal antibodies to human epidermal filaggrin, some not recognizing profilaggrin. J. Invest. Dermatol. 105:432.
33. Senshu, T., T. Sato., T. Inoue, K. Akiyama, and H. Asaga. 1992. Detection of citrulline residues in deiminated proteins on polyvinylidene difluoride membrane. Anal. Biochem. 203:94.
34. Senshu, T., K. Akiyama, S. Kan, H. Asaga, A. Ishigami, and M. Manabe. 1995. Detection of deiminated proteins in rat skin: probing with a monospecific antibody after modification of citrulline residues. J. Invest. Dermatol 105:163.
35. McKinley-Grant, L. J., W. W. Idler, I. A. Bernstein, D. A. D. Parry, L. Cannizzaro, C. M. Croce, K. Huebner, S. R. Lessin, and P. M. Steinert. 1989. Characterization of a cDNA clone encoding human filaggrin and localization of the gene to chromosome tq21. Proc. Natl. Acad. Sci. USA 86:4848.
36. Deibel, M. R., T. J. Lobl, and A. W. Yern. 1989. A technique for rapid purification of low yield products: biotinylation of chemically synthesized proteins on-resin. Peptide Res. 2:189.
37. Tarsca, E., L. N. Marekov, G. Mei, G. Melino, S.-C. Lee, and P. M. Steinert. 1996. Protein unfolding by peptidylarginine deiminase: substrate specificity and structural relationships of the natural substrates trichohyalin and filaggrin. J. Biol. Chem. 271:30709.
38. Kubilus, J., R. W. Waitkus, and H. P. Baden. 1980. Partial purification and specificity of an arginine-converting enzyme from bovine epidermis. Biochim. Biophys. Acta 615:246.
39. Schellekens, G. A., B. A. W. de Jong, F. H. J. van den Hoogen, L. B. A. van de Putte, and W. J. van Venrooij. 1998. Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies. J. Clin. Invest. 101:273.
40. Visser, H., G. A. Schellekens, B. A. W. de Jong, W. J. van Venrooij, F. C. Breedveld, and J. M. W. Hazes. 1997. The diagnostic characteristics of a recently developed ELISA for detection of antiperinuclear factor (APF) in an early arthritis population. Arthritis Rheum. 40:S289. (Abstr.).
41. Chan, K.-W. A., D. T. Felson, R. A. Yood, and A. M. Walker. 1993. The lag time between onset of symptoms and diagnosis of rheumatoid arthritis. Arthritis Rheum. 37:814.
42. Boers, M., A. C. Verhoeven, H. M. Markusse, M. A. F. J. van de Laar, R. Westhovens, J. C. van Denderen, D. van Zebben, B. A. C. Dijkmans, A. J. Peeters, P. Jacobs, et al. 1997. Randomised comparison of combined step-down prednisolone, methotrexate and sulphasalazine with sulphasalazine alone in early rheumatoid arthritis. Lancet 350:309.
43. Watanabe, K., K. Akiyama, K. Hikichi, R. Ohtsuka, A. Okuyama, and T. Senshu. 1988. Combined biochemical and immunocytochemical comparison of peptidylarginine deiminases present in various tissues. Biochim. Biophys. Acta 966:375.
44. Terakawa, H., H. Takahara, and K. Sugawara. 1991. Three types of mouse peptidylarginine deiminase: characterization and tissue distribution. J. Biochem. 110: 661.
45. Sugawara, K., Y. Oikawa, and T. Ouchi. 1982. Identification and properties of peptidylarginine deiminase from rabbit skeletal muscle. J. Biochem. 91:1065.
46. Lamensa, J. W. E., and M. A. Moscarello. 1993. Deimination of human myelin basic protein by a peptidylarginine deiminase from bovine brain. J. Neurochem. 61:987.
47. Nagata, S., and T. Senshu. 1990. Peptidylarginine deiminase in rat and mouse hemopoietic cells. Experientia 64:72.
48. Finch, P. P., D. D. Wood, and M. A. Moscarello. 1971. The presence of citrulline in a myelin protein fraction. FEBS Lett. 15:145.
49. Wood, D. D., and M. A. Moscarello. 1989. The isolation, characterization, and lipid-aggregating properties of a citrulline containing myelin basic protein. J. Biol. Chem. 264:5121.
50. Moscarello, M. A., D. D. Wood, C. Ackerley, and C. Boulias. 1994. Myelin in multiple sclerosis is developmentally immature. J. Clin. Invest. 94:146.
51. Mastronardi, F., B. Mak, C. A. Ackerley, B. I. Roots, and M. A. Moscarello. 1996. Modifications of myelin basic protein in DM20 transgenic mice are similar to those in myelin basic protein from multiple sclerosis. J. Clin. Invest. 97:349.
52. Li, S. 1996. Myelin basic protein autoantibodies. In Autoantibodies, J. B. Peter and Y. Shoenfeld, eds. Elsevier Science B.V., Amsterdam, p. 520.
53. Wucherpfennig, K. W., I. Catz, S. Hausmann, J. L. Strominger, L. Steinman, and K. G. Warren. 1997. Recognition of the immunodominant myelin basic protein peptide by autoantibodies and HLA-DR2-restricted T cell clones from multiple sclerosis patients: identity of key contact residues in the B-cell and T-cell epitopes. J. Clin. Invest. 100:1114.
54. Utz, P. J., M. Hottelet, P. H. Schur, and P. Anderson. 1997. Proteins phosphorylated during stress-induced apoptosis are common targets for autoantibody production in patients with systemic lupus erythematosus. J. Exp. Med. 185:843.
55. Girbal-Neuhauser, E., J.-J. Durieux, L. Sailler, G. Salama, C. Masson-Bessière, M. Simon, C. Vincent, and G. Serre. 1997. The epitopes defined by the rheumatoid arthritis-specific antifilaggrin autoantibodies are generated on filaggrin by posttranslational modification. Rev. Rhum. 64:74 (Abstr.).
56. Durieux, J.-J., C. Vincent, M. Sebbag, E. Girbal-Neuhauser, and G. Serre. 1997. Identification of two major epitopes targetted by the rheumatoid arthritis-specific anti-filaggrin autoantibodies. Rev. Rhum. 64:601 (Abstr.).