Endoglycosidase treatment abrogates IgG arthritogenicity: Importance of IgG glycosylation in arthritis

European Journal of Immunology

Volumn 37, Issue 10, 2007, Pages 2973-2982

  Nandakumar, Kutty Selva ^a   Collin, Mattias ^a   Olsén, Arne ^a   Nimmerjahn, Falk ^b,c   Blom, Anna M ^a   Ravetch, Jeffrey V ^b   Holmdahl, Rikard ^a  

^a LUND UNIVERSITY   (Sweden)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Arthritis; EndoS; IgG

Indexed keywords

ASPARAGINE; COLLAGEN TYPE 2; ENDOGLYCOSIDASE; FC RECEPTOR; GLYCAN; GLYCOSIDASE; IMMUNOGLOBULIN G; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANTIGEN ANTIBODY COMPLEX; ANTIGEN BINDING; ARTHRITIS; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; GLYCOSYLATION; IN VIVO STUDY; NEWBORN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT; RECEPTOR BINDING;

ACUTE DISEASE; ANIMALS; ANTIBODIES, MONOCLONAL; ARTHRITIS, EXPERIMENTAL; BACTERIAL PROTEINS; CARBOHYDRATE METABOLISM; COLLAGEN TYPE II; GLYCOSIDE HYDROLASES; GLYCOSYLATION; IMMUNOGLOBULIN G; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; RATS; SEVERITY OF ILLNESS INDEX; STREPTOCOCCUS PYOGENES;

EID: 35348875440     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200737581     Document Type: Article

References (68)

1. Jefferis, R., Glycosylation of recombinant antibody therapeutics. Biotechnol. Prog. 2005. 21: 11-16.
2. Arnold, J. N., Wormald, M. R., Sim, R. B., Rudd, P. M. and Dwek, R. A., The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu. Rev. Immunol. 2007. 25: 21-50.
3. Deisenhofer, J., Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9- and 2.8-A resolution. Biochemistry 1981. 20: 2361-2370.
4. Sutton, B. J. and Phillips, D. C., The three-dimensional structure of the carbohydrate within the Fc fragment of immunoglobulin G. Biochem. Soc. Trans. 1983. 11: 130-132.
5. Mizuochi, T., Hamako, J. and Titani, K., Structures of the sugar chains of mouse immunoglobulin G. Arch. Biochem. Biophys. 1987. 257: 387-394.
6. Parekh, R. B., Dwek, R. A., Sutton, B. J., Fernandes, D. L., Leung, A., Stanworth, D., Rademacher, T. W. et al., Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature 1985. 316: 452-457.
7. Burton, D. R. and Woof, J. M., Human antibody effector function. Adv. Immunol. 1992. 51: 1-84.
8. Jefferis, R., Lund, J. and Pound, J. D., IgG-Fc-mediated effector functions: Molecular definition of interaction sites for effector ligands and the role of glycosylation. Immunol. Rev. 1998. 163: 59-76.
9. Matsuda, H., Nakamura, S., Ichikawa, Y., Kozai, K., Takano, R., Nose, M., Endo, S., Nishimura, Y. and Arata, Y., Proton nuclear magnetic resonance studies of the structure of the Fc fragment of human immunoglobulin G1: Comparisons of native and recombinant proteins. Mol. Immunol. 1990. 27: 571-579.
10. Malhotra, R., Wormald, M. R., Rudd, P. M., Fischer, P. B., Dwek, R. A. and Sim, R. B., Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat. Med. 1995. 1: 237-243.
11. Wormald, M. R., Rudd, P. M., Harvey, D. J., Chang, S. C., Scragg, I. G. and Dwek, R. A., Variations in oligosaccharide-protein interactions in immunoglobulin G determine the site-specific glycosylation profiles and modulate the dynamic motion of the Fc oligosaccharides. Biochemistry 1997. 36: 1370-1380.
12. Bond, A., Jones, M. G. and Hay, F. C., Human IgG preparations isolated by ion-exchange or protein G affinity chromatography differ in their glycosylation profiles. J. Immunol. Methods 1993. 166: 27-33.
13. Boyd, P. N., Lines, A. C. and Patel, A. K., The effect of the removal of sialic acid, galactose and total carbohydrate on the functional activity of Campath-1H. Mol. Immunol. 1995. 32: 1311-1318.
14. Jefferis, R., Lund, J. and Goodall, M., Recognition sites on human IgG for Fc gamma receptors: The role of glycosylation. Immunol. Lett. 1995. 44: 111-117.
15. Lund, J., Takahashi, N., Goodall, M., Pound, J. D. and Jefferis, R., Oligosaccharide-protein interactions in IgG antibody molecules: Structural and functional consequences. Biochem. Soc. Trans. 1995. 23: 102S.
16. Lund, J., Takahashi, N., Pound, J. D., Goodall, M. and Jefferis, R., Multiple interactions of IgG with its core oligosaccharide can modulate recognition by complement and human Fc gamma receptor I and influence the synthesis of its oligosaccharide chains. J. Immunol. 1996. 157: 4963-4969.
17. Wright, A. and Morrison, S. L., Effect of glycosylation on antibody function: Implications for genetic engineering. Trends Biotechnol. 1997. 15: 26-32.
18. Leatherbarrow, R. J. and Dwek, R. A., The effect of aglycosylation on the binding of mouse IgG to staphylococcal protein A. FEBS Lett. 1983. 164: 227-230.
19. Nose, M. and Wigzell, H., Biological significance of carbohydrate chains on monoclonal antibodies. Proc. Natl. Acad. Sci. USA 1983. 80: 6632-6636.
20. Leatherbarrow, R. J., Rademacher, T. W., Dwek, R. A., Woof, J. M., Clark, A., Burton, D. R., Richardson, N. and Feinstein, A., Effector functions of a monoclonal aglycosylated mouse IgG2a: Binding and activation of complement component C1 and interaction with human monocyte Fc receptor. Mol. Immunol. 1985. 22: 407-415.
21. Tao, M. H. and Morrison, S. L., Studies of aglycosylated chimeric mouse-human IgG. Role of carbohydrate in the structure and effector functions mediated by the human IgG constant region. J. Immunol. 1989. 143: 2595-2601.
22. Tsuchiya, N., Endo, T., Matsuta, K., Yoshinoya, S., Aikawa, T., Kosuge, E., Takeuchi, F. et al., Effects of galactose depletion from oligosaccharide chains on immunological activities of human IgG. J. Rheumatol. 1989. 16: 285-290.
23. Nechansky, A., Schuster, M., Jost, W., Siegl, P., Wiederkum, S., Gorr, G. and Kircheis, R., Compensation of endogenous IgG mediated inhibition of antibody-dependent cellular cytotoxicity by glyco-engineering of therapeutic antibodies. Mol. Immunol. 2007. 44: 1815-1817.
24. Wright, A. and Morrison, S. L., Antibody variable region glycosylation: Biochemical and clinical effects. Springer Semin. Immunopathol. 1993. 15: 259-273.
25. Endo, T., Wright, A., Morrison, S. L. and Kobata, A., Glycosylation of the variable region of immunoglobulin G - Site specific maturation of the sugar chains. Mol. Immunol. 1995. 32: 931-940.
26. Leibiger, H., Wustner, D., Stigler, R. D. and Marx, U., Variable domain-linked oligosaccharides of a human monoclonal IgG: Structure and influence on antigen binding. Biochem. J. 1999. 338 (Pt 2): 529-538.
27. Parekh, R. B., Roitt, I. M., Isenberg, D. A., Dwek, R. A., Ansell, B. M. and Rademacher, T. W., Galactosylation of IgG associated oligosaccharides: Reduction in patients with adult and juvenile onset rheumatoid arthritis and relation to disease activity. Lancet 1988. 1: 966-969.
28. Collin, M. and Olsen, A., EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J. 2001. 20: 3046-3055.
29. Collin, M., Svensson, M. D., Sjoholm, A. G., Jensenius, J. C., Sjobring, U. and Olsen, A., EndoS and SpeB from Streptococcus pyogenes inhibit immunoglobulin-mediated opsonophagocytosis. Infect. Immun. 2002. 70: 6646-6651.
30. Terato, K., Hasty, K A., Reffe, R. A., Cremer, M. A., Kang, A. H. and Stuart, J. M., Induction of arthritis with monoclonal antibodies to collagen. J. Immunol. 1992. 148: 2103-2108.
31. Terato, K., Harper, D. S., Griffiths, M. M., Hasty, D. L., Ye, X. J., Cremer, M. A. and Seyer, J. M., Collagen-induced arthritis in mice: Synergistic effect of E. coli lipopolysaccharide bypasses epitope specificity in the induction of arthritis with monoclonal antibodies to type II collagen. Autoimmunity 1995. 22: 137-147.
32. Nandakumar, K. S., Svensson, L. and Holmdahl, R., Collagen type IT-specific monoclonal antibody-induced arthritis in mice: Description of the disease and the influence of age, sex, and genes. Am. J. Pathol. 2003. 163: 1827-1837.
33. Nandakumar, K. S. and Holmdahl, R., Efficient promotion of collagen antibody induced arthritis (CAIA) using four monoclonal antibodies specific for the major epitopes recognized in both collagen induced arthritis and rheumatoid arthritis. J. Immunol. Methods 2005. 304: 126-136.
34. Hietala, M. A., Nandakumar, K S., Persson, L., Fahlen, S., Holmdahl, R. and Pekna, M., Complement activation by both classical and alternative pathways is critical for the effector phase of arthritis. Eur. J. Immunol. 2004. 34: 1208-1216.
35. Kagari, T., Tanaka, D., Doi, H. and Shimozato, T., Essential role of Fc gamma receptors in anti-type II collagen antibody-induced arthritis. J. Immunol. 2003. 170: 4318-4324.
36. Nandakumar, K. S., Andren, M., Martinsson, P., Bajtner, E., Hellstrom, S., Holmdahl, R. and Kleinau, S., Induction of arthritis by single monoclonal IgG anti-collagen type II antibodies and enhancement of arthritis in mice lacking inhibitory FcgammaRIIB. Eur. J. Immunol. 2003. 33: 2269-2277.
37. Kagari, T., Doi, H. and Shimozato, T., The importance of IL-1 beta and TNF-alpha, and the noninvolvement of IL-6, in the development of monoclonal antibody-induced arthritis. J. Immunol. 2002. 169: 1459-1466.
38. Collin, M. and Fischetti, V. A., A novel secreted endoglycosidase from Enterococcus faecalis with activity on human immunoglobulin G and ribonuclease B. J. Biol. Chem. 2004. 279: 22558-22570.
39. Nandakumar, K. S. and Holmdahl, R., Antibody-induced arthritis: Disease mechanisms and genes involved at the effector phase of arthritis. Arthritis Res. Ther. 2007. 8: 223-233.
40. Winkelhake, J. L., Kunicki, T. J., Elcombe, B. M. and Aster, R. H., Effects of pH treatments and deglycosylation of rabbit immunoglobulin G on the binding of C1q. J. Biol. Chem. 1980. 255: 2822-2828.
41. Taves, C. J., Kusumi, A. and Winkelhake, J. L., Human aglycosyl-IgG exhibits increased hydrophobicity. Binding/fluorescence studies with 8-anilinonaphthalene-1-sulfonic acid (ANS). Biochem. Biophys. Res. Commun. 1984. 124: 605-613.
42. Holmdahl, R., Mo, J. A., Jonsson, R., Karlstrom, K. and Scheynius, A., Multiple epitopes on cartilage type II collagen are accessible for antibody binding in vivo. Autoimmunity 1991. 10: 27-34.
43. Amirahmadi, S. F., Whittingham, S., Crumble, D. E., Nandakumar, K. S., Holmdahl, R., Mackay, I. R., van Damme, M. P. and Rowley, M. J., Arthritogenic anti-type II collagen antibodies are pathogenic for cartilage-derived chondrocytes independent of inflammatory cells. Arthritis Rheum. 2005. 52: 1897-1906.
44. Carlsen, S., Nandakumar, K. S. and Holmdahl, R., Type IX collagen deficiency enhances the binding of cartilage-specific antibodies and arthritis severity. Arthritis Res. Ther. 2006. 8: R102-R109.
45. Wipke, B. T., Wang, Z., Nagengast, W., Reichert, D. E. and Allen, P. M., Staging the initiation of autoantibody-induced arthritis: A critical role for immune complexes. J. Immunol. 2004. 172: 7694-7702.
46. Moller, N. P. and Steensgaard, J., Fc-mediated immune precipitation. II. Analysis of precipitating immune complexes by rate-zonal ultracentrifugation. Immunology 1979. 38: 641-648.
47. Moller, N. P. and Christiansen, G., Fc-mediated immune precipitation. III. Visualization by electron microscopy. Immunology 1983. 48: 469-476.
48. Easterbrook-Smith, S. B., Vandenberg, R. J. and Alden, J. R., The role of Fc:FC interactions in insoluble immune complex formation and complement activation. Mol. Immunol. 1988. 25: 1331-1337.
49. Parekh, R., Isenberg, D., Rook, G., Roitt, I., Dwek, R. and Rademacher, T., A comparative analysis of disease-associated changes in the galactosylation of serum IgG. J. Autoimmun. 1989. 2: 101-114.
50. Rook, G. A., Steele, J., Brealey, R., Whyte, A., Isenberg, D., Sumar, N., Nelson, J. L. et al., Changes in IgG glycoform levels are associated with remission of arthritis during pregnancy. J. Autoimmun. 1991. 4: 779-794.
51. Parekh, R., Roitt, I., Isenberg, D., Dwek, R. and Rademacher, T., Age-related galactosylation of the N-linked oligosaccharides of human serum IgG. J. Exp. Med. 1988. 167: 1731-1736.
52. Yamada, E., Tsukamoto, Y., Sasaki, R., Yagyu, K. and Takahashi, N., Structural changes of immunoglobulin G oligosaccharides with age in healthy human serum. Glycoconj. J. 1997. 14: 401-405.
53. Kuroki, A., Shibata, T., Honda, H., Totsuka, D., Kobayashi, K. and Sugisaki, T., Glomerular and serum IgG subclasses in diffuse proliferative lupus nephritis, membranous lupus nephritis, and idiopathic membranous nephropathy. Intern. Med. 2002. 41: 936-942.
54. Kuroda, Y., Nakata, M., Nose, M., Kojima, N. and Mizuochi, T., Abnormal IgG galactosylation and arthritis in MRL-Fas(1pr) or MRL-FasL(gld) mice are under the control of the MRL genetic background. FEBS Lett. 2001. 507: 210-214.
55. Kuroda, Y., Nakata, M., Hirose, S., Shirai, T., Iwamoto, M., Izui, S., Kojima, N. and Mizuochi, T., Abnormal IgG galactosylation in MRL-1pr/1pr mice: Pathogenic role in the development of arthritis. Pathol. Int. 2001. 51: 909-915.
56. Shikata, K., Yasuda, T., Takeuchi, F., Konishi, T., Nakata, M. and Mizuochi, T., Structural changes in the oligosaccharide moiety of human IgG with aging. Glycoconj. J. 1998. 15: 683-689.
57. Nimmerjahn, F., Anthony, R. M. and Ravetch, J. V., Agalactosylated IgG antibodies depend on cellular Fc receptors for in vivo activity. Proc. Natl. Acad. Sci. USA 2007. 104: 8433-8437
58. Sarmay, G., Lund, J., Rozsnyay, Z., Gergely, J. and Jefferis, R., Mapping and comparison of the interaction sites on the Fc region of IgG responsible for triggering antibody dependent cellular cytotoxicity (ADCC) through different types of human Fc gamma receptor. Mol. Immunol. 1992. 29: 633-639.
59. Pound, J. D., Lund, J. and Jefferis, R., Aglycosylated chimaeric human IgG3 can trigger the/human phagocyte respiratory burst. Mol. Immunol. 1993. 30: 233-241.
60. Mimura, Y., Church, S., Ghirlando, R., Ashton, P. R., Dong, S., Goodall, M., Lund, J. and Jefferis, R., The influence of glycosylation on the thermal stability and effector function expression of human IgG1-Fc: Properties of a series of truncated glycoforms. Mol. Immunol. 2000. 37: 697-706.
61. Walker, M. R., Lee, J. and Jefferis, R., Immunogenicity and antigenicity of immunoglobulins: Detection of human immunoglobulin light-chain carbohydrate, using concanavalin A. Biochim. Biophys. Acta 1987. 915: 314-320.
62. Kaneko, Y., Nimmerjahn, F. and Ravetch, J. V., Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 2006. 313: 670-673.
63. Baudino, L., Azeredo da Silveira, S., Nakata, M. and Izui, S., Molecular and cellular basis for pathogenicity of autoantibodies: Lessons from murine monoclonal autoantibodies. Springer Semin. Immunopathol. 2006. 28: 175-184.
64. Holmdahl, R., Rubin, K., Klareskog, L., Larsson, E. and Wigzell, H., Characterization of the antibody response in mice with type II collagen-induced arthritis, using monoclonal anti-type II collagen antibodies. Arthritis Rheum. 1986. 29: 400-410.
65. Schulte, S., Unger, C., Mo, J. A., Wendler, O., Bauer, E., Frischholz, S., von der Mark K., Kalden, J. R. et al., Arthritis-related B cell epitopes in collagen II are conformation-dependent and sterically privileged in accessible sites of cartilage collagen fibrils. J. Biol. Chem. 1998. 273: 1551-1561.
66. Collin, M. and Olsen, A., Effect of SpeB and EndoS from Streptococcus pyogenes on human immunoglobulins. Infect. Immun. 2001. 69: 7187-7189.
67. Nimmerjahn, F., Bruhns, P., Horiuchi, K. and Ravetch, J. V., FcgammaRIV: A novel FcR with distinct IgG subclass specificity. Immunity 2005. 23: 41-51.
68. Holmdahl, R., Carlsen, S., Mikulowska, A., Vestberg, M., Brunsberg, U., Hansson, A.-S., Sundvall, M. et al., Genetic analysis of murine models for rheumatoid arthritis.In Adolpho, K. (Ed.) Human Genome Methods. CRC Press, New York 1998, pp 215-238.