Altered glycosylation of complexed native IgG molecules is associated with disease activity of systemic lupus erythematosus

Lupus

Volumn 24, Issue 6, 2015, Pages 569-581

  Sjowall C ^a   Zapf, J ^b   Von Lohneysen S ^a,b   Magorivska, I ^b,c   Biermann, M ^b   Janko, C ^b,d   Winkler, S ^b   Bilyy, R ^c   Schett, G ^b   Herrmann, Martin ^b   Munoz L E ^b  

^a LINKÖPING UNIVERSITY   (Sweden)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c INSTITUTE OF CELL BIOLOGY   (Ukraine)

^d UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

Aleura aurantia; glycosylation; IgG; immune complex; lectin ELISA; Lens culinaris; physicians global assessment; SLEDAI

Indexed keywords

AGGLUTININ; C REACTIVE PROTEIN; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3C; GLYCAN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LECTIN; ANTIGEN ANTIBODY COMPLEX; COMPLEMENT; LECTIN, ALEURIA AURANTIA;

ADULT; ARTICLE; BINDING SITE; BLOOD ANALYSIS; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; ELLIPSOMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FUCOSYLATION; GLYCOSYLATION; HUMAN; LENTIL; MALE; MIDDLE AGED; PREDICTIVE VALUE; PRIORITY JOURNAL; REMISSION; SLEDAI; SYSTEMIC LUPUS ERYTHEMATOSUS; YOUNG ADULT; ADOLESCENT; ANTIGEN ANTIBODY COMPLEX; BLOOD; IMMUNOLOGY; METABOLISM; PROCEDURES;

ADOLESCENT; ADULT; ANTIGEN-ANTIBODY COMPLEX; C-REACTIVE PROTEIN; COHORT STUDIES; COMPLEMENT C1Q; COMPLEMENT SYSTEM PROTEINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN G; LECTINS; LENS PLANT; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; PREDICTIVE VALUE OF TESTS; YOUNG ADULT;

EID: 84928045896     PISSN: 09612033     EISSN: 14770962     Source Type: Journal    
DOI: 10.1177/0961203314558861     Document Type: Article

References (49)

1. Elkon K, Casali P. Nature and functions of autoantibodies. Nat Clin Pract Rheumato. 2008 ; 4: 491-498
2. Munoz LE, Lauber K, Schiller M, Manfredi AA, Herrmann M. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat Rev Rheumatol. 2010 ; 6: 280-289
3. Skogh T, Stendahl O. Complement-mediated delay in immune complex clearance from the blood owing to reduced deposition outside the reticuloendothelial system. Immunology. 1983 ; 49: 53-59
4. Johansson AG, Lovdal T, Magnusson KE, Berg T, Skogh T. Liver cell uptake and degradation of soluble immunoglobulin G immune complexes in vivo and in vitro in rats. Hepatology (Baltimore, MD). 1996 ; 24: 169-175
5. Sjowall C, Olin AI, Skogh T, et al. C-reactive protein, immunoglobulin G and complement co-localize in renal immune deposits of proliferative lupus nephritis. Autoimmunity. 2013 ; 46: 205-214
6. Munoz LE, Janko C, Grossmayer GE, et al. Remnants of secondarily necrotic cells fuel inflammation in systemic lupus erythematosus. Arthritis Rheum. 2009 ; 60: 1733-1742
7. Munoz LE, Janko C, Chaurio RA, Schett G, Gaipl US, Herrmann M. IgG opsonized nuclear remnants from dead cells cause systemic inflammation in SLE. Autoimmunity. 2010 ; 43: 232-235
8. Jefferis R, Lund J, Pound JD. 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. Wuhrer M, Stam JC, van de Geijn FE, et al. Glycosylation profiling of immunoglobulin G (IgG) subclasses from human serum. Proteomics. 2007 ; 7: 4070-4081
10. Wang J, Balog CI, Stavenhagen K, et al. Fc-glycosylation of IgG1 is modulated by B-cell stimuli. MCP. 2011 ; 10: M110.004655
11. Huhn C, Selman MH, Ruhaak LR, Deelder AM, Wuhrer M. IgG glycosylation analysis. Proteomics. 2009 ; 9: 882-913
12. Arnold JN, Wormald MR, Sim RB, Rudd PM, Dwek RA. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev Immunol. 2007 ; 25: 21-50
13. Qian J, Liu T, Yang L, Daus A, Crowley R, Zhou Q. Structural characterization of N-linked oligosaccharides on monoclonal antibody cetuximab by the combination of orthogonal matrix-assisted laser desorption/ionization hybrid quadrupole-quadrupole time-of-flight tandem mass spectrometry and sequential enzymatic digestion. Anal Biochem. 2007 ; 364: 8-18
14. Molinari M. N-glycan structure dictates extension of protein folding or onset of disposal. Nature Chem Biol. 2007 ; 3: 313-320
15. Aebi M, Bernasconi R, Clerc S, Molinari M. N-glycan structures: recognition and processing in the ER. Trends Biochem Sci. 2010 ; 35: 74-82
16. Nandakumar KS, Collin M, Olsen A, et al. Endoglycosidase treatment abrogates IgG arthritogenicity: importance of IgG glycosylation in arthritis. Eur J Immunol. 2007 ; 37: 2973-2982
17. Siberil S, de Romeuf C, Bihoreau N, et al. Selection of a human anti-RhD monoclonal antibody for therapeutic use: impact of IgG glycosylation on activating and inhibitory Fc gamma R functions. Clin Immunol. 2006 ; 118: 170-179
18. Peipp M, Lammerts van Bueren JJ, Schneider-Merck T, et al. Antibody fucosylation differentially impacts cytotoxicity mediated by NK and PMN effector cells. Blood. 2008 ; 112: 2390-2399
19. Anthony RM, Nimmerjahn F. The role of differential IgG glycosylation in the interaction of antibodies with FcgammaRs in vivo. Curr Opin Organ Transplant. 2011 ; 16: 7-14
20. Umana P, Jean-Mairet J, Moudry R, Amstutz H, Bailey JE. Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nature Biotechnol. 1999 ; 17: 176-180
21. Shields RL, Lai J, Keck R, et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem. 2002 ; 277: 26733-26740
22. Williams PJ, Arkwright PD, Rudd P, et al. Short communication: selective placental transport of maternal IgG to the fetus. Placenta. 1995 ; 16: 749-756
23. Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science. 2006 ; 313: 670-673
24. Chen S, Lu C, Gu H, et al. Aleuria Aurantia Lectin (AAL)-reactive immunoglobulin G rapidly appears in sera of animals following antigen exposure. PloS One. 2012 ; 7: e44422
25. Tan EM, Cohen AS, Fries JF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis and rheumatism. 1982 ; 25: 1271-1277
26. Petri M, Orbai AM, Alarcon GS, et al. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 2012 ; 64: 2677-2686
27. Gladman DD, Ibanez D, Urowitz MB. Systemic lupus erythematosus disease activity index 2000. J Rheumatol. 2002 ; 29: 288-291
28. Elwing H. Protein absorption and ellipsometry in biomaterial research. Biomaterials. 1998 ; 19: 397-406
29. Sjowall C, Wettero J, Bengtsson T, et al. Solid-phase classical complement activation by C-reactive protein (CRP) is inhibited by fluid-phase CRP-C1q interaction. Biochem Biophys Res Commun. 2007 ; 352: 251-258
30. Skoglund C, Wettero J, Skogh T, Sjowall C, Tengvall P, Bengtsson T. C-reactive protein and C1q regulate platelet adhesion and activation on adsorbed immunoglobulin G and albumin. Immunol Cell Biol. 2008 ; 86: 466-474
31. Lood C, Allhorn M, Lood R, et al. IgG glycan hydrolysis by endoglycosidase S diminishes the proinflammatory properties of immune complexes from patients with systemic lupus erythematosus: a possible new treatment?. Arthritis Rheum. 2012 ; 64: 2698-2706
32. Forger F, Matthias T, Oppermann M, Becker H, Helmke K. Clinical significance of anti-dsDNA antibody isotypes: IgG/IgM ratio of anti-dsDNA antibodies as a prognostic marker for lupus nephritis. Lupus. 2004 ; 13: 36-44
33. Gaipl US, Munoz LE, Grossmayer G, et al. Clearance deficiency and systemic lupus erythematosus (SLE). J Autoimmun. 2007 ; 28: 114-121
34. Baumann I, Kolowos W, Voll RE, et al. Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum. 2002 ; 46: 191-201
35. Munoz LE, Janko C, Schulze C, et al. Autoimmunity and chronic inflammation - two clearance-related steps in the etiopathogenesis of SLE. Autoimmun Rev. 2010 ; 10: 38-42
36. Albert H, Collin M, Dudziak D, Ravetch JV, Nimmerjahn F. In vivo enzymatic modulation of IgG glycosylation inhibits autoimmune disease in an IgG subclass-dependent manner. Proc Nat Acad Sci. 2008 ; 105: 15005-15009
37. Van Beneden K, Coppieters K, Laroy W, et al. Reversible changes in serum immunoglobulin galactosylation during the immune response and treatment of inflammatory autoimmune arthritis. Ann Rheum Dis. 2009 ; 68: 1360-1365
38. Gornik I, Maravic G, Dumic J, Flogel M, Lauc G. Fucosylation of IgG heavy chains is increased in rheumatoid arthritis. Clin Biochem. 1999 ; 32: 605-608
39. van de Geijn FE, Wuhrer M, Selman MH, et al. Immunoglobulin G galactosylation and sialylation are associated with pregnancy-induced improvement of rheumatoid arthritis and the postpartum flare: results from a large prospective cohort study. Arthritis Res Ther. 2009 ; 11: R193
40. Bilyy R, Stoika R. Search for novel cell surface markers of apoptotic cells. Autoimmunity. 2007 ; 40: 249-253
41. Bilyy RO, Shkandina T, Tomin A, et al. Macrophages discriminate glycosylation patterns of apoptotic cell-derived microparticles. J Biol Chem. 2012 ; 287: 496-503
42. Blaess S, Kammerer RA, Hall H. Structural analysis of the sixth immunoglobulin-like domain of mouse neural cell adhesion molecule L1 and its interactions with alpha(v)beta3, alpha(IIb)beta3, and alpha5beta1 integrins. J Neurochem. 1998 ; 71: 2615-2625
43. Gornik O, Lauc G. Glycosylation of serum proteins in inflammatory diseases. Dis Markers. 2008 ; 25: 267-278
44. Raju TS. Terminal sugars of Fc glycans influence antibody effector functions of IgGs. Curr Opin Immunol. 2008 ; 20: 471-478
45. Swaak AJ, van Rooyen A, Vogelaar C, Pillay M, Hack E. Complement (C3) metabolism in systemic lupus erythematosus in relation to the disease course. Rheumatol Int. 1986 ; 6: 221-226
46. Satoh M, Iida S, Shitara K. Non-fucosylated therapeutic antibodies as next-generation therapeutic antibodies. Expert Opin Biol Ther. 2006 ; 6: 1161-1173
47. Zhou Q, Shankara S, Roy A, et al. Development of a simple and rapid method for producing non-fucosylated oligomannose containing antibodies with increased effector function. Biotechnol Bioeng. 2008 ; 99: 652-665
48. Wright A, Sato Y, Okada T, Chang K, Endo T, Morrison S. In vivo trafficking and catabolism of IgG1 antibodies with Fc associated carbohydrates of differing structure. Glycobiology. 2000 ; 10: 1347-1355
49. Saevarsdottir S, Steinsson K, Ludviksson BR, Grondal G, Valdimarsson H. Mannan-binding lectin may facilitate the clearance of circulating immune complexes-implications from a study on C2-deficient individuals. Clin Exp Immunol. 2007 ; 148: 248-253