Antibody glycosylation and inflammation

Antibodies

Volumn 2, Issue 3, 2013, Pages 392-414

  Shade, Kai Ting C ^a   Anthony, Robert M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

ADCC; Anti inflammatory; Immunoglobulin

Indexed keywords

ALPHA 1, 3 FUCOSYLTRANSFERASE; ANTIBODY; CETUXIMAB; COMPLEMENT COMPONENT C1Q; DECTIN 1; FC RECEPTOR; GLYCAN; IMMUNOGLOBULIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INFLIXIMAB; INTERLEUKIN 6; METHOTREXATE; RITUXIMAB; TRASTUZUMAB; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIINFLAMMATORY ACTIVITY; ANTIVIRAL ACTIVITY; AUTOIMMUNE DISEASE; BREAST METASTASIS; COMPLEMENT DEPENDENT CYTOTOXICITY; DEMYELINATING NEUROPATHY; DRUG MEGADOSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FOLLICULAR LYMPHOMA; GLYCOSYLATION; HUMAN; IMMUNE COMPLEX NEPHRITIS; IMMUNOPATHOLOGY; IMMUNOTHROMBOCYTOPENIA; INFLAMMATION; METASTATIC COLORECTAL CANCER; MULTIPLE SCLEROSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW; RHEUMATOID ARTHRITIS; SIALYLATION; SYSTEMIC LUPUS ERYTHEMATOSUS; X RAY CRYSTALLOGRAPHY;

EID: 84911946438     PISSN: 20734468     EISSN: None     Source Type: Journal    
DOI: 10.3390/antib2030392     Document Type: Review

References (124)

1. Chang, T. W.; Wu, P. C.; Hsu, C. L.; Hung, A. F. Anti-IgE Antibodies for the treatment of IgE-mediated allergic diseases. Adv Immunol. 2007, 93, 63-119.
2. Kempeni, J. Preliminary results of early clinical trials with the fully human anti-TNFα monoclonal antibody D2E7. Ann. Rheum. Dis. 1999, 58, I70-I72.
3. Maini, R.; St Clair, E. W.; Breedveld, F.; Furst, D.; Kalden, J.; Weisman, M.; Smolen, J.; Emery, P.; Harriman, G.; Feldmann, M.; et al. Infliximab (chimeric anti-tumour necrosis factor α monoclonal antibody) versus placebo in rheumatoid arthritis patients receiving concomitant methotrexate: A randomised phase III trial. Lancet 1999, 354, 1932-1939.
4. Targan, S. R. S.; Hanauer, S. B. S.; van Deventer, S. J. S.; Mayer, L. L.; Present, D. H. D.; Braakman, T. T.; DeWoody, K. L. K.; Schaible, T. F. T.; Rutgeerts, P. J. P. A short-term study of chimeric monoclonal antibody cA2 to tumor necrosis factor alpha for Crohn"s disease. Crohn"s Disease cA2 Study Group. N. Engl. J. Med. 1997, 337, 1029-1035.
5. Hudis, C. A. Trastuzumab-Mechanism of action and use in clinical practice. N. Engl. J. Med. 2007, 357, 39-51.
6. Maloney, D. G.; Grillo-López, A. J.; White, C. A.; Bodkin, D.; Schilder, R. J.; Neidhart, J. A.; Janakiraman, N.; Foon, K. A.; Liles, T. M.; Dallaire, B. K.; et al. IDEC-C2B8 (Rituximab) anti-CD20 monoclonal antibody therapy in patients with relapsed low-grade non-Hodgkin's lymphoma. Blood 1997, 90, 2188-2195.
7. Scott, A. M.; Wolchok, J. D.; Old, L. J. Antibody therapy of cancer. Nat. Rev. Cancer 2012, 12, 278-287.
8. Harris, L. J. L.; Larson, S. B. S.; Hasel, K. W. K.; Day, J. J.; Greenwood, A. A.; McPherson, A. A. The three-dimensional structure of an intact monoclonal antibody for canine lymphoma. Nature 1992, 360, 369-372.
9. Schroeder, H. W., Jr, Cavacini, L. Structure and function of immunoglobulins. J. Allergy Clin. Immunol. 2010, 125, S41-S52.
10. Gould, H. J.; Sutton, B. J.; Beavil, A. J.; Beavil, R. L.; McCloskey, N.; Coker, H. A.; Fear, D.; Smurthwaite, L. The biology of IGE and the basis of allergic disease. Annu. Rev. Immunol. 2003, 21, 579-628.
11. Daëron, M. Fc receptor biology. Annu. Rev. Immunol. 1997, 15, 203-234.
12. Takai, T. Roles of Fc receptors in autoimmunity. Nat. Rev. Immunol. 2002, 2, 580-592.
13. Nimmerjahn, F.; Ravetch, J. V. Fcγ receptors as regulators of immune responses. Nat. Rev. Immunol. 2008, 8, 34-47.
14. Nimmerjahn, F.; Ravetch, J. V. Antibody_mediated modulation of immune responses. Immunol. Rev. 2010, 236, 265-275.
15. Schwab, I.; Nimmerjahn, F. Intravenous immunoglobulin therapy: How does IgG modulate the immune system? Nat. Rev. Immunol. 2013, 13, 176-189.
16. Nimmerjahn, F.; Ravetch, J. V. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 2005, 310, 1510-1512.
17. Wu, J.; Edberg, J. C.; Redecha, P. B.; Bansal, V.; Guyre, P. M.; Coleman, K.; Salmon, J. E.; Kimberly, R. P. A novel polymorphism of FcgammaRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. J. Clin. Invest. 1997, 100, 1059-1070.
18. Shields, R. L.; Namenuk, A. K.; Hong, K.; Meng, Y. G.; Rae, J.; Briggs, J.; Xie, D.; Lai, J.; Stadlen, A.; Li, B.; et al. High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fc gamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R. J. Biol. Chem. 2001, 276, 6591-6604.
19. Koene, H. R. H.; Kleijer, M. M.; Algra, J. J.; Roos, D. D.; von dem Borne, A. E. A.; de Haas, M. M. Fc gammaRIIIa-158V/F polymorphism influences the binding of IgG by natural killer cell Fc gammaRIIIa, independently of the Fc gammaRIIIa-48L/R/H phenotype. Blood 1997, 90, 1109-1114.
20. Warmerdam, P. A. P.; van de Winkel, J. G. J.; Vlug, A. A.; Westerdaal, N. A. N.; Capel, P. J. P. A single amino acid in the second Ig-like domain of the human Fc gamma receptor II is critical for human IgG2 binding. J. Immunol. 1991, 147, 1338-1343.
21. Parren, P. W.; Warmerdam, P. A.; Boeije, L. C.; Arts, J.; Westerdaal, N. A.; Vlug, A.; Capel, P. J.; Aarden, L. A.; van de Winkel, J. G. On the interaction of IgG subclasses with the low affinity Fc gamma RIIa (CD32) on human monocytes, neutrophils, and platelets. Analysis of a functional polymorphism to human IgG2. J. Clin. Invest. 1992, 90, 1537-1546.
22. Musolino, A.; Naldi, N.; Bortesi, B.; Pezzuolo, D.; Capelletti, M.; Missale, G.; Laccabue, D.; Zerbini, A.; Camisa, R.; Bisagni, G.; et al. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer. J. Clin. Oncol. 2008, 26, 1789-1796.
23. Weng, W.-K. W.; Levy, R. R. Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J. Clin. Oncol. 2003, 21, 3940-3947.
24. Tamura, K.; Shimizu, C.; Hojo, T.; Akashi-Tanaka, S.; Kinoshita, T.; Yonemori, K.; Kouno, T.; Katsumata, N.; Ando, M.; Aogi, K.; et al. FcγR2A and 3A polymorphisms predict clinical outcome of trastuzumab in both neoadjuvant and metastatic settings in patients with HER2-positive breast cancer. Ann. Oncol. 2011, 22, 1302-1307.
25. Bibeau, F.; Lopez-Crapez, E.; Di Fiore, F.; Thezenas, S.; Ychou, M.; Blanchard, F.; Lamy, A.; Penault-Llorca, F.; Frebourg, T.; Michel, P.; et al. Impact of Fc RIIa-Fc RIIIa Polymorphisms and KRAS Mutations on the Clinical Outcome of Patients With Metastatic Colorectal Cancer Treated With Cetuximab Plus Irinotecan. J. Clin. Oncol. 2009, 27, 1122-1129.
26. Kuo, T. T.; Aveson, V. G. Neonatal Fc receptor and IgG-based therapeutics. MAbs 2011, 3, 422-430.
27. Jefferis, R. R. Isotype and glycoform selection for antibody therapeutics. Arch. Biochem. Biophys. 2012, 526, 159-166.
28. Idusogie, E. E. E.; Presta, L. G. L.; Gazzano-Santoro, H. H.; Totpal, K. K.; Wong, P. Y. P.; Ultsch, M. M.; Meng, Y. G. Y.; Mulkerrin, M. G. M. Mapping of the C1q binding site on rituxan, a chimeric antibody with a human IgG1 Fc. J. Immunol. 2000, 164, 4178-4184.
29. 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-. ANG. resolution. Biochemistry 1981, 20, 2361-2370.
30. Feige, M. J.; Nath, S.; Catharino, S. R.; Weinfurtner, D.; Steinbacher, S.; Buchner, J. Structure of the Murine Unglycosylated IgG1 Fc Fragment. J. Mol. Biol. 2009, 391, 599-608.
31. Jefferis, R. R.; Lund, J. J. Interaction sites on human IgG-Fc for FcgammaR: Current models. Immunol. Lett. 2002, 82, 57-65.
32. Jefferis, R. The glycosylation of antibody molecules: Functional significance. Glycoconjug. J. 1993, 10, 358-361.
33. Arnold, J. N. J.; Wormald, M. R. M.; Sim, R. B. R.; Rudd, P. M. P.; Dwek, R. A. R. The impact of glycosylation on the biological function and structure of human immunoglobulins. Immunology 2007, 25, 21-50.
34. Routier, F. H.; Hounsell, E. F.; Rudd, P. M.; Takahashi, N.; Bond, A.; Hay, F. C.; Alavi, A.; Axford, J. S.; Jefferis, R. Quantitation of the oligosaccharides of human serum IgG from patients with rheumatoid arthritis: A critical evaluation of different methods. J. Immunol. Methods 1998, 213, 113-130.
35. Zauner, G.; Selman, M. H. J.; Bondt, A.; Rombouts, Y.; Blank, D.; Deelder, A. M.; Wuhrer, M. Glycoproteomic analysis of antibodies. Mol. Cell. Proteomics 2013, 12, 856-865.
36. Stadlmann, J.; Weber, A.; Pabst, M.; Anderle, H.; Kunert, R.; Ehrlich, H.; Peter Schwarz, H.; Altmann, F. A close look at human IgG sialylation and subclass distribution after lectin fractionation. Proteomics 2009, 9, 4143-4153.
37. Wuhrer, M.; Stam, J. C.; van de Geijn, F. E.; Koeleman, C. A. M.; Verrips, C. T.; Dolhain, R. J. E. M.; Hokke, C. H.; Deelder, A. M. Glycosylation profiling of immunoglobulin G (IgG) subclasses from human serum. Proteomics 2007, 7, 4070-4081.
38. Anthony, R. M.; Wermeling, F.; Ravetch, J. V. Novel roles for the IgG Fc glycan. Ann. NY Acad. Sci. 2012, 1253, 170-180.
39. Shinkawa, T. T.; Nakamura, K. K.; Yamane, N. N.; Shoji-Hosaka, E. E.; Kanda, Y. Y.; Sakurada, M. M.; Uchida, K. K.; Anazawa, H. H.; Satoh, M. M.; Yamasaki, M. M.; et al. The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. J. Biol. Chem. 2003, 278, 3466-3473.
40. Shields, R. L.; Lai, J.; Keck, R.; O'Connell, L. Y.; Hong, K.; Meng, Y. G.; Weikert, S. H. A.; Presta, L. G. 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.
41. Forthal, D. N.; Gach, J. S.; Landucci, G.; Jez, J.; Strasser, R.; Kunert, R.; Steinkellner, H. Fc-glycosylation influences Fcγ receptor binding and cell-mediated anti-HIV activity of monoclonal antibody 2G12. J. Immunol. 2010, 185, 6876-6882.
42. Zeitlin, L. L.; Pettitt, J. J.; Scully, C. C.; Bohorova, N. N.; Do, D. K.; Pauly, M. M.; Hiatt, A. A.; Ngo, L. L.; Steinkellner, H. H.; Whaley, K. J. K.; et al. Enhanced potency of a fucose-free monoclonal antibody being developed as an Ebola virus immunoprotectant. Proc. Natl. Acad. Sci. USA 2011, 108, 20690-20694.
43. Junttila, T. T.; Parsons, K.; Olsson, C.; Lu, Y.; Xin, Y.; Theriault, J.; Crocker, L.; Pabonan, O.; Baginski, T.; Meng, G.; et al. Superior In vivo Efficacy of Afucosylated Trastuzumab in the Treatment of HER2-Amplified Breast Cancer. Cancer Res. 2010, 70, 4481-4489.
44. Ferrara, C.; Grau, S.; Jäger, C.; Sondermann, P.; Brünker, P.; Waldhauer, I.; Hennig, M.; Ruf, A.; Rufer, A. C.; Stihle, M.; et al. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc. Natl. Acad. Sci. USA 2011, 108, 12669-12674.
45. Ferrara, C. C.; Stuart, F. F.; Sondermann, P. P.; Brünker, P. P.; Umaña, P. P. The carbohydrate at FcgammaRIIIa Asn-162. An element required for high affinity binding to non-fucosylated IgG glycoforms. J. Biol. Chem. 2006, 281, 5032-5036.
46. Davies, J.; Jiang, L.; Pan, L. Z.; LaBarre, M. J.; Anderson, D.; Reff, M. Expression of GnTIII in a recombinant anti-CD20 CHO production cell line: Expression of antibodies with altered glycoforms leads to an increase in ADCC through higher affinity for FC gamma RIII. Biotechnol. Bioeng. 2001, 74, 288-294.
47. Umaña, P.; Jean-Mairet, J.; Moudry, R.; Amstutz, H.; Bailey, J. E. Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nat. Biotechnol. 1999, 17, 176-180.
48. Hodoniczky, J.; Zheng, Y. Z.; James, D. C. Control of recombinant monoclonal antibody effector functions by Fc N-glycan remodeling in vitro. Biotechnol. Prog. 2005, 21, 1644-1652.
49. Boyd, P. N.; Lines, A. C.; 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.
50. Nimmerjahn, F.; Anthony, R. M.; Ravetch, J. V. Agalactosylated IgG antibodies depend on cellular Fc receptors for in vivo activity. Proc. Natl. Acad. Sci. USA 2007, 104, 8433-8437.
51. Malhotra, R.; Wormald, M. R.; Rudd, P. M.; Fischer, P. B.; Dwek, R. A.; Sim, R. B. Glycosylation changes of IgG associated with rheumatooid arthritis can activate complement via the mannose-binding protein. Nat. Med. 1995, 1, 237-243.
52. Ackerman, M. E.; Crispin, M.; Yu, X.; Baruah, K.; Boesch, A. W.; Harvey, D. J.; Dugast, A.-S.; Heizen, E. L.; Ercan, A.; Choi, I.; et al. Natural variation in Fc glycosylation of HIV-specific antibodies impacts antiviral activity. J. Clin. Invest. 2013, 123, 2183-2192.
53. Karsten, C. M. C.; Pandey, M. K. M.; Figge, J. J.; Kilchenstein, R. R.; Taylor, P. R. P.; Rosas, M. M.; McDonald, J. U. J.; Orr, S. J. S.; Berger, M. M.; Petzold, D. D.; et al. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcγRIIB and dectin-1. Nat. Med. 2012, 18, 1401-1406.
54. Kaneko, Y.; Nimmerjahn, F.; Ravetch, J. V. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 2006, 313, 670-673.
55. Anthony, R. M.; Nimmerjahn, F.; Ashline, D. J.; Reinhold, V. N.; Paulson, J. C.; Ravetch, J. V. Recapitulation of IVIG Anti-Inflammatory Activity with a Recombinant IgG Fc. Science 2008, 320, 373-376.
56. Anthony, R. M.; Kobayashi, T.; Wermeling, F.; Ravetch, J. V. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature 2011, 475, 110-113.
57. Anthony, R. M. R.; Wermeling, F. F.; Karlsson, M. C. I. M.; Ravetch, J. V. J. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc. Natl. Acad. Sci. USA 2008, 105, 19571-19578.
58. Schwab, I.; Biburger, M.; Krönke, G.; Schett, G.; Nimmerjahn, F. IVIg-mediated amelioration of ITP in mice is dependent on sialic acid and SIGNR1. Eur. J. Immunol. 2012, 42, 826-830.
59. Scallon, B. J.; Tam, S. H.; McCarthy, S. G.; Cai, A. N.; Raju, T. S. Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Mol. Immunol. 2007, 44, 1524-1534.
60. Imbach, P.; Wagner, H. P.; Berchtold, W.; Gaedicke, G.; Hirt, A.; Joller, P.; Mueller-Eckhardt, C.; Müller, B.; Rossi, E.; Barandun, S. Intravenous immunoglobulin versus oral corticosteroids in acute immune thrombocytopenic purpura in childhood. Lancet 1985, 2, 464-468.
61. Levy, Y.; Sherer, Y.; Ahmed, A.; Langevitz, P.; George, J.; Fabbrizzi, F.; Terryberry, J.; Meissner, M.; Lorber, M.; Peter, J. B.; et al. A study of 20 SLE patients with intravenous immunoglobulin-Clinical and serologic response. Lupus 1999, 8, 705-712.
62. Hughes, R. A. C. R.; Donofrio, P. P.; Bril, V. V.; Dalakas, M. C. M.; Deng, C. C.; Hanna, K. K.; Hartung, H.-P. H.; Latov, N.; Merkies, I. S. J. I.; van Doorn, P. A. P. Intravenous immune globulin (10% caprylate-chromatography purified) for the treatment of chronic inflammatory demyelinating polyradiculoneuropathy (ICE study): A randomised placebo-controlled trial. Lancet Neurol. 2008, 7, 136-144.
63. Kaneko, Y. Y.; Nimmerjahn, F. F.; Madaio, M. P. M.; Ravetch, J. V. J. Pathology and protection in nephrotoxic nephritis is determined by selective engagement of specific Fc receptors. J. Exp. Med. 2006, 203, 789-797.
64. Guhr, T. T.; Bloem, J. J.; Derksen, N. I. L. N.; Wuhrer, M. M.; Koenderman, A. H. L. A.; Aalberse, R. C. R.; Rispens, T. T. Enrichment of sialylated IgG by lectin fractionation does not enhance the efficacy of immunoglobulin G in a murine model of immune thrombocytopenia. PLoS One 2011, 6, e21246.
65. Leontyev, D.; Katsman, Y.; Ma, X.-Z.; Miescher, S.; Käsermann, F.; Branch, D. R. Sialylation-independent mechanism involved in the amelioration of murine immune thrombocytopenia using intravenous gammaglobulin. Transfusion 2012, 52, 1799-1805.
66. Sondermann, P.; Pincetic, A.; Maamary, J.; Lammens, K.; Ravetch, J. V. General mechanism for modulating immunoglobulin effector function. Proc. Natl. Acad. Sci. USA 2013, 110, 9868-9873.
67. Richards, M. L. M.; Katz, D. H. D. The binding of IgE to murine Fc epsilon RII is calcium-dependent but not inhibited by carbohydrate. J. Immunol. 1990, 144, 2638-2646.
68. Yu, X.; Vasiljevic, S.; Mitchell, D. A.; Crispin, M.; Scanlan, C. N. Dissecting the Molecular Mechanism of IVIg Therapy: The Interaction between Serum IgG and DC-SIGN is Independent of Antibody Glycoform or Fc Domain. J. Mol. Biol. 2013, 425, 1253-1258.
69. Oaks, M.; Taylor, S.; Shaffer, J. Autoantibodies targeting tumor-associated antigens in metastatic cancer: Sialylated IgGs as candidate anti-inflammatory antibodies. OncoImmunology 2013, 2, eLocation ID: e24841.
70. Käsermann, F. F.; Boerema, D. J. D.; Rüegsegger, M. M.; Hofmann, A. A.; Wymann, S. S.; Zuercher, A. W. A.; Miescher, S. S. Analysis and functional consequences of increased Fab-sialylation of intravenous immunoglobulin (IVIG) after lectin fractionation. PLoS One 2012, 7, e37243.
71. Barb, A. W. A.; Prestegard, J. H. J. NMR analysis demonstrates immunoglobulin G N-glycans are accessible and dynamic. Nat. Chem. Biol. 2011, 7, 147-153.
72. Gerdes, C. A.; Nicolini, V.; Herter, S.; van Puijenbroek, E.; Lang, S.; Roemmele, M.; Moessner, E.; Freytag, O.; Friess, T.; Ries, C. H.; et al. GA201 (RG7160): A novel, humanised, glycoengineered anti-EGFR antibody with enhanced ADCC and superior in vivo efficacy compared with cetuximab. Clin. Cancer Res. 2012, 19, 1126.
73. Gasdaska, J. R.; Sherwood, S.; Regan, J. T.; Dickey, L. F. An afucosylated anti-CD20 monoclonal antibody with greater antibody-dependent cellular cytotoxicity and B-cell depletion and lower complement-dependent cytotoxicity than rituximab. Mol. Immunol. 2012, 50, 134-141.
74. van de Geijn, F. E.; Wuhrer, M.; Selman, M. H. J.; Willemsen, S. P.; de Man, Y. A.; Deelder, A. M.; Hazes, J. M. W.; Dolhain, R. J. 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-R193.
75. Rook, G. A. W.; Steele, J.; Brealey, R.; Whyte, A.; Isenberg, D.; Sumar, N.; Nelson, J. L.; Bodman, K. B.; Young, A.; Roitt, I. M.; et al. Changes in IgG glycoform levels are associated with remission of arthritis during pregnancy. Trends Biotechnol. 1991, 4, 779-794.
76. Parekh, R. R.; Roitt, I. I.; Isenberg, D. D.; Dwek, R. R.; Rademacher, T. T. Age-related galactosylation of the N-linked oligosaccharides of human serum IgG. J. Exp. Med. 1988, 167, 1731-1736.
77. Shikata, K. K.; Yasuda, T. T.; Takeuchi, F.; Konishi, T. T.; Nakata, M. M.; Mizuochi, T. T. Structural changes in the oligosaccharide moiety of human IgG with aging. Glycoconjug. J. 1998, 15, 683-689.
78. Parekh, R. B.; Dwek, R. A.; Sutton, B. J.; Fernandes, D. L.; Leung, A.; Stanworth, D.; Rademacher, T. W. Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature 1985, 316, 452-457.
79. Parekh, R. B.; Roitt, I. M.; Isenberg, D. A.; Dwek, R. A.; Ansell, B. M.; 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.
80. Espy, C. C.; Morelle, W. W.; Kavian, N. N.; Grange, P. P.; Goulvestre, C. C.; Viallon, V. V.; Chéreau, C. C.; Pagnoux, C. C.; Michalski, J.-C. J.; Guillevin, L. L.; et al. Sialylation levels of anti-proteinase 3 antibodies are associated with the activity of granulomatosis with polyangiitis (Wegener's). Arthritis Rheum. 2011, 63, 2105-2115.
81. Parekh, R.; Isenberg, D.; Rook, G.; Roitt, I.; Dwek, R.; Rademacher, T. A comparative analysis of disease-associated changes in the galactosylation of serum IgG. Trends Biotechnol. 1989, 2, 101-114.
82. Mehta, A. S.; Long, R. E.; Comunale, M. A.; Wang, M.; Rodemich, L.; Krakover, J.; Philip, R.; Marrero, J. A.; Dwek, R. A.; Block, T. M. Increased levels of galactose-deficient anti-Gal immunoglobulin G in the sera of hepatitis C virus-infected individuals with fibrosis and cirrhosis. J. Virol. 2008, 82, 1259-1270.
83. Kodar, K. K.; Stadlmann, J. J.; Klaamas, K. K.; Sergeyev, B. B.; Kurtenkov, O. O. Immunoglobulin G Fc N-glycan profiling in patients with gastric cancer by LC-ESI-MS: Relation to tumor progression and survival. Glycoconjug. J. 2012, 29, 57-66.
84. Saldova, R. R.; Royle, L. L.; Radcliffe, C. M. C.; Hamid, U. M. U. A.; Evans, R. R.; Arnold, J. N. J.; Banks, R. E. R.; Hutson, R. R.; Harvey, D. J. D.; Antrobus, R. R.; et al. Ovarian cancer is associated with changes in glycosylation in both acute-phase proteins and IgG. Glycobiology 2007, 17, 1344-1356.
85. Scherer, H. U. H.; van der Woude, D. D.; Ioan-Facsinay, A. A.; Bannoudi, el, H. H.; Trouw, L. A. L.; Wang, J. J.; Häupl, T. T.; Burmester, G.-R. G.; Deelder, A. M. A.; Huizinga, T. W. J. T.; et al. Glycan profiling of anti-citrullinated protein antibodies isolated from human serum and synovial fluid. Arthritis Rheum. 2010, 62, 1620-1629.
86. Pekelharing, J. M.; Hepp, E.; Kamerling, J. P.; Gerwig, G. J.; Leijnse, B. Alterations in carbohydrate composition of serum IgG from patients with rheumatoid arthritis and from pregnant women. Ann. Rheum. Dis. 1988, 47, 91-95.
87. Gornik, I. I.; Maravić, G. G.; Dumić, J. J.; Flögel, M. M.; Lauc, G. G. Fucosylation of IgG heavy chains is increased in rheumatoid arthritis. Clin. Biochem. 1999, 32, 605-608.
88. Guo, N.; Liu, Y.; Masuda, Y.; Kawagoe, M.; Ueno, Y.; Kameda, T.; Sugiyama, T. Repeated immunization induces the increase in fucose content on antigen-specific IgG N-linked oligosaccharides. Clin. Biochem. 2005, 38, 149-153.
89. Wang, J.; Balog, C. I. A.; Stavenhagen, K.; Koeleman, C. A. M.; Scherer, H. U.; Selman, M. H. J.; Deelder, A. M.; Huizinga, T. W. J.; Toes, R. E. M.; Wuhrer, M. Fc-glycosylation of IgG1 is modulated by B-cell stimuli. Mol. Cell. Proteomics 2011, 10, M110. 004655.
90. Croce, A.; Firuzi, O.; Altieri, F.; Eufemi, M.; Agostino, R.; Priori, R.; Bombardieri, M.; Alessandri, C.; Valesini, G.; Saso, L. Effect of infliximab on the glycosylation of IgG of patients with rheumatoid arthritis. J. Clin. Lab. Anal. 2007, 21, 303-314.
91. Pasek, M.; Duk, M.; Podbielska, M.; Sokolik, R.; Szechiński, J.; Lisowska, E.; Krotkiewski, H. Galactosylation of IgG from rheumatoid arthritis (RA) patients-Changes during therapy. Glycoconjug. J. 2006, 23, 463-471.
92. Axford, J. S. J. Decreased B-cell galactosyltransferase activity in rheumatoid arthritis. Rheumatology (Oxford) 1988, 27, 170.
93. Furukawa, K. K.; Matsuta, K. K.; Takeuchi, F. F.; Kosuge, E. E.; Miyamoto, T. T.; Kobata, A. A. Kinetic study of a galactosyltransferase in the B cells of patients with rheumatoid arthritis. Int. Immunol. 1990, 2, 105-112.
94. Axford, J. S.; Sumar, N.; Alavi, A.; Isenberg, D. A.; Young, A.; Bodman, K. B.; Roitt, I. M. Changes in normal glycosylation mechanisms in autoimmune rheumatic disease. J. Clin. Invest. 1992, 89, 1021-1031.
95. Alavi, A.; Axford, J. S.; Pool, A. J. Serum galactosyltransferase isoform changes in rheumatoid arthritis. J. Rheumatol. 2004, 31, 1513-1520.
96. Keusch, J. J.; Lydyard, P. M. P.; Berger, E. G. E.; Delves, P. J. P. B lymphocyte galactosyltransferase protein levels in normal individuals and in patients with rheumatoid arthritis. Glycoconjug. J. 1998, 15, 1093-1097.
97. Jeddi, P. A. P.; Bodman-Smith, K. B. K.; Lund, T. T.; Lydyard, P. M. P.; Mengle-Gaw, L. L.; Isenberg, D. A. D.; Youinou, P. P.; Delves, P. J. P. Agalactosyl IgG and beta-1, 4-galactosyltransferase gene expression in rheumatoid arthritis patients and in the arthritis-prone MRL lpr/lpr mouse. Immunology 1996, 87, 654-659.
98. Omtvedt, L. A.; Royle, L.; Husby, G.; Sletten, K.; Radcliffe, C. M.; Harvey, D. J.; Dwek, R. A.; Rudd, P. M. Glycan analysis of monoclonal antibodies secreted in deposition disorders indicates that subsets of plasma cells differentially process IgG glycans. Arthritis Rheum. 2006, 54, 3433-3440.
99. Nasirikenari, M.; Chandrasekaran, E. V.; Matta, K. L.; Segal, B. H.; Bogner, P. N.; Lugade, A. A.; Thanavala, Y.; Lee, J. J.; Lau, J. T. Y. Altered eosinophil profile in mice with ST6Gal-1 deficiency: an additional role for ST6Gal-1 generated by the P1 promoter in regulating allergic inflammation. J. Leukoc. Biol. 2010, 87, 457-466.
100. Jones, M. B.; Nasirikenari, M.; Lugade, A. A.; Thanavala, Y.; Lau, J. T. Y. Anti-inflammatory IgG Production Requires Functional P1 Promoter in-Galactoside 2, 6-Sialyltransferase 1 (ST6Gal-1) Gene. J. Biol. Chem. 2012, 287, 15365-15370.
101. Gould, H. J.; Sutton, B. J. IgE in allergy and asthma today. Nat. Rev. Immunol. 2008, 8, 205-217.
102. Galli, S. J.; Tsai, M. IgE and mast cells in allergic disease. Nat. Med. 2012, 18, 693-704.
103. Dorrington, K. J.; Bennich, H. H. Structure-function relationships in human immunoglobulin E. Immunol. Rev. 1978, 41, 3-25.
104. Arnold, J. N. J.; Radcliffe, C. M. C.; Wormald, M. R. M.; Royle, L. L.; Harvey, D. J. D.; Crispin, M. M.; Dwek, R. A. R.; Sim, R. B. R.; Rudd, P. M. P. The glycosylation of human serum IgD and IgE and the accessibility of identified oligomannose structures for interaction with mannan-binding lectin. J. Immunol. 2004, 173, 6831-6840.
105. Basu, M. M.; Hakimi, J. J.; Dharm, E. E.; Kondas, J. A. J.; Tsien, W. H. W.; Pilson, R. S. R.; Lin, P. P.; Gilfillan, A. A.; Haring, P. P.; Braswell, E. H. E. Purification and characterization of human recombinant IgE-Fc fragments that bind to the human high affinity IgE receptor. J. Biol. Chem. 1993, 268, 13118-13127.
106. Young, R. J. R.; Owens, R. J. R.; Mackay, G. A. G.; Chan, C. M. C.; Shi, J. J.; Hide, M. M.; Francis, D. M. D.; Henry, A. J. A.; Sutton, B. J. B.; Gould, H. J. H. Secretion of recombinant human IgE-Fc by mammalian cells and biological activity of glycosylation site mutants. Protein Eng. 1995, 8, 193-199.
107. Björklund, J. E. M.; Karlsson, T.; Magnusson, C. G. M. N-glycosylation influences epitope expression and receptor binding structures in human IgE. Mol. Immunol. 1999, 36, 213-221.
108. Björklund, J. E.; Schmidt, M.; Magnusson, C. G. Characterisation of recombinant human IgE-Fc fragments expressed in baculovirus-infected insect cells. Mol. Immunol. 2000, 37, 169-177.
109. Garman, S. C.; Wurzburg, B. A.; Tarchevskaya, S. S.; Kinet, J. P.; Jardetzky, T. S. Structure of the Fc fragment of human IgE bound to its high-affinity receptor Fc epsilonRI alpha. Nature 2000, 406, 259-266.
110. Nettleton, M. Y.; Kochan, J. P. Role of Glycosylation Sites in the IgE Fc Molecule. Int. Arch. Allergy Immunol. 1995, 107, 328-329.
111. Vercelli, D.; Helm, B.; Marsh, P.; Padlan, E.; Geha, R. S.; Gouid, H. The B-cell binding site on human immunoglobulin E. Nature 1989, 338, 649-651.
112. Nadesalingam, J. J.; Reid, K. B. M. K.; Palaniyar, N. N. Collectin surfactant protein D binds antibodies and interlinks innate and adaptive immune systems. FEBS Lett. 2005, 579, 4449-4453.
113. Rutishauser, U.; Acheson, A.; Hall, A. K.; Mann, D. M.; Sunshine, J. The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions. Science 1988, 240, 53-57.
114. Monteiro, R. C. The role of IgA and IgA Fc receptors as anti-inflammatory agents. J. Clin. Immunol. 2010, 30, S61-S64.
115. Bakema, J. E. J.; van Egmond, M. M. Immunoglobulin A: A next generation of therapeutic antibodies? J. Biol. Chem. 2011, 3, 352-361.
116. Novak, J. J.; Julian, B. A. B.; Mestecky, J. J.; Renfrow, M. B. M. Glycosylation of IgA1 and pathogenesis of IgA nephropathy. Semin. Immunopathol. 2012, 34, 365-382.
117. Mattu, T. S.; Pleass, R. J.; Willis, A. C.; Kilian, M.; Wormald, M. R.; Lellouch, A. C.; Rudd, P. M.; Woof, J. M.; Dwek, R. A. The glycosylation and structure of human serum IgA1, Fab, and Fc regions and the role of N-glycosylation on Fc alpha receptor interactions. J. Biol. Chem. 1998, 273, 2260-2272.
118. Carayannopoulos, L.; Max, E. E.; Capra, J. D. Recombinant human IgA expressed in insect cells. Proc. Natl. Acad. Sci. USA 1994, 91, 8348-8352.
119. Basset, C. C.; Durand, V. V.; Jamin, C. C.; Clément, J. J.; Pennec, Y. Y.; Youinou, P. P.; Dueymes, M. M.; Roitt, I. M. I. Increased N-linked glycosylation leading to oversialylation of monomeric immunoglobulin A1 from patients with Sjögren's syndrome. Scand. J. Immunol. 2000, 51, 300-306.
120. Suzuki, H.; Moldoveanu, Z.; Hall, S.; Brown, R.; Vu, H. L.; Novak, L.; Julian, B. A.; Tomana, M.; Wyatt, R. J.; Edberg, J. C.; et al. IgA1-secreting cell lines from patients with IgA nephropathy produce aberrantly glycosylated IgA1. J. Clin. Invest. 2008, 118, 629-639.
121. Tomana, M.; Novak, J.; Julian, B. A.; Matousovic, K.; Konecny, K.; Mestecky, J. Circulating immune complexes in IgA nephropathy consist of IgA1 with galactose-deficient hinge region and antiglycan antibodies. J. Clin. Invest. 1999, 104, 73-81.
122. Coppo, R.; Basolo, B.; Martina, G.; Rollino, C.; De Marchi, M.; Giacchino, F.; Mazzucco, G.; Messina, M.; Piccoli, G. Circulating immune complexes containing IgA, IgG and IgM in patients with primary IgA nephropathy and with Henoch-Schoenlein nephritis. Correlation with clinical and histologic signs of activity. Clin. Nephrol. 1982, 18, 230-239.
123. Lai, K. N. Pathogenesis of IgA nephropathy. Nat. Rev. Nephrol. 2012, 8, 275-283.
124. Arnold, J. N.; Wormald, M. R.; Suter, D. M.; Radcliffe, C. M.; Harvey, D. J.; Dwek, R. A.; Rudd, P. M.; Sim, R. B. Human serum IgM glycosylation: identification of glycoforms that can bind to mannan-binding lectin. J. Biol. Chem. 2005, 280, 29080-29087.