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Published in: Journal of Clinical Immunology 1/2014

01-07-2014

Fc Glycan-Modulated Immunoglobulin G Effector Functions

Authors: Isaak Quast, Jan D. Lünemann

Published in: Journal of Clinical Immunology | Special Issue 1/2014

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Abstract

Immunoglobulin G (IgG) molecules are glycoproteins and residues in the sugar moiety attached to the IgG constant fragment (Fc) are essential for IgG functionality such as binding to cellular Fc receptors and complement activation. The core of this sugar moiety consists of a bi-antennary heptameric structure of mannose and N-acetylglucosamine (GlcNAc), further decorated with terminal and branching residues including galactose, sialic acid, fucose, and GlcNAc. Presence or absence of distinct residues such as fucose and sialic acid can dramatically alter pro- and anti-inflammatory IgG activities which could be harnessed for immunotherapeutic purposes. Here we review recent advances in understanding the role of the IgG-Fc glycan during immune responses and for immunotherapy with a focus on sialic acid and intravenous immunoglobulin (IVIG) treatment.
Literature
1.
go back to reference Abbas AK, Lichtman AH, Pillai S. Cellular and molecular immunology. 6th ed. Philadelphia: Saunders (Elsevier); 2007. Abbas AK, Lichtman AH, Pillai S. Cellular and molecular immunology. 6th ed. Philadelphia: Saunders (Elsevier); 2007.
2.
go back to reference Ackerman ME, Crispin M, Yu X, Baruah K, Boesch AW, Harvey DJ, et al. Natural variation in Fc glycosylation of HIV-specific antibodies impacts antiviral activity. J Clin Invest. 2013;123:2183–92.PubMedCentralPubMedCrossRef Ackerman ME, Crispin M, Yu X, Baruah K, Boesch AW, Harvey DJ, et al. Natural variation in Fc glycosylation of HIV-specific antibodies impacts antiviral activity. J Clin Invest. 2013;123:2183–92.PubMedCentralPubMedCrossRef
3.
go back to reference Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics. 2002;1:845–67.PubMedCrossRef Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics. 2002;1:845–67.PubMedCrossRef
4.
go back to reference Anthony RM, Kobayashi T, Wermeling F, Ravetch JV. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature. 2011;475:110–3.PubMedCentralPubMedCrossRef Anthony RM, Kobayashi T, Wermeling F, Ravetch JV. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature. 2011;475:110–3.PubMedCentralPubMedCrossRef
5.
go back to reference Anthony RM, Nimmerjahn F, Ashline DJ, Reinhold VN, Paulson JC, Ravetch JV. Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science. 2008;320:373–6.PubMedCentralPubMedCrossRef Anthony RM, Nimmerjahn F, Ashline DJ, Reinhold VN, Paulson JC, Ravetch JV. Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science. 2008;320:373–6.PubMedCentralPubMedCrossRef
6.
go back to reference Anthony RM, Wermeling F, Karlsson MC, Ravetch JV. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci U S A. 2008;105:19571–8.PubMedCentralPubMedCrossRef Anthony RM, Wermeling F, Karlsson MC, Ravetch JV. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci U S A. 2008;105:19571–8.PubMedCentralPubMedCrossRef
7.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
9.
go back to reference Bayry J, Lacroix-Desmazes S, Carbonneil C, Misra N, Donkova V, Pashov A, et al. Inhibition of maturation and function of dendritic cells by intravenous immunoglobulin. Blood. 2003;101:758–65.PubMedCrossRef Bayry J, Lacroix-Desmazes S, Carbonneil C, Misra N, Donkova V, Pashov A, et al. Inhibition of maturation and function of dendritic cells by intravenous immunoglobulin. Blood. 2003;101:758–65.PubMedCrossRef
10.
go back to reference Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, Colombat P, et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood. 2002;99:754–8.PubMedCrossRef Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, Colombat P, et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood. 2002;99:754–8.PubMedCrossRef
11.
go back to reference De Groot AS, Moise L, McMurry JA, Wambre E, Van Overtvelt L, Moingeon P, et al. Activation of natural regulatory T cells by IgG Fc-derived peptide “Tregitopes”. Blood. 2008;112:3303–11.PubMedCentralPubMedCrossRef De Groot AS, Moise L, McMurry JA, Wambre E, Van Overtvelt L, Moingeon P, et al. Activation of natural regulatory T cells by IgG Fc-derived peptide “Tregitopes”. Blood. 2008;112:3303–11.PubMedCentralPubMedCrossRef
12.
go back to reference Debre M, Bonnet MC, Fridman WH, Carosella E, Philippe N, Reinert P, et al. Infusion of Fc gamma fragments for treatment of children with acute immune thrombocytopenic purpura. Lancet. 1993;342:945–9.PubMedCrossRef Debre M, Bonnet MC, Fridman WH, Carosella E, Philippe N, Reinert P, et al. Infusion of Fc gamma fragments for treatment of children with acute immune thrombocytopenic purpura. Lancet. 1993;342:945–9.PubMedCrossRef
13.
go back to reference Dolman KM, Brouwer N, Frakking FN, Flato B, Tak PP, Kuijpers TW, et al. Mannose-binding lectin deficiency is associated with early onset of polyarticular juvenile rheumatoid arthritis: a cohort study. Arthritis Res Ther. 2008;10:R32.PubMedCentralPubMedCrossRef Dolman KM, Brouwer N, Frakking FN, Flato B, Tak PP, Kuijpers TW, et al. Mannose-binding lectin deficiency is associated with early onset of polyarticular juvenile rheumatoid arthritis: a cohort study. Arthritis Res Ther. 2008;10:R32.PubMedCentralPubMedCrossRef
15.
go back to reference Ferrara C, Grau S, Jager C, Sondermann P, Brunker P, Waldhauer I, et al. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc Natl Acad Sci U S A. 2011;108:12669–74.PubMedCentralPubMedCrossRef Ferrara C, Grau S, Jager C, Sondermann P, Brunker P, Waldhauer I, et al. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc Natl Acad Sci U S A. 2011;108:12669–74.PubMedCentralPubMedCrossRef
16.
go back to reference Gaboriaud C, Juanhuix J, Gruez A, Lacroix M, Darnault C, Pignol D, et al. The crystal structure of the globular head of complement protein C1q provides a basis for its versatile recognition properties. J Biol Chem. 2003;278:46974–82.PubMedCrossRef Gaboriaud C, Juanhuix J, Gruez A, Lacroix M, Darnault C, Pignol D, et al. The crystal structure of the globular head of complement protein C1q provides a basis for its versatile recognition properties. J Biol Chem. 2003;278:46974–82.PubMedCrossRef
17.
go back to reference Gelfand EW. Intravenous immune globulin in autoimmune and inflammatory diseases. N Engl J Med. 2012;367:2015–25.PubMedCrossRef Gelfand EW. Intravenous immune globulin in autoimmune and inflammatory diseases. N Engl J Med. 2012;367:2015–25.PubMedCrossRef
18.
go back to reference Hansen RJ, Balthasar JP. Intravenous immunoglobulin mediates an increase in anti-platelet antibody clearance via the FcRn receptor. Thromb Haemost. 2002;88:898–9.PubMed Hansen RJ, Balthasar JP. Intravenous immunoglobulin mediates an increase in anti-platelet antibody clearance via the FcRn receptor. Thromb Haemost. 2002;88:898–9.PubMed
19.
go back to reference Hess C, Winkler A, Lorenz AK, Holecska V, Blanchard V, Eiglmeier S, et al. T cell-independent B cell activation induces immunosuppressive sialylated IgG antibodies. J Clin Invest. 2013;123:3788–96.PubMedCentralPubMedCrossRef Hess C, Winkler A, Lorenz AK, Holecska V, Blanchard V, Eiglmeier S, et al. T cell-independent B cell activation induces immunosuppressive sialylated IgG antibodies. J Clin Invest. 2013;123:3788–96.PubMedCentralPubMedCrossRef
20.
go back to reference Huhn C, Selman MH, Ruhaak LR, Deelder AM, Wuhrer M. IgG glycosylation analysis. Proteomics. 2009;9:882–913.PubMedCrossRef Huhn C, Selman MH, Ruhaak LR, Deelder AM, Wuhrer M. IgG glycosylation analysis. Proteomics. 2009;9:882–913.PubMedCrossRef
21.
go back to reference Imbach P. Immune thrombocytopenic purpura and intravenous immunoglobulin. Cancer. 1991;68:1422–5.PubMedCrossRef Imbach P. Immune thrombocytopenic purpura and intravenous immunoglobulin. Cancer. 1991;68:1422–5.PubMedCrossRef
22.
go back to reference Imbach P, Barandun S, Baumgartner C, Hirt A, Hofer F, Wagner HP. High-dose intravenous gammaglobulin therapy of refractory, in particular idiopathic thrombocytopenia in childhood. Helv Paediatr Acta. 1981;36:81–6.PubMed Imbach P, Barandun S, Baumgartner C, Hirt A, Hofer F, Wagner HP. High-dose intravenous gammaglobulin therapy of refractory, in particular idiopathic thrombocytopenia in childhood. Helv Paediatr Acta. 1981;36:81–6.PubMed
23.
go back to reference Imbach P, Barandun S, d’Apuzzo V, Baumgartner C, Hirt A, Morell A, et al. High-dose intravenous gammaglobulin for idiopathic thrombocytopenic purpura in childhood. Lancet. 1981;1:1228–31.PubMedCrossRef Imbach P, Barandun S, d’Apuzzo V, Baumgartner C, Hirt A, Morell A, et al. High-dose intravenous gammaglobulin for idiopathic thrombocytopenic purpura in childhood. Lancet. 1981;1:1228–31.PubMedCrossRef
24.
go back to reference Junttila TT, Parsons K, Olsson C, Lu Y, Xin Y, Theriault J, et al. Superior in vivo efficacy of afucosylated trastuzumab in the treatment of HER2-amplified breast cancer. Cancer Res. 2010;70:4481–9.PubMedCrossRef Junttila TT, Parsons K, Olsson C, Lu Y, Xin Y, Theriault J, et al. Superior in vivo efficacy of afucosylated trastuzumab in the treatment of HER2-amplified breast cancer. Cancer Res. 2010;70:4481–9.PubMedCrossRef
25.
go back to reference Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science. 2006;313:670–3.PubMedCrossRef Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science. 2006;313:670–3.PubMedCrossRef
26.
go back to reference Kapur R, Kustiawan I, Vestrheim A, Koeleman CA, Visser R, Einarsdottir HK, et al. A prominent lack of IgG1-Fc fucosylation of platelet alloantibodies in pregnancy. Blood. 2014;123:471–80.PubMedCentralPubMedCrossRef Kapur R, Kustiawan I, Vestrheim A, Koeleman CA, Visser R, Einarsdottir HK, et al. A prominent lack of IgG1-Fc fucosylation of platelet alloantibodies in pregnancy. Blood. 2014;123:471–80.PubMedCentralPubMedCrossRef
27.
go back to reference Karsten CM, Pandey MK, Figge J, Kilchenstein R, Taylor PR, Rosas M, et al. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcgammaRIIB and dectin-1. Nat Med. 2012;18:1401–6.PubMedCentralPubMedCrossRef Karsten CM, Pandey MK, Figge J, Kilchenstein R, Taylor PR, Rosas M, et al. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcgammaRIIB and dectin-1. Nat Med. 2012;18:1401–6.PubMedCentralPubMedCrossRef
28.
go back to reference Krapp S, Mimura Y, Jefferis R, Huber R, Sondermann P. Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J Mol Biol. 2003;325:979–89.PubMedCrossRef Krapp S, Mimura Y, Jefferis R, Huber R, Sondermann P. Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J Mol Biol. 2003;325:979–89.PubMedCrossRef
29.
go back to reference Lund J, Takahashi N, Pound JD, Goodall M, 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;157:4963–9.PubMed Lund J, Takahashi N, Pound JD, Goodall M, 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;157:4963–9.PubMed
30.
go back to reference Lux A, Nimmerjahn F. Impact of differential glycosylation on IgG activity. Adv Exp Med Biol. 2011;780:113–24.PubMedCrossRef Lux A, Nimmerjahn F. Impact of differential glycosylation on IgG activity. Adv Exp Med Biol. 2011;780:113–24.PubMedCrossRef
31.
go back to reference Malhotra R, Wormald MR, Rudd PM, Fischer PB, Dwek RA, Sim RB. Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat Med. 1995;1:237–43.PubMedCrossRef Malhotra R, Wormald MR, Rudd PM, Fischer PB, Dwek RA, Sim RB. Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat Med. 1995;1:237–43.PubMedCrossRef
32.
go back to reference Mimura Y, Church S, Ghirlando R, Ashton PR, Dong S, Goodall M, et al. 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.PubMedCrossRef Mimura Y, Church S, Ghirlando R, Ashton PR, Dong S, Goodall M, et al. 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.PubMedCrossRef
33.
go back to reference Mimura Y, Sondermann P, Ghirlando R, Lund J, Young SP, Goodall M, et al. Role of oligosaccharide residues of IgG1-Fc in Fc gamma RIIb binding. J Biol Chem. 2001;276:45539–47.PubMedCrossRef Mimura Y, Sondermann P, Ghirlando R, Lund J, Young SP, Goodall M, et al. Role of oligosaccharide residues of IgG1-Fc in Fc gamma RIIb binding. J Biol Chem. 2001;276:45539–47.PubMedCrossRef
34.
go back to reference Mizuochi T, Taniguchi T, Shimizu A, Kobata A. Structural and numerical variations of the carbohydrate moiety of immunoglobulin G. J Immunol. 1982;129:2016–20.PubMed Mizuochi T, Taniguchi T, Shimizu A, Kobata A. Structural and numerical variations of the carbohydrate moiety of immunoglobulin G. J Immunol. 1982;129:2016–20.PubMed
35.
go back to reference Nimmerjahn F, Anthony RM, Ravetch JV. Agalactosylated IgG antibodies depend on cellular Fc receptors for in vivo activity. Proc Natl Acad Sci U S A. 2007;104:8433–7.PubMedCentralPubMedCrossRef Nimmerjahn F, Anthony RM, Ravetch JV. Agalactosylated IgG antibodies depend on cellular Fc receptors for in vivo activity. Proc Natl Acad Sci U S A. 2007;104:8433–7.PubMedCentralPubMedCrossRef
36.
go back to reference Nimmerjahn F, Ravetch JV. Anti-inflammatory actions of intravenous immunoglobulin. Annu Rev Immunol. 2008;26:513–33.PubMedCrossRef Nimmerjahn F, Ravetch JV. Anti-inflammatory actions of intravenous immunoglobulin. Annu Rev Immunol. 2008;26:513–33.PubMedCrossRef
37.
go back to reference Niwa R, Shoji-Hosaka E, Sakurada M, Shinkawa T, Uchida K, Nakamura K, et al. Defucosylated chimeric anti-CC chemokine receptor 4 IgG1 with enhanced antibody-dependent cellular cytotoxicity shows potent therapeutic activity to T-cell leukemia and lymphoma. Cancer Res. 2004;64:2127–33.PubMedCrossRef Niwa R, Shoji-Hosaka E, Sakurada M, Shinkawa T, Uchida K, Nakamura K, et al. Defucosylated chimeric anti-CC chemokine receptor 4 IgG1 with enhanced antibody-dependent cellular cytotoxicity shows potent therapeutic activity to T-cell leukemia and lymphoma. Cancer Res. 2004;64:2127–33.PubMedCrossRef
39.
go back to reference Oefner CM, Winkler A, Hess C, Lorenz AK, Holecska V, Huxdorf M, et al. Tolerance induction with T cell-dependent protein antigens induces regulatory sialylated IgGs. J Allergy Clin Immunol. 2012;129:1647–55. e1613.PubMedCrossRef Oefner CM, Winkler A, Hess C, Lorenz AK, Holecska V, Huxdorf M, et al. Tolerance induction with T cell-dependent protein antigens induces regulatory sialylated IgGs. J Allergy Clin Immunol. 2012;129:1647–55. e1613.PubMedCrossRef
40.
go back to reference Parekh R, Roitt I, Isenberg D, Dwek R, Rademacher T. Age-related galactosylation of the N-linked oligosaccharides of human serum IgG. J Exp Med. 1988;167:1731–6.PubMedCrossRef Parekh R, Roitt I, Isenberg D, Dwek R, Rademacher T. Age-related galactosylation of the N-linked oligosaccharides of human serum IgG. J Exp Med. 1988;167:1731–6.PubMedCrossRef
41.
go back to reference Parekh RB, Dwek RA, Sutton BJ, Fernandes DL, Leung A, Stanworth D, et al. Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature. 1985;316:452–7.PubMedCrossRef Parekh RB, Dwek RA, Sutton BJ, Fernandes DL, Leung A, Stanworth D, et al. Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature. 1985;316:452–7.PubMedCrossRef
42.
go back to reference Ramakrishna C, Newo AN, Shen YW, Cantin E. Passively administered pooled human immunoglobulins exert IL-10 dependent anti-inflammatory effects that protect against fatal HSV encephalitis. PLoS Pathog. 2011;7:e1002071.PubMedCentralPubMedCrossRef Ramakrishna C, Newo AN, Shen YW, Cantin E. Passively administered pooled human immunoglobulins exert IL-10 dependent anti-inflammatory effects that protect against fatal HSV encephalitis. PLoS Pathog. 2011;7:e1002071.PubMedCentralPubMedCrossRef
43.
go back to reference Rich JR, Withers SG. Emerging methods for the production of homogeneous human glycoproteins. Nat Chem Biol. 2009;5:206–15.PubMedCrossRef Rich JR, Withers SG. Emerging methods for the production of homogeneous human glycoproteins. Nat Chem Biol. 2009;5:206–15.PubMedCrossRef
44.
go back to reference Samuelsson A, Towers TL, Ravetch JV. Anti-inflammatory activity of IVIG mediated through the inhibitory Fc receptor. Science. 2001;291:484–6.PubMedCrossRef Samuelsson A, Towers TL, Ravetch JV. Anti-inflammatory activity of IVIG mediated through the inhibitory Fc receptor. Science. 2001;291:484–6.PubMedCrossRef
45.
go back to reference Scallon BJ, Tam SH, McCarthy SG, Cai AN, Raju TS. Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Mol Immunol. 2007;44:1524–34.PubMedCrossRef Scallon BJ, Tam SH, McCarthy SG, Cai AN, Raju TS. Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Mol Immunol. 2007;44:1524–34.PubMedCrossRef
46.
go back to reference Schwab I, Biburger M, Kronke G, Schett G, Nimmerjahn F. IVIg-mediated amelioration of ITP in mice is dependent on sialic acid and SIGNR1. Eur J Immunol. 2012;42:826–30.PubMedCrossRef Schwab I, Biburger M, Kronke G, Schett G, Nimmerjahn F. IVIg-mediated amelioration of ITP in mice is dependent on sialic acid and SIGNR1. Eur J Immunol. 2012;42:826–30.PubMedCrossRef
47.
go back to reference Schwab I, Mihai S, Seeling M, Kasperkiewicz M, Ludwig RJ, Nimmerjahn F. Broad requirement for terminal sialic acid residues and FcgammaRIIB for the preventive and therapeutic activity of intravenous immunoglobulins in vivo. Eur J Immunol. 2014. Schwab I, Mihai S, Seeling M, Kasperkiewicz M, Ludwig RJ, Nimmerjahn F. Broad requirement for terminal sialic acid residues and FcgammaRIIB for the preventive and therapeutic activity of intravenous immunoglobulins in vivo. Eur J Immunol. 2014.
48.
go back to reference Schwarz F, Aebi M. Mechanisms and principles of N-linked protein glycosylation. Curr Opin Struct Biol. 2011;21:576–82.PubMedCrossRef Schwarz F, Aebi M. Mechanisms and principles of N-linked protein glycosylation. Curr Opin Struct Biol. 2011;21:576–82.PubMedCrossRef
49.
go back to reference Selman MH, Niks EH, Titulaer MJ, Verschuuren JJ, Wuhrer M, Deelder AM. IgG fc N-glycosylation changes in Lambert-Eaton myasthenic syndrome and myasthenia gravis. J Proteome Res. 2011;10:143–52.PubMedCrossRef Selman MH, Niks EH, Titulaer MJ, Verschuuren JJ, Wuhrer M, Deelder AM. IgG fc N-glycosylation changes in Lambert-Eaton myasthenic syndrome and myasthenia gravis. J Proteome Res. 2011;10:143–52.PubMedCrossRef
50.
go back to reference Shields RL, Lai J, Keck R, O’Connell LY, Hong K, Meng YG, 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;277:26733–40.PubMedCrossRef Shields RL, Lai J, Keck R, O’Connell LY, Hong K, Meng YG, 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;277:26733–40.PubMedCrossRef
51.
go back to reference Shikata K, Yasuda T, Takeuchi F, Konishi T, Nakata M, Mizuochi T. Structural changes in the oligosaccharide moiety of human IgG with aging. Glycoconj J. 1998;15:683–9.PubMedCrossRef Shikata K, Yasuda T, Takeuchi F, Konishi T, Nakata M, Mizuochi T. Structural changes in the oligosaccharide moiety of human IgG with aging. Glycoconj J. 1998;15:683–9.PubMedCrossRef
52.
go back to reference Shoenfeld Y, Rauova L, Gilburd B, Kvapil F, Goldberg I, Kopolovic J, et al. Efficacy of IVIG affinity-purified anti-double-stranded DNA anti-idiotypic antibodies in the treatment of an experimental murine model of systemic lupus erythematosus. Int Immunol. 2002;14:1303–11.PubMedCrossRef Shoenfeld Y, Rauova L, Gilburd B, Kvapil F, Goldberg I, Kopolovic J, et al. Efficacy of IVIG affinity-purified anti-double-stranded DNA anti-idiotypic antibodies in the treatment of an experimental murine model of systemic lupus erythematosus. Int Immunol. 2002;14:1303–11.PubMedCrossRef
53.
54.
go back to reference Tackenberg B, Jelcic I, Baerenwaldt A, Oertel WH, Sommer N, Nimmerjahn F, et al. Impaired inhibitory Fcgamma receptor IIB expression on B cells in chronic inflammatory demyelinating polyneuropathy. Proc Natl Acad Sci U S A. 2009;106:4788–92.PubMedCentralPubMedCrossRef Tackenberg B, Jelcic I, Baerenwaldt A, Oertel WH, Sommer N, Nimmerjahn F, et al. Impaired inhibitory Fcgamma receptor IIB expression on B cells in chronic inflammatory demyelinating polyneuropathy. Proc Natl Acad Sci U S A. 2009;106:4788–92.PubMedCentralPubMedCrossRef
55.
go back to reference van de Geijn FE, de Man YA, Wuhrer M, Willemsen SP, Deelder AM, Hazes JM, et al. Mannose-binding lectin does not explain the course and outcome of pregnancy in rheumatoid arthritis. Arthritis Res Ther. 2011;13:R10.PubMedCentralPubMedCrossRef van de Geijn FE, de Man YA, Wuhrer M, Willemsen SP, Deelder AM, Hazes JM, et al. Mannose-binding lectin does not explain the course and outcome of pregnancy in rheumatoid arthritis. Arthritis Res Ther. 2011;13:R10.PubMedCentralPubMedCrossRef
56.
go back to reference van de Geijn FE, Hazes JM, Geleijns K, Emonts M, Jacobs BC, Dufour-van den Goorbergh BC, et al. Mannose-binding lectin polymorphisms are not associated with rheumatoid arthritis–confirmation in two large cohorts. Rheumatology (Oxford). 2008;47:1168–71.CrossRef van de Geijn FE, Hazes JM, Geleijns K, Emonts M, Jacobs BC, Dufour-van den Goorbergh BC, et al. Mannose-binding lectin polymorphisms are not associated with rheumatoid arthritis–confirmation in two large cohorts. Rheumatology (Oxford). 2008;47:1168–71.CrossRef
57.
go back to reference Wormald MR, Rudd PM, Harvey DJ, Chang SC, Scragg IG, Dwek RA. 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;36:1370–80.PubMedCrossRef Wormald MR, Rudd PM, Harvey DJ, Chang SC, Scragg IG, Dwek RA. 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;36:1370–80.PubMedCrossRef
58.
go back to reference Yamada E, Tsukamoto Y, Sasaki R, Yagyu K, Takahashi N. Structural changes of immunoglobulin G oligosaccharides with age in healthy human serum. Glycoconj J. 1997;14:401–5.PubMedCrossRef Yamada E, Tsukamoto Y, Sasaki R, Yagyu K, Takahashi N. Structural changes of immunoglobulin G oligosaccharides with age in healthy human serum. Glycoconj J. 1997;14:401–5.PubMedCrossRef
59.
go back to reference Yu X, Vasiljevic S, Mitchell DA, Crispin M, Scanlan CN. 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;425:1253–8.PubMedCrossRef Yu X, Vasiljevic S, Mitchell DA, Crispin M, Scanlan CN. 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;425:1253–8.PubMedCrossRef
Metadata
Title
Fc Glycan-Modulated Immunoglobulin G Effector Functions
Authors
Isaak Quast
Jan D. Lünemann
Publication date
01-07-2014
Publisher
Springer US
Published in
Journal of Clinical Immunology / Issue Special Issue 1/2014
Print ISSN: 0271-9142
Electronic ISSN: 1573-2592
DOI
https://doi.org/10.1007/s10875-014-0018-3

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