Association of systemic lupus erythematosus with decreased immunosuppressive potential of the IgG glycome

Arthritis and Rheumatology

Volumn 67, Issue 11, 2015, Pages 2978-2989

  Vučkovïc, Frano ^a   Krištïc, Jasminka ^a   Gudelj, Ivan ^a   Teruel, Maria ^b   Keser, Toma ^c   Pezer, Marija ^a   Pučïc Bakovïc, Maja ^a   Štambuk, Jerko ^a   Trbojevïc Akmačïc, Irena ^a   Barrios, Clara ^d,e   Pavïc, Tamara ^c   Menni, Cristina ^d   Wang, Youxin ^f   Zhou, Yong ^f,g   Cui, Liufu ^h   Song, Haicheng ^h   Zeng, Qiang ⁱ   Guo, Xiuhua ^f   Pons Estel, Bernardo A ^j   McKeigue, Paul ^k   Leslie Patrick, Alan ^l   Gornik, Olga ^c   Spector, Tim D ^d   Harjaček, Miroslav ^m   Alarcon Riquelme, Marta ^b,n   Molokhia, Mariam ^e   Wang, Wei ^f,o   Lauc, Gordan ^a,c   more..

^a GENOS GLYCOSCIENCE RESEARCH LABORATORY   (Croatia)

^b PTS Granada   (Spain)

^c UNIVERSITY OF ZAGREB   (Croatia)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e HOSPITAL DEL MAR   (Spain)

^f CAPITAL MEDICAL UNIVERSITY   (China)

^g CAPITAL MEDICAL UNIVERSITY   (China)

^h HEBEI UNITED UNIVERSITY   (China)

ⁱ CHINESE PLA GENERAL HOSPITAL   (China)

^j Sanatorio Parque   (Argentina)

^k UNIVERSITY OF EDINBURGH   (United Kingdom)

^l Kavanagh Street Medical Centre ^*  (Trinidad and Tobago)

^m SESTRE MILOSRDNICE UNIVERSITY HOSPITAL   (Croatia)

ⁿ OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^o EDITH COWAN UNIVERSITY   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; IMMUNOGLOBULIN G; N ACETYLGLUCOSAMINE; GLYCOSYLATED IGG;

ADOLESCENT; ADULT; AGED; ARTICLE; CASE CONTROL STUDY; COHORT ANALYSIS; CONTROLLED STUDY; ETHNICITY; FEMALE; GALACTOSYLATION; GLYCOSYLATION; HUMAN; MAJOR CLINICAL STUDY; MALE; MESTIZO; PRIORITY JOURNAL; SIALYLATION; SYSTEMIC LUPUS ERYTHEMATOSUS; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; CLINICAL TRIAL; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; MULTICENTER STUDY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; CASE-CONTROL STUDIES; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNOGLOBULIN G; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; YOUNG ADULT;

EID: 84946023390     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.39273     Document Type: Article

References (44)

1. Mihai S, Nimmerjahn F., The role of Fc receptors and complement in autoimmunity. Autoimmun Rev 2013; 12: 657-60.
2. Gornik O, Pavic T, Lauc G., Alternative glycosylation modulates function of IgG and other proteins: implications on evolution and disease. Biochim Biophys Acta 2012; 1820: 1318-26.
3. 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.
4. 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.
5. Ferrara C, Stuart F, Sondermann P, Brunker P, Umana P., The carbohydrate at FcγRIIIa Asn-162: an element required for high affinity binding to non-fucosylated IgG glycoforms. J Biol Chem 2006; 281: 5032-6.
6. Iida S, Misaka H, Inoue M, Shibata M, Nakano R, Yamane-Ohnuki N, et al., Nonfucosylated therapeutic IgG1 antibody can evade the inhibitory effect of serum immunoglobulin G on antibody-dependent cellular cytotoxicity through its high binding to FcγRIIIa. Clin Cancer Res 2006; 12: 2879-87.
7. Preithner S, Elm S, Lippold S, Locher M, Wolf A, da Silva AJ, et al., High concentrations of therapeutic IgG1 antibodies are needed to compensate for inhibition of antibody-dependent cellular cytotoxicity by excess endogenous immunoglobulin G. Mol Immunol 2006; 43: 1183-93.
8. Lauc G, Huffman JE, Pucic M, Zgaga L, Adamczyk B, Muzinic A, et al., Loci associated with N-glycosylation of human immunoglobulin G show pleiotropy with autoimmune diseases and haematological cancers. PLoS Genet 2013; 9: e1003225.
9. Yang W, Shen N, Ye DQ, Liu Q, Zhang Y, Qian XX, et al., Genome-wide association study in Asian populations identifies variants in ETS1 and WDFY4 associated with systemic lupus erythematosus. PLoS Genet 2010; 6: e1000841.
10. Yang W, Tang H, Zhang Y, Tang X, Zhang J, Sun L, et al., Meta-analysis followed by replication identifies loci in or near CDKN1B, TET3, CD80, DRAM1, and ARID5B as associated with systemic lupus erythematosus in Asians. Am J Hum Genet 2013; 92: 41-51.
11. Han JW, Zheng HF, Cui Y, Sun LD, Ye DQ, Hu Z, et al., Genome-wide association study in a Chinese Han population identifies nine new susceptibility loci for systemic lupus erythematosus. Nat Genet 2009; 41: 1234-7.
12. Green RS, Stone EL, Tenno M, Lehtonen E, Farquhar MG, Marth JD., Mammalian N-glycan branching protects against innate immune self-recognition and inflammation in autoimmune disease pathogenesis. Immunity 2007; 27: 308-20.
13. Moremen KW., Golgi α-mannosidase II deficiency in vertebrate systems: implications for asparagine-linked oligosaccharide processing in mammals. Biochim Biophys Acta 2002; 1573: 225-35.
14. Sanchez E, Nadig A, Richardson BC, Freedman BI, Kaufman KM, Kelly JA, et al., Phenotypic associations of genetic susceptibility loci in systemic lupus erythematosus. Ann Rheum Dis 2011; 70: 1752-7.
15. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al., The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982; 25: 1271-7.
16. Molokhia M, Hoggart C, Patrick AL, Shriver M, Parra E, Ye J, et al., Relation of risk of systemic lupus erythematosus to west African admixture in a Caribbean population. Hum Genet 2003; 112: 310-8.
17. Petri M, Orbai AM, Alarcon GS, Gordon C, Merrill JT, Fortin PR, et al., Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum 2012; 64: 2677-86.
18. Huffman JE, Pucic-Bakovic M, Klaric L, Hennig R, Selman MH, Vuckovic F, et al., Comparative performance of four methods for high-throughput glycosylation analysis of immunoglobulin G in genetic and epidemiological research. Mol Cell Proteomics 2014; 13: 1598-610.
19. Benjamini Y, Hochberg Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995: 289-300.
20. Sanchez E, Webb RD, Rasmussen A, Kelly JA, Riba L, Kaufman KM, et al., Genetically determined Amerindian ancestry correlates with increased frequency of risk alleles for systemic lupus erythematosus. Arthritis Rheum 2010; 62: 3722-9.
21. Pucic M, Knezevic A, Vidic J, Adamczyk B, Novokmet M, Polasek O, et al., High throughput isolation and glycosylation analysis of IgG-variability and heritability of the IgG glycome in three isolated human populations. Mol Cell Proteomics 2011; 10: M111.010090.
22. Kristic J, Vuckovic F, Menni C, Klaric L, Keser T, Beceheli I, et al., Glycans are a novel biomarker of chronological and biological ages. J Gerontol 2014; 69: 779-89.
23. Gornik O, Lauc G., Glycosylation of serum proteins in inflammatory diseases. Dis Markers 2008; 25: 267-78.
24. Kaneko Y, Nimmerjahn F, Ravetch JV., Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 2006; 313: 670-3.
25. Nimmerjahn F, Ravetch JV., Fcγ receptors as regulators of immune responses. Nat Rev Immunol 2008; 8: 34-47.
26. Davies J, Jiang L, Pan LZ, LaBarre MJ, 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 FCγRIII Biotechnol Bioeng 2001; 74: 288-94.
27. Ihara H, Tsukamoto H, Gu J, Miyoshi E, Taniguchi N, Ikeda Y., Fucosyltransferase 8: GDP-fucose N-glycan core α6-fucosyltransferase (FUT8). In:, Taniguchi N, Honke K, Fukuda M, Narimatsu H, Yamaguchi Y, Angata T, editors. Handbook of glycosyltransferases and related genes. Tokyo: Springer Japan; 2014. p. 581-96.
28. Saldova R, Huffman JE, Adamczyk B, Muzinic A, Kattla JJ, Pucic M, et al., Association of medication with the human plasma N-glycome. J Proteome Res 2012; 11: 1821-31.
29. Stumpo KA, Reinhold VN., The N-glycome of human plasma. J Proteome Res 2010; 9: 4823-30.
30. Menni C, Keser T, Mangino M, Bell JT, Erte I, Akmacic I, et al., Glycosylation of immunoglobulin G: role of genetic and epigenetic influences. PLoS One 2013; 8: e82558.
31. Ercan A, Cui J, Chatterton DE, Deane KD, Hazen MM, Brintnell W, et al., Aberrant IgG galactosylation precedes disease onset, correlates with disease activity, and is prevalent in autoantibodies in rheumatoid arthritis. Arthritis Rheum 2010; 62: 2239-48.
32. Novokmet M, Lukic E, Vuckovic F, Duric Z, Keser T, Rajsl K, et al., Changes in IgG and total plasma protein glycomes in acute systemic inflammation. Sci Rep 2014; 4: 4347.
33. Truedsson L, Bengtsson AA, Sturfelt G., Complement deficiencies and systemic lupus erythematosus. Autoimmunity 2007; 40: 560-6.
34. Chen Z, Koralov SB, Kelsoe G., Complement C4 inhibits systemic autoimmunity through a mechanism independent of complement receptors CR1 and CR2. J Exp Med 2000; 192: 1339-52.
35. 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 γ receptor I and influence the synthesis of its oligosaccharide chains. J Immunol 1996; 157: 4963-9.
36. 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.
37. Bouwman LH, Roep BO, Roos A., Mannose-binding lectin: clinical implications for infection, transplantation, and autoimmunity. Hum Immunol 2006; 67: 247-56.
38. Bournazos S, Woof JM, Hart SP, Dransfield I., Functional and clinical consequences of Fc receptor polymorphic and copy number variants. Clin Exp Immunol 2009; 157: 244-54.
39. Sjowall C, Zapf J, von Lohneysen S, Magorivska I, Biermann M, Janko C, et al., Altered glycosylation of complexed native IgG molecules is associated with disease activity of systemic lupus erythematosus. Lupus 2015; 24: 569-81.
40. Anumula KR., Quantitative glycan profiling of normal human plasma derived immunoglobulin and its fragments Fab and Fc. J Immunol Methods 2012; 382: 167-76.
41. Schwab I, Nimmerjahn F., Intravenous immunoglobulin therapy: how does IgG modulate the immune system? Nat Rev Immunol 2013; 13: 176-89.
42. Ogata S, Shimizu C, Franco A, Touma R, Kanegaye JT, Choudhury BP, et al., Treatment response in Kawasaki disease is associated with sialylation levels of endogenous but not therapeutic intravenous immunoglobulin G. PLoS One 2013; 8: e81448.
43. Shrestha S, Wiener HW, Olson AK, Edberg JC, Bowles NE, Patel H, et al., Functional FcγRIIB gene variants influence intravenous immunoglobulin response in patients with Kawasaki disease. J Allergy Clin Immunol 2011; 128: 677-80.
44. Bolland S, Ravetch JV., Spontaneous autoimmune disease in FcγRIIB-deficient mice results from strain-specific epistasis. Immunity 2000; 13: 277-85.