IgG glycan patterns are associated with type 2 diabetes in independent European populations

Biochimica et Biophysica Acta - General Subjects

Volumn 1861, Issue 9, 2017, Pages 2240-2249

  Lemmers, Roosmarijn F H ^a,b   Vilaj, Marija ^c   Urda, Daniel ^d   Agakov, Felix ^d   Šimurina, Mirna ^e   Klaric, Lucija ^c,e,f   Rudan, Igor ^g   Campbell, Harry ^g   Hayward, Caroline ^f   Wilson, Jim F ^f,g   Lieverse, Aloysius G ^b   Gornik, Olga ^e   Sijbrands, Eric J G ^a   Lauc, Gordan ^c,e   van Hoek, Mandy ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b MÁXIMA MEDICAL CENTER   (Netherlands)

^c GENOS GLYCOSCIENCE RESEARCH LABORATORY   (Croatia)

^d PHARMATICS LIMITED   (United Kingdom)

^e UNIVERSITY OF ZAGREB   (Croatia)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

^g UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Ageing; Glycosylation; IgG; Inflammation; Prediction; Type 2 diabetes

Indexed keywords

CREATININE; GLYCAN; HIGH DENSITY LIPOPROTEIN; IMMUNOGLOBULIN G; GALACTOSE; N ACETYLNEURAMINIC ACID;

ADULT; AGE DISTRIBUTION; AGED; ARTICLE; BODY MASS; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DISEASE ASSOCIATION; EUROPEAN; FEMALE; FUCOSYLATION; GALACTOSYLATION; HUMAN; MAJOR CLINICAL STUDY; MALE; MEASUREMENT ERROR; NON INSULIN DEPENDENT DIABETES MELLITUS; POPULATION BASED CASE CONTROL STUDY; PRIORITY JOURNAL; SEX DIFFERENCE; SIALYLATION; VALIDATION PROCESS; AREA UNDER THE CURVE; DIABETES MELLITUS, TYPE 2; GLYCOSYLATION; METABOLISM; MIDDLE AGED;

AGED; AREA UNDER CURVE; DIABETES MELLITUS, TYPE 2; FEMALE; GALACTOSE; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN G; MALE; MIDDLE AGED; N-ACETYLNEURAMINIC ACID;

EID: 85021404044     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2017.06.020     Document Type: Article

References (50)

1. WHO, Diabetes mellitus. Fact Sheet N°138, 2016.
2. Morris, A.P., Voight, B.F., Teslovich, T.M. et al., Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 diabetes. Nat. Genet. 44 (2012), 981–990.
3. Gornik, O., Pavic, T., Lauc, G., Alternative glycosylation modulates function of IgG and other proteins - implications on evolution and disease. Biochim. Biophys. Acta 1820 (2012), 1318–1326.
4. Lauc, G., Rudan, I., Campbell, H., Rudd, P.M., Complex genetic regulation of protein glycosylation. Mol. BioSyst. 6 (2010), 329–335.
5. Wang, X., Bao, W., Liu, J. et al., Inflammatory markers and risk of type 2 diabetes: a systematic review and meta-analysis. Diabetes Care 36 (2013), 166–175.
6. Nikolac Perkovic, M., Pucic Bakovic, M., Kristic, J. et al., The association between galactosylation of immunoglobulin G and body mass index. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 48 (2014), 20–25.
7. Kristic, J., Vuckovic, F., Menni, C. et al., Glycans are a novel biomarker of chronological and biological ages. J. Gerontol. A Biol. Sci. Med. Sci. 69 (2014), 779–789.
8. Knezevic, A., Gornik, O., Polasek, O. et al., Effects of aging, body mass index, plasma lipid profiles, and smoking on human plasma N-glycans. Glycobiology 20 (2010), 959–969.
9. Wang, Y., Klaric, L., Yu, X. et al., The association between glycosylation of immunoglobulin G and hypertension: a multiple ethnic cross-sectional study. Medicine (Baltimore), 95, 2016, e3379.
10. 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 320 (2008), 373–376.
11. Kaneko, Y., Nimmerjahn, F., Ravetch, J.V., Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313 (2006), 670–673.
12. Voight, B.F., Scott, L.J., Steinthorsdottir, V. et al., Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis. Nat. Genet. 42 (2010), 579–589.
13. Alberti, K.G., Zimmet, P.Z., Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet. Med. 15 (1998), 539–553.
14. American Diabetes, A., Diagnosis and classification of diabetes mellitus. Diabetes Care 34:Suppl. 1 (2011), S62–S69.
15. McQuillan, R., Leutenegger, A.L., Abdel-Rahman, R. et al., Runs of homozygosity in European populations. Am. J. Hum. Genet. 83 (2008), 359–372.
16. Rudan, I., Campbell, H., Rudan, P., Genetic epidemiological studies of eastern Adriatic Island isolates, Croatia: objective and strategies. Coll. Antropol. 23 (1999), 531–546.
17. Polašek, O., Marušić, A., Rotim, K. et al., Genome-wide association study of anthropometric traits in Korčula Island, Croatia. Croat. Med. J. 50 (2009), 7–16.
18. Vitart, V., Rudan, I., Hayward, C. et al., SLC2A9 Is a Newly Identified Urate Transporter Influencing Serum Urate Concentration, Urate Excretion and Gout. Vol. 40, 2008, 437–442.
19. Pucic, M., Knezevic, A., Vidic, J. 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, 10(M111), 2011, 010090.
20. Jaacks, L.M., Siegel, K.R., Gujral, U.P., Narayan, K.M.V., Type 2 diabetes: a 21st century epidemic. Best Pract. Res. Clin. Endocrinol. Metab. 30 (2016), 331–343.
21. Barrios, C., Zierer, J., Gudelj, I. et al., Glycosylation profile of IgG in moderate kidney dysfunction. J. Am. Soc. Nephrol. 27 (2016), 933–941.
22. RDC T, A language and environment for statistical computing. Available from http://www.R-project.org, 2008.
23. Zaykin, D.V., Optimally weighted Z-test is a powerful method for combining probabilities in meta-analysis. J. Evol. Biol. 24 (2011), 1836–1841.
24. Ercan, A., Kohrt, W.M., Cui, J. et al., Estrogens regulate glycosylation of IgG in women and men. JCI Insight, 2, 2017.
25. Karsten, C.M., Pandey, M.K., Figge, J. et al., Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcgammaRIIB and dectin-1. Nat. Med. 18 (2012), 1401–1406.
26. Masuda, K., Kubota, T., Kaneko, E. et al., Enhanced binding affinity for FcgammaRIIIa of fucose-negative antibody is sufficient to induce maximal antibody-dependent cellular cytotoxicity. Mol. Immunol. 44 (2007), 3122–3131.
27. Mihai, S., Nimmerjahn, F., The role of Fc receptors and complement in autoimmunity. Autoimmun. Rev. 12 (2013), 657–660.
28. Nimmerjahn, F., Ravetch, J.V., Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 8 (2008), 34–47.
29. 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 1 (1988), 966–969.
30. Parekh, R.B., Dwek, R.A., Sutton, B.J. et al., Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature 316 (1985), 452–457.
31. Vuckovic, F., Kristic, J., Gudelj, I. et al., Association of systemic lupus erythematosus with decreased immunosuppressive potential of the IgG glycome. Arthritis Rheum. 67 (2015), 2978–2989.
32. Trbojevic Akmacic, I., Ventham, N.T., Theodoratou, E. et al., Inflammatory bowel disease associates with proinflammatory potential of the immunoglobulin G glycome. Inflamm. Bowel Dis. 21 (2015), 1237–1247.
33. Vučković, F., Theodoratou, E., Thaçi, K. et al., IgG glycome in colorectal cancer. Clin. Cancer Res. 22 (2016), 3078–3086.
34. Russell, A.C., Šimurina, M., Garcia, M.T. et al., The N-glycosylation of immunoglobulin G as a novel biomarker of Parkinson's disease. Glycobiology 27 (2017), 501–510.
35. Dall'Olio, F., Vanhooren, V., Chen, C.C., Slagboom, P.E., Wuhrer, M., Franceschi, C., N-glycomic biomarkers of biological aging and longevity: a link with inflammaging. Ageing Res. Rev. 12 (2013), 685–698.
36. Ferrara, C., Stuart, F., Sondermann, P., Brunker, P., Umana, P., The carbohydrate at FcgammaRIIIa Asn-162. An element required for high affinity binding to non-fucosylated IgG glycoforms. J. Biol. Chem. 281 (2006), 5032–5036.
37. 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. 74 (2001), 288–294.
38. Lauc, G., Huffman, J.E., Pucic, M. et al., Loci associated with N-glycosylation of human immunoglobulin G show pleiotropy with autoimmune diseases and haematological cancers. PLoS Genet., 9, 2013, e1003225.
39. Testa, R., Vanhooren, V., Bonfigli, A.R. et al., N-glycomic changes in serum proteins in type 2 diabetes mellitus correlate with complications and with metabolic syndrome parameters. PLoS One, 10, 2015, e0119983.
40. Itoh, N., Sakaue, S., Nakagawa, H. et al., Analysis of N-glycan in serum glycoproteins from db/db mice and humans with type 2 diabetes. Am. J. Physiol. Endocrinol. Metab. 293 (2007), E1069–E1077.
41. Ercan, A., Cui, J., Chatterton, D.E. et al., Aberrant IgG galactosylation precedes disease onset, correlates with disease activity, and is prevalent in autoantibodies in rheumatoid arthritis. Arthritis Rheum. 62 (2010), 2239–2248.
42. Menni, C., Keser, T., Mangino, M. et al., Glycosylation of immunoglobulin g: role of genetic and epigenetic influences. PLoS One, 8, 2013, e82558.
43. Lauc, G., Essafi, A., Huffman, J.E. et al., Genomics meets glycomics-the first GWAS study of human N-Glycome identifies HNF1alpha as a master regulator of plasma protein fucosylation. PLoS Genet., 6, 2010, e1001256.
44. Kooner, J.S., Saleheen, D., Sim, X. et al., Genome-wide association study in individuals of South Asian ancestry identifies six new type 2 diabetes susceptibility loci. Nat. Genet. 43 (2011), 984–989.
45. Hotamisligil, G.S., Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140 (2010), 900–917.
46. Donath, M.Y., Shoelson, S.E., Type 2 diabetes as an inflammatory disease. Vol. 11, 2011, 98–107.
47. Goldberg, R.B., Cytokine and cytokine-like inflammation markers, endothelial dysfunction, and imbalanced coagulation in development of diabetes and its complications. J. Clin. Endocrinol. Metab. 94 (2009), 3171–3182.
48. Hertle, E., Stehouwer, C.D.A., van Greevenbroek, M.M.J., The complement system in human cardiometabolic disease. Mol. Immunol. 61 (2014), 135–148.
49. Ghosh, P., Sahoo, R., Vaidya, A., Chorev, M., Halperin, J.A., Role of complement and complement regulatory proteins in the complications of diabetes. Endocr. Rev. 36 (2015), 272–288.
50. Holland, M., Yagi, H., Takahashi, N. et al., Differential glycosylation of polyclonal IgG, IgG-Fc and IgG-Fab isolated from the sera of patients with ANCA-associated systemic vasculitis. Biochim. Biophys. Acta 1760 (2006), 669–677.