Profiling IgG N-glycans as potential biomarker of chronological and biological ages: A community-based study in a Han Chinese population

Medicine (United States)

Volumn 95, Issue 28, 2016, Pages

  Yu, Xinwei ^a,b   Wang, Youxin ^a,b   Kristic, Jasminka ^c   Dong, Jing ^d   Chu, Xi ^d   Ge, Siqi ^a,b   Wang, Hao ^a   Fang, Honghong ^a   Gao, Qing ^a   Liu, Di ^a   Zhao, Zhongyao ^a   Peng, Hongli ^a   Bakovic, Maja Pucic ^c   Wu, Lijuan ^a   Song, Manshu ^a   Rudan, Igor ^e   Campbell, Harry ^e   Lauc, Gordan ^c   Wang, Wei ^a,b  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b EDITH COWAN UNIVERSITY   (Australia)

^c GENOS GLYCOSCIENCE RESEARCH LABORATORY   (Croatia)

^d CAPITAL MEDICAL UNIVERSITY   (China)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

biological age; biomarker; chronological age; immunoglobulin G; N glycan

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CREATININE; GLUCOSE; GLYCAN; HIGH DENSITY LIPOPROTEIN; IMMUNOGLOBULIN G; LOW DENSITY LIPOPROTEIN; TRIACYLGLYCEROL; BIOLOGICAL MARKER; GLYCOSYLATED IGG; POLYSACCHARIDE;

ADULT; AGE; AGED; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CLINICAL FEATURE; CORRELATION ANALYSIS; CROSS-SECTIONAL STUDY; FEMALE; GLUCOSE BLOOD LEVEL; HAN CHINESE; HUMAN; MAJOR CLINICAL STUDY; MALE; OBSERVATIONAL STUDY; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; CHINA; ETHNOLOGY; GLYCOSYLATION; LONGEVITY; METABOLISM; MIDDLE AGED;

ADULT; AGED; BIOMARKERS; CHINA; CROSS-SECTIONAL STUDIES; FEMALE; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN G; LONGEVITY; MALE; MIDDLE AGED; POLYSACCHARIDES;

EID: 84980007121     PISSN: 00257974     EISSN: 15365964     Source Type: Journal    
DOI: 10.1097/MD.0000000000004112     Document Type: Article

References (50)

1. Carlos LO, Maria AB, Linda P, et al. The hallmarks of aging. Cell 2013;153:1194-217.
2. Bryan GV, Stephen AK, Philip KM, et al. The effects of fitness on the aging process. J Am Acad Orthop Surg 2014;22:576-85.
3. Blair SN, Kohl HW, Paffenbarger RSJr, et al. Physical fitness and allcause mortality. A prospective study of healthy men and women. JAMA 1989;262:2395-401.
4. Hartl FU, Bracher A, Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011;475:324-32.
5. Koga H, Kaushik S, Cuervo AM. Protein homeostasis and aging: the importance of exquisite quality control. Ageing Res Rev 2011;10: 205-15.
6. Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. Nature 2008;451:1069-75.
7. Powers ET, Morimoto RI, Dillin A, et al. Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 2009;78:959-91.
8. Apweiler R, Hermjakob H, Sharon N. On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim Biophys Acta 1999;1473:4-8.
9. Alavi A, Axford JS. Sweet and sour: the impact of sugars on disease. Rheumatology (Oxford) 2008;47:760-70.
10. 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.
11. Parekh R, Roitt I, Isenberg D, et al. Age-related galactosylation of the Nlinked oligosaccharides of human serum IgG. J Exp Med 1988;167: 1731-6.
12. Vanhooren V, Desmyter L, Liu XE, et al. N-Glycomic changes in serum proteins during human aging. Rejuvenation Res 2007;10:521-31.
13. Vanhooren V, Laroy W, Libert C, et al. N-Glycan profiling in the study of human aging. Biogerontology 2008;9:351-6.
14. Vanhooren V, Liu XE, Franceschi C, et al. N-Glycan profiles as tools in diagnosis of hepatocellular carcinoma and prediction of healthy human ageing. Mech Ageing Dev 2009;130:92-7.
15. Lu JP, Knezevic A, Wang YX, et al. Screening novel biomarkers for metabolic syndrome by profiling human plasma N-glycans in Chinese Han and Croatian populations. J Proteome Res 2011;10:4959-69.
16. Junqueira LC, Carneiro J, Kelley RO. Basic Histology. 9th ed. New York, NY: McGraw-Hill; 1998.
17. Huber R, Deisenhofer J, Colman PM. Crystallographic structure studies of an IgG molecule and an Fc fragment. Nature 1976;264:415-20.
18. Franklin EC. Structure and function of immunoglobulins. Acta Endocrinol Suppl 1975;194:77-95.
19. Arnold JN, Wormald MR, Sim RB, et al. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev Immunol 2007;25:21-50.
20. Anthony RM, Ravetch JV. A novel role for the IgG Fc glycan: the antiinflammatory activity of sialylated IgG Fcs. J Clin Immunol 2010;30: S9-14.
21. Iida S, Misaka H, Inoue M, 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 Fcgamma RIIIa. Clin Cancer Res 2006;12:2879-87.
22. Scanlan CN, Burton DR, Dwek RA. Making autoantibodies safe. Proc Natl Acad Sci U S A 2008;105:4081-2.
23. Troelsen LN, Jacobsen S, Abrahams JL, et al. IgG glycosylation changes and MBL2 polymorphisms: associations with markers of systemic inflammation and joint destruction in rheumatoid arthritis. J Rheumatol 2012;39:463-9.
24. Parekh RB, Dwek RA, Sutton BJ, et al. Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature 1985;316:452-7.
25. Sjöwall C, Zapf J, von Löhneysen S, et al. Altered glycosylation of complexed native IgG molecules is associated with disease activity of systemic lupus erythematosus. Lupus 2015;24:569-81.
26. Vuckovic F, Kristic J, Gudelj I, et al. Association of systemic lupus erythematosus with decreased immunosuppressive potential of the IgG glycome. Arthritis Rheumatol 2015;67:2978-89.
27. Martin K, Talukder R, Hay FC, et al. Characterization of changes in IgG associated oligosaccharide profiles in rheumatoid arthritis, psoriatic arthritis, and ankylosing spondylitis using fluorophore linked carbohydrate electrophoresis. J Rheumatol 2001;28:1531-6.
28. Lundström SL, Yang H, Lyutvinskiy Y, et al. Blood plasma IgG Fc glycans are significantly altered in Alzheimer's disease and progressive mild cognitive impairment. J Alzheimers Dis 2014;38:567-79.
29. Shikata K, Yasuda T, Takeuchi F, et al. Structural changes in the oligosaccharide moiety of human IgG with aging. Glycoconj J 1998;15: 683-9.
30. Jasminka K, Frano V, Cristina M, et al. Glycans are a novel biomarker of chronological and biological ages. J Gerontol A Biol Sci Med Sci 2014;69:779-89.
31. Vanhooren V, Dewaele S, Libert C, et al. Serum N-glycan profile shift during human ageing. Exp Gerontol 2010;45:738-43.
32. Ruhaak LR, Uh HW, Beekman M, et al. Plasma protein N-glycan profiles are associated with calendar age, familial longevity and health. J Proteome Res 2011;10:1667-74.
33. 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 2010;20:959-69.
34. Pucić M, Knezević 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 2011;10:M111010090.
35. Menni C, Keser T, Mangino M, et al. Glycosylation of immunoglobulin: role of genetic and epigenetic influences. PLoS One 2013;8:e82558.
36. R Development Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.
37. Akaike H. A new look at the statistical model identification. IEEE Trans Automat Contr 1974;19:716-23.
38. Zhang WG, Zhu SY, Bai XJ, et al. Select aging biomarkers based on telomere length and chronological age to build a biological age equation. Age 2014;36:1201-11.
39. Nandakumar KS, Collin M, Happonen KE, et al. Dominant suppression of inflammation by glycan-hydrolyzed IgG. PNAS 2013;18:10252-7.
40. Anthony RM, Nimmerjahn F. The role of differential IgG glycosylation in the interaction of antibodies with FcgRs in vivo. Curr Opin Organ Transplant 2011;16:7-14.
41. Dall'olio F, Vanhooren V, Chen CC, et al. N-Glycomic biomarkers of biological aging and longevity: a linkwith inflammaging. Ageing Res Rev 2013;12:685-98.
42. Malhotra R, Wormald MR, Rudd PM, et al. Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat Med 1995;1:237-43.
43. Böhm S, Schwab I, Lux A, et al. The role of sialic acid as a modulator of the anti-inflammatory activity of IgG. Semin Immunopathol 2012;34: 443-53.
44. Anthony RM, Wermeling F, Ravetch JV. Novel roles for the IgG Fc glycan. Ann N Y Acad Sci 2012;1253:170-80.
45. Zoldos V, Novokmet M, Bečeheli I, et al. Genomics and epigenomics of the human glycome. Glycoconj J 2013;30:41-50.
46. Pucic M, Muzinic A, Novokmet M, et al. Changes in plasma and IgG Nglycome during childhood and adolescence. Glycobiology 2012;22: 975-82.
47. Karsten CM, Pandey MK, Figge J, et al. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of Fcgamma RIIB and dectin-1. Nat Med 2012;18:1401-6.
48. Isaak Q, Jan DL. Fc glycan-modulated immunoglobulin G effector functions. J Clin Immunol 2014;34:S51-5.
49. O'Neill LA, Hardie DG. Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature 2013;493:346-55.
50. Novokmet M, Lukic E, Vuckovic F, et al. Changes in IgG and total plasma protein glycomes in acute systemic inflammation. Sci Rep 2014;4:4347.