Abstract
Human lifespan has increased significantly in the last 200 years, emphasizing our need to age healthily. Insights into molecular mechanisms of aging might allow us to slow down its rate or even revert it. Similar to aging, glycosylation is regulated by an intricate interplay of genetic and environmental factors. The dynamics of glycopattern variation during aging has been mostly explored for plasma/serum and immunoglobulin G (IgG) N-glycome, as we describe thoroughly in this chapter. In addition, we discuss the potential functional role of agalactosylated IgG glycans in aging, through modulation of inflammation level, as proposed by the concept of inflammaging. We also comment on the potential to use the plasma/serum and IgG N-glycome as a biomarker of healthy aging and on the interventions that modulate the IgG glycopattern. Finally, we discuss the current knowledge about animal models for human plasma/serum and IgG glycosylation and mention other, less explored, instances of glycopattern changes during organismal aging and cellular senescence.
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References
Adua E, Memarian E, Russell A et al (2019) High throughput profiling of whole plasma N-glycans in type II diabetes mellitus patients and healthy individuals: a perspective from a Ghanaian population. Arch Biochem Biophys 661:10–21. https://doi.org/10.1016/j.abb.2018.10.015
Ahn MY, Kim BJ, Kim HJ et al (2017) Anti-aging effect and gene expression profiling of dung beetle glycosaminoglycan in aged rats. Biomater Res 21:5. https://doi.org/10.1186/s40824-017-0091-9
Aminoff D, Anderson J, Dabich L, Gathmann WD (1980) Sialic acid content of erythrocytes in normal individuals and patients with certain hematologic disorders. Am J Hematol 9:381–389. https://doi.org/10.1002/ajh.2830090405
Apweiler R, Hermjakob H, Sharon N (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim Biophys Acta Gen Subj 1473:4–8. https://doi.org/10.1016/S0304-4165(99)00165-8
Arai Y, Martin-Ruiz CM, Takayama M et al (2015) Inflammation, but not telomere length, predicts successful ageing at extreme old age: a longitudinal study of semi-supercentenarians. EBioMedicine 2:1549–1558. https://doi.org/10.1016/j.ebiom.2015.07.029
Arivazhagan S, Kavitha K, Nagini S (1998) Glycoconjugate profile in plasma and erythrocytes of gastric cancer patients. Indian J Physiol Pharmacol 42:123–126
Arnold JN, Dwek RA, Rudd PM, Sim RB (2006) Mannan binding lectin and its interaction with immunoglobulins in health and in disease. Immunol Lett 106:103–110
Arnold JN, Wormald MR, Sim RB et al (2007) The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev Immunol 25:21–50. https://doi.org/10.1146/annurev.immunol.25.022106.141702
Baković MP, Selman MHJ, Hoffmann M et al (2013) High-throughput IgG fc N-glycosylation profiling by mass spectrometry of glycopeptides. J Proteome Res 12:821–831. https://doi.org/10.1021/pr300887z
Barrientos G, Habazin S, Novokmet M et al (2020) Changes in subclass-specific IgG fc glycosylation associated with the postnatal maturation of the murine immune system. Sci Rep 10:15243. https://doi.org/10.1038/s41598-020-71899-7
Bergström JP, Helander A (2008) Influence of alcohol use, ethnicity, age, gender, BMI and smoking on the serum transferrin glycoform pattern: implications for use of carbohydrate-deficient transferrin (CDT) as alcohol biomarker. Clin Chim Acta 388:59–67. https://doi.org/10.1016/j.cca.2007.10.011
Bernacki RJ, Niedbala MJ, Korytnyk W (1985) Glycosidases in cancer and invasion. Cancer Metastasis Rev 4:81–101. https://doi.org/10.1007/BF00047738
Bingle CD, Craven CJ (2002) PLUNC: a novel family of candidate host defence proteins expressed in the upper airways and nasopharynx. Hum Mol Genet 11:937–943. https://doi.org/10.1093/hmg/11.8.937
Bodman KB, Hutchings PR, Jeddi PA et al (1994) IgG glycosylation in autoimmune-prone strains of mice. Clin Exp Immunol 95:103–107. https://doi.org/10.1111/j.1365-2249.1994.tb06022.x
Bones J, Byrne JC, Odonoghue N et al (2011) Glycomic and glycoproteomic analysis of serum from patients with stomach cancer reveals potential markers arising from host defense response mechanisms. J Proteome Res 10:1246–1265. https://doi.org/10.1021/pr101036b
Borelli V, Vanhooren V, Lonardi E et al (2015) Plasma N-Glycome signature of down syndrome. J Proteome Res 14:4232–4245. https://doi.org/10.1021/acs.jproteome.5b00356
Bournazos S, Ravetch JV (2017) Diversification of IgG effector functions. Int Immunol 29:303–310. https://doi.org/10.1093/intimm/dxx025
Brinkman-Van Der Linden ECM, Havenaar EC, Van Ommen ECR et al (1996) Oral estrogen treatment induces a decrease in expression of sialyl Lewis x on α1-acid glycoprotein in females and male-to-female transsexuals. Glycobiology 6:407–412. https://doi.org/10.1093/glycob/6.4.407
Brunngraber EG, Webster JC (1986) Changes in glycoprotein carbohydrate content in the aging human brain. Neurochem Res 11:579–588. https://doi.org/10.1007/BF00965327
Buniello A, Macarthur JAL, Cerezo M et al (2019) The NHGRI-EBI GWAS Catalog of published genome-wide association studies, targeted arrays and summary statistics 2019. Nucleic Acids Res 47:D1005–D1012. https://doi.org/10.1093/nar/gky1120
Butler RN, Sprott R, Warner H et al (2004) Biomarkers of aging: from primitive organisms to humans. J Gerontol Ser A Biol Sci Med Sci 59:560–567
Callewaert N, Geysens S, Molemans F, Contreras R (2001) Ultrasensitive profiling and sequencing of N-linked oligosaccharides using standard DNA-sequencing equipment. Glycobiology 11:275–281. https://doi.org/10.1093/glycob/11.4.275
Callewaert N, Van Vlierberghe H, Van Hecke A et al (2004) Noninvasive diagnosis of liver cirrhosis using DNA sequencer-based total serum protein glycomics. Nat Med 10:429–434. https://doi.org/10.1038/nm1006
Calvert L, Atkinson H, Berry L, Chan A (2019) Age-dependent variation in glycosylation features of Alpha-2-macroglobulin. Cell Biochem Biophys 77:335–342. https://doi.org/10.1007/s12013-019-00883-4
Capri M, Olivieri F, Lanzarini C et al (2017) Identification of miR-31-5p, miR-141-3p, miR-200c-3p, and GLT1 as human liver aging markers sensitive to donor–recipient age-mismatch in transplants. Aging Cell 16:262–272. https://doi.org/10.1111/acel.12549
Catera M, Borelli V, Malagolini N et al (2016) Identification of novel plasma glycosylation-associated markers of aging. Oncotarget 7:7455–7468. https://doi.org/10.18632/oncotarget.7059
Chatterton BD, Mullington J, Yang H et al (2020) 0058 effects of acute Total sleep deprivation on human plasma N-glycans. Sleep 43:A23–A23. https://doi.org/10.1093/sleep/zsaa056.056
Chen CC, Engelborghs S, Dewaele S et al (2010) Altered serum glycomics in Alzheimer disease: a potential blood biomarker? Rejuvenation Res 13:439–444. https://doi.org/10.1089/rej.2009.0992
Chen G, Wang Y, Qiu L et al (2012) Human IgG fc-glycosylation profiling reveals associations with age, sex, female sex hormones and thyroid cancer. J Proteome 75:2824–2834. https://doi.org/10.1016/j.jprot.2012.02.001
Cheng HD, Tirosh I, de Haan N et al (2020) IgG fc glycosylation as an axis of humoral immunity in childhood. J Allergy Clin Immunol 145:710-713.e9. https://doi.org/10.1016/j.jaci.2019.10.012
Cheung P, Pawling J, Partridge EA et al (2007) Metabolic homeostasis and tissue renewal are dependent on β1,6GlcNAc-branched N-glycans. Glycobiology 17:828–837. https://doi.org/10.1093/glycob/cwm048
Clerc F, Reiding KR, Jansen BC et al (2016) Human plasma protein N-glycosylation. Glycoconj J 33:309–343. https://doi.org/10.1007/s10719-015-9626-2
Coutinho MF, Lacerda L, Alves S (2012) Glycosaminoglycan storage disorders: a review. Biochem Res Int 471325
Cruz-Jentoft AJ, Baeyens JP, Bauer JM et al (2010) Sarcopenia: European consensus on definition and diagnosis. Age Ageing 39:412–423. https://doi.org/10.1093/ageing/afq034
Cummings RD, Pierce JM (2014) The challenge and promise of glycomics. Chem Biol 21:1–15
Dall’Olio F (2018) Glycobiology of aging. Subcell Biochem 90:505–526
Dall’Olio F, Vanhooren V, Chen CC et al (2013) N-glycomic biomarkers of biological aging and longevity: a link with inflammaging. Ageing Res Rev 12:685–698. https://doi.org/10.1016/j.arr.2012.02.002
Darvin K, Randolph A, Ovalles S et al (2014) Plasma protein biomarkers of the geriatric syndrome of frailty. J Gerontol Ser A Biol Sci Med Sci 69(A):182–186. https://doi.org/10.1093/gerona/glt183
De Haan N, Reiding KR, Driessen G et al (2016) Changes in healthy human IgG fc-glycosylation after birth and during early childhood. J Proteome Res 15:1853–1861. https://doi.org/10.1021/acs.jproteome.6b00038
de Haan N, Reiding KR, Krištić J et al (2017) The N-glycosylation of mouse immunoglobulin G (IgG)-fragment crystallizable differs between IgG subclasses and strains. Front Immunol 8:608. https://doi.org/10.3389/fimmu.2017.00608
De Jong SE, Selman MHJ, Adegnika AA et al (2016) IgG1 fc N-glycan galactosylation as a biomarker for immune activation. Sci Rep 6:28207. https://doi.org/10.1038/srep28207
De Martinis M, Franceschi C, Monti D, Ginaldi L (2005) Inflamm-ageing and lifelong antigenic load as major determinants of ageing rate and longevity. FEBS Lett 579:2035–2039
de Vroome SW, Holst S, Girondo MR et al (2018) Serum N-glycome alterations in colorectal cancer associate with survival. Oncotarget 9:30610–30623. https://doi.org/10.18632/oncotarget.25753
Decker CF (2010) Infectious diseases in the athlete: an overview. Dis Mon 56:404–406. https://doi.org/10.1016/j.disamonth.2010.03.002
Dekkers G, Treffers L, Plomp R et al (2017) Decoding the human immunoglobulin G-glycan repertoire reveals a spectrum of fc-receptor- and complement-mediated-effector activities. Front Immunol 8:877. https://doi.org/10.3389/fimmu.2017.00877
Denzel MS, Storm NJ, Gutschmidt A et al (2014) Hexosamine pathway metabolites enhance protein quality control and prolong life. Cell 156:1167–1178. https://doi.org/10.1016/j.cell.2014.01.061
Dimri GP, Lee X, Basile G et al (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 92:9363–9367. https://doi.org/10.1073/pnas.92.20.9363
Ding N, Sun HN, Sun W et al (2011) Human serum N-glycan profiles are age and sex dependent. Age Ageing 40:568–575. https://doi.org/10.1093/ageing/afr084
Dobrossy L, Pavelic ZP, Bernacki RJ (1981) A correlation between cell surface Sialyltransferase, sialic acid, and glycosidase activities and the Implantability of b16 murine melanoma. Cancer Res 41:2262–2266
Doherty M, Theodoratou E, Walsh I et al (2018) Plasma N-glycans in colorectal cancer risk. Sci Rep 8:8655. https://doi.org/10.1038/s41598-018-26805-7
Dotz V, Wuhrer M (2019) N-glycome signatures in human plasma: associations with physiology and major diseases. FEBS Lett 593:2966–2976. https://doi.org/10.1002/1873-3468.13598
Dotz V, Lemmers RFH, Reiding KR et al (2018) Plasma protein N-glycan signatures of type 2 diabetes. Biochim Biophys Acta Gen Subj 1862:2613–2622. https://doi.org/10.1016/j.bbagen.2018.08.005
Dragsten P, McLellan WL, Hart IR et al (1980) Cell surface properties of B16 melanoma variants with differing metastatic potential. Cancer Res 40:1645–1651
Dunn-Walters D, Boursier L, Spencer J (2000) Effect of somatic hypermutation on potential N-glycosylation sites in human immunoglobulin heavy chain variable regions. Mol Immunol 37:107–113. https://doi.org/10.1016/S0161-5890(00)00038-9
Dunston CR, Choudhury K, Griffiths HR (2012) Terminal galactose residues on transferrin are increased in midlife adults compared to young adults. Proteomics 12:3147–3153. https://doi.org/10.1002/pmic.201100506
Durocher JR, Payne RC, Conrad ME (1975) Role of sialic acid in erythrocyte survival. Blood 45:11–20. https://doi.org/10.1182/blood.v45.1.11.bloodjournal45111
Ercan A, Kohrt WM, Cui J et al (2017) Estrogens regulate glycosylation of IgG in women and men. JCI Insight 2:e89703. https://doi.org/10.1172/jci.insight.89703
Eylar EH, Madoff MA, Brody OV, Oncley JL (1962) The contribution of sialic acid to the surface charge of the erythrocyte. J Biol Chem 237:1992–2000. https://doi.org/10.1016/S0021-9258(19)73972-6
Fernandes HP, Cesar CL, Barjas-Castro ML (2011) Electrical properties of the red blood cell membrane and immunohematological investigation. Rev Bras Hematol Hemoter 33:297–301
Franceschi C (2007) Inflammaging as a major characteristic of old people: can it be prevented or cured? Nutr Rev 65:S173–S176. https://doi.org/10.1111/j.1753-4887.2007.tb00358.x
Franceschi C, Bonafè M, Valensin S et al (2000) Inflamm-aging. An evolutionary perspective on immunosenescence. Ann N Y Acad Sci 908:244–254. https://doi.org/10.1111/j.1749-6632.2000.tb06651.x
Franceschi C, Capri M, Monti D et al (2007) Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev 128:92–105. https://doi.org/10.1016/j.mad.2006.11.016
Franceschi C, Garagnani P, Morsiani C et al (2018) The continuum of aging and age-related diseases: common mechanisms but different rates. Front Med 5:61
Garnham R, Scott E, Livermore KE, Munkley J (2019) ST6GAL1: a key player in cancer. Oncol Lett 18:983–989
Gattegno L, Bladier D, Garnier M, Cornillot P (1976) Changes in carbohydrate content of surface membranes of human erythrocytes during ageing. Carbohydr Res 52:197–208. https://doi.org/10.1016/S0008-6215(00)85960-1
Gilbertson B, Edenborough K, McVernon J, Brown LE (2019) Inhibition of influenza a virus by human infant saliva. Viruses 11:766. https://doi.org/10.3390/v11080766
Gligorijević N, Zámorová Križáková M, Penezić A et al (2018) Structural and functional changes of fibrinogen due to aging. Int J Biol Macromol 108:1028–1034. https://doi.org/10.1016/j.ijbiomac.2017.11.016
Gliwicz J (1983) Age structure. In: Acta Theriol. (Warsz). https://ourworldindata.org/age-structure. Accessed 8 Jul 2020
Gornik O, Wagner J, Pučić M et al (2009) Stability of N-glycan profiles in human plasma. Glycobiology 19:1547–1553. https://doi.org/10.1093/glycob/cwp134
Gornik O, Pavić T, Lauc G (2012) Alternative glycosylation modulates function of IgG and other proteins - implications on evolution and disease. Biochim Biophys Acta Gen Subj 1820:1318–1326
Gotovac K, Gornik O, Telarović S, et al (2014) Glycosylation profiling in plasma of patients with Parkinson’s disease reveals putative biomarkers
Graham Ruby J, Wright KM, Rand KA et al (2018) Estimates of the heritability of human longevity are substantially inflated due to assortative mating. Genetics 210:1109–1124. https://doi.org/10.1534/genetics.118.301613
Greto V, Cvetko A, Štambuk T et al (2020) Extensive weight loss can reduce immune age by altering IgG N-glycosylation. medRxiv:2020.04.24.20077867. https://doi.org/10.1101/2020.04.24.20077867
Gudelj I, Keser T, Vučković F et al (2015) Estimation of human age using N-glycan profiles from bloodstains. Int J Legal Med 129:955–961. https://doi.org/10.1007/s00414-015-1162-x
Gudelj I, Lauc G, Pezer M (2018) Immunoglobulin G glycosylation in aging and diseases. Cell Immunol 333:65–79. https://doi.org/10.1016/j.cellimm.2018.07.009
Hadengue AL, Del-Pino M, Simon A, Levenson J (1998) Erythrocyte disaggregation shear stress, sialic acid, and cell aging in humans. Hypertension 32:324–330. https://doi.org/10.1161/01.HYP.32.2.324
Hajat C, Stein E (2018) The global burden of multiple chronic conditions: a narrative review. Prev Med Reports 12:284–293
Halim A, Nilsson J, Rüetschi U et al (2012) Human urinary glycoproteomics; attachment site specific analysis of N- and O-linked glycosylations by CID and ECD. Mol Cell Proteomics 11:M111.013649. https://doi.org/10.1074/mcp.M111.013649
Hamczyk MR, Nevado RM, Barettino A et al (2020) Biological versus chronological aging: JACC focus seminar. J Am Coll Cardiol 75:919–930
Han J, Pan Y, Gu Y et al (2020) Profiling of IgG N-glycome during mouse aging: Fucosylated diantennary glycans containing one Neu5Gc-linked LacNAc are associated with age. J Proteome 229:103966. https://doi.org/10.1016/j.jprot.2020.103966
Hanisch F, Weidemann W, Großmann M et al (2013) Sialylation and muscle performance: sialic acid is a marker of muscle ageing. PLoS One 8:e80520. https://doi.org/10.1371/journal.pone.0080520
Harpole M, Davis J, Espina V (2016) Current state of the art for enhancing urine biomarker discovery. Expert Rev Proteomics 13:609–626
Hartshorn KL, White MR, Mogues T et al (2003) Lung and salivary scavenger receptor glycoprotein-340 contribute to the host defense against influenza A viruses. Am J Physiol Lung Cell Mol Physiol 285:L1066–L1076. https://doi.org/10.1152/ajplung.00057.2003
Haxho F, Allison S, Alghamdi F et al (2014) Oseltamivir phosphate monotherapy ablates tumor neovascularization, growth, and metastasis in mouse model of human triple-negative breast adenocarcinoma. Breast Cancer Targets Ther 6:191–203. https://doi.org/10.2147/BCTT.S74663
Haxho F, Neufeld RJ, Szewczuk MR (2016) Neuraminidase-1: a novel therapeutic target in multistage tumorigenesis. Oncotarget 7:40860–40881. https://doi.org/10.18632/oncotarget.8396
Hayflick L (2007) Entropy explains aging, genetic determinism explains longevity, and undefined terminology explains misunderstanding both. PLoS Genet 3:2351–2354
Hennig R, Cajic S, Borowiak M et al (2016) Towards personalized diagnostics via longitudinal study of the human plasma N-glycome. Biochim Biophys Acta Gen Subj 1860:1728–1738. https://doi.org/10.1016/j.bbagen.2016.03.035
Herskind AM, McGue M, Holm NV et al (1996) The heritability of human longevity: a population-based study of 2872 Danish twin pairs born 1870-1900. Hum Genet 97:319–323. https://doi.org/10.1007/BF02185763
Hodoniczky J, Yuan ZZ, James DC (2005) Control of recombinant monoclonal antibody effector functions by fc N-glycan remodeling in vitro. Biotechnol Prog 21:1644–1652. https://doi.org/10.1021/bp050228w
Hofman VJ, Moreilhon C, Brest PD et al (2007) Gene expression profiling in human gastric mucosa infected with helicobacter pylori. Mod Pathol 20:974–989. https://doi.org/10.1038/modpathol.3800930
Huffman JE, Knežević A, Vitart V et al (2011) Polymorphisms in B3GAT1, SLC9A9 and MGAT5 are associated with variation within the human plasma N-glycome of 3533 European adults. Hum Mol Genet 20:5000–5011. https://doi.org/10.1093/hmg/ddr414
Iida M, Matsuno Y, Watanabe A et al (2019) A sialo-oligosaccharide-rich mucin-like molecule specifically detected in the submandibular glands of aged mice. Arch Oral Biol 97:52–58. https://doi.org/10.1016/j.archoralbio.2018.10.011
Inouye SK, Studenski S, Tinetti ME, Kuchel GA (2007) Geriatric syndromes: clinical, research, and policy implications of a core geriatric concept. J Am Geriatr Soc 55:780–791
Itakura Y, Sasaki N, Kami D et al (2016) N- and O-glycan cell surface protein modifications associated with cellular senescence and human aging. Cell Biosci 6:14. https://doi.org/10.1186/s13578-016-0079-5
Itakura Y, Sasaki N, Toyoda M (2018) Qualitative and quantitative alterations in intracellular and membrane glycoproteins maintain the balance between cellular senescence and human aging. Aging (Albany NY) 10:2190–2208. https://doi.org/10.18632/aging.101540
Ji H, Ohmura K, Mahmood U et al (2002) Arthritis critically dependent on innate immune system players. Immunity 16:157–168. https://doi.org/10.1016/S1074-7613(02)00275-3
Johnson TE (2006) Recent results: biomarkers of aging. Exp Gerontol 41:1243–1246
Jones MB, Oswald DM, Joshi S et al (2016) B-cell-independent sialylation of IgG. Proc Natl Acad Sci U S A 113:7207–7212. https://doi.org/10.1073/pnas.1523968113
Jurić J, Kohrt WM, Kifer D et al (2020) Effects of estradiol on biological age measured using the glycan age index. Aging (Albany NY) 12:19756–19765. https://doi.org/10.18632/aging.104060
Karsten CM, Pandey MK, Figge J et al (2012) Anti-inflammatory activity of IgG1 mediated by fc galactosylation and association of FcγRIIB and dectin-1. Nat Med 18:1401–1406. https://doi.org/10.1038/nm.2862
Kato T, Wang Y, Yamaguchi K et al (2001) Overexpression of lysosomal-type sialidase leads to suppression of metastasis associated with reversion of malignant phenotype in murine B16 melanoma cells. Int J Cancer 92:797–804. https://doi.org/10.1002/ijc.1268
Kennedy BK, Berger SL, Brunet A et al (2014) Geroscience: linking aging to chronic disease. Cell 159:709–713
Keser T, Gornik I, Vučković F et al (2017) Increased plasma N-glycome complexity is associated with higher risk of type 2 diabetes. Diabetologia 60:2352–2360. https://doi.org/10.1007/s00125-017-4426-9
Keusch J, Levy Y, Shoenfeld Y, Youinou P (1996) Analysis of different glycosylation states in IgG subclasses. Clin Chim Acta 252:147–158. https://doi.org/10.1016/0009-8981(96)06326-7
Khoury GA, Baliban RC, Floudas CA (2011) Proteome-wide post-translational modification statistics: frequency analysis and curation of the swiss-prot database. Sci Rep 1:90. https://doi.org/10.1038/srep00090
Kikuchi N, Narimatsu H (2006) Bioinformatics for comprehensive finding and analysis of glycosyltransferases. Biochim Biophys Acta Gen Subj 1760:578–583
Klarić L, Tsepilov YA, Stanton CM et al (2020) Glycosylation of immunoglobulin G is regulated by a large network of genes pleiotropic with inflammatory diseases. Sci Adv 6:eaax0301. https://doi.org/10.1126/sciadv.aax0301
Klei TRL, De Back DZ, Asif PJ et al (2018) Glycophorin-C sialylation regulates Lu/BCAM adhesive capacity during erythrocyte aging. Blood Adv 2:14–24. https://doi.org/10.1182/bloodadvances.2017013094
Knežević A, Polašek O, Gornik O et al (2009) Variability, heritability and environmental determinants of human plasma n-glycome. J Proteome Res 8:694–701. https://doi.org/10.1021/pr800737u
Knežević A, Gornik O, Polašek O et al (2010) Effects of aging, body mass index, plasma lipid profiles, and smoking on human plasma N-glycans. Glycobiology 20:959–969. https://doi.org/10.1093/glycob/cwq051
Knežević A, Bones J, Kračun SK et al (2011) High throughput plasma N-glycome profiling using multiplexed labelling and UPLC with fluorescence detection. Analyst 136:4670–4673. https://doi.org/10.1039/c1an15684e
Kochanek KD, Murphy S, Xu J, Arias E (2017) Mortality in the United States, 2016. NCHS data brief 1–8
Komosinska-Vassev K, Blat D, Olczyk P et al (2014) Urinary glycosaminoglycan (uGAG) excretion in healthy pediatric and adolescent population. Clin Biochem 47:1341–1343. https://doi.org/10.1016/j.clinbiochem.2014.06.012
Konjevod M, Tudor L, Svob Strac D et al (2019) Metabolomic and glycomic findings in posttraumatic stress disorder. Prog Neuro-Psychopharmacol Biol Psychiatry 88:181–193. https://doi.org/10.1016/j.pnpbp.2018.07.014
Krapp S, Mimura Y, Jefferis R et al (2003) Structural analysis of human IgG-fc glycoforms reveals a correlation between glycosylation and structural integrity. J Mol Biol 325:979–989. https://doi.org/10.1016/S0022-2836(02)01250-0
Krištić J, Vučković F, Menni C et al (2014) Glycans are a novel biomarker of chronological and biological ages. J Gerontol Ser A Biol Sci Med Sci 69:779–789. https://doi.org/10.1093/gerona/glt190
Krištić J, Zaytseva OO, Ram R et al (2018) Profiling and genetic control of the murine immunoglobulin G glycome. Nat Chem Biol 14:516–524. https://doi.org/10.1038/s41589-018-0034-3
Kristic J, Lauc G, Pezer M (2021a) Glycosylation of IgG in ageing, manuscript revision in preparation. Clin Chim Acta
Kristic J, Sharapov SZ, Aulchenko YS (2021b) Quantitative genetics of human protein N-glycosylation. In: The role of glycosylation in health and disease. Springer Nature. Book chapter in press
Kumar D, Rizvi SI (2013) Erythrocyte membrane bound and plasma sialic acid during aging. Biol 68:762–765. https://doi.org/10.2478/s11756-013-0207-1
Laroy W, Contreras R, Callewaert N (2006) Glycome mapping on DNA sequencing equipment. Nat Protoc 1:397–405. https://doi.org/10.1038/nprot.2006.60
Lauc G (2016) Precision medicine that transcends genomics: Glycans as integrators of genes and environment. Biochim Biophys Acta Gen Subj 1860:1571–1573. https://doi.org/10.1016/j.bbagen.2016.05.001
Lauc G, Essafi A, Huffman JE et al (2010) Genomics meets glycomics-the first gwas study of human N-glycome identifies HNF1A as a master regulator of plasma protein fucosylation. PLoS Genet 6:1–14. https://doi.org/10.1371/journal.pgen.1001256
Lauc G, Huffman JE, Pučić M et al (2013) Loci associated with N-glycosylation of human immunoglobulin G show Pleiotropy with autoimmune diseases and haematological cancers. PLoS Genet 9:e1003225. https://doi.org/10.1371/journal.pgen.1003225
Lauc G, Pezer M, Rudan I, Campbell H (2016) Mechanisms of disease: the human N-glycome. Biochim Biophys Acta Gen Subj 1860:1574–1582. https://doi.org/10.1016/j.bbagen.2015.10.016
Lee J, Ha S, Kim M et al (2020) Spatial and temporal diversity of glycome expression in mammalian brain. Proc Natl Acad Sci U S A 117:28743–28753. https://doi.org/10.1073/pnas.2014207117
Li H, Patel V, DiMartino SE et al (2020) An in-depth comparison of the Pediatric and adult urinary N-glycomes. Mol Cell Proteomics 19:1767–1776. https://doi.org/10.1074/mcp.RA120.002225
Lindahl U, Couchman J, Kimata K, Esko JD (2015) Proteoglycans and Sulfated Glycosaminoglycans. Essentials of Glycobiology. Cold Spring Harbor Laboratory Press, In
Liu L (2015) Antibody glycosylation and its impact on the pharmacokinetics and pharmacodynamics of monoclonal antibodies and fc-fusion proteins. J Pharm Sci 104:1866–1884
Loo JA, Yan W, Ramachandran P, Wong DT (2010) Comparative human salivary and plasma proteomes. J Dent Res 89:1016–1023
López-Otín C, Blasco MA, Partridge L et al (2013) The hallmarks of aging. Cell 153:1194. https://doi.org/10.1016/j.cell.2013.05.039
Lu JP, Knežević A, Wang YX et al (2011) Screening novel biomarkers for metabolic syndrome by profiling human plasma N-glycans in Chinese han and Croatian populations. J Proteome Res 10:4959–4969. https://doi.org/10.1021/pr2004067
MacAuley MS, Crocker PR, Paulson JC (2014) Siglec-mediated regulation of immune cell function in disease. Nat Rev Immunol 14:653–666
Maier AB, Westendorp RGJ, Van Heemst D (2007) β-Galactosidase activity as a biomarker of replicative senescence during the course of human fibroblast cultures. Ann N Y Acad Sci 1100:323–332
Malamud D (2011) Saliva as a Diagnostic Fluid. Dent Clin N Am 55:159–178
Malhotra R, Wormald MR, Rudd PM et al (1995) Glycosylation changes of IgG associated with rheumatooid arthritis can activate complement via the mannose-binding protein. Nat Med 1:237–243. https://doi.org/10.1038/nm0395-237
Manhardt CT, Punch PR, Dougher CWL, Lau JTY (2017) Extrinsic sialylation is dynamically regulated by systemic triggers in vivo. J Biol Chem 292:13514–13520. https://doi.org/10.1074/jbc.C117.795138
Mazzanti L, Rabini RA, Salvolini E et al (1997) Sialic acid, diabetes, and aging: a study on the erythrocyte membrane. Metabolism 46:59–61. https://doi.org/10.1016/S0026-0495(97)90168-2
McLachlan F, Timofeeva M, Bermingham M et al (2016) A case-control study in an Orcadian population investigating the relationship between human plasma N-glycans and metabolic syndrome. J Glycomics Lipidomics 6:3. https://doi.org/10.4172/2153-0637.1000139
Mehdi MM, Singh P, Rizvi SI (2012) Erythrocyte sialic acid content during aging in humans: correlation with markers of oxidative stress. Dis Markers 32:179–186. https://doi.org/10.3233/DMA-2011-0871
Menni C, Keser T, Mangino M et al (2013) Glycosylation of immunoglobulin G: role of genetic and epigenetic influences. PLoS One 8:e82558. https://doi.org/10.1371/journal.pone.0082558
Merleev AA, Park D, Xie Y et al (2020) A site-specific map of the human plasma glycome and its age and gender-associated alterations. Sci Rep 10:17505. https://doi.org/10.1038/s41598-020-73588-x
Meyer SJ, Linder AT, Brandl C, Nitschke L (2018) B cell Siglecs-news on Signaling and its interplay with ligand binding. Front Immunol 9:2820
Mimura Y, Church S, Ghirlando R et al (2000) 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 37:697–706. https://doi.org/10.1016/S0161-5890(00)00105-X
Mistry K, Kalia K (2009) Non enzymatic glycosylation of IgG and their urinary excretion in patients with diabetic nephropathy. Indian J Clin Biochem 24:159–165. https://doi.org/10.1007/s12291-009-0029-7
Mitchell SJ, Scheibye-Knudsen M, Longo DL, De Cabo R (2015) Animal models of aging research: implications for human aging and age-related diseases. Annu Rev Anim Biosci 3:283–303. https://doi.org/10.1146/annurev-animal-022114-110829
Miura Y, Endo T (2016) Glycomics and glycoproteomics focused on aging and age-related diseases – glycans as a potential biomarker for physiological alterations. Biochim Biophys Acta Gen Subj 1860:1608–1614
Miura Y, Hashii N, Tsumoto H et al (2015) Change in N-glycosylation of plasma proteins in Japanese semisupercentenarians. PLoS One 10:e0142645. https://doi.org/10.1371/journal.pone.0142645
Miura Y, Hashii N, Ohta Y et al (2018) Characteristic glycopeptides associated with extreme human longevity identified through plasma glycoproteomics. Biochim Biophys Acta Gen Subj 1862:1462–1471. https://doi.org/10.1016/j.bbagen.2018.03.025
Miyahara K, Nouso K, Saito S et al (2013) Serum glycan markers for evaluation of disease activity and prediction of clinical course in patients with ulcerative colitis. PLoS One 8:e74861. https://doi.org/10.1371/journal.pone.0074861
Monti D, Ostan R, Borelli V et al (2017) Inflammaging and human longevity in the omics era. Mech Ageing Dev 165:129–138. https://doi.org/10.1016/j.mad.2016.12.008
Moremen KW, Tiemeyer M, Nairn AV (2012) Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol 13:448–462. https://doi.org/10.1038/nrm3383
Moreno-Villanueva M, Morath J, Vanhooren V et al (2013) N-glycosylation profiling of plasma provides evidence for accelerated physiological aging in post-traumatic stress disorder. Transl Psychiatry 3:e320. https://doi.org/10.1038/tp.2013.93
Müller J, Lunz B, Schwab I et al (2015) Siglec-G deficiency leads to autoimmunity in aging C57BL/6 mice. J Immunol 195:51–60. https://doi.org/10.4049/jimmunol.1403139
Murphy SL, Xu J, Kochanek KD, Arias E (2018) Mortality in the United States, 2017. NCHS data brief 1–8
Narimatsu H (2006) Human glycogene cloning: focus on β3-glycosyltransferase and β4-glycosyltransferase families. Curr Opin Struct Biol 16:567–575
Nasirikenari M, Segal BH, Ostberg JR et al (2006) Altered granulopoietic profile and exaggerated acute neutrophilic inflammation in mice with targeted deficiency in the sialyltransferase ST6Gal I. Blood 108:3397–3405. https://doi.org/10.1182/blood-2006-04-014779
Nasirikenari M, Chandrasekaran EV, Matta KL et al (2010) 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 87:457–466. https://doi.org/10.1189/jlb.1108704
Nasirikenari M, Veillon L, Collins CC et al (2014) Remodeling of marrow hematopoietic stem and progenitor cells by non-self ST6Gal-1 sialyltransferase. J Biol Chem 289:7178–7189. https://doi.org/10.1074/jbc.M113.508457
Navarro CL, Cau P, Lévy N (2006) Molecular bases of progeroid syndromes. Hum Mol Genet 15:R151–R161
Nigam PK, Narain VS, Kumar A, Nigam PK (2006) Sialic acid in cardiovascular diseases. Indian J Clin Biochem 21:54–61
Nimmerjahn F, Ravetch JV (2008) Fcγ receptors as regulators of immune responses. Nat Rev Immunol 8:34–47. https://doi.org/10.1038/nri2206
Novak J, Tomana M, Shah GR et al (2005) Heterogeneity of IgG glycosylation in adult periodontal disease. J Dent Res 84:897–901. https://doi.org/10.1177/154405910508401005
O’Shea LK, Abdulkhalek S, Allison S et al (2014) Therapeutic targeting of Neu1 sialidase with oseltamivir phosphate (Tamiflu®) disables cancer cell survival in human pancreatic cancer with acquired chemoresistance. Onco Targets Ther 7:117–134. https://doi.org/10.2147/OTT.S55344
Ohkawa SI, Hata R, Nagai Y, Sugiura M (1972) Urinary excretion of acidic glycosaminoglycans in the aged. J Biochem 72:1495–1501. https://doi.org/10.1093/oxfordjournals.jbchem.a130041
Okajima T, Fukumoto S, Furukawat K et al (1999) Molecular basis for the progeroid variant of Ehlers-Danlos syndrome. Identification and characterization of two mutations in galactosyltransferase I gene. J Biol Chem 274:28841–28844. https://doi.org/10.1074/jbc.274.41.28841
Our World in Data (2020a) Life expectancy has improved globally. https://ourworldindata.org/life-expectancy#life-expectancy-has-improved-globally. Accessed 8 Jul 2020
Our World in Data (2020b) Why is life expectancy in the US lower than in other rich countries? https://ourworldindata.org/us-life-expectancy-low. Accessed 7 Nov 2020
Pacchiarotta T, Hensbergen PJ, Wuhrer M et al (2012) Fibrinogen alpha chain O-glycopeptides as possible markers of urinary tract infection. J Proteome 75:1067–1073. https://doi.org/10.1016/j.jprot.2011.10.021
Panda S, Ding JL (2015) Natural antibodies bridge innate and adaptive immunity. J Immunol 194:13–20. https://doi.org/10.4049/jimmunol.1400844
Pavić T, Dilber D, Kifer D et al (2018) N-glycosylation patterns of plasma proteins and immunoglobulin G in chronic obstructive pulmonary disease 11 medical and health sciences 1102 cardiorespiratory medicine and haematology. J Transl Med 16:323. https://doi.org/10.1186/s12967-018-1695-0
Pawłowski T, Mackiewicz A, Mackiewicz S (1986) Studies on microheterogeneity of acute-phase proteins in rheumatoid arthritis by using crossed affinoimmuno-electrophoresis with free concanavalin a. Behring Inst Mitt 80:11–15
Pearce OMT, Läubli H (2015) Sialic acids in cancer biology and immunity. Glycobiology 26:111–128. https://doi.org/10.1093/glycob/cwv097
Peng J, Vongpatanasin W, Sacharidou A et al (2019) Supplementation with the sialic acid precursor N-acetyl-D-Mannosamine breaks the link between obesity and hypertension. Circulation 140:2005–2018. https://doi.org/10.1161/CIRCULATIONAHA.119.043490
Peschke B, Keller CW, Weber P et al (2017) Fc-galactosylation of human immunoglobulin gamma isotypes improves C1q binding and enhances complement-dependent cytotoxicity. Front Immunol 8:646. https://doi.org/10.3389/fimmu.2017.00646
Pezer M, Stambuk J, Perica M et al (2016) Effects of allergic diseases and age on the composition of serum IgG glycome in children. Sci Rep 6:33198. https://doi.org/10.1038/srep33198
Pincetic A, Bournazos S, Dilillo DJ et al (2014) Type i and type II fc receptors regulate innate and adaptive immunity. Nat Immunol 15:707–716. https://doi.org/10.1038/ni.2939
Pinho SS, Reis CA (2015) Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer 15:540–555
Pinti M, Appay V, Campisi J et al (2016) Aging of the immune system: focus on inflammation and vaccination. Eur J Immunol 46:2286–2301. https://doi.org/10.1002/eji.201546178
Plomp R, Dekkers G, Rombouts Y et al (2015) Hinge-region O-glycosylation of human immunoglobulin G3 (IgG3). Mol Cell Proteomics 14:1373–1384. https://doi.org/10.1074/mcp.M114.047381
Plomp R, Ruhaak LR, Uh HW et al (2017) Subclass-specific IgG glycosylation is associated with markers of inflammation and metabolic health. Sci Rep 7:12325. https://doi.org/10.1038/s41598-017-12495-0
Pučić M, Knežević A, Vidič J et al (2011) High throughput isolation and glycosylation analysis of IgG-variability and heritability of the IgG glycome in three isolated human populations. Mol Cell Proteomics 10:M111.010090–M111.010090. https://doi.org/10.1074/mcp.M111.010090
Pučić M, Mužinić A, Novokmet M et al (2012) Changes in plasma and IgG N-glycome during childhood and adolescence. Glycobiology 22:975–982. https://doi.org/10.1093/glycob/cws062
Qin Y, Zhong Y, Zhu M et al (2013) Age- and sex-associated differences in the glycopatterns of human salivary glycoproteins and their roles against influenza a virus. J Proteome Res 12:2742–2754. https://doi.org/10.1021/pr400096w
Qorri B, Harless W, Szewczuk MR (2020) Novel molecular mechanism of aspirin and celecoxib targeting mammalian neuraminidase-1 impedes epidermal growth factor receptor signaling axis and induces apoptosis in pancreatic cancer cells. Drug Des Devel Ther 14:4149–4167. https://doi.org/10.2147/DDDT.S264122
Quentin E, Gladen A, Rodén L, Kresse H (1990) A genetic defect in the biosynthesis of dermatan sulfate proteoglycan: galactosyltransferase I deficiency in fibroblasts from a patient with a progeroid syndrome. Proc Natl Acad Sci U S A 87:1342–1346. https://doi.org/10.1073/pnas.87.4.1342
Raghunathan R, Polinski NK, Klein J et al (2018) Glycomic and proteomic changes in aging brain nigrostriatal pathway. Mol Cell Proteomics 17:1778–1787. https://doi.org/10.1074/mcp.RA118.000680
Raghunathan R, Hogan JD, Labadorf A et al (2020) A glycomics and proteomics study of aging and Parkinson’s disease in human brain. Sci Rep 10:12804. https://doi.org/10.1038/s41598-020-69480-3
Reiding KR, Ruhaak LR, Uh HW et al (2017) Human plasma N-glycosylation as analyzed by matrix-assisted laser desorption/ionization-Fourier transform ion cyclotron resonance-MS associates with markers of inflammation and metabolic health. Mol Cell Proteomics 16:228–242. https://doi.org/10.1074/mcp.M116.065250
Rini JM, Esko JD (2015) Glycosyltransferases and glycan-processing enzymes. In: Essentials of glycobiology. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Robajac D, Masnikosa R, Vanhooren V et al (2014) The N-glycan profile of placental membrane glycoproteins alters during gestation and aging. Mech Ageing Dev 138:1–9. https://doi.org/10.1016/j.mad.2014.01.010
Royle L, Campbell MP, Radcliffe CM et al (2008) HPLC-based analysis of serum N-glycans on a 96-well plate platform with dedicated database software. Anal Biochem 376:1–12. https://doi.org/10.1016/j.ab.2007.12.012
Ruhaak LR, Huhn C, Waterreus WJ et al (2008) Hydrophilic interaction chromatography-based high-throughput sample preparation method for N-glycan analysis from total human plasma glycoproteins. Anal Chem 80:6119–6126. https://doi.org/10.1021/ac800630x
Ruhaak LR, Uh HW, Beekman M et al (2010a) Decreased levels of bisecting GLcNAc glycoforms of IgG are associated with human longevity. PLoS One 5:1–8. https://doi.org/10.1371/journal.pone.0012566
Ruhaak LR, Zauner G, Huhn C et al (2010b) Glycan labeling strategies and their use in identification and quantification. Anal Bioanal Chem 397:3457–3481. https://doi.org/10.1007/s00216-010-3532-z
Ruhaak LR, Uh HW, Beekman M et al (2011) Plasma protein N-glycan profiles are associated with calendar age, familial longevity and health. J Proteome Res 10:1667–1674. https://doi.org/10.1021/pr1009959
Ruhaak LR, Miyamoto S, Kelly K, Lebrilla CB (2012) N -glycan profiling of dried blood spots. Anal Chem 84:396–402. https://doi.org/10.1021/ac202775t
Ruhaak LR, Koeleman CAM, Uh HW et al (2013) Targeted biomarker discovery by high throughput glycosylation profiling of human plasma Alpha1-antitrypsin and immunoglobulin a. PLoS One 8:e73082. https://doi.org/10.1371/journal.pone.0073082
Russell AC, Kepka A, Trbojević-Akmačić I et al (2019a) Increased central adiposity is associated with pro-inflammatory immunoglobulin G N-glycans. Immunobiology 224:110–115. https://doi.org/10.1016/j.imbio.2018.10.002
Russell AC, Kepka A, Trbojević-Akmačić I et al (2019b) Why not use the immunoglobulin G N-Glycans as predictor variables in disease biomarker-phenotype association studies? A multivariate analysis. Omi A J Integr Biol 23:668–670. https://doi.org/10.1089/omi.2019.0155
Saldova R, Asadi Shehni A, Haakensen VD et al (2014) Association of N-glycosylation with breast carcinoma and systemic features using high-resolution quantitative UPLC. J Proteome Res 13:2314–2327. https://doi.org/10.1021/pr401092y
Sanda M, Benicky J, Wu J et al (2016) Increased sialylation of site specific O-glycoforms of hemopexin in liver disease. Clin Proteomics 13:1–12. https://doi.org/10.1186/s12014-016-9125-x
Saraswat K, Kumar R, Rizvi SI (2019) Glycolytic inhibitor 2-Deoxy-D-glucose at chronic low dose mimics calorie restriction in rats through Mitohormetic induction of reactive oxygen species. Rejuvenation Res 22:377–384. https://doi.org/10.1089/rej.2018.2125
Sarin HV, Gudelj I, Honkanen J et al (2019) Molecular pathways mediating immunosuppression in response to prolonged intensive physical training, low-energy availability, and intensive weight loss. Front Immunol 10:907. https://doi.org/10.3389/fimmu.2019.00907
Sarrats A, Saldova R, Pla E et al (2010) Glycosylation of liver acute-phase proteins in pancreatic cancer and chronic pancreatitis. Proteomics Clin Appl 4:432–448. https://doi.org/10.1002/prca.200900150
Sasaki N, Itakura Y, Toyoda M (2017) Sialylation regulates myofibroblast differentiation of human skin fibroblasts. Stem Cell Res Ther 8:81. https://doi.org/10.1186/s13287-017-0534-1
Sawada M, Moriya S, Saito S et al (2002) Reduced sialidase expression in highly metastatic variants of mouse colon adenocarcinoma 26 and retardation of their metastatic ability by sialidase overexpression. Int J Cancer 97:180–185. https://doi.org/10.1002/ijc.1598
Schachter H, Freeze HH (2009) Glycosylation diseases: quo vadis? Biochim Biophys Acta Mol basis Dis 1792:925–930
Schaffert A, Hanić M, Novokmet M et al (2020) Minimal B cell extrinsic IgG glycan modifications of pro- and anti-inflammatory IgG preparations in vivo. Front Immunol 10:3024. https://doi.org/10.3389/fimmu.2019.03024
Schwarz F, Pearce OMT, Wang X et al (2015) Siglec receptors impact mammalian lifespan by modulating oxidative stress. elife 4:e06184. https://doi.org/10.7554/eLife.06184
Selman MHJ, McDonnell LA, Palmblad M et al (2010) Immunoglobulin G glycopeptide profiling by matrix-assisted laser desorption ionization Fourier transform ion cyclotron resonance mass spectrometry. Anal Chem 82:1073–1081. https://doi.org/10.1021/ac9024413
Shade KTC, Platzer B, Washburn N et al (2015) A single glycan on IgE is indispensable for initiation of anaphylaxis. J Exp Med 212:457–467. https://doi.org/10.1084/jem.20142182
Shamsi KS, Pierce A, Ashton AS et al (2012) Proteomic screening of glycoproteins in human plasma for frailty biomarkers. J Gerontol Ser A Biol Sci Med Sci 67(A):853–864. https://doi.org/10.1093/gerona/glr224
Sharapov SZ, Tsepilov YA, Klaric L et al (2019) Defining the genetic control of human blood plasma N-glycome using genome-wide association study. Hum Mol Genet 28:2062–2077. https://doi.org/10.1093/hmg/ddz054
Sharapov SZ, Shadrina AS, Tsepilov YA, et al (2020) Replication of 15 loci involved in human plasma protein N-glycosylation in 4802 samples from four cohorts. Glycobiology cwaa053. https://doi.org/10.1093/glycob/cwaa053
Shen X, Klarić L, Sharapov S et al (2017) Multivariate discovery and replication of five novel loci associated with immunoglobulin G N-glycosylation. Nat Commun 8:447. https://doi.org/10.1038/s41467-017-00453-3
Shields RL, Lai J, Keck R et al (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human FcγRIII and antibody-dependent cellular toxicity. J Biol Chem 277:26733–26740. https://doi.org/10.1074/jbc.M202069200
Shikata K, Yasuda T, Takeuchi F et al (1998) Structural changes in the oligosaccharide moiety of human IgG with aging. Glycoconj J 15:683–689. https://doi.org/10.1023/A:1006936431276
Shimizu K, Hirose N, Ebihara Y et al (2004) Blood type B might imply longevity. Exp Gerontol 39:1563–1565. https://doi.org/10.1016/j.exger.2004.08.004
Shinkawa T, Nakamura K, Yamane N et al (2003) 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 278:3466–3473. https://doi.org/10.1074/jbc.M210665200
Shinozaki S, Nakamura T, Iimura M et al (2001) Upregulation of Reg 1α and GW112 in the epithelium of inflamed colonic mucosa. Gut 48:623–629. https://doi.org/10.1136/gut.48.5.623
Simantov R, Febbraio M, Crombie R et al (2001) Histidine-rich glycoprotein inhibits the antiangiogenic effect of thrombospondin-1. J Clin Invest 107:45–52. https://doi.org/10.1172/JCI9061
Simon F, Bork K, Gnanapragassam VS et al (2019) Increased expression of immature mannose-containing glycoproteins and sialic acid in aged mouse brains. Int J Mol Sci 20:6118. https://doi.org/10.3390/ijms20246118
Simunovic J, Vilaj M, Trbojevic-Akmacic I et al (2019) Comprehensive N-glycosylation analysis of immunoglobulin G from dried blood spots. Glycobiology 29:817–821. https://doi.org/10.1093/glycob/cwz061
Sonesson M, Wickström C, Kinnby B et al (2008) Mucins MUC5B and MUC7 in minor salivary gland secretion of children and adults. Arch Oral Biol 53:523–527. https://doi.org/10.1016/j.archoralbio.2008.01.002
Spazzafumo L, Mensà E, Matacchione G et al (2017) Age-related modulation of plasmatic beta-Galactosidase activity in healthy subjects and in patients affected by T2DM. Oncotarget 8:93338–93348. https://doi.org/10.18632/oncotarget.21848
Speicher DJ, Luinstra K, Smith EJ et al (2020) Non-invasive detection of IgG antibodies from common pathogenic viruses using oral flocked swabs. Diagn Microbiol Infect Dis 97:115038. https://doi.org/10.1016/j.diagmicrobio.2020.115038
Stack KM, Papas AS (2001) Xerostomia: Etiology and clinical management. Nutr Clin Care 4:15–21. https://doi.org/10.1046/j.1523-5408.2001.00103.x
Štambuk J, Nakić N, Vučković F et al (2020) Global variability of the human IgG glycome. Aging (Albany NY) 12:1–13. https://doi.org/10.18632/AGING.103884
Stanley P, Cummings RD (2015) Structures common to different Glycans. Essentials of Glycobiology. Cold Spring Harbor Laboratory Press, In
States U (2017) The Shortening American Lifespan. https://www.commonwealthfund.org/blog/2017/shortening-american-lifespan. Accessed 13 Jul 2020
Sun YX (1988) Relationship between the contents of sialic acid and fucose on red cell membrane and occurrence of atrophic gastritis and gastric cancer. Chinese J Oncol 10:346–348
Sun S, Zhao F, Wang Q et al (2014) Analysis of age and gender associated N-glycoproteome in human whole saliva. Clin Proteomics 11:25. https://doi.org/10.1186/1559-0275-11-25
Šunderić M, Križáková M, Malenković V et al (2019) Changes due to ageing in the glycan structure of Alpha-2-macroglobulin and its reactivity with ligands. Protein J 38:23–29. https://doi.org/10.1007/s10930-018-9806-6
Tadokoro T, Yamamoto K, Kuwahara I et al (2006) Preferential reduction of the α-2-6-sialylation from cell surface N-glycans of human diploid fibroblastic cells by in vitro aging. Glycoconj J 23:443–452. https://doi.org/10.1007/s10719-006-7152-y
Testa R, Vanhooren V, Bonfigli AR et al (2015) N-Glycomic changes in serum proteins in type 2 diabetes mellitus correlate with complications and with metabolic syndrome parameters. PLoS One 10:e0119983. https://doi.org/10.1371/journal.pone.0119983
Tijardović M, Marijančević D, Bok D et al (2019) Intense physical exercise induces an anti-inflammatory change in IgG N-glycosylation profile. Front Physiol 10:1522. https://doi.org/10.3389/fphys.2019.01522
Titorenko VI (2018) Molecular and cellular mechanisms of aging and age-related disorders. Int J Mol Sci 19:2049
Tsuchiya N, Endo T, Matsuta K et al (1993) Detection of glycosylation abnormality in rheumatoid IgG using N- acetylglucosamine-specific Psathyrella velutina lectin. J Immunol 151:1137–1146
Uemura T, Shiozaki K, Yamaguchi K et al (2009) Contribution of sialidase NEU1 to suppression of metastasis of human colon cancer cells through desialylation of integrin β4. Oncogene 28:1218–1229. https://doi.org/10.1038/onc.2008.471
Ukraintseva SV, Yashin AI (2003) Opposite phenotypes of Cancer and aging Arise from alternative regulation of common Signaling pathways. Annals of the New York Academy of Sciences, In, pp 489–492
van de Bovenkamp FS, Hafkenscheid L, Rispens T, Rombouts Y (2016) The emerging importance of IgG fab glycosylation in immunity. J Immunol 196:1435–1441. https://doi.org/10.4049/jimmunol.1502136
van de Bovenkamp FS, Derksen NIL, van Breemen MJ et al (2018) Variable domain N-linked glycans acquired during antigen-specific immune responses can contribute to immunoglobulin G antibody stability. Front Immunol 9:740. https://doi.org/10.3389/fimmu.2018.00740
Vanderschaeghe D, Laroy W, Sablon E et al (2009) GlycoFibroTest is a highly performant liver fibrosis biomarker derived from DNA sequencer-based serum protein glycomics. Mol Cell Proteomics 8:986–994. https://doi.org/10.1074/mcp.M800470-MCP200
Vanderschaeghe D, Szekrényes Á, Wenz C et al (2010) High-throughput profiling of the serum N-glycome on capillary electrophoresis microfluidics systems: toward clinical implementation of GlycoHepatoTest. Anal Chem 82:7408–7415. https://doi.org/10.1021/ac101560a
Vanhooren V, Desmyter L, Liu XE et al (2007) N-glycomic changes in serum proteins during human aging. Rejuvenation Res 10:521–531. https://doi.org/10.1089/rej.2007.0556
Vanhooren V, Laroy W, Libert C, Chen C (2008) N-glycan profiling in the study of human aging. Biogerontology 9:351–356. https://doi.org/10.1007/s10522-008-9140-z
Vanhooren V, Liu XE, Franceschi C et al (2009) N-glycan profiles as tools in diagnosis of hepatocellular carcinoma and prediction of healthy human ageing. Mech Ageing Dev 130:92–97. https://doi.org/10.1016/j.mad.2008.11.008
Vanhooren V, Dewaele S, Libert C et al (2010) Serum N-glycan profile shift during human ageing. Exp Gerontol 45:738–743. https://doi.org/10.1016/j.exger.2010.08.009
Vanhooren V, Dewaele S, Kuro-o M et al (2011) Alteration in N-glycomics during mouse aging: a role for FUT8. Aging Cell 10:1056–1066. https://doi.org/10.1111/j.1474-9726.2011.00749.x
Varki A (2017) Biological roles of glycans. Glycobiology 27:3–49. https://doi.org/10.1093/glycob/cww086
Vilaj M, Gudelj I, Trbojević-Akmačić I et al (2019) IgG Glycans as a biomarker of biological age. In: Moskalev A (ed) Biomarkers of human aging. Springer, Dordrecht, pp 81–99
Wada Y, Azadi P, Costello CE et al (2007) Comparison of the methods for profiling glycoprotein glycans - HUPO human disease glycomics/proteome initiative multi-institutional study. Glycobiology 17:411–422. https://doi.org/10.1093/glycob/cwl086
Wahl A, Kasela S, Carnero-Montoro E et al (2018a) IgG glycosylation and DNA methylation are interconnected with smoking. Biochim Biophys Acta Gen Subj 1862:637–648. https://doi.org/10.1016/j.bbagen.2017.10.012
Wahl A, van den Akker E, Klaric L et al (2018b) Genome-wide association study on immunoglobulin G glycosylation patterns. Front Immunol 9:277. https://doi.org/10.3389/fimmu.2018.00277
Wandall HH, Rumjantseva V, Sørensen ALT et al (2012) The origin and function of platelet glycosyltransferases. Blood 120:625–635. https://doi.org/10.1182/blood-2012-02-409235
Wang X, Gu J, Miyoshi E et al (2006) Phenotype changes of Fut8 knockout mouse: Core Fucosylation is crucial for the function of growth factor receptor(s). Methods Enzymol 417:11–22
White MR, Helmerhorst EJ, Ligtenberg A et al (2009) Multiple components contribute to ability of saliva to inhibit influenza viruses. Oral Microbiol Immunol 24:18–24. https://doi.org/10.1111/j.1399-302X.2008.00468.x
Wittenbecher C, Štambuk T, Kuxhaus O et al (2020) Plasma N-glycans as emerging biomarkers of cardiometabolic risk: a prospective investigation in the epic-potsdamcohort study. Diabetes Care 43:661–668. https://doi.org/10.2337/dc19-1507
Wu SJ, Luo J, O’Neil KT et al (2010) Structure-based engineering of a monoclonal antibody for improved solubility. Protein Eng Des Sel 23:643–651. https://doi.org/10.1093/protein/gzq037
Xu J, Murphy SL, Kochanek KD, Arias E (2016) Mortality in the United States, 2015. NCHS data brief 1–8
Xu F, Laguna L, Sarkar A (2019) Aging-related changes in quantity and quality of saliva: where do we stand in our understanding? J Texture Stud 50:27–35
Yamada E, Tsukamoto Y, Sasaki R et al (1997) Structural changes of immunoglobulin G oligosaccharides with age in healthy human serum. Glycoconj J 14:401–405. https://doi.org/10.1023/A:1018582930906
Yu X, Wang Y, Kristic J et al (2016) Profiling IgG N-glycans as potential biomarker of chronological and biological ages: a community-based study in a Han Chinese population. Med (United States) 95:e4112. https://doi.org/10.1097/MD.0000000000004112
Zaytseva OO, Freidin MB, Keser T et al (2020) Heritability of human plasma N-Glycome. J Proteome Res 19:85–91. https://doi.org/10.1021/acs.jproteome.9b00348
Zierer J, Pallister T, Tsai PC et al (2016) Exploring the molecular basis of age-related disease comorbidities using a multi-omics graphical model. Sci Rep 6:37646. https://doi.org/10.1038/srep37646
Zoldoš V, Novokmet M, Bečeheli I, Lauc G (2013) Genomics and epigenomics of the human glycome. Glycoconj J 30:41–50. https://doi.org/10.1007/s10719-012-9397-y
Acknowledgements
We kindly thank our colleague Thomas Klaric for his help with the literature search on brain glycosylation , and our colleagues Olga O. Zaytseva and Lucija Klaric for a helpful discussion of glycosylation genome-wide association studies.
Disclosure of Interests
AC, JK, MMK, and MP are employees of Genos Ltd.—a private research organization that specializes in the high-throughput glycomic analysis and has several patents in the field. AC and MP are also employees of Genos Glycoscience Ltd.—a spin-off of Genos Ltd. that commercializes its scientific discoveries.
Ethical Approval
This work involves no human participants, animals, their data, or biological material, therefore no ethical approval was required.
Funding
This work was partly supported by the European Structural and Investment Funds IRI grant (#KK.01.2.1.01.0003), CEKOM grant (#KK.01.2.2.03.0006) and the Croatian Centre of Research Excellence in Personalized Healthcare grant (#KK.01.1.1.01.0010); as well as the “Research Cooperability” Program of the Croatian Science Foundation funded by the European Union from the European Social Fund under the Operational Programme Efficient Human Resources 2014–2020 (project PZS-2019-02-4277, Protein glycosylation in aging-related diseases through study of Down syndrome as accelerated aging condition).
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Cindrić, A., Krištić, J., Martinić Kavur, M., Pezer, M. (2021). Glycosylation and Aging. In: Lauc, G., Trbojević-Akmačić, I. (eds) The Role of Glycosylation in Health and Disease. Advances in Experimental Medicine and Biology, vol 1325. Springer, Cham. https://doi.org/10.1007/978-3-030-70115-4_17
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