Human disease glycomics: technology advances enabling protein glycosylation analysis – part 2

ABSTRACT Introduction: The changes in glycan structures have been attributed to disease states for several decades. The surface glycosylation pattern is a signature of physiological state of a cell. In this review we provide a link between observed substructural glycan changes and a range of diseases. Areas covered: We highlight biologically relevant glycan substructure expression in cancer, inflammation, neuronal diseases and diabetes. Furthermore, the alterations in antibody glycosylation in a disease context are described. Expert commentary: Advances in technologies, as described in Part 1 of this review have now enabled the characterization of specific glycan structural markers of a range of disease states. The requirement of including glycomics in cross-disciplinary omics studies, such as genomics, proteomics, epigenomics, transcriptomics and metabolomics towards a systems glycobiology approach to understanding disease mechanisms and management are highlighted.

[1]  M. Abba,et al.  Lewis x Antigen is Associated to Head and Neck Squamous Cell Carcinoma Survival , 2018, Pathology & Oncology Research.

[2]  PyleLaura,et al.  Can Biomarkers Help Target Maturity-Onset Diabetes of the Young Genetic Testing in Antibody-Negative Diabetes? , 2018 .

[3]  K. Blennow,et al.  Proteomic studies of cerebrospinal fluid biomarkers of Alzheimer’s disease: an update , 2017, Expert review of proteomics.

[4]  Kiyoshi Saito,et al.  A unique glycan-isoform of transferrin in cerebrospinal fluid: A potential diagnostic marker for neurological diseases. , 2017, Biochimica et biophysica acta. General subjects.

[5]  N. Hacker,et al.  Tissue glycomics distinguish tumour sites in women with advanced serous adenocarcinoma , 2017, Molecular oncology.

[6]  Mao Zhang,et al.  The glycosyltransferase GnT-III activates Notch signaling and drives stem cell expansion to promote the growth and invasion of ovarian cancer , 2017, The Journal of Biological Chemistry.

[7]  R. Haltiwanger,et al.  Biological functions of fucose in mammals. , 2017, Glycobiology.

[8]  Karin Milde-Langosch,et al.  Role of protein glycosylation in cancer metastasis. , 2017, Seminars in cancer biology.

[9]  I. Rudan,et al.  The N-glycosylation of immunoglobulin G as a novel biomarker of Parkinson's disease , 2017, Glycobiology.

[10]  F. dall’Olio,et al.  Selectin Ligands Sialyl-Lewis a and Sialyl-Lewis x in Gastrointestinal Cancers , 2017, Biology.

[11]  A. Herr,et al.  Immunoglobulin Glycosylation Effects in Allergy and Immunity , 2016, Current Allergy and Asthma Reports.

[12]  G. Garden,et al.  Glial biomarkers in human central nervous system disease , 2016, Glia.

[13]  R. Zahedi.  Joining forces: studying multiple post-translational modifications to understand dynamic disease mechanisms , 2016, Expert review of proteomics.

[14]  P. Loadman,et al.  Polysialic Acid Sustains Cancer Cell Survival and Migratory Capacity in a Hypoxic Environment Original Citation , 2022 .

[15]  Daniel Kolarich,et al.  The promise of protein glycosylation for personalised medicine. , 2016, Biochimica et biophysica acta.

[16]  M. Przybyło,et al.  Towards understanding the role of sialylation in melanoma progression. , 2016, Acta biochimica Polonica.

[17]  M. Anugraham,et al.  Epigenetic activation of MGAT3 and corresponding bisecting GlcNAc shortens the survival of cancer patients , 2016, Oncotarget.

[18]  I. Gudelj,et al.  The Association Between Low Back Pain and Composition of IgG Glycome , 2016, Scientific Reports.

[19]  J. Gildersleeve,et al.  Perspectives on Anti-Glycan Antibodies Gleaned from Development of a Community Resource Database , 2016, ACS chemical biology.

[20]  W. Gao,et al.  Oncotargets and Therapy Dovepress Clinicopathological and Prognostic Significance of Sialyl Lewis X Overexpression in Patients with Cancer: a Meta-analysis , 2022 .

[21]  N. Taniguchi,et al.  Enzymes for N-Glycan Branching and Their Genetic and Nongenetic Regulation in Cancer , 2016, Biomolecules.

[22]  N. Packer,et al.  Site-Specific N-Glycosylation of Recombinant Pentameric and Hexameric Human IgM , 2016, Journal of The American Society for Mass Spectrometry.

[23]  N. Taniguchi,et al.  Atomic visualization of a flipped-back conformation of bisected glycans bound to specific lectins , 2016, Scientific Reports.

[24]  C. Freire-de-Lima,et al.  The Sweet Side of Immune Evasion: Role of Glycans in the Mechanisms of Cancer Progression , 2016, Front. Oncol..

[25]  O. Pearce,et al.  Sialic acids in cancer biology and immunity. , 2016, Glycobiology.

[26]  A. Piwowar,et al.  Changes in glycosylation of human blood plasma chitotriosidase in patients with type 2 diabetes , 2016, Glycoconjugate Journal.

[27]  A. Messina,et al.  CSF N-glycoproteomics for early diagnosis in Alzheimer's disease. , 2016, Journal of proteomics.

[28]  J. Buchner,et al.  Multi-Angle Effector Function Analysis of Human Monoclonal IgG Glycovariants , 2015, PloS one.

[29]  U. Reichl,et al.  Site-specific O-Glycosylation Analysis of Human Blood Plasma Proteins* , 2015, Molecular & Cellular Proteomics.

[30]  Takanori Nakamura,et al.  Cooperative Interactions of Oligosaccharide and Peptide Moieties of a Glycopeptide Derived from IgE with Galectin-9* , 2015, The Journal of Biological Chemistry.

[31]  Magnus Palmblad,et al.  MassyTools: A High-Throughput Targeted Data Processing Tool for Relative Quantitation and Quality Control Developed for Glycomic and Glycoproteomic MALDI-MS. , 2015, Journal of proteome research.

[32]  David E James,et al.  Terminal Galactosylation and Sialylation Switching on Membrane Glycoproteins upon TNF-Alpha-Induced Insulin Resistance in Adipocytes* , 2015, Molecular & Cellular Proteomics.

[33]  Manfred Wuhrer,et al.  Mass spectrometry for glycosylation analysis of biopharmaceuticals , 2015 .

[34]  S. Nishimura,et al.  A comprehensive glycome profiling of Huntington's disease transgenic mice. , 2015, Biochimica et biophysica acta.

[35]  R. Peracaula,et al.  Inflammatory cytokines regulate the expression of glycosyltransferases involved in the biosynthesis of tumor-associated sialylated glycans in pancreatic cancer cell lines. , 2015, Cytokine.

[36]  S. Pinho,et al.  Glycosylation in cancer: mechanisms and clinical implications , 2015, Nature Reviews Cancer.

[37]  Chi‐Huey Wong,et al.  A common glycan structure on immunoglobulin G for enhancement of effector functions , 2015, Proceedings of the National Academy of Sciences.

[38]  Ian Loke,et al.  Paucimannosidic glycoepitopes are functionally involved in proliferation of neural progenitor cells in the subventricular zone. , 2015, Glycobiology.

[39]  M. Tomita,et al.  Glycoengineered Monoclonal Antibodies with Homogeneous Glycan (M3, G0, G2, and A2) Using a Chemoenzymatic Approach Have Different Affinities for FcγRIIIa and Variable Antibody-Dependent Cellular Cytotoxicity Activities , 2015, PloS one.

[40]  M. Vankemmelbeke,et al.  Cancer cell associated glycans as targets for immunotherapy , 2015, Oncoimmunology.

[41]  H. Hildebrandt,et al.  Polysialic acid on SynCAM 1 in NG2 cells and on neuropilin‐2 in microglia is confined to intracellular pools that are rapidly depleted upon stimulation , 2015, Glia.

[42]  Jörn Lötsch,et al.  Pain research funding by the European Union Seventh Framework Programme , 2015, European journal of pain.

[43]  E. Fiebiger,et al.  A single glycan on IgE is indispensable for initiation of anaphylaxis , 2015, The Journal of experimental medicine.

[44]  P. Dittrich,et al.  A Microarray-Matrix-assisted Laser Desorption/Ionization-Mass Spectrometry Approach for Site-specific Protein N-glycosylation Analysis, as Demonstrated for Human Serum Immunoglobulin M (IgM)* , 2015, Molecular & Cellular Proteomics.

[45]  R. Testa,et al.  N-Glycomic Changes in Serum Proteins in Type 2 Diabetes Mellitus Correlate with Complications and with Metabolic Syndrome Parameters , 2015, PloS one.

[46]  N. Packer,et al.  Glycomic characterization of basal tears and changes with diabetes and diabetic retinopathy. , 2015, Glycobiology.

[47]  D. Shin,et al.  Spatially-resolved exploration of the mouse brain glycome by tissue glyco-capture (TGC) and nano-LC/MS. , 2015, Analytical chemistry.

[48]  C. Lebrilla,et al.  Glycans in the immune system and The Altered Glycan Theory of Autoimmunity: a critical review. , 2015, Journal of autoimmunity.

[49]  Richard D Cummings,et al.  Protein glycosylation in cancer. , 2015, Annual review of pathology.

[50]  S. Nagalla,et al.  Salivary Protein Glycosylation as a Noninvasive Biomarker for Assessment of Glycemia , 2014, Journal of diabetes science and technology.

[51]  F. dall’Olio,et al.  Sialosignaling: sialyltransferases as engines of self-fueling loops in cancer progression. , 2014, Biochimica et biophysica acta.

[52]  L. Lee,et al.  Differential Site Accessibility Mechanistically Explains Subcellular-Specific N-Glycosylation Determinants , 2014, Front. Immunol..

[53]  B. Julian,et al.  Enzymatic Sialylation of IgA1 O-Glycans: Implications for Studies of IgA Nephropathy , 2014, PloS one.

[54]  M. Anugraham,et al.  Specific Glycosylation of Membrane Proteins in Epithelial Ovarian Cancer Cell Lines: Glycan Structures Reflect Gene Expression and DNA Methylation Status * , 2014, Molecular & Cellular Proteomics.

[55]  Rita Gerardy-Schahn,et al.  Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. , 2014, Physiological reviews.

[56]  C. Oostenbrink,et al.  Expression and glycoengineering of functionally active heteromultimeric IgM in plants , 2014, Proceedings of the National Academy of Sciences.

[57]  P. Singh,et al.  Decreased O-Linked GlcNAcylation Protects from Cytotoxicity Mediated by Huntingtin Exon1 Protein Fragment* , 2014, The Journal of Biological Chemistry.

[58]  Jodie L. Abrahams,et al.  Cell surface protein glycosylation in cancer , 2014, Proteomics.

[59]  André M Deelder,et al.  Site-specific N-glycosylation analysis of human immunoglobulin e. , 2014, Journal of proteome research.

[60]  C. Bertozzi,et al.  Glycotherapy: new advances inspire a reemergence of glycans in medicine. , 2014, Chemistry & biology.

[61]  N. Packer,et al.  Comparative N-glycan profiling of colorectal cancer cell lines reveals unique bisecting GlcNAc and α-2,3-linked sialic acid determinants are associated with membrane proteins of the more metastatic/aggressive cell lines. , 2014, Journal of proteome research.

[62]  M. Ratner.  Genentech's glyco-engineered antibody to succeed Rituxan , 2014, Nature Biotechnology.

[63]  T. Spector,et al.  Glycans Are a Novel Biomarker of Chronological and Biological Ages , 2013, The journals of gerontology. Series A, Biological sciences and medical sciences.

[64]  Kai-Ting C. Shade,et al.  Antibody Glycosylation and Inflammation , 2013 .

[65]  H. Lee,et al.  Expression of Lewis X is associated with poor prognosis in triple-negative breast cancer. , 2013, American journal of clinical pathology.

[66]  K. Ohtsubo,et al.  N-Glycosylation modulates the membrane sub-domain distribution and activity of glucose transporter 2 in pancreatic beta cells. , 2013, Biochemical and biophysical research communications.

[67]  L. Dell’Italia,et al.  Cardiac O-GlcNAcylation blunts autophagic signaling in the diabetic heart. , 2013, Life sciences.

[68]  Mark I. McCarthy,et al.  Mutations in HNF1A Result in Marked Alterations of Plasma Glycan Profile , 2013, Diabetes.

[69]  Jianxin Gu,et al.  Clinical and prognostic implications of β1, 6‐N‐acetylglucosaminyltransferase V in patients with gastric cancer , 2013, Cancer science.

[70]  M. Schachner,et al.  Expression of glycogenes in differentiating human NT2N neurons. Downregulation of fucosyltransferase 9 leads to decreased Lewis(x) levels and impaired neurite outgrowth. , 2012, Biochimica et biophysica acta.

[71]  Nicolle H Packer,et al.  Site-specific glycoproteomics confirms that protein structure dictates formation of N-glycan type, core fucosylation and branching. , 2012, Glycobiology.

[72]  Pauline M Rudd,et al.  Glycans as cancer biomarkers. , 2012, Biochimica et biophysica acta.

[73]  R. Schiffmann,et al.  CSF N-Glycan Profiles to Investigate Biomarkers in Brain Developmental Disorders: Application to Leukodystrophies Related to eIF2B Mutations , 2012, PloS one.

[74]  P. Taylor,et al.  Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcγRIIB and dectin-1 , 2012, Nature Medicine.

[75]  J. Ko,et al.  Overexpression and β-1,6-N-Acetylglucosaminylation-initiated Aberrant Glycosylation of TIMP-1 , 2012, The Journal of Biological Chemistry.

[76]  M. Schultz,et al.  Regulation of the metastatic cell phenotype by sialylated glycans , 2012, Cancer and Metastasis Reviews.

[77]  Yasuhiko Kizuka,et al.  Regulated expression and neural functions of human natural killer-1 (HNK-1) carbohydrate , 2012, Cellular and Molecular Life Sciences.

[78]  V. Drory,et al.  Glycans in Sera of Amyotrophic Lateral Sclerosis Patients and Their Role in Killing Neuronal Cells , 2012, PloS one.

[79]  B. G. Davis,et al.  An endoglycosidase with alternative glycan specificity allows broadened glycoprotein remodelling. , 2012, Journal of the American Chemical Society.

[80]  R. Cummings,et al.  The bisecting GlcNAc in cell growth control and tumor progression , 2012, Glycoconjugate Journal.

[81]  H. Matsumoto,et al.  Fucosylation Is a Promising Target for Cancer Diagnosis and Therapy , 2012, Biomolecules.

[82]  Lai-Xi Wang,et al.  Chemoenzymatic synthesis and Fcγ receptor binding of homogeneous glycoforms of antibody Fc domain. Presence of a bisecting sugar moiety enhances the affinity of Fc to FcγIIIa receptor. , 2011, Journal of the American Chemical Society.

[83]  M. Fiala,et al.  Delineating Alzheimer's disease progression with MGAT3, a biomarker for improved prognosis and personalized therapy. , 2011, Biomarkers in medicine.

[84]  J. Marth,et al.  Pathway to diabetes through attenuation of pancreatic beta cell glycosylation and glucose transport , 2011, Nature Medicine.

[85]  Armin Ruf,et al.  Unique carbohydrate–carbohydrate interactions are required for high affinity binding between FcγRIII and antibodies lacking core fucose , 2011, Proceedings of the National Academy of Sciences.

[86]  Chien-Yu Chen,et al.  Sialylation and fucosylation of epidermal growth factor receptor suppress its dimerization and activation in lung cancer cells , 2011, Proceedings of the National Academy of Sciences.

[87]  Pauline M. Rudd,et al.  High Throughput Isolation and Glycosylation Analysis of IgG–Variability and Heritability of the IgG Glycome in Three Isolated Human Populations* , 2011, Molecular & Cellular Proteomics.

[88]  T. Aye,et al.  Proteomics of human cerebrospinal fluid: discovery and verification of biomarker candidates in neurodegenerative diseases using quantitative proteomics. , 2011, Journal of proteomics.

[89]  A. Dell,et al.  Glycosylation Failure Extends to Glycoproteins in Gestational Diabetes Mellitus , 2011, Diabetes.

[90]  Jayne E. Telford,et al.  Discovering new clinical markers in the field of glycomics. , 2011, Biochemical Society transactions.

[91]  J. Houwing-Duistermaat,et al.  Decreased Levels of Bisecting GlcNAc Glycoforms of IgG Are Associated with Human Longevity , 2010, PloS one.

[92]  S. Engelborghs,et al.  Altered serum glycomics in Alzheimer disease: a potential blood biomarker? , 2010, Rejuvenation research.

[93]  M. Reth,et al.  N-linked glycosylation selectively regulates autonomous precursor BCR function , 2010, Nature Immunology.

[94]  E. Miyoshi,et al.  Fucosylation and gastrointestinal cancer. , 2010, World journal of hepatology.

[95]  P. Stanley,et al.  Tumor and Stem Cell Biology Cancer Research The Bisecting GlcNAc on N-Glycans Inhibits Growth Factor Signaling and Retards Mammary Tumor Progression , 2010 .

[96]  T. Sørlie,et al.  Glycan gene expression signatures in normal and malignant breast tissue; possible role in diagnosis and progression , 2010, Molecular oncology.

[97]  Roy Jefferis,et al.  Glycosylation as a strategy to improve antibody-based therapeutics , 2009, Nature Reviews Drug Discovery.

[98]  M. Schachner,et al.  Glycomic analysis of N-linked carbohydrate epitopes from CD24 of mouse brain. , 2009, Journal of proteome research.

[99]  G. Lauc,et al.  Glycosylation of Serum Proteins in Inflammatory Diseases , 2009, Disease markers.

[100]  Ken S Lau,et al.  N-Glycans in cancer progression. , 2008, Glycobiology.

[101]  D. Dinulescu,et al.  Focused glycomic analysis of the N‐linked glycan biosynthetic pathway in ovarian cancer , 2008, Proteomics.

[102]  Naoyuki Taniguchi,et al.  Functional roles of N‐glycans in cell signaling and cell adhesion in cancer , 2008, Cancer science.

[103]  T. Nakagawa,et al.  Biological function of fucosylation in cancer biology. , 2007, Journal of biochemistry.

[104]  M. Nishimura,et al.  Analysis of N-glycan in serum glycoproteins from db/db mice and humans with type 2 diabetes. , 2007, American journal of physiology. Endocrinology and metabolism.

[105]  R. Kannagi.  Carbohydrate antigen sialyl Lewis a--its pathophysiological significance and induction mechanism in cancer progression. , 2007, Chang Gung medical journal.

[106]  J. Marth,et al.  Glycosylation in Cellular Mechanisms of Health and Disease , 2006, Cell.

[107]  J. Marth,et al.  Dietary and Genetic Control of Glucose Transporter 2 Glycosylation Promotes Insulin Secretion in Suppressing Diabetes , 2005, Cell.

[108]  U. Jeschke,et al.  Expression of sialyl lewis X, sialyl Lewis A, E-cadherin and cathepsin-D in human breast cancer: immunohistochemical analysis in mammary carcinoma in situ, invasive carcinomas and their lymph node metastasis. , 2005, Anticancer research.

[109]  C. Rogler,et al.  Reduced hepatocyte proliferation is the basis of retarded liver tumor progression and liver regeneration in mice lacking N-acetylglucosaminyltransferase III. , 2003, Cancer research.

[110]  L. Hornez,et al.  Prognostic value of tumoral sialyltransferase expression and circulating E-selectin concentrations in node-negative breast cancer patients. , 2003, The International journal of biological markers.

[111]  Y. Azuma,et al.  Altered glycosylation of α1-acid glycoprotein in patients with inflammation and diabetes mellitus , 2003 .

[112]  S. Morrison,et al.  The Role of Constant Region Carbohydrate in the Assembly and Secretion of Human IgD and IgA1* , 2002, The Journal of Biological Chemistry.

[113]  T. Nagayasu,et al.  Expression of ABH/Lewis-related antigens as prognostic factors in patients with breast cancer , 2002, Journal of Cancer Research and Clinical Oncology.

[114]  C. Stehouwer,et al.  Increased α3-fucosylation of α1-acid glycoprotein in Type I diabetic patients is related to vascular function , 2001, Glycoconjugate Journal.

[115]  Y. Tagawa,et al.  Expression of Lewis(a), sialyl Lewis(a), Lewis(x) and sialyl Lewis(x) antigens as prognostic factors in patients with colorectal cancer. , 2000, Canadian journal of gastroenterology = Journal canadien de gastroenterologie.

[116]  C. Rogler,et al.  New evidence for an extra-hepatic role of N-acetylglucosaminyltransferase III in the progression of diethylnitrosamine-induced liver tumors in mice. , 2000, Cancer research.

[117]  J. Dennis,et al.  Suppression of tumor growth and metastasis in Mgat5-deficient mice , 2000, Nature Medicine.

[118]  Gerardo Heiss,et al.  Markers of inflammation and prediction of diabetes mellitus in adults (Atherosclerosis Risk in Communities study): a cohort study , 1999, The Lancet.

[119]  M. Lagarde,et al.  In vitro and in vivo alterations of enzymatic glycosylation in diabetes. , 1999, Life sciences.

[120]  L. Hornez,et al.  Multiplex reverse transcription polymerase chain reaction assessment of sialyltransferase expression in human breast cancer. , 1998, Cancer research.

[121]  R. Dwek,et al.  The Glycosylation and Structure of Human Serum IgA1, Fab, and Fc Regions and the Role of N-Glycosylation on Fcα Receptor Interactions* , 1998, The Journal of Biological Chemistry.

[122]  M. Lagarde,et al.  Advanced glycation end products induce specific glycoprotein alterations in retinal microvascular cells. , 1997, Biochemical and biophysical research communications.

[123]  S. Morrison,et al.  Elimination of N-linked glycosylation sites from the human IgA1 constant region: effects on structure and function. , 1997, Journal of immunology.

[124]  T. Hansen,et al.  Mutations in the hepatocyte nuclear factor-1α gene in maturity-onset diabetes of the young (MODY3) , 1996, Nature.

[125]  R. Niemelä,et al.  Expression and function of α2,3‐sialyl‐ and α,3/l,4‐fucosyltransferases in colon adenocarcinoma cell lines: Role in synthesis of E‐selectin counter‐receptors , 1995 .

[126]  M. Nimtz,et al.  Carbohydrate Structures of β‐Trace Protein from Human Cerebrospinal Fluid: Evidence for “Brain‐Type”N‐Glycosylation , 1994, Journal of neurochemistry.

[127]  R. Niemelä,et al.  α2,3‐Sialyl and α1,3‐fucosyltransferase‐dependent synthesis of sialyl Lewis x, an essential oligosaccharide present on L‐selectin counterreceptors, in cultured endothelial cells , 1994 .

[128]  E. E. Max,et al.  Recombinant human IgA expressed in insect cells. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[129]  S. Nagataki,et al.  Early recognition of hepatocellular carcinoma based on altered profiles of alpha-fetoprotein. , 1993, The New England journal of medicine.

[130]  F. Finkelman,et al.  Specificity of the murine IgD receptor on T cells is for N-linked glycans on IgD molecules. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[131]  H. Kobayashi,et al.  Clinical evaluation of circulating serum sialyl Tn antigen levels in patients with epithelial ovarian cancer. , 1991, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[132]  S. Marshall,et al.  Discovery of a metabolic pathway mediating glucose-induced desensitization of the glucose transport system. Role of hexosamine biosynthesis in the induction of insulin resistance. , 1991, The Journal of biological chemistry.

[133]  J. F. Wright,et al.  C1 binding by mouse IgM. The effect of abnormal glycosylation at position 402 resulting from a serine to asparagine exchange at residue 406 of the mu-chain. , 1990, The Journal of biological chemistry.

[134]  M. Shulman,et al.  Structural requirements for IgM assembly and cytolytic activity. Effects of mutations in the oligosaccharide acceptor site at Asn402. , 1989, Journal of immunology.

[135]  Jimmy D Bell,et al.  Assignment of resonances for ‘acute‐phase’ glycoproteins in high resolution proton NMR spectra of human blood plasma , 1987, FEBS letters.

[136]  G. Springer.  T and Tn, general carcinoma autoantigens. , 1984, Science.

[137]  A. Cerami,et al.  Measurement of Glycosylated Amino Acids and Peptides from Urine of Diabetic Patients Using Affinity Chromatography , 1980, Diabetes.

[138]  D. McMillan.  Elevation of Glycoprotein Fucose in Diabetes Mellitus , 1972, Diabetes.

[139]  A. Steck,et al.  Can Biomarkers Help Target Maturity-Onset Diabetes of the Young Genetic Testing in Antibody-Negative Diabetes? , 2018, Diabetes technology & therapeutics.

[140]  E. Pocheć,et al.  On the trail of the glycan codes stored in cancer-related cell adhesion proteins. , 2017, Biochimica et biophysica acta. General subjects.

[141]  Xia Li,et al.  Enhanced expression of polysialic acid correlates with malignant phenotype in breast cancer cell lines and clinical tissue samples. , 2016, International journal of molecular medicine.

[142]  C. Lebrilla,et al.  Glycans and glycoproteins as specific biomarkers for cancer , 2016, Analytical and Bioanalytical Chemistry.

[143]  K. Ohtsubo.  Glyco-Predisposing Factor of Diabetes , 2015 .

[144]  Naoyuki Taniguchi,et al.  Glycans and cancer: role of N-glycans in cancer biomarker, progression and metastasis, and therapeutics. , 2015, Advances in cancer research.

[145]  I. Radziejewska,et al.  Changes of the expression of Lewis blood group antigens in glycoproteins of renal cancer tissues. , 2013, Acta biochimica Polonica.

[146]  Dongxing Zha.  Glycoengineered Pichia-based expression of monoclonal antibodies. , 2013, Methods in molecular biology.

[147]  James Sayre,et al.  MGAT3 mRNA: a biomarker for prognosis and therapy of Alzheimer's disease by vitamin D and curcuminoids. , 2011, Journal of Alzheimer's disease : JAD.

[148]  M. Buse.  Hexosamines, insulin resistance, and the complications of diabetes: current status. , 2006, American journal of physiology. Endocrinology and metabolism.

[149]  Anna Laskowska,et al.  Sialyl Lewis(a): a tumor-associated carbohydrate antigen involved in adhesion and metastatic potential of cancer cells. , 2002, Acta biochimica Polonica.

[150]  N. Taniguchi,et al.  Beta1,6-N-acetylglucosamine-bearing N-glycans in human gliomas: implications for a role in regulating invasivity. , 2000, Cancer research.

[151]  T. Simmen,et al.  IgM polymerization inhibits the Golgi-mediated processing of the mu-chain carboxy-terminal glycans. , 1996, Molecular immunology.

[152]  B. Spiegelman,et al.  Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. , 1993, Science.