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From glycophenotyping by (plant) lectin histochemistry to defining functionality of glycans by pairing with endogenous lectins

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Abstract

About 60 years ago, the efforts to identify blood group-specific haemagglutinins in plant extracts by broad-scale testing were beginning to make a large panel of these proteins available as laboratory tools. Their ability to ‘read’ cell surface signals like antibodies do was the reason for W. C. Boyd to call them lectins, from Latin legere (to read). These proteins turned out to be as widely present in nature as glycans (polysaccharides or carbohydrate chains of cellular glycoconjugates) are. Since carbohydrates have the virtue to facilitate high-density coding in a minimum of space and lectins (initially mostly from plants called phytohaemagglutinins) turned out to be receptors for glycans, their pairing made many applications possible. Most prominently, these proteins were instrumental to map glycome complexity and sites of product generation during glycan assembly in the cell. The detection of mammalian (tissue) lectins and the emerging evidence for intimate molecular recognition between this class of receptors and their (glycoconjugate) counterreceptors substantiate that understanding the rules of the sugar code is presently a major challenge.

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Fig. 1

(from Rüdiger and Gabius 2009, with permission; please see also; Gabius and Roth 2017)

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References

  • Agrawal BBL, Goldstein IJ (1965) Specific binding of concanavalin A to cross-linked dextran gel. Biochem J 96:23c–25c

    Article  Google Scholar 

  • Allen NK, Brilliantine L (1969) A survey of hemagglutinins in various seeds. J Immunol 102:1295–1299

    PubMed  CAS  Google Scholar 

  • Amano M, Eriksson H, Manning JC, Detjen KM, André S, Nishimura S-I, Lehtiö J, Gabius H-J (2012) Tumour suppressor p16INK4a: anoikis-favouring decrease in N/O-glycan/cell surface sialylation by down-regulation of enzymes in sialic acid biosynthesis in tandem in a pancreatic carcinoma model. FEBS J 279:4062–4080

    Article  PubMed  CAS  Google Scholar 

  • André S, Sanchez-Ruderisch H, Nakagawa H, Buchholz M, Kopitz J, Forberich P, Kemmner W, Böck C, Deguchi K, Detjen KM, Wiedenmann B, von Knebel-Döberitz M, Gress TM, Nishimura S-I, Rosewicz S, Gabius H-J (2007) Tumor suppressor p16INK4a: modulator of glycomic profile and galectin-1 expression to increase susceptibility to carbohydrate-dependent induction of anoikis in pancreatic carcinoma cells. FEBS J 274:3233–3256

    Article  PubMed  CAS  Google Scholar 

  • André S, Kozár T, Kojima S, Unverzagt C, Gabius H-J (2009) From structural to functional glycomics: core substitutions as molecular switches for shape and lectin affinity of N-glycans. Biol Chem 390:557–565

    Article  PubMed  CAS  Google Scholar 

  • André S, Singh T, Lacal JC, Smetana K Jr, Gabius H-J (2014) Rho GTPase Rac1: molecular switch within the galectin network and for N-glycan α2,6-sialylation/O-glycan core 1 sialylation in colon cancer in vitro. Folia Biol (Praha) 60:95–107

    Google Scholar 

  • André S, Kaltner H, Kayser K, Murphy PV, Gabius H-J (2016) Merging carbohydrate chemistry with lectin histochemistry to study inhibition of lectin binding by glycoclusters in the natural tissue context. Histochem Cell Biol 145:185–199

    Article  PubMed  CAS  Google Scholar 

  • Angata T, Brinkman-Van der Linden ECM (2002) I-type lectins. Biochim Biophys Acta 1572:294–316

    Article  PubMed  CAS  Google Scholar 

  • Aub JC, Tieslau C, Lankester A (1963) Reactions of normal and tumor cell surfaces to enzymes. I. Wheat-germ lipase and associated mucopolysaccharides. Proc Natl Acad Sci USA 50:613–619

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Avery OT, Göbel WF (1929) Chemo-immunological studies on conjugated carbohydrate–proteins. II. Immunological specificity of synthetic sugar-protein antigens. J Exp Med 50:533–550

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Avery OT, Göbel WF (1931) Chemo-immunological studies on conjugated carbohydrate–proteins. V. The immunological specificity of an antigen prepared by combining the capsular polysaccharide of type III Pneumococcus with foreign protein. J Exp Med 54:437–447

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Avrameas S (1970) Emploi de la concanavaline-A pour l’isolement, la détection et la mesure des glycoprotéines et glucides extra- ou endo-cellulaires. C R Acad Sci (Paris) 18:2205–2208

    CAS  Google Scholar 

  • Barondes SH (1988) Bifunctional properties of lectins: lectins redefined. Trends Biochem Sci 13:480–482

    Article  PubMed  CAS  Google Scholar 

  • Barondes SH (1997) Galectins: a personal review. Trends Glycosci Glycotechnol 9:1–7

    Article  CAS  Google Scholar 

  • Bennett HS (1963) Morphological aspects of extracellular polysaccharides. J Histochem Cytochem 11:14–23

    Article  Google Scholar 

  • Bernhard W, Avrameas S (1971) Ultrastructural visualization of cellular carbohydrate components by means of concanavalin A. Exp Cell Res 64:232–236

    Article  PubMed  CAS  Google Scholar 

  • Bhide GP, Colley KJ (2017) Sialylation of N-glycans: mechanism, cellular compartmentalization and function. Histochem Cell Biol 147:149–174

    Article  PubMed  CAS  Google Scholar 

  • Bittiger H, Schnebli HP (eds) (1976) Concanavalin A as a tool. Wiley, London

    Google Scholar 

  • Borrebaeck CAK, Carlsson R (1989) Lectins as mitogens. Adv Lectin Res 2:10–27

    Article  Google Scholar 

  • Boyd WC (1963) The lectins: their present status. Vox Sang 8:1–32

    Article  PubMed  CAS  Google Scholar 

  • Boyd WC, Reguera RM (1949) Heamagglutinating substances for human cells in various plants. J Immunol 62:333–339

    PubMed  CAS  Google Scholar 

  • Boyd WC, Shapleigh E (1954) Specific precipitating activity of plant agglutinins (lectins). Science 119:419

    Article  PubMed  CAS  Google Scholar 

  • Brockhausen I, Schachter H (1997) Glycosyltransferases involved in N- and O-glycan biosynthesis. In: Gabius H-J, Gabius S (eds) Glycosciences: status and perspectives. Chapman & Hall, London, pp 79–113

    Google Scholar 

  • Bucior I, Burger MM, Fernàndez-Busquets X (2009) Carbohydrate–carbohydrate interactions. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 347–362

    Google Scholar 

  • Buddecke E (2009) Proteoglycans. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 199–216

    Google Scholar 

  • Burger MM, Goldberg AR (1967) Identification of a tumor-specific determinant on neoplastic cell surfaces. Proc Natl Acad Sci USA 57:359–366

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cabrera PV, Amano M, Mitoma J, Chan J, Said J, Fukuda M, Baum LG (2006) Haploinsufficiency of C2GnT-I glycosyltransferase renders T lymphoma cells resistant to cell death. Blood 108:2399–2406

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chambers R (1940) The relation of the extraneous coats to the organization and permeability of cell membranes. Cold Spring Harb Symp Quant Biol 9:144–153

    Article  Google Scholar 

  • Contessa JN, Bhojani MS, Freeze HH, Rehemtulla A, Lawrence TS (2008) Inhibition of N-linked glycosylation disrupts receptor tyrosine kinase signaling in tumor cells. Cancer Res 68:3803–3809

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cooper DNW (2002) Galectinomics: finding themes in complexity. Biochim Biophys Acta 1572:209–231

    Article  PubMed  CAS  Google Scholar 

  • Corfield AP (2015) Mucins: a biologically relevant glycan barrier in mucosal protection. Biochim Biophys Acta 1850:236–252

    Article  PubMed  CAS  Google Scholar 

  • Corfield AP (2017) Eukaryotic protein glycosylation: a primer for histochemists and cell biologists. Histochem Cell Biol 147:119–147

    Article  PubMed  CAS  Google Scholar 

  • Corfield AP, Berry M (2015) Glycan variation and evolution in the eukaryotes. Trends Biochem Sci 40:351–359

    Article  PubMed  CAS  Google Scholar 

  • Creite A (1869) Versuche über die Wirkung des Serumeiweisses nach Injektion in das Blut. Z Ration Med 36:90–108

    Google Scholar 

  • Cummings RD (2009) The repertoire of glycan determinants in the human glycome. Mol BioSyst 5:1087–1104

    Article  PubMed  CAS  Google Scholar 

  • Cummings RD, Pierce JM (2014) The challenge and promise of glycomics. Chem Biol 21:1–15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dahms NM, Hancock MK (2002) P-type lectins. Biochim Biophys Acta 1572:317–340

    Article  PubMed  CAS  Google Scholar 

  • Dawson H, André S, Karamitopoulou E, Zlobec I, Gabius H-J (2013) The growing galectin network in colon cancer and clinical relevance of cytoplasmic galectin-3 reactivity. Anticancer Res 33:3053–3059

    PubMed  CAS  Google Scholar 

  • Delacour D, Gouyer V, Zanetta J-P, Drobecq H, Leteurtre E, Grard G, Moreau-Hannedouche O, Maes E, Pons A, André S, Le Bivic A, Gabius H-J, Manninen A, Simons K, Huet G (2005) Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J Cell Biol 169:491–501

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dettmann W, Grandbois M, André S, Benoit M, Wehle AK, Kaltner H, Gabius H-J, Gaub HE (2000) Differences in zero-force and force-driven kinetics of ligand dissociation from β-galactoside-specific proteins (plant and animal lectins, immunoglobulin G) monitored by plasmon resonance and dynamic single molecule force microscopy. Arch Biochem Biophys 383:157–170

    Article  PubMed  CAS  Google Scholar 

  • Díez-Revuelta N, Higuero AM, Velasco S, Penas-de-la-Iglesia M, Gabius H-J, Abad-Rodríguez J (2017) Neurons define non-myelinated axon segments by the regulation of galectin-4-containing axon membrane domains. Sci Rep 7:12246

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dröscher A (1998) Camillo Golgi and the discovery of the Golgi apparatus. Histochem Cell Biol 109:425–430

    Article  PubMed  Google Scholar 

  • Eichwald E (1865) Beiträge zur Chemie der gewebbildenden Substanzen und ihrer Abkömmlinge. I. Ueber das Mucin, besonders der Weinbergschnecke. Ann Chem Pharm 134:177–211

    Article  Google Scholar 

  • Elfstrand M (1898) Ueber blutkörperchenagglutinierende Eiweisse. In: Kobert R (ed) Görbersdorfer Veröffentlichungen. F. Enke, Stuttgart, pp 1–159

    Google Scholar 

  • Gabius H-J (1987) Endogenous lectins in tumors and the immune system. Cancer Investig 5:39–46

    Article  CAS  Google Scholar 

  • Gabius H-J (1997) Animal lectins. Eur J Biochem 243:543–576

    Article  PubMed  CAS  Google Scholar 

  • Gabius H-J (ed) (2009) The sugar code. Fundamentals of glycosciences. Wiley-VCH, Weinheim

    Google Scholar 

  • Gabius H-J (2015) The magic of the sugar code. Trends Biochem Sci 40:341

    Article  PubMed  CAS  Google Scholar 

  • Gabius H-J (2017) How to crack the sugar code. Folia Biol (Praha) 63:121–131

    Google Scholar 

  • Gabius H-J, Roth J (2017) An introduction to the sugar code. Histochem Cell Biol 147:111–117

    Article  PubMed  CAS  Google Scholar 

  • Gabius H-J, Engelhardt R, Rehm S, Cramer F (1984) Biochemical characterization of endogenous carbohydrate-binding proteins from spontaneous murine rhabdomyosarcoma, mammary adenocarcinoma, and ovarian teratoma. J Natl Cancer Inst 73:1349–1357

    PubMed  CAS  Google Scholar 

  • Gabius H-J, Springer WR, Barondes SH (1985) Receptor for the cell binding site of discoidin I. Cell 42:449–456

    Article  PubMed  CAS  Google Scholar 

  • Gabius H-J, Brehler R, Schauer A, Cramer F (1986) Localization of endogenous lectins in normal human breast, benign breast lesions and mammary carcinomas. Virch Arch (Cell Pathol) 52:107–115

    Article  CAS  Google Scholar 

  • Gabius H-J, Wosgien B, Hendrys M, Bardosi A (1991) Lectin localization in human nerve by biochemically defined lectin-binding glycoproteins, neoglycoprotein and lectin-specific antibody. Histochemistry 95:269–277

    Article  PubMed  CAS  Google Scholar 

  • Gabius H-J, André S, Jiménez-Barbero J, Romero A, Solís D (2011) From lectin structure to functional glycomics: principles of the sugar code. Trends Biochem Sci 36:298–313

    Article  PubMed  CAS  Google Scholar 

  • Gabius H-J, van de Wouwer M, André S, Villalobo A (2012) Down-regulation of the epidermal growth factor receptor by altering N-glycosylation: emerging role of β1,4-galactosyltransferases. Anticancer Res 32:1565–1572

    PubMed  CAS  Google Scholar 

  • Gabius H-J, Kaltner H, Kopitz J, André S (2015) The glycobiology of the CD system: a dictionary for translating marker designations into glycan/lectin structure and function. Trends Biochem Sci 40:360–376

    Article  PubMed  CAS  Google Scholar 

  • Gabius H-J, Manning JC, Kopitz J, André S, Kaltner H (2016) Sweet complementarity: the functional pairing of glycans with lectins. Cell Mol Life Sci 73:1989–2016

    Article  PubMed  CAS  Google Scholar 

  • García Caballero G, Flores-Ibarra A, Michalak M, Khasbiullina N, Bovin NV, André S, Manning JC, Vértesy S, Ruiz FM, Kaltner H, Kopitz J, Romero A, Gabius H-J (2016a) Galectin-related protein: an integral member of the network of chicken galectins. 1. From strong sequence conservation of the gene confined to vertebrates to biochemical characteristics of the chicken protein and its crystal structure. Biochim Biophys Acta 1860:2285–2297

    Article  PubMed  CAS  Google Scholar 

  • García Caballero G, Kaltner H, Michalak M, Shilova N, Yegres M, André S, Ludwig A-K, Manning JC, Schmidt S, Schnölzer M, Bovin NV, Reusch D, Kopitz J, Gabius H-J (2016b) Chicken GRIFIN: a homodimeric member of the galectin network with canonical properties and a unique expression profile. Biochimie 128–129:34–47

    Article  PubMed  CAS  Google Scholar 

  • García Caballero G, Manning JC, Ludwig A-K, Ruiz FM, Romero A, Kaltner H, Gabius H-J (2018) Members of the galectin network with deviations from the canonical sequence signature. 1. Galectin-Related Inter-Fiber Protein (GRIFIN). Trends Glycosci Glycotechnol 30:SE1-SE9

    Article  Google Scholar 

  • Gasic G, Gasic T (1962) Removal and regeneration of the cell coating in tumour cells. Nature 196:170

    Article  PubMed  CAS  Google Scholar 

  • Göbel WF, Avery OT (1929) Chemo-immunological studies on conjugated carbohydrate-proteins. I. The synthesis of p-aminophenyl β-glucoside, p-aminophenyl β-galactoside, and their coupling with serum globulin. J Exp Med 50:521–531

    Article  Google Scholar 

  • Göbel WF, Avery OT, Babers FH (1934) Chemo-immunological studies on conjugated carbohydrate-proteins. IX. The specificity of antigens prepared by combining the p-aminophenol glycosides of disaccharides with protein. J Exp Med 60:599–617

    Article  Google Scholar 

  • Goetz R, Nakada Y, Hu MC, Kurosu H, Wang L, Nakatani T, Shi M, Eliseenkova AV, Razzaque MS, Moe OW, Kuro-o M, Mohammadi M (2010) Isolated C-terminal tail of FGF23 alleviates hypophosphatemia by inhibiting FGF23-FGFR-Klotho complex formation. Proc Natl Acad Sci USA 107:407–412

    Article  PubMed  Google Scholar 

  • Gready JN, Zelensky AN (2009) Routes in lectin evolution: case study on the C-type lectin-like domains. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 329–346

    Google Scholar 

  • Hadaczek P, Wu G, Sharma N, Ciesielska A, Bankiewicz K, Davidow AL, Lu ZH, Forsayeth J, Ledeen RW (2015) GDNF signaling implemented by GM1 ganglioside; failure in Parkinson’s disease and GM1-deficient murine model. Exp Neurol 263:177–189

    Article  PubMed  CAS  Google Scholar 

  • Haworth WN, Lake WHG, Peat S (1939) The configuration of glucosamine (chitosamine). J Chem Soc:271–274

    Google Scholar 

  • Hennet T, Cabalzar J (2015) Congenital disorders of glycosylation: a concise chart of glycocalyx dysfunction. Trends Biochem Sci 40:377–384

    Article  PubMed  CAS  Google Scholar 

  • Higuero AM, Diéz-Revuelta N, Abad-Rodríguez J (2017) The sugar code in neuronal physiology. Histochem Cell Biol 147:257–267

    Article  PubMed  CAS  Google Scholar 

  • Hofmann A (1929) Über den enzymatischen Abbau des Chitins und Chitosans. Dissertationsschrift. Universität Zürich, Zürich, Switzerland

  • Holgersson S, Gustafsson A, Gaunitz S (2009) Bacterial and viral lectins. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 279–300

    Google Scholar 

  • Honke K, Taniguchi N (2009) Animal models to delineate glycan functionality. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 385–401

    Google Scholar 

  • Houzelstein D, Gonçalves IR, Fadden AJ, Sidhu SS, Cooper DNW, Drickamer K, Leffler H, Poirier F (2004) Phylogenetic analysis of the vertebrate galectin family. Mol Biol Evol 21:1177–1187

    Article  PubMed  CAS  Google Scholar 

  • Hu D, Tateno H, Hirabayashi J (2015) Lectin engineering, a molecular evolutionary approach to expanding the lectin utilities. Molecules 20:7637–7656

    Article  PubMed  CAS  Google Scholar 

  • Huang ML, Godula K (2016) Nanoscale materials for probing the biological functions of the glycocalyx. Glycobiology 26:797–803

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hudgin RL, Pricer WEJ, Ashwell G, Stockert RJ, Morell AG (1974) The isolation and properties of a rabbit liver binding protein specific for asialoglycoproteins. J Biol Chem 249:5536–5543

    PubMed  CAS  Google Scholar 

  • Hughes-Jones NC, Gardner B (2002) Red cell agglutination: the first description by Creite (1869) and further observations made by Landois (1875) and Landsteiner (1901). Br J Haematol 119:889–893

    Article  PubMed  CAS  Google Scholar 

  • Ichikawa S, Lyles KW, Econs MJ (2005) A novel GALNT3 mutation in a pseudoautosomal dominant form of tumoral calcinosis: evidence that the disorder is autosomal recessive. J Clin Endocrinol Metab 90:2420–2423

    Article  PubMed  CAS  Google Scholar 

  • Ito S (1969) Structure and function of the glycocalyx. Fed Proc 28:12–25

    PubMed  CAS  Google Scholar 

  • Jentoft N (1990) Why are proteins O-glycosylated? Trends Biochem Sci 15:291–294

    Article  PubMed  CAS  Google Scholar 

  • Kaltner H, Singh T, Manning JC, Raschta A-S, André S, Sinowatz F, Gabius H-J (2015) Network monitoring of adhesion/growth-regulatory galectins: localization of the five canonical chicken proteins in embryonic and maturing bone and cartilage and their introduction as histochemical tools. Anat Rec 298:2051–2070

    Article  CAS  Google Scholar 

  • Kaltner H, García Caballero G, Sinowatz F, Schmidt S, Manning JC, André S, Gabius H-J (2016) Galectin-related protein: an integral member of the network of chicken galectins. 2. From expression profiling to its immunocyto- and histochemical localization and application as tool for ligand detection. Biochim Biophys Acta 1860:2298–2312

    Article  PubMed  CAS  Google Scholar 

  • Kaltner H, Toegel S, García Caballero G, Manning JC, Ledeen RW, Gabius H-J (2017) Galectins: their network and roles in immunity/tumor growth control. Histochem Cell Biol 147:239–256

    Article  PubMed  CAS  Google Scholar 

  • Karsdal MA, Henriksen K, Leeming DJ, Woodworth T, Vassiliadis E, Bay-Jensen AC (2010) Novel combinations of post-translational modification (PTM) neo-epitopes provide tissue-specific biochemical markers: are they the cause or the consequence of the disease? Clin Biochem 43:793–804

    Article  PubMed  CAS  Google Scholar 

  • Kato K, Jeanneau C, Tarp MA, Benet-Pages A, Lorenz-Depiereux B, Bennett EP, Mandel U, Strom TM, Clausen H (2006) Polypeptide GalNAc-transferase T3 and familial tumoral calcinosis. Secretion of fibroblast growth factor 23 requires O-glycosylation. J Biol Chem 281:18370–18377

    Article  PubMed  CAS  Google Scholar 

  • Kawashima H, Sueyoshi S, Li H, Yamamoto K, Osawa T (1990) Carbohydrate binding specificities of several poly-N-acetyllactosamine-binding lectins. Glycoconj J 7:323–334

    Article  PubMed  CAS  Google Scholar 

  • Katzenmaier E-M, André S, Kopitz J, Gabius H-J (2014) Impact of sodium butyrate on the network of adhesion/growth-regulatory galectins in human colon cancer in vitro. Anticancer Res 34:5429–5438

    PubMed  CAS  Google Scholar 

  • Kilpatrick DC, Green C (1992) Lectins as blood typing reagents. Adv Lectin Res 5:51–94

    CAS  Google Scholar 

  • Kingsley DM, Kozarsky KF, Segal M, Krieger M (1986) Three types of low density lipoprotein receptor-deficient mutant have pleiotropic defects in the synthesis of N-linked, O-linked, and lipid-linked carbohydrate chains. J Cell Biol 102:1576–1585

    Article  PubMed  CAS  Google Scholar 

  • Klenk E (1942) Über die Ganglioside, eine neue Gruppe von zuckerhaltigen Gehirnlipoiden. Hoppe-Seyler’s Z Physiol Chem 273:76–86

    Article  CAS  Google Scholar 

  • Klenk E (1970) On the discovery and chemistry of neuraminic acid and gangliosides. Chem Phys Lipids 5:193–197

    Article  PubMed  CAS  Google Scholar 

  • Kocourek J (1986) Historical background. In: Liener IE, Sharon N, Goldstein IJ (eds) The lectins. Properties, functions and applications in biology and medicine. Academic Press, New York, pp 1–32

    Google Scholar 

  • Kopitz J (2009) Glycolipids. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 177–198

    Google Scholar 

  • Kopitz J (2017) Lipid glycosylation: a primer for histochemists and cell biologists. Histochem Cell Biol 147:175–198

    Article  PubMed  CAS  Google Scholar 

  • Kopitz J, von Reitzenstein C, Burchert M, Cantz M, Gabius H-J (1998) Galectin-1 is a major receptor for ganglioside GM1, a product of the growth-controlling activity of a cell surface ganglioside sialidase, on human neuroblastoma cells in culture. J Biol Chem 273:11205–11211

    Article  PubMed  CAS  Google Scholar 

  • Kopitz J, von Reitzenstein C, André S, Kaltner H, Uhl J, Ehemann V, Cantz M, Gabius H-J (2001) Negative regulation of neuroblastoma cell growth by carbohydrate-dependent surface binding of galectin-1 and functional divergence from galectin-3. J Biol Chem 276:35917–35923

    Article  PubMed  CAS  Google Scholar 

  • Kopitz J, Vértesy S, André S, Fiedler S, Schnölzer M, Gabius H-J (2014) Human chimera-type galectin-3: defining the critical tail length for high-affinity glycoprotein/cell surface binding and functional competition with galectin-1 in neuroblastoma cell growth regulation. Biochimie 104:90–99

    Article  PubMed  CAS  Google Scholar 

  • Kopitz J, Xiao Q, Ludwig A-K, Romero A, Michalak M, Sherman SE, Zhou X, Dazen C, Vértesy S, Kaltner H, Klein ML, Gabius H-J, Percec V (2017) Reaction of a programmable glycan presentation of glycodendrimersomes and cells with engineered human lectins to show the sugar functionality of the cell surface. Angew Chem Int Ed 56:14677–14681

    Article  CAS  Google Scholar 

  • Koulumies R (1950) Nature of hemagglutinins in seeds of Cytisus sessilifolius. Ann Med Exp Biol Fenn 28:160–167

    PubMed  CAS  Google Scholar 

  • Krüpe M (1950) Über Anti-0-Hämaggluninine pflanzlicher Herkunft. Z Immunitätsforschg Exp Ther 107:450–464

    Google Scholar 

  • Laine RA (1997) The information-storing potential of the sugar code. In: Gabius H-J, Gabius S (eds) Glycosciences: status and perspectives. Chapman & Hall, London, pp 1–14

    Google Scholar 

  • Landsteiner K (1900) Zur Kenntnis der antifermentativen, lytischen und agglutinierenden Wirkungen des Blutserums in der Lymphe. Zbl Bakteriol Orig 27:357–362

    Google Scholar 

  • Landsteiner K (1901) Ueber Agglutinationserscheinungen normalen menschlichen Blutes. Wien Klin Wochenschr 46:1132–1134

    Google Scholar 

  • Landsteiner K (1945) The specificity of serological reactions. Harvard University Press, Cambridge

    Google Scholar 

  • Landsteiner K, Raubitschek H (1907) Beobachtungen über Hämolyse und Hämagglutination. Zbl Bakt 45:660–667

    Google Scholar 

  • Ledderhose G (1876) Ueber salzsaures Glycosamin. Ber Dt Chem Ges 9:1200–1201

    Article  Google Scholar 

  • Ledderhose G (1879) Ueber Chitin und seine Spaltungsprodukte. Z Physiol Chem 2:213–227

    Google Scholar 

  • Ledderhose G (1880) Ueber Glykosamin. Z Physiol Chem 4:139–159

    Google Scholar 

  • Ledeen RW, Wu G (2015) The multi-tasked life of GM1 ganglioside, a true factotum of nature. Trends Biochem Sci 40:407–418

    Article  PubMed  CAS  Google Scholar 

  • Ledeen RW, Wu G, André S, Bleich D, Huet G, Kaltner H, Kopitz J, Gabius H-J (2012) Beyond glycoproteins as galectin counterreceptors: tumor/effector T cell growth control via ganglioside GM1. Ann NY Acad Sci 1253:206–221

    Article  PubMed  CAS  Google Scholar 

  • Ledeen RW, Kopitz J, Abad-Rodríguez J, Gabius H-J (2018) Glycan chains of gangliosides: functional ligands for tissue lectins (siglecs/galectins). Progr Mol Biol Transl Sci 156:289–324

    Article  Google Scholar 

  • Levene PA (1925) Hexosamines and mucoproteins. Longmans and Green, New York

    Google Scholar 

  • Lothrop AP, Torres MP, Fuchs SM (2013) Deciphering post-translational modification codes. FEBS Lett 587:1247–1257

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ludwig A-K, Vértesy S, Michalak M, Manning JC, André S, Kübler D, Kopitz J, Kaltner H, Gabius H-J (2016) Playing modular puzzle with adhesion/growth-regulatory galectins: design and testing of a hybrid to unravel structure-activity relationships. Protein Pept Lett 23:1003–1012

    Article  PubMed  CAS  Google Scholar 

  • Ludwig A-K, Michalak M, Shilova N, André S, Kaltner H, Bovin NV, Kopitz J, Gabius H-J (2017) Studying the structural significance of galectin design by playing a modular puzzle: homodimer generation from human tandem-repeat-type (heterodimeric) galectin-8 by domain shuffling. Molecules 22:1572

    Article  CAS  Google Scholar 

  • Manning JC, García Caballero G, Knospe C, Kaltner H, Gabius H-J (2017a) Network analysis of adhesion/growth-regulatory galectins and their binding sites in adult chicken retina and choroid. J Anat 231:23–37

    Article  PubMed  CAS  Google Scholar 

  • Manning JC, Romero A, Habermann FA, García Caballero G, Kaltner H, Gabius H-J (2017b) Lectins: a primer for histochemists and cell biologists. Histochem Cell Biol 147:199–222

    Article  PubMed  CAS  Google Scholar 

  • Manning JC, García Caballero G, Knospe C, Kaltner H, Gabius H-J (2018) Three-step monitoring of glycan and galectin profiles in the anterior segment of the adult chicken eye. Ann Anat 217:66–81

    Article  PubMed  Google Scholar 

  • Mayer S, Raulf MK, Lepenies B (2017) C-type lectins: their network and roles in pathogen recognition and immunity. Histochem Cell Biol 147:223–237

    Article  PubMed  CAS  Google Scholar 

  • Merzendorfer H (2009) Chitin: structure, function and metabolism. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 217–229

    Google Scholar 

  • Miller MC, Ludwig A-K, Wichapong K, Kaltner H, Kopitz J, Gabius H-J, Mayo KH (2018) Adhesion/growth-regulatory galectins tested in combination: evidence for formation of hybrids as homodimers. Biochem J 475:1003–1018

    Article  PubMed  CAS  Google Scholar 

  • Mitchell SW (1860) Researches upon the venom of the rattlesnake: with an investigation of the anatomy and physiology of the organs concerned. Smithsonian Contributions to Knowledge, vol 12. The Smithsonian Institution, Washington DC (Article VI)

    Google Scholar 

  • Mitchell SW, Reichert ET (1886) Researches upon the venoms of poisonous serpents. The Smithsonian Institution, Washington DC

    Book  Google Scholar 

  • Moremen KW, Tiemeyer M, Nairn AV (2012) Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol 13:448–462

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morgan WT, Watkins WM (1953) The inhibition of the haemagglutinins in plant seeds by human blood group substances and simple sugars. Br J Exp Pathol 34:94–103

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mutoh T, Tokuda A, Miyadai T, Hamaguchi M, Fujiki N (1995) Ganglioside GM1 binds to the Trk protein and regulates receptor function. Proc Natl Acad Sci USA 92:5087–5091

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nairn AV, York WS, Harris K, Hall EM, Pierce JM, Moremen KW (2008) Regulation of glycan structures in animal tissues: transcript profiling of glycan-related genes. J Biol Chem 283:17298–17313

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Neelamegham S, Mahal LK (2016) Multi-level regulation of cellular glycosylation: from genes to transcript to enzyme to structure. Curr Opin Struct Biol 40:145–152

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nguyen JT, Evans DP, Galvan M, Pace KE, Leitenberg D, Bui TN, Baum LG (2001) CD45 modulates galectin-1-induced T cell death: regulation by expression of core 2 O-glycans. J Immunol 167:5697–5707

    Article  PubMed  CAS  Google Scholar 

  • Nicolson GL (1974) The interactions of lectins with animal cell surfaces. Int Rev Cytol 39:89–190

    Article  PubMed  CAS  Google Scholar 

  • Nowell PC (1960) Phytohemagglutinin: an inhibitor of mitosis in cultures of normal human leukocytes. Cancer Res 20:462–466

    PubMed  CAS  Google Scholar 

  • Nussinov R, Tsai CJ, Xin F, Radivojac P (2012) Allosteric post-translational modification codes. Trends Biochem Sci 37:447–455

    Article  PubMed  CAS  Google Scholar 

  • Odier A (1829) Mémoire sur la composition chimique des parties cornées des insectes. Mémoires de la Société d’Histoire Naturelle de Paris 1:29–42

    Google Scholar 

  • Oguri S (2005) Analysis of sugar chain-binding specificity of tomato lectin using lectin blot: recognition of high-mannose-type N-glycans produced by plants and yeast. Glycoconj J 22:453–461

    Article  PubMed  CAS  Google Scholar 

  • Oscarson S (2009) The chemist’s way to synthesize glycosides. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 31–51

    Google Scholar 

  • Patnaik SK, Stanley P (2006) Lectin-resistant CHO glycosylation mutants. Methods Enzymol 416:159–182

    Article  PubMed  CAS  Google Scholar 

  • Patsos G, Corfield A (2009) O-Glycosylation: structural diversity and function. In: Gabius H-J (ed) The sugar code fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 111–137

    Google Scholar 

  • Patsos G, André S, Roeckel N, Gromes R, Gebert J, Kopitz J, Gabius H-J (2009) Compensation of loss of protein function in microsatellite-unstable colon cancer cells (HCT116): a gene-dependent effect on the cell surface glycan profile. Glycobiology 19:726–734

    Article  PubMed  CAS  Google Scholar 

  • Pavelka M (1997) Topology of glycosylation—a histochemist’s view. In: Gabius H-J, Gabius S (eds) Glycosciences: status and perspectives. Chapman & Hall, London, pp 115–120

    Google Scholar 

  • Peltier P, Euzen R, Daniellou R, Nugier-Chauvin C, Ferrieres V (2008) Recent knowledge and innovations related to hexofuranosides: structure, synthesis and applications. Carbohydr Res 343:1897–1923

    Article  PubMed  CAS  Google Scholar 

  • Percec V, Leowanawat P, Sun HJ, Kulikov O, Nusbaum CD, Tran TM, Bertin A, Wilson DA, Peterca M, Zhang S, Kamat NP, Vargo K, Moock D, Johnston ED, Hammer DA, Pochan DJ, Chen Y, Chabre YM, Shiao TC, Bergeron-Brlek M, André S, Roy R, Gabius H-J, Heiney PA (2013) Modular synthesis of amphiphilic Janus glycodendrimers and their self-assembly into glycodendrimersomes and other complex architectures with bioactivity to biomedically relevant lectins. J Am Chem Soc 135:9055–9077

    Article  PubMed  CAS  Google Scholar 

  • Petrosyan A, Holzapfel MS, Muirhead DE, Cheng PW (2014) Restoration of compact Golgi morphology in advanced prostate cancer enhances susceptibility to galectin-1-induced apoptosis by modifying mucin O-glycan synthesis. Mol Cancer Res 12:1704–1716

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pierce M, Arango J (1986) Rous sarcoma virus-transformed baby hamster kidney cells express higher levels of asparagine-linked tri- and tetraantennary glycopeptides containing [GlcNAcβ(1,6)Manα(1,6)Man] and poly-N-acetyllactosamine sequences than baby hamster kidney cells. J Biol Chem 261:10772–10777

    PubMed  CAS  Google Scholar 

  • Rambourg A, Neutra M, Leblond CP (1966) Presence of a “cell coat” rich in carbohydrate at the surface of cells in the rat. Anat Rec 154:41–71

    Article  PubMed  CAS  Google Scholar 

  • Renkonen KO (1948) Studies on the nature of hemagglutinins present in seeds of some representatives of the family of leguminosae. Ann Med Exp Biol Fenn 26:66–72

    Google Scholar 

  • Reuter G, Gabius H-J (1999) Eukaryotic glycosylation: whim of nature or multipurpose tool? Cell Mol Life Sci 55:368–422

    Article  PubMed  CAS  Google Scholar 

  • Richards MR, Lowary TL (2009) Chemistry and biology of galactofuranose-containing polysaccharides. ChemBioChem 10:1920–1938

    Article  PubMed  CAS  Google Scholar 

  • Roth J (1984) Cytochemical localization of terminal N-acetyl-D-galactosamine residues in cellular compartments of intestinal goblet cells: implications for the topology of O-glycosylation. J Cell Biol 98:399–406

    Article  PubMed  CAS  Google Scholar 

  • Roth J (1987) Subcellular organization of glycosylation in mammalian cells. Biochim Biophys Acta 906:405–436

    Article  PubMed  CAS  Google Scholar 

  • Roth J (1993) Cellular sialoglycoconjugates: a histochemical perspective. Histochem J 25:687–710

    PubMed  CAS  Google Scholar 

  • Roth J (1996) Protein glycosylation in the endoplasmic reticulum and the Golgi apparatus and cell-type specificity of cell surface glycoconjugate expression: analysis by protein A-gold and lectin-gold techniques. Histochem Cell Biol 106:79–92

    Article  PubMed  CAS  Google Scholar 

  • Roth J (2002) Protein N-glycosylation along the secretory pathway: relationship to organelle topography and function, protein quality control, and cell interactions. Chem Rev 102:285–303

    Article  PubMed  CAS  Google Scholar 

  • Roth J (2011) Lectins for histochemical demonstration of glycans. Histochem Cell Biol 136:117–130

    Article  PubMed  CAS  Google Scholar 

  • Roth J, Thoss K (1974) Light and electron microscopic demonstration of d-mannose and d-glucose like sites at the cell surface by means of the lectin from the Lens culinaris. Experientia 30:414

    Article  PubMed  CAS  Google Scholar 

  • Roth J, Franz H (1975) Ultrastructural detection of lectin receptors by cytochemical affinity reaction using mannan-iron complex. Histochemistry 41:365–368

    Article  PubMed  CAS  Google Scholar 

  • Roth J, Zuber C (2017) Quality control of glycoprotein folding and ERAD: the role of N-glycan handling, EDEM1 and OS-9. Histochem Cell Biol 147:269–284

    Article  PubMed  CAS  Google Scholar 

  • Roth J, Meyer HW, Bolck F, Stiller D (1972) Electron microscopic visualization of carbohydrate components in the glycocalyx of tumor cells using Concanavalin A. Exp Pathol (Jena) 6:189–192

    CAS  Google Scholar 

  • Roth J, Taatjes DJ, Lucocq JM, Weinstein J, Paulson JC (1985) Demonstration of an extensive trans-tubular network continuous with the Golgi apparatus stack that may function in glycosylation. Cell 43:287–295

    Article  PubMed  CAS  Google Scholar 

  • Roth J, Taatjes DJ, Lucocq JM, Charest PM (1988) Light and electron microscopical detection of sugar residues in tissue sections by gold labeled lectins and glycoproteins. II. Applications in the study of the topology of Golgi apparatus glycosylation steps and the regional distribution of lectin binding sites in the plasma membrane. Acta Histochem Suppl 36:125–140

    PubMed  CAS  Google Scholar 

  • Roy R, Murphy PV, Gabius H-J (2016) Multivalent carbohydrate–lectin interactions: how synthetic chemistry enables insights into nanometric recognition. Molecules 21:629

    Article  CAS  Google Scholar 

  • Roy R, Cao Y, Kaltner H, Kottari N, Shiao TC, Belkhadem K, André S, Manning JC, Murphy PV, Gabius H-J (2017) Teaming up synthetic chemistry and histochemistry for activity screening in galectin-directed inhibitor design. Histochem Cell Biol 147:285–301

    Article  PubMed  CAS  Google Scholar 

  • Rüdiger H, Gabius H-J (2009) The biochemical basis and coding capacity of the sugar code. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 3–13

    Google Scholar 

  • Sanchez-Ruderisch H, Fischer C, Detjen KM, Welzel M, Wimmel A, Manning JC, André S, Gabius H-J (2010) Tumor suppressor p16INK4a: downregulation of galectin-3, an endogenous competitor of the pro-anoikis effector galectin-1, in a pancreatic carcinoma model. FEBS J 277:3552–3563

    Article  PubMed  CAS  Google Scholar 

  • Schachter H (2005) The search for glycan function: fucosylation of the TGF-β1 receptor is required for receptor activation. Proc Natl Acad Sci USA 102:15721–15722

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schengrund C-L (2015) Gangliosides: glycosphingolipids essential for normal neural development and function. Trends Biochem Sci 40:397–406

    Article  PubMed  CAS  Google Scholar 

  • Schrével J, Gros D, Monsigny M (1981) Cytochemistry of cell glycoconjugates. Progr Histochem Cytochem 14(2):1–269

    Article  Google Scholar 

  • Schwarz HP, Dorner F (2003) Karl Landsteiner and his major contributions to haematology. Br J Haematol 121:556–565

    Article  PubMed  Google Scholar 

  • Semel AC, Seales EC, Singhal A, Eklund EA, Colley KJ, Bellis SL (2002) Hyposialylation of integrins stimulates the activity of myeloid fibronectin receptors. J Biol Chem 277:32830–32836

    Article  PubMed  CAS  Google Scholar 

  • Sharon N (1975) Complex carbohydrates. Their chemistry, biosynthesis, and functions. Addison-Wesley Publ. Co., Reading

    Google Scholar 

  • Sharon N, Lis H (1997) Glycoproteins: structure and function. In: Gabius H-J, Gabius S (eds) Glycosciences: status and perspectives. Chapman & Hall, London, pp 133–162

    Google Scholar 

  • Siebert H-C, André S, Lu S-Y, Frank M, Kaltner H, van Kuik JA, Korchagina EY, Bovin NV, Tajkhorshid E, Kaptein R, Vliegenthart JFG, von der Lieth C-W, Jiménez-Barbero J, Kopitz J, Gabius H-J (2003) Unique conformer selection of human growth-regulatory lectin galectin-1 for ganglioside GM1 versus bacterial toxins. Biochemistry 42:14762–14773

    Article  PubMed  CAS  Google Scholar 

  • Solís D, Bovin NV, Davis AP, Jiménez-Barbero J, Romero A, Roy R, Smetana K Jr, Gabius H-J (2015) A guide into glycosciences: how chemistry, biochemistry and biology cooperate to crack the sugar code. Biochim Biophys Acta 1850:186–235

    Article  PubMed  CAS  Google Scholar 

  • Spiro RG (2002) Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12:43R–56R

    Article  PubMed  CAS  Google Scholar 

  • Stillmark H (1888) Ueber Ricin, ein giftiges Ferment aus den Samen von Ricinus comm. L. und einigen anderen Euphorbiaceen. Schnakenburg’s Buchdruckerei, Dorpat

    Google Scholar 

  • Sumner JB, Howell SF (1935) The non-identity of jack bean agglutinin with crystalline urease. J Immunol 29:133–134

    CAS  Google Scholar 

  • Sumner JB, Howell SF (1936) The identification of a hemagglutinin of the jack bean with concanavalin A. J Bacteriol 32:227–237

    PubMed  PubMed Central  CAS  Google Scholar 

  • Swanson MD, Boudreaux DM, Salmon L, Chugh J, Winter HC, Meagher JL, André S, Murphy PV, Oscarson S, Roy R, King S, Kaplan MH, Goldstein IJ, Tarbet EB, Hurst BL, Smee DF, de la Fuente C, Hoffmann HH, Xue Y, Rice CM, Schols D, García JV, Stuckey JA, Gabius H-J, Al-Hashimi HM, Markovitz DM (2015) Engineering a therapeutic lectin by uncoupling mitogenicity from antiviral activity. Cell 163:746–758

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Taatjes DJ, Roth J (1991) Glycosylation in intestinal epithelium. Int Rev Cytol 126:135–193

    Article  PubMed  CAS  Google Scholar 

  • Tefsen B, Ram AF, van Die I, Routier FH (2012) Galactofuranose in eukaryotes: aspects of biosynthesis and functional impact. Glycobiology 22:456–469

    Article  PubMed  CAS  Google Scholar 

  • Teichberg VI, Silman I, Beitsch DD, Resheff G (1975) A β-d-galactoside binding protein from electric organ tissue of Electrophorus electricus. Proc Natl Acad Sci USA 72:1383–1387

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thudichum JLW (1874) Researches on the chemical constitution of the brain. Report of the Medical Offices of the Privy Councel and Local Government Board, London

  • Toegel S, Bieder D, André S, Kayser K, Walzer SM, Hobusch G, Windhager R, Gabius H-J (2014) Human osteoarthritic knee cartilage: fingerprinting of adhesion/growth-regulatory galectins in vitro and in situ indicates differential upregulation in severe degeneration. Histochem Cell Biol 142:373–388

    Article  PubMed  CAS  Google Scholar 

  • Topaz O, Shurman DL, Bergman R, Indelman M, Ratajczak P, Mizrachi M, Khamaysi Z, Behar D, Petronius D, Friedman V, Zelikovic I, Raimer S, Metzker A, Richard G, Sprecher E (2004) Mutations in GALNT3, encoding a protein involved in O-linked glycosylation, cause familial tumoral calcinosis. Nat Genet 36:579–581

    Article  PubMed  CAS  Google Scholar 

  • Unverzagt C, André S, Seifert J, Kojima S, Fink C, Srikrishna G, Freeze H, Kayser K, Gabius H-J (2002) Structure-activity profiles of complex biantennary glycans with core fucosylation and with/without additional α2,3/α2,6-sialylation: synthesis of neoglycoproteins and their properties in lectin assays, cell binding, and organ uptake. J Med Chem 45:478–491

    Article  PubMed  CAS  Google Scholar 

  • Valenzuela HF, Pace KE, Cabrera PV, White R, Porvari K, Kaija H, Vihko P, Baum LG (2007) O-Glycosylation regulates LNCaP prostate cancer cell susceptibility to apoptosis induced by galectin-1. Cancer Res 67:6155–6162

    Article  PubMed  CAS  Google Scholar 

  • van den Berg TK, Honing H, Franke N, van Remoortere A, Schiphorst WECM., Liu F-T, Deelder AM, Cummings RD, Hokke CH, van Die I (2004) LacdiNAc-glycans constitute a parasite pattern for galectin-3-mediated immune recognition. J Immunol 173:1902–1907

    Article  PubMed  Google Scholar 

  • Vasta GR, Amzel LM, Bianchet MA, Cammarata M, Feng C, Saito K (2017) F-type lectins: a highly diversified family of fucose-binding proteins with a unique sequence motif and structural fold, involved in self/non-self recognition. Front Immunol 8:1648

    Article  PubMed  PubMed Central  Google Scholar 

  • Vértesy S, Michalak M, Miller MC, Schnölzer M, André S, Kopitz J, Mayo KH, Gabius H-J (2015) Structural significance of galectin design: impairment of homodimer stability by linker insertion and partial reversion by ligand presence. Protein Eng Des Sel 28:199–210

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Inoue S, Gu J, Miyoshi E, Noda K, Li W, Mizuno-Horikawa Y, Nakano M, Asahi M, Takahashi M, Uozumi N, Ihara S, Lee SH, Ikeda Y, Yamaguchi Y, Aze Y, Tomiyama Y, Fujii J, Suzuki K, Kondo A, Shapiro SD, Lopez-Otin C, Kuwaki T, Okabe M, Honke K, Taniguchi N (2005) Dysregulation of TGF-β1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice. Proc Natl Acad Sci USA 102:15791–15796

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang J, Lu ZH, Gabius H-J, Rohowsky-Kochan C, Ledeen RW, Wu G (2009) Cross-linking of GM1 ganglioside by galectin-1 mediates regulatory T cell activity involving TRPC5 channel activation: possible role in suppressing experimental autoimmune encephalomyelitis. J Immunol 182:4036–4045

    Article  PubMed  CAS  Google Scholar 

  • Watkins WM (1966) Blood-group substances. Science 152:172–181

    Article  PubMed  CAS  Google Scholar 

  • Watkins WM (1999) A half century of blood-group antigen research: some personal recollections. Trends Glycosci Glycotechnol 11:391–411

    Article  CAS  Google Scholar 

  • Watkins WM, Morgan WTJ (1952) Neutralisation of the anti-H agglutinin in eel serum by simple sugars. Nature 169:825–826

    Article  PubMed  CAS  Google Scholar 

  • Weinmann D, Schlangen K, André S, Schmidt S, Walzer SM, Kubista B, Windhager R, Toegel S, Gabius H-J (2016) Galectin-3 induces a pro-degradative/inflammatory gene signature in human chondrocytes, teaming up with galectin-1 in osteoarthritis pathogenesis. Sci Rep 6:39112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wesener DA, Wangkanont K, McBride R, Song X, Kraft MB, Hodges HL, Zarling LC, Splain RA, Smith DF, Cummings RD, Paulson JC, Forest KT, Kiessling LL (2015) Recognition of microbial glycans by human intelectin-1. Nat Struct Mol Biol 22:603–610

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Winterburn PJ, Phelps CF (1972) The significance of glycosylated proteins. Nature 236:147–151

    Article  PubMed  CAS  Google Scholar 

  • Xiao Q, Wang Z, Williams D, Leowanawat P, Peterca M, Sherman SE, Zhang S, Hammer DA, Heiney PA, King SR, Markovitz DM, André S, Gabius H-J, Klein ML, Percec V (2016) Why do membranes of some unhealthy cells adopt a cubic architecture? ACS Cent Sci 2:943–953

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xiao Q, Ludwig A-K, Romano C, Buzzacchera I, Sherman SE, Vetro M, Vértesy S, Kaltner H, Reed EH, Moller M, Wilson CJ, Hammer DA, Oscarson S, Klein ML, Gabius H-J, Percec V (2018) Exploring functional pairing between surface glycoconjugates and human galectins using programmable glycodendrimersomes. Proc Natl Acad Sci USA 115:E2509–E2518

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamashita K, Ohkura T, Tachibana Y, Takasaki S, Kobata A (1984) Comparative study of the oligosaccharides released from baby hamster kidney cells and their polyoma transformant by hydrazinolysis. J Biol Chem 259:10834–10840

    PubMed  CAS  Google Scholar 

  • Zhang S, Moussodia R-O, Murzeau C, Sun HJ, Klein ML, Vértesy S, André S, Roy R, Gabius H-J, Percec V (2015) Dissecting molecular aspects of cell interactions using glycodendrimersomes with programmable glycan presentation and engineered human lectins. Angew Chem Int Ed 54:4036–4040

    Article  CAS  Google Scholar 

  • Zivicová V, Broz P, Fík Z, Mifková A, Plzák J, Cada Z, Kaltner H, Kucerová JF, Gabius H-J, Smetana K Jr (2017) Genome-wide expression profiling (with focus on the galectin network) in tumor, transition zone and normal tissue of head and neck cancer: marked differences between individual patients and the site of specimen origin. Anticancer Res 37:2275–2288

    Article  PubMed  Google Scholar 

  • Zivicová V, Gal P, Mifková A, Novak S, Kaltner H, Kolár M, Strnad H, Sachová J, Hradilová M, Chovanec M, Gabius H-J, Smetana K Jr, Fík Z (2018) Detection of distinct changes in gene-expression profiles in specimens of tumors and transition zones of tenascin-positive/-negative head and neck squamous cell carcinima. Anticancer Res 38:1279–1290

    PubMed  Google Scholar 

  • Zuber C, Roth J (2009) N-Glycosylation. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 87–110

    Google Scholar 

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We gratefully acknowledge inspiring discussion with Drs. B. Friday and A. Leddoz.

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Kaltner, H., García Caballero, G., Ludwig, AK. et al. From glycophenotyping by (plant) lectin histochemistry to defining functionality of glycans by pairing with endogenous lectins. Histochem Cell Biol 149, 547–568 (2018). https://doi.org/10.1007/s00418-018-1676-7

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