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Thromb Haemost 2019; 119(04): 517-533
DOI: 10.1055/s-0038-1676968
Theme Issue Article
Georg Thieme Verlag KG Stuttgart · New York

Sensing Glycans as Biochemical Messages by Tissue Lectins: The Sugar Code at Work in Vascular Biology

Herbert Kaltner
1   Institut für Physiologische Chemie, Tierärztliche Fakultät, Ludwig-Maximilians-Universität München, München, Germany
,
Hans-Joachim Gabius
1   Institut für Physiologische Chemie, Tierärztliche Fakultät, Ludwig-Maximilians-Universität München, München, Germany
› Author Affiliations
Further Information

Publication History

01 October 2018

15 November 2018

Publication Date:
08 January 2019 (online)

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Abstract

Although a plethora of players has already been revealed to be engaged in the haemostatic system, a fundamental consideration of the molecular nature of information coding can give further explorations of the mechanisms of blood clotting, platelet functionality and vascular trafficking direction. By any measures, looking at ranges of occurrence and of potential for structural versatility, at strategic positioning to influence protein and cell sociology as well as at dynamics of processing and restructuring for phenotypic variability, using sugars as an alphabet of life for generating the glycan part of glycoconjugates is a success story. The handiwork by the complex system for glycan biosynthesis renders biochemical messages of exceptionally high coding capacity available. They are read and translated into cellular effects by receptors termed lectins. The different levels of regulation on both sides, that is, glycan and lectin, establish an intriguingly fine-tuned capacity for functional pairing. The emerging insights into the highly branched routes of glycosylation, into lectin structures up to complete characterization in solution and the shape of lectin networks, first obtained for the three selectins, now extended to considering many other C-type lectins, galectins and siglecs, as well as into intra- and inter-family cross-talk and cooperations are sure to push boundaries in our understanding of the molecular basis of haemostasis.

Keywords

C-type lectin - galectin - mucin - selectin - siglec - von Willebrand factor
 

  • References

  • 1 Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009
    Google Scholar
  • 2 Bennett HS. Morphological aspects of extracellular polysaccha-rides. J Histochem Cytochem 1963; 11: 14-23
    CrossrefPubMedGoogle Scholar
  • 3 Bettelheim-Jevons FR. Protein-carbohydrate complexes. Adv Protein Chem 1958; 13: 35-105
    PubMedGoogle Scholar
  • 4 Klenk E. On the discovery and chemistry of neuraminic acid and gangliosides. Chem Phys Lipids 1970; 5 (01) 193-197
    CrossrefPubMedGoogle Scholar
  • 5 Sharon N. Complex Carbohydrates. Their Chemistry, Biosynthesis, and Functions. Reading, MA: Addison-Wesley Publ. Co.; 1975
    Google Scholar
  • 6 Montreuil J. The history of glycoprotein research, a personal view. In: Montreuil J, Vliegenthart JFG, Schachter H. , eds. Glycoproteins. Amsterdam, The Netherlands: Elsevier; 1995: 1-12
    Google Scholar
  • 7 Reuter G, Gabius H-J. Eukaryotic glycosylation: whim of nature or multipurpose tool?. Cell Mol Life Sci 1999; 55 (03) 368-422
    CrossrefPubMedGoogle Scholar
  • 8 Buddecke E. Proteoglycans. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 199-216
    Google Scholar
  • 9 Merzendorfer H. Chitin: structure, function and metabolism. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 217-229
    Google Scholar
  • 10 Corfield AP, Berry M. Glycan variation and evolution in the eukaryotes. Trends Biochem Sci 2015; 40 (07) 351-359
    CrossrefPubMedGoogle Scholar
  • 11 Tan FY, Tang CM, Exley RM. Sugar coating: bacterial protein glycosylation and host-microbe interactions. Trends Biochem Sci 2015; 40 (07) 342-350
    CrossrefPubMedGoogle Scholar
  • 12 Corfield A. Eukaryotic protein glycosylation: a primer for histochemists and cell biologists. Histochem Cell Biol 2017; 147 (02) 119-147
    CrossrefPubMedGoogle Scholar
  • 13 Kopitz J. Lipid glycosylation: a primer for histochemists and cell biologists. Histochem Cell Biol 2017; 147 (02) 175-198
    CrossrefPubMedGoogle Scholar
  • 14 Schnaar RL, Lopez PHH. Preface and ganglioside nomenclature. Prog Mol Biol Transl Sci 2018; 156: xvii-xxi
    PubMedGoogle Scholar
  • 15 Laine RA. The information-storing potential of the sugar code. In: Gabius H-J, Gabius S. , eds. Glycosciences: Status and Perspectives. London, UK and Weinheim, Germany: Chapman & Hall; 1997: 1-14
    Google Scholar
  • 16 Roseman S. Reflections on glycobiology. J Biol Chem 2001; 276 (45) 41527-41542
    CrossrefPubMedGoogle Scholar
  • 17 Kornfeld S. A lifetime of adventures in glycobiology. Annu Rev Biochem 2018; 87: 1-21
    CrossrefPubMedGoogle Scholar
  • 18 Gesner BM, Ginsburg V. Effect of glycosidases on the fate of transfused lymphocytes. Proc Natl Acad Sci U S A 1964; 52: 750-755
    CrossrefPubMedGoogle Scholar
  • 19 Morell AG, Irvine RA, Sternlieb I, Scheinberg IH, Ashwell G. Physical and chemical studies on ceruloplasmin. V. Metabolic studies on sialic acid-free ceruloplasmin in vivo. J Biol Chem 1968; 243 (01) 155-159
    CrossrefPubMedGoogle Scholar
  • 20 Roseman S. The synthesis of complex carbohydrates by multiglycosyltransferase systems and their potential function in intercellular adhesion. Chem Phys Lipids 1970; 5 (01) 270-297
    CrossrefPubMedGoogle Scholar
  • 21 Winterburn PJ, Phelps CF. The significance of glycosylated proteins. Nature 1972; 236 (5343): 147-151
    CrossrefPubMedGoogle Scholar
  • 22 Brockhausen I, Schachter H. Glycosyltransferases involved in N- and O-glycan biosynthesis. In: Gabius H-J, Gabius S. , eds. Glycosciences: Status and Perspectives. London, UK and Weinheim, Germany: Chapman & Hall; 1997: 79-113
    Google Scholar
  • 23 Sears P, Wong C-H. Enzyme action in glycoprotein synthesis. Cell Mol Life Sci 1998; 54 (03) 223-252
    CrossrefPubMedGoogle Scholar
  • 24 Endo T. O-mannosyl glycans in mammals. Biochim Biophys Acta 1999; 1473 (01) 237-246
    CrossrefPubMedGoogle Scholar
  • 25 Dall'Olio F, Chiricolo M. Sialyltransferases in cancer. Glycoconj J 2001; 18 (11-12): 841-850
    CrossrefPubMedGoogle Scholar
  • 26 Harduin-Lepers A, Mollicone R, Delannoy P, Oriol R. The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach. Glycobiology 2005; 15 (08) 805-817
    CrossrefPubMedGoogle Scholar
  • 27 Patsos G, Corfield A. O-Glycosylation: structural diversity and function. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 111-137
    Google Scholar
  • 28 Wilson IBH, Paschinger H, Rendic D. Glycosylation of model and ‘lower’ organisms. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 139-154
    Google Scholar
  • 29 Zuber C, Roth J. N-Glycosylation. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 87-110
    Google Scholar
  • 30 Takashima S, Tsuji S. Functional diversity of mammalian sialyltransferases. Trends Glycosci Glycotechnol 2011; 23 (132) 178-193
    CrossrefPubMedGoogle Scholar
  • 31 Aplin JD, Jones CJ. Fucose, placental evolution and the glycocode. Glycobiology 2012; 22 (04) 470-478
    CrossrefPubMedGoogle Scholar
  • 32 Bennett EP, Mandel U, Clausen H, Gerken TA, Fritz TA, Tabak LA. Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 2012; 22 (06) 736-756
    CrossrefPubMedGoogle Scholar
  • 33 Raman J, Guan Y, Perrine CL, Gerken TA, Tabak LA. UDP-N-acetyl-α-D-galactosamine:polypeptide N-acetylgalactosaminyltransferases: completion of the family tree. Glycobiology 2012; 22 (06) 768-777
    CrossrefPubMedGoogle Scholar
  • 34 Togayachi A, Narimatsu H. Functional analysis of β1,3-N-acetylglucosaminyltransferases and regulation of immunological function by polylactosamine. Trends Glycosci Glycotechnol 2012; 24 (137) 95-111
    CrossrefPubMedGoogle Scholar
  • 35 Hennet T, Cabalzar J. Congenital disorders of glycosylation: a concise chart of glycocalyx dysfunction. Trends Biochem Sci 2015; 40 (07) 377-384
    CrossrefPubMedGoogle Scholar
  • 36 Schengrund C-L. Gangliosides: glycosphingolipids essential for normal neural development and function. Trends Biochem Sci 2015; 40 (07) 397-406
    CrossrefPubMedGoogle Scholar
  • 37 Bhide GP, Colley KJ. Sialylation of N-glycans: mechanism, cellular compartmentalization and function. Histochem Cell Biol 2017; 147 (02) 149-174
    CrossrefPubMedGoogle Scholar
  • 38 Honke K, Taniguchi N. Animal models to delineate glycan functionality. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 385-401
    Google Scholar
  • 39 Takamatsu S, Antonopoulos A, Ohtsubo K. , et al. Physiological and glycomic characterization of N-acetylglucosaminyltransferase-IVa and -IVb double deficient mice. Glycobiology 2010; 20 (04) 485-497
    CrossrefPubMedGoogle Scholar
  • 40 Ohtsubo K. Biological significance of N-acetylglucosaminyltransferase-IV-mediated protein glycosylation on the homeostasis of cellular physiological functions. Trends Glycosci Glycotechnol 2011; 23 (130) 103-105
    CrossrefPubMedGoogle Scholar
  • 41 Roth J. Subcellular organization of glycosylation in mammalian cells. Biochim Biophys Acta 1987; 906 (03) 405-436
    CrossrefPubMedGoogle Scholar
  • 42 Varki A. Factors controlling the glycosylation potential of the Golgi apparatus. Trends Cell Biol 1998; 8 (01) 34-40
    CrossrefPubMedGoogle Scholar
  • 43 Gabius H-J, André S, Kaltner H, Siebert HC. The sugar code: functional lectinomics. Biochim Biophys Acta 2002; 1572 (2-3): 165-177
    CrossrefPubMedGoogle Scholar
  • 44 Cummings RD. The repertoire of glycan determinants in the human glycome. Mol Biosyst 2009; 5 (10) 1087-1104
    CrossrefPubMedGoogle Scholar
  • 45 Moremen KW, Tiemeyer M, Nairn AV. Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol 2012; 13 (07) 448-462
    PubMedGoogle Scholar
  • 46 Manning JC, Romero A, Habermann FA, García Caballero G, Kaltner H, Gabius HJ. Lectins: a primer for histochemists and cell biologists. Histochem Cell Biol 2017; 147 (02) 199-222
    CrossrefPubMedGoogle Scholar
  • 47 Kaltner H, García Caballero G, Ludwig A-K, Manning JC, Gabius HJ. From glycophenotyping by (plant) lectin histochemistry to defining functionality of glycans by pairing with endogenous lectins. Histochem Cell Biol 2018; 149 (06) 547-568
    CrossrefPubMedGoogle Scholar
  • 48 Nakagawa H. Analytical aspects: analysis of protein-bound glycans. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 71-83
    Google Scholar
  • 49 Novotny MV, Alley Jr WR, Mann BF. Analytical glycobiology at high sensitivity: current approaches and directions. Glycoconj J 2013; 30 (02) 89-117
    CrossrefPubMedGoogle Scholar
  • 50 Gabius H-J. How to crack the sugar code. Folia Biol (Praha) 2017; 63 (04) 121-131
    PubMedGoogle Scholar
  • 51 Oscarson S. The chemist's way to synthesize glycosides. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 31-51
    Google Scholar
  • 52 von der Lieth CW, Siebert HC, Kožár T. , et al. Lectin ligands: new insights into their conformations and their dynamic behavior and the discovery of conformer selection by lectins. Acta Anat (Basel) 1998; 161 (1-4): 91-109
    CrossrefPubMedGoogle Scholar
  • 53 Tyler A. An auto-antibody concept of cell structure, growth and differentiation. Growth 1946; 10 (06) 7-19
    PubMedGoogle Scholar
  • 54 Weiss P. The problem of specificity in growth and development. Yale J Biol Med 1947; 19 (03) 235-278
    PubMedGoogle Scholar
  • 55 Fischer E. Einfluss der Configuration auf die Wirkung der Enzyme. Ber Dtsch Chem Ges 1894; 27: 2985-2993
    CrossrefPubMedGoogle Scholar
  • 56 Mitchell SW. Researches upon the venom of the rattlesnake: with an investigation of the anatomy and physiology of the organs concerned. Smithsonian Contributions to Knowledge; 1860: 89-90
    Google Scholar
  • 57 Flexner S, Noguchi H. Snake venom in relation to haemolysis, bacteriolysis and toxicity. J Exp Med 1902; 6 (03) 277-301
    CrossrefPubMedGoogle Scholar
  • 58 Gartner TK, Stocker K, Williams DC. Thrombolectin: a lectin isolated from Bothrops atrox venom. FEBS Lett 1980; 117 (01) 13-16
    CrossrefPubMedGoogle Scholar
  • 59 Kocourek J. Historical background. In: Liener IE, Sharon N, Goldstein IJ. , eds. The Lectins. Properties, Functions and Applications in Biology and Medicine. New York: Academic Press; 1986: 1-32
    Google Scholar
  • 60 Kilpatrick DC, Green C. Lectins as blood typing reagents. Adv Lectin Res 1992; 5: 51-94
    PubMedGoogle Scholar
  • 61 Gabius H-J. The history of lectinology. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 261-268
    Google Scholar
  • 62 Landsteiner K. Zur Kenntnis der antifermentativen, lytischen und agglutinierenden Wirkungen des Blutserums in der Lymphe. Zbl Bakteriol Orig 1900; 27: 357-362
    PubMedGoogle Scholar
  • 63 Landsteiner K. Ueber Agglutinationserscheinungen normalen menschlichen Blutes. Wien Klin Wochenschr 1901; 46: 1132-1134
    PubMedGoogle Scholar
  • 64 Boyd WC. The proteins of immune reactions. In: Neurath H, Bailey K. , eds. The Proteins. New York: Academic Press; 1954: 756-844
    Google Scholar
  • 65 Boyd WC. The lectins: their present status. Vox Sang 1963; 8: 1-32
    CrossrefPubMedGoogle Scholar
  • 66 Bird GWG. Lectins in immunohematology. Transfus Med Rev 1989; 3 (01) 55-62
    CrossrefPubMedGoogle Scholar
  • 67 Nowell PC. Phytohemagglutinin: an initiator of mitosis in cultures of normal human leukocytes. Cancer Res 1960; 20: 462-466
    PubMedGoogle Scholar
  • 68 Landsteiner K, Raubitschek H. Ueber die Adsorption von Immunstoffen. V. Mitteilung. Biochem Z 1909; 15: 33-51
    PubMedGoogle Scholar
  • 69 Freier T, Fleischmann G, Rüdiger H. Affinity chromatography on immobilized hog gastric mucin and ovomucoid. A general method for isolation of lectins. Biol Chem Hoppe Seyler 1985; 366 (11) 1023-1028
    CrossrefPubMedGoogle Scholar
  • 70 Watkins WM, Morgan WTJ. Neutralization of the anti-H agglutinin in eel serum by simple sugars. Nature 1952; 169 (4307): 825-826
    CrossrefPubMedGoogle Scholar
  • 71 Watkins WM. A half century of blood-group antigen research: some personal recollections. Trends Glycosci Glycotechnol 1999; 11 (62) 391-411
    CrossrefPubMedGoogle Scholar
  • 72 Barondes SH. Bifunctional properties of lectins: lectins redefined. Trends Biochem Sci 1988; 13 (12) 480-482
    CrossrefPubMedGoogle Scholar
  • 73 Gabius H-J, André S, Jiménez-Barbero J, Romero A, Solís D. From lectin structure to functional glycomics: principles of the sugar code. Trends Biochem Sci 2011; 36 (06) 298-313
    CrossrefPubMedGoogle Scholar
  • 74 Fujimoto Z, Tateno H, Hirabayashi J. Lectin structures: classification based on the 3-D structures. Methods Mol Biol 2014; 1200: 579-606
    PubMedGoogle Scholar
  • 75 Solís D, Bovin NV, Davis AP. , et al. A guide into glycosciences: how chemistry, biochemistry and biology cooperate to crack the sugar code. Biochim Biophys Acta 2015; 1850 (01) 186-235
    CrossrefPubMedGoogle Scholar
  • 76 Gabius H-J, Springer WR, Barondes SH. Receptor for the cell binding site of discoidin I. Cell 1985; 42 (02) 449-456
    CrossrefPubMedGoogle Scholar
  • 77 Gabius H-J. Animal lectins. Eur J Biochem 1997; 243 (03) 543-576
    CrossrefPubMedGoogle Scholar
  • 78 Gready JN, Zelensky AN. Routes in lectin evolution: case study on the C-type lectin-like domains. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 329-346
    Google Scholar
  • 79 Drickamer K, Taylor ME. Recent insights into structures and functions of C-type lectins in the immune system. Curr Opin Struct Biol 2015; 34: 26-34
    CrossrefPubMedGoogle Scholar
  • 80 Mayer S, Raulf MK, Lepenies B. C-type lectins: their network and roles in pathogen recognition and immunity. Histochem Cell Biol 2017; 147 (02) 223-237
    CrossrefPubMedGoogle Scholar
  • 81 Angata T, Brinkman-Van der Linden E. I-type lectins. Biochim Biophys Acta 2002; 1572 (2-3): 294-316
    CrossrefPubMedGoogle Scholar
  • 82 Macauley MS, Crocker PR, Paulson JC. Siglec-mediated regulation of immune cell function in disease. Nat Rev Immunol 2014; 14 (10) 653-666
    CrossrefPubMedGoogle Scholar
  • 83 Hirabayashi J. , ed. Recent topics on galectins. Trends Glycosci Glycotechnol 1997; 9: 1-180
    CrossrefPubMedGoogle Scholar
  • 84 Cooper DNW. Galectinomics: finding themes in complexity. Biochim Biophys Acta 2002; 1572 (2-3): 209-231
    CrossrefPubMedGoogle Scholar
  • 85 Kaltner H, Toegel S, García Caballero G, Manning JC, Ledeen RW, Gabius HJ. Galectins: their network and roles in immunity/tumor growth control. Histochem Cell Biol 2017; 147 (02) 239-256
    CrossrefPubMedGoogle Scholar
  • 86 García Caballero G, Manning JC, Ludwig A-K. , et al. Members of the galectin network with deviations from the canonical sequence signature. 1. Galectin-Related Inter-Fiber Protein (GRIFIN). Trends Glycosci Glycotechnol 2018; 30 (172) SE1-SE9
    CrossrefPubMedGoogle Scholar
  • 87 Leffler H. Galectin history, some stories, and some outstanding questions. Trends Glycosci Glycotechnol 2018; 30 (172) SE129-SE135
    CrossrefPubMedGoogle Scholar
  • 88 Kasai K-i. Galectins: quadruple-faced proteins. Trends Glycosci Glycotechnol 2018; 30 (172) SE221-SE223
    CrossrefPubMedGoogle Scholar
  • 89 Kaltner H, Raschta A-S, Manning JC, Gabius HJ. Copy-number variation of functional galectin genes: studying animal galectin-7 (p53-induced gene 1 in man) and tandem-repeat-type galectins-4 and -9. Glycobiology 2013; 23 (10) 1152-1163
    CrossrefPubMedGoogle Scholar
  • 90 Gabius H-J, Manning JC, Kopitz J, André S, Kaltner H. Sweet complementarity: the functional pairing of glycans with lectins. Cell Mol Life Sci 2016; 73 (10) 1989-2016
    CrossrefPubMedGoogle Scholar
  • 91 Iborra S, Sancho D. Signalling versatility following self and non-self sensing by myeloid C-type lectin receptors. Immunobiology 2015; 220 (02) 175-184
    CrossrefPubMedGoogle Scholar
  • 92 Drummond RA, Brown GD. Signalling C-type lectins in antimicrobial immunity. PLoS Pathog 2013; 9 (07) e1003417
    CrossrefPubMedGoogle Scholar
  • 93 Shiokawa M, Yamasaki S, Saijo S. C-type lectin receptors in anti-fungal immunity. Curr Opin Microbiol 2017; 40: 123-130
    CrossrefPubMedGoogle Scholar
  • 94 Gabius H-J, Brehler R, Schauer A, Cramer F. Localization of endogenous lectins in normal human breast, benign breast lesions and mammary carcinomas. Virchows Arch B Cell Pathol Incl Mol Pathol 1986; 52 (02) 107-115 [Cell Pathol]
    CrossrefPubMedGoogle Scholar
  • 95 Kaltner H, García Caballero G, Sinowatz F. , et al. 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 2016; 1860 (10) 2298-2312
    CrossrefPubMedGoogle Scholar
  • 96 Manning JC, García Caballero G, Knospe C, Kaltner H, Gabius HJ. Network analysis of adhesion/growth-regulatory galectins and their binding sites in adult chicken retina and choroid. J Anat 2017; 231 (01) 23-37
    CrossrefPubMedGoogle Scholar
  • 97 Zivicová V, Broz P, Fík Z. , et al. 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 2017; 37 (05) 2275-2288
    PubMedGoogle Scholar
  • 98 Manning JC, García Caballero G, Knospe C, Kaltner H, Gabius HJ. Three-step monitoring of glycan and galectin profiles in the anterior segment of the adult chicken eye. Ann Anat 2018; 217: 66-81
    CrossrefPubMedGoogle Scholar
  • 99 Kopitz J, Xiao Q, Ludwig A-K. , et al. 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 Engl 2017; 56 (46) 14677-14681
    CrossrefPubMedGoogle Scholar
  • 100 Xiao Q, Ludwig AK, Romanò C. , et al. Exploring functional pairing between surface glycoconjugates and human galectins using programmable glycodendrimersomes. Proc Natl Acad Sci U S A 2018; 115 (11) E2509-E2518
    CrossrefPubMedGoogle Scholar
  • 101 Kopitz J, von Reitzenstein C, André S. , et al. Negative regulation of neuroblastoma cell growth by carbohydrate-dependent surface binding of galectin-1 and functional divergence from galectin-3. J Biol Chem 2001; 276 (38) 35917-35923
    CrossrefPubMedGoogle Scholar
  • 102 Weinmann D, Schlangen K, André S. , et al. Galectin-3 induces a pro-degradative/inflammatory gene signature in human chondrocytes, teaming up with galectin-1 in osteoarthritis pathogenesis. Sci Rep 2016; 6: 39112
    CrossrefPubMedGoogle Scholar
  • 103 Weinmann D, Kenn M, Schmidt S. , et al. Galectin-8 induces functional disease markers in human osteoarthritis and cooperates with galectins-1 and -3. Cell Mol Life Sci 2018; 75 (22) 4187-4205
    CrossrefPubMedGoogle Scholar
  • 104 Gabius H-J, Roth J. An introduction to the sugar code. Histochem Cell Biol 2017; 147 (02) 111-117
    CrossrefPubMedGoogle Scholar
  • 105 Schweizer A, Fransen JA, Bächi T, Ginsel L, Hauri HP. Identification, by a monoclonal antibody, of a 53-kD protein associated with a tubulo-vesicular compartment at the cis-side of the Golgi apparatus. J Cell Biol 1988; 107 (05) 1643-1653
    CrossrefPubMedGoogle Scholar
  • 106 Appenzeller C, Andersson H, Kappeler F, Hauri HP. The lectin ERGIC-53 is a cargo transport receptor for glycoproteins. Nat Cell Biol 1999; 1 (06) 330-334
    CrossrefPubMedGoogle Scholar
  • 107 Nichols WC, Seligsohn U, Zivelin A. , et al. Mutations in the ER-Golgi intermediate compartment protein ERGIC-53 cause combined deficiency of coagulation factors V and VIII. Cell 1998; 93 (01) 61-70
    CrossrefPubMedGoogle Scholar
  • 108 Zhang B, Cunningham MA, Nichols WC. , et al. Bleeding due to disruption of a cargo-specific ER-to-Golgi transport complex. Nat Genet 2003; 34 (02) 220-225
    CrossrefPubMedGoogle Scholar
  • 109 Kawasaki N, Ichikawa Y, Matsuo I. , et al. The sugar-binding ability of ERGIC-53 is enhanced by its interaction with MCFD2. Blood 2008; 111 (04) 1972-1979
    CrossrefPubMedGoogle Scholar
  • 110 Yoshida Y. F-box proteins that contain sugar-binding domains. Biosci Biotechnol Biochem 2007; 71 (11) 2623-2631
    CrossrefPubMedGoogle Scholar
  • 111 Aebi M, Bernasconi R, Clerc S, Molinari M. N-glycan structures: recognition and processing in the ER. Trends Biochem Sci 2010; 35 (02) 74-82
    CrossrefPubMedGoogle Scholar
  • 112 Roth J, Zuber C. Quality control of glycoprotein folding and ERAD: the role of N-glycan handling, EDEM1 and OS-9. Histochem Cell Biol 2017; 147 (02) 269-284
    CrossrefPubMedGoogle Scholar
  • 113 Springer T, Galfré G, Secher DS, Milstein C. Mac-1: a macrophage differentiation antigen identified by monoclonal antibody. Eur J Immunol 1979; 9 (04) 301-306
    CrossrefPubMedGoogle Scholar
  • 114 Josefsson EC, Gebhard HH, Stossel TP, Hartwig JH, Hoffmeister KM. The macrophage αMβ2 integrin αM lectin domain mediates the phagocytosis of chilled platelets. J Biol Chem 2005; 280 (18) 18025-18032
    CrossrefPubMedGoogle Scholar
  • 115 Hoffmeister K, Falet H. Platelet glycoproteins as lectin in hematology. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 485-493
    Google Scholar
  • 116 Yamanoi K, Nakayama J. Reduced αGlcNAc glycosylation on gastric gland mucin is a biomarker of malignant potential for gastric cancer, Barrett's adenocarcinoma, and pancreatic cancer. Histochem Cell Biol 2018; 149 (06) 569-575
    CrossrefPubMedGoogle Scholar
  • 117 Holla A, Skerra A. Comparative analysis reveals selective recognition of glycans by the dendritic cell receptors DC-SIGN and Langerin. Protein Eng Des Sel 2011; 24 (09) 659-669
    CrossrefPubMedGoogle Scholar
  • 118 Feinberg H, Rowntree TJ, Tan SL, Drickamer K, Weis WI, Taylor ME. Common polymorphisms in human langerin change specificity for glycan ligands. J Biol Chem 2013; 288 (52) 36762-36771
    CrossrefPubMedGoogle Scholar
  • 119 Pipirou Z, Powlesland AS, Steffen I, Pöhlmann S, Taylor ME, Drickamer K. Mouse LSECtin as a model for a human Ebola virus receptor. Glycobiology 2011; 21 (06) 806-812
    CrossrefPubMedGoogle Scholar
  • 120 Davis CW, Mattei LM, Nguyen HY, Ansarah-Sobrinho C, Doms RW, Pierson TC. The location of asparagine-linked glycans on West Nile virions controls their interactions with CD209 (dendritic cell-specific ICAM-3 grabbing nonintegrin). J Biol Chem 2006; 281 (48) 37183-37194
    CrossrefPubMedGoogle Scholar
  • 121 Powlesland AS, Ward EM, Sadhu SK, Guo Y, Taylor ME, Drickamer K. Widely divergent biochemical properties of the complete set of mouse DC-SIGN-related proteins. J Biol Chem 2006; 281 (29) 20440-20449
    CrossrefPubMedGoogle Scholar
  • 122 Sodetz JM, Paulson JC, Pizzo SV, McKee PA. Carbohydrate on human factor VIII/von Willebrand factor. Impairment of function by removal of specific galactose residues. J Biol Chem 1978; 253 (20) 7202-7206
    CrossrefPubMedGoogle Scholar
  • 123 Smedsrød B, Einarsson M, Pertoft H. Tissue plasminogen activator is endocytosed by mannose and galactose receptors of rat liver cells. Thromb Haemost 1988; 59 (03) 480-484
    Article in Thieme ConnectPubMedGoogle Scholar
  • 124 Grozovsky R, Begonja AJ, Liu K. , et al. The Ashwell-Morell receptor regulates hepatic thrombopoietin production via JAK2-STAT3 signaling. Nat Med 2015; 21 (01) 47-54
    CrossrefPubMedGoogle Scholar
  • 125 Grewal PK, Uchiyama S, Ditto D. , et al. The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat Med 2008; 14 (06) 648-655
    CrossrefPubMedGoogle Scholar
  • 126 Ellies LG, Ditto D, Levy GG. , et al. Sialyltransferase ST3Gal-IV operates as a dominant modifier of hemostasis by concealing asialoglycoprotein receptor ligands. Proc Natl Acad Sci U S A 2002; 99 (15) 10042-10047
    CrossrefPubMedGoogle Scholar
  • 127 Unverzagt C, André S, Seifert J. , et al. Structure-activity profiles of complex biantennary glycans with core fucosylation and with/without additional α 2,3/α 2,6 sialylation: synthesis of neoglycoproteins and their properties in lectin assays, cell binding, and organ uptake. J Med Chem 2002; 45 (02) 478-491
    CrossrefPubMedGoogle Scholar
  • 128 Park EI, Mi Y, Unverzagt C, Gabius HJ, Baenziger JU. The asialoglycoprotein receptor clears glycoconjugates terminating with sialic acid α 2,6GalNAc. Proc Natl Acad Sci U S A 2005; 102 (47) 17125-17129
    CrossrefPubMedGoogle Scholar
  • 129 Steirer LM, Park EI, Townsend RR, Baenziger JU. The asialoglycoprotein receptor regulates levels of plasma glycoproteins terminating with sialic acid α2,6-galactose. J Biol Chem 2009; 284 (06) 3777-3783
    CrossrefPubMedGoogle Scholar
  • 130 Iwaki J, Hirabayashi J. Carbohydrate-binding specificity of human galectins: an overview by frontal affinity chromatography. Trends Glycosci Glycotechnol 2018; 30 (172) SE137-SE153
    CrossrefPubMedGoogle Scholar
  • 131 Romaniuk MA, Tribulatti MV, Cattaneo V. , et al. Human platelets express and are activated by galectin-8. Biochem J 2010; 432 (03) 535-547
    CrossrefPubMedGoogle Scholar
  • 132 Zappelli C, van der Zwaan C, Thijssen-Timmer DC, Mertens K, Meijer AB. Novel role for galectin-8 protein as mediator of coagulation factor V endocytosis by megakaryocytes. J Biol Chem 2012; 287 (11) 8327-8335
    CrossrefPubMedGoogle Scholar
  • 133 Kamitori S. Three-dimensional structures of galectins. Trends Glycosci Glycotechnol 2018; 30 (172) SE41-SE50
    CrossrefPubMedGoogle Scholar
  • 134 Pegon JN, Kurdi M, Casari C. , et al. Factor VIII and von Willebrand factor are ligands for the carbohydrate-receptor Siglec-5. Haematologica 2012; 97 (12) 1855-1863
    CrossrefPubMedGoogle Scholar
  • 135 Krzeminski M, Singh T, André S. , et al. Human galectin-3 (Mac-2 antigen): defining molecular switches of affinity to natural glycoproteins, structural and dynamic aspects of glycan binding by flexible ligand docking and putative regulatory sequences in the proximal promoter region. Biochim Biophys Acta 2011; 1810 (02) 150-161
    CrossrefPubMedGoogle Scholar
  • 136 Nonaka M, Ma BY, Murai R. , et al. Glycosylation-dependent interactions of C-type lectin DC-SIGN with colorectal tumor-associated Lewis glycans impair the function and differentiation of monocyte-derived dendritic cells. J Immunol 2008; 180 (05) 3347-3356
    CrossrefPubMedGoogle Scholar
  • 137 McEver RP. Selectins: novel receptors that mediate leukocyte adhesion during inflammation. Thromb Haemost 1991; 65 (03) 223-228
    Article in Thieme ConnectPubMedGoogle Scholar
  • 138 Furie B, Furie BC, Flaumenhaft R. A journey with platelet P-selectin: the molecular basis of granule secretion, signalling and cell adhesion. Thromb Haemost 2001; 86 (01) 214-221
    Article in Thieme ConnectPubMedGoogle Scholar
  • 139 Wu KK. TM hidden treasure: lectin-like domain. Blood 2012; 119 (05) 1103-1104
    CrossrefPubMedGoogle Scholar
  • 140 Gallatin WM, Weissman IL, Butcher EC. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature 1983; 304 (5921): 30-34
    CrossrefPubMedGoogle Scholar
  • 141 Bevilacqua MP, Pober JS, Mendrick DL, Cotran RS, Gimbrone Jr MA. Identification of an inducible endothelial-leukocyte adhesion molecule. Proc Natl Acad Sci U S A 1987; 84 (24) 9238-9242
    CrossrefPubMedGoogle Scholar
  • 142 McEver RP, Martin MN. A monoclonal antibody to a membrane glycoprotein binds only to activated platelets. J Biol Chem 1984; 259 (15) 9799-9804
    CrossrefPubMedGoogle Scholar
  • 143 Stenberg PE, McEver RP, Shuman MA, Jacques YV, Bainton DF. A platelet α-granule membrane protein (GMP-140) is expressed on the plasma membrane after activation. J Cell Biol 1985; 101 (03) 880-886
    CrossrefPubMedGoogle Scholar
  • 144 Berman CL, Yeo EL, Wencel-Drake JD, Furie BC, Ginsberg MH, Furie B. A platelet α granule membrane protein that is associated with the plasma membrane after activation. Characterization and subcellular localization of platelet activation-dependent granule-external membrane protein. J Clin Invest 1986; 78 (01) 130-137
    CrossrefPubMedGoogle Scholar
  • 145 McEver RP. GMP-140: a receptor for neutrophils and monocytes on activated platelets and endothelium. J Cell Biochem 1991; 45 (02) 156-161
    CrossrefPubMedGoogle Scholar
  • 146 Geng JG, Bevilacqua MP, Moore KL. , et al. Rapid neutrophil adhesion to activated endothelium mediated by GMP-140. Nature 1990; 343 (6260): 757-760
    CrossrefPubMedGoogle Scholar
  • 147 Rosen SD, Singer MS, Yednock TA, Stoolman LM. Involvement of sialic acid on endothelial cells in organ-specific lymphocyte recirculation. Science 1985; 228 (4702): 1005-1007
    CrossrefPubMedGoogle Scholar
  • 148 Ali S, Jenkins Y, Kirkley M. , et al. Leukocyte extravasation: an immunoregulatory role for α-L-fucosidase?. J Immunol 2008; 181 (04) 2407-2413
    CrossrefPubMedGoogle Scholar
  • 149 Imai Y, Lasky LA, Rosen SD. Sulphation requirement for GlyCAM-1, an endothelial ligand for L-selectin. Nature 1993; 361 (6412): 555-557
    CrossrefPubMedGoogle Scholar
  • 150 Hooper LV, Manzella SM, Baenziger JU. The biology of sulfated oligosaccharides. In: Gabius H-J, Gabius S. , eds. Glycosciences: Status and Perspectives. London, UK and Weinheim, Germany: Chapman & Hall; 1997: 261-276
    Google Scholar
  • 151 Hemmerich S, Rosen SD. Carbohydrate sulfotransferases in lymphocyte homing. Glycobiology 2000; 10 (09) 849-856
    CrossrefPubMedGoogle Scholar
  • 152 Fukuda M, Hiraoka N, Akama TO, Fukuda MN. Carbohydrate-modifying sulfotransferases: structure, function, and pathophysiology. J Biol Chem 2001; 276 (51) 47747-47750
    CrossrefPubMedGoogle Scholar
  • 153 Kawashima H. Two roles of mucin sulfation. Trends Glycosci Glycotechnol 2010; 22 (127) 211-225
    CrossrefPubMedGoogle Scholar
  • 154 Baenziger JU. Glycoprotein hormone GalNAc-4-sulphotransferase. Biochem Soc Trans 2003; 31 (02) 326-330
    CrossrefPubMedGoogle Scholar
  • 155 André S, Sanchez-Ruderisch H, Nakagawa H. , et al. 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 2007; 274 (13) 3233-3256
    CrossrefPubMedGoogle Scholar
  • 156 Amano M, Eriksson H, Manning JC. , et al. 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 2012; 279 (21) 4062-4080
    CrossrefPubMedGoogle Scholar
  • 157 Amano M, Galvan M, He J, Baum LG. The ST6Gal I sialyltransferase selectively modifies N-glycans on CD45 to negatively regulate galectin-1-induced CD45 clustering, phosphatase modulation, and T cell death. J Biol Chem 2003; 278 (09) 7469-7475
    CrossrefPubMedGoogle Scholar
  • 158 Sperandio M. Selectins and glycosyltransferases in leukocyte rolling in vivo. FEBS J 2006; 273 (19) 4377-4389
    CrossrefPubMedGoogle Scholar
  • 159 Marathe DD, Chandrasekaran EV, Lau JT, Matta KL, Neelamegham S. Systems-level studies of glycosyltransferase gene expression and enzyme activity that are associated with the selectin binding function of human leukocytes. FASEB J 2008; 22 (12) 4154-4167
    CrossrefPubMedGoogle Scholar
  • 160 Lo CY, Antonopoulos A, Gupta R. , et al. Competition between core 2 GlcNAc-transferase and ST6GalNAc-transferase regulates the synthesis of the leukocyte selectin ligand on human P-selectin glycoprotein ligand-1. J Biol Chem 2013; 288 (20) 13974-13987
    CrossrefPubMedGoogle Scholar
  • 161 Moreau R, Dausset J, Bernard J, Moullec J. Acquired hemolytic anemia with polyagglutinability of erythrocytes by a new factor present in normal blood [in French]. Bull Mem Soc Med Hop Paris 1957; 73 (20-21): 569-587
    PubMedGoogle Scholar
  • 162 Berger EG. Tn-syndrome. Biochim Biophys Acta 1999; 1455 (2-3): 255-268
    PubMedGoogle Scholar
  • 163 Ju T, Otto VI, Cummings RD. The Tn antigen-structural simplicity and biological complexity. Angew Chem Int Ed Engl 2011; 50 (08) 1770-1791
    CrossrefPubMedGoogle Scholar
  • 164 Hounsell EF, Davies MJ, Renouf DV. O-linked protein glycosylation structure and function. Glycoconj J 1996; 13 (01) 19-26
    CrossrefPubMedGoogle Scholar
  • 165 Dam TK, Gerken TA, Brewer CF. Thermodynamics of multivalent carbohydrate-lectin cross-linking interactions: importance of entropy in the bind and jump mechanism. Biochemistry 2009; 48 (18) 3822-3827
    CrossrefPubMedGoogle Scholar
  • 166 Dam TK, Brewer CF. Multivalent lectin-carbohydrate interactions energetics and mechanisms of binding. Adv Carbohydr Chem Biochem 2010; 63: 139-164
    PubMedGoogle Scholar
  • 167 Corfield AP. Mucins: a biologically relevant glycan barrier in mucosal protection. Biochim Biophys Acta 2015; 1850 (01) 236-252
    CrossrefPubMedGoogle Scholar
  • 168 Hurtado-Guerrero R. Recent structural and mechanistic insights into protein O-GalNAc glycosylation. Biochem Soc Trans 2016; 44 (01) 61-67
    CrossrefPubMedGoogle Scholar
  • 169 Tenno M, Ohtsubo K, Hagen FK. , et al. Initiation of protein O glycosylation by the polypeptide GalNAcT-1 in vascular biology and humoral immunity. Mol Cell Biol 2007; 27 (24) 8783-8796
    CrossrefPubMedGoogle Scholar
  • 170 Iida S, Yamamoto K, Irimura T. Interaction of human macrophage C-type lectin with O-linked N-acetylgalactosamine residues on mucin glycopeptides. J Biol Chem 1999; 274 (16) 10697-10705
    CrossrefPubMedGoogle Scholar
  • 171 Wu AM, Wu JH, Liu J-H. , et al. Effects of polyvalency of glycotopes and natural modifications of human blood group ABH/Lewis sugars at the Galβ1-terminated core saccharides on the binding of domain-I of recombinant tandem-repeat-type galectin-4 from rat gastrointestinal tract (G4-N). Biochimie 2004; 86 (4-5): 317-326
    CrossrefPubMedGoogle Scholar
  • 172 Wahrenbrock MG, Varki A. Multiple hepatic receptors cooperate to eliminate secretory mucins aberrantly entering the bloodstream: are circulating cancer mucins the “tip of the iceberg”?. Cancer Res 2006; 66 (04) 2433-2441
    CrossrefPubMedGoogle Scholar
  • 173 Li Y, Fu J, Ling Y. , et al. Sialylation on O-glycans protects platelets from clearance by liver Kupffer cells. Proc Natl Acad Sci U S A 2017; 114 (31) 8360-8365
    CrossrefPubMedGoogle Scholar
  • 174 Mortezai N, Behnken HN, Kurze AK. , et al. Tumor-associated Neu5Ac-Tn and Neu5Gc-Tn antigens bind to C-type lectin CLEC10A (CD301, MGL). Glycobiology 2013; 23 (07) 844-852
    CrossrefPubMedGoogle Scholar
  • 175 Takamiya R, Ohtsubo K, Takamatsu S, Taniguchi N, Angata T. The interaction between Siglec-15 and tumor-associated sialyl-Tn antigen enhances TGF-β secretion from monocytes/macrophages through the DAP12-Syk pathway. Glycobiology 2013; 23 (02) 178-187
    CrossrefPubMedGoogle Scholar
  • 176 Angata T, Tabuchi Y, Nakamura K, Nakamura M. Siglec-15: an immune system Siglec conserved throughout vertebrate evolution. Glycobiology 2007; 17 (08) 838-846
    CrossrefPubMedGoogle Scholar
  • 177 Lu Q, Lu G, Qi J. , et al. PILRα and PILRβ have a siglec fold and provide the basis of binding to sialic acid. Proc Natl Acad Sci U S A 2014; 111 (22) 8221-8226
    CrossrefPubMedGoogle Scholar
  • 178 Kuroki K, Wang J, Ose T. , et al. Structural basis for simultaneous recognition of an O-glycan and its attached peptide of mucin family by immune receptor PILRα. Proc Natl Acad Sci U S A 2014; 111 (24) 8877-8882
    CrossrefPubMedGoogle Scholar
  • 179 Gabius H-J, Kaltner H, Kopitz J, André S. The glycobiology of the CD system: a dictionary for translating marker designations into glycan/lectin structure and function. Trends Biochem Sci 2015; 40 (07) 360-376
    CrossrefPubMedGoogle Scholar
  • 180 Rodriguez MC, Yegorova S, Pitteloud JP. , et al. Thermodynamic switch in binding of adhesion/growth regulatory human galectin-3 to tumor-associated TF antigen (CD176) and MUC1 glycopeptides. Biochemistry 2015; 54 (29) 4462-4474
    CrossrefPubMedGoogle Scholar
  • 181 Artigas G, Hinou H, Garcia-Martin F, Gabius HJ, Nishimura SI. Synthetic mucin-like glycopeptides as versatile tools to measure effects of glycan structure/density/position on the interaction with adhesion/growth-regulatory galectins in arrays. Chem Asian J 2017; 12 (01) 159-167
    CrossrefPubMedGoogle Scholar
  • 182 Crocker PR, Hartnell A, Munday J, Nath D. The potential role of sialoadhesin as a macrophage recognition molecule in health and disease. Glycoconj J 1997; 14 (05) 601-609
    CrossrefPubMedGoogle Scholar
  • 183 Beatson R, Tajadura-Ortega V, Achkova D. , et al. The mucin MUC1 modulates the tumor immunological microenvironment through engagement of the lectin Siglec-9. Nat Immunol 2016; 17 (11) 1273-1281
    CrossrefPubMedGoogle Scholar
  • 184 Blixt O, Collins BE, van den Nieuwenhof IM, Crocker PR, Paulson JC. Sialoside specificity of the siglec family assessed using novel multivalent probes: identification of potent inhibitors of myelin-associated glycoprotein. J Biol Chem 2003; 278 (33) 31007-31019
    CrossrefPubMedGoogle Scholar
  • 185 Bannert N, Craig S, Farzan M. , et al. Sialylated O-glycans and sulfated tyrosines in the NH2-terminal domain of CC chemokine receptor 5 contribute to high affinity binding of chemokines. J Exp Med 2001; 194 (11) 1661-1673
    CrossrefPubMedGoogle Scholar
  • 186 Frommhold D, Ludwig A, Bixel MG. , et al. Sialyltransferase ST3Gal-IV controls CXCR2-mediated firm leukocyte arrest during inflammation. J Exp Med 2008; 205 (06) 1435-1446
    CrossrefPubMedGoogle Scholar
  • 187 Sperandio M. The expanding role of α2-3 sialylation for leukocyte trafficking in vivo. Ann N Y Acad Sci 2012; 1253: 201-205
    CrossrefPubMedGoogle Scholar
  • 188 Kudelka MR, Ju T, Heimburg-Molinaro J, Cummings RD. Simple sugars to complex disease--mucin-type O-glycans in cancer. Adv Cancer Res 2015; 126: 53-135
    PubMedGoogle Scholar
  • 189 Dimitroff CJ. Galectin-binding O-glycosylations as regulators of malignancy. Cancer Res 2015; 75 (16) 3195-3202
    CrossrefPubMedGoogle Scholar
  • 190 Murugaesu N, Iravani M, van Weverwijk A. , et al. An in vivo functional screen identifies ST6GalNAc2 sialyltransferase as a breast cancer metastasis suppressor. Cancer Discov 2014; 4 (03) 304-317
    CrossrefPubMedGoogle Scholar
  • 191 Reticker-Flynn NE, Bhatia SN. Aberrant glycosylation promotes lung cancer metastasis through adhesion to galectins in the metastatic niche. Cancer Discov 2015; 5 (02) 168-181
    CrossrefPubMedGoogle Scholar
  • 192 Galvan M, Tsuboi S, Fukuda M, Baum LG. Expression of a specific glycosyltransferase enzyme regulates T cell death mediated by galectin-1. J Biol Chem 2000; 275 (22) 16730-16737
    CrossrefPubMedGoogle Scholar
  • 193 Cabrera PV, Amano M, Mitoma J. , et al. Haploinsufficiency of C2GnT-I glycosyltransferase renders T lymphoma cells resistant to cell death. Blood 2006; 108 (07) 2399-2406
    CrossrefPubMedGoogle Scholar
  • 194 Valenzuela HF, Pace KE, Cabrera PV. , et al. O-glycosylation regulates LNCaP prostate cancer cell susceptibility to apoptosis induced by galectin-1. Cancer Res 2007; 67 (13) 6155-6162
    CrossrefPubMedGoogle Scholar
  • 195 Tsuboi S, Sutoh M, Hatakeyama S. , et al. A novel strategy for evasion of NK cell immunity by tumours expressing core 2 O-glycans. EMBO J 2011; 30 (15) 3173-3185
    CrossrefPubMedGoogle Scholar
  • 196 Ledeen RW, Kopitz J, Abad-Rodríguez J, Gabius HJ. Glycan chains of gangliosides: functional ligands for tissue lectins (siglecs/galectins). Prog Mol Biol Transl Sci 2018; 156: 289-324
    PubMedGoogle Scholar
  • 197 Bucior I, Burger MM. Fernàndez-Busquets. Carbohydrate-carbohydrate interactions. In: Gabius H-J. , ed. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009: 347-362
    Google Scholar
  • 198 Sanchez-Ruderisch H, Fischer C, Detjen KM. , et al. Tumor suppressor p16INK4a: downregulation of galectin-3, an endogenous competitor of the pro-anoikis effector galectin-1, in a pancreatic carcinoma model. FEBS J 2010; 277 (17) 3552-3563
    CrossrefPubMedGoogle Scholar
  • 199 Ruiz FM, Gilles U, Ludwig A-K. , et al. Chicken GRIFIN: structural characterization in crystals and in solution. Biochimie 2018; 146: 127-138
    CrossrefPubMedGoogle Scholar
  • 200 Kopitz J, Vértesy S, André S, Fiedler S, Schnölzer M, Gabius HJ. 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 2014; 104: 90-99
    CrossrefPubMedGoogle Scholar
  • 201 Flores-Ibarra A, Vértesy S, Medrano FJ, Gabius HJ, Romero A. Crystallization of a human galectin-3 variant with two ordered segments in the shortened N-terminal tail. Sci Rep 2018; 8 (01) 9835
    CrossrefPubMedGoogle Scholar
  • 202 Springer TA. Monoclonal antibody analysis of complex biological systems. Combination of cell hybridization and immunoadsorbents in a novel cascade procedure and its application to the macrophage cell surface. J Biol Chem 1981; 256 (08) 3833-3839
    CrossrefPubMedGoogle Scholar
  • 203 Ho MK, Springer TA. Mac-2, a novel 32,000 Mr mouse macrophage subpopulation-specific antigen defined by monoclonal antibodies. J Immunol 1982; 128 (03) 1221-1228
    PubMedGoogle Scholar
  • 204 Flotte TJ, Springer TA, Thorbecke GJ. Dendritic cell and macrophage staining by monoclonal antibodies in tissue sections and epidermal sheets. Am J Pathol 1983; 111 (01) 112-124
    PubMedGoogle Scholar
  • 205 Hughes RC. Mac-2: a versatile galactose-binding protein of mammalian tissues. Glycobiology 1994; 4 (01) 5-12
    CrossrefPubMedGoogle Scholar
  • 206 Dawson H, André S, Karamitopoulou E, Zlobec I, Gabius HJ. The growing galectin network in colon cancer and clinical relevance of cytoplasmic galectin-3 reactivity. Anticancer Res 2013; 33 (08) 3053-3059
    PubMedGoogle Scholar
  • 207 Ahmad N, Gabius H-J, André S. , et al. Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes. J Biol Chem 2004; 279 (12) 10841-10847
    CrossrefPubMedGoogle Scholar
  • 208 Halimi H, Rigato A, Byrne D. , et al. Glycan dependence of Galectin-3 self-association properties. PLoS One 2014; 9 (11) e111836
    CrossrefPubMedGoogle Scholar
  • 209 Ippel H, Miller MC, Vértesy S. , et al. Intra- and intermolecular interactions of human galectin-3: assessment by full-assignment-based NMR. Glycobiology 2016; 26 (08) 888-903
    CrossrefPubMedGoogle Scholar
  • 210 Lin YH, Qiu DC, Chang WH. , et al. The intrinsically disordered N-terminal domain of galectin-3 dynamically mediates multisite self-association of the protein through fuzzy interactions. J Biol Chem 2017; 292 (43) 17845-17856
    CrossrefPubMedGoogle Scholar
  • 211 Linsley PS, Horn D, Marquardt H. , et al. Identification of a novel serum protein secreted by lung carcinoma cells. Biochemistry 1986; 25 (10) 2978-2986
    CrossrefPubMedGoogle Scholar
  • 212 Rosenberg I, Cherayil BJ, Isselbacher KJ, Pillai S. Mac-2-binding glycoproteins. Putative ligands for a cytosolic β-galactoside lectin. J Biol Chem 1991; 266 (28) 18731-18736
    CrossrefPubMedGoogle Scholar
  • 213 Sasaki T, Brakebusch C, Engel J, Timpl R. Mac-2 binding protein is a cell-adhesive protein of the extracellular matrix which self-assembles into ring-like structures and binds β1 integrins, collagens and fibronectin. EMBO J 1998; 17 (06) 1606-1613
    CrossrefPubMedGoogle Scholar
  • 214 DeRoo EP, Wrobleski SK, Shea EM. , et al. The role of galectin-3 and galectin-3-binding protein in venous thrombosis. Blood 2015; 125 (11) 1813-1821
    CrossrefPubMedGoogle Scholar
  • 215 Blostein M, Cuerquis J, Galipeau J. Galectin 3-binding protein is a potential contaminant of recombinantly produced factor IX. Haemophilia 2007; 13 (06) 701-706
    CrossrefPubMedGoogle Scholar
  • 216 Papaspyridonos M, McNeill E, de Bono JP. , et al. Galectin-3 is an amplifier of inflammation in atherosclerotic plaque progression through macrophage activation and monocyte chemoattraction. Arterioscler Thromb Vasc Biol 2008; 28 (03) 433-440
    CrossrefPubMedGoogle Scholar
  • 217 Filer A, Bik M, Parsonage GN. , et al. Galectin 3 induces a distinctive pattern of cytokine and chemokine production in rheumatoid synovial fibroblasts via selective signaling pathways. Arthritis Rheum 2009; 60 (06) 1604-1614
    CrossrefPubMedGoogle Scholar
  • 218 Miller MC, Ludwig A-K, Wichapong K. , et al. Adhesion/growth-regulatory galectins tested in combination: evidence for formation of hybrids as heterodimers. Biochem J 2018; 475 (05) 1003-1018
    CrossrefPubMedGoogle Scholar
  • 219 Vértesy S, Michalak M, Miller MC. , et al. Structural significance of galectin design: impairment of homodimer stability by linker insertion and partial reversion by ligand presence. Protein Eng Des Sel 2015; 28 (07) 199-210
    CrossrefPubMedGoogle Scholar
  • 220 Sharon N. Glycoproteins now and then: a personal account. Acta Anat (Basel) 1998; 161 (1-4): 7-17
    CrossrefPubMedGoogle Scholar
  • 221 Damjanov I. Lectin cytochemistry and histochemistry. Lab Invest 1987; 57 (01) 5-20
    PubMedGoogle Scholar
  • 222 Spicer SS, Schulte BA. Detection and differentiation of glycoconjugates in various cell types by lectin histochemistry. Basic Appl Histochem 1988; 32 (03) 307-320
    PubMedGoogle Scholar
  • 223 Gabius H-J, Wosgien B, Hendrys M, Bardosi A. Lectin localization in human nerve by biochemically defined lectin-binding glycoproteins, neoglycoprotein and lectin-specific antibody. Histochemistry 1991; 95 (03) 269-277
    CrossrefPubMedGoogle Scholar
  • 224 Spicer SS, Schulte BA. Diversity of cell glycoconjugates shown histochemically: a perspective. J Histochem Cytochem 1992; 40 (01) 1-38
    CrossrefPubMedGoogle Scholar
  • 225 Danguy A, Akif F, Pajak B, Gabius HJ. Contribution of carbohydrate histochemistry to glycobiology. Histol Histopathol 1994; 9 (01) 155-171
    PubMedGoogle Scholar
  • 226 Roth J. Lectins for histochemical demonstration of glycans. Histochem Cell Biol 2011; 136 (02) 117-130
    CrossrefPubMedGoogle Scholar
  • 227 Roy R, Cao Y, Kaltner H. , et al. Teaming up synthetic chemistry and histochemistry for activity screening in galectin-directed inhibitor design. Histochem Cell Biol 2017; 147 (02) 285-301
    CrossrefPubMedGoogle Scholar
  • 228 Gabius H-J. Cell surface glycans: the why and how of their functionality as biochemical signals in lectin-mediated information transfer. Crit Rev Immunol 2006; 26 (01) 43-79
    CrossrefPubMedGoogle Scholar
  • 229 Randi AM, Smith KE, Castaman G. von Willebrand factor regulation of blood vessel formation. Blood 2018; 132 (02) 132-140
    CrossrefPubMedGoogle Scholar
  • 230 Degn SE, Jensenius JC, Bjerre M. The lectin pathway and its implications in coagulation, infections and auto-immunity. Curr Opin Organ Transplant 2011; 16 (01) 21-27
    CrossrefPubMedGoogle Scholar
  • 231 Larsen JB, Hvas CL, Hvas AM. The lectin pathway in thrombotic conditions-a systematic review. Thromb Haemost 2018; 118 (07) 1141-1166
    Article in Thieme ConnectPubMedGoogle Scholar