Cellular and Molecular Life Sciences

, Volume 73, Issue 10, pp 1989–2016 | Cite as

Sweet complementarity: the functional pairing of glycans with lectins

  • H.-J. GabiusEmail author
  • J. C. Manning
  • J. Kopitz
  • S. André
  • H. Kaltner


Carbohydrates establish the third alphabet of life. As part of cellular glycoconjugates, the glycans generate a multitude of signals in a minimum of space. The presence of distinct glycotopes and the glycome diversity are mapped by sugar receptors (antibodies and lectins). Endogenous (tissue) lectins can read the sugar-encoded information and translate it into functional aspects of cell sociology. Illustrated by instructive examples, each glycan has its own ligand properties. Lectins with different folds can converge to target the same epitope, while intrafamily diversification enables functional cooperation and antagonism. The emerging evidence for the concept of a network calls for a detailed fingerprinting. Due to the high degree of plasticity and dynamics of the display of genes for lectins the validity of extrapolations between different organisms of the phylogenetic tree yet is inevitably limited.


Agglutinin Antibodies Glycobiology Glycome Lectins Sialylation Sugar code 



Blood-dendritic cell antigen-2


Chicken galectin


Cluster of differentiation


Carbohydrate recognition domain




Dendritic cell-specific ICAM-3-grabbing nonintegrin(-related protein)


Deoxyribonucleic acid


Epidermal growth factor (receptor)








Immunoglobulin G


3-deoxy-d-manno-oct-2-ulosonic acid






Liver and lymph node sinusoidal endothelial cell C-type lectin




Mannose (or mannan)-binding protein/lectin


Macrophage galactose(-binding C)-type lectin




Osteoclast inhibitory lectin


Paired Ig-like receptors


Sialic acid-binding immunoglobulin-like lectin


Single nucleotide polymorphism

T(F) antigen

Thomsen(-Friedenreich) antigen


Transforming growth factor (receptor)

Tn antigen

T antigen nouvelle


Transient receptor potential [canonical] channel 5



We are indebted to Drs. B. Friday, R. Gabius, M. Ilsüm, A. Leddoz, A.W.L. Nose and B. Onil for inspiring discussions and the reviewers for their valuable input.

Supplementary material

18_2016_2163_MOESM1_ESM.pdf (171 kb)
Supplementary material 1 (PDF 172 kb)
18_2016_2163_MOESM2_ESM.tif (1.8 mb)
Supplementary material 2 (TIFF 1863 kb)
18_2016_2163_MOESM3_ESM.tif (6.5 mb)
Supplementary material 3 (TIFF 6623 kb)
18_2016_2163_MOESM4_ESM.tif (10.6 mb)
Supplementary material 4 (TIFF 10834 kb)
18_2016_2163_MOESM5_ESM.pptx (71 kb)
Supplementary material 5 (PPTX 71 kb)


  1. 1.
    Sharon N (1975) Complex Carbohydrates. Their Chemistry, Biosynthesis, and Functions. Addison-Wesley Publ. Co., Reading, MA, USAGoogle Scholar
  2. 2.
    Reuter G, Gabius H-J (1999) Eukaryotic glycosylation: whim of nature or multipurpose tool? Cell Mol Life Sci 55(3):368–422PubMedCrossRefGoogle Scholar
  3. 3.
    Haji-Ghassemi O, Blackler RJ, Young NM, Evans SV (2015) Antibody recognition of carbohydrate epitopes. Glycobiology 25(9):920–952. doi: 10.1093/glycob/cwv037 PubMedCrossRefGoogle Scholar
  4. 4.
    Avery OT, Macleod CM, McCarty M (1944) Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type I. J Exp Med 79(2):137–158PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Ioffe E, Stanley P (1994) Mice lacking N-acetylglucosaminyltransferase I activity die at mid-gestation, revealing an essential role for complex or hybrid N-linked carbohydrates. Proc Natl Acad Sci USA 91(2):728–732PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Metzler M, Gertz A, Sarkar M, Schachter H, Schrader JW, Marth JD (1994) Complex asparagine-linked oligosaccharides are required for morphogenic events during post-implantation development. EMBO J 13(9):2056–2065PubMedPubMedCentralGoogle Scholar
  7. 7.
    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, Germany, pp 385–401Google Scholar
  8. 8.
    Schachter H (2014) Complex N-glycans: the story of the “yellow brick road”. Glycoconj J 31(1):1–5. doi: 10.1007/s10719-013-9507-5 PubMedCrossRefGoogle Scholar
  9. 9.
    Hennet T (2009) Diseases of glycosylation. In: Gabius H-J (ed) The Sugar Code. Fundamentals of glycosciences, Wiley-VCH, Weinheim, Germany, pp 365–383Google Scholar
  10. 10.
    Hennet T, Cabalzar J (2015) Congenital disorders of glycosylation: a concise chart of glycocalyx dysfunction. Trends Biochem Sci 40(7):377–384. doi: 10.1016/j.tibs.2015.03.002 PubMedCrossRefGoogle Scholar
  11. 11.
    Sly WS (2000) The missing link in lysosomal enzyme targeting. J Clin Invest 105:563–564PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Kollmann K, Pohl S, Marschner K, Encarnacao M, Sakwa I, Tiede S, Poorthuis BJ, Lubke T, Muller-Loennies S, Storch S, Braulke T (2010) Mannose phosphorylation in health and disease. Eur J Cell Biol 89(1):117–123. doi: 10.1016/j.ejcb.2009.10.008 PubMedCrossRefGoogle Scholar
  13. 13.
    Roseman S (2001) Reflections on glycobiology. J Biol Chem 276(45):41527–41542PubMedCrossRefGoogle Scholar
  14. 14.
    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 - Weinheim, pp 1–14Google Scholar
  15. 15.
    Gabius H-J, André S, Kaltner H, Siebert H-C (2002) The sugar code: functional lectinomics. Biochim Biophys Acta 1572(2–3):165–177PubMedCrossRefGoogle Scholar
  16. 16.
    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, Germany, pp 3–13Google Scholar
  17. 17.
    Buddecke E (2009) Proteoglycans. In: Gabius H-J (ed) The Sugar Code. Fundamentals of glycosciences, Wiley-VCH, Weinheim, Germany, pp 199–216Google Scholar
  18. 18.
    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, Germany, pp 111–137Google Scholar
  19. 19.
    Zuber C, Roth J (2009) N-Glycosylation. In: Gabius H-J (ed) The Sugar Code. Fundamentals of glycosciences, Wiley-VCH, Weinheim, Germany, pp 87–110Google Scholar
  20. 20.
    Lee YC (2009) Tracing the development of structural elucidation of N-glycans. Trends Glycosci Glycotechnol 21:53–69CrossRefGoogle Scholar
  21. 21.
    Rees DA (1972) Shapely polysaccharides. Biochem J 126(2):257–273PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Winterburn PJ, Phelps CF (1972) The significance of glycosylated proteins. Nature 236:147–151PubMedCrossRefGoogle Scholar
  23. 23.
    Wilson IBH, Paschinger H, Rendic D (2009) Glycosylation of model and ‘lower’ organisms. In: Gabius H-J (ed) The Sugar Code. Fundamentals of glycosciences, Wiley-VCH, Weinheim, Germany, pp 139–154Google Scholar
  24. 24.
    Jarrell KF, Ding Y, Meyer BH, Albers SV, Kaminski L, Eichler J (2014) N-Linked glycosylation in Archaea: a structural, functional, and genetic analysis. Microbiol Mol Biol Rev 78(2):304–341. doi: 10.1128/MMBR.00052-13 PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Tytgat HL, Lebeer S (2014) The sweet tooth of bacteria: common themes in bacterial glycoconjugates. Microbiol Mol Biol Rev 78(3):372–417. doi: 10.1128/MMBR.00007-14 PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Corfield AP, Berry M (2015) Glycan variation and evolution in the eukaryotes. Trends Biochem Sci 40(7):351–359. doi: 10.1016/j.tibs.2015.04.004 PubMedCrossRefGoogle Scholar
  27. 27.
    Tan FY, Tang CM, Exley RM (2015) Sugar coating: bacterial protein glycosylation and host-microbe interactions. Trends Biochem Sci 40(7):342–350. doi: 10.1016/j.tibs.2015.03.016 PubMedCrossRefGoogle Scholar
  28. 28.
    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(7):360–376. doi: 10.1016/j.tibs.2015.03.013 PubMedCrossRefGoogle Scholar
  29. 29.
    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 1–32Google Scholar
  30. 30.
    Rüdiger H, Gabius H-J (2009) The history of lectinology. In: Gabius H-J (ed) The Sugar Code. Fundamentals of glycosciences, Wiley-VCH, Weinheim, Germany, pp 261–268Google Scholar
  31. 31.
    Landsteiner K (1901) Ueber Agglutinationserscheinungen normalen menschlichen Blutes. Wien Klin Wochenschr 46:1132–1134Google Scholar
  32. 32.
    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(4):889–893PubMedCrossRefGoogle Scholar
  33. 33.
    Schwarz HP, Dorner F (2003) Karl Landsteiner and his major contributions to haematology. Br J Haematol 121(4):556–565PubMedCrossRefGoogle Scholar
  34. 34.
    Mitchell SW (1860) Researches upon the venom of the rattlesnake. Smithsonian Contributions to Knowledge XII (Article VI):89-90Google Scholar
  35. 35.
    Stillmark H (1888) Ueber Ricin, ein giftiges Ferment aus den Samen von Ricinus comm. L. und einigen anderen Euphorbiaceen. Inaugural-Dissertation, Dorpat: Schnakenburg’s BuchdruckereiGoogle Scholar
  36. 36.
    Kilpatrick DC, Green C (1992) Lectins as blood typing reagents. Adv Lectin Res 5:51–94Google Scholar
  37. 37.
    Elfstrand M (1898) Ueber blutkörperchenagglutinierende Eiweisse. In: Kobert R (ed) Görbersdorfer Veröffentlichungen. Enke, Stuttgart, pp 1-159Google Scholar
  38. 38.
    Krüpe M (1956) Blutgruppenspezifische pflanzliche Eiweißkörper, Phytagglutinine. Enke, StuttgartGoogle Scholar
  39. 39.
    Allen NK, Brilliantine L (1969) A survey of hemagglutinins in various seeds. J Immunol 102(5):1295–1299PubMedGoogle Scholar
  40. 40.
    Boyd WC (1963) The lectins: their present status. Vox Sang 8:1–32PubMedCrossRefGoogle Scholar
  41. 41.
    Landsteiner K (1945) The Specificity of Serological Reactions. Harvard University Press, CambridgeGoogle Scholar
  42. 42.
    Watkins WM, Morgan WTJ (1952) Neutralisation of the anti-H agglutinin in eel serum by simple sugars. Nature 169:825–826PubMedCrossRefGoogle Scholar
  43. 43.
    Watkins WM (1999) A half century of blood-group antigen research: some personal recollections. Trends Glycosci Glycotechnol 11:391–411CrossRefGoogle Scholar
  44. 44.
    Boyd WC (1954) The proteins of immune reactions. In: Neurath H, Bailey K (eds) The Proteins, vol 2., Part 2. Academic Press, New York, pp 756–844Google Scholar
  45. 45.
    Sumner JB, Howell SF (1936) The identification of a hemagglutinin of the jack bean with concanavalin A. J Bacteriol 32:227–237PubMedPubMedCentralGoogle Scholar
  46. 46.
    Bird GWG (1989) Lectins in immunohematology. Transfusion Med Rev 3:55–62CrossRefGoogle Scholar
  47. 47.
    Barondes SH (1988) Bifunctional properties of lectins: lectins redefined. Trends Biochem Sci 13:480–482PubMedCrossRefGoogle Scholar
  48. 48.
    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(6):298–313. doi: 10.1016/j.tibs.2011.01.005 PubMedCrossRefGoogle Scholar
  49. 49.
    Gabius HJ, Springer WR, Barondes SH (1985) Receptor for the cell binding site of discoidin I. Cell 42(2):449–456PubMedCrossRefGoogle Scholar
  50. 50.
    Goldstein IJ, Poretz RD (1986) Isolation, physicochemical characterization, and carbohydrate-binding specificity of lectins. In: Liener IE, Sharon N, Goldstein IJ (eds) The Lectins. Properties, Functions, and Applications in Biology and Medicine. Academic Press, Orlando, pp 33-247Google Scholar
  51. 51.
    Kilpatrick DC (2000) Handbook of Animal Lectins. J. Wiley & Sons, ChichesterGoogle Scholar
  52. 52.
    Loris R (2002) Principles of structures of animal and plant lectins. Biochim Biophys Acta 1572:198–208PubMedCrossRefGoogle Scholar
  53. 53.
    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, Germany, pp 279–300Google Scholar
  54. 54.
    Rüdiger H, Gabius H-J (2009) Plant lectins. In: Gabius H-J (ed) The Sugar Code. Fundamentals of glycosciences, Wiley-VCH, Weinheim, Germany, pp 301–315Google Scholar
  55. 55.
    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. doi: 10.1016/j.bbagen.2014.03.016 PubMedCrossRefGoogle Scholar
  56. 56.
    Lehotzky RE, Partch CL, Mukherjee S, Cash HL, Goldman WE, Gardner KH, Hooper LV (2010) Molecular basis for peptidoglycan recognition by a bactericidal lectin. Proc Natl Acad Sci USA 107(17):7722–7727PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    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(8):603–610. doi: 10.1038/nsmb.3053 PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Matsunaga I, Moody DB (2009) Mincle is a long sought receptor for mycobacterial cord factor. J Exp Med 206(13):2865–2868. doi: 10.1084/jem.20092533 PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Ishikawa E, Ishikawa T, Morita YS, Toyonaga K, Yamada H, Takeuchi O, Kinoshita T, Akira S, Yoshikai Y, Yamasaki S (2009) Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J Exp Med 206(13):2879–2888. doi: 10.1084/jem.20091750 PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Furukawa A, Kamishikiryo J, Mori D, Toyonaga K, Okabe Y, Toji A, Kanda R, Miyake Y, Ose T, Yamasaki S, Maenaka K (2013) Structural analysis for glycolipid recognition by the C-type lectins Mincle and MCL. Proc Natl Acad Sci USA 110(43):17438–17443. doi: 10.1073/pnas.1312649110 PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Jegouzo SA, Harding EC, Acton O, Rex MJ, Fadden AJ, Taylor ME, Drickamer K (2014) Defining the conformation of human mincle that interacts with mycobacterial trehalose dimycolate. Glycobiology 24(12):1291–1300. doi: 10.1093/glycob/cwu072 PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Nicolson GL (1974) The interactions of lectins with animal cell surfaces. Int Rev Cytol 39:89–190PubMedCrossRefGoogle Scholar
  63. 63.
    Roth J (1978) The lectins: molecular probes in cell biology and membrane research. Exp Pathol 3(Suppl 1):1–186Google Scholar
  64. 64.
    Spicer SS, Schulte BA (1992) Diversity of cell glycoconjugates shown histochemically: a perspective. J Histochem Cytochem 40:1–38PubMedCrossRefGoogle Scholar
  65. 65.
    Danguy A, Akif F, Pajak B, Gabius H-J (1994) Contribution of carbohydrate histochemistry to glycobiology. Histol Histopathol 9:155–171PubMedGoogle Scholar
  66. 66.
    Roth J (2011) Lectins for histochemical demonstration of glycans. Histochem Cell Biol 136(2):117–130. doi: 10.1007/s00418-011-0848-5 PubMedCrossRefGoogle Scholar
  67. 67.
    Josefsson EC, Gebhard HH, Stossel TP, Hartwig JH, Hoffmeister KM (2005) The macrophage αMβ2 integrin αM lectin domain mediates the phagocytosis of chilled platelets. J Biol Chem 280(18):18025–18032PubMedCrossRefGoogle Scholar
  68. 68.
    Hoffmeister K, Falet H (2009) Platelet glycoproteins as lectin in hematology. In: Gabius H-J (ed) The Sugar Code. Fundamentals of glycosciences, Wiley-VCH, Weinheim, Germany, pp 485–493Google Scholar
  69. 69.
    de Jong MAWP, Vriend LE, Theelen B, Taylor ME, Fluitsma D, Boekhout T, Geijtenbeek TB (2010) C-Type lectin Langerin is a β-glucan receptor on human Langerhans cells that recognizes opportunistic and pathogenic fungi. Mol Immunol 47(6):1216–1225. doi: 10.1016/j.molimm.2009.12.016 PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Holla A, Skerra A (2011) Comparative analysis reveals selective recognition of glycans by the dendritic cell receptors DC-SIGN and Langerin. Protein Eng Des Sel 24(9):659–669. doi: 10.1093/protein/gzr016 PubMedCrossRefGoogle Scholar
  71. 71.
    Feinberg H, Rowntree TJ, Tan SL, Drickamer K, Weis WI, Taylor ME (2013) Common polymorphisms in human langerin change specificity for glycan ligands. J Biol Chem 288(52):36762–36771. doi: 10.1074/jbc.M113.528000 PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Dominguez-Soto A, Aragoneses-Fenoll L, Martin-Gayo E, Martinez-Prats L, Colmenares M, Naranjo-Gomez M, Borras FE, Munoz P, Zubiaur M, Toribio ML, Delgado R, Corbi AL (2007) The DC-SIGN-related lectin LSECtin mediates antigen capture and pathogen binding by human myeloid cells. Blood 109(12):5337–5345. doi: 10.1182/blood-2006-09-048058 PubMedCrossRefGoogle Scholar
  73. 73.
    Tang L, Yang J, Tang X, Ying W, Qian X, He F (2010) The DC-SIGN family member LSECtin is a novel ligand of CD44 on activated T cells. Eur J Immunol 40(4):1185–1191. doi: 10.1002/eji.200939936 PubMedCrossRefGoogle Scholar
  74. 74.
    Pipirou Z, Powlesland AS, Steffen I, Pohlmann S, Taylor ME, Drickamer K (2011) Mouse LSECtin as a model for a human Ebola virus receptor. Glycobiology 21(6):806–812. doi: 10.1093/glycob/cwr008 PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Zhang F, Ren S, Zuo Y (2014) DC-SIGN, DC-SIGNR and LSECtin: C-type lectins for infection. Int Rev Immunol 33(1):54–66. doi: 10.3109/08830185.2013.834897 PubMedCrossRefGoogle Scholar
  76. 76.
    Thomsen T, Schlosser A, Holmskov U, Sorensen GL (2011) Ficolins and FIBCD1: soluble and membrane bound pattern recognition molecules with acetyl group selectivity. Mol Immunol 48(4):369–381. doi: 10.1016/j.molimm.2010.09.019 PubMedCrossRefGoogle Scholar
  77. 77.
    Terada M, Khoo KH, Inoue R, Chen CI, Yamada K, Sakaguchi H, Kadowaki N, Ma BY, Oka S, Kawasaki T, Kawasaki N (2005) Characterization of oligosaccharide ligands expressed on SW1116 cells recognized by mannan-binding protein. A highly fucosylated polylactosamine type N-glycan. J Biol Chem 280(12):10897–10913PubMedCrossRefGoogle Scholar
  78. 78.
    Kawasaki N, Lin CW, Inoue R, Khoo KH, Kawasaki N, Ma BY, Oka S, Ishiguro M, Sawada T, Ishida H, Hashimoto T, Kawasaki T (2009) Highly fucosylated N-glycan ligands for mannan-binding protein expressed specifically on CD26 (DPPVI) isolated from a human colorectal carcinoma cell line, SW1116. Glycobiology 19(4):437–450PubMedCrossRefGoogle Scholar
  79. 79.
    Kawasaki N, Kawasaki T (2010) Recognition of endogenous ligands by C-type lectins: interaction of serum mannan-binding protein with tumor-associated oligosaccharide epitopes. Trends Glycosci Glycotechnol 22(125):141–151CrossRefGoogle Scholar
  80. 80.
    Davis CW, Mattei LM, Nguyen HY, Ansarah-Sobrinho C, Doms RW, Pierson TC (2006) 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 281(48):37183–37194. doi: 10.1074/jbc.M605429200 PubMedCrossRefGoogle Scholar
  81. 81.
    Powlesland AS, Ward EM, Sadhu SK, Guo Y, Taylor ME, Drickamer K (2006) Widely divergent biochemical properties of the complete set of mouse DC-SIGN-related proteins. J Biol Chem 281(29):20440–20449. doi: 10.1074/jbc.M601925200 PubMedCrossRefGoogle Scholar
  82. 82.
    Nakayama J, Yeh JC, Misra AK, Ito S, Katsuyama T, Fukuda M (1999) Expression cloning of a human α1,4-N-acetylglucosaminyltransferase that forms GlcNAcα1,4Galβ-R, a glycan specifically expressed in the gastric gland mucous cell-type mucin. Proc Natl Acad Sci USA 96(16):8991–8996PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    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(2):185–199. doi: 10.1007/s00418-015-1383-6
  84. 84.
    Hoffmann W (2015) TFF2, a MUC6-binding lectin stabilizing the gastric mucus barrier and more. Int J Oncol 47(3):806–816. doi: 10.3892/ijo.2015.3090 PubMedGoogle Scholar
  85. 85.
    Nakayama J (2014) Dual roles of gastric gland mucin-specific O-glycans in prevention of gastric cancer. Acta Histochem Cytochem 47(1):1–9. doi: 10.1267/ahc.13034 PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Becker DJ, Lowe JB (2003) Fucose: biosynthesis and biological functions in mammals. Glycobiology 13:41R–53RPubMedCrossRefGoogle Scholar
  87. 87.
    Martinez-Duncker I, Mollicone R, Candelier J-J, Breton C, Oriol R (2003) A new superfamily of protein-O-fucosyltransferases, α2-fucosyltransferases, and α6-fucosyltransferases: phylogeny and identification of conserved peptide motifs. Glycobiology 13(12):1C–5CPubMedCrossRefGoogle Scholar
  88. 88.
    Ma B, Simala-Grant JL, Taylor DE (2006) Fucosylation in prokaryotes and eukaryotes. Glycobiology 16(12):158R–184R. doi: 10.1093/glycob/cwl040 PubMedCrossRefGoogle Scholar
  89. 89.
    Aplin JD, Jones CJ (2012) Fucose, placental evolution and the glycocode. Glycobiology 22(4):470–478. doi: 10.1093/glycob/cwr156 PubMedCrossRefGoogle Scholar
  90. 90.
    Furukawa K, Sato T (1999) β1,4-Galactosylation of N-glycans is a complex process. Biochim Biophys Acta 1473(1):54–66PubMedCrossRefGoogle Scholar
  91. 91.
    Guo S, Sato T, Shirane K, Furukawa K (2001) Galactosylation of N-linked oligosaccharides by human β1,4-galactosyltransferases I, II, III, IV, V, and VI expressed in Sf-9 cells. Glycobiology 11(10):813–820PubMedCrossRefGoogle Scholar
  92. 92.
    Hennet T (2002) The galactosyltransferase family. Cell Mol Life Sci 59(7):1081–1095PubMedCrossRefGoogle Scholar
  93. 93.
    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(5):1565–1572PubMedGoogle Scholar
  94. 94.
    Morell AG, van den Hamer CJA, Scheinberg IH, Ashwell G (1966) Physical and chemical studies on ceruloplasmin. IV. Preparation of radioactive, sialic acid-free ceruloplasmin labeled with tritium on terminal d-galactose residues. J Biol Chem 241(16):3745–3749PubMedGoogle Scholar
  95. 95.
    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(17):5536–5543PubMedGoogle Scholar
  96. 96.
    Grewal PK, Uchiyama S, Ditto D, Varki N, Le DT, Nizet V, Marth JD (2008) The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat Med 14(6):648–655. doi: 10.1038/nm1760 PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Grozovsky R, Begonja AJ, Liu K, Visner G, Hartwig JH, Falet H, Hoffmeister KM (2015) The Ashwell-Morell receptor regulates hepatic thrombopoietin production via JAK2-STAT3 signaling. Nat Med 21(1):47–54. doi: 10.1038/nm.3770 PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Riboldi E, Daniele R, Parola C, Inforzato A, Arnold PL, Bosisio D, Fremont DH, Bastone A, Colonna M, Sozzani S (2011) Human C-type lectin domain family 4, member C (CLEC4C/BDCA-2/CD303) is a receptor for asialo-galactosyl-oligosaccharides. J Biol Chem 286(41):35329–35333. doi: 10.1074/jbc.C111.290494 PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Barondes SH (1984) Soluble lectins: a new class of extracellular proteins. Science 223:1259–1264PubMedCrossRefGoogle Scholar
  100. 100.
    Barondes SH (1997) Galectins: a personal review. Trends Glycosci Glycotechnol 9:1–7CrossRefGoogle Scholar
  101. 101.
    Hirabayashi J (ed) (1997) Recent topics on galectins. Trends Glycosci Glycotechnol 9:1–180CrossRefGoogle Scholar
  102. 102.
    Cooper DNW (2002) Galectinomics: finding themes in complexity. Biochim Biophys Acta 1572:209–231PubMedCrossRefGoogle Scholar
  103. 103.
    Kaltner H, Gabius H-J (2012) A toolbox of lectins for translating the sugar code: the galectin network in phylogenesis and tumors. Histol Histopathol 27(4):397–416PubMedGoogle Scholar
  104. 104.
    Dam TK, Gabius H-J, André S, Kaltner H, Lensch M, Brewer CF (2005) Galectins bind to the multivalent glycoprotein asialofetuin with enhanced affinities and a gradient of decreasing binding constants. Biochemistry 44:12564–12571PubMedCrossRefGoogle Scholar
  105. 105.
    Togayachi A, Narimatsu H (2012) Functional analysis of β1,3-N-acetylglucosaminyltransferases and regulation of immunological function by polylactosamine. Trends Glycosci Glycotechnol 24:95–111CrossRefGoogle Scholar
  106. 106.
    Fiete D, Beranek M, Baenziger JU (2012) Molecular basis for protein-specific transfer of N-acetylgalactosamine to N-linked glycans by the glycosyltransferases β1,4-N-acetylgalactosaminyl transferase 3 (β4GalNAc-T3) and β4GalNAc-T4. J Biol Chem 287(34):29194–29203. doi: 10.1074/jbc.M112.371567 PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Park EI, Baenziger JU (2004) Closely related mammals have distinct asialoglycoprotein receptor carbohydrate specificities. J Biol Chem 279(39):40954–40959. doi: 10.1074/jbc.M406647200 PubMedCrossRefGoogle Scholar
  108. 108.
    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(3):1902–1907PubMedCrossRefGoogle Scholar
  109. 109.
    Fiete D, Srivastava V, Hindsgaul O, Baenziger JU (1991) A hepatic reticuloendothelial cell receptor specific for SO4-4GalNAcβ1,4GlcNAcβ1,2Manα that mediates rapid clearance of lutropin. Cell 67(6):1103–1110PubMedCrossRefGoogle Scholar
  110. 110.
    Fiete D, Beranek MC, Baenziger JU (1997) The macrophage/endothelial cell mannose receptor cDNA encodes a protein that binds oligosaccharides terminating with SO4-4-GalNAcβ1,4GlcNAcβ or Man at independent sites. Proc Natl Acad Sci USA 94:11256–11261PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Hooper LV, Manzella SM, Baenziger JU (1997) The biology of sulfated oligosaccharides. In: Gabius H-J, Gabius S (eds) Glycosciences: Status and Perspectives. Chapman & Hall, London - Weinheim, pp 261–276Google Scholar
  112. 112.
    East L, Isacke CM (2002) The mannose receptor family. Biochim Biophys Acta 1572(2–3):364–386PubMedCrossRefGoogle Scholar
  113. 113.
    Chapman E, Best MD, Hanson SR, Wong CH (2004) Sulfotransferases: structure, mechanism, biological activity, inhibition, and synthetic utility. Angew Chem Int Ed 43(27):3526–3548. doi: 10.1002/anie.200300631 CrossRefGoogle Scholar
  114. 114.
    Kawashima H (2010) Two roles of mucin sulfation. Trends Glycosci Glycotechnol 22:211–225CrossRefGoogle Scholar
  115. 115.
    Laporte B, Gonzalez-Hilarion S, Maftah A, Petit JM (2009) The second bovine β-galactoside-α2,6-sialyltransferase (ST6Gal II): genomic organization and stimulation of its in vitro expression by IL-6 in bovine mammary epithelial cells. Glycobiology 19(10):1082–1093. doi: 10.1093/glycob/cwp094 PubMedCrossRefGoogle Scholar
  116. 116.
    Takashima S, Tsuji S (2011) Functional diversity of mammalian sialyltransferases. Trends Glycosci Glycotechnol 23:178–193CrossRefGoogle Scholar
  117. 117.
    Joziasse DH, Schiphorst WECM, van den Eijnden DH, van Kuik JA, van Halbeek H, Vliegenthart JFG (1987) Branch specificity of bovine colostrum CMP-sialic acid: Galβ1-4GlcNAc-R α2-6-sialyltransferase. Sialylation of bi-, tri-, and tetraantennary oligosaccharides and glycopeptides of the N-acetyllactosamine type. J Biol Chem 262(5):2025–2033PubMedGoogle Scholar
  118. 118.
    Reuter G, Gabius H-J (1996) Sialic acids. Structure, analysis, metabolism, and recognition. Biol Chem Hoppe-Seyler 377:325–342PubMedCrossRefGoogle Scholar
  119. 119.
    Siebert H-C, Rosen J, Seyrek K, Kaltner H, André S, Bovin NV, Nyholm P-G, Sinowatz F, Gabius H-J (2006) α2,3/α2,6-Sialylation of N-glycans: non-synonymous signals with marked developmental regulation in bovine reproductive tracts. Biochimie 88:399–410PubMedCrossRefGoogle Scholar
  120. 120.
    Kadirvelraj R, Grant OC, Goldstein IJ, Winter HC, Tateno H, Fadda E, Woods RJ (2011) Structure and binding analysis of Polyporus squamosus lectin in complex with the Neu5Acα2-6Galβ1-4GlcNAc human-type influenza receptor. Glycobiology 21(7):973–984. doi: 10.1093/glycob/cwr030 PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Ahmad N, Gabius H-J, Kaltner H, André S, Kuwabara I, Liu F-T, Oscarson S, Norberg T, Brewer CF (2002) Thermodynamic binding studies of cell surface carbohydrate epitopes to galectins-1, -3 and -7. Evidence for differential binding specificities. Can J Chem 80:1096–1104CrossRefGoogle Scholar
  122. 122.
    Park EI, Manzella SM, Baenziger JU (2003) Rapid clearance of sialylated glycoproteins by the asialoglycoprotein receptor. J Biol Chem 278(7):4597–4602. doi: 10.1074/jbc.M210612200 PubMedCrossRefGoogle Scholar
  123. 123.
    Anthony RM, Wermeling F, Karlsson MC, Ravetch JV (2008) Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci USA 105(50):19571–19578. doi: 10.1073/pnas.0810163105 PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Silva-Martin N, Bartual SG, Ramirez-Aportela E, Chacon P, Park CG, Hermoso JA (2014) Structural basis for selective recognition of endogenous and microbial polysaccharides by macrophage receptor SIGN-R1. Structure 22(11):1595–1606. doi: 10.1016/j.str.2014.09.001 PubMedCrossRefGoogle Scholar
  125. 125.
    André S, Unverzagt C, Kojima S, Dong X, Fink C, Kayser K, Gabius H-J (1997) Neoglycoproteins with the synthetic complex biantennary nonasaccharide or its α2,3/α2,6-sialylated derivatives: their preparation, the assessment of their ligand properties for purified lectins, for tumor cells in vitro and in tissue sections and their biodistribution in tumor-bearing mice. Bioconjugate Chem 8:845–855CrossRefGoogle Scholar
  126. 126.
    André S, Kozár T, Schuberth R, Unverzagt C, Kojima S, Gabius H-J (2007) Substitutions in the N-glycan core as regulators of biorecognition: the case of core-fucose and bisecting GlcNAc moieties. Biochemistry 46:6984–6995PubMedCrossRefGoogle Scholar
  127. 127.
    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(7):557–565PubMedCrossRefGoogle Scholar
  128. 128.
    Ruiz FM, Scholz BA, Buzamet E, Kopitz J, André S, Menendez M, Romero A, Solís D, Gabius H-J (2014) Natural single amino acid polymorphism (F19Y) in human galectin-8: detection of structural alterations and increased growth-regulatory activity on tumor cells. FEBS J 281(5):1446–1464. doi: 10.1111/febs.12716 PubMedCrossRefGoogle Scholar
  129. 129.
    Gabius H-J (1997) Animal lectins. Eur J Biochem 243(3):543–576PubMedCrossRefGoogle Scholar
  130. 130.
    Angata T, Brinkman-van der Linden ECM (2002) I-type lectins. Biochim Biophys Acta 1572(2–3):294–316PubMedCrossRefGoogle Scholar
  131. 131.
    Macauley MS, Crocker PR, Paulson JC (2014) Siglec-mediated regulation of immune cell function in disease. Nat Rev Immunol 14(10):653–666. doi: 10.1038/nri3737 PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Ideo H, Seko A, Ishizuka I, Yamashita K (2003) The N-terminal carbohydrate recognition domain of galectin-8 recognizes specific glycosphingolipids with high affinity. Glycobiology 13(10):713–723. doi: 10.1093/glycob/cwg094 PubMedCrossRefGoogle Scholar
  133. 133.
    Nilsson EC, Storm RJ, Bauer J, Johansson SM, Lookene A, Angstrom J, Hedenstrom M, Eriksson TL, Frangsmyr L, Rinaldi S, Willison HJ, Pedrosa Domellof F, Stehle T, Arnberg N (2011) The GD1a glycan is a cellular receptor for adenoviruses causing epidemic keratoconjunctivitis. Nat Med 17(1):105–109. doi: 10.1038/nm.2267 PubMedCrossRefGoogle Scholar
  134. 134.
    Burmeister WP, Guilligay D, Cusack S, Wadell G, Arnberg N (2004) Crystal structure of species D adenovirus fiber knobs and their sialic acid binding sites. J Virol 78(14):7727–7736. doi: 10.1128/JVI.78.14.7727-7736.2004 PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Svennerholm L (1963) Chromatographic separation of human brain gangliosides. J Neurochem 10:613–623PubMedCrossRefGoogle Scholar
  136. 136.
    Chester MA (1998) IUPAC-IUB Joint Commission on Biochemical Nomenclature (JCBN). Nomenclature of glycolipids–recommendations 1997. Eur J Biochem 257(2):293–298PubMedCrossRefGoogle Scholar
  137. 137.
    Kopitz J (2009) Glycolipids. In: Gabius H-J (ed) The Sugar Code. Fundamentals of glycosciences, Wiley-VCH, Weinheim, Germany, pp 177–198Google Scholar
  138. 138.
    Schengrund CL (2015) Gangliosides: glycosphingolipids essential for normal neural development and function. Trends Biochem Sci 40(7):397–406. doi: 10.1016/j.tibs.2015.03.007 PubMedCrossRefGoogle Scholar
  139. 139.
    Rapoport E, Mikhalyov I, Zhang J, Crocker P, Bovin N (2003) Ganglioside binding pattern of CD33-related siglecs. Bioorg Med Chem Lett 13(4):675–678PubMedCrossRefGoogle Scholar
  140. 140.
    Attrill H, Imamura A, Sharma RS, Kiso M, Crocker PR, van Aalten DM (2006) Siglec-7 undergoes a major conformational change when complexed with the α(2,8)-disialylganglioside GT1b. J Biol Chem 281(43):32774–32783. doi: 10.1074/jbc.M601714200 PubMedCrossRefGoogle Scholar
  141. 141.
    Zhuravleva MA, Trandem K, Sun PD (2008) Structural implications of Siglec-5-mediated sialoglycan recognition. J Mol Biol 375(2):437–447. doi: 10.1016/j.jmb.2007.10.009 PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Zaccai NR, May AP, Robinson RC, Burtnick LD, Crocker PR, Brossmer R, Kelm S, Jones EY (2007) Crystallographic and in silico analysis of the sialoside-binding characteristics of the Siglec sialoadhesin. J Mol Biol 365(5):1469–1479. doi: 10.1016/j.jmb.2006.10.084 PubMedCrossRefGoogle Scholar
  143. 143.
    Kawasaki Y, Ito A, Withers DA, Taima T, Kakoi N, Saito S, Arai Y (2010) Ganglioside DSGb5, preferred ligand for Siglec-7, inhibits NK cell cytotoxicity against renal cell carcinoma cells. Glycobiology 20(11):1373–1379. doi: 10.1093/glycob/cwq116 PubMedCrossRefGoogle Scholar
  144. 144.
    Collins BE, Ito H, Sawada N, Ishida H, Kiso M, Schnaar RL (1999) Enhanced binding of the neural siglecs, myelin-associated glycoprotein and Schwann cell myelin protein, to Chol-1 (α-series) gangliosides and novel sulfated Chol-1 analogs. J Biol Chem 274(53):37637–37643PubMedCrossRefGoogle Scholar
  145. 145.
    Yoon SJ, Nakayama K, Hikita T, Handa K, Hakomori SI (2006) Epidermal growth factor receptor tyrosine kinase is modulated by GM3 interaction with N-linked GlcNAc termini of the receptor. Proc Natl Acad Sci USA 103(50):18987–18991. doi: 10.1073/pnas.0609281103 PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Kawashima N, Yoon SJ, Itoh K, Nakayama K (2009) Tyrosine kinase activity of epidermal growth factor receptor is regulated by GM3 binding through carbohydrate to carbohydrate interactions. J Biol Chem 284(10):6147–6155. doi: 10.1074/jbc.M808171200 PubMedCrossRefGoogle Scholar
  147. 147.
    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, Germany, pp 347–362Google Scholar
  148. 148.
    Lopez PH, Schnaar RL (2009) Gangliosides in cell recognition and membrane protein regulation. Curr Opin Struct Biol 19(5):549–557PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Phongsisay V, Iizasa E, Hara H, Yamasaki S (2015) 3-O-sulfo-β-D-galactose moiety of endogenous sulfoglycolipids is a potential ligand for immunoglobulin-like receptor LMIR5. Mol Immunol 63(2):595–599. doi: 10.1016/j.molimm.2014.07.023 PubMedCrossRefGoogle Scholar
  150. 150.
    Gabius H-J (2015) The magic of the sugar code. Trends Biochem Sci 40(7):341. doi: 10.1016/j.tibs.2015.04.003 PubMedCrossRefGoogle Scholar
  151. 151.
    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(3):491–501PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    Stechly L, Morelle W, Dessein AF, André S, Grard G, Trinel D, Dejonghe MJ, Leteurtre E, Drobecq H, Trugnan G, Gabius H-J, Huet G (2009) Galectin-4-regulated delivery of glycoproteins to the brush border membrane of enterocyte-like cells. Traffic 10(4):438–450PubMedCrossRefGoogle Scholar
  153. 153.
    Velasco S, Díez-Revuelta N, Hernández-Iglesias T, Kaltner H, André S, Gabius H-J, Abad-Rodríguez J (2013) Neuronal galectin-4 is required for axon growth and for the organization of axonal membrane L1 delivery and clustering. J Neurochem 125(1):49–62. doi: 10.1111/jnc.12148 PubMedCrossRefGoogle Scholar
  154. 154.
    Abad-Rodríguez J, Díez-Revuelta N (2015) Axon glycoprotein routing in nerve polarity, function, and repair. Trends Biochem Sci 40(7):385–396. doi: 10.1016/j.tibs.2015.03.015 PubMedCrossRefGoogle Scholar
  155. 155.
    Mamelak D, Mylvaganam M, Whetstone H, Hartmann E, Lennarz W, Wyrick PB, Raulston J, Han H, Hoffman P, Lingwood CA (2001) Hsp70 s contain a specific sulfogalactolipid binding site. Differential aglycone influence on sulfogalactosyl ceramide binding by recombinant prokaryotic and eukaryotic hsp70 family members. Biochemistry 40(12):3572–3582PubMedCrossRefGoogle Scholar
  156. 156.
    Lingwood C, Mylvaganam M, Minhas F, Binnington B, Branch DR, Pomes R (2005) The sulfogalactose moiety of sulfoglycosphingolipids serves as a mimic of tyrosine phosphate in many recognition processes. Prediction and demonstration of Src homology 2 domain/sulfogalactose binding. J Biol Chem 280(13):12542–12547. doi: 10.1074/jbc.M413724200 PubMedCrossRefGoogle Scholar
  157. 157.
    Hartmann E, Lingwood CA, Reidl J (2001) Heat-inducible surface stress protein (Hsp70) mediates sulfatide recognition of the respiratory pathogen Haemophilus influenzae. Infect Immun 69(5):3438–3441. doi: 10.1128/IAI.69.5.3438-3441.2001 PubMedPubMedCentralCrossRefGoogle Scholar
  158. 158.
    Shamshiev A, Gober HJ, Donda A, Mazorra Z, Mori L, De Libero G (2002) Presentation of the same glycolipid by different CD1 molecules. J Exp Med 195(8):1013–1021PubMedPubMedCentralCrossRefGoogle Scholar
  159. 159.
    Duchesneau P, Gallagher E, Walcheck B, Waddell TK (2007) Up-regulation of leukocyte CXCR4 expression by sulfatide: an L-selectin-dependent pathway on CD4 + T cells. Eur J Immunol 37(10):2949–2960. doi: 10.1002/eji.200737118 PubMedCrossRefGoogle Scholar
  160. 160.
    Simonis D, Schlesinger M, Seelandt C, Borsig L, Bendas G (2010) Analysis of SM4 sulfatide as a P-selectin ligand using model membranes. Biophys Chem 150(1–3):98–104. doi: 10.1016/j.bpc.2010.01.007 PubMedCrossRefGoogle Scholar
  161. 161.
    Takahashi T, Suzuki T (2012) Role of sulfatide in normal and pathological cells and tissues. J Lipid Res 53(8):1437–1450. doi: 10.1194/jlr.R026682 PubMedPubMedCentralCrossRefGoogle Scholar
  162. 162.
    Tiemeyer M, Yasuda Y, Schnaar RL (1989) Ganglioside-specific binding protein on rat brain membranes. J Biol Chem 264:1671–1681PubMedGoogle Scholar
  163. 163.
    Gabius S, Kayser K, Hellmann KP, Ciesiolka T, Trittin A, Gabius H-J (1990) Carrier-immobilized derivatized lysoganglioside GM1 is a ligand for specific binding sites in various human tumor cell types and peripheral blood lymphocytes and monocytes. Biochem Biophys Res Commun 169:239–244PubMedCrossRefGoogle Scholar
  164. 164.
    Kayser K, Böhm G, Blum S, Beyer M, Zink S, André S, Gabius H-J (2001) Glyco- and immunohistochemical refinement of the differential diagnosis between mesothelioma and metastatic carcinoma and survival analysis of patients. J Pathol 193:175–180PubMedCrossRefGoogle Scholar
  165. 165.
    Sonnino S, Aureli M, Loberto N, Chigorno V, Prinetti A (2010) Fine tuning of cell functions through remodeling of glycosphingolipids by plasma membrane-associated glycohydrolases. FEBS Lett 584(9):1914–1922PubMedCrossRefGoogle Scholar
  166. 166.
    Lewis AL, Lewis WG (2012) Host sialoglycans and bacterial sialidases: a mucosal perspective. Cell Microbiol 14(8):1174–1182. doi: 10.1111/j.1462-5822.2012.01807.x PubMedCrossRefGoogle Scholar
  167. 167.
    Miyagi T, Yamaguchi K (2012) Mammalian sialidases: physiological and pathological roles in cellular functions. Glycobiology 22(7):880–896. doi: 10.1093/glycob/cws057 PubMedCrossRefGoogle Scholar
  168. 168.
    Pshezhetsky AV, Ashmarina LI (2013) Desialylation of surface receptors as a new dimension in cell signaling. Biochemistry (Moscow) 78(7):736–745. doi: 10.1134/S0006297913070067 CrossRefGoogle Scholar
  169. 169.
    Miyagi T (2010) Mammalian sialidases and their functions. Trends Glycosci Glycotechnol 22:162–172CrossRefGoogle Scholar
  170. 170.
    Pitto M, Chigorno V, Giglioni A, Valsecchi M, Tettamanti G (1989) Sialidase in cerebellar granule cells differentiating in culture. J Neurochem 53(5):1464–1470PubMedCrossRefGoogle Scholar
  171. 171.
    Wu G, Ledeen RW (1991) Stimulation of neurite outgrowth in neuroblastoma cells by neuraminidase: putative role of GM1 ganglioside in differentiation. J Neurochem 56(1):95–104PubMedCrossRefGoogle Scholar
  172. 172.
    Kopitz J, von Reitzenstein C, Mühl C, Cantz M (1994) Role of plasma membrane ganglioside sialidase of human neuroblastoma cells in growth control and differentiation. Biochem Biophys Res Comm 199(3):1188–1193PubMedCrossRefGoogle Scholar
  173. 173.
    Kopitz J, Mühl C, Ehemann V, Lehmann C, Cantz M (1997) Effects of cell surface ganglioside sialidase inhibition on growth control and differentiation of human neuroblastoma cells. Eur J Cell Biol 73:1–7PubMedGoogle Scholar
  174. 174.
    Abad-Rodríguez J, Piddini E, Hasegawa T, Miyagi T, Dotti CG (2001) Plasma membrane ganglioside sialidase regulates axonal growth and regeneration in hippocampal neurons in culture. J Neurosci 21(21):8387–8395Google Scholar
  175. 175.
    Da Silva JS, Hasegawa T, Miyagi T, Dotti CG, Abad-Rodríguez J (2005) Asymmetric membrane ganglioside sialidase activity specifies axonal fate. Nat Neurosci 8(5):606–615. doi: 10.1038/nn1442 PubMedCrossRefGoogle Scholar
  176. 176.
    Abad-Rodríguez J, Robotti A (2007) Regulation of axonal development by plasma membrane gangliosides. J Neurochem 103(Suppl 1):47–55. doi: 10.1111/j.1471-4159.2007.04713.x PubMedCrossRefGoogle Scholar
  177. 177.
    Kappagantula S, Andrews MR, Cheah M, Abad-Rodríguez J, Dotti CG, Fawcett JW (2014) Neu3 sialidase-mediated ganglioside conversion is necessary for axon regeneration and is blocked in CNS axons. J Neurosci 34(7):2477–2492. doi: 10.1523/JNEUROSCI.4432-13.2014 PubMedCrossRefGoogle Scholar
  178. 178.
    Vyas AA, Blixt O, Paulson JC, Schnaar RL (2005) Potent glycan inhibitors of myelin-associated glycoprotein enhance axon outgrowth in vitro. J Biol Chem 280(16):16305–16310. doi: 10.1074/jbc.M500250200 PubMedPubMedCentralCrossRefGoogle Scholar
  179. 179.
    Quarles RH (2007) Myelin-associated glycoprotein (MAG): past, present and beyond. J Neurochem 100(6):1431–1448. doi: 10.1111/j.1471-4159.2006.04319.x PubMedGoogle Scholar
  180. 180.
    Minami A, Suzuki T (2012) Distribution of sialidase activity and the role of sialidase in the brain. Trends Glycosci Glycotechnol 24:112–121CrossRefGoogle Scholar
  181. 181.
    Ledeen RW, Wu G (2009) Neurobiology meets glycosciences. In: Gabius H-J (ed) The Sugar Code. Fundamentals of glycosciences, Wiley-VCH, Weinheim, Germany, pp 495–516Google Scholar
  182. 182.
    Wu G, Lu Z-H, André S, Gabius H-J, Ledeen RW (2016) Functional interplay between ganglioside GM1 and cross-linking galectin-1 induces axon-like neuritogenesis via integrin-based signaling and TRPC5-dependent Ca2+ influx. J Neurochem 136(3):550–563. doi:  10.1111/jnc.13418
  183. 183.
    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(18):11205–11211PubMedCrossRefGoogle Scholar
  184. 184.
    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(50):14762–14773PubMedCrossRefGoogle Scholar
  185. 185.
    André S, Kaltner H, Lensch M, Russwurm R, Siebert H-C, Fallsehr C, Tajkhorshid E, Heck AJR, von Knebel-Döberitz M, Gabius H-J, Kopitz J (2005) Determination of structural and functional overlap/divergence of five proto-type galectins by analysis of the growth-regulatory interaction with ganglioside GM1 in silico and in vitro on human neuroblastoma cells. Int J Cancer 114:46–57PubMedCrossRefGoogle Scholar
  186. 186.
    André S, Kaltner H, Manning JC, Murphy PV, Gabius H-J (2015) Lectins: getting familiar with translators of the sugar code. Molecules 20(2):1788–1823. doi: 10.3390/molecules20021788 PubMedCrossRefGoogle Scholar
  187. 187.
    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(11):5087–5091PubMedPubMedCentralCrossRefGoogle Scholar
  188. 188.
    Rusnati M, Urbinati C, Tanghetti E, Dell’Era P, Lortat-Jacob H, Presta M (2002) Cell membrane GM1 ganglioside is a functional coreceptor for fibroblast growth factor 2. Proc Natl Acad Sci USA 99(7):4367–4372. doi: 10.1073/pnas.072651899 PubMedPubMedCentralCrossRefGoogle Scholar
  189. 189.
    Prinetti A, Loberto N, Chigorno V, Sonnino S (2009) Glycosphingolipid behaviour in complex membranes. Biochim Biophys Acta 1788(1):184–193PubMedCrossRefGoogle Scholar
  190. 190.
    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(7):4036–4045PubMedCrossRefGoogle Scholar
  191. 191.
    Wu G, Lu ZH, Gabius H-J, Ledeen RW, Bleich D (2011) Ganglioside GM1 deficiency in effector T cells from NOD mice induces resistance to regulatory T cell suppression. Diabetes 60(9):2341–2349. doi: 10.2337/db10-1309 PubMedPubMedCentralCrossRefGoogle Scholar
  192. 192.
    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 N Y Acad Sci 1253:206–221. doi: 10.1111/j.1749-6632.2012.06479.x PubMedCrossRefGoogle Scholar
  193. 193.
    Kopitz J, Bergmann M, Gabius H-J (2010) How adhesion/growth-regulatory galectins-1 and -3 attain cell specificity: case study defining their target on neuroblastoma cells (SK-N-MC) and marked affinity regulation by affecting microdomain organization of the membrane. IUBMB Life 62(8):624–628. doi: 10.1002/iub.358 PubMedCrossRefGoogle Scholar
  194. 194.
    Majewski J, André S, Jones E, Chi E, Gabius H-J (2015) X-ray reflectivity and grazing incidence diffraction studies of interaction between huma adhesion/growth-regulatory galectin-1 and DPPE:GM1 lipid monolayer at the air/water interface. Biochemistry (Moscow) 80:943–956CrossRefGoogle Scholar
  195. 195.
    Hardy BJ (1997) The glycosidic linkage flexibility and time-scale similarity hypotheses. J Mol Struct 395–396:187–200CrossRefGoogle Scholar
  196. 196.
    He L, André S, Siebert H-C, Helmholz H, Niemeyer B, Gabius H-J (2003) Detection of ligand- and solvent-induced shape alterations of cell-growth-regulatory human lectin galectin-1 in solution by small angle neutron and X-ray scattering. Biophys J 85(1):511–524PubMedPubMedCentralCrossRefGoogle Scholar
  197. 197.
    Göhler A, André S, Kaltner H, Sauer M, Gabius H-J, Doose S (2010) Hydrodynamic properties of human adhesion/growth-regulatory galectins studied by fluorescence correlation spectroscopy. Biophys J 98(12):3044–3053PubMedPubMedCentralCrossRefGoogle Scholar
  198. 198.
    Diehl C, Genheden S, Modig K, Ryde U, Akke M (2009) Conformational entropy changes upon lactose binding to the carbohydrate recognition domain of galectin-3. J Biomol NMR 45(1–2):157–169PubMedCrossRefGoogle Scholar
  199. 199.
    Diehl C, Engstrom O, Delaine T, Hakansson M, Genheden S, Modig K, Leffler H, Ryde U, Nilsson UJ, Akke M (2010) Protein flexibility and conformational entropy in ligand design targeting the carbohydrate recognition domain of galectin-3. J Am Chem Soc 132(41):14577–14589. doi: 10.1021/ja105852y PubMedPubMedCentralCrossRefGoogle Scholar
  200. 200.
    Ruiz FM, Gilles U, Lindner I, André S, Romero A, Reusch D, Gabius H-J (2015) Combining crystallography and hydrogen-deuterium exchange to study galectin-ligand complexes. Chem Eur J 21(39):13558–13568. doi: 10.1002/chem.201501961 PubMedCrossRefGoogle Scholar
  201. 201.
    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(38):35917–35923PubMedCrossRefGoogle Scholar
  202. 202.
    Kopitz J, Ballikaya S, André S, Gabius H-J (2012) Ganglioside GM1/galectin-dependent growth regulation in human neuroblastoma cells: special properties of bivalent galectin-4 and significance of linker length for ligand selection. Neurochem Res 37(6):1267–1276. doi: 10.1007/s11064-011-0693-x PubMedCrossRefGoogle Scholar
  203. 203.
    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. doi: 10.1016/j.biochi.2014.05.010 PubMedCrossRefGoogle Scholar
  204. 204.
    Villalobo A, Nogales-Gonzáles A, Gabius H-J (2006) A guide to signaling pathways connecting protein-glycan interaction with the emerging versatile effector functionality of mammalian lectins. Trends Glycosci Glycotechnol 18(99):1–37CrossRefGoogle Scholar
  205. 205.
    Kasai K-i, Hirabayashi J (1996) Galectins: a family of animal lectins that decipher glycocodes. J Biochem 119:1–8PubMedCrossRefGoogle Scholar
  206. 206.
    Dahms NM, Hancock MK (2002) P-Type lectins. Biochim Biophys Acta 1572(2–3):317–340PubMedCrossRefGoogle Scholar
  207. 207.
    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, Germany, pp 329–346Google Scholar
  208. 208.
    Satoh T (2012) Molecular and structural basis for sugar recognition by mannose-6-phosphate receptor homology domain-containing lectins and proteins. Trends Glycosci Glycotechnol 24:193–202CrossRefGoogle Scholar
  209. 209.
    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(24):9055–9077. doi: 10.1021/ja403323y PubMedCrossRefGoogle Scholar
  210. 210.
    Zhang S, Moussodia R-O, Vértesy S, André S, Klein ML, Gabius H-J, Percec V (2015) Unraveling functional significance of natural variations of a human galectin by glycodendrimersomes with programmable glycan surface. Proc Natl Acad Sci USA 112(18):5585–5590. doi: 10.1073/pnas.1506220112 PubMedPubMedCentralCrossRefGoogle Scholar
  211. 211.
    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(13):4036–4040. doi: 10.1002/anie.201410882 CrossRefGoogle Scholar
  212. 212.
    Zhang S, Xiao Q, Sherman SE, Muncan A, Ramos Vicente AD, Wang Z, Hammer DA, Williams D, Chen Y, Pochan DJ, Vértesy S, André S, Klein ML, Gabius H-J, Percec V (2015) Glycodendrimersomes from sequence-defined Janus glycodendrimers reveal high activity and sensor capacity for the agglutination by natural variants of human lectins. J Am Chem Soc 137(41):13334–13344. doi: 10.1021/jacs.5b08844 PubMedCrossRefGoogle Scholar
  213. 213.
    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(7):199–210. doi: 10.1093/protein/gzv014 PubMedCrossRefGoogle Scholar
  214. 214.
    Kaltner H, Kübler D, López-Merino L, Lohr M, Manning JC, Lensch M, Seidler J, Lehmann WD, André S, Solís D, Gabius H-J (2011) Toward comprehensive analysis of the galectin network in chicken: unique diversity of galectin-3 and comparison of its localization profile in organs of adult animals to the other four members of this lectin family. Anat Rec 294(3):427–444. doi: 10.1002/ar.21341 CrossRefGoogle Scholar
  215. 215.
    Kaltner H, Singh T, Manning JC, Raschta AS, André S, Sinowatz F, Gabius H-J (2015) Network monitoring of adhesion/growth-regulatory galectins: localization of the ive canonical chicken proteins in embryonic and maturing bone and cartilage and their introduction as histochemical tools. Anat Rec 298(12):2051–2070. doi: 10.1002/ar.23265 CrossRefGoogle Scholar
  216. 216.
    Wang JL, Gray RM, Haudek KC, Patterson RJ (2004) Nucleocytoplasmic lectins. Biochim Biophys Acta 1673(1–2):75–93PubMedCrossRefGoogle Scholar
  217. 217.
    Smetana K Jr, André S, Kaltner H, Kopitz J, Gabius H-J (2013) Context-dependent multifunctionality of galectin-1: a challenge for defining the lectin as therapeutic target. Expert Opin Ther Targets 17(4):379–392. doi: 10.1517/14728222.2013.750651 PubMedCrossRefGoogle Scholar
  218. 218.
    Kozireski-Chuback D, Wu G, Ledeen RW (1999) Developmental appearance of nuclear GM1 in neurons of the central and peripheral nervous systems. Brain Res Dev Brain Res 115(2):201–208PubMedCrossRefGoogle Scholar
  219. 219.
    Ledeen RW, Wu G (2007) GM1 in the nuclear envelope regulates nuclear calcium through association with a nuclear sodium-calcium exchanger. J Neurochem 103(Suppl 1):126–134. doi: 10.1111/j.1471-4159.2007.04722.x PubMedCrossRefGoogle Scholar
  220. 220.
    Nowycky MC, Wu G, Ledeen RW (2014) Glycobiology of ion transport in the nervous system. Adv Neurobiol 9:321–342. doi: 10.1007/978-1-4939-1154-7_15 PubMedCrossRefGoogle Scholar
  221. 221.
    Schlötzer-Schrehardt U, André S, Janko C, Kaltner H, Kopitz J, Gabius H-J, Herrmann M (2012) Adhesion/growth-regulatory galectins in the human eye: localization profiles and tissue reactivities as a standard to detect disease-associated alterations. Graefes Arch Clin Exp Ophthalmol 250(8):1169–1180. doi: 10.1007/s00417-012-2021-9 PubMedCrossRefGoogle Scholar
  222. 222.
    Park JW, Voss PG, Grabski S, Wang JL, Patterson RJ (2001) Association of galectin-1 and galectin-3 with Gemin4 in complexes containing the SMN protein. Nucleic Acids Res 29(17):3595–3602PubMedPubMedCentralCrossRefGoogle Scholar
  223. 223.
    Purkrábková T, Smetana K Jr, Dvoránková B, Holíková Z, Böck C, Lensch M, André S, Pytlík R, Liu F-T, Klíma J, Smetana K, Motlik J, Gabius H-J (2003) New aspects of galectin functionality in nuclei of cultured bone marrow stromal and epidermal cells: biotinylated galectins as tool to detect specific binding sites. Biol Cell 95:535–545PubMedCrossRefGoogle Scholar
  224. 224.
    Haudek KC, Patterson RJ, Wang JL (2010) SR proteins and galectins: what’s in a name? Glycobiology 20(10):1199–1207. doi: 10.1093/glycob/cwq097 PubMedPubMedCentralCrossRefGoogle Scholar
  225. 225.
    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 95:269–277PubMedCrossRefGoogle Scholar
  226. 226.
    Solís D, Romero A, Kaltner H, Gabius H-J, Díaz-Mauriño T (1996) Different architecture of the combining sites of two chicken galectins revealed by chemical-mapping studies with synthetic ligand derivatives. J Biol Chem 271:12744–12748PubMedCrossRefGoogle Scholar
  227. 227.
    Wu AM, Singh T, Liu J-H, Krzeminski M, Russwurm R, Siebert H-C, Bonvin AMJJ, André S, Gabius H-J (2007) Activity-structure correlations in divergent lectin evolution: fine specificity of chicken galectin CG-14 and computational analysis of flexible ligand docking for CG-14 and the closely related CG-16. Glycobiology 17:165–184PubMedCrossRefGoogle Scholar
  228. 228.
    Rapoport EM, Matveeva VK, Kaltner H, André S, Vokhmyanina OA, Pazynina GV, Severov VV, Ryzhov IM, Korchagina EY, Belyanchikov IM, Gabius H-J, Bovin NV (2015) Comparative lectinology: delineating glycan-specificity profiles of the chicken galectins using neoglycoconjugates in a cell assay. Glycobiology 25(7):726–734. doi: 10.1093/glycob/cwv012 PubMedCrossRefGoogle Scholar
  229. 229.
    Lohr M, Kaltner H, Schwartz-Albiez R, Sinowatz F, Gabius H-J (2010) Towards functional glycomics by lectin histochemistry: strategic probe selection to monitor core and branch-end substitutions and detection of cell-type and regional selectivity in adult mouse testis and epididymis. Anat Histol Embryol 39(6):481–493PubMedCrossRefGoogle Scholar
  230. 230.
    Celie JW, Beelen RHJ, van den Born J (2005) Effect of fixation protocols on in situ detection of L-selectin ligands. J Immunol Methods 298(1–2):155–159. doi: 10.1016/j.jim.2005.01.009 PubMedCrossRefGoogle Scholar
  231. 231.
    Schwarz A, Futerman AH (1997) Determination of the localization of gangliosides using anti-ganglioside antibodies: comparison of fixation methods. J Histochem Cytochem 45(4):611–618PubMedCrossRefGoogle Scholar
  232. 232.
    Nagy N, Legendre H, Engels O, André S, Kaltner H, Wasano K, Zick Y, Pector J-C, Decaestecker C, Gabius H-J, Salmon I, Kiss R (2003) Refined prognostic evaluation in colon cancer using immunohistochemical galectin fingerprinting. Cancer 97:1849–1858PubMedCrossRefGoogle Scholar
  233. 233.
    Remmelink M, de Leval L, Decaestecker C, Duray A, Crompot E, Sirtaine N, André S, Kaltner H, Leroy X, Gabius H-J, Saussez S (2011) Quantitative immunohistochemical fingerprinting of adhesion/growth-regulatory galectins in salivary gland tumours: divergent profiles with diagnostic potential. Histopathology 58(4):543–556PubMedCrossRefGoogle Scholar
  234. 234.
    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(8):3053–3059PubMedGoogle Scholar
  235. 235.
    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(10):5429–5438PubMedGoogle Scholar
  236. 236.
    Rorive S, Belot N, Decaestecker C, Lefranc F, Gordower L, Micik S, Maurage C-A, Kaltner H, Ruchoux M-M, Danguy A, Gabius H-J, Salmon I, Kiss R, Camby I (2001) Galectin-1 is highly expressed in human gliomas with relevance for modulation of invasion of tumor astrocytes into the brain parenchyma. Glia 33(3):241–255PubMedCrossRefGoogle Scholar
  237. 237.
    Camby I, Belot N, Lefranc F, Sadeghi N, de Launoit Y, Kaltner H, Musette S, Darro F, Danguy A, Salmon I, Gabius H-J, Kiss R (2002) Galectin-1 modulates human glioblastoma cell migration into the brain through modifications to the actin cytoskeleton and levels of expression of small GTPases. J Neuropathol Exp Neurol 61(7):585–596PubMedCrossRefGoogle Scholar
  238. 238.
    Hann A, Gruner A, Chen Y, Gress TM, Buchholz M (2011) Comprehensive analysis of cellular galectin-3 reveals no consistent oncogenic function in pancreatic cancer cells. PLoS ONE 6(6):e20859. doi: 10.1371/journal.pone.0020859 PubMedPubMedCentralCrossRefGoogle Scholar
  239. 239.
    Plzák J, Betka J, Smetana K Jr, Chovanec M, Kaltner H, André S, Kodet R, Gabius H-J (2004) Galectin-3: an emerging prognostic indicator in advanced head and neck carcinoma. Eur J Cancer 40(15):2324–2330PubMedCrossRefGoogle Scholar
  240. 240.
    Yang RY, Hsu DK, Liu F-T (1996) Expression of galectin-3 modulates T-cell growth and apoptosis. Proc Natl Acad Sci USA 93:6737–6742PubMedPubMedCentralCrossRefGoogle Scholar
  241. 241.
    Akahani S, Nangia-Makker P, Inohara H, Kim H-RC, Raz A (1997) Galectin-3: a novel antiapoptotic molecule with a functional BH1 (NWGR) domain of Bcl-2 family. Cancer Res 57:5272–5276PubMedGoogle Scholar
  242. 242.
    Harazono Y, Kho DH, Balan V, Nakajima K, Zhang T, Hogan V, Raz A (2014) Galectin-3 leads to attenuation of apoptosis through Bax heterodimerization in human thyroid carcinoma cells. Oncotarget 5(20):9992–10001PubMedPubMedCentralCrossRefGoogle Scholar
  243. 243.
    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(4):373–388. doi: 10.1007/s00418-014-1234-x PubMedCrossRefGoogle Scholar
  244. 244.
    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 274:3233–3256PubMedCrossRefGoogle Scholar
  245. 245.
    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(21):4062–4080. doi: 10.1111/febs.12001 PubMedCrossRefGoogle Scholar
  246. 246.
    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(17):3552–3563PubMedCrossRefGoogle Scholar
  247. 247.
    Gitt MA, Colnot C, Poirier F, Nani KJ, Barondes SH, Leffler H (1998) Galectin-4 and galectin-6 are two closely related lectins expressed in mouse gastrointestinal tract. J Biol Chem 273:2954–2960PubMedCrossRefGoogle Scholar
  248. 248.
    Gitt MA, Xia YR, Atchison RE, Lusis AJ, Barondes SH, Leffler H (1998) Sequence, structure, and chromosomal mapping of the mouse Lgals6 gene, encoding galectin-6. J Biol Chem 273(5):2961–2970PubMedCrossRefGoogle Scholar
  249. 249.
    Houzelstein D, Goncalves IR, Orth A, Bonhomme F, Netter P (2008) Lgals6, a 2-million-year-old gene in mice: a case of positive Darwinian selection and presence/absence polymorphism. Genetics 178(3):1533–1545. doi: 10.1534/genetics.107.082792 PubMedPubMedCentralCrossRefGoogle Scholar
  250. 250.
    Gitt MA, Wiser MF, Leffler H, Herrmann J, Xia Y, Massa SM, Cooper DNW, Lusis AJ, Barondes SH (1995) Sequence and mapping of galectin-5, a β-galactoside-binding lectin, found in rat erythrocytes. J Biol Chem 270:5032–5038PubMedCrossRefGoogle Scholar
  251. 251.
    Wada J, Kanwar YS (1997) Identification and characterization of galectin-9, a novel β-galactoside-binding mammalian lectin. J Biol Chem 272(9):6078–6086PubMedCrossRefGoogle Scholar
  252. 252.
    Lensch M, Lohr M, Russwurm R, Vidal M, Kaltner H, André S, Gabius H-J (2006) Unique sequence and expression profiles of rat galectins-5 and -9 as a result of species-specific gene divergence. Int J Biochem Cell Biol 38(10):1741–1758PubMedCrossRefGoogle Scholar
  253. 253.
    Kaltner H, Raschta A-S, Manning JC, Gabius H-J (2013) 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 23(10):1152–1163. doi: 10.1093/glycob/cwt052 PubMedCrossRefGoogle Scholar
  254. 254.
    Suzuki N, Yamamoto K, Toyoshima S, Osawa T, Irimura T (1996) Molecular cloning and expression of cDNA encoding human macrophage C-type lectin. J Immunol 156:128–135PubMedGoogle Scholar
  255. 255.
    Tsuiji M, Fujimori M, Ohashi Y, Higashi N, Onami TM, Hedrick SM, Irimura T (2002) Molecular cloning and characterization of a novel mouse macrophage C-type lectin, mMGL2, which has a distinct carbohydrate specificity from mMGL1. J Biol Chem 277(32):28892–28901. doi: 10.1074/jbc.M203774200 PubMedCrossRefGoogle Scholar
  256. 256.
    Soilleux EJ, Barten R, Trowsdale J (2000) DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19p13. J Immunol 165(6):2937–2942PubMedCrossRefGoogle Scholar
  257. 257.
    Park CG, Takahara K, Umemoto E, Yashima Y, Matsubara K, Matsuda Y, Clausen BE, Inaba K, Steinman RM (2001) Five mouse homologues of the human dendritic cell C-type lectin. DC-SIGN. Int Immunol 13(10):1283–1290PubMedCrossRefGoogle Scholar
  258. 258.
    Bashirova AA, Wu L, Cheng J, Martin TD, Martin MP, Benveniste RE, Lifson JD, KewalRamani VN, Hughes A, Carrington M (2003) Novel member of the CD209 (DC-SIGN) gene family in primates. J Virol 77(1):217–227PubMedPubMedCentralCrossRefGoogle Scholar
  259. 259.
    Huang YW, Dryman BA, Li W, Meng XJ (2009) Porcine DC-SIGN: molecular cloning, gene structure, tissue distribution and binding characteristics. Dev Comp Immunol 33(4):464–480. doi: 10.1016/j.dci.2008.09.010 PubMedCrossRefGoogle Scholar
  260. 260.
    Huang YW, Meng XJ (2009) Identification of a porcine DC-SIGN-related C-type lectin, porcine CLEC4G (LSECtin), and its order of intron removal during splicing: comparative genomic analyses of the cluster of genes CD23/CLEC4G/DC-SIGN among mammalian species. Dev Comp Immunol 33(6):747–760. doi: 10.1016/j.dci.2008.12.007 PubMedCrossRefGoogle Scholar
  261. 261.
    Guo N, Mogues T, Weremowicz S, Morton CC, Sastry KN (1998) The human ortholog of rhesus mannose-binding protein-A gene is an expressed pseudogene that localizes to chromosome 10. Mamm Genome 9(3):246–249PubMedCrossRefGoogle Scholar
  262. 262.
    Bordet J, Gay FP (1906) Sur les relations des sensibilisatrices avec l’alexine. Ann Inst Pasteur 20:467–498Google Scholar
  263. 263.
    Gjerstorff M, Hansen S, Jensen B, Dueholm B, Horn P, Bendixen C, Holmskov U (2004) The genes encoding bovine SP-A, SP-D, MBL-A, conglutinin, CL-43 and CL-46 form a distinct collectin locus on Bos taurus chromosome 28 (BTA28) at position q.1.8-1.9. Anim Genet 35(4):333–337. doi: 10.1111/j.1365-2052.2004.01167.x PubMedCrossRefGoogle Scholar
  264. 264.
    Cao H, Crocker PR (2011) Evolution of CD33-related siglecs: regulating host immune functions and escaping pathogen exploitation? Immunology 132(1):18–26. doi: 10.1111/j.1365-2567.2010.03368.x PubMedPubMedCentralCrossRefGoogle Scholar
  265. 265.
    Martick M, Horan LH, Noller HF, Scott WG (2008) A discontinuous hammerhead ribozyme embedded in a mammalian messenger RNA. Nature 454(7206):899–902. doi: 10.1038/nature07117 PubMedPubMedCentralCrossRefGoogle Scholar
  266. 266.
    Talini G, Branciamore S, Gallori E (2011) Ribozymes: flexible molecular devices at work. Biochimie 93(11):1998–2005. doi: 10.1016/j.biochi.2011.06.026 PubMedCrossRefGoogle Scholar
  267. 267.
    Pál Z, Antal P, Srivastava SK, Hullám G, Semsei AF, Gál J, Svébis M, Soós G, Szalai C, André S, Gordeeva E, Nagy G, Kaltner H, Bovin NV, Molnár MJ, Falus A, Gabius H-J, Buzás EI (2012) Non-synonymous single nucleotide polymorphisms in genes for immunoregulatory galectins: association of galectin-8 (F19Y) occurrence with autoimmune diseases in a Caucasian population. Biochim Biophys Acta 1820:1512–1518. doi: 10.1016/j.bbagen.2012.05.015 PubMedCrossRefGoogle Scholar
  268. 268.
    Pineda B, Laporta P, Cano A, Garcia-Perez MA (2008) The Asn19Lys substitution in the osteoclast inhibitory lectin (OCIL) gene is associated with a reduction of bone mineral density in postmenopausal women. Calcif Tissue Int 82(5):348–353. doi: 10.1007/s00223-008-9135-4 PubMedCrossRefGoogle Scholar
  269. 269.
    Marakalala MJ, Kerrigan AM, Brown GD (2011) Dectin-1: a role in antifungal defense and consequences of genetic polymorphisms in humans. Mamm Genome 22(1–2):55–65. doi: 10.1007/s00335-010-9277-3 PubMedPubMedCentralCrossRefGoogle Scholar
  270. 270.
    Rooryck C, Diaz-Font A, Osborn DP, Chabchoub E, Hernandez-Hernandez V, Shamseldin H, Kenny J, Waters A, Jenkins D, Kaissi AA, Leal GF, Dallapiccola B, Carnevale F, Bitner-Glindzicz M, Lees M, Hennekam R, Stanier P, Burns AJ, Peeters H, Alkuraya FS, Beales PL (2011) Mutations in lectin complement pathway genes COLEC11 and MASP1 cause 3MC syndrome. Nat Genet 43(3):197–203. doi: 10.1038/ng.757 PubMedPubMedCentralCrossRefGoogle Scholar
  271. 271.
    Selman L, Hansen S (2012) Structure and function of collectin liver 1 (CL-L1) and collectin 11 (CL-11, CL-K1). Immunobiology 217(9):851–863. doi: 10.1016/j.imbio.2011.12.008 PubMedCrossRefGoogle Scholar
  272. 272.
    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, Garcia JV, Stuckey JA, Gabius H-J, Al-Hashimi HM, Markovitz DM (2015) Engineering a therapeutic lectin by uncoupling mitogenicity from antiviral activity. Cell 163(3):746–758. doi: 10.1016/j.cell.2015.09.056 PubMedCrossRefGoogle Scholar
  273. 273.
    Gabius H-J (2009) Animal and human lectins. In: Gabius H-J (ed) The Sugar Code. Fundamentals of glycosciences, Wiley-VCH, Weinheim, Germany, pp 317–328Google Scholar
  274. 274.
    Kaltner H, Solís D, Kopitz J, Lensch M, Lohr M, Manning JC, Mürnseer M, Schnölzer M, André S, Sáiz JL, Gabius H-J (2008) Prototype chicken galectins revisited: characterization of a third protein with distinctive hydrodynamic behaviour and expression pattern in organs of adult animals. Biochem J 409(2):591–599PubMedCrossRefGoogle Scholar
  275. 275.
    Kaltner H, Solís D, André S, Lensch M, Manning JC, Mürnseer M, Saíz JL, Gabius H-J (2009) Unique chicken tandem-repeat-type galectin: implications of alternative splicing and a distinct expression profile compared to those of the three proto-type proteins. Biochemistry 48(20):4403–4416PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing 2016

Authors and Affiliations

  • H.-J. Gabius
    • 1
    Email author
  • J. C. Manning
    • 1
  • J. Kopitz
    • 2
  • S. André
    • 1
  • H. Kaltner
    • 1
  1. 1.Institute of Physiological Chemistry, Faculty of Veterinary MedicineLudwig-Maximilians-University MunichMunichGermany
  2. 2.Institute of Pathology, Department of Applied Tumor BiologyRuprecht-Karls-University HeidelbergHeidelbergGermany

Personalised recommendations