Skip to main content
SpringerLink
Log in

Human tandem-repeat-type galectins bind bacterial non-βGal polysaccharides

  • Glycoarray Section
  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Galectins are multifunctional effectors, for example acting as regulators of cell growth via protein-glycan interactions. The observation of capacity to kill bacteria for two tandem-repeat-type galectins, which target histo-blood epitopes toward this end (Stowell et al. Nat. Med. 16:295–301, 2010), prompted us to establish an array with bacterial polysaccharides. We addressed the question whether sugar determinants other than β-galactosides may be docking sites, using human galectins-4, -8, and -9. Positive controls with histo-blood group ABH-epitopes and the E. coli 086 polysaccharide ascertained the suitability of the set-up. Significant signal generation, depending on type of galectin and polysacchride, was obtained. Presence of cognate β-galactoside-related epitopes within a polysaccharide chain or its branch will not automatically establish binding properties, and structural constellations lacking galactosides, like rhamnan, were found to be active. These data establish the array as valuable screening tool, giving direction to further functional and structural studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

BSA:

Bovine serum albumin

CRD:

Carbohydrate recognition domain

PS:

Polysaccharide

RFU:

Relative Fluorescence Units

References

  1. Gabius, H.-J. (ed.): The Sugar Code. Fundamentals of glycosciences. Wiley-VCH, Weinheim (2009)

    Google Scholar 

  2. 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. 36, 298–313 (2011)

    Article  CAS  PubMed  Google Scholar 

  3. Cambi, A., Koopman, M., Figdor, C.G.: How C-type lectins detect pathogens. Cell. Microbiol. 7, 481–488 (2005)

    Article  CAS  PubMed  Google Scholar 

  4. Vasta, G.R.: Roles of galectins in infection. Nat. Rev. Microbiol. 7, 424–438 (2009)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Mey, A., Leffler, H., Hmama, Z., Normier, G., Revillard, J.-P.: The animal lectin galectin-3 interacts with bacterial lipopolysaccharides via two independent sites. J. Immunol. 156, 1572–1577 (1996)

    CAS  PubMed  Google Scholar 

  6. Kohatsu, L., Hsu, D.K., Jegalian, A.G., Liu, F.-T., Baum, L.G.: Galectin-3 induces death of Candida species expressing specific β1,2-linked mannans. J. Immunol. 177, 4718–4726 (2006)

    CAS  PubMed  Google Scholar 

  7. Cooper, D.N.W.: Galectinomics: finding themes in complexity. Biochim. Biophys. Acta 1572, 209–231 (2002)

    Article  CAS  PubMed  Google Scholar 

  8. Kaltner, H., Gabius, H.-J.: A toolbox of lectins for translating the sugar code: the galectin network in phylogenesis and tumors. Histol. Histopathol. 27, 397–416 (2012)

    CAS  PubMed  Google Scholar 

  9. Stowell, S.R., Arthur, C.M., Dias-Baruffi, M., Rodrigues, L.C., Gourdine, J.P., Heimburg-Molinaro, J., Ju, T., Molinaro, R.J., Rivera-Marrero, C., Xia, B., Smith, D.F., Cummings, R.D.: Innate immune lectins kill bacteria expressing blood group antigen. Nat. Med. 16, 295–301 (2010)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Herget, S., Toukach, P.V., Ranzinger, R., Hull, W.E., Knirel, Y.A., von der Lieth, C.-W.: Statistical analysis of the Bacterial Carbohydrate Structure Data Base (BCSDB): characteristics and diversity of bacterial carbohydrates in comparison with mammalian glycans. BMC Struct. Biol. 8, 35 (2008)

    Article  PubMed Central  PubMed  Google Scholar 

  11. Oda, Y., Herrmann, J., Gitt, M.A., Turck, C.W., Burlingame, A.L., Barondes, S.H., Leffler, H.: Soluble lactose-binding lectin from rat intestine with two different carbohydrate-binding domains in the same peptide chain. J. Biol. Chem. 268, 5929–5939 (1993)

    CAS  PubMed  Google Scholar 

  12. Hirabayashi, J., Hashidate, T., Arata, Y., Nishi, N., Nakamura, T., Hirashima, M., Urashima, T., Oka, T., Futai, M., Müller, W.E.G., Yagi, F., Kasai, K.-i.: Oligosaccharide specificity of galectins: a search by frontal affinity chromatography. Biochim. Biophys. Acta 1572, 232–254 (2002)

    Article  CAS  PubMed  Google Scholar 

  13. Wu, A.M., Wu, J.H., Liu, J.-H., Singh, T., André, S., Kaltner, H., Gabius, H.-J.: 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 86, 317–326 (2004)

    Article  CAS  PubMed  Google Scholar 

  14. Ideo, H., Seko, A., Yamashita, K.: Galectin-4 binds to sulfated glycosphingolipids and carcinoembryonic antigen in patches on the cell surface of human colon adenocarcinoma cells. J. Biol. Chem. 280, 4730–4737 (2005)

    Article  CAS  PubMed  Google Scholar 

  15. Stowell, S.R., Arthur, C.M., Slanina, K.A., Horton, J.R., Smith, D.F., Cummings, R.D.: Dimeric Galectin-8 induces phosphatidylserine exposure in leukocytes through polylactosamine recognition by the C-terminal domain. J. Biol. Chem. 283, 20547–20559 (2008)

    Article  CAS  PubMed  Google Scholar 

  16. Rapoport, E.M., André, S., Kurmyshkina, O.V., Pochechueva, T.V., Severov, V.V., Pazynina, G.V., Gabius, H.-J., Bovin, N.V.: Galectin-loaded cells as a platform for the profiling of lectin specificity by fluorescent neoglycoconjugates: a case study on galectins-1 and -3 and the impact of assay setting. Glycobiology 18, 315–324 (2008)

    Article  CAS  PubMed  Google Scholar 

  17. Vokhmyanina, O.A., Rapoport, E.M., André, S., Severov, V.V., Ryzhov, I., Pazynina, G.V., Korchagina, E., Gabius, H.-J., Bovin, N.V.: Comparative study of the glycan specificities of cell-bound human tandem-repeat-type galectin-4, -8 and -9. Glycobiology 22, 1207–1217 (2012)

    Article  CAS  PubMed  Google Scholar 

  18. Vokhmyanina, O.A., Rapoport, E.M., Ryzhov, I.M., Korchagina, E.Y., Pazynina, G.V., Severov, V.V., Kaltner, H., André, S., Gabius, H.-J., Bovin, N.V.: Carbohydrate specificity of chicken and human tandem-repeat-type galectins-8 in composition of cells. Biochem. Mosc. 76, 1185–1192 (2011)

    Article  CAS  Google Scholar 

  19. Krzeminski, M., Singh, T., André, S., Lensch, M., Wu, A.M., Bonvin, A.M.J.J., Gabius, H.-J.: 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 1810, 150–161 (2011)

    Article  CAS  PubMed  Google Scholar 

  20. Murphy, P.V., André, S., Gabius, H.-J.: The third dimension of reading the sugar code by lectins: design of glycoclusters with cyclic scaffolds as tools with the aim to define correlations between spatial presentation and activity. Molecules 18, 4026–4053 (2013)

    Article  CAS  PubMed  Google Scholar 

  21. Huflejt, M.E., Vuskovic, M., Vasiliu, D., Xu, H., Obukhova, P., Shilova, N., Tuzikov, A., Galanina, O., Arun, B., Lu, K., Bovin, N.: Anti-carbohydrate antibodies of normal sera: findings, surprises and challenges. Mol. Immunol. 46, 3037–3049 (2009)

    Article  CAS  PubMed  Google Scholar 

  22. Gabius, H.-J.: Influence of type of linkage and spacer on the interaction of β-galactoside-binding proteins with immobilized affinity ligands. Anal. Biochem. 189, 91–94 (1990)

    Article  CAS  PubMed  Google Scholar 

  23. Pál, Z., Antal, P., Srivastava, S.K., Hullám, G., Semsei, A.F., Gál, J., Svébis, M., Soós, G., Szalai, C., André, S., Gordeeva, E., Nagy, G., Kaltner, H., Bovin, N.V., Molnár, M.J., Falus, A., Gabius, H.-J., Buzás, E.I.: 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 (2012)

    Article  PubMed  Google Scholar 

  24. 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 95, 269–277 (1991)

    Article  CAS  PubMed  Google Scholar 

  25. André, S., Jarikote, D.V., Yan, D., Vincenz, L., Wang, G.N., Kaltner, H., Murphy, P.V., Gabius, H.-J.: Synthesis of bivalent lactosides and their activity as sensors for differences between lectins in inter- and intrafamily comparisons. Bioorg. Med. Chem. Lett. 22, 313–318 (2012)

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  27. Westphal, O., Jann, K.: Bacterial lipopolysaccharides. Extraction with phenol-water and further applications of the procedure. Methods Carbohydr. Chem. 5, 83–91 (1965)

    CAS  Google Scholar 

  28. Arbatsky, N.P., Wang, M., Shashkov, A.S., Chizhov, A.O., Feng, L., Knirel, Y.A., Wang, L.: Structure of the O-polysaccharide of Cronobacter sakazakii O2 with a randomly O-acetylated l-rhamnose residue. Carbohydr. Res. 345, 2090–2094 (2010)

    Article  CAS  PubMed  Google Scholar 

  29. Blixt, O., Head, S., Mondala, T., Scanlan, C., Huflejt, M.E., Alvarez, R., Bryan, M.C., Fazio, F., Calarese, D., Stevens, J., Razi, N., Stevens, D.J., Skehel, J.J., van Die, I., Burton, D.R., Wilson, I.A., Cummings, R., Bovin, N., Wong, C.H., Paulson, J.C.: Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc. Natl. Acad. Sci. U. S. A. 101, 17033–17038 (2004)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Habermann, F.A., André, S., Kaltner, H., Kübler, D., Sinowatz, F., Gabius, H.-J.: Galectins as tools for glycan mapping in histology: comparison of their binding profiles to the bovine zona pellucida by confocal laser scanning microscopy. Histochem. Cell Biol. 135, 539–552 (2011)

    Article  CAS  PubMed  Google Scholar 

  31. Schlötzer-Schrehardt, U., Andre, S., Janko, C., Kaltner, H., Kopitz, J., Gabius, H.J., Herrmann, M.: 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, 1169–1180 (2012)

    Article  PubMed  Google Scholar 

  32. Monsigny, M., Kieda, C., Roche, A.-C.: Membrane glycoproteins glycolipids and membrane lectins as recognition signals in normal and malignant cells. Biol. Cell 47, 95–110 (1983)

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the RAS Presidium Program “Molecular and cell biology” and RFBR grants #1304-00096 and 13-04-00549 as well as EC FP7 funding (GlycoHIT, contract no. 260600; ITN GLYCOPHARM, contract no. 317297). EC FP7 GlycoBioM (no. 259869)

Author information

Authors and Affiliations

  1. N. D. Zelinsky Institute of Organic Chemistry, Russian Academy of Sciences, Leninsky prosp., 47, Moscow, 119991, Russian Federation

    Yu. A. Knirel

  2. Institute of Physiological Chemistry, Faculty of Veterinary Medicine, Ludwig Maximilians University, Veterinarstr. 13, 80539, Munich, Germany

    H.-J. Gabius

  3. Department of Chemistry, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, DK-1871, Copenhagen, Denmark

    O. Blixt

  4. Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Miklukho-Maklaya 16/10, 117997, Moscow, Russia

    E. M. Rapoport, N. R. Khasbiullina, N. V. Shilova & N. V. Bovin

Authors
  1. Yu. A. Knirel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H.-J. Gabius
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. Blixt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. M. Rapoport
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. R. Khasbiullina
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. N. V. Shilova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. N. V. Bovin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. V. Bovin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Knirel, Y.A., Gabius, HJ., Blixt, O. et al. Human tandem-repeat-type galectins bind bacterial non-βGal polysaccharides. Glycoconj J 31, 7–12 (2014). https://doi.org/10.1007/s10719-013-9497-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-013-9497-3

Keywords

Search

Navigation