Abstract
Polyacrylamide conjugates of glycans have long been widely used in many research areas of glycobiology, mainly for immobilizing glycans in solid-phase assays and as multivalent inhibitors. Pending biotin tag allows immobilizing Glyc-PAA quantitatively on any surface, and acts as a tracer for detection of carbohydrate-binding proteins. However, the scope of already realized capabilities of these probes is immeasurably richer than those listed above. This review is not so much about routine as about less common, but not less significant applications. Also, the data on the glycopolymers themselves, their molecular weight, size and polymer chain flexibility are presented, as well as the methods of synthesis, clusterisation and entropy factor in their interaction with proteins.
Similar content being viewed by others
Abbreviations
- 6’SLN:
-
Neu5Acα2-6Galβ1-4GlcNAc
- biot:
-
Biotin residue
- BSA:
-
Bovine serum albumin
- DOPE:
-
Dioleoylphosphatidyl ethanolamine
- ELISA:
-
Enzyme-linked immunosorbent assay
- Fluo:
-
Fluorescein residue
- Glyc:
-
Carbohydrate residue, usually spacer (sp) armed
- HRP:
-
Horse-radish peroxidase
- mol%:
-
Molar percent
- NHS:
-
N-hydroxysuccinimide
- PAA:
-
Polyacrylamide
- PGA:
-
Printed glycan array
- TF:
-
Thomsen-Friedenreich antigen
References
Hořoejší, V., Chaloupecká, O., Kocourek, J.: Studies on lectins: XLIII. Isolation and characterization of the lectin from restharrow boots (Ononis hircine Jacq.). Biochim Blophys Acta. 538, 293–298 (1978)
Kocourek, J.: Synthetic glycosyl polymers in isolation, characterization and immobilization of lectins. Acta Histochem. 71, 57–66 (1982)
Chernyak, A.Y., Levinsky, A.B., Dmitriev, B.A., Kochetkov, N.K.: A new type of carbohydrate-containing synthetic antigen: synthesis of carbohydrate-containing polyacrylamide copolymers having the specificity of O:3 and O:4 factors of Salmonella. Carbohydr. Res. 28, 269–282 (1984)
Bovin, N.V.: Synthesis of blood group related oligosaccharides H, A, and Lea, and their immobilisation on polymeric matrix, PhD Thesis, Institute of Bioorganic Chemistry, Moscow (1982)
Bovin, N.V., Korchagina, E.Y., Zemlyanukhina, T.V., Byramova, N.E., Galanina, O.E., Zemlyakov, A.E., Ivanov, A.E., Zubov, V.P., Mochalova, L.V.: Synthesis of polymeric neoglycoconjugates based on N-substituted polyacrylamide. Glycoconj. J. 10, 142–151 (1993)
Mammen, M., Dahmann, G., Whitesides, G.M.: Effective inhibitors of hemagglutination by influenza virus synthesized from polymers having active ester groups. Insight into mechanism of inhibition. J. Med. Chem. 38, 4179–4190 (1995)
Bovin, N.V.: Polyacrylamide-based neoglycoconjugates as tools in glycobiology. Glycoconj. J. 15, 431–446 (1998)
Bovin, N.V.: Sugar-polyacrylamide conjugates as probes for cell lectins. In: Gabius, H.-J., Gabius, S. (eds.) Lectins and Glycobiology, pp. 23–30. Springer-Verlag, Berlin (1993)
Bovin, N.V.: Neoglycoconjugates: trade and art. In: Drickamer, K., Dell, A. (eds.) Glycogenomics: the Impact of Genomics and Informatics on Glycobiology, Biochem. Soc. Symp. № 69, pp. 143–160. Cambridge, Portland Press (2002)
Bovin, N.V.: Neoglycoconjugates as probes in glycobiology. In: Schneider, M.P. (ed.) Chemical Probes in Biology, pp. 207–225. Kluwer, the Netherlands (2003)
Lopes, A., Breiman, A., Lora, M., Le Moullac-Vaidye, B., Galanina, O., Nyström, K., Marchandeau, S., Le Gall-Reculé, G., Strive, T., Neimanis, A., Bovin, N., Ruvoën-Clouet, N., Esteves, P., Abrantes, J., Le Pendu, J.: Host specific glycans are correlated with susceptibility to infection by lagoviruses, but not with their virulence. J. Virology. 92, e01759–e01717 (2017). https://doi.org/10.1128/JVI.01759-17
Meichenin, A.M., Rocher, J., Galanina, O., Bovin, N., Nifant’ev, N., Sherman, A., Cassagnau, E., Heymann, M.F., Bara, J., Fraser, R.H., Le Pendu, J.: Tk, a new colon tumor-associated antigen resulting from altered O-glycosylation. Cancer Res. 60, 5499–5507 (2000)
Khraltsova, L.S., Sablina, M.A., Melikhova, T.D., Joziasse, D.H., Kaltner, H., Gabius, H.-J., Bovin, N.V.: An enzyme-linked lectin assay for α1,3-galactosyltransferase. Anal. Biochem. 280, 250–257 (2000)
Pochechueva, T.V., Ushakova, N.A., Preobrazhenskaya, M.E., Nifantiev, N.E., Tsvetkov, Y.E., Sablina, M.A., Tuzikov, A.B., Bird, M.I., Rieben, R., Bovin, N.V.: P-selectin blocking potency of multimeric tyrosine sulfates in vitro and in vivo. Bioorgan. Med. Chem. Lett. 13, 1709–1712 (2003)
Obukhova, P., Tsygankova, S., Chinarev, A., Shilova, N., Nokel, A., Kosma, P., Bovin, N.: Are there specific antibodies against Neu5Gc epitopes in the blood of healthy individuals? Glycobiology. 30, 395–406 (2020). https://doi.org/10.1093/glycob/cwz107
Weitz-Schmidt, G., Stokmaier, D., Scheel, G., Nifant'ev, N.E., Tuzikov, A.B., Bovin, N.V.: An E-selectin binding assay based on polyacrylamide-type glycoconjugates. Anal. Biochem. 238, 184–190 (1996)
Gabius, H.-J., Gabius, S., Zemlyanukhina, T.V., Bovin, N.V., Brinck, U., Danguy, A., Joshi, S.S., Kayser, K., Schottelius, J., Sinowatz, F., Tietze, L.F., Vidal-Vanaclocha, F., Zanetta, J.-P.: Reverse lectin histochemistry: design and application of glycoligands for detection of cell and tissue lectins. Histol. Histopathol. 8, 369–383 (1993)
Rapoport, E.M., Moiseeva, E.V., Aronov, D.A., Khaidukov, S.V., Pazynina, G.V., Tsygankova, S.V., Ryzhov, I.M., Belyanchikov, I.M., Tyrtysh, T.V., McCullough, K.C., Bovin, N.V.: Glycan-binding profile of DC-like cells. Glycoconj. J. 37, 129–138 (2020). https://doi.org/10.1007/s10719-019-09897-9
Chinarev, A.A., Galanina, O.E., Bovin, N.V.: Biotinylated multivalent glycoconjugates for surface coating. Methods Mol. Biol. 600, 67–78 (2010)
Navakouski, M., Shilova, N., Khasbiullina, N., Feofanov, A., Pudova, E., Chen, K., Blixt, O., Bovin, N.: Improved spot morphology for printed glycan arrays. BioTechniques. 64, 110–116 (2018). https://doi.org/10.4155/btn-2017-0111
Matrosovich, M.N., Gambaryan, A.S.: Solid-phase assays of receptor-binding specificity. Methods Mol. Biol. 865, 71–94 (2012). https://doi.org/10.1007/978-1-61779-621-0_5
Rye, P.D., Bovin, N.V.: Selection of carbohydrate-binding cell phenotypes using oligosaccharide-coated magnetic particles. Glycobiology. 7, 179–182 (1997)
Bovin N.V.: unpublished results
Kurmyshkina, O., Rapoport, E., Moiseeva, E., Korchagina, E., Ovchinnikova, T., Pazynina, G., Belyanchikov, I., Bovin, N.: Glycoprobes as a tool for the study of lectins expressed on tumor cells. Acta Histochem. 112, 118–126 (2010)
Rapoport, E.M., Khaidukov, S.V., Gaponov, A.M., Pazynina, G.V., Tsygankova, S.V., Ryzhov, I.M., Belyanchikov, I.M., Milona, P., Bovin, N.V., McCullough, K.C.: Glycan recognition by human blood mononuclear cells with an emphasis on dendritic cells. Glycoconj. J. 35, 191–203 (2018). https://doi.org/10.1007/s10719-017-9811-6
Galanina, O., Feofanov, A., Tuzikov, A.B., Rapoport, E., Crocker, P.R., Grichine, A., Egret-Charlier, M., Vigny, P., Le Pendu, J., Bovin, N.V.: Fluorescent carbohydrate probes for cell lectins. Spectrochim. Acta A. 57, 2285–2296 (2001)
Galanina, O.E., Tuzikov, A.B., Rapoport, E.M., Le Pendu, J., Bovin, N.V.: Carbohydrate-based probes for detection of cellular lectins. Anal. Biochem. 265, 282–289 (1998)
Dutta, S., Aoki, K., Doungkamchan, K., Tiemeyer, M., Bovin, N.V., Miller, D.J.: Sulfated Lewis a trisaccharide on oviduct membrane glycoproteins binds bovine sperm and lengthens sperm lifespan. J. Biol. Chem. 294, 13445–13463 (2019). https://doi.org/10.1074/jbc.RA119.007695
Silva,E., Frost, D., Li, L., Bovin, N., Miller, D.J.: Lactadherin is a candidate oviduct Lewis X trisaccharide receptor on porcine spermatozoa. Andrology 5, 589–597 (2017). https://doi.org/10.1111/andr.12340
Dobrochaeva, K.L., Khasbiullina, N.R., Shilova, N.V., Knirel, Y.A., Nokel, A.Y., Bovin, N.V.: Human antibodies eluted from ligand free Sepharose capable of binding bacterial polysaccharides and sulfated glycans. Molec. Immunol. 106, 63–68 (2019). https://doi.org/10.1016/j.molimm.2018.12.011
Gerber, B., Tinguely, C., Bovin, N.V., Rieben, R., Carrel, T., Nydegger, U.E.: Differences between synthetic oligosaccharide immunoabsorbents in depletion capacity for xenoreactive anti-Galα1-3Gal antibodies from human serum. Xenotransplantation. 8, 106–114 (2001)
Shilova, N.V., Galanina, O.E., Pochechueva, T.V., Chinarev, A.A., Kadykov, V.A., Tuzikov, A.B., Bovin, N.V.: High molecular weight neoglycoconjugates for solid phase assays. Glycoconj. J. 22, 43–51 (2005)
Gordeeva, E.A., Tuzikov, A.B., Galanina, O.E., Pochechueva, T.V., Bovin, N.V.: Microscale synthesis of glycoconjugate series and libraries. Anal. Biochem. 278, 230–232 (2000)
Alikhani, A., Korchagina, E.Y., Chinarev, A.A., Bovin, N.V., Federspiel, W.J.: High molecular weight blood group a trisaccharide-polyacrylamide glycoconjugates as synthetic blood group a antigens for anti-a antibody removal devices. J Biomed Mater Res B Appl Biomater. 91, 845–854 (2009)
Collins, B.E., Blixt, O., Bovin, N.V., Danzer, C.-P., Chui, D., Marth, J.D., Nitschke, L., Paulson, J.C.: Constitutively unmasked CD22 on B cells of ST6Gal I knock-out mice: novel sialoside probes for murine CD22. Glycobiology. 12, 563–571 (2002)
Collins, B.E., Blixt, O., Han, S., Duong, B., Li, H., Nathan, J.K., Bovin, N., Paulson, J.C.: High-affinity ligand probes of CD22 overcome the threshold set by cis ligands to allow for binding, endocytosis, and killing of B cells. J. Immunol. 77, 2994–3003 (2006)
Duong, B.H., Tian, H., Ota, T., Completo, G., Han, S., Vela, J.L., Ota, M., Kubitz, M., Bovin, N., Paulson, J., Nemazee, D.: Decoration of T-independent antigen with ligands for CD22 and siglec-G can suppress immunity and induce B cell tolerance in vivo. J. Exp. Med. 207, 173–187 (2010)
Pochechueva, T., Chinarev, A., Spengler, M., Korchagina, E., Heinzelmann-Schwarz, V., Bovin, N., Rieben, R.: Multiplex suspension array for human anti-carbohydrate antibody profiling. Analyst. 136, 560–569 (2011). https://doi.org/10.1039/c0an00758g
Pochechueva, T., Chinarev, A., Schötzau, A., Fedier, A., Bovin, N.V., Hacker, N.F., Jacob, F., Heinzelmann-Schwarz, V.: Blood plasma-derived anti-glycan antibodies to sialylated and sulfated glycans identify ovarian cancer patients. PLoS One. 11(10), e0164230 (2016). https://doi.org/10.1371/journal.pone.0164230
Galanina, O.E., Mecklenburg, M., Nifantiev, N.E., Pazynina, G.V., Bovin, N.V.: GlycoChip: multiarray for the study of carbohydrate-binding proteins. Lab Chip. 3, 260–265 (2003)
Rye, P.D., Bovin, N.V.: Carbohydrate affinity PAGE for the study of carbohydrate-binding proteins. BioTechniques. 25, 146–151 (1998)
Dyukova, V.I., Dementieva, E.I., Zubtsov, D.A., Galanina, O.E., Bovin, N.V., Rubina, A.Y.: Hydrogel glycan microarrays. Anal. Biochem. 347, 94–105 (2005)
Dobrochaeva, K., Khasbiullina, N., Shilova, N., Antipova, N., Obukhova, P., Galanina, O., Blixt, O., Kunz, H., Filatov, A., Knirel, Y., LePendu, J., Khaidukov, S., Bovin, N.: Specificity of human natural antibodies referred to as anti-Tn. Mol. Immunol. 120, 74–82 (2020). https://doi.org/10.1016/j.molimm.2020.02.005
Blixt, O., Lavrova, O.I., Mazurov, D.V., Clo, E., Kracun, S.K., Bovin, N.V., Filatov, A.V.: Analysis of Tn-antigenicity with a panel of new IgM and IgG1 monoclonal antibodies raised against leukemic cells. Glycobiology. 22, 529–542 (2011)
Flechner, A., Butschak, G., Löffler, A., Rühmann, J., Nishimura, S.-I., Dölling, R., Purfürst, B., Goletz, S., Danielczyk, A., Karsten, U.: Cluster binding studies with two anti-Thomsen-Friedenreich (anti-core-1, CD176) antibodies: evidence for a quadruple epitope. Int. Immunopharmacol. 72, 186–194 (2019). https://doi.org/10.1016/j.intimp.2019.03.058
Kitov, P.I., Paszkiewicz, E., Sadowska, J.M., Deng, Z., Ahmed, M., Narain, R., Griener, T.P., Mulvey, G.L., Armstrong, G.D., Bundle, D.R.: Impact of the nature and size of the polymeric backbone on the ability of heterobifunctional ligands to mediate Shiga toxin and serum amyloid p component ternary complex formation. Toxins (Basel). 3, 1065–1088 (2011). https://doi.org/10.3390/toxins3091065
Tuzikov, A.B., Chinarev, A.A., Gambaryan, A.S., Oleinikov, V.A., Klinov, D.V., Matsko, N.B., Kadykov, V.A., Ermishov, M.A., Demin, I.V., Demin, V.V., Rye, P.D., Bovin, N.V.: Polyglycine II nanosheets: Supramolecular antivirals? ChemBioChem. 4, 147–154 (2003)
Gorokhova, I.V., Chinarev, A.A., Tuzikov, A.B., Tsygankova, S.V., Bovin, N.V.: Spontaneous and promoted association of linear oligoglycines. Rus. J. Bioorgan. Chem. 32, 420–428 (2006)
Kovalenko, E.I., Sablina, M.A., Khaidukov, S.V., Khirova, E.V., Bovin, N.V.: The incorporation of neoglycolipids into K562 cells. A model for the study of carbohydrate-dependent cytolysis of target cells by natural killer (NK) cells. Rus. J. Bioorgan. Chem. 24, 200–203 (1998)
Rapoport, E.M., Kovalenko, E.I., Belyanchikov, I.M., Bovin, N.V.: Probing cell surface lectins with neoglycoconjugates. In: Nilsson, B. (ed.) Lectins. Analytical Technologies, pp. 397–414. Elsevier, Amsterdam (2007)
Pochechueva, T.V., Galanina, O.E., Bird, M.I., Nifantiev, N.E., Bovin, N.V.: Assembly of P-selectin ligands on a polymeric template. Chem. Biol. 9, 1–20 (2002)
Choi, S.-K., Mammen, M., Whitesides, G.: Generation and in situ evaluation of libraries of poly(acrylic acid) presenting sialosides as side chains as polyvalent inhibitors of influenza-mediated hemagglutination. J. Am. Chem. Soc. 119, 4103–4111 (1997). https://doi.org/10.1021/ja963519x
Tran, H.A., Kitov, P.I., Paszkiewicz, T., Sadowska, J.M., Bundle, D.R.: Multifunctional multivalency: a focused library of polymeric cholera toxin antagonists. Org. Biomol. Chem. 9, 3658–3671 (2011). https://doi.org/10.1039/c0ob01089h
Game, S.M., Rajapurohit, P.K., Clifford, M., Bird, M.I., Priest, R., Bovin, N.V., Nifant’ev, N.E., O’Beirne, G., Cook, N.D.: Scintillation proximity assay for E-, P-, and L-selectin utilizing polyacrylamide-based neoglycoconjugates as ligands. Anal. Biochem. 258, 127–135 (1998)
Galanina, O.E., Chinarev, A.A., Shilova, N.V., Sablina, M.A., Bovin, N.V.: Immobilization of polyacrylamide-based glycoconjugates on solid phase in immunosorbent assays. Methods Mol. Biol. 808, 167–182 (2012)
Gambaryan, A.S., Tuzikov, A.B., Piskarev, V.E., Yamnikova, S.S., Lvov, D.K., Robertson, J.S., Bovin, N.V., Matrosovich, M.N.: Specification of receptor-binding phenotypes of influenza virus isolates from different hosts using synthetic sialylglycopolymers: non-egg-adapted human H1 and H3 influenza a and influenza B viruses share a common high binding affinity for 6′-sialyl(N-acetyllactosamine). Virology. 232, 345–350 (1997)
Matrosovich, M., Tuzikov, A., Bovin, N., Gambaryan, A., Klimov, A., Cox, N., Castrucci, M., Donatelli, I., Kawaoka, Y.: Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J. Virol. 74, 8502–8512 (2000)
Gambaryan, A.S., Karasin, A.I., Tuzikov, A.B., Chinarev, A.A., Pazynina, G.V., Bovin, N.V., Olsen, C.W., Klimov, A.I.: Receptor-binding properties of swine influenza viruses isolated and propagated in MDCK cells. Virus Res. 114, 15–22 (2005)
Gambaryan, A.S., Tuzikov, A.B., Pazynina, G.V., Webster, R.G., Matrosovich, M.N., Bovin, N.V.: H5N1 chicken influenza viruses display a high binding affinity for Neu5Acalpha2-3Galbeta1-4(6-HSO(3))GlcNAc-containing receptors. Virology. 326, 310–316 (2004)
Gambaryan, A., Yamnikova, S., Lvov, D., Tuzikov, A., Chinarev, A., Pazynina, G., Webster, R., Matrosovich, M., Bovin, N.: Receptor specificity of influenza viruses from birds and mammals: new data on involvement of the inner fragments of the carbohydrate chain. Virology. 334, 276–283 (2005)
Gambaryan, A.S., Tuzikov, A.B., Pazynina, G.V., Desheva, J.A., Bovin, N.V., Matrosovich, M.N., Klimov, A.I.: 6-sulfo sialyl Lewis X is the common receptor determinant recognized by H5, H6, H7 and H9 influenza viruses of terrestrial poultry. Virol. J. 5, 85 (2008). https://doi.org/10.1186/1743-422X-5-85
Mochalova, L., Gambaryan, A., Romanova, J., Tuzikov, A., Chinarev, A., Katinger, D., Katinger, H., Egorov, A., Bovin, N.: Receptor-binding properties of modern human influenza viruses primarily isolated in Vero and MDCK cells and chicken embryonated eggs. Virology. 313, 473–480 (2003)
Gambaryan, A.S., Marinina, V.P., Tuzikov, A.B., Bovin, N.V., Rudneva, I.A., Sinitsyn, B.V., Shilov, A.A., Matrosovich, M.N.: Effects of host-dependent glycosylation of hemagglutinin on receptor-binding properties of H1N1 human influenza a virus grown in MDCK cells and in embryonated eggs. Virology. 247, 170–177 (1998)
Gambaryan, A., Tuzikov, A., Pazynina, G., Bovin, N., Balish, A., Klimov, A.: Evolution of the receptor binding phenotype of influenza a (H5) viruses. Virology. 344, 432–438 (2006)
Keleta, L., Ibricevic, A., Bovin, N.V., Brody, S.L., Brown, E.G.: Experimental evolution of human influenza virus H3 hemagglutinin in the mouse lung identifies adaptive regions in HA1 and HA2. J. Virol. 82, 11599–11608 (2008)
Kaltner, H., Abad-Rodríguez, J., Corfield, A.P., Kopitz, J., Gabius, H.-J.: The sugar code: letters and vocabulary, writers, editors and readers and biosignificance of functional glycan-lectin pairing. Biochem. J. 476, 2623–2655 (2019). https://doi.org/10.1042/BCJ20170853
Acknowledgments
The work was supported by the Russian Science Foundation grant № 20-63-47110.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests
The authors declare that they have no conflicts of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Tuzikov, A., Chinarev, A., Shilova, N. et al. 40 years of glyco-polyacrylamide in glycobiology. Glycoconj J 38, 89–100 (2021). https://doi.org/10.1007/s10719-020-09965-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10719-020-09965-5