Synthesis of S-sialyl polymers as efficient polyvalent influenza inhibitors and capturers

Reference

• Grove, J.; Marsh, M. The cell biology of receptor-mediated virus entry. J. Cell Bio. 2011, 195, 1071–1082.
   PubMed Web of Science ®Google Scholar
• Bhatia, S.; Camacho, L. C.; Haag, R. Pathogen Inhibition by Multivalent Ligand Architectures. J. Am. Chem. Soc. 2016, 138, 8654–8666.
   PubMed Web of Science ®Google Scholar
• von Itzstein, M. The war against influenza: discovery and development of sialidase inhibitors. Nat. Rev. Drug Discovery. 2007, 6, 967–974.
   PubMed Web of Science ®Google Scholar
• Wagner, R.; Matrosovich, M.; Klenk, H. D. Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev. Med. Virol. 2002, 12, 159–166.
   PubMed Web of Science ®Google Scholar
• Mueller, K. H.; Kakkola, L.; Nagaraj, A. S.; Cheltsov, A. V.; Anastasina, M.; Kainov, D. E. Emerging cellular targets for influenza antiviral agents. Trends Pharmacol. Sci. 2012, 33, 89–99.
   PubMed Web of Science ®Google Scholar
• Fasting, C.; Schalley, C. A.; Weber, M.; Seitz, O.; Hecht, S.; Koksch, B.; Dernedde, J.; Graf, C.; Knapp, E.-W.; Haag, R. Multivalency as a Chemical Organization and Action Principle. Angew. Chem. Int. Ed. 2012, 51, 10472–10498.
   PubMed Web of Science ®Google Scholar
• Leser, G. P.; Lamb, R. A. Influenza virus assembly and budding in raft-derived microdomains: A quantitative analysis of the surface distribution of HA, NA and M2 proteins. Virology. 2005, 342, 215–227.
   PubMed Web of Science ®Google Scholar
• Sun, X.-L. Recent anti-influenza strategies in multivalent sialyloligosaccharides and sialylmimetics approaches. Curr. Med. Chem. 2007, 14, 2304–2313.
   PubMed Web of Science ®Google Scholar
• Linden, S. K.; Sutton, P.; Karlsson, N. G.; Korolik, V.; McGuckin, M. A. Mucins in the mucosal barrier to infection. Mucosal Immunol. 2008, 1, 183–197.
   PubMed Web of Science ®Google Scholar
• Lieleg, O.; Lieleg, C.; Bloom, J.; Buck, C. B.; Ribbeck, K. Mucin Biopolymers As Broad-Spectrum Antiviral Agents. Biomacromolecules. 2012, 13, 1724–1732.
   PubMed Web of Science ®Google Scholar
• Matrosovich, M.; Klenk, H. D. Natural and synthetic sialic acid-containing inhibitors of influenza virus receptor binding. Polym. Chem. 2003, 13, 85–97.
   Google Scholar
• Smith, A. A. A.; Kryger, M. B. L.; Wohl, B. M.; Ruiz-Sanchis, P.; Zuwala, K.; Tolstrup, M.; Zelikin, A. N. Macromolecular (pro) drugs in antiviral research. Polym. Chem. 2014, 5, 6407–6425.
   Web of Science ®Google Scholar
• Wilson, J. C.; Kiefel, M. J.; Angus, D. I.; von Itzstein, M. Investigation of the Stability of Thiosialosides toward Hydrolysis by Sialidases Using NMR Spectroscopy. Org. Lett. 1999, 1, 443–446.
   PubMed Web of Science ®Google Scholar
• Yang, Y.; Liu, H.-P.; Yu, Q.; Yang, M.-B.; Wang, D.-M.; Jia, T.-W.; He, H.-J.; He, Y.; Xiao, H.-X.; Iyer, S. S.; Fan, Z.-C.; Meng, X.; Yu, P. Multivalent S-sialoside protein conjugates block influenza hemagglutinin and neuraminidase. Carbohydr. Res. 2016, 435, 68–75.
   PubMed Web of Science ®Google Scholar
• Matsuoka, K.; Takita, C.; Koyama, T.; Miyamoto, D.; Yingsakmongkon, S.; Hidari, K. I.; Jampangern, W.; Suzuki, T.; Suzuki, Y.; Hatano, K.; Terunuma, D. Novel linear polymers bearing thiosialosides as pendant-type epitopes for influenza neuraminidase inhibitors. Bioorg. Med. Chem. Lett. 2007, 17, 3826–3830.
   PubMed Web of Science ®Google Scholar
• Prakobphol, A.; Thomsson, K. A.; Hansson, G. C.; Rosen, S. D.; Singer, M. S.; Phillips, N. J.; Medzihradszky, K. F.; Burlingame, A. L.; Leffler, H.; Fisher, S. J. Human low-molecular-weight salivary mucin expresses the sialyl lewisx determinant and has L-selectin ligand activity. Biochemistry. 1998, 37, 4916–4927.
   PubMed Web of Science ®Google Scholar
• Zhang, W.-Q.; He, Y.; Yu, Q.; Liu, H.-P.; Wang, D.-M.; Li, X.-B.; Luo, J.; Meng, X.; Qin, H.-J.; Lucchi, N. W.; Udhayakumar, V.; Iyer, S. S.; Yang, Y.; Yu, P. Polyvalent effect enhances diglycosidic antiplasmodial activity. Eur. J. Med. Chem. 2016, 121, 640–648.
   PubMed Web of Science ®Google Scholar
• Kenawy, E. R.; Sakran, M. A. Controlled release of polymer conjugated agrochemicals. System based on poly(methyl vinyl ether- alt -maleic anhydride). J. Appl. Polym. Sci. 2001, 80, 415–421.
   Web of Science ®Google Scholar
• Gardner, C. M.; Burke, N. A.; Chu, T.; Shen, F.; Potter, M. A.; Stover, H. D. Poly(methyl vinyl ether-alt-maleic acid) polymers for cell encapsulation. J. Biomater. Sci., Polym. Ed. 2011, 22, 2127–2145.
   PubMed Web of Science ®Google Scholar
• Ma, X.; Zhou, N.; Zhang, T.; Guo, Z.; Hu, W.; Zhu, C.; Ma, D.; Gu, N. In formation of multiple stimuli-responsive poly[(methyl vinyl ether)- -(maleic acid)]-based supramolecular hydrogels by inclusion complexation between cyclodextrin and azobenzene. Rsc Adv. 2016, 6, 13129–13136.
   Web of Science ®Google Scholar
• Henry, S. M.; El-Sayed, M. E. H.; Pirie, C. M.; Hoffman, A. S.; Stayton, P. S. pH-Responsive Poly(styrene-alt-maleic anhydride) Alkylamide Copolymers for Intracellular Drug Delivery. Biomacromolecules. 2006, 7, 2407–2414.
   PubMed Web of Science ®Google Scholar
• Tai, H.; Wang, W.; Howdle, S. M. High molecular weight graft stabilisers for dispersion polymerisation of vinylidene fluoride in supercritical carbon dioxide: the effect of architecture. Polymer. 2005, 46, 10626–10636.
   Web of Science ®Google Scholar
• Katz, J. M.; Hancock, K.; Xu, X. Serologic assays for influenza surveillance, diagnosis and vaccine evaluation. Expert Rev. Anti-Infect. Ther. 2011, 9, 669–683.
   PubMed Web of Science ®Google Scholar
• Sever, J. L. Application of a Microtechnique to Viral Serological Investigations. J. Immunol. 1962, 88, 320–329.
   PubMed Web of Science ®Google Scholar
• Tang, S.; Puryear, W. B.; Seifried, B. M.; Dong, X.; Runstadler, J. A.; Ribbeck, K.; Olsen, B. D. Antiviral Agents from Multivalent Presentation of Sialyl Oligosaccharides on Brush Polymers. ACS Macro Lett. 2016, 5, 413–418.
   Web of Science ®Google Scholar
• Lundquist, J. J.; Toone, E. J. The Cluster Glycoside Effect. Chem. Rev. 2002, 102, 555–578.
   PubMed Web of Science ®Google Scholar
• Cecioni, S.; Imberty, A.; Vidal, S. Glycomimetics versus Multivalent Glycoconjugates for the Design of High Affinity Lectin Ligands. Chem. Rev. 2015, 115, 525–561.
   PubMed Web of Science ®Google Scholar
• Bansil, R.; Turner, B. S. Mucin structure, aggregation, physiological functions and biomedical applications. Curr. Opin. Colloid Interface Sci. 2006, 11, 164–170.
   Web of Science ®Google Scholar
• Hushegyi, A.; Bertok, T.; Damborsky, P.; Katrlik, J.; Tkac, J. An ultrasensitive impedimetric glycan biosensor with controlled glycan density for detection of lectins and influenza hemagglutinins. Chem. Commun. 2015, 51, 7474–7477.
   PubMed Web of Science ®Google Scholar
• Bradley, K. C.; Jones, C. A.; Tompkins, S. M.; Tripp, R. A.; Russell, R. J.; Gramer, M. R.; Heimburg-Molinaro, J.; Smith, D. F.; Cummings, R. D.; Steinhauer, D. A. Comparison of the receptor binding properties of contemporary swine isolates and early human pandemic H1N1 isolates (Novel 2009 H1N1). Virology. 2011, 413, 169–182.
   PubMed Web of Science ®Google Scholar
• Chandrasekaran, A.; Srinivasan, A.; Raman, R.; Viswanathan, K.; Raguram, S.; Tumpey, T. M.; Sasisekharan, V.; Sasisekharan, R. Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin. Nat. Biotechnol. 2008, 26, 107–113.
   PubMed Web of Science ®Google Scholar
• Huang, M. L.; Cohen, M.; Fisher, C. J.; Schooley, R. T.; Gagneux, P.; Godula, K. Determination of receptor specificities for whole influenza viruses using multivalent glycan arrays. Chem. Commun. 2015, 51, 5326–5329.
   PubMed Web of Science ®Google Scholar
• Glaser, L.; Conenello, G.; Paulson, J.; Palese, P. Effective replication of human influenza viruses in mice lacking a major α2,6 sialyltransferase. Virus Res. 2007, 126, 9–18.
   PubMed Web of Science ®Google Scholar
• Barrett, S.; Mohr, P. G.; Schmidt, P. M.; McKimm-Breschkin, J. L. Real Time Enzyme Inhibition Assays Provide Insights into Differences in Binding of Neuraminidase Inhibitors to Wild Type and Mutant Influenza Viruses. PLoS ONE. 2011, 6, e23627.
   PubMed Web of Science ®Google Scholar
• Freyer, M. W.; Lewis, E. A. Isothermal titration calorimetry: Experimental design, data analysis, and probing Macromolecule/Ligand binding and kinetic interactions. In Meth. Cell Biol.; Correia, J. J., Detrich, H. W., Eds.;
   Google Scholar
  Meth. Cell Biol. Biophysical Tools for Biologists: Vol 1 in Vitro Techniques, 2008; Vol. 84; pp 79–113.
   Google Scholar
• Hidari, K. I. P. J.; Shimada, S.; Suzuki, Y.; Suzuki, T. Binding kinetics of influenza viruses to sialic acid-containing carbohydrates. Glycoconjugate J. 2007, 24, 583–590.
   PubMed Web of Science ®Google Scholar
• Humphrey, A. J.; Fremann, C.; Critchley, P.; Malykh, Y.; Schauer, R.; Bugg, T. D. H. Biological Properties of N-Acyl and N-Haloacetyl Neuraminic Acids: Processing by Enzymes of Sialic Acid Metabolism, and Interaction with Influenza Virus. Bioorg. Med. Chem. 2002, 10, 3175–3185.
   PubMed Web of Science ®Google Scholar
• Wang, X.; Matei, E.; Gronenborn, A. M.; Ramstrom, O.; Yan, M. Direct Measurement of Glyconanoparticles and Lectin Interactions by Isothermal Titration Calorimetry. Anal. Chem. 2012, 84, 4248–4252.
   PubMed Web of Science ®Google Scholar
• Sauter, N. K.; Bednarski, M. D.; Wurzburg, B. A.; Hanson, J. E.; Whitesides, G. M.; Skehel, J. J.; Wiley, D. C. Hemagglutinins from two influenza virus variants bind to sialic acid derivatives with millimolar dissociation constants: a 500-MHz proton nuclear magnetic resonance study. Biochemistry. 1989, 28, 8388–8396.
   PubMed Web of Science ®Google Scholar
• Mammen, M.; Choi, S.-K.; Whitesides, G. M. Polyvalent Interactions in Biological Systems: Implications for Design and Use of Multivalent Ligands and Inhibitors. Angew. Chem. Int. Ed. 1998, 37, 2754–2794.
   PubMed Web of Science ®Google Scholar
• Yang, Y.; Xue, X.-C.; Jin, X.-F.; Wang, L.-J.; Sha, Y.-L.; Li, Z.-J. Synthesis of multivalent N-acetyl lactosamine modified quantum dots for the study of carbohydrate and galectin-3 interactions. Tetrahedron. 2012, 68, 7148–7154.
   Web of Science ®Google Scholar
• Yu, M.; Yang, Y.; Han, R.; Zheng, Q.; Wang, L.; Hong, Y.; Li, Z.; Sha, Y. Polyvalent Lactose−Quantum Dot Conjugate for Fluorescent Labeling of Live Leukocytes. Langmuir. 2010, 26, 8534–8539.
   PubMed Web of Science ®Google Scholar