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Conformation and Linkage Studies of Specific Oligosaccharides Related to H1N1, H5N1, and Human Flu for Developing the Second Tamiflu

  • Yoo, Eunsun (College of Health Science, Honam University)
  • Received : 2014.01.20
  • Accepted : 2014.03.04
  • Published : 2014.03.31

Abstract

The interaction between viral HA (hemagglutinin) and oligosaccharide of the host plays an important role in the infection and transmission of avian and human flu viruses. Until now, this interaction has been classified by sialyl(${\alpha}2-3$) or sialyl(${\alpha}2-6$) linkage specificity of oligosaccharide moieties for avian or human virus, respectively. In the case of H5N1 and newly mutated flu viruses, classification based on the linkage type does not correlate with human infection and human-to-human transmission of these viruses. It is newly suggested that flu infection and transmission to humans require high affinity binding to the extended conformation with long length sialyl(${\alpha}2-6$)galactose containing oligosaccharides. On the other hand, the avian flu virus requires folded conformation with sialyl(${\alpha}2-3$) or short length sialyl(${\alpha}2-6$) containing trisaccharides. This suggests a potential future direction for the development of new species-specific antiviral drugs to prevent and treat pandemic flu.

Keywords

References

  1. Babu, Y. S., Chand, P., Bantia, S., Kotian, P., Dehghani, A., El-Kattan, Y., Lin, T. H., Hutchison, T. L., Elliott, A. J., Parker, C. D., Ananth, S. L., Horn, L. L., Laver, G. W. and Montgomery, J. A. (2000) BCX-1812 (RWJ-270201): discovery of a novel, highly potent, orally active, and selective influenza neuraminidase inhibitor through structure-based drug design. J. Med. Chem. 43, 3482-3486. https://doi.org/10.1021/jm0002679
  2. Bantia, S., Parker, C. D., Ananth, S. L., Horn, L. L., Andries, K., Chand, P., Kotian, P. L., Dehghani, A., El-Kattan, Y., Lin, T., Hutchison, T. L., Montgomery, J. A., Kellog, D. L. and Babu, Y. S. (2001) Comparison of the anti-influenza virus activity of RWJ-270201 with those of oseltamivir and zanamivir. Antimicrob. Agents Chemother. 45, 1162-1167. https://doi.org/10.1128/AAC.45.4.1162-1167.2001
  3. Baz, M., Abed, Y., Papenburg, J., Bouhy, X., Hamelin, M. E. and Boivin, G. (2009) Emergence of oseltamivir-resistant pandemic H1N1 virus during prophylaxis. N. Engl. J. Med. 361, 2296-2297. https://doi.org/10.1056/NEJMc0910060
  4. Bateman, A. C., Karamanska, R., Busch, M. G., Dell, A., Olsen, C. W. and Haslam, S. M. (2010) Glycan analysis and influenza A virus infection of primary swine respiratory epithelial cells: the importance of $NeuAc{\alpha}2-6$ glycans. J. Biol. Chem. 285, 34016-34026. https://doi.org/10.1074/jbc.M110.115998
  5. Belser, J. A., Blixt, O., Chen, L. M., Pappas, C., Maines, T. R., Van Hoeven, N., Donis, R., Busch, J., McBride, R., Paulson, J. C., Katz, J. M. and Tumpey, T. M. (2008) Contemporary North American influenza H7 viruses possess human receptor specificity: Implications for virus transmissibility. Proc. Natl. Acad. Sci. U.S.A. 105, 7558-7563. https://doi.org/10.1073/pnas.0801259105
  6. Belshe, R. B. (2005) The origins of pandemic influenza--lessons from the 1918 virus. N. Engl. J. Med. 353, 2209-2211. https://doi.org/10.1056/NEJMp058281
  7. Claas, E. C., Osterhaus, A. D., van Beek, R., De Jong, J. C., Rimmelzwaan, G. F., Senne, D. A., Krauss, S., Shortridge, K. F. and Webster, R. G. (1998) Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351, 472-477. https://doi.org/10.1016/S0140-6736(97)11212-0
  8. Chandrasekaran, A., Srinivasan, A., Raman, R., Viswanathan, K., Raguram, S., Tumpey, T. M., Sasisekharan, V. and Sasisekharan, R. (2008) Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin. Nat. Biotechnol. 26, 107-113. https://doi.org/10.1038/nbt1375
  9. Chen, L. M., Blixt, O., Stevens, J., Lipatov, A. S., Davis, C. T., Collins, B. E., Cox, N. J., Paulson, J. C. and Donis, R. O. (2012) In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity. Virology 422, 105-113. https://doi.org/10.1016/j.virol.2011.10.006
  10. Cohen, J. (2013) Influenza. New flu virus in China worries and confuses. Science 340, 129-130. https://doi.org/10.1126/science.340.6129.129
  11. Clercq, E.D. (2013) Antivirals: Past, present and future. Biochem. Pharmacol. 85, 727-744. https://doi.org/10.1016/j.bcp.2012.12.011
  12. Collins, P. J., Haire, L. F., Lin, Y. P., Liu, J., Russell, R. J., Walker, P. A., Skehel, J. J., Martin, S. R., Hay, A. J. and Gamblin, S. J. (2008) Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants. Nature 453, 1258-1261. https://doi.org/10.1038/nature06956
  13. Colman, P. M., Varghese, J. N. and Laver, W. G. (1983) Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 303, 41-44. https://doi.org/10.1038/303041a0
  14. Gambaryan, A., Yamnikova, S., Lvov, D., Tuzikov, A., Chinarev, A., Pazynina, G., Webster, R., Matrosovich, M. and Bovin, N. (2005) 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. https://doi.org/10.1016/j.virol.2005.02.003
  15. Gubareva, L. V., Kaiser, L. and Hayden, F. G. (2000) Influenza virus neuraminidase inhibitors. Lancet 355, 827-835. https://doi.org/10.1016/S0140-6736(99)11433-8
  16. Ha, Y., Stevens, D. J., Skehel, J. J. and Wiley, D. C. (2001) X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc. Natl. Acad. Sci. U.S.A. 98, 11181-11186. https://doi.org/10.1073/pnas.201401198
  17. Ha, Y., Stevens, D. J., Skehel, J. J. and Wiley, D. C. (2003) X-ray structure of the hemagglutinin of a potential H3 avian progenitor of the 1968 Hong Kong pandemic influenza virus. Virology 309, 209-218. https://doi.org/10.1016/S0042-6822(03)00068-0
  18. Haselhorst, T., Garcia, J. M., Islam, T., Lai, J. C., Rose, F. J., Nicholls, J. M., Peiris, J. S. and von Itzstein, M. (2008) Avian influenza H5-containing virus-like particles (VLPs): host-cell receptor specificity by STD NMR spectroscopy. Angew. Chem. Int. Ed. Engl. 47, 1910-1912. https://doi.org/10.1002/anie.200704872
  19. Hatta, M., Gao, P., Halfmann, P. and Kawaoka, Y. (2001) Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293, 1840-1842. https://doi.org/10.1126/science.1062882
  20. Hayden, F. (2009) Developing new antiviral agents for influenza treatment: what does the future hold? Clin. Infect. Dis. 48 Suppl 1, S3-13. https://doi.org/10.1086/591851
  21. Hayden, F. G. and Pavia, A. T. (2006) Antiviral management of seasonal and pandemic influenza. J. Infect. Dis. 194 Suppl 2, S119-126. https://doi.org/10.1086/507552
  22. Hvistendahl, M., Normile, D. and Cohen, J. (2013) Influenza. Despite large research effort, H7N9 continues to baffle. Science 340, 414-415. https://doi.org/10.1126/science.340.6131.414
  23. Imai, M. and Kawaoka, Y. (2012) The role of receptor binding specificity in interspecies transmission of influenza viruses. Curr. Opin. Virol. 2, 160-167. https://doi.org/10.1016/j.coviro.2012.03.003
  24. Ison, M. G. (2011) Antivirals and resistance: influenza virus. Curr. Opin. Virol. 1, 563-573 https://doi.org/10.1016/j.coviro.2011.09.002
  25. Jimenez-Alberto, A., Alvarado-Facundo, E., Ribas-Aparicio, R. M. and Castelan-Vega, J. A. (2013) Analysis of adaptation mutants in the hemagglutinin of the influenza A(H1N1)pdm09 virus. PloS One 8, e70005. https://doi.org/10.1371/journal.pone.0070005
  26. Kumari, K., Gulati, S., Smith, D. F., Gulati, U., Cummings, R. D. and Air, G. M. (2007) Receptor binding specificity of recent human H3N2 influenza viruses. Virol. J. 4, 42. https://doi.org/10.1186/1743-422X-4-42
  27. Laver, G. (2006) Antiviral drugs for influenza: Tamiflu past, present and future. Future Virol. 1, 577-586. https://doi.org/10.2217/17460794.1.5.577
  28. Layne, S. P., Monto, A. S. and Taubenberger, J. K. (2009) Pandemic influenza: an inconvenient mutation. Science 323, 1560-1561. https://doi.org/10.1126/science.323.5921.1560
  29. Lee, S. M. and Yen, H. L. (2012) Targeting the host or the virus: current and novel concepts for antiviral approaches against influenza virus infection. Antiviral Res. 96, 391-404. https://doi.org/10.1016/j.antiviral.2012.09.013
  30. Mair, C. M., Ludwig, K., Herrmann, A. and Sieben, C. (2014) Receptor binding and pH stability - How influenza A virus hemagglutinin affects host-specific virus infection. Biochim. Biophys. Acta 1838, 1153-1168. https://doi.org/10.1016/j.bbamem.2013.10.004
  31. Matrosovich, M., Herrler, G. and Klenk, H. D. (2013) Sialic acid receptors of viruses. Top. Curr. Chem. 128, 466.
  32. Memoli, M. J., Hrabal, R. J., Hassantoufighi, A., Eichelberger, M. C. and Taubenberger, J. K. (2010) Rapid selection of oseltamivir- and peramivir-resistant pandemic H1N1 virus during therapy in 2 immunocompromised hosts. Clin. Infect. Dis. 50, 1252-1255. https://doi.org/10.1086/651605
  33. Neumann, G. and Kawaoka, Y. (2006) Host range restriction and pathogenicity in the context of influenza pandemic. Emerg. Infect. Dis. 12, 881-886. https://doi.org/10.3201/eid1206.051336
  34. Neumann, G., Noda, T. and Kawaoka, Y. (2009) Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459, 931-939. https://doi.org/10.1038/nature08157
  35. Nguyen, D. C., Uyeki, T. M., Jadhao, S., Maines, T., Shaw, M., Matsuoka, Y., Smith, C., Rowe, T., Lu, X., Hall, H., Xu, X., Balish, A., Klimov, A., Tumpey, T. M., Swayne, D. E., Huynh, L. P., Nghiem, H. K., Nguyen, H. H., Hoang, L. T., Cox, N. J. and Katz, J. M. (2005) Isolation and characterization of avian influenza viruses, including highly pathogenic H5N1, from poultry in live bird markets in Hanoi, Vietnam, in 2001. J. Virol. 79, 4201-4212. https://doi.org/10.1128/JVI.79.7.4201-4212.2005
  36. Nicholls, J. M., Bourne, A. J., Chen, H., Guan, Y. and Peiris, J. S. (2007) Sialic acid receptor detection in the human respiratory tract: evidence for widespread distribution of potential binding sites for human and avian influenza viruses. Respir. Res. 8, 73. https://doi.org/10.1186/1465-9921-8-73
  37. Pappas, C., Viswanathan, K., Chandrasekaran, A., Raman, R., Katz, J. M., Sasisekharan, R. and Tumpey, T. M. (2010) Receptor specificity and transmission of H2N2 subtype viruses isolated from the pandemic of 1957. PloS One 5, e11158. https://doi.org/10.1371/journal.pone.0011158
  38. Paulson, J. C., Blixt, O. and Collins, B. E. (2006) Sweet spots in functional glycomics. Nat. Chem. Biol. 2, 238-248. https://doi.org/10.1038/nchembio785
  39. Perrone, L. A. and Tumpey, T. M. (2007) Reconstruction of the 1918 pandemic influenza virus: how revealing the molecular secrets of the virus responsible for the worst pandemic in recorded history can guide our response to future influenza pandemics. Infect. Disord. Drug Targets 7, 294-303. https://doi.org/10.2174/187152607783018772
  40. Puzelli, S., Facchini, M., Di Martino, A., Fabiani, C., Lackenby, A., Zambon, M. and Donatelli, I. (2011) Evaluation of the antiviral drug susceptibility of influenza viruses in Italy from 2004/05 to 2009/10 epidemics and from the recent 2009 pandemic. Antiviral Res. 90, 205-212. https://doi.org/10.1016/j.antiviral.2011.04.003
  41. Raman, R. and Sasisekharan, R. (2007) Cooperativity in glycan-protein interactions. Chem. Biol. 14, 873-874. https://doi.org/10.1016/j.chembiol.2007.08.003
  42. Rumschlag-Booms, E. and Rong, L. (2013) Influenza a virus entry: implications in virulence and future therapeutics. Adv. Virol. 2013, 121924.
  43. Russel, R. J., Haire, L. F., Stevens, D. J., Collins, P. J., Lin, Y. P., Blackburn, G. M., Hay, A. J., Gamblin, S. J. and Skehe, J. J. (2006) The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 443, 45-49. https://doi.org/10.1038/nature05114
  44. Samson, M., Pizzorno, A., Abed, Y. and Boivin, G. (2013) Influenza virus resistance to neuraminidase inhibitors. Antiviral Res. 98, 174-185. https://doi.org/10.1016/j.antiviral.2013.03.014
  45. Shriver, Z., Raman, R., Viswanathan, K. and Sasisekharan, R. (2009) Context-specific target definition in influenza a virus hemagglutinin-glycan receptor interactions. Chem. Biol. 16, 803-814. https://doi.org/10.1016/j.chembiol.2009.08.002
  46. Sorrell, E. M., Schrauwen, E. J., Linster, M., De Graaf, M., Herfst, S. and Fouchier, R. A. (2011) Predicting 'airborne' influenza viruses: (trans-) mission impossible? Curr. Opin. Virol. 1, 635-642. https://doi.org/10.1016/j.coviro.2011.07.003
  47. Srinivasan, A., Viswanathan, K., Raman, R., Chandrasekaran, A., Raguram, S., Tumpey, T. M., Sasisekharan, V. and Sasisekharan, R. (2008) Quantitative biochemical rationale for differences in transmissibility of 1918 pandemic influenza A viruses. Proc. Natl. Acad. Sci. U.S.A. 105, 2800-2805. https://doi.org/10.1073/pnas.0711963105
  48. Stevens, J., Blixt, O., Chen, L. M., Donis, R. O., Paulson, J. C. and Wilson, I. A. (2008) Recent avian H5N1 viruses exhibit increased propensity for acquiring human receptor specificity. J. Mol. Biol. 381, 1382-1394. https://doi.org/10.1016/j.jmb.2008.04.016
  49. Stevens, J., Blixt, O., Paulson, J. C. and Wilson, I. A. (2006a) Glycan microarray technologies: tools to survey host specificity of influenza viruses. Nat. Rev. Microbiol. 4, 857-864. https://doi.org/10.1038/nrmicro1530
  50. Stevens, J., Blixt, O., Tumpey, T. M., Taubenberger, J. K., Paulson, J. C. and Wilson, I. A. (2006b) Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312, 404-410. https://doi.org/10.1126/science.1124513
  51. Stevens, J., Corper, A. L., Basler, C. F., Taubenberger, J. K., Palese, P. and Wilson, I. A. (2004) Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303, 1866-1870. https://doi.org/10.1126/science.1093373
  52. Stoner, T. D., Krauss, S., DuBois, R. M., Negovetich, N. J., Stallknecht, D. E., Senne, D. A., Gramer, M. R., Swafford, S., DeLiberto, T., Govorkova, E. A. and Webster, R. G. (2010) Antiviral susceptibility of avian and swine influenza virus of the N1 neuraminidase subtype. J. Virol. 84, 9800-9809. https://doi.org/10.1128/JVI.00296-10
  53. Taylo, M. E. and Drickame, K. (2011) Viruses use lectins to target cell surfaces, Introduction to Glycobiology, Oxford University Press, London.
  54. Tumpey, T. M., Basler, C. F., Aguilar, P. V., Zeng, H., Solorzano, A., Swayne, D. E., Cox, N. J., Katz, J. M., Taubenberger, J. K., Palese, P. and Garcia-Sastre, A. (2005) Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310, 77-80. https://doi.org/10.1126/science.1119392
  55. Varghese, J. N., Laver, W. G. and Colman, P. M. (1983) Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 A resolution. Nature 303, 35-40. https://doi.org/10.1038/303035a0
  56. Vavricka, C. J., Li, Q., Wu, Y., Qi, J., Wang, M., Liu, Y., Gao, F., Liu, J., Feng, E., He, J., Wang, J., Liu, H., Jiang, H. and Gao, G. F. (2011) Structural and functional analysis of laninamivir and its octanoate prodrug reveals group specific mechanisms for influenza NA inhibition. PLoS Pathog. 7, e1002249. https://doi.org/10.1371/journal.ppat.1002249
  57. Viswanathan, K., Chandrasekaran, A., Srinivasan, A., Raman, R., Sasisekharan, V. and Sasisekharan, R. (2010) Glycans as receptors for influenza pathogenesis. Glycoconj. J. 27, 561-570. https://doi.org/10.1007/s10719-010-9303-4
  58. Walther, T., Karamanska, R., Chan, R. W., Chan, M. C., Jia, N., Air, G., Hopton, C., Wong, M. P., Dell, A., Malik Peiris, J. S., Haslam, S. M. and Nicholls, J. M. (2013) Glycomic analysis of human respiratory tract tissues and correlation with influenza virus infection. PLoS Pathog. 9, e1003223. https://doi.org/10.1371/journal.ppat.1003223
  59. Wang, N. X. and Zheng, J. J. (2009) Computational studies of H5N1 influenza virus resistance to oseltamivir. Protein Sci. 18, 707-715.
  60. Watanabe, Y., Ibrahim, M. S., Suzuki, Y. and Ikuta, K. (2012) The changing nature of avian influenza A virus (H5N1). Trends Microbiol. 20, 11-20. https://doi.org/10.1016/j.tim.2011.10.003
  61. Xu, D., Newhouse, E. I., Amaro, R. E., Pao, H. C., Cheng, L. S., Markwick, P. R., McCammon, J. A., Li, W. W. and Arzberger, P. W. (2009) Distinct glycan topology for avian and human sialopentasaccharide receptor analogues upon binding different hemagglutinins: a molecular dynamics perspective. J. Mol. Biol. 387, 465-491. https://doi.org/10.1016/j.jmb.2009.01.040
  62. Xu, R., McBride, R., Nycholat, C. M., Paulson, J. C. and Wilson, I. A. (2012) Structural characterization of the hemagglutinin receptor specificity from the 2009 H1N1 influenza pandemic. J. Virol. 86, 982-990. https://doi.org/10.1128/JVI.06322-11
  63. Xu, X., Zhu, X., Dwek, R. A., Stevens, J. and Wilson, I. A. (2008) Structural characterization of the 1918 influenza virus H1N1 neuraminidase. J. Virol. 82, 10493-10501. https://doi.org/10.1128/JVI.00959-08
  64. Yamada, S., Shinya, K., Takada, A., Ito, T., Suzuki, T., Suzuki, Y., Le, Q. M., Ebina, M., Kasai, N., Kida, H., Horimoto, T., Rivailler, P., Chen, L. M., Donis, R. O. and Kawaoka, Y. (2012) Adaptation of a duck influenza A virus in quail. J. Virol. 86, 1411-1420. https://doi.org/10.1128/JVI.06100-11
  65. Yen, H. L., Lipatov, A. S., Ilyushina, N. A., Govorkova, E. A., Franks, J., Yilmaz, N., Douglas, A., Hay, A., Krauss, S., Rehg, J. E., Hoffmann, E. and Webster, R. G. (2007) Inefficient transmission of H5N1 influenza viruses in a ferret contact model. J. Virol. 81, 6890-6898. https://doi.org/10.1128/JVI.00170-07
  66. Yoo, E. (2001) A conformational study of oligosaccharides investigated by tandem mass spectrometry and molecular modeling. Bull. Korean Chem. Soc. 22, 293-297.
  67. Yoo, E. (2011) Study of specific oligosaccharide structures related with swine flu (H1N1) and avian flu, and tamiflu as their remedy. J. Microbiol. Biotechnol. 21, 449-454. https://doi.org/10.4014/jmb.1009.09013
  68. Yoo, E. and Yoon, I. (2008) Molecular simulations and conformational studies of fucose((${\alpha}1-3)Gal({\beta}1-X$)GlcNAc where X=3,4, or 6 oligosaccharides. Bull. Korean Chem. Soc. 29, 1755-1760. https://doi.org/10.5012/bkcs.2008.29.9.1755
  69. Zurcher, T., Yates, P. J., Daly, J., Sahasrabudhe, A., Walters, M., Dash, L., Tisdale, M. and McKimm-Breschkin, J. L. (2006) Mutations conferring zanamivir resistance in human influenza virus N2 neuraminidases compromise virus fitness and are not stably maintained in vitro. J. Antimicrob. Chemother. 58, 723-732. https://doi.org/10.1093/jac/dkl321