Receptor binding by influenza virus: Using computational techniques to extend structural data

Biochemistry

Volumn 51, Issue 12, 2012, Pages 2359-2365

  Kasson, Peter M ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACES; COMPUTATIONAL TECHNIQUE; DYNAMIC DATA; DYNAMIC NATURE; FLEXIBLE LIGANDS; GLYCANS; HOST CELLS; HOST-SPECIFICITY; INFLUENZA VIRUS; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR SIMULATIONS; PROTEIN FLEXIBILITY; RECENT PROGRESS; RECEPTOR BINDING; STRUCTURAL CHARACTERIZATION; STRUCTURAL DATA;

CELL MEMBRANES; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; TISSUE; VIRUSES;

LIGANDS;

GLYCAN; INFLUENZA VIRUS HEMAGGLUTININ;

ASSAY; BINDING AFFINITY; CRYSTAL STRUCTURE; CRYSTALLIZATION; IMAGE ANALYSIS; INFLUENZA VIRUS; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECEPTOR BINDING; REVIEW; SIMULATION; SOLID PHASE ASSAY;

ANIMALS; CELL MEMBRANE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; MOLECULAR DYNAMICS SIMULATION; OLIGOSACCHARIDES; ORTHOMYXOVIRIDAE; POLYSACCHARIDES;

ORTHOMYXOVIRIDAE;

EID: 84859175128     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201684v     Document Type: Review

References (54)

1. Takemoto, D. K., Skehel, J. J., and Wiley, D. C. (1996) A surface plasmon resonance assay for the binding of influenza virus hemagglutinin to its sialic acid receptor Virology 217, 452-458
2. Sauter, N. K., Hanson, J. E., Glick, G. D., Brown, J. H., Crowther, R. L., Park, S. J., Skehel, J. J., and Wiley, D. C. (1992) Binding of influenza virus hemagglutinin to analogs of its cell-surface receptor, sialic acid: Analysis by proton nuclear magnetic resonance spectroscopy and X-ray crystallography Biochemistry 31, 9609-9621
3. Couceiro, J., Paulson, J. C., and Baum, L. G. (1993) Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity Virus Res. 29, 155-165
4. van Riel, D., Munster, V. J., de Wit, E., Rimmelzwaan, G. F., Fouchier, R. A., Osterhaus, A. D., and Kuiken, T. (2007) Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals Am. J. Pathol. 171, 1215-1223
5. Shinya, K., Ebina, M., Yamada, S., Ono, M., Kasai, N., and Kawaoka, Y. (2006) Avian flu: Influenza virus receptors in the human airway Nature 440, 435-436
6. Wagner, R., Heuer, D., Wolff, T., Herwig, A., and Klenk, H. D. (2002) N-Glycans attached to the stem domain of haemagglutinin efficiently regulate influenza A virus J. Gen. Virol. 83, 601-609
7. Mitnaul, L. J., Matrosovich, M. N., Castrucci, M. R., Tuzikov, A. B., Bovin, N. V., Kobasa, D., and Kawaoka, Y. (2000) Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus J. Virol. 74, 6015-6020
8. Gubareva, L. V., Nedyalkova, M. S., Novikov, D. V., and Murti, K. G. (2002) A release-competent influenza A virus mutant lacking the coding capacity for the neuraminidase active site J. Gen. Virol. 83, 2683-2692
9. Ferraris, O., Kessler, N., Valette, M., and Lina, B. (2006) Evolution of the susceptibility to antiviral drugs of A/H3N2 influenza viruses isolated in France from 2002 to 2005 Vaccine 24, 6656-6659
10. Wilson, I. A., Skehel, J. J., and Wiley, D. C. (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution Nature 289, 366-373
11. Gambaryan, A. S., Marinina, V. P., Tuzikov, A. B., Bovin, N. V., Rudneva, I. A., Sinitsyn, B. V., Shilov, A. A., and Matrosovich, M. N. (1998) Effects of host-dependent glycosylation of hemagglutinin on receptor-binding properties on H1N1 human influenza A virus grown in MDCK cells and in embryonated eggs Virology 247, 170-177
12. Gambaryan, A. S., Robertson, J. S., and Matrosovich, M. N. (1999) Effects of egg-adaptation on the receptor-binding properties of human influenza A and B viruses Virology 258, 232-239
13. Wang, C. C., Chen, J. R., Tseng, Y. C., Hsu, C. H., Hung, Y. F., Chen, S. W., Chen, C. M., Khoo, K. H., Cheng, T. J., Cheng, Y. S., Jan, J. T., Wu, C. Y., Ma, C., and Wong, C. H. (2009) Glycans on influenza hemagglutinin affect receptor binding and immune response Proc. Natl. Acad. Sci. U.S.A. 106, 18137-18142
14. de Vries, R. P., de Vries, E., Bosch, B. J., de Groot, R. J., Rottier, P. J., and de Haan, C. A. (2010) The influenza A virus hemagglutinin glycosylation state affects receptor-binding specificity Virology 403, 17-25
15. 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., and Paulson, J. C. (2004) Printed covalent glycan array for ligand profiling of diverse glycan binding proteins Proc. Natl. Acad. Sci. U.S.A. 101, 17033-17038
16. Stevens, J., Blixt, O., Glaser, L., Taubenberger, J. K., Palese, P., Paulson, J. C., and Wilson, I. A. (2006) Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities J. Mol. Biol. 355, 1143-1155
17. Stevens, J., Blixt, O., Tumpey, T. M., and Taubenberger, J. K. (2006) Structure and Receptor Specificity of the Hemagglutinin from an H5N1 Influenza Virus Science 312, 404-410
18. Stevens, J., Blixt, O., Paulson, J. C., and Wilson, I. A. (2006) Glycan microarray technologies: Tools to survey host specificity of influenza viruses Nat. Rev. Microbiol. 4, 857-864
19. Liang, R., Yan, L., Loebach, J., Ge, M., Uozumi, Y., Sekanina, K., Horan, N., Gildersleeve, J., Thompson, C., Smith, A., Biswas, K., Still, W. C., and Kahne, D. (1996) Parallel synthesis and screening of a solid phase carbohydrate library Science 274, 1520-1522
20. Chandrasekaran, A., Srinivasan, A., and Raman, R. (2008) Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin Nat. Biotechnol. 26, 107-113
21. Hidari, K. I., Shimada, S., Suzuki, Y., and Suzuki, T. (2007) Binding kinetics of influenza viruses to sialic acid-containing carbohydrates Glycoconjugate J. 24, 583-590
22. Lewallen, D. M., Siler, D., and Iyer, S. S. (2009) Factors affecting protein-glycan specificity: Effect of spacers and incubation time ChemBioChem 10, 1486-1489
23. Bradley, K. C., Galloway, S. E., Lasanajak, Y., Song, X., Heimburg-Molinaro, J., Yu, H., Chen, X., Talekar, G. R., Smith, D. F., Cummings, R. D., and Steinhauer, D. A. (2011) Analysis of influenza virus hemagglutinin receptor binding mutants with limited receptor recognition properties and conditional replication characteristics J. Virol. 85, 12387-12398
24. Deng, Y., Wang, Y., Holtz, B., Li, J., Traaseth, N., Veglia, G., Stottrup, B. J., Elde, R., Pei, D., Guo, A., and Zhu, X. Y. (2008) Fluidic and air-stable supported lipid bilayer and cell-mimicking microarrays J. Am. Chem. Soc. 130, 6267-6271
25. Zhu, X. Y., Holtz, B., Wang, Y., Wang, L. X., Orndorff, P. E., and Guo, A. (2009) Quantitative glycomics from fluidic glycan microarrays J. Am. Chem. Soc. 131, 13646-13650
26. Kirschner, K. N., Yongye, A. B., Tschampel, S. M., Gonzalez- Outeiriño, J., Daniels, C. R., Foley, B. L., and Woods, R. J. (2008) GLYCAM06: A generalizable biomolecular force field. Carbohydrates J. Comput. Chem. 29, 622-655
27. Kuttel, M., Brady, J. W., and Naidoo, K. J. (2002) Carbohydrate solution simulations: Producing a force field with experimentally consistent primary alcohol rotational frequencies and populations J. Comput. Chem. 23, 1236-1243
28. Jayachandran, G., Vishal, V., and Pande, V. S. (2006) Using massively parallel simulation and Markovian models to study protein folding: Examining the dynamics of the villin headpiece J. Chem. Phys. 124, 164902
29. Noe, F. and Fischer, S. (2008) Transition networks for modeling the kinetics of conformational change in macromolecules Curr. Opin. Struct. Biol. 18, 154-162
30. Swope, W. C., Pitera, J. W., and Suits, F. (2004) Describing protein folding kinetics by molecular dynamics simulations. 1. Theory J. Phys. Chem. B 108, 6571-6581
31. Lang, P. T., Ng, H. L., Fraser, J. S., Corn, J. E., Echols, N., Sales, M., Holton, J. M., and Alber, T. (2010) Automated electron-density sampling reveals widespread conformational polymorphism in proteins Protein Sci. 19, 1420-1431
32. Rieping, W., Habeck, M., and Nilges, M. (2005) Inferential structure determination Science 309, 303-306
33. Rieping, W., Nilges, M., and Habeck, M. (2008) ISD: A software package for Bayesian NMR structure calculation Bioinformatics 24, 1104-1105
34. Grubmuller, H. (1995) Predicting slow structural transitions in macromolecular systems: Conformational flooding Phys. Rev. E: Stat. Phys., Plasmas, Fluids, Relat. Interdiscip. Top. 52, 2893-2906
35. Hamelberg, D., Mongan, J., and McCammon, J. A. (2004) Accelerated molecular dynamics: A promising and efficient simulation method for biomolecules J. Chem. Phys. 120, 11919-11929
36. Singhal, N. and Pande, V. S. (2005) Error analysis and efficient sampling in Markovian state models for molecular dynamics J. Chem. Phys. 123, 204909
37. Kasson, P., Kelley, N., Singhal, N., Vrljic, M., Brunger, A. T., and Pande, V. S. (2006) Ensemble molecular dynamics yields sub-millisecond kinetics and intermediates of membrane fusion Proc. Natl. Acad. Sci. U.S.A. 103, 11916-11921
38. Elber, R. (2005) Long-timescale simulation methods Curr. Opin. Struct. Biol. 15, 151-156
39. Eklund, R. and Widmalm, G. (2003) Molecular dynamics simulations of an oligosaccharide using a force field modified for carbohydrates Carbohydr. Res. 338, 393-398
40. Kasson, P. M. and Pande, V. S. (2008) Structural basis for influence of viral glycans on ligand binding by influenza hemagglutinin Biophys. J. 95, L48-L50
41. Hunenberger, P. H., Mark, A. E., and van Gunsteren, W. F. (1995) Fluctuation and cross-correlation analysis of protein motions observed in nanosecond molecular dynamics simulations J. Mol. Biol. 252, 492-503
42. 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
43. Eisen, M. B., Sabesan, S., Skehel, J. J., and Wiley, D. C. (1997) Binding of the influenza A virus to cell-surface receptors: Structures of five hemagglutinin-sialyloligosaccharide complexes determined by X-ray crystallography Virology 232, 19-31
44. Gamblin, S. J., Haire, L. F., Russell, R. J., and Stevens, D. J. 2004, The structure and receptor binding properties of the 1918 influenza hemagglutinin Science 303, 1838-1842
45. Lin, T., Wang, G., Li, A., Zhang, Q., Wu, C., Zhang, R., Cai, Q., Song, W., and Yuen, K. Y. (2009) The hemagglutinin structure of an avian H1N1 influenza A virus Virology 392, 73-81
46. 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
47. Wang, Q., Tian, X., Chen, X., and Ma, J. (2007) Structural basis for receptor specificity of influenza B virus hemagglutinin Proc. Natl. Acad. Sci. U.S.A. 104, 16874-16879
48. 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
49. Newhouse, E. I., Xu, D., Markwick, P. R., Amaro, R. E., Pao, H. C., Wu, K. J., Alam, M., McCammon, J. A., and Li, W. W. (2009) Mechanism of glycan receptor recognition and specificity switch for avian, swine, and human adapted influenza virus hemagglutinins: A molecular dynamics perspective J. Am. Chem. Soc. 131, 17430-17442
50. Kasson, P. M., Ensign, D. L., and Pande, V. S. (2009) Combining Molecular Dynamics with Bayesian Analysis To Predict and Evaluate Ligand-Binding Mutations in Influenza Hemagglutinin J. Am. Chem. Soc. 131, 1338-1340
51. Kasson, P. M. and Pande, V. S. (2009) Combining sequence and structural information to assess influenza host-specifcity mutants Pac. Symp. Biocomput. 2009, 492-503
52. Das, P., Li, J., Royyuru, A. K., and Zhou, R. (2009) Free energy simulations reveal a double mutant avian H5N1 virus hemagglutinin with altered receptor binding specificity J. Comput. Chem. 30, 1654-1663
53. Mir-Shekari, S. Y., Ashford, D. A., Harvey, D. J., Dwek, R. A., and Schulze, I. T. (1997) The glycosylation of the influenza A virus hemagglutinin by mammalian cells. A site-specific study J. Biol. Chem. 272, 4027-4036
54. Demarco, M. L., Woods, R. J., Prestegard, J. H., and Tian, F. (2010) Presentation of membrane-anchored glycosphingolipids determined from molecular dynamics simulations and NMR paramagnetic relaxation rate enhancement J. Am. Chem. Soc. 132, 1334-1338