Human (α2→6) and avian (α2→3) sialylated receptors of influenza A virus show distinct conformations and dynamics in solution

Biochemistry

Volumn 52, Issue 41, 2013, Pages 7217-7230

  Sassaki, Guilherme L ^a,d   Elli, Stefano ^a   Rudd, Timothy R ^a,e   Macchi, Eleonora ^a   Yates, Edwin A ^b   Naggi, Annamaria ^a   Shriver, Zachary ^c   Raman, Rahul ^c   Sasisekharan, R ^c   Torri, Giangiacomo ^a   Guerrini, Marco ^a  

^a Istituto di Ricerche Chimiche e Biochimiche G Ronzoni   (Italy)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c Massachusetts Institute of Technology   (United States)

^d FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^e DIAMOND LIGHT SOURCE LTD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DIFFERENTIAL INTERACTION; HOST-SPECIFICITY; INFLUENZA A VIRUS; MOLECULAR CHARACTERISTICS; MOLECULAR DYNAMICS SIMULATIONS; PENTASACCHARIDES; SOLUTION CONFORMATIONS; UNIQUE FEATURES;

DYNAMICS; MOLECULAR DYNAMICS; POLYSACCHARIDES; TOPOLOGY; VIRUSES;

CONFORMATIONS;

(ALPHA 2-3) SIALYLATED RECEPTOR; (ALPHA 2-6) SIALYLATED RECEPTOR; GLYCAN; INFLUENZA VIRUS HEMAGGLUTININ; PENTASACCHARIDE; SIALIC ACID; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; HUMAN; HYDROGEN BOND; INFLUENZA VIRUS; MOLECULAR DYNAMICS; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

ANIMALS; BIRDS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; MODELS, MOLECULAR; N-ACETYLNEURAMINIC ACID; POLYSACCHARIDES; RECEPTORS, VIRUS;

EID: 84885964866     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400677n     Document Type: Article

References (46)

1. 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
2. Gamblin, S. J., Haire, L. F., Russell, R. J., Stevens, D. J., Xiao, B., Ha, Y., Vasisht, N., Steinhauer, D. A., Daniels, R. S., Elliot, A., Wiley, D. C., and Skehel, J. J. (2004) The structure and receptor binding properties of the 1918 influenza hemagglutinin Science 303, 1838-1842
3. 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
4. Stevens, J., Blixt, O., Tumpey, T. M., Taubenberger, J. K., Paulson, J. C., and Wilson, I. A. (2006) Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus Science 312, 404-410
5. Weis, W., Brown, J. H., Cusack, S., Paulson, J. C., Skehel, J. J., and Wiley, D. C. (1988) Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid Nature 333, 426-431
6. Ibricevic, A., Pekosz, A., Walter, M. J., Newby, C., Battaile, J. T., Brown, E. G., Holtzman, M. J., and Brody, S. L. (2006) Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells J. Virol. 80, 7469-7480
7. 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
8. 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
9. Jayaraman, A., Pappas, C., Raman, R., Belser, J. A., Viswanathan, K., Shriver, Z., Tumpey, T. M., and Sasisekharan, R. (2011) A single base-pair change in 2009 H1N1 hemagglutinin increases human receptor affinity and leads to efficient airborne viral transmission in ferrets PLoS One 6, e17616
10. 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
11. Matrosovich, M. N., Matrosovich, T. Y., Gray, T., Roberts, N. A., and Klenk, H. D. (2004) Human and avian influenza viruses target different cell types in cultures of human airway epithelium Proc. Natl. Acad. Sci. U.S.A. 101, 4620-4624
12. Rogers, G. N., Paulson, J. C., Daniels, R. S., Skehel, J. J., Wilson, I. A., and Wiley, D. C. (1983) Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity Nature 304, 76-78
13. Russell, R. J., Stevens, D. J., Haire, L. F., Gamblin, S. J., and Skehel, J. J. (2006) Avian and human receptor binding by hemagglutinins of influenza A viruses Glycoconjugate J. 23, 85-92
14. 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
15. Bewley, C. A. (2008) Illuminating the switch in influenza viruses Nat. Biotechnol. 26, 60-62
16. 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
17. 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
18. R Development Core Team (2012) R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna.
19. Lewis, I. A., Schommer, S. C., and Markley, J. L. (2009) rNMR: Open source software for identifying and quantifying metabolites in NMR spectra Magn. Reson. Chem. 47 (Suppl. 1) S123-S126
20. Sarkar, D. (2008) Lattice: Multivariate Data Visualization with R, Springer, New York.
21. Neuhaus, D. and Williamson, M. (1989) The Nuclear Overhauser Effect in Structural and Conformational Analysis, VHC Publishers Inc., New York.
22. Angulo, J., Hricovini, M., Gairi, M., Guerrini, M., de Paz, J. L., Ojeda, R., Martin-Lomas, M., and Nieto, P. M. (2005) Dynamic properties of biologically active synthetic heparin-like hexasaccharides Glycobiology 15, 1008-1015
23. Hricovini, M. and Torri, G. (1995) Dynamics in aqueous solutions of the pentasaccharide corresponding to the binding site of heparin for antithrombin III studied by NMR relaxation measurements Carbohydr. Res. 268, 159-175
24. Poveda, A., Martin-Pastor, M., Bernabe, M., Leal, J. A., and Jimenez-Barbero, J. (1998) Solution conformation and dynamics of a fungal cell wall polysaccharide isolated from Microsporum gypseum Glycoconjugate J. 15, 309-321
25. Woods Group (2005-2012) GLYCAM Web.
26. Kirschner, K. N., Yongye, A. B., Tschampel, S. M., Gonzalez-Outeirino, 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. Jakalian, A., Jack, D. B., and Bayly, C. I. (2002) Fast, efficient generation of high-quality atomic charges. AM1-BCC model: II. Parameterization and validation J. Comput. Chem. 23, 1623-1641
28. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926
29. Case, D. A., Darden, T. A., Cheatham, T. E., III, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B. P., Wang, B., Hayik, S., Roitberg, A., Seabra, G., Kolossvai, I., Wong, K. F., Paesani, F., Vanicek, J., Liu, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Cai, Q., Ye, J., Wang, J., Hsieh, M.-J., Cui, G., Roe, D. R., Mathews, D. H., Seetin, M. G., Sagui, C., Babin, V., Luchko, T., Gusarov, S., Kovalenko, A., and Kollman, P. A. (2010) AMBER 11, University of California, San Francisco.
30. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kale, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD J. Comput. Chem. 26, 1781-1802
31. Grant, B. J., Rodrigues, A. P., ElSawy, K. M., McCammon, J. A., and Caves, L. S. (2006) Bio3d: An R package for the comparative analysis of protein structures Bioinformatics 22, 2695-2696
32. Martin-Pastor, M. (2005) NOEPROM.
33. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual molecular dynamics J. Mol. Graphics 14, 27-38
34. Schulz, R. (2009) http://www.ks.uiuc.edu/Research/vmd/mailing-list/vmd-l/ att-15365/PorcupinePlot.tcl.
35. Amadei, A., Linssen, A. B., and Berendsen, H. J. (1993) Essential dynamics of proteins Proteins 17, 412-425
36. Turner, C. J., Connolly, P. J., and Stern, A. S. (1999) Artifacts in sensitivity-enhanced HSQC J. Magn. Reson. 137, 281-284
37. Poppe, L. and Van Halbeek, H. (1992) The rigidity of sucrose: Just an illusion? J. Am. Chem. Soc. 114, 1092-1094
38. Poppe, L., van Halbeek, H., Acquotti, D., and Sonnino, S. (1994) Carbohydrate dynamics at a micellar surface: GD1a headgroup transformations revealed by NMR spectroscopy Biophys. J. 66, 1642-1652
39. Raab, M. and Tvaroska, I. (2011) The binding properties of the H5N1 influenza virus neuraminidase as inferred from molecular modeling J. Mol. Model. 17, 1445-1456
40. Sabesan, S., Bock, K., and Paulson, J. C. (1991) Conformational analysis of sialyloligosaccharides Carbohydr. Res. 218, 27-54
41. Frank, M., Lutteke, T., and von der Lieth, C. W. (2007) GlycoMapsDB: A database of the accessible conformational space of glycosidic linkages Nucleic Acids Res. 35, 287-290
42. Tvaroška, I., Hricovíni, M., and Petráková, E. (1989) An attempt to derive a new Karplus-type equation of vicinal proton-carbon coupling constants for C-O-C-H segments of bonded atoms Carbohydr. Res. 189, 359-362
43. Kitao, A. and Go, N. (1999) Investigating protein dynamics in collective coordinate space Curr. Opin. Struct. Biol. 9, 164-169
44. Gotsev, M. G. and Ivanov, P. M. (2009) Molecular dynamics of large-ring cyclodextrins: Principal component analysis of the conformational interconversions J. Phys. Chem. B 113, 5752-5759
45. Poppe, L., Stuike-Prill, R., Meyer, B., and van Halbeek, H. (1992) The solution conformation of sialyl-α (2-6)-lactose studied by modern NMR techniques and Monte Carlo simulations J. Biomol. NMR 2, 109-136
46. Liu, J., Stevens, D. J., Haire, L. F., Walker, P. A., Coombs, P. J., Russell, R. J., Gamblin, S. J., and Skehel, J. J. (2009) Structures of receptor complexes formed by hemagglutinins from the Asian Influenza pandemic of 1957 Proc. Natl. Acad. Sci. U.S.A. 106, 17175-17180