Theoretical investigation on the binding specificity of sialyldisaccharides with hemagglutinins of influenza A virus by molecular dynamics simulations

Journal of Biological Chemistry

Volumn 287, Issue 41, 2012, Pages 34547-34557

  Priyadarzini, Thanu R K ^a   Selvin, Jeyasigamani F A ^a   Gromiha, M Michael ^b   Fukui, Kazuhiko ^c   Veluraja, Kasinadar ^a  

^a MANONMANIAM SUNDARANAR UNIVERSITY   (India)

^b INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING MODES; BINDING SPECIFICITIES; CELL SURFACES; DYNAMIC BEHAVIORS; ENERGY DIFFERENCES; HYDROGEN BONDING INTERACTIONS; INFECTION PROCESS; INFLUENZA A; INFLUENZA A VIRUS; INFLUENZA VIRUS; MOLECULAR DYNAMICS SIMULATIONS; PAIR INTERACTION ENERGIES; STRUCTURAL STABILIZATION; SURFACE AREA; THEORETICAL INVESTIGATIONS; TORSIONAL ANGLE;

HYDROGEN BONDS; MOLECULAR DYNAMICS; VIRUSES;

BINDING ENERGY;

INFLUENZA VIRUS HEMAGGLUTININ; N ACETYLNEURAMINIC ACID; N ACETYLNEURAMINIC ACID ALPHA; UNCLASSIFIED DRUG; WATER;

ARTICLE; BINDING SITE; CONFORMATION; CONTROLLED STUDY; HYDROGEN BOND; INFLUENZA VIRUS A; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

DISACCHARIDES; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS; MOLECULAR DYNAMICS SIMULATION;

EID: 84867271852     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.357061     Document Type: Article

References (58)

1. Kash, J. C., Goodman, A. G., Korth, M. J., and Katze, M. G. (2006) Hijacking of the host-cell response and translational control during influenza virus infection. Virus Res. 119, 111-120 (Pubitemid 43765975)
2. Skehel, J. J., and Wiley, D. C. (1995) Influenza viruses and cell membranes. Am. J. Respir. Crit. Care Med. 152, S13-S15
3. Tobita, K. (1997) Classification and nomenclature of influenza viruses. Nihon. Rinsho. 55, 2512-2514
4. Cheung, T. K., and Poon, L. L. (2007) Biology of influenza A virus. Ann. N.Y. Acad. Sci. 1102, 1-25 (Pubitemid 47084906)
5. Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M., and Kawaoka, Y. (1992) Evolution and ecology of influenza A viruses. Microbiol. Rev. 56, 152-179
6. Subbarao, K., and Joseph, T. (2007) Scientific barriers to developing vaccines against avian influenza viruses. Nat. Rev. Immunol. 7, 267-278 (Pubitemid 46480953)
7. Fouchier, R. A., Munster, V., Wallensten, A., Bestebroer, T. M., Herfst, S., Smith, D., Rimmelzwaan, G. F., Olsen, B., and Osterhaus, A. D. (2005) Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 79, 2814-2822 (Pubitemid 40270559)
8. Lau, L. T., Banks, J., Aherne, R., Brown, I. H., Dillon, N., Collins, R. A., Chan, K. Y., Fung, Y. W., Xing, J., and Yu, A. C. (2004) Nucleic acid sequence-based amplification methods to detect avian influenza virus. Biochem. Biophys. Res. Commun. 313, 336-342 (Pubitemid 37543590)
9. Zaki, S. R., and Goldsmith, C. S. (1999) Pathologic features of filovirus infections in humans. Curr. Top. Microbiol. Immunol. 235, 97-116
10. Jo, S. K., Kim, H. S., Cho, S. W., and Seo, S. H. (2007) Pathogenesis and inflammatory responses of swine H1N2 influenza viruses in pigs. Virus Res. 129, 64-70 (Pubitemid 47332720)
11. Wang, Z., Mirza, A. M., Li, J., Mahon, P. J., and Iorio, R. M. (2004) An oligosaccharide at the C terminus of the F-specific domain in the stalk of the human parainfluenza virus 3 hemagglutinin-neuraminidase modulates fusion. Virus Res. 99, 177-185 (Pubitemid 38121666)
12. Schwahn, A. B., Wong, J. W., and Downard, K. M. (2009) Subtyping of the influenza virus by high resolution mass spectrometry. Anal. Chem. 81, 3500-3506
13. Kaverin, N. V., Matrosovich, M. N., Gambaryan, A. S., Rudneva, I. A., Shilov, A. A., Varich, N. L., Makarova, N. V., Kropotkina, E. A., and Sinitsin, B. V. (2000) Intergenic HA-NA interactions in influenza A virus. Post-reassortment substitutions of charged amino acid in the hemagglutinin of different subtypes. Virus Res. 66, 123-129 (Pubitemid 30139485)
14. 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 (Pubitemid 27244459)
15. Ghedin, E., Sengamalay, N. A., Shumway, M., Zaborsky, J., Feldblyum, T., Subbu, V., Spiro, D. J., Sitz, J., Koo, H., Bolotov, P., Dernovoy, D., Tatusova, T., Bao, Y., St George, K., Taylor, J., Lipman, D. J., Fraser, C. M., Taubenberger, J. K., and Salzberg, S. L. (2005) Large scale sequencing of human influenza reveals the dynamic nature of viral genome evolution. Nature 437, 1162-1166 (Pubitemid 41509354)
16. Dawson, E. D., Moore, C. L., Dankbar, D. M., Mehlmann, M., Townsend, M. B., Smagala, J. A., Smith, C. B., Cox, N. J., Kuchta, R. D., and Rowlen, K. L. (2007) Identification of A/H5N1 influenza viruses using a single gene diagnostic microarray. Anal. Chem. 79, 378-384 (Pubitemid 46095072)
17. Lekcharoensuk, P., Nanakorn, J., Wajjwalku, W., Webby, R., and Chumsing, W. (2010) First whole genome characterization of swine influenza virus subtype H3N2 in Thailand. Vet. Microbiol. 145, 230-244
18. Steinhauer, D. A. (1999) Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 258, 1-20
19. Gottschalk, A (1959) in The Viruses (Burnet, F. M., and Stanley, W. M., eds) Vol. 3, pp. 51-61, Academic Press, New York
20. Wang, R., Soll, L., Dugan, V., Runstadler, J., Happ, G., Slemons, R. D., and Taubenberger, J. K. (2008) Examining the hemagglutinin subtype diversity among wild duck-origin influenza A viruses using ethanol-fixed cloacal swabs and a novel RT-PCR method. Virology 375, 182-189
21. Munster, V. J., Baas, C., Lexmond, P., Waldenstrom, J., Wallensten, A., Fransson, T., Rimmelzwaan, G. F., Beyer, W. E., Schutten, M., Olsen, B., Osterhaus, A. D., and Fouchier, R. A. (2007) Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog. 3, 3630-3638
22. Yu, H., Hua, R. H., Wei, T. C., Zhou, Y. J., Tian, Z. J., Li, G. X., Liu, T. Q., and Tong, G. Z. (2008) Isolation and genetic characterization of avian origin H9N2 influenza viruses from pigs in China. Vet. Microbiol. 131, 82-92
23. Johnson, N. P., and Mueller, J. (2002) Updating the accounts. Global mortality of the 1918-1920 "Spanish" influenza pandemic. Bull. Hist. Med. 76, 105-115
24. Taubenberger, J. K., and Morens, D. M. (2006) 1918 influenza. The mother of all pandemics. Emerg. Infect. Dis. 12, 15-22 (Pubitemid 43143529)
25. Ha, Y., Stevens, D. J., Skehel, J. J., and Wiley, D. C. (2002) H5 avian and H9 swine influenza virus hemagglutinin structures. Possible origin of influenza subtypes. EMBO J. 21, 865-875 (Pubitemid 34206160)
26. Kawaoka, Y., Krauss, S., and Webster, R. G. (1989) Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J. Virol. 63, 4603-4608 (Pubitemid 19257834)
27. Couceiro, J. N., 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 (Pubitemid 23235070)
28. Günther, I., Glatthaar, B., Döller, G., and Garten, W. (1993) An H1 hemagglutinin of a human influenza A virus with a carbohydrate-modulated receptor binding site and an unusual cleavage site. Virus Res. 27, 147-160 (Pubitemid 23055737)
29. Suzuki, Y., Ito, T., Suzuki, T., Miyamoto, D., Hidari, K. I. P. J., Guo, C. T., Kida, H., Webster, R. G., Chambers, T. M., and Kawaoka, Y. (2001) Sialyl sugar chains as receptors and determinants of host range of influenza A viruses. Int. Congr. Ser. 1219, 521-525
30. Connor, R. J., Kawaoka, Y., Webster, R. G., and Paulson, J. C. (1994) Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205, 17-23 (Pubitemid 24360586)
31. Brossmer, R., Isecke, R., and Herrler, G. (1993) A sialic acid analogue acting as a receptor determinant for binding but not for infection by influenza C virus. FEBS Lett. 323, 96-98 (Pubitemid 23158340)
32. Guo, C. T., Takahashi, N., Yagi, H., Kato, K., Takahashi, T., Yi, S. Q., Chen, Y., Ito, T., Otsuki, K., Kida, H., Kawaoka, Y., Hidari, K. I., Miyamoto, D., Suzuki, T., and Suzuki, Y. (2007) The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors. Glycobiology 17, 713-724 (Pubitemid 47050660)
33. 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 (Pubitemid 43012153)
34. Baum, L. G., and Paulson, J. C. (1990) Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem. Suppl. 40, 35-38
35. Zimmer, G., Reuter, G., and Schauer, R. (1992) Use of influenza C virus for detection of 9-O-acetylated sialic acids on immobilized glycoconjugates by esterase activity. Eur. J. Biochem. 204, 209-215
36. Rogers, G. N., and Paulson, J. C. (1983) Receptor determinants of human and animal influenza virus isolates. Differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127, 361-373 (Pubitemid 13026446)
37. Rogers, G. N., Daniels, R. S., Skehel, J. J., Wiley, D. C., Wang, X. F., Higa, H. H., and Paulson, J. C. (1985) Host-mediated selection of influenza virus receptor variants. Sialic acid-α2,6Gal-specific clones of A/duck/Ukraine/1/63 revert to sialic acid-α2,3Gal-specific wild type in ovo. J. Biol. Chem. 260, 7362-7367 (Pubitemid 15063010)
38. Ledesma, J., Pozo, F., Ruiz, M. P., Navarro, J. M., Piñeiro, L., Montes, M., Castro, S. P., Fernández, J. S., Costa, J. G., Fernández, M., Galán, J. C., Cuevas, M. T., Casas, I., Breña, P. P., and Spanish Influenza Surveillance System (SISS) (2011) Substitutions in position 222 of hemagglutinin of pandemic influenza A (H1N1) 2009 viruses in Spain. J. Clin. Virol. 51, 75-78
39. 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 hemagglutinin change receptor binding specificity. Nature 304, 76-78 (Pubitemid 13063111)
40. Glaser, L., Stevens, J., Zamarin, D., Wilson, I. A., García- Sastre, A., Tumpey, T. M., Basler, C. F., Taubenberger, J. K., and Palese, P. (2005) A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity. J. Virol. 79, 11533-11536 (Pubitemid 41170697)
41. Veluraja, K., Selvin, J. F., Venkateshwari, S., and Priyadarzini, T. R. (2010) 3DSDSCAR. A three-dimensional structural database for sialic acid-containing carbohydrates through molecular dynamics simulation. Carbohydr. Res. 345, 2030-2037
42. Veluraja, K., and Rao, V. S. (1980) Theoretical studies on the conformation of β-D-N-acetylneuraminic acid (sialic acid). Biochim. Biophys. Acta 630, 442-446
43. Priyadarzini, T. R., Subashini, B., Selvin, J. F., and Veluraja, K. (2012) Molecular dynamics simulation and quantum mechanical calculations on α-D-N-acetylneuraminic acid. Carbohydr. Res. 351, 93-97
44. Vasudevan, S. V., and Balaji, P. V. (2002) Molecular dynamics simulations of α2 → 8-linked disialoside. Conformational analysis and implications for binding to proteins. Biopolymers 63, 168-180 (Pubitemid 34150363)
45. Veluraja, K., and Seethalakshmi, A. N. (2008) Dynamics of sialyl Lewis(a) in aqueous solution and prediction of the structure of the sialyl Lewis(a)-SelectinE complex. J. Theor. Biol. 252, 15-23
46. Arnott, S., and Scott, W. E. (1972) Accurate x-ray diffraction analysis of fibrous polysaccharides containing pyranose rings. Part I. The linked atom approach. J. Chem. Soc. Perkin Trans. 1 2, 324-335
47. 2O. Acta Crystallogr. B 29, 1881-1886
48. 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 (Pubitemid 38374870)
49. 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 (Pubitemid 36579216)
50. 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 (Pubitemid 32928703)
51. Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., and Case, D. A. (2004) Development and testing of a general amber force field. J. Comput. Chem. 25, 1157-1174
52. Wang, J., Cieplak, P., and Kollman, P. (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules. J. Comput. Chem. 21, 1049-1074
53. Case, D. A., Darden, T., Cheatham, T. E., Simmerling, C., Wang, J., Duke, R. E., Luo, R., Merz, K. M., Pearlman, D. A., Crowley, M., Walker, R., Zhang, W., Wang, B., Hayik, S., Roitberg, A., Seabra, G., Wong, K., Paesani, F., Wu, X., Brozell, S., Tusi, V., Gohlke, H., Yang, L., Tan, C., Mongan, J., Hornak, V., Cui, G., Beroza, P., Mathews, D. H., Schafmeister, C., Ross, W. S., and Kollman, P. A. (2006) AMBER, Version 9, University of California, San Franscisco
54. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD. Visual molecular dynamics. J. Mol. Graph. 14, 33-38
55. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (Pubitemid 43078511)
56. Kraulis, P. J. (1991) MOLSCRIPT. A program to produce both detailed and schematic plots of protein structures J. Appl. Crystallogr. 24, 946-950
57. Nunthaboot, N., Rungrotmongkol, T., Malaisree, M., Kaiyawet, N., Decha, P., Sompornpisut, P., Poovorawan, Y., and Hannongbua, S. (2010) Evolution of human receptor binding affinity of H1N1 hemagglutinins from 1918 to 2009 pandemic influenza A virus. J. Chem. Inf. Model. 50, 1410-1417
58. Nadtanet, N., Rungrotmongkol, T., Malarisree, M., Decha, P., Kaiyawet, N., Intharthep, P., Sompornpisut, P., Poovorawan, Y., and Hannongbua, S. (2010) Molecular insights into receptor binding to 2009 H1N1 influenza A hemagglutinin. Monatsh. Chem. 141, 801-807