The roles of hemagglutinin Phe-95 in receptor binding and pathogenicity of influenza B virus

Virology

Volumn 450-451, Issue , 2014, Pages 71-83

  Ni, Fengyun ^a,b   Nnadi Mbawuike, Innocent ^a   Kondrashkina, Elena ^c   Wang, Qinghua ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Rice University   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Hemagglutinin; Host range; Influenza virus; Pathogenicity; Receptor binding affinity

Indexed keywords

CELL SURFACE RECEPTOR; HEMAGGLUTININ; PHENYLALANINE; TYROSINE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; CRYSTALLIZATION; GENE MUTATION; GLYCOSYLATION; HEMAGGLUTINATION; HUMAN; HUMAN CELL; HYDROGEN BOND; INFLUENZA VIRUS B; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PURIFICATION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS;

HEMAGGLUTININ; HOST RANGE; INFLUENZA VIRUS; PATHOGENICITY; RECEPTOR-BINDING AFFINITY;

AMINO ACID MOTIFS; ANIMALS; FEMALE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; INFLUENZA B VIRUS; MICE, INBRED BALB C; MODELS, MOLECULAR; PHENYLALANINE; PROTEIN BINDING; RECEPTORS, VIRUS; VIRULENCE;

EID: 84890887255     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.11.038     Document Type: Article

References (66)

1. Adams P.D., Afonine P.V., Bunkoczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., McCoy A.J., Moriarty N.W., Oeffner R., Read R.J., Richardson D.C., Richardson J.S., Terwilliger T.C., Zwart P.H. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66(Pt 2):213-221.
2. Blasco R., Moss B. Selection of recombinant vaccinia viruses on the basis of plaque formation. Gene 1995, 158(2):157-162.
3. 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., Steinhauer D.A. Analysis of influenza virus hemagglutinin receptor binding mutants with limited receptor recognition properties and conditional replication characteristics. J. Virol. 2011, 85(23):12387-12398.
4. Brass A.L., Huang I.C., Benita Y., John S.P., Krishnan M.N., Feeley E.M., Ryan B.J., Weyer J.L., van der Weyden L., Fikrig E., Adams D.J., Xavier R.J., Farzan M., Elledge S.J. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009, 139(7):1243-1254.
5. Chen J.M., Guo Y.J., Wu K.Y., Guo J.F., Wang M., Dong J., Zhang Y., Li Z., Shu Y.L. Exploration of the emergence of the Victoria lineage of influenza B virus. Arch. Virol. 2007, 152(2):415-422.
6. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60(Pt 12 Pt 1):2126-2132.
7. Fouchier R.A., Munster V., Wallensten A., Bestebroer T.M., Herfst S., Smith D., Rimmelzwaan G.F., Olsen B., Osterhaus A.D. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 2005, 79(5):2814-2822.
8. Gambaryan A.S., Robertson J.S., Matrosovich M.N. Effects of egg-adaptation on the receptor-binding properties of human influenza A and B viruses. Virology 1999, 258(2):232-239.
9. Gamblin S.J., Skehel J.J. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J. Biol. Chem. 2010, 285(37):28403-28409.
10. Govorkova E.A., Matrosovich M.N., Tuzikov A.B., Bovin N.V., Gerdil C., Fanget B., Webster R.G. Selection of receptor-binding variants of human influenza A and B viruses in baby hamster kidney cells. Virology 1999, 262(1):31-38.
11. Govorkova E.A., Murti G., Meignier B., de Taisne C., Webster R.G. African green monkey kidney (Vero) cells provide an alternative host cell system for influenza A and B viruses. J. Virol. 1996, 70(8):5519-5524.
12. Hai R., Garcia-Sastre A., Swayne D.E., Palese P. A reassortment-incompetent live attenuated influenza virus vaccine for protection against pandemic virus strains. J. Virol. 2011, 85(14):6832-6843.
13. Hao L., Sakurai A., Watanabe T., Sorensen E., Nidom C.A., Newton M.A., Ahlquist P., Kawaoka Y. Drosophila RNAi screen identifies host genes important for influenza virus replication. Nature 2008, 454(7206):890-893.
14. Hatta M., Kawaoka Y. The NB protein of influenza B virus is not necessary for virus replication in vitro. J. Virol. 2003, 77(10):6050-6054.
15. Hensley S.E., Das S.R., Bailey A.L., Schmidt L.M., Hickman H.D., Jayaraman A., Viswanathan K., Raman R., Sasisekharan R., Bennink J.R., Yewdell J.W. Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 2009, 326(5953):734-736.
16. Ikonen N., Pyhala R., Axelin T., Kleemola M., Korpela H. Reappearance of influenza B/Victoria/2/87-lineage viruses: epidemic activity, genetic diversity and vaccination efficacy in the Finnish Defence Forces. Epidemiol. Infect. 2005, 133(2):263-271.
17. Imai M., Watanabe T., Hatta M., Das S.C., Ozawa M., Shinya K., Zhong G., Hanson A., Katsura H., Watanabe S., Li C., Kawakami E., Yamada S., Kiso M., Suzuki Y., Maher E.A., Neumann G., Kawaoka Y. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 2012, 486(7403):420-428.
18. Ito T., Suzuki Y., Mitnaul L., Vines A., Kida H., Kawaoka Y. Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology 1997, 227(2):493-499.
19. Ito T., Suzuki Y., Takada A., Kawamoto A., Otsuki K., Masuda H., Yamada M., Suzuki T., Kida H., Kawaoka Y. Differences in sialic acid-galactose linkages in the chicken egg amnion and allantois influence human influenza virus receptor specificity and variant selection. J. Virol. 1997, 71(4):3357-3362.
20. Jayaraman A., Pappas C., Raman R., Belser J.A., Viswanathan K., Shriver Z., Tumpey T.M., Sasisekharan R. A single base-pair change in 2009 H1N1 hemagglutinin increases human receptor affinity and leads to efficient airborne viral transmission in ferrets. PLoS One 2011, 6(3):e17616.
21. Karlas A., Machuy N., Shin Y., Pleissner K.P., Artarini A., Heuer D., Becker D., Khalil H., Ogilvie L.A., Hess S., Maurer A.P., Muller E., Wolff T., Rudel T., Meyer T.F. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 2010, 463(7282):818-822.
22. Konig R., Stertz S., Zhou Y., Inoue A., Hoffmann H.H., Bhattacharyya S., Alamares J.G., Tscherne D.M., Ortigoza M.B., Liang Y., Gao Q., Andrews S.E., Bandyopadhyay S., De Jesus P., Tu B.P., Pache L., Shih C., Orth A., Bonamy G., Miraglia L., Ideker T., Garcia-Sastre A., Young J.A., Palese P., Shaw M.L., Chanda S.K. Human host factors required for influenza virus replication. Nature 2010, 463(7282):813-817.
23. Li, C., Bankhead, A., 3rd, Eisfeld, A.J., Hatta, Y., Jeng, S., Chang, J.H., Aicher, L.D., Proll, S., Ellis, A.L., Law, G.L., Waters, K., Neumann, G., Katze, M.G., McWeeney, S., Kawaoka, Y., 2011. Host regulatory network response to infection with highly pathogenic H5N1 avian influenza virus. J. Virol. 85, 10955-10967.
24. Maines T.R., Jayaraman A., Belser J.A., Wadford D.A., Pappas C., Zeng H., Gustin K.M., Pearce M.B., Viswanathan K., Shriver Z.H., Raman R., Cox N.J., Sasisekharan R., Katz J.M., Tumpey T.M. Transmission and pathogenesis of swine-origin 2009A(H1N1) influenza viruses in ferrets and mice. Science 2009, 325(5939):484-487.
25. Martin J., Wharton S.A., Lin Y.P., Takemoto D.K., Skehel J.J., Wiley D.C., Steinhauer D.A. Studies of the binding properties of influenza hemagglutinin receptor- site mutants. Virology 1998, 241(1):101-111.
26. Matrosovich M.N., Gambaryan A.S., Tuzikov A.B., Byramova N.E., Mochalova L.V., Golbraikh A.A., Shenderovich M.D., Finne J., Bovin N.V. Probing of the receptor-binding sites of the H1 and H3 influenza A and influenza B virus hemagglutinins by synthetic and natural sialosides. Virology 1993, 196(1):111-121.
27. Medeiros R., Escriou N., Naffakh N., Manuguerra J.C., van der Werf S. Hemagglutinin residues of recent human A(H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes. Virology 2001, 289(1):74-85.
28. Meisner J., Szretter K.J., Bradley K.C., Langley W.A., Li Z.N., Lee B.J., Thoennes S., Martin J., Skehel J.J., Russell R.J., Katz J.M., Steinhauer D.A. Infectivity studies of influenza virus hemagglutinin receptor binding site mutants in mice. J. Virol. 2008, 82(10):5079-5083.
29. Milliken S. A delay in maturation as a cause of small plaque size with the NM strain of influenza A virus. J. Gen. Virol. 1967, 1(2):189-198.
30. Mitnaul L.J., Matrosovich M.N., Castrucci M.R., Tuzikov A.B., Bovin N.V., Kobasa D., Kawaoka Y. Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus. J. Virol. 2000, 74(13):6015-6020.
31. Nakagawa N., Kubota R., Maeda A., Nakagawa T., Okuno Y. Heterogeneity of influenza B virus strains in one epidemic season differentiated by monoclonal antibodies and nucleotide sequences. J. Clin. Microbiol. 2000, 38(9):3467-3469.
32. Nakagawa N., Kubota R., Maeda A., Okuno Y. Influenza B virus victoria group with a new glycosylation site was epidemic in Japan in the 2002-2003 season. J. Clin. Microbiol. 2004, 42(7):3295-3297.
33. Ni F., Kondrashkina E., Wang Q. Structural basis for the divergent evolution of influenza B virus hemagglutinin. Virology 2013, 446:112-122.
34. Osterhaus A.D., Rimmelzwaan G.F., Martina B.E., Bestebroer T.M., Fouchier R.A. Influenza B virus in seals. Science 2000, 288(5468):1051-1053.
35. Oxford J.S., Newman R., Corcoran T., Bootman J., Major D., Yates P., Robertson J., Schild G.C. Direct isolation in eggs of influenza A (H1N1) and B viruses with haemagglutinins of different antigenic and amino acid composition. J. Gen. Virol. 1991, 72(Pt 1):185-189.
36. Oxford J.S., Schild G.C., Corcoran T., Newman R., Major D., Robertson J., Bootman J., Higgins P., al-Nakib W., Tyrrell D.A. A host-cell-selected variant of influenza B virus with a single nucleotide substitution in HA affecting a potential glycosylation site was attenuated in virulence for volunteers. Arch. Virol. 1990, 110(1-2):37-46.
37. Pappas C., Viswanathan K., Chandrasekaran A., Raman R., Katz J.M., Sasisekharan R., Tumpey T.M. Receptor specificity and transmission of H2N2 subtype viruses isolated from the pandemic of 1957. PLoS One 2010, 5(6):e11158.
38. Robertson J.S., Bootman J.S., Nicolson C., Major D., Robertson E.W., Wood J.M. The hemagglutinin of influenza B virus present in clinical material is a single species identical to that of mammalian cell-grown virus. Virology 1990, 179(1):35-40.
39. Robertson J.S., Naeve C.W., Webster R.G., Bootman J.S., Newman R., Schild G.C. Alterations in the hemagglutinin associated with adaptation of influenza B virus to growth in eggs. Virology 1985, 143(1):166-174.
40. Saito T., Nakaya Y., Suzuki T., Ito R., Saito H., Takao S., Sahara K., Odagiri T., Murata T., Usui T., Suzuki Y., Tashiro M. Antigenic alteration of influenza B virus associated with loss of a glycosylation site due to host-cell adaptation. J. Med. Virol. 2004, 74(2):336-343.
41. Schild G.C., Oxford J.S., de Jong J.C., Webster R.G. Evidence for host-cell selection of influenza virus antigenic variants. Nature 1983, 303(5919):706-709.
42. Shapira S.D., Gat-Viks I., Shum B.O., Dricot A., de Grace M.M., Wu L., Gupta P.B., Hao T., Silver S.J., Root D.E., Hill D.E., Regev A., Hacohen N. A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell 2009, 139(7):1255-1267.
43. Shen J., Kirk B.D., Ma J., Wang Q. Diversifying selective pressure on influenza B virus hemagglutinin. J. Med. Virol. 2009, 81(1):114-124.
44. Skehel J.J., Wiley D.C. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 2000, 69:531-569.
45. Srinivasan A., Viswanathan K., Raman R., Chandrasekaran A., Raguram S., Tumpey T.M., Sasisekharan V., Sasisekharan R. Quantitative biochemical rationale for differences in transmissibility of 1918 pandemic influenza A viruses. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(8):2800-2805.
46. Steinhauer D. Influenza A virus haemagglutinin glycoproteins. Influenza: Molecular Virology 2010, 69-108. Caister Academic Press, Norfolk, UK. Q. Wang, Y.J. Tao (Eds.).
47. Stevens J., Blixt O., Glaser L., Taubenberger J.K., Palese P., Paulson J.C., Wilson I.A. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J. Mol. Biol. 2006, 355(5):1143-1155.
48. Sui B., Bamba D., Weng K., Ung H., Chang S., Van Dyke J., Goldblatt M., Duan R., Kinch M.S., Li W.B. The use of Random Homozygous Gene Perturbation to identify novel host-oriented targets for influenza. Virology 2009, 387(2):473-481.
49. Sun X., Shi Y., Lu X., He J., Gao F., Yan J., Qi J., Gao G.F. Bat-derived influenza hemagglutinin H17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Cell Rep. 2013, 3(3):769-778.
50. Suzuki Y., Matsunaga M., Matsumoto M. N-Acetylneuraminyllactosylceramide, GM3-NeuAc, a new influenza A virus receptor which mediates the adsorption-fusion process of viral infection. Binding specificity of influenza virus A/Aichi/2/68 (H3N2) to membrane-associated GM3 with different molecular species of sialic acid. J. Biol. Chem. 1985, 260(3):1362-1365.
51. Takemae N., Ruttanapumma R., Parchariyanon S., Yoneyama S., Hayashi T., Hiramatsu H., Sriwilaijaroen N., Uchida Y., Kondo S., Yagi H., Kato K., Suzuki Y., Saito T. Alterations in receptor-binding properties of swine influenza viruses of the H1 subtype after isolation in embryonated chicken eggs. J. Gen. Virol. 2010, 91(Pt 4):938-948.
52. Tang X., Chong K.T. Histopathology and growth kinetics of influenza viruses (H1N1 and H3N2) in the upper and lower airways of guinea pigs. J. Gen. Virol. 2009, 90(Pt 2):386-391.
53. Tharakaraman K., Raman R., Viswanathan K., Stebbins N.W., Jayaraman A., Krishnan A., Sasisekharan V., Sasisekharan R. Structural determinants for naturally evolving H5N1 hemagglutinin to switch its receptor specificity. Cell 2013, 153(7):1475-1485.
54. Tong S., Li Y., Rivailler P., Conrardy C., Castillo D.A., Chen L.M., Recuenco S., Ellison J.A., Davis C.T., York I.A., Turmelle A.S., Moran D., Rogers S., Shi M., Tao Y., Weil M.R., Tang K., Rowe L.A., Sammons S., Xu X., Frace M., Lindblade K.A., Cox N.J., Anderson L.J., Rupprecht C.E., Donis R.O. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(11):4269-4274.
55. Viswanathan K., Chandrasekaran A., Srinivasan A., Raman R., Sasisekharan V., Sasisekharan R. Glycans as receptors for influenza pathogenesis. Glycoconj. J. 2010, 27(6):561-570.
56. Viswanathan K., Koh X., Chandrasekaran A., Pappas C., Raman R., Srinivasan A., Shriver Z., Tumpey T.M., Sasisekharan R. Determinants of glycan receptor specificity of H2N2 influenza A virus hemagglutinin. PLoS One 2010, 5(10):e13768.
57. Wang Q. Influenza Type B virus haemagglutinin: antigenicity, receptor binding and membrane fusion. Influenza: Molecular Virology 2010, 29-52. Caister Adademic Press, Norfolk, UK. Q. Wang, Y.J. Tao (Eds.).
58. Wang Q., Cheng F., Lu M., Tian X., Ma J. Crystal structure of unliganded influenza B virus hemagglutinin. J. Virol. 2008, 82:3011-3020.
59. Wang Q., Tian X., Chen X., Ma J. Structural basis for receptor specificity of influenza B virus hemagglutinin. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(43):16874-16879.
60. Watanabe T., Watanabe S., Kawaoka Y. Cellular networks involved in the influenza virus life cycle. Cell Host Microbe 2010, 7(6):427-439.
61. Weis W., Brown J.H., Cusack S., Paulson J.C., Skehel J.J., Wiley D.C. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 1988, 333(6172):426-431.
62. WHO-MEMORANDUM A revision of the system of nomenclature for influenza viruses. Bull. World Health Organ. 1980, 58:585-591.
63. Wiley D.C., Skehel J.J. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 1987, 56:365-394.
64. Wilson I.A., Skehel J.J., Wiley D.C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3Å resolution. Nature 1981, 289(5796):366-373.
65. Yen H.L., Webster R.G. Pandemic influenza as a current threat. Curr. Top. Microbiol. Immunol. 2009, 333:3-24.
66. Zhu X., Yu W., McBride R., Li Y., Chen L.M., Donis R.O., Tong S., Paulson J.C., Wilson I.A. Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(4):1458-1463.