A Single Amino Acid in the Stalk Region of the H1N1pdm Influenza Virus HA Protein Affects Viral Fusion, Stability and Infectivity

PLoS Pathogens

Volumn 10, Issue 1, 2014, Pages

  Cotter, Christopher R ^a   Jin, Hong ^a   Chen, Zhongying ^a  

^a MEDIMMUNE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

H1N1 VIRUS HEMAGGLUTININ; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ;

AMINO ACID SUBSTITUTION; ANIMAL; CELL MEMBRANE; CHICK EMBRYO; DOG; FERRET; GENETICS; HEAT; HUMAN; INFLUENZA VIRUS A H1N1; MDCK CELL LINE; METABOLISM; MISSENSE MUTATION; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PH; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; VIRUS ENTRY; VIRUS REPLICATION;

AMINO ACID SUBSTITUTION; ANIMALS; CELL MEMBRANE; CHICK EMBRYO; DOGS; FERRETS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HOT TEMPERATURE; HUMANS; HYDROGEN-ION CONCENTRATION; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; MADIN DARBY CANINE KIDNEY CELLS; MUTATION, MISSENSE; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN STRUCTURE, TERTIARY; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 84893787458     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003831     Document Type: Article

References (37)

1. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, et al. (2009) Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325: 197-201.
2. WHO (2010) WHO global alert and response: pandemic (H1N1) 2009- update 112, weekly update.
3. Dawood FS, Iuliano AD, Reed C, Meltzer MI, Shay DK, et al. (2012) Estimated global mortality associated with the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modelling study. Lancet Infect Dis 12: 687-695.
4. Hancock K, Veguilla V, Lu X, Zhong W, Butler EN, et al. (2009) Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med 361: 1945-1952.
5. Chen Z, Wang W, Zhou H, Suguitan ALJ, Shambaugh C, et al. (2010) Generation of live attenuated novel influenza virus A/California/7/09 (H1N1) vaccines with high yield in embryonated chicken eggs. J Virol 84: 44-51.
6. Wang W, Suguitan AL Jr, Zengel J, Chen Z, Jin H, (2012) Generation of recombinant pandemic H1N1 influenza virus with the HA cleavable by bromelain and identification of the residues influencing HA bromelain cleavage. Vaccine 30: 872-878.
7. Imai M, Kawaoka Y, (2012) The role of receptor binding specificity in interspecies transmission of influenza viruses. Curr Opin Virol 2: 160-167.
8. Bullough PA, Hughson FM, Skehel JJ, Wiley DC, (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371: 37-43.
9. DuBois RM, Zaraket H, Reddivari M, Heath RJ, White SW, et al. (2011) Acid stability of the hemagglutinin protein regulates H5N1 influenza virus pathogenicity. PLoS Pathog 7: e1002398.
10. Galloway SE, Reed ML, Russell CJ, Steinhauer DA, (2013) Influenza HA subtypes demonstrate divergent phenotypes for cleavage activation and pH of fusion: implications for host range and adaptation. PLoS Pathog 9: e1003151.
11. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, et al. (2012) Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486: 420-428.
12. Koerner I, Matrosovich MN, Haller O, Staeheli P, Kochs G, (2012) Altered receptor specificity and fusion activity of the haemagglutinin contribute to high virulence of a mouse-adapted influenza A virus. J Gen Virol 93: 970-979.
13. Zaraket H, Bridges OA, Russell CJ, (2013) The pH of activation of the hemagglutinin protein regulates H5N1 influenza virus replication and pathogenesis in mice. J Virol 87: 4826-4834.
14. Barr IG, Cui L, Komadina N, Lee RT, Lin RT, et al. (2010) A new pandemic influenza A(H1N1) genetic variant predominated in the winter 2010 influenza season in Australia, New Zealand and Singapore. Euro Surveill 15: pii: 19692.
15. Ikonen N, Haanpaa M, Ronkko E, Lyytikainen O, Kuusi M, et al. (2009) Genetic diversity of the 2009 pandemic influenza A(H1N1) viruses in Finland. PLoS One 5: e13329.
16. Mak GC, Leung CK, Cheng KC, Wong KY, Lim W, (2011) Evolution of the haemagglutinin gene of the influenza A(H1N1)2009 virus isolated in Hong Kong, 2009-2011. Euro Surveill 16: pii: 19807.
17. Maurer-Stroh S, Lee RT, Eisenhaber F, Cui L, Phuah SP, et al. (2010) A new common mutation in the hemagglutinin of the 2009 (H1N1) influenza A virus. PLoS Curr 2: RRN1162.
18. Xu R, Ekiert DC, Krause JC, Hai R, Crowe JEJ, et al. (2010) Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 328: 357-360.
19. Yang H, Carney P, Stevens J, (2010) Structure and Receptor binding properties of a pandemic H1N1 virus hemagglutinin. PLoS Curr Mar 22: RRN1152.
20. Murakami S, Horimoto T, Ito M, Takano R, Katsura H, et al. (2011) Enhanced growth of influenza vaccine seed viruses in vero cells mediated by broadening the optimal pH range for virus membrane fusion. J Virol 86: 1405-1410.
21. Carr CM, Chaudhry C, Kim PS, (1997) Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc Natl Acad Sci U S A 94: 14306-14313.
22. Haywood AM, Boyer BP, (1986) Time and temperature dependence of influenza virus membrane fusion at neutral pH. J Gen Virol 67 (Pt 12) (): 2813-2817.
23. Ruigrok RW, Martin SR, Wharton SA, Skehel JJ, Bayley PM, et al. (1986) Conformational changes in the hemagglutinin of influenza virus which accompany heat-induced fusion of virus with liposomes. Virology 155: 484-497.
24. Strengell M, Ikonen N, Ziegler T, Julkunen I, (2011) Minor changes in the hemagglutinin of influenza A(H1N1)2009 virus alter its antigenic properties. PLoS One 6: e25848.
25. Steinhauer DA, Martín J, Lin YP, Wharton SA, Oldstone MB, et al. (1996) Studies using double mutants of the conformational transitions in influenza hemagglutinin required for its membrane fusion activity. Proc Natl Acad Sci U S A 93: 12873-12878.
26. Daniels RS, Downie JC, Hay AJ, Knossow M, Skehel JJ, et al. (1985) Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell 40: 431-439.
27. Giannecchini S, Campitelli L, Calzoletti L, De Marco MA, Azzi A, et al. (2006) Comparison of in vitro replication features of H7N3 influenza viruses from wild ducks and turkeys: potential implications for interspecies transmission. J Gen Virol 87: 171-175.
28. Lin YP, Wharton SA, Martín J, Skehel JJ, Wiley DC, et al. (1997) Adaptation of egg-grown and transfectant influenza viruses for growth in mammalian cells: selection of hemagglutinin mutants with elevated pH of membrane fusion. Virology 233: 402-410.
29. Reed ML, Bridges OA, Seiler P, Kim JK, Yen HL, et al. (2010) The pH of activation of the hemagglutinin protein regulates H5N1 influenza virus pathogenicity and transmissibility in ducks. J Virol 84: 1527-1535.
30. Reed ML, Yen HL, DuBois RM, Bridges OA, Salomon R, et al. (2009) Amino acid residues in the fusion peptide pocket regulate the pH of activation of the H5N1 influenza virus hemagglutinin protein. J Virol 83: 3568-3580.
31. Steinhauer DA, Wharton SA, Skehel JJ, Wiley DC, Hay AJ, (1991) Amantadine selection of a mutant influenza virus containing an acid-stable hemagglutinin glycoprotein: evidence for virus-specific regulation of the pH of glycoprotein transport vesicles. Proc Natl Acad Sci U S A 88: 11525-11529.
32. Krenn BM, Egorov A, Romanovskaya-Romanko E, Wolschek M, Nakowitsch S, et al. (2011) Single HA2 mutation increases the infectivity and immunogenicity of a live attenuated H5N1 intranasal influenza vaccine candidate lacking NS1. PLoS One 6: e18577.
33. Fukuyama S, Kawaoka Y, (2011) The pathogenesis of influenza virus infections: the contributions of virus and host factors. Curr Opin Immunol 23: 481-486.
34. Smeenk CA, Brown EG, (1994) The influenza virus variant A/FM/1/47-MA possesses single amino acid replacements in the hemagglutinin, controlling virulence, and in the matrix protein, controlling virulence as well as growth. J Virol 68: 530-534.
35. Smeenk CA, Wright KE, Burns BF, Thaker AJ, Brown EG, (1996) Mutations in the hemagglutinin and matrix genes of a virulent influenza virus variant, A/FM/1/47-MA, control different stages in pathogenesis. Virus Res 44: 79-95.
36. Suguitan ALJ, Zengel JR, Jacobson S, Gee S, Cetz J, et al. (2013) Influenza H1N1pdm-specific maternal antibodies offer limited protection against wild-type virus replication and influenced influenza vaccination in ferrets. Influenza Other Respi Viruses in press.
37. Jin H, Lu B, Zhou H, Ma C, Zhao J, et al. (2003) Multiple amino acid residues confer temperature sensitivity to human influenza virus vaccine strains (FluMist) derived from cold-adapted A/Ann Arbor/6/60. Virology 306: 18-24.