Hemagglutinin 222D/G polymorphism facilitates fast intra-host evolution of pandemic (H1N1) 2009 influenza A viruses

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Seidel, Nora ^a   Sauerbrei, Andreas ^a   Wutzler, Peter ^a   Schmidtke, Michaela ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ; NEUTRALIZING ANTIBODY; HEMAGGLUTININ, HUMAN INFLUENZA A VIRUS; INFLUENZA VIRUS HEMAGGLUTININ; SIALIC ACID DERIVATIVE; VIRUS ANTIBODY; VIRUS RECEPTOR;

2009 H1N1 INFLUENZA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CLINICAL FEATURE; DISEASE COURSE; DISEASE SEVERITY; DNA POLYMORPHISM; FEMALE; GENE SEQUENCE; GENETIC VARIABILITY; HA D222 GENE; HA G222 GENE; INFLUENZA A (H1N1); MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PNEUMONIA; RECEPTOR BINDING; SEQUENCE ANALYSIS; TROPISM; VIRUS GENE; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS TITRATION; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CHEMISTRY; GENE EXPRESSION; GENETIC POLYMORPHISM; GENETICS; HOST RANGE; HUMAN; IMMUNE EVASION; IMMUNOLOGY; INFLUENZA VIRUS A H1N1; LUNG; MOLECULAR EVOLUTION; MOLECULAR GENETICS; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; TRACHEA; VIRAL TROPISM; VIROLOGY;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BASE SEQUENCE; EVOLUTION, MOLECULAR; GENE EXPRESSION; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HOST SPECIFICITY; HUMANS; IMMUNE EVASION; INFLUENZA A VIRUS, H1N1 SUBTYPE; LUNG; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; ORTHOMYXOVIRIDAE INFECTIONS; POLYMORPHISM, GENETIC; RECEPTORS, VIRUS; SIALIC ACIDS; TRACHEA; VIRAL TROPISM;

EID: 84929941132     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104233     Document Type: Article

References (51)

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. Dawood FS, Jain S, Finelli L, Shaw MW, Lindstrom S, et al. (2009) Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 360: 2605-2615.
3. Louie JK, Acosta M, Winter K, Jean C, Gavali S, et al. (2009) Factors associated with death or hospitalization due to pandemic 2009 influenza A(H1N1) infection in California. JAMA 302: 1896-1902.
4. Louie JK, Acosta M, Jamieson DJ, Honein MA (2010) Severe 2009 H1N1 influenza in pregnant and postpartum women in California. N Engl J Med 362: 27-35.
5. Jamieson DJ, Honein MA, Rasmussen SA, Williams JL, Swerdlow DL, et al. (2009) H1N1 2009 influenza virus infection during pregnancy in the USA. Lancet 374: 451-458.
6. Jain S, Kamimoto L, Bramley AM, Schmitz AM, Benoit SR, et al. (2009) Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N Engl J Med 361: 1935-1944.
7. Chen H, Wen X, To KK, Wang P, Tse H, et al. (2010) Quasispecies of the D225G substitution in the hemagglutinin of pandemic influenza A(H1N1) 2009 virus from patients with severe disease in Hong Kong, China. J Infect Dis 201: 1517-1521.
8. Kilander A, Rykkvin R, Dudman SG, Hungnes O (2010) Observed association between the HA1 mutation D222G in the 2009 pandemic influenza A(H1N1) virus and severe clinical outcome, Norway 2009-2010. Euro Surveill 15.
9. Mak GC, Au KW, Tai LS, Chuang KC, Cheng KC, et al. (2010) Association of D222G substitution in haemagglutinin of 2009 pandemic influenza A (H1N1) with severe disease. Euro Surveill 15.
10. Miller RR, MacLean AR, Gunson RN, Carman WF (2010) Occurrence of haemagglutinin mutation D222G in pandemic influenza A(H1N1) infected patients in the West of Scotland, United Kingdom, 2009-10. Euro Surveill 15.
11. Vazquez-Perez JA, Isa P, Kobasa D, Ormsby CE, Ramirez-Gonzalez JE, et al. (2013) A (H1N1) pdm09 HA D222 variants associated with severity and mortality in patients during a second wave in Mexico. Virol J 10: 41.
12. Melidou A, Gioula G, Exindari M, Chatzidimitriou D, Diza E, et al. (2010) Molecular and phylogenetic analysis of the haemagglutinin gene of pandemic influenza H1N1 2009 viruses associated with severe and fatal infections. Virus Res 151: 192-199.
13. Wang B, Dwyer DE, Soedjono M, Shi H, Matlho K, et al. (2011) Evidence of the circulation of pandemic influenza (H1N1) 2009 with D222D/G/N/S hemagglutinin polymorphisms during the first wave of the 2009 influenza pandemic. J Clin Virol 52: 304-306.
14. WHO (2010) Preliminary review of D222G amino acid substitution in the haemagglutinin of pandemic influenza A (H1N1) 2009 viruses. Wkly Epidemiol Rec 85: 21-22.
15. Xu L, Bao L, Lv Q, Deng W, Ma Y, et al. (2010) A single-amino-acid substitution in the HA protein changes the replication and pathogenicity of the 2009 pandemic A (H1N1) influenza viruses in vitro and in vivo. Virol J 7: 325.
16. Wedde M, Wahlisch S, Wolff T, Schweiger B (2013) Predominance of HA-222D/G polymorphism in influenza A(H1N1)pdm09 viruses associated with fatal and severe outcomes recently circulating in Germany. PLoS One 8: e57059.
17. Ilyushina NA, Khalenkov AM, Seiler JP, Forrest HL, Bovin NV, et al. (2010) Adaptation of pandemic H1N1 influenza viruses in mice. J Virol 84: 8607-8616.
18. Sakabe S, Ozawa M, Takano R, Iwastuki-Horimoto K, Kawaoka Y (2011) Mutations in PA, NP, and HA of a pandemic (H1N1) 2009 influenza virus contribute to its adaptation to mice. Virus Res 158: 124-129.
19. Seyer R, Hrincius ER, Ritzel D, Abt M, Mellmann A, et al. (2012) Synergistic adaptive mutations in the hemagglutinin and polymerase acidic protein lead to increased virulence of pandemic 2009 H1N1 influenza A virus in mice. J Infect Dis 205: 262-271.
20. Zheng B, Chan KH, Zhang AJ, Zhou J, Chan CC, et al. (2010) D225G mutation in hemagglutinin of pandemic influenza H1N1 (2009) virus enhances virulence in mice. Exp Biol Med (Maywood) 235: 981-988.
21. Abed Y, Pizzorno A, Hamelin ME, Leung A, Joubert P, et al. (2011) The 2009 pandemic H1N1 D222G hemagglutinin mutation alters receptor specificity and increases virulence in mice but not in ferrets. J Infect Dis 204: 1008-1016.
22. Chutinimitkul S, Herfst S, Steel J, Lowen AC, Ye J, et al. (2010) Virulence-associated substitution D222G in the hemagglutinin of 2009 pandemic influenza A(H1N1) virus affects receptor binding. J Virol 84: 11802-11813.
23. Igarashi M, Ito K, Yoshida R, Tomabechi D, Kida H, et al. (2010) Predicting the antigenic structure of the pandemic (H1N1) 2009 influenza virus hemagglutinin. PLoS One 5: e8553.
24. Weis W, Brown JH, Cusack S, Paulson JC, Skehel JJ, et al. (1988) Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 333: 426-431.
25. Childs RA, Palma AS, Wharton S, Matrosovich T, Liu Y, et al. (2009) Receptor-binding specificity of pandemic influenza A (H1N1) 2009 virus determined by carbohydrate microarray. Nat Biotechnol 27: 797-799.
26. Liu Y, Childs RA, Matrosovich T, Wharton S, Palma AS, et al. (2010) Altered receptor specificity and cell tropism of D222G hemagglutinin mutants isolated from fatal cases of pandemic A(H1N1) 2009 influenza virus. J Virol 84: 12069-12074.
27. Takemae N, Ruttanapumma R, Parchariyanon S, Yoneyama S, Hayashi T, et al. (2010) Alterations in receptor-binding properties of swine influenza viruses of the H1 subtype after isolation in embryonated chicken eggs. J Gen Virol 91: 938-948.
28. Hamelin ME, Baz M, Abed Y, Couture C, Joubert P, et al. (2010) Oseltamivir-resistant pandemic A/H1N1 virus is as virulent as its wild-type counterpart in mice and ferrets. PLoS Pathog 6: e1001015.
29. Manchanda H, Seidel N, Krumbholz A, Sauerbrei A, Schmidtke M, et al. (2014) Within-host influenza dynamics: A small-scale mathematical modeling approach. Biosystems 118: 51-59.
30. Kirchmair J, Rollinger JM, Liedl KR, Seidel N, Krumbholz A, et al. (2011) Novel neuraminidase inhibitors: identification, biological evaluation and investigations of the binding mode. Future Med Chem 3: 437-450.
31. Reed LJ, Muench H (1938) A simple method of estimating fifty per cent endpoints. Am J Hyg 27: 493-497.
32. Bauer K, Richter M, Wutzler P, Schmidtke M (2009) Different neuraminidase inhibitor susceptibilities of human H1N1, H1N2, and H3N2 influenza A viruses isolated in Germany from 2001 to 2005/2006. Antiviral Res 82: 34-41.
33. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR (2001) Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146: 2275-2289. (Pubitemid 34682391)
34. Bauer K, Durrwald R, Schlegel M, Pfarr K, Topf D, et al. (2012) Neuraminidase inhibitor susceptibility of swine influenza A viruses isolated in Germany between 1981 and 2008. Med Microbiol Immunol 201: 61-72.
35. McKimm-Breschkin JL, Williams J, Barrett S, Jachno K, McDonald M, et al. (2013) Reduced susceptibility to all neuraminidase inhibitors of influenza H1N1 viruses with haemagglutinin mutations and mutations in non-conserved residues of the neuraminidase. J Antimicrob Chemother 68: 2210-2221.
36. Uraki R, Kiso M, Shinya K, Goto H, Takano R, et al. (2013) Virulence determinants of pandemic A(H1N1)2009 influenza virus in a mouse model. J Virol 87: 2226-2233.
37. Medeiros R, Escriou N, Naffakh N, Manuguerra JC, van der Werf S (2001) Hemagglutinin residues of recent human A(H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes. Virology 289: 74-85. (Pubitemid 33016239)
38. Wagner R, Matrosovich M, Klenk HD (2002) Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev Med Virol 12: 159-166. (Pubitemid 34516947)
39. Hayden FG, Treanor JJ, Fritz RS, Lobo M, Betts RF, et al. (1999) Use of the oral neuraminidase inhibitor oseltamivir in experimental human influenza - Randomized controlled trials for prevention and treatment. Jama-Journal of the American Medical Association 282: 1240-1246. (Pubitemid 29468495)
40. Corcioli F, Arvia R, Pierucci F, Clausi V, Bonizzoli M, et al. (2014) HA222 polymorphism in Influenza A(H1N1) 2009 isolates from Intensive Care Units and ambulatory patients during three influenza seasons. Virus Res 180: 39-42.
41. Levine M, Sheu TG, Gubareva LV, Mishin VP (2011) Detection of hemagglutinin variants of the pandemic influenza A (H1N1) 2009 virus by pyrosequencing. J Clin Microbiol 49: 1307-1312.
42. Selleri M, Piralla A, Rozera G, Giombini E, Bartolini B, et al. (2013) Detection of haemagglutinin D222 polymorphisms in influenza A(H1N1)pdm09- infected patients by ultra-deep pyrosequencing. Clin Microbiol Infect 19: 668-673.
43. Domingo E, Sheldon J, Perales C (2012) Viral quasispecies evolution. Microbiol Mol Biol Rev 76: 159-216.
44. Nguyen HT, Trujillo AA, Sheu TG, Levine M, Mishin VP, et al. (2012) Analysis of influenza viruses from patients clinically suspected of infection with an oseltamivir resistant virus during the 2009 pandemic in the United States. Antiviral Res 93: 381-386.
45. Ye J, Sorrell EM, Cai Y, Shao H, Xu K, et al. (2010) Variations in the hemagglutinin of the 2009 H1N1 pandemic virus: potential for strains with altered virulence phenotype? PLoS Pathog 6: e1001145.
46. Ning ZY, Luo MY, Qi WB, Yu B, Jiao PR, et al. (2009) Detection of expression of influenza virus receptors in tissues of BALB/c mice by histochemistry. Vet Res Commun 33: 895-903.
47. Wyde PR, Couch RB, Mackler BF, Cate TR, Levy BM (1977) Effects of low- and high-passage influenza virus infection in normal and nude mice. Infect Immun 15: 221-229. (Pubitemid 8022710)
48. Xu L, Bao L, Li F, Lv Q, Ma Y, et al. (2011) Adaption of seasonal H1N1 influenza virus in mice. PLoS One 6: e28901.
49. Brown EG, Liu H, Kit LC, Baird S, Nesrallah M (2001) Pattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: identification of functional themes. Proc Natl Acad Sci U S A 98: 6883-6888. (Pubitemid 32538311)
50. 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.
51. Hauge S, Madhun A, Cox RJ, Haaheim LR (2007) Quality and kinetics of the antibody response in mice after three different low-dose influenza virus vaccination strategies. Clin Vaccine Immunol 14: 978-983.