Analysis of Adaptation Mutants in the Hemagglutinin of the Influenza A(H1N1)pdm09 Virus

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Jiménez Alberto, Alicia ^a   Alvarado Facundo, Esmeralda ^a,b   Ribas Aparicio, Rosa María ^a   Castelán Vega, Juan A ^a  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUSION PEPTIDE; INFLUENZA VIRUS HEMAGGLUTININ; MUTANT PROTEIN; UNCLASSIFIED DRUG;

2009 H1N1 INFLUENZA; ADAPTATION; AMINO ACID SEQUENCE; ANTIGEN RECOGNITION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; EVOLUTION; GENETIC DISTANCE; GENETIC STABILITY; GENETIC VARIABILITY; IMMUNE EVASION; IMMUNE RESPONSE; INFLUENZA VIRUS A H1N1; LIGAND BINDING; MOLECULAR DYNAMICS; NONHUMAN; PANDEMIC; RECEPTOR BINDING; SEQUENCE ALIGNMENT; SPECIES INVASION;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BRAIN MAPPING; CASE-CONTROL STUDIES; CELL PHYSIOLOGICAL PHENOMENA; FEMALE; FLUORODEOXYGLUCOSE F18; FOLLOW-UP STUDIES; GLUCOSE; HUMANS; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; NEURAL NETWORKS (COMPUTER); NEUROIMAGING; POSITRON-EMISSION TOMOGRAPHY;

EID: 84880758889     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070005     Document Type: Article

References (41)

1. Varki NM, Varki A, (2007) Diversity in cell surface sialic acid presentations: implications for biology and disease. Lab Invest 87: 851-857 doi:10.1038/labinvest.3700656.
2. Skehel JJ, Wiley DC, (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69: 531-569 doi:10.1146/annurev.biochem.69.1.531.
3. Bouvier NM, Palese P, (2008) The biology of influenza viruses. Vaccine 12: D49-D53 doi:10.1016/j.vaccine.2008.07.039.
4. 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 doi:10.1128/JVI.01136-10.
5. Belser JA, Jayaraman A, Raman R, Pappas C, Zeng H, et al. (2011) Effect of D222G Mutation in the Hemagglutinin Protein on Receptor Binding, Pathogenesis and Transmissibility of the 2009 Pandemic H1N1 Influenza Virus. PLoS ONE 6: e25091 doi:10.1371/journal.pone.0025091.
6. Rykkvin R, Kilander A, Dudman SG, Hungnes O, (2013) Within-patient emergence of the influenza A(H1N1)pdm09 HA1 222G variant and clear association with severe disease, Norway. Euro Surveill 18: 20369.
7. Kao CL, Chan TC, Tsai CH, Chu KY, Chuang SF, et al. (2012) Emerged HA and NA Mutants of the Pandemic Influenza H1N1 Viruses with Increasing Epidemiological Significance in Taipei and Kaohsiung, Taiwan, 2009-10. PLoS ONE 7: e31162 doi:10.1371/journal.pone.0031162.
8. Puzelli S, Facchini M, De Marco MA, Palmieri A, Spagnolo D, et al. (2010) Molecular surveillance of pandemic influenza A(H1N1) viruses circulating in Italy from May 2009 to February 2010: association between haemagglutinin mutations and clinical outcome. Euro Surveill 15: pii = 19696.
9. Hug S, (2013) Classical molecular dynamics in a nutshell. Methods Mol Biol 924: 127-152 doi: _10.1007/978-1-62703-017-5_6.
10. Priyadarzini TR, Selvin JF, Gromiha MM, Fukui K, Veluraja K, (2012) Theoretical investigation on the binding specificity of sialyldisaccharides with hemagglutinins of influenza A virus by molecular dynamics simulations. J Biol Chem 287: 34547-34557 doi: 10.1074/jbc.M112.357061.
11. Chen W, Sun S, Li Z, (2012) Two glycosylation sites in H5N1 influenza virus hemagglutinin that affect binding preference by computer-based analysis. PLoS One 7: e38794 doi: 10.1371/journal.pone.0038794.
12. Xu D, Newhouse EI, Amaro RE, Pao HC, Cheng LS, et al. (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 doi: 10.1016/j.jmb.2009.01.040.
13. Jongkon N, Mokmak W, Chuakheaw D, Shaw PJ, Tongsima S, et al. (2009) Prediction of avian influenza A binding preference to human receptor using conformational analysis of receptor bound to hemagglutinin. BMC Genomics 10: S24 doi: 10.1186/1471-2164-10-S3-S24.
14. Newhouse EI, Xu D, Markwick PR, Amaro RE, Pao HC, et al. (2009) Mechanism of glycan receptor recognition and specificity switch for avian, swine, and human adapted influenza virus hemagglutinins: a molecular dynamics perspective. J Am Chem Soc 131: 17430-17442 doi: 10.1021/ja904052q.
15. Liechti R, Gleizes A, Kuznetsov D, Bougueleret L, Le Mercier P, et al. (2010) OpenFluDB, a database for human and animal influenza virus. Database 2010: baq004-baq004 doi:10.1093/database/baq004.
16. Katoh K, Toh H, (2008) Recent Developments in the MAFFT Multiple Sequence Alignment Program. Brief Bioinform 9: 286-298 doi:10.1093/bib/bbn013.
17. Hall T, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
18. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, et al. (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comput Chem 24: 1999-2012.
19. Kirschner KN, Yongye AB, Tschampel SM, González-Outeiriño J, Daniels CR, et al. (2008) GLYCAM06: a generalizable biomolecular force field. Carbohydrates. J Comput Chem 29: 622-655.
20. Case DA, Darden TA, Cheatham TE, Simmerling CL, Wang J, et al. (2012) AMBER 12.University of California, San Francisco.
21. Hess B, Kutzner C, Van der Spoel D, Lindahl E, (2008) GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. J Chem Theory Comput 4: 435-447 doi:10.1021/ct700301q.
22. Darden T, Perera L, Li L, Pedersen L, (1999) New tricks for modelers from the crystallography toolkit: the particle mesh Ewald algorithm and its use in nucleic acid simulations. Structure 7: R55-60.
23. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) AID-JCC4>3.0.CO;2-H.
24. Berendsen HJC, Postma JPM, Van Gunsteren WF, DiNola A, Haak JR, (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81: 3684-3690 doi:doi:10.1063/1.448118.
25. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38, 27-28.
26. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-10041.
27. Parthiban V, Gromiha MM, Schomburg D, (2006) CUPSAT: prediction of protein stability upon point mutations. Nucleic Acids Res 34: W239-W242 doi: 10.1093/nar/gkl190.
28. Bava KA, Gromiha MM, Uedaira H, Kitajima K, Sarai A, (2004) ProTherm, version 4.0: thermodynamic database for proteins and mutants. Nucleic Acids Res 32: D120-D121 doi:10.1093/nar/gkh082.
29. Naïm M, Bhat S, Rankin KN, Dennis S, Chowdhury SF, et al. (2007) Solvated Interaction Energy (SIE) for Scoring Protein-Ligand Binding Affinities. 1. Exploring the Parameter Space. J Chem Inf Model 47: 122-133 doi:10.1021/ci600406v.
30. Cui Q, Sulea T, Schrag JD, Munger C, Hung M-N, et al. (2008) Molecular Dynamics-Solvated Interaction Energy Studies of Protein-Protein Interactions: The MP1-p14 Scaffolding Complex. J Mol Biol 379: 787-802 doi:10.1016/j.jmb.2008.04.035.
31. Chen GW, Tsao KC, Huang CG, Gong YN, Chang SC, et al. (2012) Amino Acids Transitioning of 2009 H1N1pdm in Taiwan from 2009 to 2011. PLoS ONE 7: e45946 doi:10.1371/journal.pone.0045946.
32. O'Donnell CD, Vogel L, Wright A, Das SR, Wrammert J, et al. (2012) Antibody pressure by a human monoclonal antibody targeting the 2009 pandemic H1N1 virus hemagglutinin drives the emergence of a virus with increased virulence in mice. MBio 29: e00120-12 doi:10.1128/mBio.00120-12.
33. 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 doi:10.1128/JVI.01639-10.
34. Yasugi M, Nakamura S, Daidoji T, Kawashita N, Ramadhany R, et al. (2012) Frequency of D222G and Q223R Hemagglutinin Mutants of Pandemic (H1N1) 2009 Influenza Virus in Japan between 2009 and 2010. PLoS ONE 7: e30946 doi:10.1371/journal.pone.0030946.
35. 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 doi:10.1128/JVI.00159-10.
36. Seyer R, Hrincius ER, Ritzel D, Abt M, Mellmann A, et al. (2011) 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 doi: 10.1093/infdis/jir716.
37. 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 doi: 10.1016/j.virusres.2011.03.022.
38. Yen H-L, Liang C-H, Wu C-Y, Forrest HL, Ferguson A, et al. (2011) Hemagglutinin-neuraminidase balance confers respiratory-droplet transmissibility of the pandemic H1N1 influenza virus in ferrets. P Natl Acad Sci USA 108: 14264-14269 doi:10.1073/pnas.1111000108.
39. Xu R, Zhu X, McBride R, Nycholat CM, Yu W, et al. (2012) Functional Balance of the Hemagglutinin and Neuraminidase Activities Accompanies the Emergence of the 2009 H1N1 Influenza Pandemic. J Virol 86: 9221-9232 doi: 10.1128/JVI.00697-12.
40. Thoennes S, Li ZN, Lee BJ, Langley WA, Skehel JJ, et al. (2008) Analysis of residues near the fusion peptide in the influenza hemagglutinin structure for roles in triggering membrane fusion. Virology 370: 403-414 doi:10.1016/j.virol.2007.08.035.
41. 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 doi:10.1371/journal.ppat.1002398.