Evolution of the neuraminidase gene of seasonal influenza A and B viruses in Thailand between 2010 and 2015

PLoS ONE

Volumn 12, Issue 4, 2017, Pages

  Tewawong, Nipaporn ^a   Vichiwattana, Preeyaporn ^a   Korkong, Sumeth ^a   Klinfueng, Sirapa ^a   Suntronwong, Nungruthai ^a   Thongmee, Thanunrat ^a   Theamboonlers, Apiradee ^a   Vongpunsawad, Sompong ^a   Poovorawan, Yong ^a  

^a CHULALONGKORN UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; OSELTAMIVIR; SIALIDASE INHIBITOR; SIALIDASE; VIRUS RNA;

AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; ARTICLE; EVOLUTIONARY RATE; GENE AMPLIFICATION; GENE SEQUENCE; INFLUENZA A VIRUS; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H2N2); INFLUENZA B VIRUS; MOLECULAR PHYLOGENY; NEURAMINIDASE GENE; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PROTEIN GLYCOSYLATION; THAILAND; CLASSIFICATION; DRUG EFFECTS; ENZYMOLOGY; GENETICS; GENOTYPE; GLYCOSYLATION; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS (H3N2); INFLUENZA, HUMAN; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; SEASON; VIROLOGY;

DRUG RESISTANCE, VIRAL; EPITOPES, B-LYMPHOCYTE; EVOLUTION, MOLECULAR; GENOTYPE; GLYCOSYLATION; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA B VIRUS; INFLUENZA, HUMAN; NEURAMINIDASE; OSELTAMIVIR; PHYLOGENY; RNA, VIRAL; SEASONS; THAILAND;

EID: 85017443574     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0175655     Document Type: Article

References (65)

1. Influenza-seasonal: World Health Organization; March 2014 [cited 2015 September 25]. Available from: http://www.who.int/mediacentre/factsheets/fs211/en/
2. Fiore AE, Uyeki TM, Broder K, Finelli L, Euler GL, Singleton JA, et al. Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWRRecomm Rep. 2010; 59: 1-62.
3. Su YC, Bahl J, Joseph U, Butt KM, Peck HA, Koay ES, et al. Phylodynamics of H1N1/2009 influenza reveals the transition from host adaptation to immune-driven selection. Nat Commun. 2015; 6: 7952. https://doi.org/10.1038/ncomms8952 PMID: 26245473
4. Hayden FG, Atmar RL, Schilling M, Johnson C, Poretz D, Paar D, et al. Use of the selective oral neuraminidase inhibitor oseltamivir to prevent influenza. N Engl J Med 1999; 341: 1336-43. https://doi.org/10.1056/NEJM199910283411802 PMID: 10536125
5. Jain S, Kamimoto L, Bramley AM, Schmitz AM, Benoit SR, Louie J, et al. Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N Engl J Med 2009; 361: 1935-44. https://doi.org/10.1056/NEJMoa0906695 PMID: 19815859
6. Fiore AE, Fry A, Shay D, Gubareva L, Bresee JS, Uyeki TM, et al. Antiviral agents for the treatment and chemoprophylaxis of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWRRecomm Rep. 2011; 60(1): 1-24. PMID: 21248682
7. Sauter NK, Bednarski MD, Wurzburg BA, Hanson JE, Whitesides GM, Skehel JJ, et al. Hemagglutinins from two influenza virus variants bind to sialic acid derivatives with millimolar dissociation constants: a 500-MHz proton nuclear magnetic resonance study. Biochemistry. 1989; 28(21): 8388-96. PMID: 2605190
8. Li W, Shi W, Qiao H, Ho SY, Luo A, Zhang Y, et al. Positive selection on hemagglutinin and neuraminidase genes of H1N1 influenza viruses. Virol J. 2011; 8: 183. https://doi.org/10.1186/1743-422X-8-183 PMID: 21507270
9. Palese P, Tobita K, Ueda M, Compans RW. Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology. 1974; 61(2): 397-410. PMID: 4472498
10. Schild GC, Oxford JS, Dowdle WR, Coleman M, Pereira MS, Chakraverty P. Antigenic variation in current influenza A viruses: evidence for a high frequency of antigenic 'drift' for the Hong Kong virus. Bull World Health Organ. 1974; 51(1): 1-11. PMID: 4218138
11. Kim CU, Lew W, Williams MA, Liu H, Zhang L, Swaminathan S, et al. Influenza neuraminidase inhibitors possessing a novel hydrophobic interaction in the enzyme active site: design, synthesis, and structural analysis of carbocyclic sialic acid analogues with potent anti-influenza activity. J Am Chem Soc. 1997; 119(4): 681-90. PMID: 16526129
12. Colman PM, Varghese JN, Laver WG. Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature. 1983; 303(5912): 41-4. PMID: 6188957
13. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992; 56(1): 152-79. PMID: 1579108
14. Steinhauer DA, Holland JJ. Rapid evolution of RNA viruses. Annu Rev Microbiol. 1987; 41: 409-33. https://doi.org/10.1146/annurev.mi.41.100187.002205 PMID: 3318675
15. Abed Y, Baz M, Boivin G. Impact of neuraminidase mutations conferring influenza resistance to neuraminidase inhibitors in the N1 and N2 genetic backgrounds. Antivir Ther. 2006; 11(8): 971-6. PMID: 17302366
16. Li TC, Chan MC, Lee N. Clinical Implications of Antiviral Resistance in Influenza. Viruses. 2015; 7(9): 4929-44. https://doi.org/10.3390/v7092850 PMID: 26389935
17. de Jong MD, Ison MG, Monto AS, Metev H, Clark C, O'Neil B, et al. Evaluation of intravenous peramivir for treatment of influenza in hospitalized patients. Clin Infect Dis. 2014; 59(12): e172-85. https://doi. org/10.1093/cid/ciu632 PMID: 25115871
18. Meijer A, Lackenby A, Hungnes O, Lina B, van-der-Werf S, Schweiger B, et al. Oseltamivir-resistant influenza virus A(H1N1), Europe, 2007-08 season. Emerg Infect Dis 2009; 15(4): 552e60.
19. Hatakeyama S, Sugaya N, Ito M, Yamazaki M, Ichikawa M, Kimura K, et al. Emergence of influenza B viruses with reduced sensitivity to neuraminidase inhibitors. JAMA. 2007; 297(13): 1435-42. https://doi.org/10.1001/jama.297.13.1435 PMID: 17405969
20. The WHO GISRS antiviral susceptibility expert working group (AVWG). Summary of neuraminidase amino acid substitutions associated with reduced inhibition by neuraminidase inhibitors (NAI). Last updated 21 October 2016. Available from: http://www.who.int/influenza/gisrs-laboratory/antiviral-susceptibility/avwg2014-nai-substitution-table.pdf?ua=1
21. Baz M, Abed Y, Papenburg J, Bouhy X, Hamelin ME, Boivin G. Emergence of oseltamivir-resistant pandemic H1N1 virus during prophylaxis. N Engl J Med. 2009; 361(23): 2296-7. https://doi.org/10.1056/NEJMc0910060 PMID: 19907034
22. Hurt AC, Lee RT, Leang SK, Cui L, Deng YM, Phuah SP, et al. Increased detection in Australia and Singapore of a novel influenza A(H1N1)2009 variant with reduced oseltamivir and zanamivir sensitivity due to a S247N neuraminidase mutation. Euro Surveill. 2011; 16(23).
23. Richard M, Ferraris O, Erny A, Barthélémy M, Traversier A, Sabatier M, et al. Combinatorial effect of two framework mutations (E119 and I222L) in the neuraminidase active site of H3N2 influenza virus on resistance to oseltamivir. Antimicrob Agents Chemother. 2011; 55(6): 2942-52. https://doi.org/10. 1128/AAC.01699-10 PMID: 21422222
24. Leang SK, Kwok S, Sullivan SG, Maurer-Stroh S, Kelso A, Barr IG, et al. Peramivir and laninamivir susceptibility of circulating influenza A and B viruses. Influenza Other Respir Viruses. 2014; 8(2): 135-9. https://doi.org/10.1111/irv.12187 PMID: 24734292
25. Tewawong N, Chansaenroj J, Klinfueng S, Vichiwattana P, Korkong S, Thongmee T, et al. Lineage-specific detection of influenza B virus using real-time polymerase chain reaction with melting curve analysis. Arch Virol. 2016; 161: 1425-35. https://doi.org/10.1007/s00705-016-2802-2 PMID: 26923928
26. Chutinimitkul S, Chieochansin T, Payungporn S, Samransamruajkit R, Hiranras T, Theamboonlers A, et al. Molecular characterization and phylogeneticanalysis of H1N1 and H3N2 human influenza A viruses among infants and children in Thailand. Virus Res. 2008; 132(1-2): 122-31. https://doi.org/10.1016/j.virusres.2007.11.007 PMID: 18160168
27. Makkoch J, Suwannakarn K, Payungporn S, Prachayangprecha S, Cheiocharnsin T, Linsuwanon P, et al. Whole genome characterization, phylogenetic and genome signature analysis of human pandemic H1N1 virus in Thailand, 2009-2012. PLoS One. 2012; 7(12): e51275. https://doi.org/10.1371/journal.pone.0051275 PMID: 23251479
28. Tewawong N, Suwannakarn K, Prachayangprecha S, Korkong S, Vichiwattana P, Vongpunsawad S, et al. Molecular epidemiology and phylogenetic analyses of influenza B virus in Thailand during 2010 to 2014. PLoS One 2015; 10(1):e0116302. https://doi.org/10.1371/journal.pone.0116302 PMID: 25602617
29. Payungporn S, Poomipak W, Makkoch J, Rianthavorn P, Theamboonlers A, Poovorawan Y. Detection of oseltamivir sensitive/resistant strains of pandemic influenza A virus (H1N1) from patients admitted to hospitals in Thailand. J Virol Methods. 2011; 177(2): 133-9. https://doi.org/10.1016/j.jviromet.2011.07.008 PMID: 21820468
30. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. ClustalWand Clustal X version 2.0. Bioinformatics. 2007; 23(21): 2947-8. https://doi.org/10.1093/bioinformatics/btm404 PMID: 17846036
31. Nei M. and Kumar S. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York.
32. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013; 30(12): 2725-9. https://doi.org/10.1093/molbev/mst197PMID: 24132122
33. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012; 9(8): 772.
34. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 7. Mol Biol Evol. 2012; 29(8): 1969-73. https://doi.org/10.1093/molbev/mss075 PMID: 22367748
35. Delport W, Poon AF, Frost SD, Kosakovsky Pond SL. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics. 2010; 26(19): 2455-7. https://doi.org/10.1093/bioinformatics/btq429 PMID: 20671151
36. Gupta R, Jung E, Brunak S. 2004. Prediction of N-glycosylation sites in human proteins. http://www.cbs.dtu.dk/services/NetNGlyc/. Accessed 26 January 2016
37. Larsen JE, Lund O, Nielsen M. Improved method for predicting linear B-cell epitopes. Immunome Res. 2006; 2: 2. https://doi.org/10.1186/1745-7580-2-2 PMID: 16635264
38. McCauley J, Daniels R, Lin YP, Xiang Z, Gregory V, Whittaker L, et al. Report prepared for the WHO annual consultation on the composition of influenza vaccine for the Southern Hemisphere 2017: 26th- 28th September 2016. Worldwide influenza centre the Francis Crick institute Mill Hill Laboratory London. Available from: https://www.crick.ac.uk/media/326439/september-2016-interim-report.pdf.
39. Okomo-Adhiambo M, Fry AM, Su S, Nguyen HT, Elal AA, Negron E, 2013-14 US Influenza Antiviral Working Group. Oseltamivir-resistant influenza A(H1N1)pdm09 viruses, United States, 2013-14. Emerg Infect Dis. 2015; 21(1): 136-41. https://doi.org/10.3201/eid2101.141006 PMID: 25532050
40. Huang W, Li X, Cheng Y, Tan M, Guo J, Wei H, et al. Characteristics of oseltamivir-resistant influenza A (H1N1) pdm09 virus during the 2013-2014 influenza season in Mainland China. Virol J. 2015; 12: 96. https://doi.org/10.1186/s12985-015-0317-1 PMID: 26103966
41. Ghedin E, Holmes EC, DePasse JV, Pinilla LT, Fitch A, Hamelin ME, et al. Presence of oseltamivirresistant pandemic A/H1N1 minor variants before drug therapy with subsequent selection and transmission. J Infect Dis. 2012; 206(10): 1504-11. https://doi.org/10.1093/infdis/jis571 PMID: 22966122
42. Hurt AC, Chotpitayasunondh T, Cox NJ, Daniels R, Fry AM, Gubareva LV, et al. WHO Consultation on Pandemic Influenza A (H1N1) 2009 Virus Resistance to Antivirals. Antiviral resistance during the 2009 influenza A H1N1 pandemic: public health, laboratory, and clinical perspectives. Lancet Infect Dis. 2012; 12(3): 240-8. https://doi.org/10.1016/S1473-3099(11)70318-8 PMID: 22186145
43. Butler J, Hooper KA, Petrie S, Lee R, Maurer-Stroh S, Reh L, et al. Estimating the fitness advantage conferred by permissive neuraminidase mutations in recent oseltamivir-resistant A(H1N1)pdm09 influenza viruses. PLoS Pathog. 2014; 10(4): e1004065. https://doi.org/10.1371/journal.ppat.1004065PMID: 24699865
44. Dharan NJ, Gubareva LV, Meyer JJ, Okomo-Adhiambo M, McClinton RC, Marshall SA, et al. Oseltamivir- Resistance Working Group. Infections with oseltamivir-resistant influenza A(H1N1) virus in the United States. JAMA. 2009; 301(10): 1034-41. https://doi.org/10.1001/jama.2009.294 PMID: 19255110
45. Hurt AC. The epidemiology and spread of drug resistant human influenza viruses. Curr Opin Virol. 2014; 8: 22-9. https://doi.org/10.1016/j.coviro.2014.04.009 PMID: 24866471
46. Duan S, Govorkova EA, Bahl J, Zaraket H, Baranovich T, Seiler P, et al. Epistatic interactions between neuraminidase mutations facilitated the emergence of the oseltamivir-resistant H1N1 influenza viruses. Nat Commun. 2014; 5: 5029. https://doi.org/10.1038/ncomms6029 PMID: 25297528
47. Takashita E, Meijer A, Lackenby A, Gubareva L, Rebelo-de-Andrade H, Besselaar T, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013-2014. Antiviral Res. 2015 May; 117: 27-38. https://doi.org/10.1016/j.antiviral.2015.02.003 PMID: 25721488
48. Whitley RJ, Boucher CA, Lina B, Nguyen-Van-Tam JS, Osterhaus A, Schutten M, et al. Global assessment of resistance to neuraminidase inhibitors, 2008-2011: the Influenza Resistance Information Study (IRIS). Clin Infect Dis. 2013; 56(9): 1197-205. https://doi.org/10.1093/cid/cis1220 PMID: 23307766
49. Saito T, Kawano K. Loss of glycosylation at Asn144 alters the substrate preference of the N8 influenza A virus neuraminidase. J Vet Med Sci. 1997; 59(10): 923-6. PMID: 9362042
50. Li S, Schulman J, Itamura S, Palese P. Glycosylation of neuraminidase determines the neurovirulence of influenza A/WSN/33 virus. J Virol. 1993; 67(11): 6667-73. PMID: 8411368
51. Westgeest KB, Russell CA, Lin X, Spronken MI, Bestebroer TM, Bahl J, et al. Genomewide analysis of reassortment and evolution of human influenza A(H3N2) viruses circulating between 1968 and 2011. J Virol. 2014; 88(5): 2844-57. https://doi.org/10.1128/JVI.02163-13 PMID: 24371052
52. Nelson MI, Simonsen L, Viboud C, Miller MA, Taylor J, George KS, Griesemer SB, Ghedin E, Sengamalay NA, Spiro DJ, Volkov I, Grenfell BT, Lipman DJ, Taubenberger JK, Holmes EC. Stochastic processes are key determinants of short-term evolution in influenza a virus. PLoS Pathog. 2006 Dec; 2 (12):e125. https://doi.org/10.1371/journal.ppat.0020125 PMID: 17140286
53. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC. The genomic and epidemiological dynamics of human influenza A virus. Nature. 2008 May 29; 453(7195):615-9. https://doi. org/10.1038/nature06945 PMID: 18418375
54. Vijaykrishna D, Holmes EC, Joseph U, Fourment M, Su YC, Halpin R, et al. The contrasting phylodynamics of human influenza B viruses. Elife. 2015; 4: e05055. https://doi.org/10.7554/eLife.05055 PMID: 25594904
55. Oong XY, Ng KT, Lam TT, Pang YK, Chan KG, Hanafi NS, Kamarulzaman A, Tee KK. Epidemiological and Evolutionary Dynamics of Influenza B Viruses in Malaysia, 2012-2014. PLoS One. 2015 Aug 27; 10(8):e0136254. https://doi.org/10.1371/journal.pone.0136254 PMID: 26313754
56. Makkoch J, Suwannakarn K, Payungporn S, Prachayangprecha S, Cheiocharnsin T, Linsuwanon P, Theamboonlers A, Poovorawan Y. Whole genome characterization, phylogenetic and genome signature analysis of human pandemic H1N1 virus in Thailand, 2009-2012. PLoS One. 2012; 7(12):e51275. https://doi.org/10.1371/journal.pone.0051275 PMID: 23251479
57. Suzuki Y. Natural selection on the influenza virus genome. Mol Biol Evol. 2006; 23(10): 1902-11. https://doi.org/10.1093/molbev/msl050 PMID: 16818477
58. Lin JH, Chiu SC, Cheng JC, Chang HW, Hsiao KL, Lin YC, Wu HS, Liu HF. Molecular epidemiology and antigenic analyses of influenza A viruses H3N2 in Taiwan. Clin Microbiol Infect. 2011 Feb; 17(2):214-22. https://doi.org/10.1111/j.1469-0691.2010.03228.x PMID: 20370800
59. Mostafa A, Abdelwhab ESM, Slanina H, Hussein MA, Kuznetsova I, Schü ttler CG, Ziebuhr J, Pleschka S. Phylogenetic analysis of human influenza A/H3N2 viruses circulated in 2015 in Germany indicates significant genetic divergence from vaccine strains. Arch Virol. 2016 Jun; 161(6):1505-15. https://doi.org/10.1007/s00705-016-2815-x PMID: 26973232
60. Xu R, Zhu X, McBride R, Nycholat CM, Yu W, Paulson JC, et al. Functional balance of the hemagglutinin and neuraminidase activities accompanies the emergence of the 2009 H1N1 influenza pandemic. J Virol. 2012; 86: 9221-32. https://doi.org/10.1128/JVI.00697-12 PMID: 22718832
61. Wan H, Gao J, Xu K, Chen H, Couzens LK, Rivers KH, et al. Molecular basis for broad neuraminidase immunity: conserved epitopes in seasonal and pandemic H1N1 as well as H5N1 influenza viruses. J Virol. 2013; 87: 9290-300. https://doi.org/10.1128/JVI.01203-13 PMID: 23785204
62. Takahashi T, Suzuki T, Hidari KI, Miyamoto D, Suzuki Y. A molecular mechanism for the low-pH stability of sialidase activity of influenza A virus N2 neuraminidases. FEBS Lett. 2003; 543: 71-5. PMID: 12753908
63. Takahashi T, Song J, Suzuki T, Kawaoka Y. Mutations in NA that induced low pH-stability and enhanced the replication of pandemic (H1N1) 2009 influenza A virus at an early stage of the pandemic. PLoS One. 2013; 5: e64439.
64. Nelson MI, Holmes EC. The evolution of epidemic influenza. Nat Rev Genet. 2007; 8: 196-205. https://doi.org/10.1038/nrg2053 PMID: 17262054
65. Bedford T, Riley S, Barr IG, Broor S, Chadha M, Cox NJ, et al. Global circulation patterns of seasonal influenza viruses vary with antigenic drift. Nature. 2015; 7559: 217-20.