Intrahost dynamics of antiviral resistance in influenza a virus reflect complex patterns of segment linkage, reassortment, and natural selection

mBio

Volumn 6, Issue 2, 2015, Pages

  Rogers, Matthew B ^a   Song, Timothy ^a,b   Sebra, Robert ^c   Greenbaum, Benjamind D ^c   Hamelin, Marie Eve ^d   Fitch, Adam ^a   Twaddle, Alan ^b   Cui, Lijia ^a,e   Holmes, Edward C ^f   Boivin, Guy ^d   Ghedina, Elodie ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d LAVAL UNIVERSITY   (Canada)

^e Tsinghua University   (China)

^f University of Sydney   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMANTADINE; HEMAGGLUTININ; OSELTAMIVIR; ZANAMIVIR; ANTIVIRUS AGENT; VIRUS RNA;

ANTIVIRAL RESISTANCE; ARTICLE; CASE REPORT; CHILD; CONTROLLED STUDY; GENETIC LINKAGE; GENETIC REASSORTMENT; GENETIC VARIABILITY; HUMAN; IMMUNOCOMPROMISED PATIENT; INFLUENZA A (H3N2); INFLUENZA VIRUS A H3N2; NATURAL SELECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRESCHOOL CHILD; PRIORITY JOURNAL; SEVERE COMBINED IMMUNODEFICIENCY; VIRUS MUTATION; VIRUS SHEDDING; VIRUS STRAIN; CLASSIFICATION; DNA SEQUENCE; GENETIC SELECTION; GENETICS; INFLUENZA A VIRUS (H3N2); INFLUENZA, HUMAN; ISOLATION AND PURIFICATION; MOLECULAR EVOLUTION; MOLECULAR GENETICS; VIROLOGY;

HUMAN INFLUENZA VIRUS; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; EVOLUTION, MOLECULAR; HUMANS; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA, HUMAN; MOLECULAR SEQUENCE DATA; RNA, VIRAL; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84929999966     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02464-14     Document Type: Article

References (35)

1. Drake JW. 1993. Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci U S A 90:4171–4175. http://dx.doi.org/10.1073/pnas.90.9.4171.
2. Desselberger U, Nakajima K, Alfino P, Pedersen FS, Haseltine WA, Hannoun C, Palese P. 1978. Biochemical evidence that “new” influenza virus strains in nature may arise by recombination (reassortment). Proc Natl Acad Sci U S A 75:3341–3345. http://dx.doi.org/10.1073/pnas.75.7.3341.
3. Bush RM, Fitch WM, Bender CA, Cox NJ. 1999. Positive selection on the H3 hemagglutinin gene of human influenza virus A. Mol Biol Evol 16: 1457–1465. http://dx.doi.org/10.1093/oxfordjournals.molbev.a026057.
4. Viboud C, Nelson MI, Tan Y, Holmes EC. 2013. Contrasting the epidemiological and evolutionary dynamics of influenza spatial transmission. Philos Trans R Soc Lond B Biol Sci 368:20120199. http://dx.doi.org/10.1098/rstb.2012.0199.
5. Leekha S, Zitterkopf NL, Espy MJ, Smith TF, Thompson RL, Sampathkumar P. 2007. Duration of influenza A virus shedding in hospitalized patients and implications for infection control. Infect Control Hosp Epidemiol 28:1071–1076. http://dx.doi.org/10.1086/520101.
6. Suess T, Buchholz U, Dupke S, Grunow R, an der Heiden M, Heider A, Biere B, Schweiger B, Haas W, Krause G, Robert Koch Institute Shedding Investigation Group. 2010. Shedding and transmission of novel influenza virus A/H1N1 infection in households—Germany, 2009. Am J Epidemiol 171:1157–1164. http://dx.doi.org/10.1093/aje/kwq071.
7. Baz M, Abed Y, McDonald J, Boivin G. 2006. Characterization of multidrug-resistant influenza A/H3N2 viruses shed during 1 year by an immunocompromised child. Clin Infect Dis 43:1555–1561. http://dx.doi.org/10.1086/508777.
8. Boivin G, Goyette N, Bernatchez H. 2002. Prolonged excretion of amantadine-resistant influenza A virus quasi species after cessation of antiviral therapy in an immunocompromised patient. Clin Infect Dis 34: e23–e25. http://dx.doi.org/10.1086/338870.
9. Vega E, Donaldson E, Huynh J, Barclay L, Lopman B, Baric R, Chen LF, Vinjé J. 2014. RNA populations in immunocompromised patients as reservoirs for novel norovirus variants. J Virol 88:14184–14196. http://dx.doi.org/10.1128/JVI.02494-14.
10. Geis S, Prifert C, Weissbrich B, Lehners N, Egerer G, Eisenbach C, Buchholz U, Aichinger E, Dreger P, Neben K, Burkhardt U, Ho AD, Kräusslich HG, Heeg K, Schnitzler P. 2013. Molecular characterization of a respiratory syncytial virus outbreak in a hematology unit in Heidelberg, Germany. J Clin Microbiol 51:155–162. http://dx.doi.org/10.1128/JCM.02151-12.
11. van der Vries E, Stittelaar KJ, van Amerongen G, Veldhuis Kroeze EJ, de Waal L, Fraaij PL, Meesters RJ, Luider TM, van der Nagel B, Koch B, Vulto AG, Schutten M, Osterhaus AD. 2013. Prolonged influenza virus shedding and emergence of antiviral resistance in immunocompromised patients and ferrets. PLoS Pathog 9:e1003343. http://dx.doi.org/10.1371/journal.ppat.1003343.
12. Abed Y, Baz M, Boivin G. 2009. A novel neuraminidase deletion mutation conferring resistance to oseltamivir in clinical influenza A/H3N2 virus. J Infect Dis 199:180–183. http://dx.doi.org/10.1086/595736.
13. Hayden FG, Belshe RB, Clover RD, Hay AJ, Oakes MG, Soo W. 1989. Emergence and apparent transmission of rimantadine-resistant influenza A virus in families. N Engl J Med 321:1696–1702. http://dx.doi.org/10.1056/NEJM198912213212502.
14. Memoli MJ, Hrabal RJ, Hassantoufighi A, Eichelberger MC, Taubenberger JK. 2010. Rapid selection of oseltamivir- and peramivir-resistant pandemic H1N1 virus during therapy in 2 immunocompromised hosts. Clin Infect Dis 50:1252–1255. http://dx.doi.org/10.1086/651605.
15. Samson M, Pizzorno A, Abed Y, Boivin G. 2013. Influenza virus resistance to neuraminidase inhibitors. Antiviral Res 98:174–185. http://dx.doi.org/10.1016/j.antiviral.2013.03.014.
16. Abed Y, Baz M, Boivin G. 2006. Impact of neuraminidase mutations conferring influenza resistance to neuraminidase inhibitors in the N1 and N2 genetic backgrounds. Antivir Ther 11:971–976.
17. Ruiz-Carrascoso G, Casas I, Pozo F, González-Vincent M, Pérez-Breña P. 2010. Prolonged shedding of amantadine- and oseltamivir-resistant influenza A(H3N2) virus with dual mutations in an immunocompromised infant. Antivir Ther 15:1059–1063. http://dx.doi.org/10.3851/IMP1657.
18. Eshaghi A, Shalhoub S, Rosenfeld P, Li A, Higgins RR, Stogios PJ, Savchenko A, Bastien N, Li Y, Rotstein C, Gubbay JB. 2014. Multiple influenza A (H3N2) mutations conferring resistance to neuraminidase inhibitors in a bone marrow transplant recipient. Antimicrob Agents Chemother 58:7188–7197. http://dx.doi.org/10.1128/AAC.03667-14.
19. Greenbaum BD, Li OT, Poon LL, Levine AJ, Rabadan R. 2012. Viral reassortment as an information exchange between viral segments. Proc Natl Acad Sci U S A 109:3341–3346. http://dx.doi.org/10.1073/pnas.1113300109.
20. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC. 2008. The genomic and epidemiological dynamics of human influenza A virus. Nature 453:615–619. http://dx.doi.org/10.1038/nature06945.
21. Ince WL, Gueye-Mbaye A, Bennink JR, Yewdell JW. 2013. Reassortment complements spontaneous mutation in influenza A virus NP and M1 genes to accelerate adaptation to a new host. J Virol 87:4330–4338. http://dx.doi.org/10.1128/JVI.02749-12.
22. Nelson MI, Simonsen L, Viboud C, Miller MA, Holmes EC. 2009. The origin and global emergence of adamantane resistant A/H3N2 influenza viruses. Virology 388:270–278. http://dx.doi.org/10.1016/j.virol.2009.03.026.
23. Simonsen L, Viboud C, Grenfell BT, Dushoff J, Jennings L, Smit M, Macken C, Hata M, Gog J, Miller MA, Holmes EC. 2007. The genesis and spread of reassortment human influenza A/H3N2 viruses conferring adamantane resistance. Mol Biol Evol 24:1811–1820. http://dx.doi.org/10.1093/molbev/msm103.
24. Yang JR, Lin YC, Huang YP, Su CH, Lo J, Ho YL, Yao CY, Hsu LC, Wu HS, Liu MT. 2011. Reassortment and mutations associated with emergence and spread of oseltamivir-resistant seasonal influenza A/H1N1 viruses in 2005–2009. PLoS One 6:e18177. http://dx.doi.org/10.1371/journal.pone.0018177.
25. Zhou B, Donnelly ME, Scholes DT, St George K, Hatta M, Kawaoka Y, Wentworth DE. 2009. Single-reaction genomic amplification accelerates sequencing and vaccine production for classical and swine origin human influenza A viruses. J Virol 83:10309–10313. http://dx.doi.org/10.1128/JVI.01109-09.
26. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359. http://dx.doi.org/10.1038/nmeth.1923.
27. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. http://dx.doi.org/10.1093/bioinformatics/btp352.
28. Milne I, Stephen G, Bayer M, Cock PJ, Pritchard L, Cardle L, Shaw PD, Marshall D. 2013. Using tablet for visual exploration of secondgeneration sequencing data. Brief Bioinform 14:193–202. http://dx.doi.org/10.1093/bib/bbs012.
29. Wilm A, Aw PP, Bertrand D, Yeo GH, Ong SH, Wong CH, Khor CC, Petric R, Hibberd ML, Nagarajan N. 2012. LoFreq: a sequence-quality aware, ultra-sensitive variant caller for uncovering cell-population heterogeneity from high-throughput sequencing datasets. Nucleic Acids Res 40:11189–11201. http://dx.doi.org/10.1093/nar/gks918.
30. Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B, Bibillo A, Bjornson K, Chaudhuri B, Christians F, Cicero R, Clark S, Dalal R, Dewinter A, Dixon J, Foquet M, Gaertner A, Hardenbol P, Heiner C, Hester K, Holden D, Kearns G, Kong X, Kuse R, Lacroix Y, Lin S, Lundquist P, Ma C, Marks P, Maxham M, Murphy D, Park I, Pham T, Phillips M, Roy J, Sebra R, Shen G, Sorenson J, Tomaney A, Travers K, Trulson M, Vieceli J, Wegener J, Wu D, Yang A, Zaccarin D, Zhao P, Zhong F, Korlach J, Turner S. 2009. Real-time DNA sequencing from single polymerase molecules. Science 323:133–138. http://dx.doi.org/10.1126/science.1162986.
31. Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26:589–595. http://dx.doi.org/10.1093/bioinformatics/btp698.
32. Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066. http://dx.doi.org/10.1093/nar/gkf436.
33. Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224. http://dx.doi.org/10.1093/molbev/msp259.
34. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. http://dx.doi.org/10.1093/bioinformatics/btu033.
35. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. http://dx.doi.org/10.1080/10635150390235520.