Genetic diversity among pandemic 2009 influenza viruses isolated from a transmission chain

Virology Journal

Volumn 10, Issue , 2013, Pages

  Fordyce, Sarah L ^a,b   Bragstad, Karoline ^b   Pedersen, Svend Stenvang ^c   Jensen, Thøger G ^c   Gahrn Hansen, Bente ^c   Daniels, Rod ^d   Hay, Alan ^d   Kampmann, Marie Louise ^a,b   Bruhn, Christian Aw ^a   Moreno Mayar, J Victor ^a   Ávila Arcos, María C ^a   Gilbert, M Thomas P ^a   Nielsen, Lars P ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b STATENS SERUM INSTITUT   (Denmark)

^c ODENSE UNIVERSITY HOSPITAL   (Denmark)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

A(H1N1)pdm09 influenza; Deep sequencing; Intra host variation; Oseltamivir resistance

Indexed keywords

OSELTAMIVIR; ZANAMIVIR;

2009 H1N1 INFLUENZA; ARTICLE; CONTROLLED STUDY; GENE MUTATION; GENE SEQUENCE; GENETIC VARIABILITY; HUMAN; INFLUENZA VIRUS; NUCLEOTIDE SEQUENCE; VIRUS ISOLATION; VIRUS TRANSMISSION;

EID: 84877774936     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-10-116     Document Type: Article

References (33)

1. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Smith GJD, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JS, Guan Y, Rambaut A, Nature 2009 459 1122 1126 10.1038/nature08182 19516283
2. The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance-a review. Domingo E, Martinez-Salas E, Sobrino F, de la Torre JC, Portela A, Ortin J, Lopez-Galindez C, Perenz-Brena P, Villanueva N, Najera R, VandePol S, Steinhauer D, DePolo N, Holland J, Gene 1985 40 521 527
3. RNA virus mutations and fitness for survival. Domingo E, Holland JJ, Annu Rev Microbiol 1997 51 151 178 10.1146/annurev.micro.51.1.151 9343347
4. The Evolutionary Genetics and Emergence of Avian Influenza Viruses in Wild Bird. Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborksy J, Ghedin E, Nolting J, Swayne DE, Runstadler JA, Happ GM, Senne DA, Wang R, Slemons RD, Holmes EC, Taubenberger JK, PLoS Path 2008 4 1000076 10.1371/journal.ppat. 1000076
5. Global Surveillance of Emerging Influenza Virus Genotypes by Mass Spectrometry. Sampath R, Russell KL, Massire C, Eshoo MW, Harpin V, Blyn LB, Melton R, Ivy C, Pennella T, Li F, Levene H, Hall TA, Libby B, Fan N, Walcott DJ, Ranken R, Pear M, Schink A, Gutierrez J, Drader J, Moore D, Metzgar D, Addlington L, Rothman R, Gaydos CA, Yang S, Fuschino ME, Dean AB, Stallknecht DE, Goekjian G, Yingst S, Monteville M, Saad MD, Whitehouse CA, Baldwin C, Rudnick KH, Hofstadler SA, Lemon SM, Ecker DJ, St. George K, PLoS One 2007 5 489
6. Examining the hemagglutinin subtype diversity among wild duck-origin influenza A viruses using ethanol-fixed cloacal swabs and a novel RT-PCR method. Wang R, Soll L, Dugan V, Runstadler JA, Happ GM, Slemons RD, Taubenberger JK, Virology 2008 375 182 189 10.1016/j.virol.2008.01.041 18308356
7. Characterization of quasispecies of pandemic 2009 influenza A virus (A/H1N1/2009) by de novo sequencing using a next-generation DNA sequencer. Kuroda M, Katano H, Nakjima N, Tobiume M, Ainai A, Sekizuka T, Hasegawa H, Tashiro M, Sasaki Y, Arakawa Y, Hata S, Watanabe M, Sata T, PLoS One 2010 5 10256 10.1371/journal.pone.0010256 20428231
8. The feasibility of using high resolution genome sequencing of influenza A viruses to detect mixed infections and quasispecies. Ramakrishnan MA, Tu ZJ, Singh S, Chockalingam AK, Gramer MR, Wang P, Goyal SM, Yang M, Halvorson DA, Sreevatsan S, PLoS One 2009 4 7105 10.1371/journal.pone.0007105 19771155
9. Deep sequencing reveals mixed infection with 2009 pandemic influenza A (H1N1) virus strains and the emergence of oseltamivir resistance. Ghedin E, Laplante J, DePasse J, Wentworth DE, Santos RP, Lepow ML, Porter J, Stellrecht K, Lin X, Operario D, Griesemer S, Fitch A, Halpin RA, Stockwell TB, Spiro DJ, Holmes EC, St George K, J Infect Dis 2011 203 168 174 10.1093/infdis/jiq040 21288815
10. A metagenomic analysis of pandemic influenza A (2009 H1N1) infection in patients from North America. Greninger AL, Chen EC, Sittler T, Scheinerman A, Roubinian N, Yu G, Kim E, Pillai DR, Guyard C, Mazzulli T, Isa P, Arias CF, Hackett J, Schochetman G, Miller S, Tang P, Chiu CY, PLoS One 2010 5 13381 10.1371/journal.pone.0013381 20976137
11. Variations in the hemagglutinin of the 2009 H1N1 pandemic virus: potential for strains with altered virulence phenotype? Ye J, Sorrell EM, Cai Y, Shao H, Xu K, Pena L, Hickman D, Song H, Angel M, Medina RA, Manicassamy B, Garcia-Sastre A, Perez DR, PLoS Pathog 2010 6 1001145 10.1371/journal.ppat. 1001145 20976194
12. Continued emergence and changing epidemiology of oseltamivir-resistant influenza A(H1N1)2009 virus, United Kingdom, winter 2010/11. Lackenby A, Gilad JM, Pebody R, Miah A, Calatayud L, Bolotin S, Vipond I, Muir P, Guiver M, McMenamin J, Reynolds A, Moore C, Gunson R, Thompson C, Galiano M, Bermingham A, Ellis J, Zambon M, Euro Surveill 2011 16 19784 21315056
13. Oseltamivir-resistant pandemic H1N1/2009 influenza virus possesses lower transmissibility and fitness in ferrets. Duan S, Boltz DA, Seiler P, Li J, Bragstad K, Nielsen LP, Webby RJ, Webster RG, Govorkova EA, PLoS Path 2010 6 1001022 10.1371/journal.ppat.1001022
14. Oseltamivir-resistant pandemic A/H1N1 virus is as virulent as its wild-type counterpart in mice and ferrets. Hamelin ME, Baz M, Abed Y, Couture C, Joubert P, Beaulieu E, Bellerose N, Plante M, Mallett C, Schumer G, Kobinger GP, Boivin G, PLoS Path 2010 6 1001015 10.1371/journal.ppat.1001015
15. Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Bloom JD, Gong LI, Baltimore D, Science 2010 328 1272 1275 10.1126/science.1187816 20522774
16. Effect of the neuraminidase mutation H274Y conferring resistance to oseltamivir on the replicative capacity and virulence of old and recent human influenza A(H1N1) viruses. Baz M, Abed Y, Simon P, Hamelin ME, Boivin G, J Infect Dis 2010 201 740 745 10.1086/650464 20100088
17. 2008-09 outbreaks in India reveals a third introduction and possible endemicity. Chakrabarti AK, Pawar SD, Cherian SS, Koratkar SS, Jadhav SM, Pal B, Thite V, Kode SS, Keng SS, Payyapilly BJ, Mullick J, Mishra AC, PLoS One 2009 4 7846 10.1371/journal.pone.0007846 19924254
18. Importance of neuraminidase active-site residues to the neuraminidase inhibitor resistance of influenza viruses. Yen H, Hoffmann E, Taylor G, Scholtissek C, Monto AS, Webster RG, Govorkova EA, J Virol 2006 80 8787 8795 10.1128/JVI.00477-06 16912325
19. Large-scale Sequence Analysis of Hemagglutinin of Influenza A Virus Identifies Conserved Regions Suitable for Targeting an Anti-Viral Response. Sahini L, Tempczyk-Russell A, Agarwal R, PLoS One 2010 5 9268 10.1371/journal.pone.0009268 20174650
20. Identification of novel conserved functional motifs across most influenza A viral strains. ElHefnawi M, AlAidi O, Mohamed N, Kamar M, El-Azab I, Zada S, Siam R, Virol J 2011 8 44 54 10.1186/1743-422X-8-44 21272360
21. Evolutionary conserved protein sequences of influenza A viruses, avian and human, as vaccine targets. Heiny AT, Miotto O, Srinivasan KN, Khan SM, Zhang GL, Brusic V, Tan TW, August JT, PLoS One 2007 11 1190
22. Genetic bottlenecks reduce population variation in an experimental RNA virus population. Li H, Roossinck MJ, J Virol 2004 78 10582 10587 10.1128/JVI.78.19.10582-10587.2004 15367625
23. Exponential increases of RNA virus fitness during large population transmissions. Novella IS, Duarte EA, Elena SF, Moya A, Domingo E, Holland JJ, PNAS 1995 92 5841 5844 10.1073/pnas.92.13.5841 7597039
24. Resistance of virus to extinction on bottleneck passages: Study of a decaying and fluctuating pattern of fitness loss. Lazaro E, Escarmis C, Perez-Mercader J, Manrubia SC, Domingo E, PNAS 2003 100 10830 10835 10.1073/pnas.1332668100 12960384
25. The evolution of human influenza A viruses from 1999 to 2006: a complete genome study. Bragstad K, Nielsen LP, Fomsgaard A, Virol J 2008 5 40 10.1186/1743-422X-5-40 18325125
26. Evaluation of Neuraminidase Enzyme Assays Using Different Substrates To Measure Susceptibility of Influenza Virus Clinical Isolates to Neuraminidase Inhibitors: Report of the Neuraminidase Inhibitor Susceptibility Network. Wetherall N, Trivedi T, Zeller J, Hodges-Savola C, McKimm-Breschkin J, Zambon M, Hayden FG, J Clin Microbiol 2003 41 742 750 10.1128/JCM.41.2.742-750.2003 12574276
27. Single reaction genome amplification accelerates sequencing and vaccine production for classical and swine origin human influenza A viruses. Zhou B, Donnelly ME, Scholes DT, Hatta M, Kawaoka Y, Wentworth DE, St. George K, J Virol 2009 83 10309 10313 10.1128/JVI.01109-09 19605485
28. Sequencing primers and protocol, 12 May 2009 http://www.who.int/csr/ resources/publications/swineflu/GenomePrimers-20090512
29. A simple method for the parallel deep sequencing of full influenza A genomes. Kampmann ML, Fordyce SL, Ávila-Arcos MC, Rasmussen M, Willerslev E, Nielsen LP, Gilbert MT, J Virol Methods 2011 178 243 248 10.1016/j.jviromet.2011.09.001 21946287
30. Fast and accurate short read alignment with Burrows-Wheeler Transform. Li H, Durbin R, Bioinformatics 2009 25 1754 1760 10.1093/bioinformatics/btp324 19451168
31. The Sequence alignment/map (SAM) format and SAMtools. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genomes Project Data Processing SubGroup, Bioinformatics 2009 25 2078 2079 10.1093/bioinformatics/btp352 19505943
32. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altschuler D, Gabriel S, Daly M, DePristo MA, Genome Res 2010 20 1297 1303 10.1101/gr.107524.110 20644199
33. A framework for variation discovery and genotyping using next-generation DNA sequencing data. DePristo M, Banks E, Poplin R, Garimella K, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ, Nat Genet 2011 43 491 498 10.1038/ng.806 21478889