Reassortment between Influenza B Lineages and the Emergence of a Coadapted PB1-PB2-HA Gene Complex

Molecular Biology and Evolution

Volumn 32, Issue 1, 2015, Pages 162-172

  Dudas, Gytis ^a   Bedford, Trevor ^b   Lycett, Samantha ^a,c   Rambaut, Andrew ^a,d  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b USA   (United States)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Evolution; Influenza; Phylogenetics; Reassortment; Speciation

Indexed keywords

HEMAGGLUTININ; POLYMERASE BASIC 1 PROTEIN; POLYMERASE BASIC 2 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; INFLUENZA VIRUS HEMAGGLUTININ; INFLUENZA VIRUS POLYMERASE BASIC PROTEIN 1; PB2 PROTEIN, INFLUENZA VIRUS;

ARTICLE; GENETIC CODE; GENETIC REASSORTMENT; GENETIC VARIABILITY; INFLUENZA VIRUS B; NONHUMAN; PHYLOGENETIC TREE; VIRUS STRAIN; BIOLOGY; BLOOD; CLASSIFICATION; GENETIC SELECTION; GENETICS; HUMAN; INFLUENZA; INFLUENZA B VIRUS; MOLECULAR EVOLUTION; PHYLOGENY; PROCEDURES; SPECIES DIFFERENTIATION; VIROLOGY; VIRUS GENOME;

INFLUENZA B VIRUS;

COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENETIC SPECIATION; GENOME, VIRAL; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA B VIRUS; INFLUENZA, HUMAN; PHYLOGENY; SELECTION, GENETIC; VIRAL PROTEINS;

EID: 84922052901     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu287     Document Type: Article

References (49)

1. Ansaldi F, D'Agaro P, de Florentiis D, Puzelli S, Lin YP, Gregory V, Bennett M, Donatelli I, Gasparini R, Crovari P, et al. 2003. Molecular characterization of influenza B viruses circulating in northern Italy during the 2001-2002 epidemic season. J Med Virol 70: 463-469.
2. Bedford T, Cobey S, Pascual M. 2011. Strength and tempo of selection revealed in viral gene genealogies. BMC Evol Biol. 11: 220.
3. Bedford T, Suchard MA, Lemey P, Dudas G, Gregory V, Hay AJ, McCauley JW, Russell CA, Smith DJ, Rambaut A. 2014. Integrating influenza antigenic dynamics with molecular evolution. eLife 3: p. e01914.
4. Bergeron C, Valette M, Lina B, Ottmann M. 2010. Genetic content of influenza H3N2 vaccine seeds. PLoS Curr. 2: RRN1165.
5. Bodewes R, Morick D, de Mutsert G, Osinga N, Bestebroer T, van der Vliet S, Smits SL, Kuiken T, Rimmelzwaan GF, Fouchier RA, et al. 2013. Recurring influenza B virus infections in seals. Emerg Infect Dis. 19: 511-512.
6. Bogner P, Capua I, Lipman DJ, Cox NJ, et al. 2006. A global initiative on sharing avian flu data. Nature 442: 981.
7. Boni MF, Zhou Y, Taubenberger JK, Holmes EC. 2008. Homologous recombination is very rare or absent in human influenza A virus. J Virol. 82: 4807-4811.
8. Broberg E, Beauté J, Snacken R 2013. Fortnightly influenza surveillance overview, 24 May 2013 -weeks 19-20/2013. Available from: http: //ecdc.europa.eu/en/publications/Publications/influenza-fort nightly-surveillance-overview-24-may-2013.pdf.
9. Burnet SFM. 1955. Principles of animal virology. New York: Academic Press.
10. Chare ER, Gould EA, Holmes EC. 2003. Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. J Gen Virol. 84: 2691-2703.
11. Chen R, Holmes EC. 2008. The evolutionary dynamics of human influenza B virus. J Mol Evol. 66: 655-663.
12. Cobbin JCA, Verity EE, Gilbertson BP, Rockman SP, Brown LE. 2013. The source of the PB1 gene in influenza vaccine reassortants selectively alters the hemagglutinin content of the resulting seed virus. J Virol. 87: 5577-5585.
13. Dobzhansky T. 1937. Genetics and the origin of species. New York: Columbia University Press.
14. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4: e88.
15. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 29: 1969-1973.
16. Fulvini AA, Ramanunninair M, Le J, Pokorny BA, Arroyo JM, Silverman J,Devis R, Bucher D. 2011. Gene constellation of influenza A virus reassortants with high growth phenotype prepared as seed candidates for vaccine production. PLoS One 6: e20823.
17. Gregory V, Bennett M, Orkhan M, Hajjar SA, Varsano N, Mendelson E,Zambon M, Ellis J, Hay A, Lin Y. 2002. Emergence of influenza A H1N2 reassortant viruses in the human population during 2001. Virology 300: 1-7.
18. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52: 696-704.
19. Han GZ, Boni MF, Li SS. 2010. No observed effect of homologous recombination on influenza C virus evolution. Virol J. 7: 227.
20. Hasegawa M, Kishino H, Yano TA. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 22: 160-174.
21. Hay AJ, Gregory V, Douglas AR, Lin YP. 2001. The evolution of human influenza viruses. Philos Trans R Soc Lond B Biol Sci. 356: 1861-1870.
22. Hedrick PW, Thomson G. 1986. A two-locus neutrality test: applications to humans, E. coli and lodgepole pine. Genetics 112: 135-156.
23. Hoffmann E,Mahmood K, Yang CF,Webster RG, Greenberg HB, Kemble G. 2002. Rescue of influenza B virus from eight plasmids. Proc Natl Acad Sci U S A. 99: 11411-11416.
24. Kanegae Y, Sugita S, Endo A, IshidaM, Senya S,Osako K, Nerome K, Oya A. 1990. Evolutionary pattern of the hemagglutinin gene of influenza B viruses isolated in Japan: cocirculating lineages in the same epidemic season. J Virol. 64: 2860-2865.
25. Kawaoka Y, Krauss S, Webster RG. 1989. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J Virol. 63: 4603-4608.
26. Lee HY, Chou JY, Cheong L, Chang NH, Yang SY, Leu JY. 2008. Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135: 1065-1073.
27. Lemey P, Rambaut A, Drummond AJ, Suchard MA. 2009. Bayesian phylogeography finds its roots. PLoS Comput Biol. 5: e1000520.
28. Lewontin RC. 1964. The interaction of selection and linkage. I. general considerations; heterotic models. Genetics 49: 49-67.
29. Lindstrom SE, Hiromoto Y, Nishimura H, Saito T, Nerome R, Nerome K. 1999. Comparative analysis of evolutionarymechanisms of the hemagglutinin and three internal protein genes of influenza B virus: multiple cocirculating lineages and frequent reassortment of the NP, m, and NS genes. J Virol. 73: 4413-4426.
30. Longdon B, Hadfield JD, Webster CL, Obbard DJ, Jiggins FM. 2011. Host phylogeny determines viral persistence and replication in novel hosts. PLoS Pathog. 7: e1002260.
31. Lu L, Lycett SJ, Brown AJL. 2014. Reassortment patterns of avian influenza virus internal segments among different subtypes. BMC Evol Biol. 14: 16.
32. Lycett SJ, Baillie G, Coulter E, Bhatt S, Kellam P, McCauley JW, Wood JL, Brown IH, Pybus OG, Leigh Brown AJ Combating Swine Influenza Initiative-COSI Consortium. 2012. Estimating reassortment rates in co-circulating Eurasian swine influenza viruses. J Gen Virol. 93: 2326-2336.
33. Minin VN, Bloomquist EW, Suchard MA. 2008. Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol Biol Evol. 25: 1459-1471.
34. Muller H. 1942. Isolating mechanisms, evolution and temeperature. Biol Symp. 6: 71-125.
35. Nakagawa N, Nukuzuma S, Haratome S, Go S, Nakagawa T, Hayashi K. 2002. Emergence of an influenza B virus with antigenic change. J Clin Microbiol. 40: 3068-3070.
36. Nerome R, Hiromoto Y, Sugita S, Tanabe N, Ishida M, Matsumoto M,Lindstrom SE, Takahashi T, Nerome K. 1998. Evolutionary characteristics of influenza B virus since its first isolation in 1940: dynamic circulation of deletion and insertion mechanism. Arch Virol. 143: 1569-1583.
37. O'Brien JD, Minin VN, Suchard MA. 2009. Learning to count: robust estimates for labeled distances between molecular sequences. Mol Biol Evol. 26: 801-814.
38. Osterhaus ADME, Rimmelzwaan GF, Martina BEE, Bestebroer TM,Fouchier RAM. 2000. Influenza B virus in seals. Science 288: 1051-1053.
39. Presgraves DC. 2010. The molecular evolutionary basis of species formation. Nat Rev Genet. 11: 175-180.
40. Rambaut A, Suchard M, Drummond A 2009. Tracer v1.5. [Internet]. Available from: http: //tree.bio.ed.ac.uk/software/tracer/.
41. Reed C, Meltzer MI, Finelli L, Fiore A. 2012. Public health impact of including two lineages of influenza B in a quadrivalent seasonal influenza vaccine. Vaccine 30: 1993-1998.
42. Rota PA, Wallis TR, Harmon MW, Rota JS, Kendal AP, Nerome K. 1990. Cocirculation of two distinct evolutionary lineages of influenza type B virus since 1983. Virology 175: 59-68.
43. Ruane S, Pyron RA, Burbrink FT. 2011. Phylogenetic relationships of the cretaceous frog Beelzebufo from Madagascar and the placement of fossil constraints based on temporal and phylogenetic evidence. J Evol Biol. 24: 274-285.
44. Shaw MW, Xu X, Li Y, Normand S, Ueki RT, Kunimoto GY, Hall H, Klimov A, Cox NJ, Subbarao K. 2002. Reappearance and global spread of variants of influenza B/Victoria/2/87 lineage viruses in the 2000-2001 and 2001-2002 seasons. Virology 303: 1-8.
45. Smith GJD, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, et al. 2009. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459: 1122-1125.
46. Turner TL, Hahn MW, Nuzhdin SV. 2005. Genomic islands of speciation in Anopheles gambiae. PLoS Biol. 3: e285.
47. Ward MJ, Lycett SJ, Kalish ML, Rambaut A, Brown AJL. 2013. Estimating the rate of intersubtype recombination in early HIV-1 group M strains. J Virol. 87: 1967-1973.
48. World Health Organization. 2009. Influenza fact sheet. Available from: http: //www.who.int/mediacentre/factsheets/fs211/en/.
49. Zhao H, Nettleton D, Soller M, Dekkers JCM. 2005. Evaluation of linkage disequilibrium measures between multi-allelic markers as predictors of linkage disequilibrium between markers and QTL. Genet Res. 86: 77-87