Selective Bottlenecks Shape Evolutionary Pathways Taken during Mammalian Adaptation of a 1918-like Avian Influenza Virus

Cell Host and Microbe

Volumn 19, Issue 2, 2016, Pages 169-180

  Moncla, Louise H ^a,b   Zhong, Gongxun ^a   Nelson, Chase W ^c   Dinis, Jorge M ^a,b   Mutschler, James ^a,b   Hughes, Austin L ^c   Watanabe, Tokiko ^a,d   Kawaoka, Yoshihiro ^a,d   Friedrich, Thomas C ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ;

ARTICLE; AVIAN INFLUENZA VIRUS; BOTTLENECK POPULATION; CONTROLLED STUDY; FERRET; GENE MUTATION; GENETIC POLYMORPHISM; GENETIC REASSORTMENT; GENETIC VARIABILITY; HAPLOTYPE; MAMMAL; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SPANISH INFLUENZA; VIRUS REPLICATION; VIRUS TRANSMISSION; ADAPTATION; ANIMAL; AVIAN INFLUENZA; BIRD; EVOLUTION; GENETICS; HUMAN; INFLUENZA; INFLUENZA A VIRUS; METABOLISM; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY; TRANSMISSION; VIROLOGY;

ADAPTATION, BIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; BIRDS; FERRETS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; MAMMALS; ORTHOMYXOVIRIDAE INFECTIONS;

EID: 85011973238     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.01.011     Document Type: Article

References (48)

1. Baccam, P., Beauchemin, C., Macken, C.A., Hayden, F.G., Perelson, A.S., Kinetics of influenza A virus infection in humans. J. Virol. 80 (2006), 7590–7599.
2. Bailey, A.L., Lauck, M., Weiler, A., Sibley, S.D., Dinis, J.M., Bergman, Z., Nelson, C.W., Correll, M., Gleicher, M., Hyeroba, D., et al. High genetic diversity and adaptive potential of two simian hemorrhagic fever viruses in a wild primate population. PLoS ONE, 9, 2014, e90714.
3. Brown, R.J., Hudson, N., Wilson, G., Rehman, S.U., Jabbari, S., Hu, K., Tarr, A.W., Borrow, P., Joyce, M., Lewis, J., et al. Hepatitis C virus envelope glycoprotein fitness defines virus population composition following transmission to a new host. J. Virol. 86 (2012), 11956–11966.
4. Chandrasekaran, A., Srinivasan, A., Raman, R., Viswanathan, K., Raguram, S., Tumpey, T.M., Sasisekharan, V., Sasisekharan, R., Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin. Nat. Biotechnol. 26 (2008), 107–113.
5. Chinese SARS Molecular Epidemiology Consortium. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303 (2004), 1666–1669.
6. de Vries, R.P., Zhu, X., McBride, R., Rigter, A., Hanson, A., Zhong, G., Hatta, M., Xu, R., Yu, W., Kawaoka, Y., et al. Hemagglutinin receptor specificity and structural analyses of respiratory droplet-transmissible H5N1 viruses. J. Virol. 88 (2014), 768–773.
7. Drake, J.W., Holland, J.J., Mutation rates among RNA viruses. Proc. Natl. Acad. Sci. USA 96 (1999), 13910–13913.
8. Edo-Matas, D., Rachinger, A., Setiawan, L.C., Boeser-Nunnink, B.D., van ‘t Wout, A.B., Lemey, P., Schuitemaker, H., The evolution of human immunodeficiency virus type-1 (HIV-1) envelope molecular properties and coreceptor use at all stages of infection in an HIV-1 donor-recipient pair. Virology 422 (2012), 70–80.
9. Hamilton, M.B., Matrosovich, T.Y., Gray, T., Roberts, N.A., Klenk, H.D., Population Genetics. 2012, Wiley-Blackwell, Oxford, UK.
10. Imai, M., Watanabe, T., Hatta, M., Das, S.C., Ozawa, M., Shinya, K., Zhong, G., Hanson, A., Katsura, H., Watanabe, S., et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486 (2012), 420–428.
11. Jayaraman, A., Chandrasekaran, A., Viswanathan, K., Raman, R., Fox, J.G., Sasisekharan, R., Decoding the distribution of glycan receptors for human-adapted influenza A viruses in ferret respiratory tract. PLoS ONE, 7, 2012, e27517.
12. Karlsson, E.A., Meliopoulos, V.A., Savage, C., Livingston, B., Mehle, A., Schultz-Cherry, S., Visualizing real-time influenza virus infection, transmission and protection in ferrets. Nat. Commun., 6, 2015, 6378.
13. Kofler, R., Orozco-terWengel, P., De Maio, N., Pandey, R.V., Nolte, V., Futschik, A., Kosiol, C., Schlötterer, C., PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS ONE, 6, 2011, e15925.
14. Kong, W., Liu, L., Wang, Y., Gao, H., Wei, K., Sun, H., Sun, Y., Liu, J., Ma, G., Pu, J., Hemagglutinin mutation D222N of the 2009 pandemic H1N1 influenza virus alters receptor specificity without affecting virulence in mice. Virus Res. 189 (2014), 79–86.
15. Lakdawala, S.S., Jayaraman, A., Halpin, R.A., Lamirande, E.W., Shih, A.R., Stockwell, T.B., Lin, X., Simenauer, A., Hanson, C.T., Vogel, L., et al. The soft palate is an important site of adaptation for transmissible influenza viruses. Nature 526 (2015), 122–125.
16. Lauring, A.S., Andino, R., Quasispecies theory and the behavior of RNA viruses. PLoS Pathog., 6, 2010, e1001005.
17. Lauring, A.S., Acevedo, A., Cooper, S.B., Andino, R., Codon usage determines the mutational robustness, evolutionary capacity, and virulence of an RNA virus. Cell Host Microbe 12 (2012), 623–632.
18. Linster, M., van Boheemen, S., de Graaf, M., Schrauwen, E.J., Lexmond, P., Mänz, B., Bestebroer, T.M., Baumann, J., van Riel, D., Rimmelzwaan, G.F., et al. Identification, characterization, and natural selection of mutations driving airborne transmission of A/H5N1 virus. Cell 157 (2014), 329–339.
19. Mak, G.C., Au, K.W., Tai, L.S., Chuang, K.C., Cheng, K.C., Shiu, T.C., Lim, W., Association of D222G substitution in haemagglutinin of 2009 pandemic influenza A (H1N1) with severe disease. Euro Surveill., 15, 2010, 19534 author reply pii/19535.
20. Matos-Patrón, A., Byrd-Leotis, L., Steinhauer, D.A., Barclay, W.S., Ayora-Talavera, G., Amino acid substitution D222N from fatal influenza infection affects receptor-binding properties of the influenza A(H1N1)pdm09 virus. Virology 484 (2015), 15–21.
21. Matrosovich, M.N., Matrosovich, T.Y., Gray, T., Roberts, N.A., Klenk, H.D., Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc. Natl. Acad. Sci. USA 101 (2004), 4620–4624.
22. Nei, M., Gojobori, T., Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3 (1986), 418–426.
23. Nelson, C.W., Hughes, A.L., Within-host nucleotide diversity of virus populations: insights from next-generation sequencing. Infect. Genet. Evol. 30 (2015), 1–7.
24. Nelson, C.W., Moncla, L.H., Hughes, A.L., SNPGenie: estimating evolutionary parameters to detect natural selection using pooled next-generation sequencing data. Bioinformatics 31 (2015), 3709–3711.
25. Nielsen, R., Molecular signatures of natural selection. Annu. Rev. Genet. 39 (2005), 197–218.
26. Nobusawa, E., Sato, K., Comparison of the mutation rates of human influenza A and B viruses. J. Virol. 80 (2006), 3675–3678.
27. Parrish, C.R., Holmes, E.C., Morens, D.M., Park, E.C., Burke, D.S., Calisher, C.H., Laughlin, C.A., Saif, L.J., Daszak, P., Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol. Mol. Biol. Rev. 72 (2008), 457–470.
28. Parvin, J.D., Moscona, A., Pan, W.T., Leider, J.M., Palese, P., Measurement of the mutation rates of animal viruses: influenza A virus and poliovirus type 1. J. Virol. 59 (1986), 377–383.
29. Poon, L.L., Song, T., Rosenfeld, R., Lin, X., Rogers, M.B., Zhou, B., Sebra, R., Halpin, R.A., Guan, Y., Twaddle, A., et al. Quantifying influenza virus diversity and transmission in humans. Nat. Genet., 2016, 10.1038/ng.3479 Published online January 4, 2016.
30. Reid, A.H., Fanning, T.G., Hultin, J.V., Taubenberger, J.K., Origin and evolution of the 1918 “Spanish” influenza virus hemagglutinin gene. Proc. Natl. Acad. Sci. USA 96 (1999), 1651–1656.
31. Reid, A.H., Janczewski, T.A., Lourens, R.M., Elliot, A.J., Daniels, R.S., Berry, C.L., Oxford, J.S., Taubenberger, J.K., 1918 influenza pandemic caused by highly conserved viruses with two receptor-binding variants. Emerg. Infect. Dis. 9 (2003), 1249–1253.
32. Rogers, M.B., Song, T., Sebra, R., Greenbaum, B.D., Hamelin, M.E., Fitch, A., Twaddle, A., Cui, L., Holmes, E.C., Boivin, G., Ghedin, E., Intrahost dynamics of antiviral resistance in influenza A virus reflect complex patterns of segment linkage, reassortment, and natural selection. MBio, 6, 2015, 6.
33. Sanjuán, R., Nebot, M.R., Chirico, N., Mansky, L.M., Belshaw, R., Viral mutation rates. J. Virol. 84 (2010), 9733–9748.
34. Sheng, Z.M., Chertow, D.S., Ambroggio, X., McCall, S., Przygodzki, R.M., Cunningham, R.E., Maximova, O.A., Kash, J.C., Morens, D.M., Taubenberger, J.K., Autopsy series of 68 cases dying before and during the 1918 influenza pandemic peak. Proc. Natl. Acad. Sci. USA 108 (2011), 16416–16421.
35. Song, H.D., Tu, C.C., Zhang, G.W., Wang, S.Y., Zheng, K., Lei, L.C., Chen, Q.X., Gao, Y.W., Zhou, H.Q., Xiang, H., et al. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc. Natl. Acad. Sci. USA 102 (2005), 2430–2435.
36. Taubenberger, J.K., Reid, A.H., Krafft, A.E., Bijwaard, K.E., Fanning, T.G., Initial genetic characterization of the 1918 “Spanish” influenza virus. Science 275 (1997), 1793–1796.
37. Taubenberger, J.K., Reid, A.H., Janczewski, T.A., Fanning, T.G., Integrating historical, clinical and molecular genetic data in order to explain the origin and virulence of the 1918 Spanish influenza virus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356 (2001), 1829–1839.
38. Taubenberger, J.K., Reid, A.H., Lourens, R.M., Wang, R., Jin, G., Fanning, T.G., Characterization of the 1918 influenza virus polymerase genes. Nature 437 (2005), 889–893.
39. Thompson, C.I., Barclay, W.S., Zambon, M.C., Pickles, R.J., Infection of human airway epithelium by human and avian strains of influenza a virus. J. Virol. 80 (2006), 8060–8068.
40. Tumpey, T.M., Maines, T.R., Van Hoeven, N., Glaser, L., Solórzano, A., Pappas, C., Cox, N.J., Swayne, D.E., Palese, P., Katz, J.M., García-Sastre, A., A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 315 (2007), 655–659.
41. Vana, G., Westover, K.M., Origin of the 1918 Spanish influenza virus: a comparative genomic analysis. Mol. Phylogenet. Evol. 47 (2008), 1100–1110.
42. Varble, A., Albrecht, R.A., Backes, S., Crumiller, M., Bouvier, N.M., Sachs, D., García-Sastre, A., tenOever, B.R., Influenza A virus transmission bottlenecks are defined by infection route and recipient host. Cell Host Microbe 16 (2014), 691–700.
43. Watanabe, T., Zhong, G., Russell, C.A., Nakajima, N., Hatta, M., Hanson, A., McBride, R., Burke, D.F., Takahashi, K., Fukuyama, S., et al. Circulating avian influenza viruses closely related to the 1918 virus have pandemic potential. Cell Host Microbe 15 (2014), 692–705.
44. Wilker, P.R., Dinis, J.M., Starrett, G., Imai, M., Hatta, M., Nelson, C.W., O'Connor, D.H., Hughes, A.L., Neumann, G., Kawaoka, Y., Friedrich, T.C., Selection on haemagglutinin imposes a bottleneck during mammalian transmission of reassortant H5N1 influenza viruses. Nat. Commun., 4, 2013, 2636.
45. Worobey, M., Han, G.Z., Rambaut, A., Genesis and pathogenesis of the 1918 pandemic H1N1 influenza A virus. Proc. Natl. Acad. Sci. USA 111 (2014), 8107–8112.
46. Wu, C., Cheng, X., Wang, X., Lv, X., Yang, F., Liu, T., Fang, S., Zhang, R., Jinquan, C., Clinical and molecular characteristics of the 2009 pandemic influenza H1N1 infection with severe or fatal disease from 2009 to 2011 in Shenzhen, China. J. Med. Virol. 85 (2013), 405–412.
47. Zaraket, H., Baranovich, T., Kaplan, B.S., Carter, R., Song, M.S., Paulson, J.C., Rehg, J.E., Bahl, J., Crumpton, J.C., Seiler, J., et al. Mammalian adaptation of influenza A(H7N9) virus is limited by a narrow genetic bottleneck. Nat. Commun., 6, 2015, 6553.
48. Zhang, C.Y., Wei, J.F., He, S.H., Adaptive evolution of the spike gene of SARS coronavirus: changes in positively selected sites in different epidemic groups. BMC Microbiol., 6, 2006, 88.