Characterization of Uncultivable Bat Influenza Virus Using a Replicative Synthetic Virus


The identification of influenza virus-like sequences in two different bat species has generated great interest in understanding their biology, ability to mix with other influenza viruses, and their public health threat. Unfortunately, bat-influenza viruses couldn't be cultured from the samples containing the influenza-like nucleic acids. We used synthetic genomics strategies to create wild type bat-influenza, or bat-influenza modified by substituting the surface glycoproteins with those of model influenza A viruses. Although influenza virus-like particles were produced from both synthetic genomes, only the modified bat-influenza viruses could be cultured. The modified bat-influenza viruses replicated efficiently in vitro and an H1N1 modified version caused severe disease in mice. Collectively our data show: (1) the two bat-flu genomes identified in other studies are replication competent, suggesting that host cell specificity is the major limitation for propagation of bat-influenza, (2) bat-influenza NS1 antagonizes host interferon response more efficiently than that of a model influenza A virus, (3) bat-influenza has both genetic and protein incompatibility with influenza A or B viruses, and (4) that these bat-influenza lineages pose little pandemic threat.


Vyšlo v časopise: Characterization of Uncultivable Bat Influenza Virus Using a Replicative Synthetic Virus. PLoS Pathog 10(10): e32767. doi:10.1371/journal.ppat.1004420
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.ppat.1004420

Souhrn

The identification of influenza virus-like sequences in two different bat species has generated great interest in understanding their biology, ability to mix with other influenza viruses, and their public health threat. Unfortunately, bat-influenza viruses couldn't be cultured from the samples containing the influenza-like nucleic acids. We used synthetic genomics strategies to create wild type bat-influenza, or bat-influenza modified by substituting the surface glycoproteins with those of model influenza A viruses. Although influenza virus-like particles were produced from both synthetic genomes, only the modified bat-influenza viruses could be cultured. The modified bat-influenza viruses replicated efficiently in vitro and an H1N1 modified version caused severe disease in mice. Collectively our data show: (1) the two bat-flu genomes identified in other studies are replication competent, suggesting that host cell specificity is the major limitation for propagation of bat-influenza, (2) bat-influenza NS1 antagonizes host interferon response more efficiently than that of a model influenza A virus, (3) bat-influenza has both genetic and protein incompatibility with influenza A or B viruses, and (4) that these bat-influenza lineages pose little pandemic threat.


Zdroje

1. CalisherCH, ChildsJE, FieldHE, HolmesKV, SchountzT (2006) Bats: important reservoir hosts of emerging viruses. Clin Microbiol Rev 19: 531–545.

2. GeXY, LiJL, YangXL, ChmuraAA, ZhuG, et al. (2013) Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503: 535–538.

3. TongS, LiY, RivaillerP, ConrardyC, CastilloDA, et al. (2012) A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci U S A 109: 4269–4274.

4. TongS, ZhuX, LiY, ShiM, ZhangJ, et al. (2013) New world bats harbor diverse influenza A viruses. PLoS Pathog 9: e1003657.

5. WuY, TefsenB, ShiY, GaoGF (2014) Bat-derived influenza-like viruses H17N10 and H18N11. Trends Microbiol 22 (4) 183–91.

6. LiQ, SunX, LiZ, LiuY, VavrickaCJ, et al. (2012) Structural and functional characterization of neuraminidase-like molecule N10 derived from bat influenza A virus. Proc Natl Acad Sci U S A 109: 18897–18902.

7. ZhuX, YangH, GuoZ, YuW, CarneyPJ, et al. (2012) Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site. Proc Natl Acad Sci U S A 109: 18903–18908.

8. ZhuX, YuW, McBrideR, LiY, ChenLM, et al. (2013) Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc Natl Acad Sci U S A 110: 1458–1463.

9. SunX, ShiY, LuX, HeJ, GaoF, et al. (2013) Bat-derived influenza hemagglutinin H17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Cell Rep 3: 769–778.

10. TefsenB, LuG, ZhuY, HaywoodJ, ZhaoL, et al. (2014) The N-terminal domain of PA from bat-derived influenza-like virus H17N10 has endonuclease activity. J Virol 88: 1935–1941.

11. Garcia-SastreA (2012) The neuraminidase of bat influenza viruses is not a neuraminidase. Proc Natl Acad Sci U S A 109: 18635–18636.

12. WatanabeT, WatanabeS, NodaT, FujiiY, KawaokaY (2003) Exploitation of nucleic acid packaging signals to generate a novel influenza virus-based vector stably expressing two foreign genes. J Virol 77: 10575–10583.

13. GaoQ, PaleseP (2009) Rewiring the RNAs of influenza virus to prevent reassortment. Proc Natl Acad Sci U S A 106: 15891–15896.

14. SolorzanoA, WebbyRJ, LagerKM, JankeBH, Garcia-SastreA, et al. (2005) Mutations in the NS1 protein of swine influenza virus impair anti-interferon activity and confer attenuation in pigs. J Virol 79: 7535–7543.

15. RamananP, EdwardsMR, ShabmanRS, LeungDW, Endlich-FrazierAC, et al. (2012) Structural basis for Marburg virus VP35-mediated immune evasion mechanisms. Proc Natl Acad Sci U S A 109: 20661–20666.

16. LeungDW, PrinsKC, BorekDM, FarahbakhshM, TufarielloJM, et al. (2010) Structural basis for dsRNA recognition and interferon antagonism by Ebola VP35. Nat Struct Mol Biol 17: 165–172.

17. ValmasC, GroschMN, SchumannM, OlejnikJ, MartinezO, et al. (2010) Marburg virus evades interferon responses by a mechanism distinct from ebola virus. PLoS Pathog 6: e1000721.

18. ReidSP, ValmasC, MartinezO, SanchezFM, BaslerCF (2007) Ebola virus VP24 proteins inhibit the interaction of NPI-1 subfamily karyopherin alpha proteins with activated STAT1. J Virol 81: 13469–13477.

19. HaleBG, RandallRE, OrtinJ, JacksonD (2008) The multifunctional NS1 protein of influenza A viruses. J Gen Virol 89: 2359–2376.

20. TalonJ, SalvatoreM, O'NeillRE, NakayaY, ZhengH, et al. (2000) Influenza A and B viruses expressing altered NS1 proteins: A vaccine approach. Proc Natl Acad Sci U S A 97: 4309–4314.

21. QuinlivanM, ZamarinD, Garcia-SastreA, CullinaneA, ChambersT, et al. (2005) Attenuation of equine influenza viruses through truncations of the NS1 protein. Journal of Virology 79: 8431–8439.

22. ZhouB, LiY, BelserJA, PearceMB, SchmolkeM, et al. (2010) NS-based live attenuated H1N1 pandemic vaccines protect mice and ferrets. Vaccine 28: 8015–8025.

23. ZhouB, LiY, HalpinR, HineE, SpiroDJ, et al. (2011) PB2 residue 158 is a pathogenic determinant of pandemic H1N1 and H5 influenza a viruses in mice. J Virol 85: 357–365.

24. SubbaraoEK, LondonW, MurphyBR (1993) A single amino acid in the PB2 gene of influenza A virus Is a determinant of host range. Journal of Virology 67: 1761–1764.

25. GaoY, ZhangY, ShinyaK, DengG, JiangY, et al. (2009) Identification of amino acids in HA and PB2 critical for the transmission of H5N1 avian influenza viruses in a mammalian host. PLoS Pathog 5: e1000709.

26. LiZ, ChenH, JiaoP, DengG, TianG, et al. (2005) Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 79: 12058–12064.

27. HattaM, GaoP, HalfmannP, KawaokaY (2001) Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293: 1840–1842.

28. GabrielG, DauberB, WolffT, PlanzO, KlenkHD, et al. (2005) The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A 102: 18590–18595.

29. ZhouB, PearceMB, LiY, WangJ, MasonRJ, et al. (2013) Asparagine Substitution at PB2 Residue 701 Enhances the Replication, Pathogenicity, and Transmission of the 2009 Pandemic H1N1 Influenza A Virus. PLoS ONE 8: e67616.

30. DlugolenskiD, JonesL, TompkinsSM, CrameriG, WangLF, et al. (2013) Bat cells from Pteropus alecto are susceptible to influenza A virus infection and reassortment. Influenza Other Respir Viruses 7: 900–903.

31. HoffmannM, MullerMA, DrexlerJF, GlendeJ, ErdtM, et al. (2013) Differential sensitivity of bat cells to infection by enveloped RNA viruses: coronaviruses, paramyxoviruses, filoviruses, and influenza viruses. PLoS One 8: e72942.

32. DormitzerPR, SuphaphiphatP, GibsonDG, WentworthDE, StockwellTB, et al. (2013) Synthetic generation of influenza vaccine viruses for rapid response to pandemics. Sci Transl Med 5: 185ra168.

33. LiuQ, ZhouB, MaW, BawaB, MaJ, et al. (2014) Analysis of Recombinant H7N9 Wild-Type and Mutant Viruses in Pigs Shows that the Q226L Mutation in HA Is Important for Transmission. J Virol 88: 8153–8165.

34. ZhouB, LinX, WangW, HalpinRA, BeraJ, et al. (2014) Universal influenza B virus genomic amplification facilitates sequencing, diagnostics, and reverse genetics. J Clin Microbiol 52: 1330–1337.

35. ZhouB, DonnellyME, ScholesDT, St GeorgeK, HattaM, et al. (2009) Single-reaction genomic amplification accelerates sequencing and vaccine production for classical and Swine origin human influenza a viruses. J Virol 83: 10309–10313.

36. ZhouB, WentworthDE (2012) Influenza A virus molecular virology techniques. Methods Mol Biol 865: 175–192.

37. NakamuraK, OshimaT, MorimotoT, IkedaS, YoshikawaH, et al. (2011) Sequence-specific error profile of Illumina sequencers. Nucleic Acids Res 39: e90.

38. ChandranK, SullivanNJ, FelborU, WhelanSP, CunninghamJM (2005) Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308: 1643–1645.

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2014 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Eozinofilní granulomatóza s polyangiitidou
nový kurz

Betablokátory a Ca antagonisté z jiného úhlu
Autori: prof. MUDr. Michal Vrablík, Ph.D., MUDr. Petr Janský

Autori: doc. MUDr. Petr Čáp, Ph.D.

Farmakoterapie akutní a chronické bolesti

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Nemáte účet?  Registrujte sa

Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa