Human-like PB2 627K Influenza Virus Polymerase Activity Is Regulated by Importin-α1 and -α7

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Influenza A viruses may cross species barriers and transmit to humans with the potential to cause pandemics. Interplay of human- (PB2 627K) and avian-like (PB2 627E) influenza polymerase complexes with unknown host factors have been postulated to play a key role in interspecies transmission. Here, we have identified human importin-α isoforms (α1 and α7) as positive regulators of human- but not avian-like polymerase activity. Human-like polymerase activity correlated with efficient recruitment of α1 and α7 to viral ribonucleoprotein complexes (vRNPs) without affecting subcellular localization. We also observed that human-like influenza virus growth was impaired in α1 and α7 downregulated human lung cells. Mice lacking α7 were less susceptible to human- but not avian-like influenza virus infection. Thus, α1 and α7 are positive regulators of human-like polymerase activity and pathogenicity beyond their role in nuclear transport.

Vyšlo v časopise: Human-like PB2 627K Influenza Virus Polymerase Activity Is Regulated by Importin-α1 and -α7. PLoS Pathog 8(1): e32767. doi:10.1371/journal.ppat.1002488
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002488

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1. MatrosovichMNMatrosovichTYGrayTRobertsNAKlenkHD 2004 Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci U S A 101 4620 4624

2. ShinyaKEbinaMYamadaSOnoMKasaiN 2006 Avian flu: influenza virus receptors in the human airway. Nature 440 435 436

3. GabrielGDauberBWolffTPlanzOKlenkHD 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

4. GabrielGHerwigAKlenkHD 2008 Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog 4 e11

5. GabrielGKlingelKOtteAThieleSHudjetzB 2011 Differential use of importin-alpha isoforms governs cell tropism and host adaptation of influenza virus. Nat Commun 2 156

6. SubbaraoKKlimovAKatzJRegneryHLimW 1998 Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279 393 396

7. ChenHLiYLiZShiJShinyaK 2006 Properties and dissemination of H5N1 viruses isolated during an influenza outbreak in migratory waterfowl in western China. J Virol 80 5976 5983

8. HattaMGaoPHalfmannPKawaokaY 2001 Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293 1840 1842

9. ShinyaKHammSHattaMItoHItoT 2004 PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. Virology 320 258 266

10. LabadieKDos Santos AfonsoERameix-WeltiMAvan der WerfSNaffakhN 2007 Host-range determinants on the PB2 protein of influenza A viruses control the interaction between the viral polymerase and nucleoprotein in human cells. Virology 362 271 282

11. MehleADoudnaJA 2008 An inhibitory activity in human cells restricts the function of an avian-like influenza virus polymerase. Cell Host Microbe 4 111 122

12. MoncorgeOMuraMBarclayWS 2010 Evidence for avian and human host cell factors that affect the activity of influenza virus polymerase. J Virol 84 9978 9986

13. KonigRStertzSZhouYInoueAHoffmannHH 2010 Human host factors required for influenza virus replication. Nature 463 813 817

14. BortzEWesteraLMaamaryJSteelJAlbrechtRA 2011 Host- and strain-specific regulation of influenza virus polymerase activity by interacting cellular proteins. MBio 2 e00151-11

15. TarendeauFCrepinTGuilligayDRuigrokRWCusackS 2008 Host determinant residue lysine 627 lies on the surface of a discrete, folded domain of influenza virus polymerase PB2 subunit. PLoS Pathog 4 e1000136

16. BoivinSHartDJ 2011 Interaction of the Influenza A Virus Polymerase PB2 C-terminal Region with Importin {alpha} Isoforms Provides Insights into Host Adaptation and Polymerase Assembly. J Biol Chem 286 10439 10448

17. LaskeyRAGorlichDMadineMAMakkerhJPRomanowskiP 1996 Regulatory roles of the nuclear envelope. Exp Cell Res 229 204 211

18. MattajIWEnglmeierL 1998 Nucleocytoplasmic transport: the soluble phase. Annu Rev Biochem 67 265 306

19. SteelJLowenACMubarekaSPaleseP 2009 Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog 5 e1000252

20. FriedrichBQuenselCSommerTHartmannEKohlerM 2006 Nuclear localization signal and protein context both mediate importin alpha specificity of nuclear import substrates. Mol Cell Biol 26 8697 8709

21. DengTEngelhardtOGThomasBAkoulitchevAVBrownleeGG 2006 Role of ran binding protein 5 in nuclear import and assembly of the influenza virus RNA polymerase complex. J Virol 80 11911 11919

22. FodorESmithM 2004 The PA subunit is required for efficient nuclear accumulation of the PB1 subunit of the influenza A virus RNA polymerase complex. J Virol 78 9144 9153

23. HuetSAvilovSVFerbitzLDaigleNCusackS 2010 Nuclear import and assembly of influenza A virus RNA polymerase studied in live cells by fluorescence cross-correlation spectroscopy. J Virol 84 1254 1264

24. FoegleinALoucaidesEMMuraMWiseHMBarclayWS 2011 Influence of PB2 host-range determinants on the intranuclear mobility of the influenza A virus polymerase. J Gen Virol 92 1650 1661

25. Rameix-WeltiMATomoiuADos Santos AfonsoEvan der WerfSNaffakhN 2009 Avian Influenza A virus polymerase association with nucleoprotein, but not polymerase assembly, is impaired in human cells during the course of infection. J Virol 83 1320 1331

26. JakelSMingotJMSchwarzmaierPHartmannEGorlichD 2002 Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains. EMBO J 21 377 386

27. DiasSMCerioneRAWilsonKF 2010 Unloading RNAs in the cytoplasm: An “importin” task. Nucleus 1 139 143

28. Resa-InfantePJorbaNZamarrenoNFernandezYJuarezS 2008 The host-dependent interaction of alpha-importins with influenza PB2 polymerase subunit is required for virus RNA replication. PLoS One 3 e3904

29. TarendeauFBoudetJGuilligayDMasPJBougaultCM 2007 Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nat Struct Mol Biol 14 229 233

30. RotherFShmidtTPopovaEKrivokharchenkoAHugelS 2011 Importin alpha7 is essential for zygotic genome activation and early mouse development. PLoS One 6 e18310

31. HoffmannENeumannGKawaokaYHobomGWebsterRG 2000 A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A 97 6108 6113

32. GabrielGKlingelKPlanzOBierKHerwigA 2009 Spread of infection and lymphocyte depletion in mice depends on polymerase of influenza virus. Am J Pathol 175 1178 1186

33. ReedLHMuenchH 1938 A simple method of estimating fifty percent endpoints. Am J Hyg 27 493 497