Cryotomography of Budding Influenza A Virus Reveals Filaments with Diverse Morphologies that Mostly Do Not Bear a Genome at Their Distal End

English version České info

Influenza viruses exhibit striking variations in particle morphology between strains. Clinical isolates of influenza A virus have been shown to produce long filamentous particles while laboratory-adapted strains are predominantly spherical. However, the role of the filamentous phenotype in the influenza virus infectious cycle remains undetermined. We used cryo-electron tomography to conduct the first three-dimensional study of filamentous virus ultrastructure in particles budding from infected cells. Filaments were often longer than 10 microns and sometimes had bulbous heads at their leading ends, some of which contained tubules we attribute to M1 while none had recognisable ribonucleoprotein (RNP) and hence genome segments. Long filaments that did not have bulbs were infrequently seen to bear an ordered complement of RNPs at their distal ends. Imaging of purified virus also revealed diverse filament morphologies; short rods (bacilliform virions) and longer filaments. Bacilliform virions contained an ordered complement of RNPs while longer filamentous particles were narrower and mostly appeared to lack this feature, but often contained fibrillar material along their entire length. The important ultrastructural differences between these diverse classes of particles raise the possibility of distinct morphogenetic pathways and functions during the infectious process.

Vyšlo v časopise: Cryotomography of Budding Influenza A Virus Reveals Filaments with Diverse Morphologies that Mostly Do Not Bear a Genome at Their Distal End. PLoS Pathog 9(6): e32767. doi:10.1371/journal.ppat.1003413
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003413

Souhrn

Zdroje

1. Palese P, Shaw ML (2007) Orthomyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM, editors. Fields Virology. 5th ed. Philadelphia: Lippincott, Williams and Wilkins. pp. 1647–1689.

2. McGeochD, FellnerP, NewtonC (1976) Influenza virus genome consists of eight distinct RNA species. Proc Natl Acad Sci U S A 73: 3045–3049.

3. PaleseP, SchulmanJL (1976) Differences in RNA patterns of influenza A viruses. J Virol 17: 876–884.

4. ScholtissekC, HarmsE, RohdeW, OrlichM, RottR (1976) Correlation between RNA fragments of fowl plague virus and their corresponding gene functions. Virology 74: 332–344.

5. LambRA, ChoppinPW (1981) Identification of a second protein (M2) encoded by RNA segment 7 of influenza virus. Virology 112: 729–737.

6. LambRA, ChoppinPW (1979) Segment 8 of the influenza virus genome is unique in coding for two polypeptides. Proc Natl Acad Sci U S A 76: 4908–4912.

7. FujiiY, GotoH, WatanabeT, YoshidaT, KawaokaY (2003) Selective incorporation of influenza virus RNA segments into virions. Proc Natl Acad Sci U S A 100: 2002–2007.

8. GogJR, Afonso EdosS, DaltonRM, LeclercqI, TileyL, et al. (2007) Codon conservation in the influenza A virus genome defines RNA packaging signals. Nucleic Acids Res 35: 1897–1907.

9. ChuCM, DawsonIM, ElfordWJ (1949) Filamentous forms associated with newly isolated influenza virus. Lancet 1: 602.

10. EddyBE, WyckoffRW (1950) Influenza virus in sectioned tissues. Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine 75: 290–293.

11. EllemanCJ, BarclayWS (2004) The M1 matrix protein controls the filamentous phenotype of influenza A virus. Virology 321: 144–153.

12. ArchettiI (1955) Appearances associated with filamentous forms of influenza viruses. Archiv fur die gesamte Virusforschung 6: 29–35.

13. HarrisA, CardoneG, WinklerDC, HeymannJB, BrecherM, et al. (2006) Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc Natl Acad Sci U S A 103: 19123–19127.

14. ChenBJ, LeserGP, MoritaE, LambRA (2007) Influenza virus hemagglutinin and neuraminidase, but not the matrix protein, are required for assembly and budding of plasmid-derived virus-like particles. J Virol 81: 7111–7123.

15. AliA, AvalosRT, PonimaskinE, NayakDP (2000) Influenza virus assembly: effect of influenza virus glycoproteins on the membrane association of M1 protein. J Virol 74: 8709–8719.

16. RobertsPC, LambRA, CompansRW (1998) The M1 and M2 proteins of influenza A virus are important determinants in filamentous particle formation. Virology 240: 127–137.

17. BurleighLM, CalderLJ, SkehelJJ, SteinhauerDA (2005) Influenza a viruses with mutations in the m1 helix six domain display a wide variety of morphological phenotypes. J Virol 79: 1262–1270.

18. RobertsPC, CompansRW (1998) Host cell dependence of viral morphology. Proc Natl Acad Sci U S A 95: 5746–5751.

19. LoneyC, Mottet-OsmanG, RouxL, BhellaD (2009) Paramyxovirus ultrastructure and genome packaging: Cryo-electron tomography of Sendai virus. J Virol 83: 8191–8197.

20. BharatTA, NodaT, RichesJD, KraehlingV, KolesnikovaL, et al. (2012) Structural dissection of Ebola virus and its assembly determinants using cryo-electron tomography. Proc Natl Acad Sci U S A 109: 4275–4280.

21. CalderLJ, WasilewskiS, BerrimanJA, RosenthalPB (2010) Structural organization of a filamentous influenza A virus. Proc Natl Acad Sci U S A 107: 10685–10690.

22. NodaT, SagaraH, YenA, TakadaA, KidaH, et al. (2006) Architecture of ribonucleoprotein complexes in influenza A virus particles. Nature 439: 490–492.

23. FournierE, MoulesV, EssereB, PaillartJC, SirbatJD, et al. (2012) A supramolecular assembly formed by influenza A virus genomic RNA segments. Nucleic Acids Res 40: 2197–2209.

24. NodaT, SugitaY, AoyamaK, HiraseA, KawakamiE, et al. (2012) Three-dimensional analysis of ribonucleoprotein complexes in influenza A virus. Nat Commun 3: 639.

25. DoceulV, HollinsheadM, van der LindenL, SmithGL (2010) Repulsion of superinfecting virions: a mechanism for rapid virus spread. Science 327: 873–876.

26. LiljeroosL, HuiskonenJT, OraA, SusiP, ButcherSJ (2011) Electron cryotomography of measles virus reveals how matrix protein coats the ribonucleocapsid within intact virions. Proc Natl Acad Sci U S A 108: 18085–18090.

27. RuigrokRW, CalderLJ, WhartonSA (1989) Electron microscopy of the influenza virus submembranal structure. Virology 173: 311–316.

28. HoyleL (1950) The multiplication of influenza viruses in the fertile egg: A Report to the Medical Research Council. J Hyg (Lond) 48: 277–297.

29. CompansRW, ContentJ, DuesbergPH (1972) Structure of the ribonucleoprotein of influenza virus. J Virol 10: 795–800.

30. ArranzR, ColomaR, ChichonFJ, ConesaJJ, CarrascosaJL, et al. (2012) The structure of native influenza virion ribonucleoproteins. Science 338: 1634–1637.

31. MoellerA, KirchdoerferRN, PotterCS, CarragherB, WilsonIA (2012) Organization of the influenza virus replication machinery. Science 338: 1631–1634.

32. RossmanJS, LambRA (2011) Influenza virus assembly and budding. Virology 411: 229–236.

33. RossmanJS, LeserGP, LambRA (2012) Filamentous influenza virus enters cells via macropinocytosis. J Virol 86: 10950–10960.

34. GengY, DalhaimerP, CaiS, TsaiR, TewariM, et al. (2007) Shape effects of filaments versus spherical particles in flow and drug delivery. Nat Nanotechnol 2: 249–255.

35. AdaGL, PerryBT (1958) Properties of the nucleic acid of the Ryan strain of filamentous influenza virus. Journal of general microbiology 19: 40–54.

36. Smirnov YuA, KuznetsovaMA, KaverinNV (1991) The genetic aspects of influenza virus filamentous particle formation. Arch Virol 118: 279–284.

37. RenegarKB, SmallPAJr (1991) Passive transfer of local immunity to influenza virus infection by IgA antibody. Journal of immunology 146: 1972–1978.

38. AdrianM, DubochetJ, LepaultJ, McDowallAW (1984) Cryo-electron microscopy of viruses. Nature 308: 32–36.

39. MastronardeDN (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152: 36–51.

40. KremerJR, MastronardeDN, McIntoshJR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71–76.