1887

Abstract

In contrast to the current wealth of structural information concerning dicistrovirus particle structure, very little is known about their morphogenetic pathways. Here, we describe the expression of the two ORFs encoded by the (TrV) genome. TrV, a member of the genus of the family, infects blood-sucking insects belonging to the subfamily that act as vectors for the transmission of , the aetiological agent of the Chagas disease. We have established a baculovirus-based model for the expression of the NS (non-structural) and P1 (structural) polyproteins. A preliminary characterization of the proteolytic processing of both polyprotein precursors has been performed using this system. We show that the proteolytic processing of the P1 polyprotein is strictly dependent upon the coexpression of the NS polyprotein, and that NS/P1 coexpression leads to the assembly of virus-like particles (VLPs) exhibiting a morphology and a protein composition akin to natural TrV empty capsids. Remarkably, the unprocessed P1 polypeptide assembles into quasi-spherical structures conspicuously larger than VLPs produced in NS/P1-coexpressing cells, likely representing a previously undescribed morphogenetic intermediate. This intermediate has not been found in members of the related family currently used as a model for dicistrovirus studies, thus suggesting the existence of major differences in the assembly pathways of these two virus groups.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.071639-0
2015-01-01
2020-01-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/1/64.html?itemId=/content/journal/jgv/10.1099/vir.0.071639-0&mimeType=html&fmt=ahah

References

  1. Agirre J. , Aloria K. , Arizmendi J. M. , Iloro I. , Elortza F. , Sánchez-Eugenia R. , Marti G. A. , Neumann E. , Rey F. A. , Guérin D. M. A. . ( 2011; ). Capsid protein identification and analysis of mature Triatoma virus (TrV) virions and naturally occurring empty particles. . Virology 409:, 91–101. [CrossRef] [PubMed]
    [Google Scholar]
  2. Agirre J. , Goret G. , LeGoff M. , Sánchez-Eugenia R. , Marti G. A. , Navaza J. , Guérin D. M. A. , Neumann E. . ( 2013; ). Cryo-electron microscopy reconstructions of triatoma virus particles: a clue to unravel genome delivery and capsid disassembly. . J Gen Virol 94:, 1058–1068. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bonning B. C. , Miller W. A. . ( 2010; ). Dicistroviruses. . Annu Rev Entomol 55:, 129–150. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bostina M. , Levy H. , Filman D. J. , Hogle J. M. . ( 2011; ). Poliovirus RNA is released from the capsid near a twofold symmetry axis. . J Virol 85:, 776–783. [CrossRef] [PubMed]
    [Google Scholar]
  5. Czibener C. , La Torre J. L. , Muscio O. A. , Ugalde R. A. , Scodeller E. A. . ( 2000; ). Nucleotide sequence analysis of Triatoma virus shows that it is a member of a novel group of insect RNA viruses. . J Gen Virol 81:, 1149–1154.[PubMed]
    [Google Scholar]
  6. Czibener C. , Alvarez D. , Scodeller E. , Gamarnik A. V. . ( 2005; ). Characterization of internal ribosomal entry sites of Triatoma virus. . J Gen Virol 86:, 2275–2280. [CrossRef] [PubMed]
    [Google Scholar]
  7. de Miranda J. R. , Cordoni G. , Budge G. . ( 2010; ). The Acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. . J Invertebr Pathol 103: (Suppl 1), S30–S47. [CrossRef] [PubMed]
    [Google Scholar]
  8. Garriga D. , Pickl-Herk A. , Luque D. , Wruss J. , Castón J. R. , Blaas D. , Verdaguer N. . ( 2012; ). Insights into minor group rhinovirus uncoating: the X-ray structure of the HRV2 empty capsid. . PLoS Pathog 8:, e1002473. [CrossRef] [PubMed]
    [Google Scholar]
  9. Genersch E. , Aubert M. . ( 2010; ). Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). . Vet Res 41:, 54. [CrossRef] [PubMed]
    [Google Scholar]
  10. Goodwin S. , Tuthill T. J. , Arias A. , Killington R. A. , Rowlands D. J. . ( 2009; ). Foot-and-mouth disease virus assembly: processing of recombinant capsid precursor by exogenous protease induces self-assembly of pentamers in vitro in a myristoylation-dependent manner. . J Virol 83:, 11275–11282. [CrossRef] [PubMed]
    [Google Scholar]
  11. Grayson M. . ( 2010; ). Chagas disease. . Nature 465: (n7301_supp), S3–S22. [CrossRef] [PubMed]
    [Google Scholar]
  12. Hellen C. U. , Wimmer E. . ( 1992; ). Maturation of poliovirus capsid proteins. . Virology 187:, 391–397. [CrossRef] [PubMed]
    [Google Scholar]
  13. Hewat E. A. , Neumann E. , Blaas D. . ( 2002; ). The concerted conformational changes during human rhinovirus 2 uncoating. . Mol Cell 10:, 317–326. [CrossRef] [PubMed]
    [Google Scholar]
  14. Hu Y.-C. , Hsu J. T.-A. , Huang J.-H. , Ho M.-S. , Ho Y.-C. . ( 2003; ). Formation of enterovirus-like particle aggregates by recombinant baculoviruses co-expressing P1 and 3CD in insect cells. . Biotechnol Lett 25:, 919–925. [CrossRef] [PubMed]
    [Google Scholar]
  15. Kingsolver M. B. , Huang Z. , Hardy R. W. . ( 2013; ). Insect antiviral innate immunity: pathways, effectors, and connections. . J Mol Biol 425:, 4921–4936. [CrossRef] [PubMed]
    [Google Scholar]
  16. Le Gall O. , Christian P. , Fauquet C. M. , King A. M. Q. , Knowles N. J. , Nakashima N. , Stanway G. , Gorbalenya A. E. . ( 2008; ). Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T  =  3 virion architecture. . Arch Virol 153:, 715–727. [CrossRef] [PubMed]
    [Google Scholar]
  17. Levy H. C. , Bostina M. , Filman D. J. , Hogle J. M. . ( 2010; ). Catching a virus in the act of RNA release: a novel poliovirus uncoating intermediate characterized by cryo-electron microscopy. . J Virol 84:, 4426–4441. [CrossRef] [PubMed]
    [Google Scholar]
  18. Li C. , Wang J. C.-Y. , Taylor M. W. , Zlotnick A. . ( 2012; ). In vitro assembly of an empty picornavirus capsid follows a dodecahedral path. . J Virol 86:, 13062–13069. [CrossRef] [PubMed]
    [Google Scholar]
  19. Marti G. , Echeverría M. G. , Susevich M. L. , Ceccarelli S. , Balsalobre A. , Canale D. , Stariolo R. , Noireau F. , García A. L. . & other authors ( 2013; ). Exploration for Triatoma virus (TrV) infection in laboratory-reared triatomines of Latin America: a collaborative study. . Int J of Trop Insect Sci 33:, 294–304. [CrossRef]
    [Google Scholar]
  20. Martinez-Torrecuadrada J. L. , Castón J. R. , Castro M. , Carrascosa J. L. , Rodriguez J. F. , Casal J. I. . ( 2000; ). Different architectures in the assembly of infectious bursal disease virus capsid proteins expressed in insect cells. . Virology 278:, 322–331. [CrossRef] [PubMed]
    [Google Scholar]
  21. Mayo M. A. . ( 2002; ). Virus taxonomy – Houston 2002. . Arch Virol 147:, 1071–1076.[PubMed] [CrossRef]
    [Google Scholar]
  22. Muscio O. A. , La Torre J. L. , Scodeller E. A. . ( 1988; ). Characterization of Triatoma virus, a picorna-like virus isolated from the triatomine bug Triatoma infestans . . J Gen Virol 69:, 2929–2934. [CrossRef] [PubMed]
    [Google Scholar]
  23. Muscio O. A. , La Torre J. , Bonder M. A. , Scodeller E. A. . ( 1997; ). Triatoma virus pathogenicity in laboratory colonies of Triatoma infestans (Hemiptera: Reduviidae). . J Med Entomol 34:, 253–256.[PubMed] [CrossRef]
    [Google Scholar]
  24. Nakashima N. , Ishibashi J. . ( 2010; ). Identification of the 3C-protease-mediated 2A/2B and 2B/2C cleavage sites in the nonstructural polyprotein precursor of a Dicistrovirus lacking the NPGP motif. . Arch Virol 155:, 1477–1482. [CrossRef] [PubMed]
    [Google Scholar]
  25. Nakashima N. , Nakamura Y. . ( 2008; ). Cleavage sites of the “P3 region” in the nonstructural polyprotein precursor of a dicistrovirus. . Arch Virol 153:, 1955–1960. [CrossRef] [PubMed]
    [Google Scholar]
  26. Nakashima N. , Shibuya N. . ( 2006; ). Multiple coding sequences for the genome-linked virus protein (VPg) in dicistroviruses. . J Invertebr Pathol 92:, 100–104. [CrossRef] [PubMed]
    [Google Scholar]
  27. Oña A. , Luque D. , Abaitua F. , Maraver A. , Castón J. R. , Rodríguez J. F. . ( 2004; ). The C-terminal domain of the pVP2 precursor is essential for the interaction between VP2 and VP3, the capsid polypeptides of infectious bursal disease virus. . Virology 322:, 135–142. [CrossRef] [PubMed]
    [Google Scholar]
  28. Palmenberg A. C. . ( 1990; ). Proteolytic processing of picornaviral polyprotein. . Annu Rev Microbiol 44:, 603–623. [CrossRef] [PubMed]
    [Google Scholar]
  29. Querido J. F. B. , Agirre J. , Marti G. A. , Guérin D. M. A. , Silva M. S. . ( 2013; ). Inoculation of Triatoma virus (Dicistroviridae: Cripavirus) elicits a non-infective immune response in mice. . Parasit Vectors 6:, 66. [CrossRef] [PubMed]
    [Google Scholar]
  30. Ren J. , Cone A. , Willmot R. , Jones I. M. . ( 2014; ). Assembly of recombinant Israeli Acute Paralysis Virus capsids. . PLoS ONE 9:, e105943. [CrossRef] [PubMed]
    [Google Scholar]
  31. Rodriguez J. F. , Guérin D. M. A. . ( 2014; ). VLPs, methods for their obtention and application thereof. EU Patent EP14382001.7 pending. .
  32. Rodriguez D. , Rodriguez J. R. , Rodriguez J. F. , Trauber D. , Esteban M. . ( 1989; ). Highly attenuated vaccinia virus mutants for the generation of safe recombinant viruses. . Proc Natl Acad Sci U S A 86:, 1287–1291. [CrossRef] [PubMed]
    [Google Scholar]
  33. Snijder J. , Uetrecht C. , Rose R. J. , Sanchez-Eugenia R. , Marti G. A. , Agirre J. , Guérin D. M. A. , Wuite G. J. , Heck A. J. , Roos W. H. . ( 2013; ). Probing the biophysical interplay between a viral genome and its capsid. . Nat Chem 5:, 502–509. [CrossRef] [PubMed]
    [Google Scholar]
  34. Squires G. , Pous J. , Agirre J. , Rozas-Dennis G. S. , Costabel M. D. , Marti G. A. , Navaza J. , Bressanelli S. , Guérin D. M. A. , Rey F. A. . ( 2013; ). Structure of the Triatoma virus capsid. . Acta Crystallogr D Biol Crystallogr 69:, 1026–1037. [CrossRef] [PubMed]
    [Google Scholar]
  35. Susevich M. L. , Marti G. A. , Serena M. S. , Echeverría M. G. . ( 2012; ). New Triatoma virus hosts in wild habitats of Argentina. . J Invertebr Pathol 110:, 405–407. [CrossRef] [PubMed]
    [Google Scholar]
  36. Tate J. , Liljas L. , Scotti P. , Christian P. , Lin T. , Johnson J. E. . ( 1999; ). The crystal structure of cricket paralysis virus: the first view of a new virus family. . Nat Struct Biol 6:, 765–774. [CrossRef] [PubMed]
    [Google Scholar]
  37. Tuthill T. J. , Groppelli E. , Hogle J. M. , Rowlands D. J. . ( 2010; ). Picornaviruses. . Curr Top Microbiol Immunol 343:, 43–89.[PubMed]
    [Google Scholar]
  38. Wertheim J. O. , Tang K. F. J. , Navarro S. A. , Lightner D. V. . ( 2009; ). A quick fuse and the emergence of Taura syndrome virus. . Virology 390:, 324–329. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.071639-0
Loading
/content/journal/jgv/10.1099/vir.0.071639-0
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error