1887

Abstract

Baculovirus occlusion-derived viruses (ODVs) contain ten known infectivity factors (PIFs). These PIFs are crucial for midgut infection of insect larvae and form, with the exception of PIF5, an ODV entry complex. Previously, R18-dequenching assays have shown that PIF3 is dispensable for binding and fusion with midgut epithelial cells. Oral infection nevertheless fails in the absence of PIF3. PIF9 has not been analysed in much depth yet. Here, the biological role of these two PIFs in midgut infection was examined by monitoring the fate of fluorescently labelled ODVs when incubated with isolated midgut cells from larvae. Confocal microscopy showed that in the absence of either PIF3 or PIF9, the ODVs bound to the brush borders, but the nucleocapsids failed to enter the cells. Finally, we discuss how the results obtained for PIF3 with dequenching assays and confocal microscopy can be explained by a two-phase fusion process.

Funding
This study was supported by the:
  • Monique M. van Oers , Nederlandse Organisatie voor Wetenschappelijk Onderzoek , (Award 824.14.16)
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/content/journal/jgv/10.1099/jgv.0.001430
2020-05-14
2020-06-04
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References

  1. Williams T, Bergoin M, van Oers MM. Diversity of large DNA viruses of invertebrates. J Invertebr Pathol 2017; 147:4–22 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  2. Granados RR, Lawler KA. In vivo pathway of Autographa californica baculovirus invasion and infection. Virology 1981; 108:297–308 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  3. Kawanishi CY, Summers MD, Stoltz DB, Arnott HJ. Entry of an insect virus in vivo by fusion of viral envelope and microvillus membrane. J Invertebr Pathol 1972; 20:104–108 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  4. Faulkner P, Kuzio J, Williams GV, Wilson JA. Analysis of p74, a PDV envelope protein of Autographa californica nucleopolyhedrovirus required for occlusion body infectivity in vivo. J Gen Virol 1997; 78:3091–3100 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  5. Kikhno I, Gutiérrez S, Croizier L, Croizier G, Ferber ML. Characterization of pif, a gene required for the per os infectivity of Spodoptera littoralis nucleopolyhedrovirus. J Gen Virol 2002; 83:3013–3022 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  6. Pijlman GP, Pruijssers AJP, Vlak JM. Identification of pif-2, a third conserved baculovirus gene required for per os infection of insects. J Gen Virol 2003; 84:2041–2049 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  7. Ohkawa T, Washburn JO, Sitapara R, Sid E, Volkman LE. Specific binding of Autographa californica M nucleopolyhedrovirus occlusion-derived virus to midgut cells of Heliothis virescens larvae is mediated by products of PIF genes Ac119 and Ac022 but not by Ac115. J Virol 2005; 79:15258–15264 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  8. Fang M, Nie Y, Harris S, Erlandson MA, Theilmann DA. Autographa californica multiple nucleopolyhedrovirus core gene ac96 encodes a per os infectivity factor (PIF-4). J Virol 2009; 83:12569–12578 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  9. Sparks WO, Harrison RL, Bonning BC. Autographa californica multiple nucleopolyhedrovirus ODV-E56 is a per os infectivity factor, but is not essential for binding and fusion of occlusion-derived virus to the host midgut. Virology 2011; 409:6976 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  10. Nie Y, Fang M, Erlandson MA, Theilmann DA. Analysis of the Autographa californica multiple nucleopolyhedrovirus overlapping gene pair lef3 and ac68 reveals that AC68 is a per os infectivity factor and that LEF3 is critical, but not essential, for virus replication. J Virol 2012; 86:3985–3994 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  11. Liu J, Zhu L, Zhang S, Deng Z, Huang Z et al. The Autographa californica multiple nucleopolyhedrovirus ac110 gene encodes a new per os infectivity factor. Virus Res 2016; 221:30–37 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  12. Zhu S, Wang W, Wang Y, Yuan M, Yang K et al. The baculovirus core gene ac83 is required for nucleocapsid assembly and per os infectivity of Autographa californica nucleopolyhedrovirus. J Virol 2013; 87:10573–10586 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  13. Javed MA, Biswas S, Willis LG, Harris S, Pritchard C et al. Autographa californica Multiple Nucleopolyhedrovirus AC83 is a Per Os Infectivity Factor (PIF) Protein Required for Occlusion-Derived Virus (ODV) and Budded Virus Nucleocapsid Assembly as well as Assembly of the PIF Complex in ODV Envelopes. J Virol 2017; 91: [CrossRef][PubMed][PubMed]
    [Google Scholar]
  14. Wang X, Shang Y, Chen C, Liu S, Chang M et al. Baculovirus per os infectivity factor complex: components and assembly. J Virol 2019; 93: [CrossRef]
    [Google Scholar]
  15. Boogaard B, Evers F, van Lent JWM, van Oers MM. The baculovirus Ac108 protein is a per os infectivity factor and a component of the ODV entry complex. J Gen Virol 2019; 100:669–678 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  16. Boogaard B, van Oers MM, van Lent JWM. An advanced view on baculovirus per os infectivity factors. Insects 2018; 9:84 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  17. Peng K, van Lent JWM, Boeren S, Fang M, Theilmann DA et al. Characterization of novel components of the baculovirus per os infectivity factor complex. J Virol 2012; 86:4981–4988 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  18. Peng K, van Oers MM, Hu Z, van Lent JWM, Vlak JM. Baculovirus per os infectivity factors form a complex on the surface of occlusion-derived virus. J Virol 2010; 84:9497–9504 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  19. Boogaard B, van Lent JWM, Theilmann DA, Erlandson MA, van Oers MM. Baculoviruses require an intact ODV entry-complex to resist proteolytic degradation of per os infectivity factors by co-occluded proteases from the larval host. J Gen Virol 2017; 98:3101–3110 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  20. Haas-Stapleton EJ, Washburn JO, Volkman LE. P74 mediates specific binding of Autographa californica M nucleopolyhedrovirus occlusion-derived virus to primary cellular targets in the midgut epithelia of Heliothis virescens larvae. J Virol 2004; 78:6786–6791 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  21. Yao L, Zhou W, Xu H, Zheng Y, Qi Y. The Heliothis armigera single nucleocapsid nucleopolyhedrovirus envelope protein p74 is required for infection of the host midgut. Virus Res 2004; 104:111–121 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  22. Mu J, van Lent JWM, Smagghe G, Wang Y, Chen X et al. Live imaging of baculovirus infection of midgut epithelium cells: a functional assay of per os infectivity factors. J Gen Virol 2014; 95:2531–2539 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  23. Smith GE, Summers MD. Analysis of baculovirus genomes with restriction endonucleases. Virology 1978; 89:517–527 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  24. Luckow VA, Lee SC, Barry GF, Olins PO. Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli. J Virol 1993; 67:4566–4579 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  25. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 2000; 97:6640–6645 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  26. Li X, Song J, Jiang T, Liang C, Chen X. The N-terminal hydrophobic sequence of Autographa californica nucleopolyhedrovirus PIF-3 is essential for oral infection. Arch Virol 2007; 152:1851–1858 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  27. Westenberg M, Soedling HM, Mann DA, Nicholson LJ, Dolphin CT. Counter-selection recombineering of the baculovirus genome: a strategy for seamless modification of repeat-containing BACs. Nucleic Acids Res 2010; 38:e166 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  28. Tanada Y, Hess RT, Omi EM. Invasion of a nuclear polyhedrosis virus in midgut of the armyworm, Pseudaletia unipuncta, and the enhancement of a synergistic enzyme. J Invertebr Pathol 1975; 26:99–104 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  29. Harrap KA, Payne CC, Robertson JS. The properties of three baculoviruses from closely related hosts. Virology 1977; 79:14–31 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  30. Payne CC, Kalmakoff J. Alkaline protease associated with virus particles of a nuclear polyhedrosis virus: assay, purification and properties. J Virol 1978; 26:84–92 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  31. Wood HA. Protease degradation of Autographa californica nuclear polyhedrosis virus proteins. Virology 1980; 103:392–399 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  32. Javed MA, Coutu C, Theilmann DA, Erlandson MA, Hegedus DD. Proteomics analysis of Trichoplusia ni midgut epithelial cell brush border membrane vesicles. Insect Sci 2019; 26:424–440 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  33. Kemble GW, Danieli T, White JM. Lipid-Anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 1994; 76:383–391 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  34. Laliberte JP, Weisberg AS, Moss B. The membrane fusion step of vaccinia virus entry is cooperatively mediated by multiple viral proteins and host cell components. PLoS Pathog 2011; 7:e1002446 [CrossRef][PubMed][PubMed]
    [Google Scholar]
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