1887

Abstract

After ingestion of occlusion bodies, the occlusion-derived viruses (ODVs) of the baculoviruses establish the first round of infection within the larval host midgut cells. Several ODV envelope proteins, called per os infectivity factors (PIFs), have been shown to be essential for oral infection. Eight PIFs have been identified to date, including P74, PIFs 1–6 and Ac110. At least six PIFs, P74, PIFs 1–4 and PIF6, together with three other ODV-specific proteins, Ac5, P95 (Ac83) and Ac108, have been reported to form a complex on the ODV surface. In this study, in order to understand the interactions of these PIFs, the direct protein–protein interactions of the nine components of the Autographa californica multiple nucleopolyhedrovirus PIF complex were investigated using yeast two-hybrid (Y2H) screening combined with bimolecular fluorescence complementation (BiFC) assay. Six direct interactions, comprising PIF1–PIF2, PIF1–PIF3, PIF1–PIF4, PIF1–P95, PIF2–PIF3 and PIF3–PIF4, were identified in the Y2H analysis, and these results were further verified by BiFC. For P74, PIF6, Ac5 and Ac108, no direct interaction was identified. P95 (Ac83) was identified to interact with PIF1, and further Y2H analysis of the truncation and deletion mutants showed that the predicted P95 chitin-binding domain and amino acids 100–200 of PIF1 were responsible for P95 interaction with PIF1. Furthermore, a summary of the protein–protein interactions of PIFs reported so far, comprising 10 reciprocal interactions and two self-interactions, is presented, which will facilitate our understanding of the characteristics of the PIF complex.

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2017-05-05
2019-10-18
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References

  1. Herniou EA, Olszewski JA, Cory JS, O'Reilly DR. The genome sequence and evolution of baculoviruses. Annu Rev Entomol 2003; 48: 211– 234 [CrossRef] [PubMed]
    [Google Scholar]
  2. Jehle JA, Blissard GW, Bonning BC, Cory JS, Herniou EA et al. On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol 2006; 151: 1257– 1266 [CrossRef] [PubMed]
    [Google Scholar]
  3. Braunagel SC, Summers MD. Molecular biology of the baculovirus occlusion-derived virus envelope. Curr Drug Targets 2007; 8: 1084– 1095 [PubMed] [Crossref]
    [Google Scholar]
  4. Braunagel SC, Summers MD. Autographa californica nuclear polyhedrosis virus, PDV, and ECV viral envelopes and nucleocapsids: structural proteins, antigens, lipid and fatty acid profiles. Virology 1994; 202: 315– 328 [CrossRef] [PubMed]
    [Google Scholar]
  5. Slack J, Arif BM. The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res 2007; 69: 99– 165 [CrossRef] [PubMed]
    [Google Scholar]
  6. Kozlov EA, Levitina TL, Gusak NM. The primary structure of baculovirus inclusion body proteins. Evolution and structure-function aspects. Curr Top Microbiol Immunol 1986; 131: 135– 164 [PubMed]
    [Google Scholar]
  7. Rohrmann GF. Polyhedrin structure. J Gen Virol 1986; 67: 1499– 1513 [Crossref]
    [Google Scholar]
  8. Granados RR. Early events in the infection of Heliothis Zea midgut cells by a baculovirus. Virology 1978; 90: 170– 174 [CrossRef] [PubMed]
    [Google Scholar]
  9. Horton HM, Burand JP. Saturable attachment sites for polyhedron-derived baculovirus on insect cells and evidence for entry via direct membrane fusion. J Virol 1993; 67: 1860– 1868 [PubMed]
    [Google Scholar]
  10. 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]
    [Google Scholar]
  11. 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]
    [Google Scholar]
  12. Kuzio J, Jaques R, Faulkner P. Identification of p74, a gene essential for virulence of baculovirus occlusion bodies. Virology 1989; 173: 759– 763 [CrossRef] [PubMed]
    [Google Scholar]
  13. 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]
    [Google Scholar]
  14. 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]
    [Google Scholar]
  15. Pijlman GP, Pruijssers AJ, 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]
    [Google Scholar]
  16. 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]
    [Google Scholar]
  17. 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]
    [Google Scholar]
  18. 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: 69– 76 [CrossRef] [PubMed]
    [Google Scholar]
  19. 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]
    [Google Scholar]
  20. 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 221: 30– 37 [CrossRef] [PubMed]
    [Google Scholar]
  21. 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]
    [Google Scholar]
  22. Mu J, van Lent JW, 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]
    [Google Scholar]
  23. 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]
    [Google Scholar]
  24. Zhou W, Yao L, Xu H, Yan F, Qi Y. The function of envelope protein P74 from Autographa californica multiple nucleopolyhedrovirus in primary infection to host. Virus Genes 2005; 30: 139– 150 [CrossRef] [PubMed]
    [Google Scholar]
  25. Peng K, van Lent JW, 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]
    [Google Scholar]
  26. Peng K, van Oers MM, Hu Z, van Lent JW, 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]
    [Google Scholar]
  27. Fan JY, Cui ZQ, Wei HP, Zhang ZP, Zhou YF et al. Split mCherry as a new red bimolecular fluorescence complementation system for visualizing protein-protein interactions in living cells. Biochem Biophys Res Commun 2008; 367: 47– 53 [CrossRef] [PubMed]
    [Google Scholar]
  28. Kadlec J, Loureiro S, Abrescia NG, Stuart DI, Jones IM. The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat Struct Mol Biol 2008; 15: 1024– 1030 [CrossRef] [PubMed]
    [Google Scholar]
  29. Zhu S, Wang W, Wang Y, Yuan M, Yang K. 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]
    [Google Scholar]
  30. Peng K, Wu M, Deng F, Song J, Dong C et al. Identification of protein-protein interactions of the occlusion-derived virus-associated proteins of Helicoverpa armigera nucleopolyhedrovirus. J Gen Virol 2010; 91: 659– 670 [CrossRef] [PubMed]
    [Google Scholar]
  31. Song J, Wang R, Deng F, Wang H, Hu Z. Functional studies of per os infectivity factors of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus. J Gen Virol 2008; 89: 2331– 2338 [CrossRef] [PubMed]
    [Google Scholar]
  32. Chojnacki J, Staudt T, Glass B, Bingen P, Engelhardt J et al. Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy. Science 2012; 338: 524– 528 [CrossRef] [PubMed]
    [Google Scholar]
  33. Peng K, van Lent JW, Vlak JM, Hu Z, van Oers MM. In situ cleavage of baculovirus occlusion-derived virus receptor binding protein P74 in the peroral infectivity complex. J Virol 2011; 85: 10710– 10718 [CrossRef] [PubMed]
    [Google Scholar]
  34. Elorza MV, Rico H, Sentandreu R. Calcofluor white alters the assembly of chitin fibrils in Saccharomyces cerevisiae and Candida albicans cells. Microbiology 1983; 129: 1577– 1582 [CrossRef]
    [Google Scholar]
  35. Li Z, Li C, Yang K, Wang L, Yin C et al. Characterization of a chitin-binding protein GP37 of Spodoptera litura multicapsid nucleopolyhedrovirus. Virus Res 2003; 96: 113– 122 [PubMed] [Crossref]
    [Google Scholar]
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