1887

Abstract

nucleopolyhedrovirus (BmNPV) () and (), the orthologues of multiple nucleopolyhedrovirus (AcMNPV) and , are two adjacent genes with opposite transcriptional orientations and are highly conserved in all sequenced group I nucleopolyhedroviruses (NPVs). A double knockout bacmid was generated to enable the functional study of each gene independently or together. Compared with wild-type and double-repair viruses, deletion of both and did not affect budded virus (BV) production or viral DNA replication in transfected BmN cells. Electron microscopy revealed that the double knockout did not affect nucleocapsid assembly, virus-induced intranuclear microvesicle formation or occlusion-derived virus (ODV) production, but the number of virions embedded in the polyhedra decreased significantly. Further investigations showed that disruption of either gene was unable to recover the defect of ODV occlusion, suggesting that Bm133 and Bm134 are indispensable to the embedding of ODVs into polyhedra. Confocal microscopy analysis showed that Bm133 and Bm134 distributed throughout the whole cell during viral infection and Bm134 concentrated on the mature polyhedra in lysed cells. These results suggest that although Bm133 and Bm134 are not essential for BV or ODV development, they play vital roles in polyhedra morphogenesis.

Keyword(s): Baculovirus , Bm133 , Bm134 , BmNPV and ODV occlusion
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2018-05-01
2024-03-29
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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 [View Article][PubMed]
    [Google Scholar]
  2. Slack J, Arif BM. The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res 2007; 69:99–165 [View Article][PubMed]
    [Google Scholar]
  3. 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 [View Article][PubMed]
    [Google Scholar]
  4. Herniou EA, Luque T, Chen X, Vlak JM, Winstanley D et al. Use of whole genome sequence data to infer baculovirus phylogeny. J Virol 2001; 75:8117–8126 [View Article][PubMed]
    [Google Scholar]
  5. Rohrmann GF. Baculovirus Melocular Biology Bethesda, MD: National Library of Medicine (US), National Center for Biotechnology Information; 2013
    [Google Scholar]
  6. 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 [View Article][PubMed]
    [Google Scholar]
  7. Granados RR, Lawler KA. In vivo pathway of Autographa californica baculovirus invasion and infection. Virology 1981; 108:297–308 [View Article][PubMed]
    [Google Scholar]
  8. Gomi S, Majima K, Maeda S. Sequence analysis of the genome of Bombyx mori nucleopolyhedrovirus. J Gen Virol 1999; 80:1323–1337 [View Article][PubMed]
    [Google Scholar]
  9. Ono C, Kamagata T, Taka H, Sahara K, Asano S et al. Phenotypic grouping of 141 BmNPVs lacking viral gene sequences. Virus Res 2012; 165:197–206 [View Article][PubMed]
    [Google Scholar]
  10. Lin F, Chen K, Xia H, Yao Q, Gao L et al. Characterization of a late gene, ORF134, from Bombyx mori nucleopolyhedrovirus. Intervirology 2011; 54:113–121 [View Article][PubMed]
    [Google Scholar]
  11. Guo ZJ, Yu MH, Dong XY, Wang WL, Tian T et al. Protein composition analysis of polyhedra matrix of Bombyx mori nucleopolyhedrovirus (BmNPV) showed powerful capacity of polyhedra to encapsulate foreign proteins. Sci Rep 2017; 7:8768 [View Article][PubMed]
    [Google Scholar]
  12. Braunagel SC, Russell WK, Rosas-Acosta G, Russell DH, Summers MD. Determination of the protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus. Proc Natl Acad Sci USA 2003; 100:9797–9802 [View Article][PubMed]
    [Google Scholar]
  13. Wang R, Deng F, Hou D, Zhao Y, Guo L et al. Proteomics of the Autographa californica nucleopolyhedrovirus budded virions. J Virol 2010; 84:7233–7242 [View Article][PubMed]
    [Google Scholar]
  14. 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 [View Article][PubMed]
    [Google Scholar]
  15. Liu X, Chen K, Cai K, Yao Q. Determination of protein composition and host-derived proteins of Bombyx mori nucleopolyhedrovirus by 2-dimensional electrophoresis and mass spectrometry. Intervirology 2008; 51:369–376 [View Article][PubMed]
    [Google Scholar]
  16. Chen YR, Zhong S, Fei Z, Hashimoto Y, Xiang JZ et al. The transcriptome of the baculovirus Autographa californica multiple nucleopolyhedrovirus in Trichoplusia ni cells. J Virol 2013; 87:6391–6405 [View Article][PubMed]
    [Google Scholar]
  17. Marchler-Bauer A, Anderson JB, Derbyshire MK, Deweese-Scott C, Gonzales NR et al. CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res 2007; 35:D237–D240 [View Article][PubMed]
    [Google Scholar]
  18. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY et al. Pfam: the protein families database. Nucleic Acids Res 2014; 42:D222–D230 [View Article][PubMed]
    [Google Scholar]
  19. Xue J, Qiao N, Zhang W, Cheng RL, Zhang XQ et al. Dynamic interactions between Bombyx mori nucleopolyhedrovirus and its host cells revealed by transcriptome analysis. J Virol 2012; 86:7345–7359 [View Article][PubMed]
    [Google Scholar]
  20. Kang W, Suzuki M, Zemskov E, Okano K, Maeda S. Characterization of baculovirus repeated open reading frames (bro) in Bombyx mori nucleopolyhedrovirus. J Virol 1999; 73:10339–10345[PubMed]
    [Google Scholar]
  21. Garavaglia MJ, Miele SA, Iserte JA, Belaich MN, Ghiringhelli PD. The ac53, ac78, ac101, and ac103 genes are newly discovered core genes in the family Baculoviridae. J Virol 2012; 86:12069–12079 [View Article][PubMed]
    [Google Scholar]
  22. 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:e02115-16 [View Article][PubMed]
    [Google Scholar]
  23. Kool M, Ahrens CH, Goldbach RW, Rohrmann GF, Vlak JM. Identification of genes involved in DNA replication of the Autographa californica baculovirus. Proc Natl Acad Sci USA 1994; 91:11212–11216 [View Article][PubMed]
    [Google Scholar]
  24. Lu A, Miller LK. The roles of eighteen baculovirus late expression factor genes in transcription and DNA replication. J Virol 1995; 69:975–982[PubMed]
    [Google Scholar]
  25. Wu CP, Huang YJ, Wang JY, Wu YL, Lo HR et al. Autographa californica multiple nucleopolyhedrovirus LEF-2 is a capsid protein required for amplification but not initiation of viral DNA replication. J Virol 2010; 84:5015–5024 [View Article][PubMed]
    [Google Scholar]
  26. Kamita SG, Nagasaka K, Chua JW, Shimada T, Mita K et al. A baculovirus-encoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host. Proc Natl Acad Sci USA 2005; 102:2584–2589 [View Article][PubMed]
    [Google Scholar]
  27. Katsuma S, Kobayashi J, Koyano Y, Matsuda-Imai N, Kang W et al. Baculovirus-encoded protein BV/ODV-E26 determines tissue tropism and virulence in lepidopteran insects. J Virol 2012; 86:2545–2555 [View Article][PubMed]
    [Google Scholar]
  28. Tao XY, Choi JY, Kim WJ, An SB, Liu Q et al. Autographa californica multiple nucleopolyhedrovirus ORF11 is essential for budded-virus production and occlusion-derived-virus envelopment. J Virol 2015; 89:373–383 [View Article][PubMed]
    [Google Scholar]
  29. Dong F, Wang J, Deng R, Wang X. Autographa californica multiple nucleopolyhedrovirus gene ac81 is required for nucleocapsid envelopment. Virus Res 2016; 221:47–57 [View Article][PubMed]
    [Google Scholar]
  30. Tao XY, Choi JY, Kim WJ, Lee JH, Liu Q et al. The Autographa californica multiple nucleopolyhedrovirus ORF78 is essential for budded virus production and general occlusion body formation. J Virol 2013; 87:8441–8450 [View Article][PubMed]
    [Google Scholar]
  31. Fang M, Nie Y, Theilmann DA. Deletion of the AcMNPV core gene ac109 results in budded virions that are non-infectious. Virology 2009; 389:66–74 [View Article][PubMed]
    [Google Scholar]
  32. Yuan M, Huang Z, Wei D, Hu Z, Yang K et al. Identification of Autographa californica nucleopolyhedrovirus ac93 as a core gene and its requirement for intranuclear microvesicle formation and nuclear egress of nucleocapsids. J Virol 2011; 85:11664–11674 [View Article][PubMed]
    [Google Scholar]
  33. Guo YJ, Fu SH, Li LL. Autographa californica multiple nucleopolyhedrovirus ac75 is required for egress of nucleocapsids from the nucleus and formation of de novo intranuclear membrane microvesicles. PLoS One 2017; 12:e0185630 [View Article][PubMed]
    [Google Scholar]
  34. Shi A, Hu Z, Zuo Y, Wang Y, Wu W et al. Autographa californica multiple nucleopolyhedrovirus ac75 is required for the nuclear egress of nucleocapsids and intranuclear microvesicle formation. J Virol 2018; 92:JVI.01509-17 [View Article][PubMed]
    [Google Scholar]
  35. Hu Z, Yuan M, Wu W, Liu C, Yang K et al. Autographa californica multiple nucleopolyhedrovirus ac76 is involved in intranuclear microvesicle formation. J Virol 2010; 84:7437–7447 [View Article][PubMed]
    [Google Scholar]
  36. McCarthy CB, Dai X, Donly C, Theilmann DA. Autographa californica multiple nucleopolyhedrovirus ac142, a core gene that is essential for BV production and ODV envelopment. Virology 2008; 372:325–339 [View Article][PubMed]
    [Google Scholar]
  37. Xu HJ, Yang ZN, Zhao JF, Tian CH, Ge JQ et al. Bombyx mori nucleopolyhedrovirus ORF56 encodes an occlusion-derived virus protein and is not essential for budded virus production. J Gen Virol 2008; 89:1212–1219 [View Article][PubMed]
    [Google Scholar]
  38. 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 [View Article][PubMed]
    [Google Scholar]
  39. Yu H, Xu J, Liu Q, Liu TX, Wang D. Ha83, a chitin binding domain encoding gene, is important to Helicoverpa armigera nucleopolyhedrovirus budded virus production and occlusion body assembling. Sci Rep 2015; 5:11088 [View Article][PubMed]
    [Google Scholar]
  40. Chen X, Ijkel WF, Tarchini R, Sun X, Sandbrink H et al. The sequence of the Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus genome. J Gen Virol 2001; 82:241–257 [View Article][PubMed]
    [Google Scholar]
  41. Liu Y, de Jong J, Nagy É, Theilmann DA, Krell PJ. Nuclear translocation sequence and region in Autographa californica multiple nucleopolyhedrovirus ME53 that are important for optimal baculovirus production. J Virol 2016; 90:3953–3965 [View Article][PubMed]
    [Google Scholar]
  42. Zheng Q, Shen Y, Kon X, Zhang J, Feng M et al. Protein-protein interactions of the baculovirus per os infectivity factors (PIFs) in the PIF complex. J Gen Virol 2017; 98:853–861 [View Article][PubMed]
    [Google Scholar]
  43. Xiang X, Shen Y, Yang R, Chen L, Hu X et al. Bombyx mori nucleopolyhedrovirus BmP95 plays an essential role in budded virus production and nucleocapsid assembly. J Gen Virol 2013; 94:1669–1679 [View Article][PubMed]
    [Google Scholar]
  44. O'Reilly D, Miller L, Luckow V. Baculovirus Expression Vectors: A Laboratory Manual New York, NY: Oxford University Press; 1992
    [Google Scholar]
  45. Datsenko KA, Wanner BL, Kirill AD, Barry LW. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 2000; 97:6640–6645 [View Article][PubMed]
    [Google Scholar]
  46. Xiang X, Chen L, Guo A, Yu S, Yang R et al. The Bombyx mori nucleopolyhedrovirus (BmNPV) ODV-E56 envelope protein is also a per os infectivity factor. Virus Res 2011; 155:69–75 [View Article][PubMed]
    [Google Scholar]
  47. Harrison RL, Summers MD. Mutations in the Autographa californica multinucleocapsid nuclear polyhedrosis virus 25 kDa protein gene result in reduced virion occlusion, altered intranuclear envelopment and enhanced virus production. J Gen Virol 1995; 76:1451–1459 [View Article][PubMed]
    [Google Scholar]
  48. Yuan M, Wu W, Liu C, Wang Y, Hu Z et al. A highly conserved baculovirus gene p48 (ac103) is essential for BV production and ODV envelopment. Virology 2008; 379:87–96 [View Article][PubMed]
    [Google Scholar]
  49. Wang Y, Wang Q, Liang C, Song J, Li N et al. Autographa californica multiple nucleopolyhedrovirus nucleocapsid protein BV/ODV-C42 mediates the nuclear entry of P78/83. J Virol 2008; 82:4554–4561 [View Article][PubMed]
    [Google Scholar]
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