1887

Abstract

ORF40 (bm40) of the Bombyx mori nucleopolyhedrovirus (BmNPV) encodes a homologue of Autographa californica multiple nucleopolyhedrovirus (AcMNPV) AC51 and is a highly conserved gene in sequenced alphabaculoviruses. To investigate the role of bm40 in the baculovirus infection cycle, a bm40 knockout BmNPV bacmid was constructed via homologous recombination in Escherichia coli. Western blotting analysis revealed that bm40 is a late gene during virus infection. Compared with wild-type and repair viruses, the knockout virus exhibited a single-cell infection phenotype. Titration assays confirmed that no infectious budded viruses (BVs) were produced due to the bm40 deletion, while there was no effect on viral DNA replication. Electron microscopy revealed that Bm40 is required for nucleocapsid egress from the nucleus to the cytoplasm, nucleocapsid envelopment to form occlusion-derived viruses (ODVs) and subsequent embedding of ODVs into polyhedra. Confocal microscopy showed that Bm40 was predominantly localized in the nuclei from 48 h post-infection and subsequently condensed on the nuclear membrane and polyhedra at the late phase of infection. Taken together, these results demonstrate that Bm40 plays an essential role in BV production and ODV envelopment in the BmNPV infection cycle.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001066
2018-04-19
2019-09-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/99/6/837.html?itemId=/content/journal/jgv/10.1099/jgv.0.001066&mimeType=html&fmt=ahah

References

  1. Clem RJ, Passarelli AL. Baculoviruses: sophisticated pathogens of insects. PLoS Pathog 2013;9:e1003729 [CrossRef][PubMed]
    [Google Scholar]
  2. Rohrmann GF. Baculovirus Melocular Biolog Bethesda, MD: National Library of Medicine (US): National Center for Biotechnology Information; 2013
    [Google Scholar]
  3. Slack J, Arif BM. The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res 2007;69:99–165 [CrossRef][PubMed]
    [Google Scholar]
  4. 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]
  5. Harrison RL, Rowley DL, Mowery JD, Bauchan GR, Burand JP. The Operophtera brumata nucleopolyhedrovirus (OpbuNPV) represents an early, divergent lineage within genus Alphabaculovirus. Viruses 2017;9:307 [CrossRef][PubMed]
    [Google Scholar]
  6. Harrison RL, Mowery JD, Rowley DL, Bauchan GR, Theilmann DA et al. The complete genome sequence of a third distinct baculovirus isolated from the true armyworm, Mythimna unipuncta, contains two copies of the lef-7 gene. Virus Genes 2018;54:297–310 [CrossRef][PubMed]
    [Google Scholar]
  7. 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]
  8. Granados RR, Lawler KA. In vivo pathway of Autographa californica baculovirus invasion and infection. Virology 1981;108:297–308 [CrossRef][PubMed]
    [Google Scholar]
  9. Gomi S, Majima K, Maeda S. Sequence analysis of the genome of Bombyx mori nucleopolyhedrovirus. J Gen Virol 1999;80:1323–1337 [CrossRef][PubMed]
    [Google Scholar]
  10. 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 [CrossRef][PubMed]
    [Google Scholar]
  11. Ayres MD, Howard SC, Kuzio J, Lopez-Ferber M, Possee RD. The complete DNA sequence of Autographa californica nuclear polyhedrosis virus. Virology 1994;202:586–605 [CrossRef][PubMed]
    [Google Scholar]
  12. Rohrmann GF. Baculovirus nucleocapsid aggregation (MNPV vs SNPV): an evolutionary strategy, or a product of replication conditions?. Virus Genes 2014;49:351–357 [CrossRef][PubMed]
    [Google Scholar]
  13. Wang L, Yu J, Yin C, Li Z, Hu X et al. Characterization of a J domain gene of Spodoptera litura multicapsid nucleopolyhedrovirus. Virus Genes 2002;25:291–297 [CrossRef][PubMed]
    [Google Scholar]
  14. Xu H, Liu Y, Yang Z, Zhang C. Characterization of ORF39 from Helicoverpa armigera single-nucleocapsid nucleopolyhedrovirus, the gene containing RNA recognition motif. J Biochem Mol Biol 2006;39:263–269[PubMed]
    [Google Scholar]
  15. Dreyfuss G, Kim V, Kataoka N. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 2002;3:195–205 [CrossRef][PubMed]
    [Google Scholar]
  16. Hou D, Zhang L, Deng F, Fang W, Wang R et al. Comparative proteomics reveal fundamental structural and functional differences between the two progeny phenotypes of a baculovirus. J Virol 2013;87:829–839 [CrossRef][PubMed]
    [Google Scholar]
  17. Zhang C, Ma X, Guo Z. Comparison of the complete genome sequence between C1 and G4 isolates of the Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus. Virology 2005;333:190–199 [CrossRef][PubMed]
    [Google Scholar]
  18. 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 [CrossRef][PubMed]
    [Google Scholar]
  19. 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 [CrossRef][PubMed]
    [Google Scholar]
  20. Xu F, Ince IA, Boeren S, Vlak JM, van Oers MM. Protein composition of the occlusion derived virus of Chrysodeixis chalcites nucleopolyhedrovirus. Virus Res 2011;158:1–7 [CrossRef][PubMed]
    [Google Scholar]
  21. 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 [CrossRef][PubMed]
    [Google Scholar]
  22. Cléry A, Blatter M, Allain FH. RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 2008;18:290–298 [CrossRef][PubMed]
    [Google Scholar]
  23. Kelley WL. The J-domain family and the recruitment of chaperone power. Trends Biochem Sci 1998;23:222–227 [CrossRef][PubMed]
    [Google Scholar]
  24. Lupas AN, Bassler J. Coiled coils – a model system for the 21st century. Trends Biochem Sci 2017;42:130–140 [CrossRef][PubMed]
    [Google Scholar]
  25. 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 [CrossRef][PubMed]
    [Google Scholar]
  26. Chen Y, Zhong S, Fei Z, Hashimoto Y, Xiang J et al. The transcriptome of the baculovirus Autographa californica multiple nucleopolyhedrovirus in Trichoplusia ni cells. J Virol 2013;87:6391–6405 [CrossRef][PubMed]
    [Google Scholar]
  27. Xue J, Qiao N, Zhang W, Cheng R, Zhang X et al. Dynamic interactions between Bombyx mori nucleopolyhedrovirus and its host cells revealed by transcriptome analysis. J Virol 2012;86:7345–7359 [CrossRef][PubMed]
    [Google Scholar]
  28. 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]
  29. Lange A, Mills RE, Lange CJ, Stewart M, Devine SE et al. Classical nuclear localization signals: definition, function, and interaction with importin α. J Biol Chem 2007;282:5101–5105 [CrossRef][PubMed]
    [Google Scholar]
  30. Kosugi S, Hasebe M, Matsumura N, Takashima H, Miyamoto-Sato E et al. Six classes of nuclear localization signals specific to different binding grooves of importin alpha. J Biol Chem 2009;284:478–485 [CrossRef][PubMed]
    [Google Scholar]
  31. Tao X, Choi J, Kim W, 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 [CrossRef][PubMed]
    [Google Scholar]
  32. 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 [CrossRef][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 [CrossRef][PubMed]
    [Google Scholar]
  34. 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 [CrossRef][PubMed]
    [Google Scholar]
  35. Tao X, Choi J, Kim W, Lee J, 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 [CrossRef][PubMed]
    [Google Scholar]
  36. Huang H, Wang M, Deng F, Hou D, Arif BM et al. The ha72 core gene of baculovirus is essential for budded virus production and occlusion-derived virus embedding, and amino acid K22 plays an important role in its function. J Virol 2014;88:705–709 [CrossRef][PubMed]
    [Google Scholar]
  37. 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 [CrossRef][PubMed]
    [Google Scholar]
  38. 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 [CrossRef][PubMed]
    [Google Scholar]
  39. 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 [CrossRef][PubMed]
    [Google Scholar]
  40. 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 [CrossRef][PubMed]
    [Google Scholar]
  41. Lehiy CJ, Wu W, Berretta MF, Passarelli AL. Autographa californica M nucleopolyhedrovirus open reading frame 109 affects infectious budded virus production and nucleocapsid envelopment in the nucleus of cells. Virology 2013;435:442–452 [CrossRef][PubMed]
    [Google Scholar]
  42. 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 [CrossRef][PubMed]
    [Google Scholar]
  43. Yang M, Wang S, Yue X, Li L. Autographa californica multiple nucleopolyhedrovirus orf132 encodes a nucleocapsid-associated protein required for budded-virus and multiply enveloped occlusion-derived virus production. J Virol 2014;88:12586–12598 [CrossRef][PubMed]
    [Google Scholar]
  44. 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 [CrossRef][PubMed]
    [Google Scholar]
  45. Fang Z, Li C, Wu W, Yuan M, Yang K. The Autographa californica multiple nucleopolyhedrovirus Ac132 plays a role in nuclear entry. J Gen Virol 2016;97:3030–3038 [CrossRef][PubMed]
    [Google Scholar]
  46. Alfonso V, Maroniche GA, Reca SR, López MG, del Vas M et al. AcMNPV core gene ac109 is required for budded virion transport to the nucleus and for occlusion of viral progeny. PLoS One 2012;7:e46146 [CrossRef][PubMed]
    [Google Scholar]
  47. Wei D, Wang Y, Zhang X, Hu Z, Yuan M et al. Autographa californica Nucleopolyhedrovirus Ac76: a dimeric type II integral membrane protein that contains an inner nuclear membrane-sorting motif. J Virol 2014;88:1090–1103 [CrossRef][PubMed]
    [Google Scholar]
  48. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F et al. CDD: NCBI's conserved domain database. Nucleic Acids Res 2015;43:D222–D226 [CrossRef][PubMed]
    [Google Scholar]
  49. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK et al. CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 2011;39:D225–D229 [CrossRef][PubMed]
    [Google Scholar]
  50. Zimmermann L, Stephens A, Nam SZ, Rau D, Kübler J et al. A completely reimplemented MPI Bioinformatics Toolkit with a new HHpred server at its core. J Mol Biol 2017; [CrossRef][PubMed]
    [Google Scholar]
  51. Letunic I, Doerks T, Bork P. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 2015;43:D257–D260 [CrossRef][PubMed]
    [Google Scholar]
  52. Letunic I, Bork P. 20 years of the SMART protein domain annotation resource. Nucleic Acids Res 2018;46:D493–D496 [CrossRef][PubMed]
    [Google Scholar]
  53. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007;23:2947–2948 [CrossRef][PubMed]
    [Google Scholar]
  54. He Z, Zhang H, Gao S, Lercher MJ, Chen W et al. Evolview v2: an online visualization and management tool for customized and annotated phylogenetic trees. Nucleic Acids Res 2016;44:W236–W241 [CrossRef][PubMed]
    [Google Scholar]
  55. O'Reilly D, Miller L, Luckow V. Baculovirus Expression Vectors: A Laboratory Manual New York, NY: Oxford University Press; 1992
    [Google Scholar]
  56. 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 [CrossRef][PubMed]
    [Google Scholar]
  57. Wu W, Passarelli AL. Autographa californica multiple nucleopolyhedrovirus Ac92 (ORF92, P33) is required for budded virus production and multiply enveloped occlusion-derived virus formation. J Virol 2010;84:12351–12361 [CrossRef][PubMed]
    [Google Scholar]
  58. 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 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001066
Loading
/content/journal/jgv/10.1099/jgv.0.001066
Loading

Data & Media loading...

Supplementary File 2

PDF

Most Cited This Month

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