1887

Abstract

nucleopolyhedrovirus () and its homologues are highly conserved in genomes of all sequenced group I alphabaculoviruses and its function is still unknown. Transcriptional analysis revealed that is a very late gene initiated from a late transcriptional start motif TAAG. To examine its role in the virus, a knockout virus (vBm) was generated through homologous recombination in . Analysis of fluorescence microscopy, titration assays and electron microscopy examination showed that the deletion of did not affect viral replication and occlusion bodies formation , indicating that is not required for viral propagation. However, vBm did not result in cell lysis when wild-type virus infected cells began to lyse, and the vBm infected cells remained intact until 2 weeks post-infection. Quantification of polyhedra release from cells confirmed this observation. Accordingly, though deletion of did not reduce nucleopolyhedrovirus infectivity in bioassays, it did significantly disrupt the larval liquefaction, reducing the level of polyhedra release from infected host. Immunofluorescence analysis demonstrated that Bm58a was predominantly localized on the cellular membrane at the late stage of infection, which may contribute to its function of facilitating cell lysis and larval liquefaction. Our results suggest that although is not essential for viral propagation as an auxiliary gene, it is a key factor of virus-induced cell lysis and larval liquefaction and .

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000614
2016-11-10
2019-12-11
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/11/3039.html?itemId=/content/journal/jgv/10.1099/jgv.0.000614&mimeType=html&fmt=ahah

References

  1. Blissard G. W., Rohrmann G. F.. 1990; Baculovirus diversity and molecular biology. Annu Rev Entomol35:127–155 [CrossRef][PubMed]
    [Google Scholar]
  2. Braunagel S. C., Russell W. K., Rosas-Acosta G., Russell D. H., Summers M. D.. 2003; Determination of the protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus. Proc Natl Acad Sci U S A100:9797–9802 [CrossRef][PubMed]
    [Google Scholar]
  3. Carrasco L.. 1995; Modification of membrane permeability by animal viruses. Adv Virus Res45:61–112[PubMed][CrossRef]
    [Google Scholar]
  4. Chen L., Shen Y. W., Yang R., Wu X. F., Hu W. J., Shen G. X.. 2015; Bombyx mori nucleopolyhedrovirus (BmNPV) Bm64 is required for BV production and per os infection. Virol J12:173 [CrossRef][PubMed]
    [Google Scholar]
  5. D'Amico V., Slavicek J., Podgwaite J. D., Webb R., Fuester R., Peiffer R. A.. 2013; Deletion of v-chiA from a baculovirus reduces horizontal transmission in the field. Appl Environ Microbiol79:4056–4064 [CrossRef][PubMed]
    [Google Scholar]
  6. Detvisitsakun C., Berretta M. F., Lehiy C., Passarelli A. L.. 2005; Stimulation of cell motility by a viral fibroblast growth factor homolog: proposal for a role in viral pathogenesis. Virology336:308–317 [CrossRef][PubMed]
    [Google Scholar]
  7. Detvisitsakun C., Cain E. L., Passarelli A. L.. 2007; The Autographa californica M nucleopolyhedrovirus fibroblast growth factor accelerates host mortality. Virology365:70–78 [CrossRef][PubMed]
    [Google Scholar]
  8. Fang M., Dai X., Theilmann D. A.. 2007; Autographa californica multiple nucleopolyhedrovirus EXON0 (ORF141) is required for efficient egress of nucleocapsids from the nucleus. J Virol81:9859–9869 [CrossRef][PubMed]
    [Google Scholar]
  9. Fang M., Nie Y., Harris S., Erlandson M. A., Theilmann D. A.. 2009; Autographa californica multiple nucleopolyhedrovirus core gene ac96 encodes a per os infectivity factor (PIF-4). J Virol83:12569–12578 [CrossRef][PubMed]
    [Google Scholar]
  10. Friesen A. D.. 1997; Regulation of baculovirus early gene expression. In The Baculoviruses , pp.141–166 Edited by Miller L. K. E.. New York: Plenum Press;[CrossRef]
    [Google Scholar]
  11. Gomi S., Majima K., Maeda S.. 1999; Sequence analysis of the genome of Bombyx mori nucleopolyhedrovirus. J Gen Virol80:1323–1337 [CrossRef][PubMed]
    [Google Scholar]
  12. Gonzalez M. E., Carrasco L.. 2003; Viroporins. FEBS Lett552:28–34 [CrossRef][PubMed]
    [Google Scholar]
  13. Haas A. L., Katzung D. J., Reback P. M., Guarino L. A.. 1996; Functional characterization of the ubiquitin variant encoded by the baculovirus Autographa californica. Biochemistry35:5385–5394 [CrossRef][PubMed]
    [Google Scholar]
  14. Hawtin R. E., Zarkowska T., Arnold K., Thomas C. J., Gooday G. W., King L. A., Kuzio J. A., Possee R. D.. 1997; Liquefaction of Autographa californica nucleopolyhedrovirus-infected insects is dependent on the integrity of virus-encoded chitinase and cathepsin genes. Virology238:243–253 [CrossRef][PubMed]
    [Google Scholar]
  15. Herniou E. A., Olszewski J. A., Cory J. S., O'Reilly D. R.. 2003; The genome sequence and evolution of baculoviruses. Annu Rev Entomol48:211–234 [CrossRef][PubMed]
    [Google Scholar]
  16. Hodgson J. J., Arif B. M., Krell P. J.. 2011; Interaction of Autographa californica multiple nucleopolyhedrovirus cathepsin protease progenitor (proV-CATH) with insect baculovirus chitinase as a mechanism for proV-CATH cellular retention. J Virol85:3918–3929 [CrossRef][PubMed]
    [Google Scholar]
  17. Hodgson J. J., Arif B. M., Krell P. J.. 2013; Role of interactions between Autographa californica multiple nucleopolyhedrovirus procathepsin and chitinase chitin-binding or active-site domains in viral cathepsin processing. J Virol87:3471–3483 [CrossRef][PubMed]
    [Google Scholar]
  18. Hu Z., Yuan M., Wu W., Liu C., Yang K., Pang Y.. 2010; Autographa californica multiple nucleopolyhedrovirus ac76 is involved in intranuclear microvesicle formation. J Virol84:7437–7447 [CrossRef][PubMed]
    [Google Scholar]
  19. Jain A., Hasnain S. E.. 1996; A 30-kDa host protein binds to two very-late baculovirus promoters. Eur J Biochem239:384–390 [CrossRef][PubMed]
    [Google Scholar]
  20. Kamita S. G., Nagasaka K., Chua J. W., Shimada T., Mita K., Kobayashi M., Maeda S., Hammock B. D.. 2005; A baculovirus-encoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host. Proc Natl Acad Sci U S A102:2584–2589 [CrossRef][PubMed]
    [Google Scholar]
  21. Katsuma S., Fujii T., Kawaoka S., Shimada T.. 2008; Bombyx mori nucleopolyhedrovirus SNF2 global transactivator homologue (Bm33) enhances viral pathogenicity in B. mori larvae. J Gen Virol89:3039–3046 [CrossRef][PubMed]
    [Google Scholar]
  22. Katsuma S., Nakanishi T., Daimon T., Shimada T.. 2009; N-linked glycans located in the pro-region of Bombyx mori nucleopolyhedrovirus V-CATH are essential for the proper folding of V-CATH and V-CHIA. J Gen Virol90:170–176 [CrossRef][PubMed]
    [Google Scholar]
  23. Lama J., Carrasco L.. 1992; Expression of poliovirus nonstructural proteins in Escherichia coli cells. modification of membrane permeability induced by 2B and 3A. J Biol Chem267:15932–15937[PubMed]
    [Google Scholar]
  24. Lehiy C. J., Martinez O., Passarelli A. L.. 2009; Virion-associated viral fibroblast growth factor stimulates cell motility. Virology395:152–160 [CrossRef][PubMed]
    [Google Scholar]
  25. Li Y., Wang J., Deng R., Zhang Q., Yang K., Wang X.. 2005; vlf-1 deletion brought AcMNPV to defect in nucleocapsid formation. Virus Genes31:275–284 [CrossRef][PubMed]
    [Google Scholar]
  26. Lin G., Blissard G. W.. 2002; Analysis of an Autographa californica nucleopolyhedrovirus lef-11 knockout: LEF-11 is essential for viral DNA replication. J Virol76:2770–2779 [CrossRef][PubMed]
    [Google Scholar]
  27. Marchler-Bauer A., Bryant S. H.. 2004; CD-Search: protein domain annotations on the fly. Nucleic Acids Res32:W327–W331 [CrossRef][PubMed]
    [Google Scholar]
  28. Marchler-Bauer A., Anderson J. B., Chitsaz F., Derbyshire M. K., DeWeese-Scott C., Fong J. H., Geer L. Y., Geer R. C., Gonzales N. R. et al. 2009; CDD: specific functional annotation with the conserved domain database. Nucleic Acids Res37:D205–D210 [CrossRef][PubMed]
    [Google Scholar]
  29. Marchler-Bauer A., Lu S., Anderson J. B., Chitsaz F., Derbyshire M. K., DeWeese-Scott C., Fong J. H., Geer L. Y., Geer R. C. et al. 2011; CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res39:D225–D229 [CrossRef][PubMed]
    [Google Scholar]
  30. Marchler-Bauer A., Derbyshire M. K., Gonzales N. R., Lu S., Chitsaz F., Geer L. Y., Geer R. C., He J., Gwadz M. et al. 2015; CDD: NCBI's conserved domain database. Nucleic Acids Res43:D222–D226 [CrossRef][PubMed]
    [Google Scholar]
  31. Nieva J. L., Madan V., Carrasco L.. 2012; Viroporins: structure and biological functions. Nat Rev Microbiol10:563–574 [CrossRef][PubMed]
    [Google Scholar]
  32. O'Reilly D. R.. 1997; Auxiliary genes of baculoviruses. In The Baculoviruses , pp.267–300 Edited by Miller L. K.. New York, USA: Plenum Press;[CrossRef]
    [Google Scholar]
  33. O'Reilly D. R., Miller L. K.. 1989; A baculovirus blocks insect molting by producing ecdysteroid UDP-glucosyl transferase. Science245:1110–1112 [CrossRef][PubMed]
    [Google Scholar]
  34. O'Reilly D. R., Miller L. K., Luckow V. A.. 1992; Baculovirus Expression Vector: A Laboratory Manual New York, NY: W.H. Freeman;
    [Google Scholar]
  35. Ohkawa T., Majima K., Maeda S.. 1994; A cysteine protease encoded by the baculovirus Bombyx mori nuclear polyhedrosis virus. J Virol68:6619–6625[PubMed]
    [Google Scholar]
  36. Ono C., Kamagata T., Taka H., Sahara K., Asano S., Bando H.. 2012; Phenotypic grouping of 141 BmNPVs lacking viral gene sequences. Virus Res165:197–206 [CrossRef][PubMed]
    [Google Scholar]
  37. Ooi B. G., Miller L. K.. 1988; Regulation of host RNA levels during baculovirus infection. Virology166:515–523 [CrossRef][PubMed]
    [Google Scholar]
  38. Passarelli A. L., Miller L. K.. 1993; Identification and characterization of lef-1, a baculovirus gene involved in late and very late gene expression. J Virol67:3481–3488[PubMed]
    [Google Scholar]
  39. Patmanidi A. L., Possee R. D., King L. A.. 2003; Formation of P10 tubular structures during AcMNPV infection depends on the integrity of host-cell microtubules. Virology317:308–320 [CrossRef][PubMed]
    [Google Scholar]
  40. Rohrmann G. F.. 2013; Baculovirus Molecular Biology Bethesda, MD: National Center for Biotechnology Information, National Library of Medicine;
    [Google Scholar]
  41. Sanz M. A., Pérez L., Carrasco L.. 1994; Semliki forest virus 6K protein modifies membrane permeability after inducible expression in Escherichia coli cells. J Biol Chem269:12106–12110[PubMed]
    [Google Scholar]
  42. Saville G. P., Patmanidi A. L., Possee R. D., King L. A.. 2004; Deletion of the Autographa californica nucleopolyhedrovirus chitinase KDEL motif and in vitro and in vivo analysis of the modified virus. J Gen Virol85:821–831 [CrossRef][PubMed]
    [Google Scholar]
  43. Slack J., Arif B. M.. 2007; The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res69:99–165 [CrossRef][PubMed]
    [Google Scholar]
  44. Slack J. M., Kuzio J., Faulkner P.. 1995; Characterization of v-cath, a cathepsin L-like proteinase expressed by the baculovirus Autographa californica multiple nuclear polyhedrosis virus. J Gen Virol76:1091–1098 [CrossRef][PubMed]
    [Google Scholar]
  45. Suzuki T., Orba Y., Okada Y., Sunden Y., Kimura T., Tanaka S., Nagashima K., Hall W. W., Sawa H.. 2010; The human polyoma JC virus agnoprotein acts as a viroporin. PLoS Pathog6:e1000801 [CrossRef][PubMed]
    [Google Scholar]
  46. Theilmann D. A., Blissard G. W., Bonning B., Jehle J. A., O'Reilly D. R., Rohrmann G. F., Thiem S., Vlak J. M.. 2005; Baculoviridae. In Virus Taxonomy-Eighth Report of the International Committee on Taxonomy of Viruses , pp.1129–1185 Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A.. New York: Springer;
    [Google Scholar]
  47. Thomas C. J., Brown H. L., Hawes C. R., Lee B. Y., Min M. K., King L. A., Possee R. D.. 1998; Localization of a baculovirus-induced chitinase in the insect cell endoplasmic reticulum. J Virol72:10207–10212[PubMed]
    [Google Scholar]
  48. Tomita S., Kanaya T., Kobayashi J., Imanishi S.. 1995; Isolation of p10 gene from Bombyx mori nuclear polyhedrosis virus and study of its promoter activity in recombinant baculovirus vector system. Cytotechnology17:65–70 [CrossRef][PubMed]
    [Google Scholar]
  49. van Houte S., Ros V. I. D., Mastenbroek T. G., Vendrig N. J., Hoover K., Spitzen J., van Oers M. M.. 2012; Protein tyrosine phosphatase-induced hyperactivity is a conserved strategy of a subset of baculoviruses to manipulate lepidopteran host behavior. PLoS One7:e46933 [CrossRef][PubMed]
    [Google Scholar]
  50. van Oers M. M., Flipsen J. T., Reusken C. B., Sliwinsky E. L., Goldbach R. W., Vlak J. M.. 1993; Functional domains of the p10 protein of Autographa californica nuclear polyhedrosis virus. J Gen Virol74:563–574 [CrossRef][PubMed]
    [Google Scholar]
  51. Wang R., Deng F., Hou D., Zhao Y., Guo L., Wang H., Hu Z.. 2010; Proteomics of the Autographa californica nucleopolyhedrovirus budded virions. J Virol84:7233–7242 [CrossRef][PubMed]
    [Google Scholar]
  52. Williams G. V., Rohel D. Z., Kuzio J., Faulkner P.. 1989; A cytopathological investigation of Autographa californica nuclear polyhedrosis virus p10 gene function using insertion/deletion mutants. J Gen Virol70:187–202 [CrossRef][PubMed]
    [Google Scholar]
  53. Wu W., Lin T., Pan L., Yu M., Li Z., Pang Y., Yang K.. 2006; Autographa californica multiple nucleopolyhedrovirus nucleocapsid assembly is interrupted upon deletion of the 38K gene. J Virol80:11475–11485 [CrossRef][PubMed]
    [Google Scholar]
  54. Xu H. J., Yang Z. N., Zhao J. F., Tian C. H., Ge J. Q., Tang X. D., Bao Y. Y., Zhang C. X.. 2008; Bombyx mori nucleopolyhedrovirus ORF56 encodes an occlusion-derived virus protein and is not essential for budded virus production. J Gen Virol89:1212–1219 [CrossRef][PubMed]
    [Google Scholar]
  55. Yang Z. N., Xu H. J., Thiem S. M., Xu Y. P., Ge J. Q., Tang X. D., Tian C. H., Zhang C. X.. 2009; Bombyx mori nucleopolyhedrovirus ORF9 is a gene involved in the budded virus production and infectivity. J Gen Virol90:162–169 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000614
Loading
/content/journal/jgv/10.1099/jgv.0.000614
Loading

Data & Media loading...

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