1887

Abstract

Cell lines derived from the silkworm, , are only permissive for nucleopolyhedrovirus (NPV), with other NPVs generally resulting in abortive infection. Here, we demonstrate that rRNA of BM-N cells undergoes rapid degradation through site-specific cleavage upon infection with NPVs from (AcMNPV), (HycuMNPV), (SeMNPV) and (SpltMNPV). No significant decreases in cellular RNA were observed in Ld652Y, Se301, Sf9, SpIm and S2 cells infected with AcMNPV or HycuMNPV, indicating the response is unique to BM-N cells. A transient expression assay using a cosmid library of the HycuMNPV genome demonstrated that HycuMNPV P143 is responsible for rRNA degradation, which was also detected in BM-N cells transfected with plasmids expressing the P143 proteins from AcMNPV, SeMNPV and SpltMNPV. These results indicate that evolved to acquire a unique antiviral immune mechanism that is activated by P143 proteins from heterologous NPVs.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.053645-0
2013-09-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/9/2102.html?itemId=/content/journal/jgv/10.1099/vir.0.053645-0&mimeType=html&fmt=ahah

References

  1. Applebaum S. W., Ebstein R. P., Wyatt G. R. 1966; Dissociation of ribosomal ribonucleic acid from silkmoth pupae by heat and dimethylsulfoxide: evidence for specific cleavage points. J Mol Biol 21:29–41 [View Article][PubMed]
    [Google Scholar]
  2. Argaud O., Croizier L., López-Ferber M., Croizier G. 1998; Two key mutations in the host-range specificity domain of the p143 gene of Autographa californica nucleopolyhedrovirus are required to kill Bombyx mori larvae. J Gen Virol 79:931–935[PubMed]
    [Google Scholar]
  3. Banerjee S., An S., Zhou A., Silverman R. H., Makino S. 2000; RNase L-independent specific 28S rRNA cleavage in murine coronavirus-infected cells. J Virol 74:8793–8802 [View Article][PubMed]
    [Google Scholar]
  4. Chejanovsky N., Gershburg E. 1995; The wild-type Autographa californica nuclear polyhedrosis virus induces apoptosis of Spodoptera littoralis cells. Virology 209:519–525 [View Article][PubMed]
    [Google Scholar]
  5. Chen Z., Carstens E. B. 2005; Identification of domains in Autographa californica multiple nucleopolyhedrovirus late expression factor 3 required for nuclear transport of P143. J Virol 79:10915–10922 [View Article][PubMed]
    [Google Scholar]
  6. Clarke T. E., Clem R. J. 2003a; Insect defenses against virus infection: the role of apoptosis. Int Rev Immunol 22:401–424 [View Article][PubMed]
    [Google Scholar]
  7. Clarke T. E., Clem R. J. 2003b; In vivo induction of apoptosis correlating with reduced infectivity during baculovirus infection. J Virol 77:2227–2232 [View Article][PubMed]
    [Google Scholar]
  8. Clem R. J. 2005; The role of apoptosis in defense against baculovirus infection in insects. Curr Top Microbiol Immunol 289:113–129 [View Article][PubMed]
    [Google Scholar]
  9. Clem R. J., Miller L. K. 1993; Apoptosis reduces both the in vitro replication and the in vivo infectivity of a baculovirus. J Virol 67:3730–3738[PubMed]
    [Google Scholar]
  10. Croizier G., Croizier L., Argaud O., Poudevigne D. 1994; Extension of Autographa californica nuclear polyhedrosis virus host range by interspecific replacement of a short DNA sequence in the p143 helicase gene. Proc Natl Acad Sci U S A 91:48–52 [View Article][PubMed]
    [Google Scholar]
  11. Dai X., Shi X., Pang Y., Su D. 1999; Prevention of baculovirus-induced apoptosis of BTI-Tn-5B1-4 (Hi5) cells by the p35 gene of Trichoplusia ni multicapsid nucleopolyhedrovirus. J Gen Virol 80:1841–1845[PubMed]
    [Google Scholar]
  12. Datsenko K. A., Wanner B. L. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645 [View Article][PubMed]
    [Google Scholar]
  13. Du X., Thiem S. M. 1997a; Responses of insect cells to baculovirus infection: protein synthesis shutdown and apoptosis. J Virol 71:7866–7872[PubMed]
    [Google Scholar]
  14. Du X., Thiem S. M. 1997b; Characterization of host range factor 1 (hrf-1) expression in Lymantria dispar M nucleopolyhedrovirus- and recombinant Autographa californica M nucleopolyhedrovirus-infected IPLB-Ld652Y cells. Virology 227:420–430 [View Article][PubMed]
    [Google Scholar]
  15. Erlandson M., Skepasts P., Kuzio J., Carstens E. B. 1984; Genomic variants of a temperature-sensitive mutant of Autographa californica nuclear polyhedrosis virus containing specific reiterations of viral DNA. Virus Res 1:565–584 [View Article]
    [Google Scholar]
  16. Felipe Alves C. A., Ikeda M., Kobayashi M. 2002; Identification and characterization of Hyphantria cunea nucleopolyhedrovirus homologous repeated regions. Virus Genes 25:281–290 [View Article][PubMed]
    [Google Scholar]
  17. Fujita R., Asano S., Sahara K., Bando H. 2005; Marked decrease of ribosomal RNA in BmN cells infected with AcMNPV. J Insect Biotechnol Sericol 74:125–128
    [Google Scholar]
  18. Goodwin R. H., Tompkins G. J., McCawley P. 1978; Gypsy moth cell lines divergent in viral susceptibility. I. Culture and identification.. In Vitro 14485–494 [CrossRef]
    [Google Scholar]
  19. Gordon J. D., Carstens E. B. 1984; Phenotypic characterization and physical mapping of a temperature-sensitive mutant of Autographa californica nuclear polyhedrosis virus defective in DNA synthesis. Virology 138:69–81 [View Article][PubMed]
    [Google Scholar]
  20. Greenberg J. R. 1969; Synthesis and properties of ribosomal RNA in Drosophila. . J Mol Biol 46:85–98 [View Article][PubMed]
    [Google Scholar]
  21. Guzo D., Dougherty E. M., Lynn D. E., Braun S. K., Weiner R. M. 1991; Changes in macromolecular synthesis of gypsy moth cell line IPLB-Ld652Y induced by Autographa californica nuclear polyhedrosis virus infection. J Gen Virol 72:1021–1029 [View Article][PubMed]
    [Google Scholar]
  22. Hara K., Funakoshi M., Kawarabata T. 1995; A cloned cell line of Spodoptera exigua has a highly increased susceptibility to the Spodoptera exigua nuclear polyhedrosis virus. Can J Microbiol 41:1111–1116 [View Article]
    [Google Scholar]
  23. Herniou E. A., Olszewski J. A., Cory J. S., O’Reilly D. R. 2003; The genome sequence and evolution of baculoviruses. Annu Rev Entomol 48:211–234 [View Article][PubMed]
    [Google Scholar]
  24. Hershberger P. A., Dickson J. A., Friesen P. D. 1992; Site-specific mutagenesis of the 35-kilodalton protein gene encoded by Autographa californica nuclear polyhedrosis virus: cell line-specific effects on virus replication. J Virol 66:5525–5533[PubMed]
    [Google Scholar]
  25. Ikeda M., Yanagimoto K., Kobayashi M. 2004; Identification and functional analysis of Hyphantria cunea nucleopolyhedrovirus iap genes. Virology 321:359–371 [View Article][PubMed]
    [Google Scholar]
  26. Ikeda M., Shikata M., Shirata N., Chaeychomsri S., Kobayashi M. 2006; Gene organization and complete sequence of the Hyphantria cunea nucleopolyhedrovirus genome. J Gen Virol 87:2549–2562 [View Article][PubMed]
    [Google Scholar]
  27. Ikeda M., Yamada H., Ito H., Kobayashi M. 2011; Baculovirus IAP1 induces caspase-dependent apoptosis in insect cells. J Gen Virol 92:2654–2663 [View Article][PubMed]
    [Google Scholar]
  28. Ikeda M., Yamada H., Hamajima R., Kobayashi M. 2013; Baculovirus genes modulating intracellular innate antiviral immunity of lepidopteran insect cells. Virology 435:1–13 [View Article][PubMed]
    [Google Scholar]
  29. Ishikawa H., Newburgh R. W. 1972; Studies of the thermal conversion of 28 S RNA of Galleria mellonella (L.) to an 18 S product. J Mol Biol 64:135–144 [View Article][PubMed]
    [Google Scholar]
  30. Ishikawa H., Ikeda M., Yanagimoto K., Alves C. A., Katou Y., Laviña-Caoili B. A., Kobayashi M. 2003; Induction of apoptosis in an insect cell line, IPLB-Ld652Y, infected with nucleopolyhedroviruses. J Gen Virol 84:705–714 [View Article][PubMed]
    [Google Scholar]
  31. Ishikawa H., Ikeda M., Alves C. A., Thiem S. M., Kobayashi M. 2004; Host range factor 1 from Lymantria dispar nucleopolyhedrovirus (NPV) is an essential viral factor required for productive infection of NPVs in IPLB-Ld652Y cells derived from L. dispar. . J Virol 78:12703–12708 [View Article][PubMed]
    [Google Scholar]
  32. Ito E., Sahri D., Knippers R., Carstens E. B. 2004; Baculovirus proteins IE-1, LEF-3, and P143 interact with DNA in vivo: a formaldehyde cross-linking study. Virology 329:337–347 [View Article][PubMed]
    [Google Scholar]
  33. Kamita S. G., Maeda S. 1993; Inhibition of Bombyx mori nuclear polyhedrosis virus (NPV) replication by the putative DNA helicase gene of Autographa californica NPV. J Virol 67:6239–6245[PubMed]
    [Google Scholar]
  34. Kamita S. G., Maeda S. 1997; Sequencing of the putative DNA helicase-encoding gene of the Bombyx mori nuclear polyhedrosis virus and fine-mapping of a region involved in host range expansion. Gene 190:173–179 [View Article][PubMed]
    [Google Scholar]
  35. Kamiya K., Okimoto N., Ikeda M., Kunimi Y., Kobayashi M., Kawamura S. 2003; Genotypic variation of a wild isolate of Hyphantria cunea nucleopolyhedrovirus. J Insect Biotechnol Sericol 72:57–64
    [Google Scholar]
  36. Katou Y., Ikeda M., Kobayashi M. 2006; Abortive replication of Bombyx mori nucleopolyhedrovirus in Sf9 and High Five cells: defective nuclear transport of the virions. Virology 347:455–465 [View Article][PubMed]
    [Google Scholar]
  37. Katou Y., Yamada H., Ikeda M., Kobayashi M. 2010; A single amino acid substitution modulates low-pH-triggered membrane fusion of GP64 protein in Autographa californica and Bombyx mori nucleopolyhedroviruses. Virology 404:204–214 [View Article][PubMed]
    [Google Scholar]
  38. Laufs S., Lu A., Arrell K., Carstens E. B. 1997; Autographa californica nuclear polyhedrosis virus p143 gene product is a DNA-binding protein. Virology 228:98–106 [View Article][PubMed]
    [Google Scholar]
  39. Laviña B. A., Padua L. E., Wu F. Q., Shirata N., Ikeda M., Kobayashi M. 2001; Biological characterization of a nucleopolyhedrovirus of Spodoptera litura (Lepidoptera: Noctuidae) isolated from the Philippines. Biol Control 20:39–47 [View Article]
    [Google Scholar]
  40. Laviña-Caoili B. A., Kamiya K., Kawamura S., Ikeda M., Kobayashi M. 2001; Comparative in vitro analysis of geographic variants of nucleopolyhedrovirus of Spodoptera litura isolated from China and the Philippines. J Insect Biotechnol Sericol 70:199–209
    [Google Scholar]
  41. Liang S.-L., Quirk D., Zhou A. 2006; RNase L: its biological roles and regulation. IUBMB Life 58:508–514 [View Article][PubMed]
    [Google Scholar]
  42. Lu A., Carstens E. B. 1991; Nucleotide sequence of a gene essential for viral DNA replication in the baculovirus Autographa californica nuclear polyhedrosis virus. Virology 181:336–347 [View Article][PubMed]
    [Google Scholar]
  43. Lu A., Miller L. K. 1996; Species-specific effects of the hcf-1 gene on baculovirus virulence. J Virol 70:5123–5130[PubMed]
    [Google Scholar]
  44. McDougal V. V., Guarino L. A. 2000; The Autographa californica nuclear polyhedrosis virus p143 gene encodes a DNA helicase. J Virol 74:5273–5279 [View Article][PubMed]
    [Google Scholar]
  45. Miller L. K., Lu A. 1997; The moleculr basis of baculovirus host range. In The Baculoviruses pp. 217–235 Edited by Miller L. K. New York: Plenum Press; [View Article]
    [Google Scholar]
  46. Mitsuhashi J., Inoue H. 1988; Obtainment of a continuous cell line from the larval fat bodies of the mulberry tiger moth, Spilosoma imparilis (Lepidoptera: Arctiidae). Appl Entomol Zool (Jpn) 23:488–490
    [Google Scholar]
  47. Mitsutake H., Kobayashi J. 2011; piggyBac-mediated stable transformation of cultured Bombyx mori cells using in vitro synthesized transposase mRNA. J Insect Biotechnol Sericol 80:15–24
    [Google Scholar]
  48. Morris T. D., Miller L. K. 1993; Characterization of productive and non-productive AcMNPV infection in selected insect cell lines. Virology 197:339–348 [View Article][PubMed]
    [Google Scholar]
  49. Nagamine T., Shimomura M., Sugimori H., Kobayashi M. 1989; Titration of Bombyx mori (Lepidoptera: Bombycidae) nuclear polyhedrosis virus in a Bombyx mori cell line. Appl Entomol Zool (Jpn) 24:235–237
    [Google Scholar]
  50. Nagamine T., Kawasaki Y., Matsumoto S. 2006; Induction of a subnuclear structure by the simultaneous expression of baculovirus proteins, IE1, LEF3, and P143 in the presence of hr. . Virology 352:400–407 [View Article][PubMed]
    [Google Scholar]
  51. Nagamine T., Abe A., Suzuki T., Dohmae N., Matsumoto S. 2011; Co-expression of four baculovirus proteins, IE1, LEF3, P143, and PP31, elicits a cellular chromatin-containing reticulate structure in the nuclei of uninfected cells. Virology 417:188–195 [View Article][PubMed]
    [Google Scholar]
  52. Palli S. R., Caputo G. F., Sohi S. S., Brownwright A. J., Ladd T. R., Cook B. J., Primavera M., Arif B. M., Retnakaran A. 1996; CfMNPV blocks AcMNPV-induced apoptosis in a continuous midgut cell line. Virology 222:201–213 [View Article][PubMed]
    [Google Scholar]
  53. Schneider I. 1972; Cell lines derived from late embryonic stages of Drosophila melanogaster. . J Embryol Exp Morphol 27:353–365[PubMed]
    [Google Scholar]
  54. Shirata N., Ikeda M., Kamiya K., Kawamura S., Kunimi Y., Kobayashi M. 1999; Replication of nucleopolyhedrovirus of Autographa californica (Lepidoptera: Noctuidae), Bombyx mori (Lepidoptera: Bombycidae), Hyphantria cunea (Lepidoptera: Arctiidae), and Spodoptera exigua (Lepidoptera: Noctuidae) in four lepidopteran cell lines. Appl Entomol Zool (Jpn) 34:507–516
    [Google Scholar]
  55. Shirata N., Ikeda M., Kamiya K., Kawamura S., Kobayashi M. 2004; Restriction of Bombyx mori nucleopolyhedrovirus (NPV) replication by Hyphantria cunea NPV in a cell line from B. mori. . J Insect Biotechnol Sericol 73:22–33
    [Google Scholar]
  56. Shirata N., Ikeda M., Kobayashi M. 2010; Identification of a Hyphantria cunea nucleopolyhedrovirus (NPV) gene that is involved in global protein synthesis shutdown and restricted Bombyx mori NPV multiplication in a B. mori cell line. Virology 398:149–157 [View Article][PubMed]
    [Google Scholar]
  57. Silverman R. H. 2007; Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J Virol 81:12720–12729 [View Article][PubMed]
    [Google Scholar]
  58. Smith G. E., Summers M. D. 1978; Analysis of baculovirus genomes with restriction endonucleases. Virology 89:517–527 [View Article][PubMed]
    [Google Scholar]
  59. Sobol P. T., Mossman K. L. 2006; ICP0 prevents RNase L-independent rRNA cleavage in herpes simplex virus type 1-infected cells. J Virol 80:218–225 [View Article][PubMed]
    [Google Scholar]
  60. Suganuma I., Ushiyama T., Yamada H., Iwamoto A., Kobayashi M., Ikeda M. 2011; Cloning and characterization of a dronc homologue in the silkworm, Bombyx mori. . Insect Biochem Mol Biol 41:909–921 [View Article][PubMed]
    [Google Scholar]
  61. Thiem S. M. 2009; Baculovirus genes affecting host function.. In Vitro Cell Dev Biol – Animal 45111–126 [CrossRef]
    [Google Scholar]
  62. van Oers M. M., Vlak J. M. 2007; Baculovirus genomics. Curr Drug Targets 8:1051–1068 [View Article][PubMed]
    [Google Scholar]
  63. Vaughn J. L., Goodwin R. H., Tompkins G. J., McCawley P. 1977; The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera; Noctuidae). In Vitro 13:213–217 [View Article][PubMed]
    [Google Scholar]
  64. Volkman L. E., Goldsmith P. A. 1982; Generalized immunoassay for Autographa californica nuclear polyhedrosis virus infectivity in vitro. Appl Environ Microbiol 44:227–233[PubMed]
    [Google Scholar]
  65. Winnebeck E. C., Millar C. D., Warman G. R. 2010; Why does insect RNA look degraded?. J Insect Sci 10:1–7 [View Article][PubMed]
    [Google Scholar]
  66. Wu F. Q., Laviña B. A., Ikeda M., Sirata N., Cai Y. X., Pan S. X., Kobayashi M. 2000; Cloning and biological characterization of Spodoptera exigua nucleopolyhedroviruses isolated in China. J Sericult Sci Jpn 69:177–189
    [Google Scholar]
  67. Yanase T., Yasunaga C., Kawarabata T. 1998; Replication of Spodoptera exigua nucleopolyhedrovirus in permissive and non-permissive lepidopteran cell lines. Acta Virol 42:293–298[PubMed]
    [Google Scholar]
  68. Yu M., Carstens E. B. 2012; Choristoneura fumiferana multiple nucleopolyhedrovirus LEF-3-P143 complex can complement DNA replication and budded virus in an AcMNPV LEF-3-P143 double knockout bacmid. J Gen Virol 93:383–388 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.053645-0
Loading
/content/journal/jgv/10.1099/vir.0.053645-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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