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. 1993 Jul;67(7):3730–3738. doi: 10.1128/jvi.67.7.3730-3738.1993

Apoptosis reduces both the in vitro replication and the in vivo infectivity of a baculovirus.

R J Clem 1, L K Miller 1
PMCID: PMC237736  PMID: 8510202

Abstract

Apoptotic programmed cell death occurs when the insect cell line SF-21, derived from Spodoptera frugiperda, is infected with mutants of the baculovirus Autographa californica nuclear polyhedrosis virus (AcMNPV) which lack a functional p35 gene. However, infection of the Trichoplusia ni TN-368 cell line with p35 mutants does not result in apoptosis (R. Clem, M. Fechheimer, and L. Miller, Science 254:1388-1390, 1991). We have examined the effect of apoptosis on AcMNPV infections in cell lines and larvae of these two insect species. Production of viral progeny was significantly lower in SF-21 cells infected with p35 mutants than in cells infected with wild-type (wt) or revertant viruses. Viral gene expression was abnormal in SF-21 cells infected with p35 mutants; there was a delay in the transcription and translation of early and late viral genes, a lack of expression of very late genes, and a total cessation of protein synthesis late in the apoptotic process. In vivo analysis revealed that the dose of budded virus required for 50% lethality in S. frugiperda larvae was approximately 1,000-fold higher for p35 mutants than for wt or revertant viruses. In contrast, the replication and infectivity of p35 mutant viruses was equivalent to that of wt AcMNPV during infection of both TN-368 cells and T. ni larvae. Thus, the data indicate that a host apoptotic response provides protection against viral infection at the organismal level and that the p35 gene constitutes a host range determinant for AcMNPV infection.

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Selected References

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  1. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  2. Chou J., Roizman B. The gamma 1(34.5) gene of herpes simplex virus 1 precludes neuroblastoma cells from triggering total shutoff of protein synthesis characteristic of programed cell death in neuronal cells. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3266–3270. doi: 10.1073/pnas.89.8.3266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Clem R. J., Fechheimer M., Miller L. K. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science. 1991 Nov 29;254(5036):1388–1390. doi: 10.1126/science.1962198. [DOI] [PubMed] [Google Scholar]
  4. Clouston W. M., Kerr J. F. Apoptosis, lymphocytotoxicity and the containment of viral infections. Med Hypotheses. 1985 Dec;18(4):399–404. doi: 10.1016/0306-9877(85)90107-0. [DOI] [PubMed] [Google Scholar]
  5. Crawford A. M., Miller L. K. Characterization of an early gene accelerating expression of late genes of the baculovirus Autographa californica nuclear polyhedrosis virus. J Virol. 1988 Aug;62(8):2773–2781. doi: 10.1128/jvi.62.8.2773-2781.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crook N. E., Clem R. J., Miller L. K. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J Virol. 1993 Apr;67(4):2168–2174. doi: 10.1128/jvi.67.4.2168-2174.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Danyluk G. M., Maruniak J. E. In vivo and in vitro host range of Autographa californica nuclear polyhedrosis virus and Spodoptera frugiperda nuclear polyhedrosis virus. J Invertebr Pathol. 1987 Nov;50(3):207–212. doi: 10.1016/0022-2011(87)90084-x. [DOI] [PubMed] [Google Scholar]
  8. Dickson J. A., Friesen P. D. Identification of upstream promoter elements mediating early transcription from the 35,000-molecular-weight protein gene of Autographa californica nuclear polyhedrosis virus. J Virol. 1991 Aug;65(8):4006–4016. doi: 10.1128/jvi.65.8.4006-4016.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Friesen P. D., Miller L. K. Divergent transcription of early 35- and 94-kilodalton protein genes encoded by the HindIII K genome fragment of the baculovirus Autographa californica nuclear polyhedrosis virus. J Virol. 1987 Jul;61(7):2264–2272. doi: 10.1128/jvi.61.7.2264-2272.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gordon J. D., Carstens E. B. Phenotypic characterization and physical mapping of a temperature-sensitive mutant of Autographa californica nuclear polyhedrosis virus defective in DNA synthesis. Virology. 1984 Oct 15;138(1):69–81. doi: 10.1016/0042-6822(84)90148-x. [DOI] [PubMed] [Google Scholar]
  11. Gregory C. D., Dive C., Henderson S., Smith C. A., Williams G. T., Gordon J., Rickinson A. B. Activation of Epstein-Barr virus latent genes protects human B cells from death by apoptosis. Nature. 1991 Feb 14;349(6310):612–614. doi: 10.1038/349612a0. [DOI] [PubMed] [Google Scholar]
  12. Griebel P. J., Ohmann H. B., Lawman M. J., Babiuk L. A. The interaction between bovine herpesvirus type 1 and activated bovine T lymphocytes. J Gen Virol. 1990 Feb;71(Pt 2):369–377. doi: 10.1099/0022-1317-71-2-369. [DOI] [PubMed] [Google Scholar]
  13. Henderson S., Rowe M., Gregory C., Croom-Carter D., Wang F., Longnecker R., Kieff E., Rickinson A. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell. 1991 Jun 28;65(7):1107–1115. doi: 10.1016/0092-8674(91)90007-l. [DOI] [PubMed] [Google Scholar]
  14. Hershberger P. A., Dickson J. A., Friesen P. D. 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. 1992 Sep;66(9):5525–5533. doi: 10.1128/jvi.66.9.5525-5533.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hink W. F. Established insect cell line from the cabbage looper, Trichoplusia ni. Nature. 1970 May 2;226(5244):466–467. doi: 10.1038/226466b0. [DOI] [PubMed] [Google Scholar]
  16. Huh N. E., Weaver R. F. Identifying the RNA polymerases that synthesize specific transcripts of the Autographa californica nuclear polyhedrosis virus. J Gen Virol. 1990 Jan;71(Pt 1):195–201. doi: 10.1099/0022-1317-71-1-195. [DOI] [PubMed] [Google Scholar]
  17. Jeurissen S. H., Wagenaar F., Pol J. M., van der Eb A. J., Noteborn M. H. Chicken anemia virus causes apoptosis of thymocytes after in vivo infection and of cell lines after in vitro infection. J Virol. 1992 Dec;66(12):7383–7388. doi: 10.1128/jvi.66.12.7383-7388.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kamita S. G., Majima K., Maeda S. Identification and characterization of the p35 gene of Bombyx mori nuclear polyhedrosis virus that prevents virus-induced apoptosis. J Virol. 1993 Jan;67(1):455–463. doi: 10.1128/jvi.67.1.455-463.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kerr J. F., Wyllie A. H., Currie A. R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972 Aug;26(4):239–257. doi: 10.1038/bjc.1972.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  21. Lee H. H., Miller L. K. Isolation of genotypic variants of Autographa californica nuclear polyhedrosis virus. J Virol. 1978 Sep;27(3):754–767. doi: 10.1128/jvi.27.3.754-767.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Levine B., Huang Q., Isaacs J. T., Reed J. C., Griffin D. E., Hardwick J. M. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature. 1993 Feb 25;361(6414):739–742. doi: 10.1038/361739a0. [DOI] [PubMed] [Google Scholar]
  23. Lu A., Carstens E. B. Nucleotide sequence of a gene essential for viral DNA replication in the baculovirus Autographa californica nuclear polyhedrosis virus. Virology. 1991 Mar;181(1):336–347. doi: 10.1016/0042-6822(91)90500-b. [DOI] [PubMed] [Google Scholar]
  24. Martz E., Howell D. M. CTL: virus control cells first and cytolytic cells second? DNA fragmentation, apoptosis and the prelytic halt hypothesis. Immunol Today. 1989 Mar;10(3):79–86. doi: 10.1016/0167-5699(89)90231-4. [DOI] [PubMed] [Google Scholar]
  25. Meyaard L., Otto S. A., Jonker R. R., Mijnster M. J., Keet R. P., Miedema F. Programmed death of T cells in HIV-1 infection. Science. 1992 Jul 10;257(5067):217–219. doi: 10.1126/science.1352911. [DOI] [PubMed] [Google Scholar]
  26. Morris T. D., Miller L. K. Promoter influence on baculovirus-mediated gene expression in permissive and nonpermissive insect cell lines. J Virol. 1992 Dec;66(12):7397–7405. doi: 10.1128/jvi.66.12.7397-7405.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nissen M. S., Friesen P. D. Molecular analysis of the transcriptional regulatory region of an early baculovirus gene. J Virol. 1989 Feb;63(2):493–503. doi: 10.1128/jvi.63.2.493-503.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. O'Reilly D. R., Crawford A. M., Miller L. K. Viral proliferating cell nuclear antigen. Nature. 1989 Feb 16;337(6208):606–606. doi: 10.1038/337606a0. [DOI] [PubMed] [Google Scholar]
  29. O'Reilly D. R., Miller L. K. Regulation of expression of a baculovirus ecdysteroid UDPglucosyltransferase gene. J Virol. 1990 Mar;64(3):1321–1328. doi: 10.1128/jvi.64.3.1321-1328.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. O'Reilly D. R., Passarelli A. L., Goldman I. F., Miller L. K. Characterization of the DA26 gene in a hypervariable region of the Autographa californica nuclear polyhedrosis virus genome. J Gen Virol. 1990 May;71(Pt 5):1029–1037. doi: 10.1099/0022-1317-71-5-1029. [DOI] [PubMed] [Google Scholar]
  31. Ooi B. G., Rankin C., Miller L. K. Downstream sequences augment transcription from the essential initiation site of a baculovirus polyhedrin gene. J Mol Biol. 1989 Dec 20;210(4):721–736. doi: 10.1016/0022-2836(89)90105-8. [DOI] [PubMed] [Google Scholar]
  32. Passarelli A. L., Miller L. K. Three baculovirus genes involved in late and very late gene expression: ie-1, ie-n, and lef-2. J Virol. 1993 Apr;67(4):2149–2158. doi: 10.1128/jvi.67.4.2149-2158.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rice W. C., Miller L. K. Baculovirus transcription in the presence of inhibitors and in nonpermissive Drosophila cells. Virus Res. 1986 Nov;6(2):155–172. doi: 10.1016/0168-1702(86)90047-x. [DOI] [PubMed] [Google Scholar]
  34. Thiem S. M., Miller L. K. Identification, sequence, and transcriptional mapping of the major capsid protein gene of the baculovirus Autographa californica nuclear polyhedrosis virus. J Virol. 1989 May;63(5):2008–2018. doi: 10.1128/jvi.63.5.2008-2018.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Umar M. H., van Griensven L. J. Effects of Rauscher leukemia virus infection on BALB/c mouse embryos. J Natl Cancer Inst. 1976 Feb;56(2):375–380. doi: 10.1093/jnci/56.2.375. [DOI] [PubMed] [Google Scholar]
  36. Vaughn J. L., Goodwin R. H., Tompkins G. J., McCawley P. The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera; Noctuidae). In Vitro. 1977 Apr;13(4):213–217. doi: 10.1007/BF02615077. [DOI] [PubMed] [Google Scholar]
  37. Walker N. I., Harmon B. V., Gobé G. C., Kerr J. F. Patterns of cell death. Methods Achiev Exp Pathol. 1988;13:18–54. [PubMed] [Google Scholar]
  38. White E., Sabbatini P., Debbas M., Wold W. S., Kusher D. I., Gooding L. R. The 19-kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor alpha. Mol Cell Biol. 1992 Jun;12(6):2570–2580. doi: 10.1128/mcb.12.6.2570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Whitford M., Stewart S., Kuzio J., Faulkner P. Identification and sequence analysis of a gene encoding gp67, an abundant envelope glycoprotein of the baculovirus Autographa californica nuclear polyhedrosis virus. J Virol. 1989 Mar;63(3):1393–1399. doi: 10.1128/jvi.63.3.1393-1399.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

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