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. 1997 Oct;71(10):7933–7941. doi: 10.1128/jvi.71.10.7933-7941.1997

Identification of the early actin-rearrangement-inducing factor gene, arif-1, from Autographa californica multicapsid nuclear polyhedrosis virus.

R Roncarati 1, D Knebel-Mörsdorf 1
PMCID: PMC192151  PMID: 9311884

Abstract

In response to Autographa californica multicapsid nuclear polyhedrosis virus (AcMNPV) infection, a sequential rearrangement of the actin cytoskeleton occurs. Previous studies suggest that the penetration of nucleocapsids induces early actin cables followed by further changes of the actin cytoskeleton which depend on early viral gene expression. By transfection of a plasmid library into Trichoplusia ni TN-368 cells, we have identified an early viral gene, designated arif-1, that is able to induce actin rearrangement. The determination of the nucleotide sequence of arif-1 revealed one open reading frame potentially encoding a gene product of 45 kDa with no significant sequence homology to known proteins. After expression of arif-1 in transfected cells, the induced actin rearrangement, visualized by fluorescence microscopy, was comparable to the changes of the actin cytoskeleton at 3 to 7 h postinfection. These changes are based on early viral gene expression during the infection cycle. A causal link between arif-1 expression and actin rearrangement in infected cells is suggested by infection studies with the AcMNPV/Spodoptera frugiperda MNPV hybrid, which carries a deletion in the arif-1 gene. In transfection experiments the presence of the known viral transactivator IE1 was required in addition to ARIF-1 to induce actin rearrangement. IE1 was needed for promoter activation of the arif-1 gene, since arif-1 expression under the control of the early pe38 promoter was sufficient to induce actin rearrangement in transfected cells. Primer extension analyses showed that the arif-1 gene is transcribed only during the early phase of AcMNPV infection in T. ni TN-368 cells. There was a delay of about 1 h compared to ie1 transcription, which is in agreement with the assumption that IE1 transactivates the arif-1 promoter during infection.

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Selected References

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  1. Ayres M. D., Howard S. C., Kuzio J., Lopez-Ferber M., Possee R. D. The complete DNA sequence of Autographa californica nuclear polyhedrosis virus. Virology. 1994 Aug 1;202(2):586–605. doi: 10.1006/viro.1994.1380. [DOI] [PubMed] [Google Scholar]
  2. Becker D., Knebel-Mörsdorf D. Sequence and temporal appearance of the early transcribed baculovirus gene HE65. J Virol. 1993 Oct;67(10):5867–5872. doi: 10.1128/jvi.67.10.5867-5872.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blissard G. W., Rohrmann G. F. Baculovirus diversity and molecular biology. Annu Rev Entomol. 1990;35:127–155. doi: 10.1146/annurev.en.35.010190.001015. [DOI] [PubMed] [Google Scholar]
  4. Braunagel S. C., Daniel K. D., Reilly L. M., Guarino L. A., Hong T., Summers M. D. Sequence, genomic organization of the EcoRI-A fragment of Autographa californica nuclear polyhedrosis virus, and identification of a viral-encoded protein resembling the outer capsid protein VP8 of rotavirus. Virology. 1992 Dec;191(2):1003–1008. doi: 10.1016/0042-6822(92)90281-s. [DOI] [PubMed] [Google Scholar]
  5. Carson D. D., Guarino L. A., Summers M. D. Functional mapping of an AcNPV immediately early gene which augments expression of the IE-1 trans-activated 39K gene. Virology. 1988 Feb;162(2):444–451. doi: 10.1016/0042-6822(88)90485-0. [DOI] [PubMed] [Google Scholar]
  6. Charlton C. A., Volkman L. E. Penetration of Autographa californica nuclear polyhedrosis virus nucleocapsids into IPLB Sf 21 cells induces actin cable formation. Virology. 1993 Nov;197(1):245–254. doi: 10.1006/viro.1993.1585. [DOI] [PubMed] [Google Scholar]
  7. Charlton C. A., Volkman L. E. Sequential rearrangement and nuclear polymerization of actin in baculovirus-infected Spodoptera frugiperda cells. J Virol. 1991 Mar;65(3):1219–1227. doi: 10.1128/jvi.65.3.1219-1227.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chisholm G. E., Henner D. J. Multiple early transcripts and splicing of the Autographa californica nuclear polyhedrosis virus IE-1 gene. J Virol. 1988 Sep;62(9):3193–3200. doi: 10.1128/jvi.62.9.3193-3200.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cudmore S., Reckmann I., Griffiths G., Way M. Vaccinia virus: a model system for actin-membrane interactions. J Cell Sci. 1996 Jul;109(Pt 7):1739–1747. doi: 10.1242/jcs.109.7.1739. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Gonzalez M. A., Smith G. E., Summers M. D. Insertion of the SfMNPV polyhedrin gene into an AcMNPV polyhedrin deletion mutant during viral infection. Virology. 1989 May;170(1):160–175. doi: 10.1016/0042-6822(89)90363-2. [DOI] [PubMed] [Google Scholar]
  12. Guarino L. A., Summers M. D. Functional mapping of a trans-activating gene required for expression of a baculovirus delayed-early gene. J Virol. 1986 Feb;57(2):563–571. doi: 10.1128/jvi.57.2.563-571.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Guarino L. A., Summers M. D. Nucleotide sequence and temporal expression of a baculovirus regulatory gene. J Virol. 1987 Jul;61(7):2091–2099. doi: 10.1128/jvi.61.7.2091-2099.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Knebel-Mörsdorf D., Flipsen J. T., Roncarati R., Jahnel F., Kleefsman A. W., Vlak J. M. Baculovirus infection of Spodoptera exigua larvae: lacZ expression driven by promoters of early genes pe38 and me53 in larval tissue. J Gen Virol. 1996 May;77(Pt 5):815–824. doi: 10.1099/0022-1317-77-5-815. [DOI] [PubMed] [Google Scholar]
  16. Krappa R., Knebel-Mörsdorf D. Identification of the very early transcribed baculovirus gene PE-38. J Virol. 1991 Feb;65(2):805–812. doi: 10.1128/jvi.65.2.805-812.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Krappa R., Roncarati R., Knebel-Mörsdorf D. Expression of PE38 and IE2, viral members of the C3HC4 finger family, during baculovirus infection: PE38 and IE2 localize to distinct nuclear regions. J Virol. 1995 Sep;69(9):5287–5293. doi: 10.1128/jvi.69.9.5287-5293.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lanier L. M., Slack J. M., Volkman L. E. Actin binding and proteolysis by the baculovirus AcMNPV: the role of virion-associated V-CATH. Virology. 1996 Feb 15;216(2):380–388. doi: 10.1006/viro.1996.0073. [DOI] [PubMed] [Google Scholar]
  19. Lu A., Carstens E. B. Immediate-early baculovirus genes transactivate the p143 gene promoter of Autographa californica nuclear polyhedrosis virus. Virology. 1993 Aug;195(2):710–718. doi: 10.1006/viro.1993.1422. [DOI] [PubMed] [Google Scholar]
  20. Murges D., Kremer A., Knebel-Mörsdorf D. Baculovirus transactivator IE1 is functional in mammalian cells. J Gen Virol. 1997 Jun;78(Pt 6):1507–1510. doi: 10.1099/0022-1317-78-6-1507. [DOI] [PubMed] [Google Scholar]
  21. Oppenheimer D. I., Volkman L. E. Proteolysis of p6.9 induced by cytochalasin D in Autographa californica M nuclear polyhedrosis virus-infected cells. Virology. 1995 Feb 20;207(1):1–11. doi: 10.1006/viro.1995.1046. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Sanders M. C., Theriot J. A. Tails from the hall of infection: actin-based motility of pathogens. Trends Microbiol. 1996 Jun;4(6):211–213. doi: 10.1016/0966-842X(96)30017-6. [DOI] [PubMed] [Google Scholar]
  24. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tjia S. T., Carstens E. B., Doerfler W. Infection of Spodoptera frugiperda cells with Autographa californica nuclear polyhedrosis virus II. The viral DNA and the kinetics of its replication. Virology. 1979 Dec;99(2):399–409. doi: 10.1016/0042-6822(79)90018-7. [DOI] [PubMed] [Google Scholar]
  26. Vlak J. M., Smith G. E. Orientation of the Genome of Autographa californica Nuclear Polyhedrosis Virus: a Proposal. J Virol. 1982 Mar;41(3):1118–1121. doi: 10.1128/jvi.41.3.1118-1121.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Volkman L. E. Autographa californica MNPV nucleocapsid assembly: inhibition by cytochalasin D. Virology. 1988 Apr;163(2):547–553. doi: 10.1016/0042-6822(88)90295-4. [DOI] [PubMed] [Google Scholar]
  28. Volkman L. E., Zaal K. J. Autographa californica M nuclear polyhedrosis virus: microtubules and replication. Virology. 1990 Mar;175(1):292–302. doi: 10.1016/0042-6822(90)90211-9. [DOI] [PubMed] [Google Scholar]
  29. Williamson M. P. The structure and function of proline-rich regions in proteins. Biochem J. 1994 Jan 15;297(Pt 2):249–260. doi: 10.1042/bj2970249. [DOI] [PMC free article] [PubMed] [Google Scholar]

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