Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1986 Oct;60(1):215–223. doi: 10.1128/jvi.60.1.215-223.1986

Interspersed Homologous DNA of Autographa californica Nuclear Polyhedrosis Virus Enhances Delayed-Early Gene Expression

Linda A Guarino 1,*, Max D Summers 1
PMCID: PMC253919  PMID: 16789258

Abstract

The five regions of homologous DNA which are interspersed in the genome of the baculovirus Autographa californica nuclear polyhedrosis virus increased the expression of a delayed-early gene of this virus. Although this activity was first observed as a 10-fold trans effect, the homologous region 5 (hr5) enhanced the expression of linked genes 1,000-fold. The hr5 enhancer also exhibited the other characteristics associated with viral enhancer elements, including orientation independence and the abilities to function at a distance from the linked promoter, to regulate heterologous promoters, and to increase the number of RNA polymerase molecules transcribing the linked genes. The expression of the immediate-early regulatory gene was not enhanced by cis-linked hr5, although the enhancer function may require the immediate-early regulatory gene product. The hr5 enhancer was relatively insensitive to competition by an excess of enhancer molecules. The nucleotide sequence of hr5 revealed two different conserved repeats separated by nonhomologous DNA. Deletion analysis of the hr5 enhancer indicated that a 30-base-pair inverted repeat was essential for enhancer function.

Full text

PDF
219

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adang M. J., Miller L. K. Molecular cloning of DNA complementary to mRNA of the baculovirus Autographa californica nuclear polyhedrosis virus: location and gene products of RNA transcripts found late in infection. J Virol. 1982 Dec;44(3):782–793. doi: 10.1128/jvi.44.3.782-793.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Benoist C., Chambon P. In vivo sequence requirements of the SV40 early promotor region. Nature. 1981 Mar 26;290(5804):304–310. doi: 10.1038/290304a0. [DOI] [PubMed] [Google Scholar]
  3. Bergsma D. J., Olive D. M., Hartzell S. W., Subramanian K. N. Territorial limits and functional anatomy of the simian virus 40 replication origin. Proc Natl Acad Sci U S A. 1982 Jan;79(2):381–385. doi: 10.1073/pnas.79.2.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Borrelli E., Hen R., Chambon P. Adenovirus-2 E1A products repress enhancer-induced stimulation of transcription. Nature. 1984 Dec 13;312(5995):608–612. doi: 10.1038/312608a0. [DOI] [PubMed] [Google Scholar]
  5. Boshart M., Weber F., Jahn G., Dorsch-Häsler K., Fleckenstein B., Schaffner W. A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell. 1985 Jun;41(2):521–530. doi: 10.1016/s0092-8674(85)80025-8. [DOI] [PubMed] [Google Scholar]
  6. Carbonell L. F., Klowden M. J., Miller L. K. Baculovirus-mediated expression of bacterial genes in dipteran and mammalian cells. J Virol. 1985 Oct;56(1):153–160. doi: 10.1128/jvi.56.1.153-160.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Cochran M. A., Faulkner P. Location of Homologous DNA Sequences Interspersed at Five Regions in the Baculovirus AcMNPV Genome. J Virol. 1983 Mar;45(3):961–970. doi: 10.1128/jvi.45.3.961-970.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Esche H., Lübbert H., Siegmann B., Doerfler W. The translational map of the Autographa californica nuclear polyhedrosis virus (AcNPV) genome. EMBO J. 1982;1(12):1629–1633. doi: 10.1002/j.1460-2075.1982.tb01365.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Friesen P. D., Miller L. K. Temporal regulation of baculovirus RNA: overlapping early and late transcripts. J Virol. 1985 May;54(2):392–400. doi: 10.1128/jvi.54.2.392-400.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fromm M., Berg P. Deletion mapping of DNA regions required for SV40 early region promoter function in vivo. J Mol Appl Genet. 1982;1(5):457–481. [PubMed] [Google Scholar]
  13. Fuchs L. Y., Woods M. S., Weaver R. F. Viral Transcription During Autographa californica Nuclear Polyhedrosis Virus Infection: a Novel RNA Polymerase Induced in Infected Spodoptera frugiperda Cells. J Virol. 1983 Dec;48(3):641–646. doi: 10.1128/jvi.48.3.641-646.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Given D., Yee D., Griem K., Kieff E. DNA of Epstein-Barr virus. V. Direct repeats of the ends of Epstein-Barr virus DNA. J Virol. 1979 Jun;30(3):852–862. doi: 10.1128/jvi.30.3.852-862.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Gorman C. M., Merlino G. T., Willingham M. C., Pastan I., Howard B. H. The Rous sarcoma virus long terminal repeat is a strong promoter when introduced into a variety of eukaryotic cells by DNA-mediated transfection. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6777–6781. doi: 10.1073/pnas.79.22.6777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Green M. R., Treisman R., Maniatis T. Transcriptional activation of cloned human beta-globin genes by viral immediate-early gene products. Cell. 1983 Nov;35(1):137–148. doi: 10.1016/0092-8674(83)90216-7. [DOI] [PubMed] [Google Scholar]
  19. Groudine M., Peretz M., Weintraub H. Transcriptional regulation of hemoglobin switching in chicken embryos. Mol Cell Biol. 1981 Mar;1(3):281–288. doi: 10.1128/mcb.1.3.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gruss P., Dhar R., Khoury G. Simian virus 40 tandem repeated sequences as an element of the early promoter. Proc Natl Acad Sci U S A. 1981 Feb;78(2):943–947. doi: 10.1073/pnas.78.2.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Guarino L. A., Gonzalez M. A., Summers M. D. Complete Sequence and Enhancer Function of the Homologous DNA Regions of Autographa californica Nuclear Polyhedrosis Virus. J Virol. 1986 Oct;60(1):224–229. doi: 10.1128/jvi.60.1.224-229.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Hearing P., Shenk T. The adenovirus type 5 E1A transcriptional control region contains a duplicated enhancer element. Cell. 1983 Jul;33(3):695–703. doi: 10.1016/0092-8674(83)90012-0. [DOI] [PubMed] [Google Scholar]
  24. Hennessy K., Kieff E. One of two Epstein-Barr virus nuclear antigens contains a glycine-alanine copolymer domain. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5665–5669. doi: 10.1073/pnas.80.18.5665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Imperiale M. J., Feldman L. T., Nevins J. R. Activation of gene expression by adenovirus and herpesvirus regulatory genes acting in trans and by a cis-acting adenovirus enhancer element. Cell. 1983 Nov;35(1):127–136. doi: 10.1016/0092-8674(83)90215-5. [DOI] [PubMed] [Google Scholar]
  26. Kintner C. R., Sugden B. The structure of the termini of the DNA of Epstein-Barr virus. Cell. 1979 Jul;17(3):661–671. doi: 10.1016/0092-8674(79)90273-3. [DOI] [PubMed] [Google Scholar]
  27. Lang J. C., Spandidos D. A., Wilkie N. M. Transcriptional regulation of a herpes simplex virus immediate early gene is mediated through an enhancer-type sequence. EMBO J. 1984 Feb;3(2):389–395. doi: 10.1002/j.1460-2075.1984.tb01817.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lusky M., Berg L., Weiher H., Botchan M. Bovine papilloma virus contains an activator of gene expression at the distal end of the early transcription unit. Mol Cell Biol. 1983 Jun;3(6):1108–1122. doi: 10.1128/mcb.3.6.1108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  30. Rankin C., Ladin B. F., Weaver R. F. Physical mapping of temporally regulated, overlapping transcripts in the region of the 10K protein gene in Autographa californica nuclear polyhedrosis virus. J Virol. 1986 Jan;57(1):18–27. doi: 10.1128/jvi.57.1.18-27.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Schöler H. R., Gruss P. Specific interaction between enhancer-containing molecules and cellular components. Cell. 1984 Feb;36(2):403–411. doi: 10.1016/0092-8674(84)90233-2. [DOI] [PubMed] [Google Scholar]
  33. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  34. Tamanoi F., Stillman B. W. The origin of adenovirus DNA replication. Curr Top Microbiol Immunol. 1984;109:75–87. doi: 10.1007/978-3-642-69460-8_3. [DOI] [PubMed] [Google Scholar]
  35. Treisman R., Maniatis T. Simian virus 40 enhancer increases number of RNA polymerase II molecules on linked DNA. Nature. 1985 May 2;315(6014):73–75. doi: 10.1038/315072a0. [DOI] [PubMed] [Google Scholar]
  36. Tyndall C., La Mantia G., Thacker C. M., Favaloro J., Kamen R. A region of the polyoma virus genome between the replication origin and late protein coding sequences is required in cis for both early gene expression and viral DNA replication. Nucleic Acids Res. 1981 Dec 11;9(23):6231–6250. doi: 10.1093/nar/9.23.6231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Vlak J. M., Smith G. E., Summers M. D. Hybridization Selection and In Vitro Translation of Autographa californica Nuclear Polyhedrosis Virus mRNA. J Virol. 1981 Dec;40(3):762–771. doi: 10.1128/jvi.40.3.762-771.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Weaver R. F., Weissmann C. Mapping of RNA by a modification of the Berk-Sharp procedure: the 5' termini of 15 S beta-globin mRNA precursor and mature 10 s beta-globin mRNA have identical map coordinates. Nucleic Acids Res. 1979 Nov 10;7(5):1175–1193. doi: 10.1093/nar/7.5.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Weber F., Schaffner W. Simian virus 40 enhancer increases RNA polymerase density within the linked gene. Nature. 1985 May 2;315(6014):75–77. doi: 10.1038/315075a0. [DOI] [PubMed] [Google Scholar]
  41. Weeks D. L., Jones N. C. E1A control of gene expression is mediated by sequences 5' to the transcriptional starts of the early viral genes. Mol Cell Biol. 1983 Jul;3(7):1222–1234. doi: 10.1128/mcb.3.7.1222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Weiher H., König M., Gruss P. Multiple point mutations affecting the simian virus 40 enhancer. Science. 1983 Feb 11;219(4585):626–631. doi: 10.1126/science.6297005. [DOI] [PubMed] [Google Scholar]
  43. de Villiers J., Schaffner W. A small segment of polyoma virus DNA enhances the expression of a cloned beta-globin gene over a distance of 1400 base pairs. Nucleic Acids Res. 1981 Dec 11;9(23):6251–6264. doi: 10.1093/nar/9.23.6251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. de Villiers J., Schaffner W., Tyndall C., Lupton S., Kamen R. Polyoma virus DNA replication requires an enhancer. Nature. 1984 Nov 15;312(5991):242–246. doi: 10.1038/312242a0. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES