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. 1980 Jun;34(3):658–664. doi: 10.1128/jvi.34.3.658-664.1980

Adenovirus regulation of simian virus 40 macromolecular synthesis.

N Goldman, G Khoury
PMCID: PMC288754  PMID: 6247504

Abstract

At low multiplicities of infection (1 to 5 PFU/cell), human adenoviruses grew inefficiently in monkey kidney cells as the result of a late transcriptional and/or translational defect. Through an unknown mechanism, coinfection with simian virus 40 (SV40) could overcome this block. Coincident with the onset of adenovirus DNA replication in coinfected monkey cells, however, there was a marked inhibition of SV40 DNA replication. Since this inhibition in SV40 DNA synthesis occurred in the presence of normal SV40 transcription and protein synthesis, we suggest that adenovirus competes with SV40 for molecules specifically required for DNA synthesis (e.g., SV40 T-antigen). At high multiplicities of adenovirus infection (50 PFU/cell), adenoviruses could grow efficiently in monkey kidney cells. In cells coinfected under these conditions, SV40 transcription was generally inhibited, as shown by a decrease in nuclear and cytoplasmic SV40 mRNA.

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Selected References

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  1. Alton T. H., Koch A. L. Unused protein synthetic capacity of Escherichia coli grown in phosphate-limited chemostats. J Mol Biol. 1974 Jun 15;86(1):1–9. doi: 10.1016/s0022-2836(74)80002-1. [DOI] [PubMed] [Google Scholar]
  2. Baum S. G., Horwitz M. S., Maizel J. V., Jr Studies of the mechanism of enhancement of human adenovirus infection in monkey cells by simian virus 40. J Virol. 1972 Aug;10(2):211–219. doi: 10.1128/jvi.10.2.211-219.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baum S. G. Persistent adenovirus infections of nonpermissive monkey cells. J Virol. 1977 Aug;23(2):412–420. doi: 10.1128/jvi.23.2.412-420.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bello L. J., Ginsberg H. S. Inhibition of host protein synthesis in type 5 adenovirus-infected cells. J Virol. 1967 Oct;1(5):843–850. doi: 10.1128/jvi.1.5.843-850.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beltz G. A., Flint S. J. Inhibition of HeLa cell protein synthesis during adenovirus infection. Restriction of cellular messenger RNA sequences to the nucleus. J Mol Biol. 1979 Jun 25;131(2):353–373. doi: 10.1016/0022-2836(79)90081-0. [DOI] [PubMed] [Google Scholar]
  6. Chou J. Y., Avila J., Martin R. G. Viral DNA synthesis in cells infected by temperature-sensitive mutants of simian virus 40. J Virol. 1974 Jul;14(1):116–124. doi: 10.1128/jvi.14.1.116-124.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cole C. N., Crawford L. V., Berg P. Simian virus 40 mutants with deletions at the 3' end of the early region are defective in adenovirus helper function. J Virol. 1979 Jun;30(3):683–691. doi: 10.1128/jvi.30.3.683-691.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eron L. Post-transcriptional restriction of human adenovirus expression in monkey cells. J Virol. 1975 May;15(5):1256–1261. doi: 10.1128/jvi.15.5.1256-1261.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Friedman M. P., Lyons M. J., Ginsberg H. S. Biochemical consequences of type 2 adenovirus and Simian virus 40 double infections of African green monkey kidney cells. J Virol. 1970 May;5(5):586–597. doi: 10.1128/jvi.5.5.586-597.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hashimoto K., Nakajima K., Oda K., Shimojo H. Complementation of translational defect for growth of human adenovirus type 2 in Simian cells by a Simian virus 40-induced factor. J Mol Biol. 1973 Dec 5;81(2):207–223. doi: 10.1016/0022-2836(73)90190-3. [DOI] [PubMed] [Google Scholar]
  11. Hayward G. S. Gel electrophoretic separation of the complementary strands of bacteriophage DNA. Virology. 1972 Jul;49(1):342–344. doi: 10.1016/s0042-6822(72)80042-4. [DOI] [PubMed] [Google Scholar]
  12. Jerkofsky M. Enhancement of the replication of human adenovirus in simian cells by a series of temperature-sensitive mutants of simian virus 40. Virology. 1975 Jun;65(2):579–582. doi: 10.1016/0042-6822(75)90063-x. [DOI] [PubMed] [Google Scholar]
  13. Jessel D., Landau T., Hudson J., Lalor T., Tenen D., Livingston D. M. Identification of regions of the SV40 genome which contain preferred SV40 T antigen-binding sites. Cell. 1976 Aug;8(4):535–545. doi: 10.1016/0092-8674(76)90222-1. [DOI] [PubMed] [Google Scholar]
  14. Khoury G., Gruss P., Dhar R., Lai C. J. Processing and expression of early SV40 mRNA: a role for RNA conformation in splicing. Cell. 1979 Sep;18(1):85–92. doi: 10.1016/0092-8674(79)90356-8. [DOI] [PubMed] [Google Scholar]
  15. Khoury G., Howley P., Brown M., Martin M. The detection and quantitation of SV40 nucleic acid sequences using single-stranded SV40 DNA probes. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 1):147–152. doi: 10.1101/sqb.1974.039.01.020. [DOI] [PubMed] [Google Scholar]
  16. Khoury G., May E. Regulation of early and late simian virus 40 transcription: overproduction of early viral RNA in the absence of a functional T-antigen. J Virol. 1977 Jul;23(1):167–176. doi: 10.1128/jvi.23.1.167-176.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kimura G. Genetic evidence for SV40 gene function in enhancement of replication of human adenovirus in simian cells. Nature. 1974 Apr 12;248(449):590–592. doi: 10.1038/248590a0. [DOI] [PubMed] [Google Scholar]
  18. Klessig D. F., Anderson C. W. Block to multiplication of adenovirus serotype 2 in monkey cells. J Virol. 1975 Dec;16(6):1650–1668. doi: 10.1128/jvi.16.6.1650-1668.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lai C. J., Goldman N. D., Khoury G. Functional similarity between the early antigens of simian virus 40 and human papovavirus BK. J Virol. 1979 Apr;30(1):141–147. doi: 10.1128/jvi.30.1.141-147.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Levine A. J., van der Vliet P. C., Rosenwirth B., Anderson C., Rabek J., Levinson A., Anderson S. Characterization of an adenovirus early protein required for viral DNA replication: a single strand specific DNA binding proteins. Mol Cell Biochem. 1976 Apr 28;11(2):79–95. doi: 10.1007/BF01792789. [DOI] [PubMed] [Google Scholar]
  21. Lindberg U., Persson T., Philipson L. Isolation and characterization of adenovirus messenger ribonucleic acid in productive infection. J Virol. 1972 Nov;10(5):909–919. doi: 10.1128/jvi.10.5.909-919.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McGuire P. M., Swart C., Hodge L. D. Adenovirus messenger RNA in mammalian cells: failure of polyribosome association in the absence of nuclear cleavage. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1578–1582. doi: 10.1073/pnas.69.6.1578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Price R., Penman S. Transcription of the adenovirus genome by an -amanitine-sensitive ribonucleic acid polymerase in HeLa cells. J Virol. 1972 Apr;9(4):621–626. doi: 10.1128/jvi.9.4.621-626.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. RABSON A. S., O'CONOR G. T., BEREZESKY I. K., PAUL F. J. ENHANCEMENT OF ADENOVIRUS GROWTH IN AFRICAN GREEN MONKEY KIDNEY CELL CULTURES BY SV40. Proc Soc Exp Biol Med. 1964 May;116:187–190. doi: 10.3181/00379727-116-29197. [DOI] [PubMed] [Google Scholar]
  25. Rapp F., Feldman L. A., Mandel M. Synthesis of virus deoxyribonucleic acid during abortive infection of simian cells by human adenoviruses. J Bacteriol. 1966 Oct;92(4):931–936. doi: 10.1128/jb.92.4.931-936.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Reed S. I., Ferguson J., Davis R. W., Stark G. R. T antigen binds to simian virus 40 DNA at the origin of replication. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1605–1609. doi: 10.1073/pnas.72.4.1605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Tegtmeyer P. Simian virus 40 deoxyribonucleic acid synthesis: the viral replicon. J Virol. 1972 Oct;10(4):591–598. doi: 10.1128/jvi.10.4.591-598.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tjian R., Fey G., Graessmann A. Biological activity of purified simian virus 40 T antigen proteins. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1279–1283. doi: 10.1073/pnas.75.3.1279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tjian R. The binding site on SV40 DNA for a T antigen-related protein. Cell. 1978 Jan;13(1):165–179. doi: 10.1016/0092-8674(78)90147-2. [DOI] [PubMed] [Google Scholar]
  31. White D. O., Scharff M. D., Maizel J. V., Jr The polypeptides of adenovirus. 3. Synthesis in infected cells. Virology. 1969 Jul;38(3):395–406. doi: 10.1016/0042-6822(69)90152-4. [DOI] [PubMed] [Google Scholar]
  32. van Roy F., Fiers W. Interference with simian virus 40 DNA replication by adenovirus type 2 during mixed infection of monkey cells. J Virol. 1978 Aug;27(2):275–287. doi: 10.1128/jvi.27.2.275-287.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]

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