Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1981 Aug;39(2):331–340. doi: 10.1128/jvi.39.2.331-340.1981

Alterations to controls of cellular DNA synthesis by adenovirus infection.

A W Braithwaite, J D Murray, A J Bellett
PMCID: PMC171341  PMID: 6268825

Abstract

Human adenovirus type 5 and temperature-sensitive mutants ts36, ts37, and ts125 induced cellular DNA synthesis in quiescent rodent cells at both permissive and nonpermissive temperatures. Cellular DNA synthesis induced by adenovirus type 5 or by serum required protein synthesis for both initiation and continuation, whereas viral DNA synthesis was not dependent upon continued protein synthesis once it was initiated. Both cellular and viral DNA replication was induced in adenovirus type 5-infected cells in the presence of dibutyryl cyclic AMP at concentrations which inhibited induction by serum which suggested that some of the controls of DNA synthesis in serum-treated and virus-infected cells are different. After adenovirus infection of quiescent cells, there was a decrease in the number of cells with G1 DNA content and an increase in cells with G2 diploid and greater DNA contents. Thus, adenovirus type 5 induces a complete round of cellular DNA replication, but in some cells, it induces a second round without completion of a normal mitosis. These results suggest that adenovirus type 5 is able to alter cell growth cycle controls in a way which may be related to its ability to transform cells.

Full text

PDF
331

Selected References

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

  1. Bellett A. J., Younghusband H. B. Spontaneous, mutagen-induced and adenovirus-induced anchorage independent tumorigenic variants of mouse cells. J Cell Physiol. 1979 Oct;101(1):33–47. doi: 10.1002/jcp.1041010106. [DOI] [PubMed] [Google Scholar]
  2. Butel J. S., Soule H. R. Role of the simian virus 40 gene A product in regulation of DNA synthesis in transformed cells. J Virol. 1978 Jun;26(3):584–594. doi: 10.1128/jvi.26.3.584-594.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Fluck M. M., Benjamin T. L. Comparisons of two early gene functions essential for transformation in polyoma virus and SV-40. Virology. 1979 Jul 15;96(1):205–228. doi: 10.1016/0042-6822(79)90185-5. [DOI] [PubMed] [Google Scholar]
  4. Gallimore P. H. Interactions of adenovirus type 2 with rat embryo cells. Permissiveness, transformation and in vitro characteristics of adenovirus transformed rat embryo cells. J Gen Virol. 1974 Nov;25(2):263–273. doi: 10.1099/0022-1317-25-2-263. [DOI] [PubMed] [Google Scholar]
  5. Galos R. S., Williams J., Binger M. H., Flint S. J. Location of additional early gene sequences in the adenoviral chromosome. Cell. 1979 Aug;17(4):945–956. doi: 10.1016/0092-8674(79)90334-9. [DOI] [PubMed] [Google Scholar]
  6. Ginsberg H. S., Ensinger M. J., Kauffman R. S., Mayer A. J., Lundholm U. Cell transformation: a study of regulation with types 5 and 12 adenovirus temperature-sensitive mutants. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 1):419–426. doi: 10.1101/sqb.1974.039.01.054. [DOI] [PubMed] [Google Scholar]
  7. Gould A. R. Combined microspectrophotometry and automated quantitative autoradiography applied to the analysis of the plant cell cycle. J Cell Sci. 1979 Oct;39:235–245. doi: 10.1242/jcs.39.1.235. [DOI] [PubMed] [Google Scholar]
  8. Graham F. L., Abrahams P. J., Mulder C., Heijneker H. L., Warnaar S. O., De Vries F. A., Fiers W., Van Der Eb A. J. Studies on in vitro transformation by DNA and DNA fragments of human adenoviruses and simian virus 40. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 1):637–650. doi: 10.1101/sqb.1974.039.01.077. [DOI] [PubMed] [Google Scholar]
  9. Graham F. L., Harrison T., Williams J. Defective transforming capacity of adenovirus type 5 host-range mutants. Virology. 1978 May 1;86(1):10–21. doi: 10.1016/0042-6822(78)90003-x. [DOI] [PubMed] [Google Scholar]
  10. Graham F. L., Smiley J., Russell W. C., Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol. 1977 Jul;36(1):59–74. doi: 10.1099/0022-1317-36-1-59. [DOI] [PubMed] [Google Scholar]
  11. Harrison T., Graham F., Williams J. Host-range mutants of adenovirus type 5 defective for growth in HeLa cells. Virology. 1977 Mar;77(1):319–329. doi: 10.1016/0042-6822(77)90428-7. [DOI] [PubMed] [Google Scholar]
  12. Horwitz M. S., Brayton C., Baum S. G. Synthesis of type 2 adenovirus DNA in the presence of cycloheximide. J Virol. 1973 Apr;11(4):544–551. doi: 10.1128/jvi.11.4.544-551.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ide T., Ohta T., Shinohara Y., Ishibashi S. Persisting DNA synthesis in SV40-transformed cells in the presence of cycloheximide. Nature. 1979 Mar 15;278(5701):264–265. doi: 10.1038/278264a0. [DOI] [PubMed] [Google Scholar]
  14. Jones N., Shenk T. Isolation of deletion and substitution mutants of adenovirus type 5. Cell. 1978 Jan;13(1):181–188. doi: 10.1016/0092-8674(78)90148-4. [DOI] [PubMed] [Google Scholar]
  15. Kobayashi N., Kaji A. Induction of DNA synthesis in terminally differentiated myotubes by the activation of the src gene of Rous sarcoma virus. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5501–5505. doi: 10.1073/pnas.75.11.5501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lehman J. M., Defendi V. Changes in deoxyribonucleic acid synthesis regulation in Chinese hamster cells infected with simian virus 40. J Virol. 1970 Dec;6(6):738–749. doi: 10.1128/jvi.6.6.738-749.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. PHILIPSON L. Adenovirus assay by the fluorescent cell-counting procedure. Virology. 1961 Nov;15:263–268. doi: 10.1016/0042-6822(61)90357-9. [DOI] [PubMed] [Google Scholar]
  18. Pardee A. B. A restriction point for control of normal animal cell proliferation. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1286–1290. doi: 10.1073/pnas.71.4.1286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Shimojo H., Yamashita T. Induction of DNA synthesis by adenoviruses in contact-inhibited hamster cells. Virology. 1968 Nov;36(3):422–433. doi: 10.1016/0042-6822(68)90167-0. [DOI] [PubMed] [Google Scholar]
  20. Stillman B. W., Lewis J. B., Chow L. T., Mathews M. B., Smart J. E. Identification of the gene and mRNA for the adenovirus terminal protein precursor. Cell. 1981 Feb;23(2):497–508. doi: 10.1016/0092-8674(81)90145-8. [DOI] [PubMed] [Google Scholar]
  21. Strohl W. A. The response of BHK21 cells to infection with type 12 adenovirus. II. Relationship of virus-stimulated DNA synthesis to other viral functions. Virology. 1969 Dec;39(4):653–665. doi: 10.1016/0042-6822(69)90004-x. [DOI] [PubMed] [Google Scholar]
  22. Taylor I. W. A rapid single step staining technique for DNA analysis by flow microfluorimetry. J Histochem Cytochem. 1980 Sep;28(9):1021–1024. doi: 10.1177/28.9.6157714. [DOI] [PubMed] [Google Scholar]
  23. Todaro G. J., Green H. Cell growth and the initiation of transformation by SV40. Proc Natl Acad Sci U S A. 1966 Feb;55(2):302–308. doi: 10.1073/pnas.55.2.302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Vliet P. C., Sussenbach J. S. An adenovirus type 5 gene function required for initiation of viral DNA replication. Virology. 1975 Oct;67(2):415–426. doi: 10.1016/0042-6822(75)90443-2. [DOI] [PubMed] [Google Scholar]
  25. Williams J. F., Gharpure M., Ustacelebi S., McDonald S. Isolation of temperature-sensitive mutants of adenovirus type 5. J Gen Virol. 1971 May;11(2):95–101. doi: 10.1099/0022-1317-11-2-95. [DOI] [PubMed] [Google Scholar]
  26. Willians J. F., Young C. S., Austin P. E. Genetic analysis of human adenovirus type 5 in permissive and nonpermissive cells. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 1):427–437. doi: 10.1101/sqb.1974.039.01.055. [DOI] [PubMed] [Google Scholar]
  27. Younghusband H. B., Bellett A. J. Mature form of the deoxyribonucleic acid from chick embryo lethal orphan virus. J Virol. 1971 Sep;8(3):265–274. doi: 10.1128/jvi.8.3.265-274.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Younghusband H. B., Tyndall C., Bellett A. J. Replication and interaction of virus DNA and cellular DNA in mouse cells infected by a human adenovirus. J Gen Virol. 1979 Nov;45(2):455–467. doi: 10.1099/0022-1317-45-2-455. [DOI] [PubMed] [Google Scholar]
  29. Zimmerman J. E., Jr, Raska K., Jr Inhibition of adenovirus type 12 induced DNA synthesis in G1-arrested BHK21 cells by dibutyryl adenosine cyclic 3':5'-monophosphate. Nat New Biol. 1972 Oct 4;239(92):145–147. doi: 10.1038/newbio239145a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES