Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1981 Feb;37(2):759–769. doi: 10.1128/jvi.37.2.759-769.1981

Adenovirus type 2 expresses fiber in monkey-human hybrids and reconstructed cells.

G A Zorn, C W Anderson
PMCID: PMC171064  PMID: 7218436

Abstract

Adenovirus type 2 protein expression was measured by indirect immunofluorescence in monkey-human hybrids and in cells reconstructed from monkey and human cell karyoplasts and cytoplasts. Monkey-human hybrid clones infected with adenovirus type 2 expressed fiber protein, whereas infected monkey cells alone did not. Hybrids constructed after the parental monkey cells were infected with adenovirus type 2 demonstrated that fiber synthesis in these cells could be rescued by fusion to uninfected human cells. Thus, human cells contain a dominant factor that acts in trans and overcomes the inability of monkey cells to synthesize fiber. Cells reconstructed from infected human karyoplasts and monkey cytoplasts expressed fiber, whereas cells reconstructed from infected monkey karyoplasts and human cytoplasts did not. These results are consistent with the hypothesis that the block to adenovirus replication in monkey cells involves a nuclear event that prevents the formation of functional mRNA for some late viral proteins including fiber polypeptide. Furthermore, they suggest that the translational apparatus of monkey cells is competent to translate functional fiber mRNA synthesized in human cells.

Full text

PDF
759

Images in this article

Selected References

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

  1. Anderson C. W., Lewis J. B., Atkins J. F., Gesteland R. F. Cell-free synthesis of adenovirus 2 proteins programmed by fractionated messenger RNA: a comparison of polypeptide products and messenger RNA lengths. Proc Natl Acad Sci U S A. 1974 Jul;71(7):2756–2760. doi: 10.1073/pnas.71.7.2756. [DOI] [PMC free article] [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., Wiese W. H., Reich P. R. Studies on the mechanism of enhancement of adenovirus 7 infection in African green monkey cells by simian virus 40: formation of adenovirus-specific RNA. Virology. 1968 Feb;34(2):373–376. doi: 10.1016/0042-6822(68)90253-5. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Boulanger P. A., Puvion F. Large-scale preparation of soluble adenovirus hexon, penton and fiber antigens in highly purified form. Eur J Biochem. 1973 Nov 1;39(1):37–42. doi: 10.1111/j.1432-1033.1973.tb03100.x. [DOI] [PubMed] [Google Scholar]
  6. Ege T., Hamberg H., Krondahl U., Ericsson J., Ringertz N. R. Characterization of minicells (nuclei) obtained by cytochalasin enucleation. Exp Cell Res. 1974 Aug;87(2):365–377. doi: 10.1016/0014-4827(74)90493-5. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Farber M. S., Baum S. G. Transcription of adenovirus RNA in permissive and nonpermissive infections. J Virol. 1978 Jul;27(1):136–148. doi: 10.1128/jvi.27.1.136-148.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Feldman L. A., Butel J. S., Rapp F. Interaction of a simian papovavirus and adenoviruses. I. Induction of adenovirus tumor antigen during abortive infection of simian cells. J Bacteriol. 1966 Feb;91(2):813–818. doi: 10.1128/jb.91.2.813-818.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fournier R. E., Ruddle F. H. Microcell-mediated transfer of murine chromosomes into mouse, Chinese hamster, and human somatic cells. Proc Natl Acad Sci U S A. 1977 Jan;74(1):319–323. doi: 10.1073/pnas.74.1.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fox R. I., Baum S. G. Synthesis of viral ribonucleic acid during restricted adenovirus infection. J Virol. 1972 Aug;10(2):220–227. doi: 10.1128/jvi.10.2.220-227.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Graessmann A., Graessmann M., Mueller C. Regulatory function of simian virus 40 DNA replication for late viral gene expression. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4831–4834. doi: 10.1073/pnas.74.11.4831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Graessmann M., Graessman A. "Early" simian-virus-40-specific RNA contains information for tumor antigen formation and chromatin replication. Proc Natl Acad Sci U S A. 1976 Feb;73(2):366–370. doi: 10.1073/pnas.73.2.366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grodzicker T., Anderson C., Sharp P. A., Sambrook J. Conditional lethal mutants of adenovirus 2-simian virus 40 hybrids. I. Host range mutants of Ad2+ND1. J Virol. 1974 Jun;13(6):1237–1244. doi: 10.1128/jvi.13.6.1237-1244.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grodzicker T., Lewis J. B., Anderson C. W. Conditional lethal mutants of adenovirus type 2-simian virus 40 hybrids. II. Ad2+ND1 host-range mutants that synthesize fragments of the Ad2+ND1 30K protein. J Virol. 1976 Aug;19(2):559–571. doi: 10.1128/jvi.19.2.559-571.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Jerkofsky M., Rapp F. Stimulation of adenovirus replication in simian cells in the absence of a helper virus by pretreatment of the cells with iododeoxyuridine. J Virol. 1975 Feb;15(2):253–258. doi: 10.1128/jvi.15.2.253-258.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Klessig D. F., Chow L. T. Incomplete splicing and deficient accumulation of the fiber messenger RNA in monkey cells infected by human adenovirus type 2. J Mol Biol. 1980 May 15;139(2):221–242. doi: 10.1016/0022-2836(80)90306-x. [DOI] [PubMed] [Google Scholar]
  21. Klessig D. F., Grodzicker T. Mutations that allow human Ad2 and Ad5 to express late genes in monkey cells map in the viral gene encoding the 72K DNA binding protein. Cell. 1979 Aug;17(4):957–966. doi: 10.1016/0092-8674(79)90335-0. [DOI] [PubMed] [Google Scholar]
  22. Klessig D. F., Hassell J. A. Characterization of a variant of human adenovirus type 2 which multiples efficiently in simian cells. J Virol. 1978 Dec;28(3):945–956. doi: 10.1128/jvi.28.3.945-956.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Klessig D. F. Isolation of a variant of human adenovirus serotype 2 that multiplies efficiently on monkey cells. J Virol. 1977 Mar;21(3):1243–1246. doi: 10.1128/jvi.21.3.1243-1246.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lewis A. M., Jr, Levin M. J., Wiese W. H., Crumpacker C. S., Henry P. H. A nondefective (competent) adenovirus-SV40 hybrid isolated from the AD.2-SV40 hybrid population. Proc Natl Acad Sci U S A. 1969 Aug;63(4):1128–1135. doi: 10.1073/pnas.63.4.1128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lewis A. M., Jr, Rowe W. P. Studies on nondefective adenovirus-simian virus 40 hybrid viruses. I. A newly characterized simian virus 40 antigen induced by the Ad2+ND 1 virus. J Virol. 1971 Feb;7(2):189–197. doi: 10.1128/jvi.7.2.189-197.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lucas J. J., Ginsberg H. S. Transcription and transport of virus-specific ribonucleic acids in African green monkey kidney cells abortively infected with type 2 adenovirus. J Virol. 1972 Dec;10(6):1109–1117. doi: 10.1128/jvi.10.6.1109-1117.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lucas J. J., Kates J. R. The construction of viable nuclear-cytoplasmic hybrid cells by nuclear transplantation. Cell. 1976 Mar;7(3):397–405. doi: 10.1016/0092-8674(76)90169-0. [DOI] [PubMed] [Google Scholar]
  28. Nakajima K., Ishitsuka H., Oda K. An SV40-induced initiation factor for protein synthesis concerned with the regulation of permissiveness. Nature. 1974 Dec 20;252(5485):649–653. doi: 10.1038/252649a0. [DOI] [PubMed] [Google Scholar]
  29. Nakajima K., Oda K. The alteration of ribosomes for mRNA selection concerned with adenovirus growth in SV40-infected simian cells. Virology. 1975 Sep;67(1):85–93. doi: 10.1016/0042-6822(75)90406-7. [DOI] [PubMed] [Google Scholar]
  30. PEREIRA H. G., HUEBNER R. J., GINSBERG H. S., VAN DER VEEN J. A SHORT DESCRIPTION OF THE ADENOVIRUS GROUP. Virology. 1963 Aug;20:613–620. doi: 10.1016/0042-6822(63)90286-1. [DOI] [PubMed] [Google Scholar]
  31. Pettersson U., Philipson L., Höglund S. Structural proteins of adenoviruses. I. Purification and characterization of the adenovirus type 2 hexon antigen. Virology. 1967 Dec;33(4):575–590. doi: 10.1016/0042-6822(67)90057-8. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Reich P. R., Baum S. G., Rose J. A., Rowe W. P., Weissman S. M. Nucleic acid homology studies of adenovirus type 7-SV40 interactions. Proc Natl Acad Sci U S A. 1966 Feb;55(2):336–341. doi: 10.1073/pnas.55.2.336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Robb J. A., Martin R. G. Genetic analysis of simian virus 40. 3. Characterization of a temperature-sensitive mutant blocked at an early stage of productive infection in monkey cells. J Virol. 1972 Jun;9(6):956–968. doi: 10.1128/jvi.9.6.956-968.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ross J., Ikawa Y., Leder P. Globin messenger-RNA induction during erythroid differentiation of cultured leukemia cells. Proc Natl Acad Sci U S A. 1972 Dec;69(12):3620–3623. doi: 10.1073/pnas.69.12.3620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Staal S. P., Rowe W. P. Enhancement of adenovirus infection in WI-38 and AGMK cells by pretreatment of cells with 5-iododeoxyuridine. Virology. 1975 Apr;64(2):513–519. doi: 10.1016/0042-6822(75)90128-2. [DOI] [PubMed] [Google Scholar]
  37. Thomas D. C., Green M. Biochemical studies on adenovirus multiplication. XV. Transcription of the adenovirus type II genome during productive infection. Virology. 1969 Oct;39(2):205–210. doi: 10.1016/0042-6822(69)90040-3. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Williams J. F. Enhancement of adenovirus plaque formation on HeLa cells by magnesium chloride. J Gen Virol. 1970 Dec;9(3):251–255. doi: 10.1099/0022-1317-9-3-251. [DOI] [PubMed] [Google Scholar]
  40. Zorn G. A., Lucas J. J., Kates J. R. Purification and characterization of regenerating mouse L929 karyoplasts. Cell. 1979 Nov;18(3):659–672. doi: 10.1016/0092-8674(79)90121-1. [DOI] [PubMed] [Google Scholar]

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

RESOURCES