Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1968 Mar;2(3):224–237. doi: 10.1128/jvi.2.3.224-237.1968

Production of Virus by Mammalian Cells Transformed by Rous Sarcoma and Murine Sarcoma Viruses

Artrice F Valentine 1, John P Bader 1
PMCID: PMC375605  PMID: 4316021

Abstract

Cultured cells of mammalian tumors induced by ribonucleic acid (RNA)-containing oncogenic viruses were examined for production of virus. The cell lines were established from tumors induced in rats and hamsters with either Rous sarcoma virus (Schmidt-Ruppin or Bryan strains) or murine sarcoma virus (Moloney strain). When culture fluids from each of the cell lines were examined for transforming activity or production of progeny virus, none of the cell lines was found to be infectious. However, electron microscopic examination of the various cell lines revealed the presence of particles in the rat cells transformed by either Rous sarcoma virus or murine sarcoma virus. These particles, morphologically similar to those associated with murine leukemias, were found both in the extracellular fluid concentrates and in whole-cell preparations. In the latter, they were seen budding from the cell membranes or lying in the intercellular spaces. No viruslike particles were seen in preparations from hamster tumors. Exposure of the rat cells to 3H-uridine resulted in the appearance of labeled particles with densities in sucrose gradients typical of virus (1.16 g/ml.). RNA of high molecular weight was extracted from these particles, and double-labeling experiments showed that this RNA sedimented at the same rate as RNA extracted from Rous sarcoma virus. None of the hamster cell lines gave radioactive peaks in the virus density range, and no extractable high molecular weight RNA was found. These studies suggest that the murine sarcoma virus produces an infection analogous to certain “defective” strains of Rous sarcoma virus, in that particles produced by infected cells have a low efficiency of infection. The control of the host cell over the production and properties of the RNA-containing tumorigenic viruses is discussed.

Full text

PDF
224

Images in this article

Selected References

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

  1. AHLSTROM C. G., FORSBY N. Sarcomas in hamsters after injection with Rous chicken tumor material. J Exp Med. 1962 Apr 1;115:839–852. doi: 10.1084/jem.115.4.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BADER J. P. Production of interferon by chick embryo cells exposed to Rous sarcoma virus. Virology. 1962 Apr;16:436–443. doi: 10.1016/0042-6822(62)90224-6. [DOI] [PubMed] [Google Scholar]
  3. Bader J. P. Metabolic requirements for infection by Rous sarcoma virus. II. The participation of cellular DNA. Virology. 1966 Jul;29(3):452–461. doi: 10.1016/0042-6822(66)90221-2. [DOI] [PubMed] [Google Scholar]
  4. Courington D., Vogt P. K. Electron microscopy of chick fibroblasts infected by defective rous sarcoma virus and its helper. J Virol. 1967 Apr;1(2):400–414. doi: 10.1128/jvi.1.2.400-414.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. DALTON A. J., LAW L. W., MOLONEY J. B., MANAKER R. A. An electron microscopic study of a series of murine lymphoid neoplasms. J Natl Cancer Inst. 1961 Oct;27:747–791. [PubMed] [Google Scholar]
  6. DALTON A. J. Micromorphology of murine tumor viruses and of affected cells. Fed Proc. 1962 Nov-Dec;21:936–941. [PubMed] [Google Scholar]
  7. Dalton A. J. An electron microscopic study of a virus-induced murine sarcoma (Moloney). Natl Cancer Inst Monogr. 1966 Sep;22:143–168. [PubMed] [Google Scholar]
  8. Dougherty R. M., Di Stefano H. S. Virus particles associated with "nonproducer" Rous sarcoma cells. Virology. 1965 Nov;27(3):351–359. doi: 10.1016/0042-6822(65)90115-7. [DOI] [PubMed] [Google Scholar]
  9. Duesberg P. H., Robinson W. S. Nucleic acid and proteins isolated from the Rauscher mouse leukemia virus (MLV). Proc Natl Acad Sci U S A. 1966 Jan;55(1):219–227. doi: 10.1073/pnas.55.1.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. HANAFUSA H., HANAFUSA T., RUBIN H. The defectiveness of Rous sarcoma virus. Proc Natl Acad Sci U S A. 1963 Apr;49:572–580. doi: 10.1073/pnas.49.4.572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Huebner R. J., Hartley J. W., Rowe W. P., Lane W. T., Capps W. I. Rescue of the defective genome of Moloney sarcoma virus from a noninfectious hamster tumor and the production of pseudotype sarcoma viruses with various murine leukemia viruses. Proc Natl Acad Sci U S A. 1966 Oct;56(4):1164–1169. doi: 10.1073/pnas.56.4.1164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. MOLLENHAUER H. H. PLASTIC EMBEDDING MIXTURES FOR USE IN ELECTRON MICROSCOPY. Stain Technol. 1964 Mar;39:111–114. [PubMed] [Google Scholar]
  13. Robinson W. S., Pitkanen A., Rubin H. The nucleic acid of the Bryan strain of Rous sarcoma virus: purification of the virus and isolation of the nucleic acid. Proc Natl Acad Sci U S A. 1965 Jul;54(1):137–144. doi: 10.1073/pnas.54.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Robinson W. S., Robinson H. L., Duesberg P. H. Tumor virus RNA's. Proc Natl Acad Sci U S A. 1967 Sep;58(3):825–834. doi: 10.1073/pnas.58.3.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. SABATINI D. D., BENSCH K., BARRNETT R. J. Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J Cell Biol. 1963 Apr;17:19–58. doi: 10.1083/jcb.17.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. SVOBODA J., CHYLE P., SIMKOVIC D., HILGERT I. Demonstration of the absence of infectious Rous virus in rat tumour XC, whose structurally intact cells produce Rous sarcoma when transferred to chicks. Folia Biol (Praha) 1963 Apr;9:77–81. [PubMed] [Google Scholar]
  17. SVOBODA J., KLEMENT V. FORMATION OF DELAYED TUMOURS IN HAMSTERS INOCULATED WITH ROUS VIRUS AFTER BIRTH AND FINDING OF INFECTIOUS ROUS VIRUS IN INDUCED TUMOUR P1. Folia Biol (Praha) 1963;9:403–411. [PubMed] [Google Scholar]
  18. Sarma P. S., Vass W., Huebner R. J. Evidence for the in vitro transfer of defective Rous sarcoma virus genome from hamster tumor cells to chick cells. Proc Natl Acad Sci U S A. 1966 Jun;55(6):1435–1442. doi: 10.1073/pnas.55.6.1435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Simkovic D., Svoboda J., Valentová N. Induction of formation and release of infectious Rous virus by cells of rat tumour XC in vitro. Folia Biol (Praha) 1965;11(5):350–358. [PubMed] [Google Scholar]
  20. Simons P. J., Bassin R. H., Harvey J. J. Transformation of hamster embryo cells in vitro by Murine Sarcoma Virus (Harvey). Proc Soc Exp Biol Med. 1967 Aug-Sep;125(4):1242–1246. doi: 10.3181/00379727-125-32326. [DOI] [PubMed] [Google Scholar]

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

RESOURCES