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. 1986 Sep;59(3):655–659. doi: 10.1128/jvi.59.3.655-659.1986

Ability of a T-antigen transport-defective mutant of simian virus 40 to immortalize primary cells and to complement polyomavirus middle T in tumorigenesis.

J Vass-Marengo, A Ratiarson, C Asselin, M Bastin
PMCID: PMC253229  PMID: 3016328

Abstract

The oncogenic potential of polyomavirus in newborn rats could not be expressed by a genome encoding only the middle T antigen but required the presence of one of the other two viral early genes, small T or large T. The tumorigenicity defect could also be complemented by other viral or cellular genes that are known to be implicated in immortalization and establishment functions. The simian virus 40(cT)-3 mutant (R. E. Lanford and J. S. Butel, Cell 37:801-813, 1984), which fails to localize to the nucleus, has the capacity to complement polyomavirus middle T in tumorigenesis and to immortalize primary rat embryo fibroblasts when it was cotransfected in the presence of pSV2-neo. Our data suggested that under the conditions of DNA-mediated tumor induction and cotransfection with a dominant selection marker, the cellular alterations achieved by nonnuclear oncogenes such as polyomavirus small T and simian virus 40(cT)-3 were sufficient to complement polyomavirus middle T in transformation and tumorigenesis.

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Selected References

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

  1. Asselin C., Bastin M. Sequences from polyomavirus and simian virus 40 large T genes capable of immortalizing primary rat embryo fibroblasts. J Virol. 1985 Dec;56(3):958–968. doi: 10.1128/jvi.56.3.958-968.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Asselin C., Gelinas C., Bastin M. Role of the three polyoma virus early proteins in tumorigenesis. Mol Cell Biol. 1983 Aug;3(8):1451–1459. doi: 10.1128/mcb.3.8.1451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Asselin C., Gélinas C., Branton P. E., Bastin M. Polyoma middle T antigen requires cooperation from another gene to express the malignant phenotype in vivo. Mol Cell Biol. 1984 Apr;4(4):755–760. doi: 10.1128/mcb.4.4.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Asselin C., Vass-Marengo J., Bastin M. Mutation in the polyomavirus genome that activates the properties of large T associated with neoplastic transformation. J Virol. 1986 Jan;57(1):165–172. doi: 10.1128/jvi.57.1.165-172.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bouchard L., Gelinas C., Asselin C., Bastin M. Tumorigenic activity of polyoma virus and SV40 DNAs in newborn rodents. Virology. 1984 May;135(1):53–64. doi: 10.1016/0042-6822(84)90116-8. [DOI] [PubMed] [Google Scholar]
  6. Colby W. W., Shenk T. Fragments of the simian virus 40 transforming gene facilitate transformation of rat embryo cells. Proc Natl Acad Sci U S A. 1982 Sep;79(17):5189–5193. doi: 10.1073/pnas.79.17.5189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eliyahu D., Michalovitz D., Oren M. Overproduction of p53 antigen makes established cells highly tumorigenic. Nature. 1985 Jul 11;316(6024):158–160. doi: 10.1038/316158a0. [DOI] [PubMed] [Google Scholar]
  8. Fischer-Fantuzzi L., Vesco C. Deletion of 43 amino acids in the NH2-terminal half of the large tumor antigen of simian virus 40 results in a non-karyophilic protein capable of transforming established cells. Proc Natl Acad Sci U S A. 1985 Apr;82(7):1891–1895. doi: 10.1073/pnas.82.7.1891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Harlow E., Crawford L. V., Pim D. C., Williamson N. M. Monoclonal antibodies specific for simian virus 40 tumor antigens. J Virol. 1981 Sep;39(3):861–869. doi: 10.1128/jvi.39.3.861-869.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Houweling A., van den Elsen P. J., van der Eb A. J. Partial transformation of primary rat cells by the leftmost 4.5% fragment of adenovirus 5 DNA. Virology. 1980 Sep;105(2):537–550. doi: 10.1016/0042-6822(80)90054-9. [DOI] [PubMed] [Google Scholar]
  11. Ito Y., Brocklehurst J. R., Dulbecco R. Virus-specific proteins in the plasma membrane of cells lytically infected or transformed by pol-oma virus. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4666–4670. doi: 10.1073/pnas.74.10.4666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jenuwein T., Müller D., Curran T., Müller R. Extended life span and tumorigenicity of nonestablished mouse connective tissue cells transformed by the fos oncogene of FBR-MuSV. Cell. 1985 Jun;41(2):629–637. doi: 10.1016/s0092-8674(85)80035-0. [DOI] [PubMed] [Google Scholar]
  13. Land H., Parada L. F., Weinberg R. A. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature. 1983 Aug 18;304(5927):596–602. doi: 10.1038/304596a0. [DOI] [PubMed] [Google Scholar]
  14. Lane D. P., Crawford L. V. T antigen is bound to a host protein in SV40-transformed cells. Nature. 1979 Mar 15;278(5701):261–263. doi: 10.1038/278261a0. [DOI] [PubMed] [Google Scholar]
  15. Lanford R. E., Butel J. S. Construction and characterization of an SV40 mutant defective in nuclear transport of T antigen. Cell. 1984 Jul;37(3):801–813. doi: 10.1016/0092-8674(84)90415-x. [DOI] [PubMed] [Google Scholar]
  16. Lanford R. E., Wong C., Butel J. S. Differential ability of a T-antigen transport-defective mutant of simian virus 40 to transform primary and established rodent cells. Mol Cell Biol. 1985 May;5(5):1043–1050. doi: 10.1128/mcb.5.5.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Linzer D. I., Levine A. J. Characterization of a 54K dalton cellular SV40 tumor antigen present in SV40-transformed cells and uninfected embryonal carcinoma cells. Cell. 1979 May;17(1):43–52. doi: 10.1016/0092-8674(79)90293-9. [DOI] [PubMed] [Google Scholar]
  18. Mougneau E., Lemieux L., Rassoulzadegan M., Cuzin F. Biological activities of v-myc and rearranged c-myc oncogenes in rat fibroblast cells in culture. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5758–5762. doi: 10.1073/pnas.81.18.5758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rassoulzadegan M., Cowie A., Carr A., Glaichenhaus N., Kamen R., Cuzin F. The roles of individual polyoma virus early proteins in oncogenic transformation. Nature. 1982 Dec 23;300(5894):713–718. doi: 10.1038/300713a0. [DOI] [PubMed] [Google Scholar]
  20. Rassoulzadegan M., Naghashfar Z., Cowie A., Carr A., Grisoni M., Kamen R., Cuzin F. Expression of the large T protein of polyoma virus promotes the establishment in culture of "normal" rodent fibroblast cell lines. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4354–4358. doi: 10.1073/pnas.80.14.4354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ruley H. E. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature. 1983 Aug 18;304(5927):602–606. doi: 10.1038/304602a0. [DOI] [PubMed] [Google Scholar]
  22. Sleigh M. J., Topp W. C., Hanich R., Sambrook J. F. Mutants of SV40 with an altered small t protein are reduced in their ability to transform cells. Cell. 1978 May;14(1):79–88. doi: 10.1016/0092-8674(78)90303-3. [DOI] [PubMed] [Google Scholar]
  23. Southern P. J., Berg P. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter. J Mol Appl Genet. 1982;1(4):327–341. [PubMed] [Google Scholar]
  24. Spandidos D. A., Wilkie N. M. Malignant transformation of early passage rodent cells by a single mutated human oncogene. Nature. 1984 Aug 9;310(5977):469–475. doi: 10.1038/310469a0. [DOI] [PubMed] [Google Scholar]
  25. Weinberg R. A. The action of oncogenes in the cytoplasm and nucleus. Science. 1985 Nov 15;230(4727):770–776. doi: 10.1126/science.2997917. [DOI] [PubMed] [Google Scholar]

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