1887

Abstract

The regulatory region of natural isolates of simian virus 40 (SV40) is different from that of laboratory-adapted strains of the virus. The latter have a nucleotide sequence duplication within the enhancer region which varies slightly with each strain, whereas the duplication is lacking in fresh isolates of SV40, which contain an ‘archetypal’ regulatory region. Many isolates also display nucleotide differences in the DNA encoding the carboxy terminus of large tumour antigen (T-ag). To determine whether genetic changes in these two regions of the SV40 genome were detectable during laboratory adaptation and long-term passage, low-passage virus stocks of two laboratory strains which had detailed passage histories spanning more than 25 years (Baylor strain and VA45-54) were analysed using PCR, cloning and sequencing assays. Both laboratory and archetypal regulatory regions were present in low-passage stocks. Following duplication in the regulatory region, no additional changes were detectable. The variable region at the T-ag carboxy terminus did not undergo any change with tissue culture passage and may serve as a useful site for taxonomic classification of different strains of SV40. Cloned genomes containing single or duplicated enhancers derived from both SV40 strains were viable in CV-1 cells. Attempts to induce regulatory region duplications by 14 serial passages of SV40 archetypal strains in monkey cells were not successful. The results are compatible with tissue culture adaptation of SV40, reflecting either selection of a rare variant pre-existing in the original sample or generation of a rare regulatory region duplication in infected cells.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-78-7-1697
1997-07-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/78/7/9225047.html?itemId=/content/journal/jgv/10.1099/0022-1317-78-7-1697&mimeType=html&fmt=ahah

References

  1. Cole C. N., Stacy T. P. 1987; Biological properties of simian virus 40 host range mutants lacking the COOH-terminus of large T antigen. Virology 161:170–180
    [Google Scholar]
  2. Cole C. N., Crawford L. V., Berg P. 1979; Simian virus 40 mutants with deletions at the 3ʹ end of the early region are defective in adenovirus helper function. Journal of Virology 30:683–691
    [Google Scholar]
  3. Diamandopoulos G. T., Enders J. F. 1965; Studies on transformation of Syrian hamster cells by simian virus 40 (SV40): acquisition of oncogenicity by virus-exposed cells apparently unassociated with the viral genome. Proceedings of the National Academy of Sciences USA: 541092–1099
    [Google Scholar]
  4. Fiers W., Contreras R., Haegeman G., Rogiers R., Van de Voorde A., VanHeuverswyn H., Van Herreweghe J., Volckaert G., Ysebaert M. 1978; Complete nucleotide sequence of SV40 DNA. Nature 273:113–120
    [Google Scholar]
  5. Frisque R. J., Bream G. L., Canella M. T. 1984; Human polyomavirus JC virus genome. Journal of Virology 51:458–469
    [Google Scholar]
  6. Ghosh P. K., Piatak M., Mertz J. E., Weissman S. M., Lebowitz P. 1982; Altered utilization of splice sites and 5ʹ termini in late RNAs produced by leader region mutants of simian virus 40. Journal of Virology 44:610–624
    [Google Scholar]
  7. Girardi A. J. 1965; Prevention of SV40 virus oncogenesis in hamsters. I. Tumor resistance induced by human cells transformed by SV40. Proceedings of the National Academy of Sciences USA: 54445–451
    [Google Scholar]
  8. Girardi A. J., Sweet B. H., Slotnick V. B., Hilleman M. R. 1962; Development of tumors in hamsters inoculated in the neonatal period with vacuolating virus, SV40. Proceedings of the Society for Experimental Biology and Medicine 109:649–660
    [Google Scholar]
  9. Hara K., Oya Y., Kinoshita H., Taguchi F., Yogo Y. 1986; Sequence reiteration required for the efficient growth of BK virus. Journal of General Virology 67:2555–2559
    [Google Scholar]
  10. Hay R. T., Hendrickson E. A., DePamphilis M. L. 1984; Sequence specificity for the initiation ofRNA-primed SV40 DNA synthesis in vivo. Journal of Molecular Biology 175:131–157
    [Google Scholar]
  11. Herr W., Gluzman Y. 1985; Duplications of a mutated simian virus 40 enhancer restore its activity. Nature 313:711–714
    [Google Scholar]
  12. Hirt B. 1967; Selective extraction of polyoma DNA from infected mouse cell cultures. Journal of Molecular Biology 26:365–369
    [Google Scholar]
  13. Illyinskii P. O., Daniel M. D., Horvath C. J., Desrosiers R. C. 1992; Genetic analysis of simian virus 40 from brains and kidneys of macaque monkeys. Journal of Virology 66:6353–6360
    [Google Scholar]
  14. Kelley T. J., Lewis A. M. 1973; Use of nondefective adenovirus- simian virus 40 hybrids for mapping the simian virus 40 genome. Journal of Virology 12:643–652
    [Google Scholar]
  15. Krieg P., Scherer G. 1984; Cloning of SV40 genomes from human brain tumors. Virology 138:336–340
    [Google Scholar]
  16. Lanford R. E., Butel J. S. 1984; Construction and characterization of an SV40 mutant defective in nuclear transport of T antigen. Cell 37:801–813
    [Google Scholar]
  17. Lanford R. E., Jacob J. R., Butel J. S. 1986; Genomic organization of the simian virus 40-adenovirus 7 hybrid virus, PARA(cT), that encodes a nuclear transport defective simian virus 40 T antigen. Virology 155:271–276
    [Google Scholar]
  18. Lednicky J., Folk W. R. 1992; Two synthetic Spl-binding sites functionally substitute for the 21-base-pair repeat region to activate simian virus 40 growth in CV-1 cells. Journal of Virology 66:6379–6390
    [Google Scholar]
  19. Lednicky J. A., Garcea R. L., Bergsagel D. J., Butel J. S. 1995a; Natural simian virus 40 strains are present in human choroid plexus and ependymoma tumors. Virology 212:710–717
    [Google Scholar]
  20. Lednicky J. A., Wong C., Butel J. S. 1995b; Artificial modification of the viral regulatory region improves tissue culture growth of SV40 strain 776. Virus Research 35:143–153
    [Google Scholar]
  21. Lewis E. D., Chen S., Kumar A., Blanck G., Pollack R. E., Manley J. L. 1983; A frameshift mutation affecting the carboxyl terminus of the simian virus 40 large tumor antigen results in a replication- and transformation-defective virus. Proceedings of the National Academy of Sciences USA: 807065–7069
    [Google Scholar]
  22. Loeber G., Dörries K. 1988; DNA rearrangements in organ-specific variants of polyomavirus JC strain GS. Journal of Virology 62:1730–1735
    [Google Scholar]
  23. Markowitz R.-B., Eaton B. A., Kubik M. F., Latorra D., McGregor J. A., Dynan W. S. 1991; BK virus and JC virus shed during pregnancy have predominantly archetypal regulatory regions. Journal of Virology 65:4515–4519
    [Google Scholar]
  24. Martin J. D. 1989; Regulatory sequences of SV40 variants isolated from patients with progressive multifocal leukoencephalopathy. Virus Research 14:85–94
    [Google Scholar]
  25. Martin J. D., Li P. 1991; Comparison of regulatory sequences and enhancer activities of SV40 variants isolated from patients with neurological diseases. Virus Research 19:163–172
    [Google Scholar]
  26. Mertz J. E., Berg P. 1974; Defective simian virus 40 genomes: isolation and growth of individual clones. Virology 62:112–124
    [Google Scholar]
  27. Noonan C. A., Butel J. S. 1978; Temperature-sensitive mutants of simian virus 40. Intervirology 10:181–195
    [Google Scholar]
  28. O’Neill F. J., Carroll D. 1981; Amplification of papovavirus defectives during serial low multiplicity infections. Virology 112:800–803
    [Google Scholar]
  29. Pipas J. M. 1985; Mutations near the carboxyl terminus of the simian virus 40 large tumor antigen alter viral host range. Journal of Virology 54:569–575
    [Google Scholar]
  30. Rabson A. S., O’Conner G. T., Berezesky I. K., Paul F. J. 1964; Enhancement of adenovirus growth in African green monkey kidney cell cultures by SV40. Proceedings of the Society for Experimental Biology and Medicine 116:187–190
    [Google Scholar]
  31. Reddy V. B., Thimmappaya B., Dhar R., Subramanian K. N., Zain B. S., Pan J., Ghosh P. K., Celma M. L., Weissman S. M. 1978; The genome of simian virus 40. Science 200:494–502
    [Google Scholar]
  32. Rochford R., Moreno J. P., Peake M. L., Villareal L. P. 1992; Enhancer dependence of polyomavirus persistence in mouse kidneys. Journal of Virology 66:3287–3297
    [Google Scholar]
  33. Rubinstein R., Schoonakker B. C., Harley E. H. 1991; Recurring theme of changes in the transcriptional control region of BK virus during adaptation to cell culture. Journal of Virology 65:1600–1604
    [Google Scholar]
  34. Salzman N. P., Natarajan V., Selzer G. B. 1986; Transcription of SV40 and polyomavirus and its regulation. In The Papovaviridae 1 The Polyomaviruses pp 27–98 Salzman N. Edited by New York: Plenum Press;
    [Google Scholar]
  35. Shadan F. F., Villareal L. P. 1993; Coevolution of persistently infecting small DNA tumor viruses and their hosts linked to host- interactive regulatory domains. Proceedings of the National Academy of Sciences USA: 904117–4121
    [Google Scholar]
  36. Shah K. V. 1996; Polyomaviruses. In Fields Virology, 3rd edn. pp 2027–2043 Fields B. N., Knipe D. M., Howley P. M. Edited by Philadelphia: Lippincott-Raven Publishers;
    [Google Scholar]
  37. Spence S. L., Pipas J. M. 1994; Simian virus 40 large T antigen host range domain functions in virion assembly. Journal of Virology 68:4227–4240
    [Google Scholar]
  38. Stewart A. R., Lednicky J. A., Benzick U. S., Tevethia M. J., Butel J. S. 1996; Identification of a variable region at the carboxy terminus of SV40 large T-antigen. Virology 221:355–361
    [Google Scholar]
  39. Stinebaugh S., Melnick J. L. 1962; Plaque formation by vacuolating virus. Virology 16:348–349
    [Google Scholar]
  40. Sweet B. H., Hilleman M. R. 1960; The vacuolating virus, SV40. Proceedings of the Society for Experimental Biology and Medicine 105:420–427
    [Google Scholar]
  41. Takemoto K. K., Kirschenstein R. L., Habel K. 1966; Mutants of simian virus 40 differing in plaque size, oncogenicity, and heat sensitivity. Journal of Bacteriology 92:990–994
    [Google Scholar]
  42. Tavis J. E., Walker D. L., Gardner S. D., Frisque R. J. 1989; Nucleotide sequence of the human polyomavirus AS virus, an antigenic variant of BK virus. Journal of Virology 63:901–911
    [Google Scholar]
  43. Tegtmeyer P., Dohan C.Jr Reznikoff C. 1970; Inactivating and mutagenic effects of nitrosoguanidine on simian virus 40. Proceedings of the National Academy of Sciences USA: 66745–752
    [Google Scholar]
  44. Tevethia M. J., Ripper L. W. 1977; Biology of simian virus 40 (SV40) transplantation antigen (TrAg). Virology 81:192–211
    [Google Scholar]
  45. Tominaga T., Yogo Y., Kitamura T., Aso Y. 1992; Persistence of archetypal JC virus DNA in normal renal tissue derived from tumorbearing patients. Virology 186:736–741
    [Google Scholar]
  46. Tornow J., Polvino-Bodnar M., Santangelo G., Cole C. N. 1985; Two separable functional domains of simian virus 40 large T antigen: carboxyl-terminal region of simian virus 40 large T antigen is required for efficient capsid protein synthesis. Journal of Virology 53:413–424
    [Google Scholar]
  47. Van Heuverswyn H., Fiers W. 1979; Nucleotide sequence of the Hind-C fragment of simian virus 40 DNA. Comparison of the 5ʹ- untranslated region of wild-type virus and of some deletion mutants. European Journal of Biochemistry 100:51–60
    [Google Scholar]
  48. Watanabe S., Yoshiike K. 1986; Evolutionary changes of transcriptional control region in a minute-plaque viable deletion mutant of BK virus. Journal of Virology 59:260–266
    [Google Scholar]
  49. Weiner L. P., Herndon R. M., Narayan O., Johnson R. T., Shah K., Rubinstein L. J., Preziosi T. J., Conley F. K. 1972; Isolation of virus related to SV40 from patients with progressive multifocal leukoencephalopathy. New England Journal of Medicine 286:385–390
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-78-7-1697
Loading
/content/journal/jgv/10.1099/0022-1317-78-7-1697
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error