Expression of human polyomavirus JC T antigen by an adenovirus hybrid vector and its binding to DNA sequences encompassing the JC virus origin of DNA replication Free

Abstract

SUMMARY

In the search for factors that influence the outcome of human polyomavirus JC (JCV) infection, the roles not only of host-related immunological control but also of virus-dependent regulatory steps have to be taken into account. Besides cell-specific control of early expression of the multifunctional virus protein large tumour antigen (T Ag), control mechanisms involve individual steps of the DNA replication process. For the analysis of T Ag DNA binding, the protein was expressed by an adenovirus hybrid vector in the 293 cell line to provide saturating amounts of JCV T Ag. After determination of the size and immunoreactivity, functional activity was analysed by specific DNA binding. To avoid the interference of cellular proteins, T Ag was immunoprecipitated prior to the reaction. Binding to T Ag-binding sites I and II within a 141 bp DNA segment in the control region was analysed using deletion mutants of a JCV subtype from brain tissue of a patient with fatal central nervous system disease. The specificity of the binding was confirmed by recombinant T Ag binding to origin of DNA replication (ori) sequences of wild-type JCV genomes. These data document that recombinant T Ag overexpressed by the adenovirus vector in eukaryotic cells was JCV-specific, had the expected length and exhibited specific ori-binding activity, thus providing the essential tool for future analysis of virus-host interactions at the level of viral DNA replication.

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1995-01-01
2024-03-29
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References

  1. Amirhaeri S., Wohlrab F., Major E. O., Wells R. 1988; Unusual DNA structure in the regulatory region of the human papovirus JC virus. Journal of Virology 62:922–931
    [Google Scholar]
  2. Arthur R. R., Shah K. V. 1989; Occurrence and significance of papovaviruses BK and JC in the urine. Progress in Medical Virology 36:42–61
    [Google Scholar]
  3. Berkner K. L. 1992; Expression of heterologous sequences in adenoviral vectors. Current Topics in Microbiology and Immunology 158:39–66
    [Google Scholar]
  4. Borowiec J. A., Dean F. B., Hurwitz J. 1991; Differential induction of structural changes in the simian virus 40 origin of replication by T antigen. Journal of Virology 65:1228–1235
    [Google Scholar]
  5. Deb S. P., Deb S. 1989; Preferential binding of simian virus 40 T antigen dimers to origin region I. Journal of Virology 63:2901–2907
    [Google Scholar]
  6. DePamphilis M. L. 1993; Eukaryotic DNA replication: anatomy of an origin. Annual Review of Biochemistry 62:29–63
    [Google Scholar]
  7. Dörries K. 1984; Progressive multifocal leukoencephalopathy: analysis of JC virus DNA from brain and kidney tissue. Virus Research 1:25–38
    [Google Scholar]
  8. Fanning E., Knippers R. 1992; Structure and function of simian virus 40 large tumor antigen. Annual Review of Biochemistry 61:55–85
    [Google Scholar]
  9. Feigenbaum L., Khalili K., Major E., Khoury G. 1987; Regulation of the host range of human papovavirus JCV. Proceedings of the National Academy of SciencesU.S.A. 84:3695–3698
    [Google Scholar]
  10. Fiers W., Contreras R., FIaegeman G., Rogiers R., Van de Voorde A., Van Heuverswyn H., Van Herreweghe J., Volckaert G., Ysebaert M. 1978; Complete nucleotide sequence of SV40 DNA. Science 293113–120
    [Google Scholar]
  11. Frisque R. J., White F. A. III 1992; The molecular biology of JC virus, causative agent of progressive multifocal leukoencephalopathy. In Molecular Neurovirology25–158 Roos R. P. Clifton, New Jersey: The Humana Press;
    [Google Scholar]
  12. Frisque R., Bream G. L., Cannella M. T. 1984; Human polyomavirus JC genome. Journal of Virology 51:458–469
    [Google Scholar]
  13. Graham F. L., van der Eb A. J. 1973; A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52:456–467
    [Google Scholar]
  14. Graham F. L., Smiley J., Russell W. C., Nairn R. 1977; Characteristics of a human cell line transformed by DNA from human adenovirus type 5. Journal of General Virology 36:59–72
    [Google Scholar]
  15. Haggerty S., Walker D. L., Frisque R. J. 1989; JC virus-simian virus 40 genomes containing heterologous regulatory signals and chimeric early regions: identification of regions restricting trans- formation by JC virus. Journal of Virology 63:2180–2190
    [Google Scholar]
  16. Harlow E., Lane D. 1988; . Antibodies: A Laboratory Manual New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  17. Harlow E., Crawford L. V., Pim D. C., Williamson N. M. 1981; Monoclonal antibodies specific for simian virus 40 tumor antigens. Journal of Virology 39:861–869
    [Google Scholar]
  18. Henikoff S. 1984; Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351–359
    [Google Scholar]
  19. Hinzpeter M., Fanning E., Deppert W. 1986; A new sensitive target-bound DNA binding assay for SV40 large T antigen. Virology 148:159–167
    [Google Scholar]
  20. Jones N., Shenk T. 1979; Isolation of an adenovirus type 5 host range deletion mutant defective for transformation of rat embryo cells. Cell 17:683–689
    [Google Scholar]
  21. Kerr D. A., Chang C. -F., Gordon J., Bjornsti M. -A., Khalili K. 1993; Inhibition of human neurotropic virus (JCV) DNA replication in glial cells by camptothecin. Virology 196:612–618
    [Google Scholar]
  22. Lamarche N., Massie B., Richer M., Paradis H., Langelier Y. 1990; High level expression in 293 cells of the herpes simplex virus type 2 ribonucleotide reductase subunit 2 using an adenovirus vector. Journal of General Virology 71:1785–1795
    [Google Scholar]
  23. Li J. J., Kelly T. J. 1985; Simian virus 40 DNA replication in vitro: specificity of initiation and evidence for bidirectional rep¬lication. Molecular and Cellular Biology 6:3086–3093
    [Google Scholar]
  24. Loeber G., Dörries K. 1988; DNA rearrangements in organ- specific variants of polyomavirus JC strain GS. Journal of Virology 62:1730–1735
    [Google Scholar]
  25. Lynch K. J., Frisque R. J. 1990; Identification of critical elements within the JC virus DNA replication origin. Journal of Virology 64:5812–5822
    [Google Scholar]
  26. Lynch K. J., Frisque R. J. 1991; Factors contributing to the restricted DNA replicating activity of JC virus. Virology 180:306–317
    [Google Scholar]
  27. McKay R. D. G. 1981; Binding of a simian virus 40 T antigen- related protein to DNA. Journal of Molecular Biology 145:471–188
    [Google Scholar]
  28. McVey D., Brizuela L., Mohr I., Marshak D. R., Gluzman Y., Beach D. 1989; Phosphorylation of large tumour antigen by cdc2 stimulates SV40 DNA replication. Nature 341:503–507
    [Google Scholar]
  29. Major E. O., Traub R. G. 1986; JC virus T protein during productive infection in human fetal brain and kidney cells. Virology 148:221–225
    [Google Scholar]
  30. Major E. O., Amemiya K., Tornatore C. S., Houff S. A., Berger J. R. 1992; Pathogenesis and molecular biology of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clinical Microbiology Reviews 5:49–73
    [Google Scholar]
  31. Mandl C. W., Frisque R. J. 1986; Characterization of cells transformed by the human polyomavirus JC virus. Journal of General Virology 67:1733–1739
    [Google Scholar]
  32. Martin J. D., King D. M., Slauch J. M., Frisque R. J. 1985; Differences in regulatory sequences of naturally occurring JC virus variants. Journal of Virology 53:306–311
    [Google Scholar]
  33. Myers C., Frisque R. J., Arthur R. R. 1989; Direct isolation and characterization of JC virus from urine samples of renal and bone marrow patients. Journal of Virology 63:4445–1449
    [Google Scholar]
  34. Parsons R., Anderson M. E., Tegtmeyer P. 1990; Three domains in the simian virus 40 core origin orchestrate the binding, melting, and DNA helicase activities of T antigen. Journal of Virology 64:509–518
    [Google Scholar]
  35. Precious B., Russell W. C. 1985; Growth, purification and titration of adenovirus. In Virology, a Practical Approach193–205 Mahy B. W. J. Oxford: IRL Press;
    [Google Scholar]
  36. Prives C. 1990; The replication functions of SV40 T antigen are regulated by phosphorylation. Cell 61:735–738
    [Google Scholar]
  37. Rigby P. W. J., Lane D. P. 1983; Structure and function of simian virus 40 large T antigen. In Advances in Viral Oncology 331–57 Klein G. New York: Raven Press;
    [Google Scholar]
  38. Sambrook J., Fritsch E. F., Maniatis T. 1989; . Molecular Cloning: A Laboratory Manual, 2. New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  39. Simmons D. T., Loeber G., Tegtmeyer P. 1990; Four major sequence elements of simian virus 40 large T antigen coordinate its specific and non-specific DNA binding. Journal of Virology 64:1973–1983
    [Google Scholar]
  40. Simmons D. T., Wun-Kim K., Young W. 1990; Identification of simian virus 40 T antigen residues important for specific and non- specific binding to DNA and for helicase activity. Journal of Virology 64:4858–1865
    [Google Scholar]
  41. Sock E., Wegner M., Grummt F. 1991; DNA replication of human polyomavirus JC is stimulated by NF-I in vivo. Virology 182:298–308
    [Google Scholar]
  42. Sock E., Wegner M., Fortunato E. A., Grummt F. 1993; Large T-antigen and sequences within the regulatory region of JC virus both contribute to the features of JC virus DNA replication. Virology 197:537–548
    [Google Scholar]
  43. Solnick D. 1981; Construction of an adenovirus-SV40 recombinant producing SV40 T antigen from an adenovirus late promoter. Cell 24:135–143
    [Google Scholar]
  44. Stetter G., Müller D., Montenarh M. 1988; SV40 T antigen binding to site II is functionally separated from binding to site I. Virology 164:309–317
    [Google Scholar]
  45. Stoner G. L., Ryschkewitsch C. F., Walker D. L., Soffer D., Webster H. F. 1988; A monoclonal antibody to SV40 large T antigen labels a nuclear antigen in JC virus-transformed cells and in progressive multifocal leucoencephalopathy (PML) brain infected with JC virus. Journal of Neuroimmunology 17:331–345
    [Google Scholar]
  46. Tabor S., Richardson C. C. 1987; DNA sequence analysis with a modified T7 DNA polymerase. Proceedings of the National Academy of SciencesU.S.A. 84:4767–4771
    [Google Scholar]
  47. Tavis J. E., Frisque R. J. 1991; Altered DNA binding and replication activities of JC virus T antigen mutants. Virology 183:239–250
    [Google Scholar]
  48. Walker D. L., Frisque R. J. 1986; The biology and molecular biology of JC virus. In The Papovaviridae: The Polyomaviruses327–377 Salzman N. P. New York: Plenum Press;
    [Google Scholar]
  49. Walker D. L., Padgett B. L. 1983; Progressive multifocal leukoencephalopathy. Comprehensive Virology 18:161–193
    [Google Scholar]
  50. Walker D. L., Padgett B. L., ZuRhein G. M., Albert A. D., Marsh R. F. 1973; Human polyomavirus (JC): induction of brain tumors in hamsters. Science 181:674–676
    [Google Scholar]
  51. Yogo Y., Kitamura T., Sugimoto C., Ueki T., Aso Y., Hara K., Taguchi F. C. 1990; Isolation of a possible archetypal JC virus DNA sequence from nonimmunocompromised individuals. Journal of Virology 64:3139–3143
    [Google Scholar]
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