1887

Abstract

The highly restricted host range of JC virus (JCV) has made it difficult to study the biology of this common human papovavirus. To increase our understanding of the tissue specificity of this virus, we have examined the expression of the T antigen (T-Ag) in primary and established cell lines from various tissues of transgenic mice containing the JCV early region. In contrast to earlier results from a simian virus 40-containing transgenic mouse, there was no T-Ag expression in mesenchymal fibroblasts derived from two lines of JCV-transgenic mice. Instead, we isolated T-Ag- positive (T-Ag) cells that had characteristics consistent with a neural crest origin. Furthermore, primary brain cultures contained many T-Ag+ astrocytes, but no expression was detected in macrophages, epithelial cells, neuronal cells nor, surprisingly, in oligodendrocytes. Continued passage of these cultures resulted in vigorously growing glial fibrillary acidic proteinpositive, T-Ag astrocytes. Thus, the strict tissue specificity of JCV expression was maintained, despite the fact that the viral genome pre-existed in every tissue of these transgenic mice and these constraints on expression were preserved even when cells were explanted .

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-71-1-151
1990-01-01
2021-10-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/71/1/JV0710010151.html?itemId=/content/journal/jgv/10.1099/0022-1317-71-1-151&mimeType=html&fmt=ahah

References

  1. Abney E. R., Bartlett P. P., Raff M. C. 1981; Astrocytes, ependymal cells, and oligodendrocytes develop on schedule in dissociated cell cultures of embryonic rat brain. Developmental Biology 83:301–310
    [Google Scholar]
  2. Aksamit A. J., Mourrain P., Sever J. L., Major E. O. 1985; Progressive multifocal leukoencephalopathy: investigation of three cases using in situ hybridization with JC virus biotinylated DNA probe. Annals of Neurology 18:490–496
    [Google Scholar]
  3. Beckmann A. M., Shah K. V., Padgett B. L. 1982; Propagation and primary isolation of papovavirus JC in epithelial cells derived from human urine. Infection and Immunity 38:774–777
    [Google Scholar]
  4. Beggs A. H., Scangos G. A. 1986; Serum-free selection of one genes. In Gene Amplification and Analysis 4 pp. 177–195 Chirikjian J. G., Pappas T. S. Edited by New York: Elsevier;
    [Google Scholar]
  5. Beggs A. H., Frisque R. J., Scangos G. A. 1988; Extinction of JC virus tumor-antigen expression in glial cell-fibroblast hybrids. Proceedings of the National Academy of Sciences, U.S.A 85:7632–7636
    [Google Scholar]
  6. Bollag B., Chuke W-F., Frisque R. J. 1989; Hybrid genomes of the polyomaviruses JC virus, BK virus, and simian virus 40: identification of sequences important for efficient transformation. Journal of Virology 63:863–872
    [Google Scholar]
  7. Brinster R. L., Chen H. Y., Messing A., Van Dyke T., Levine A. J., Palmiter R. D. 1984; Transgenic mice harboring SV40 TAg genes develop characteristic brain tumors. Cell 37:367–379
    [Google Scholar]
  8. Castaigne P., Rondot P., Escourolle R. J., Ridadeau-Dumas J., Cathala F., Hauw J.-J. 1974; Leucoencephalopathie multi-focale progressive et “gliomes” multiples. Reviews of Neurology 130:379–392
    [Google Scholar]
  9. Chen T. R. 1977; In situ detection of mycoplasma contamination in cell cultures by fluorescent Hoechst 33258 stain. Experimental Cell Research 130:379–392
    [Google Scholar]
  10. Chirgwin J. M., Przybyla A. E., Macdonald R. J., Rutter W. J. 1979; Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294–5299
    [Google Scholar]
  11. Dippold W. G., Jay G., Deleo A. B., Khoury G., Old L. J. 1981; p53 transformation-related protein: detection by monoclonal antibody in mouse and human cells. Proceedings of the National Academy of Sciences, U.S.A 78:1695–1699
    [Google Scholar]
  12. Fareed G. C., Takemoto K. K., Gimbrone M. A. 1978; Interaction of simian virus 40 and human papovaviruses, BK, and JC, with human vascular endothelial cells. In Microbiology pp. 427–431 Schlessinger D. Edited by Washington D.C: American Society for Microbiology;
    [Google Scholar]
  13. Frisque R. J., Martin J. D., Padgett B. L., Walker D. L. 1979; Infectivity of the DNA from four isolates of JC virus. Journal of Virology 32:476–482
    [Google Scholar]
  14. Frisque R. J., Rifkin D. B., Walker D. L. 1980; Transformation of primary hamster brain cells with JC virus and its DNA. Journal of Virology 35:265–269
    [Google Scholar]
  15. Giarusso M. H., Koeppen A. H. 1978; Atypical progressive multifocal leukoencephalopathy and primary malignant lymphoma. Journal of Neurological Sciences 35:391–398
    [Google Scholar]
  16. Haggerty S., Walker D. L., Frisque R. J. 1989; JC virus-simian virus 40 viral genomes containing heterologous regulatory signals and chimeric early regions: identification of regions restricting transformation by JC virus. Journal of Virology 63:2180–2190
    [Google Scholar]
  17. Howley P. M., Rentier-Delrue F., Heilman C. A., Law M., Chowdhury K., Israel M. A., Takemoto K. K. 1980; Cloned human polyomavirus JC DNA can transform human amnion cells. Journal of Virology 36:878–882
    [Google Scholar]
  18. Huttner K. M., Scangos G. A., Ruddle F. H. 1979; DNA-mediated gene transfer of a circular plasmid into murine cells. Proceedings of the National Academy of Sciences, U.S.A 76:5820–5824
    [Google Scholar]
  19. Jay G., Khoury G., Deleo A. B., Dippold W. G., Old L. J. 1981; p53 transformation-related protein: detection of an associated phosphotransferase activity. Proceedings of the National Academy of Sciences, U.S.A 78:2932–2936
    [Google Scholar]
  20. Johnson D., Lanahan A., Buck C. R., Sehgal A., Morgan C., Mercer E., Bothwell M., Chao M. 1986; Expression and structure of human NGF receptor. Cell 47:545–554
    [Google Scholar]
  21. Loeb D. M., Woolford J., Beemon K. 1987; pp60 c-src has less affinity for the detergent-insoluble cellular matrix than do pp60 v-src and other viral protein-tyrosine kinases. Journal of Virology 61:2420–2427
    [Google Scholar]
  22. London W. T., Houff S. A., Madden D. L., Fucillo D. A., Gravell M., Wallen W. C., Palmer A. E., Sever J. L. 1978; Brain tumors in owl monkeys inoculated with a human polyomavirus (JC virus). Science 201:1246–1248
    [Google Scholar]
  23. Mcmorris F. A., Smith T. M., Desalvo S., Furlanetto R. W. 1986; Insulin-like growth factor I/somatomedin C: a potent inducer of oligodendrocyte development. Proceedings of the National Academy of Sciences, U.S.A 83:822–826
    [Google Scholar]
  24. 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]
  25. Major E. O., Mourrain P., Cummins C. 1984; JC virus-induced owl monkey glioblastoma cells in culture: biological properties associated with the viral early gene product. Virology 136:359–367
    [Google Scholar]
  26. Major E. O., Vacante D. A., Traub R. G., London W. T., Sever J. L. 1987; Owl monkey astrocytoma cells in culture spontaneously produce infectious JC virus which demonstrates altered biological properties. Journal of Virology 61:1435–1441
    [Google Scholar]
  27. Mandl C., Walker D. L., Frisque R. J. 1987; Derivation and characterization of POJ cells, transformed human fetal glial cells that retain their permissivity for JC virus. Journal of Virology 61:755–763
    [Google Scholar]
  28. Mazlo M., Tariska I. 1982; Are astrocytes infected in progressive multifocal leukoencephalopathy (PML)?. Acta neuropathologica 56:45–51
    [Google Scholar]
  29. Narayan O. 1976; On the neoplastic viral transformation of astrocytes in cases of progressive multifocal leukoencephalopathy. Journal of Neuropathology and Experimental Neurology 35:313
    [Google Scholar]
  30. Osborn M., Altmannsberger M., Debus E., Weber K. 1984; Conventional and monoclonal antibodies to intermediate filament proteins in human tumor diagnosis. Cancer Cells 1:191–200
    [Google Scholar]
  31. Padgett B. L., Walker D. L. 1976; New human papovaviruses. Progress in Medical Virology 22:1–35
    [Google Scholar]
  32. Padgett B. L., Rogers C. M., Walker D. L. 1977a; JC virus, a human polyomavirus associated with progressive multifocal leukoencephalopathy: additional biological characteristics and antigenic relationships. Infection and Immunity 14:656–662
    [Google Scholar]
  33. Padgett B. L., Walker D. L., Zurhein G. M., Varakis J. N. 1977b; Differential neuro-oncogenicity of strains of JC virus, a human polyoma virus, in newborn Syrian hamsters. Cancer Research 37:718–720
    [Google Scholar]
  34. Prochiantz A., Delacourte A., Daguet M., Paulin K. 1982; Intermediate filament proteins in mouse brain cells cultured in the presence or absence of fetal calf serum. Experimental Cell Research 139:404–410
    [Google Scholar]
  35. Raff M. C., Abney E. A., Cohen J., Lindsay R., Noble M. 1983; Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides and growth characteristics. Journal of Neuroscience 3:1289–1300
    [Google Scholar]
  36. Raff M. C., Fields K. L., Hakomori S.-I., Mirsky R., Pruss R. M., Winter J. 1979; Cell-type-specific markers for distinguishing and studying neurons and the major classes of glial cells in culture. Brain Research 174:283–308
    [Google Scholar]
  37. Richardson E. P. Jr 1961; Progressive multifocal leukoencephalopathy. New England Journal of Medicine 265:815–823
    [Google Scholar]
  38. Ross A. H., Grob P., Bothwell M., Elder D. E., Ernst C. S., Marano N., Ghrist B. F. D., Slemp C. C., Herlyn M., Atkinson B., Koprowski H. 1984; Characterization of nerve growth factor receptor in neural crest tumors using monoclonal antibodies. Proceedings of the National Academy of Sciences, U.S.A 81:6681–6685
    [Google Scholar]
  39. Small J. A., Blair D. G., Showalter S. D., Scangos G. A. 1985; Analysis of a transgenic mouse containing simian virus 40 and v-myc sequences. Molecular and Cellular Biology 5:642–648
    [Google Scholar]
  40. Small J. A., Khoury G., Jay G., Howley P. M., Scangos G. A. 1986a; Early regions of JC virus and BK virus induce distinct and tissue-specific tumors in transgenic mice. Proceedings of the National Academy of Sciences, U.S.A 83:8288–8292
    [Google Scholar]
  41. Small J. A., Scangos G. A., Cork L., Jay G., Khoury G. 1986b; The early region of human papovavirus JC induces dysmyelination in transgenic mice. Cell 46:13–18
    [Google Scholar]
  42. Stoner G. L., Ryschkewitsch C. F., Walker D. L., Webster H. DeF. 1986; JC papovavirus large tumor (T)-antigen expression in brain tissue of acquired immune deficiency syndrome (AIDS) and non-AIDS patients with progressive multifocal leukoencephalopathy. Proceedings of the National Academy of Sciences, U.S.A 83:2271–2275
    [Google Scholar]
  43. Takemoto K. K., Howley P. M., Miyamura T. 1979; JC human papovavirus replication in human amnion cells. Journal of Virology 30:384–389
    [Google Scholar]
  44. Todaro G. J., Green H. 1963; Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. Journal of Cell Biology 17:299–313
    [Google Scholar]
  45. Tooze J. 1981 The Molecular Biology of Tumor Viruses part 2 , 2nd edn. New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  46. Trapp B. D., Small J. A., Pulley M., Khoury G., Scangos G. A. 1988; Dysmyelination in transgenic mice containing JC virus early region. Annals of Neurology 23:38–48
    [Google Scholar]
  47. Wahl G. M., Stern M., Stark G. R. 1979; Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization using dextran sulfate. Proceedings of the National Academy of Sciences, U.S.A 76:3683–3687
    [Google Scholar]
  48. Walker D. L., Frisque R. J. 1986; The biology and molecular biology of JC virus. In The Papovaviridae: the Polyomaviruses pp. 327–377 Salzman N. P. Edited by New York: Plenum Press;
    [Google Scholar]
  49. Walker D. L., Padgett B. L., Zurhein G. M., Albert A. E., Marsh R. F. 1973; Human papovavirus (JC): induction of brain tumors in hamsters. Science 181:674–676
    [Google Scholar]
  50. Wigler M., Sweet R., Sim G. K., Wold B., Pellicer A., Lacy E., Maniatis T., Silverstein S., Axel R. 1979; Transformation of mammalian cells with genes from prokaryotes and eukaryotes. Cell 16:777–785
    [Google Scholar]
  51. Williams B. P., Abney E. R., Raff M. C. 1985; Macroglial cell development in embryonic rat brain: studies using monoclonal antibodies, fluorescence activated cell sorting, and cell culture. Developmental Biology 112:126–134
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-71-1-151
Loading
/content/journal/jgv/10.1099/0022-1317-71-1-151
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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