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. 1981 Oct;40(1):276–284. doi: 10.1128/jvi.40.1.276-284.1981

BK virus-transformed inbred hamster brain cells. I. Status of the viral DNA and the association of BK virus early antigens with purified plasma membranes.

E Beth, G Giraldo, R Schmidt-Ullrich, M M Pater, A Pater, G di Mayorca
PMCID: PMC256617  PMID: 6270380

Abstract

Inbred LSH hamster brain cells were transformed in vitro by the GS strain of BK virus (BKV), and transplantable tumors classified as undifferentiated glioblastomas were induced in the syngeneic host. The viral status in the transformed cells, designated LSH-BR-BK, was established. About 46 genome equivalents per cell of viral DNA was detected, with the majority of sequences in a free form. The transformed cells expressed large quantities of tumor (T) antigen as well as surface (S) antigen as demonstrated by indirect immunofluorescence. Sixty-three percent of tumor-bearing hamsters produced high-titer antibodies against T, whereas 3 of 14 (21%) hamsters also produced antibodies against the BKV-specific S antigen. Furthermore, the relatedness of BKV early gene products, including T, S, and tumor-specific transplantation antigen, was established by the production of a rabbit antiserum against highly purified plasma membranes of LSH-BR-BK cells and by the induction of a BKV-specific tumor-specific transplantation antigen response by these plasma membranes in the syngeneic host.

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Selected References

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

  1. Basilico C., Gattoni S., Zouzias D., Valle G. D. Loss of integrated viral DNA sequences in polyomatransformed cells is associated with an active viral A function. Cell. 1979 Jul;17(3):645–659. doi: 10.1016/0092-8674(79)90272-1. [DOI] [PubMed] [Google Scholar]
  2. Beth E., Cikes M., Giraldo G. Microfluorometric analysis of anti-complement and indirect immunofluorescence tests for human papovavirus (JCV and BKV) T antigens. Int J Cancer. 1978 Jan 15;21(1):1–5. doi: 10.1002/ijc.2910210102. [DOI] [PubMed] [Google Scholar]
  3. Beth E., Cikes M., Schloen L., di Mayorca G., Giraldo G. Interspecies-, species- and type-specific T antigenic determinants of human papovaviruses (JC and BK) and of Simian virus 40. Int J Cancer. 1977 Oct 15;20(4):551–559. doi: 10.1002/ijc.2910200412. [DOI] [PubMed] [Google Scholar]
  4. Birg F., Dulbecco R., Fried M., Kamen R. State and organization of polyoma virus DNA sequences in transformed rat cell lines. J Virol. 1979 Feb;29(2):633–648. doi: 10.1128/jvi.29.2.633-648.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Botchan M., Stringer J., Mitchison T., Sambrook J. Integration and excision of SV40 DNA from the chromosome of a transformed cell. Cell. 1980 May;20(1):143–152. doi: 10.1016/0092-8674(80)90242-1. [DOI] [PubMed] [Google Scholar]
  6. Botchan M., Topp W., Sambrook J. The arrangement of simian virus 40 sequences in the DNA of transformed cells. Cell. 1976 Oct;9(2):269–287. doi: 10.1016/0092-8674(76)90118-5. [DOI] [PubMed] [Google Scholar]
  7. Butel J. S., Tevethia S. S., Melnick J. L. Oncogenicity and cell transformation by papovavirus SV40: the role of the viral genome. Adv Cancer Res. 1972;15:1–55. doi: 10.1016/s0065-230x(08)60371-1. [DOI] [PubMed] [Google Scholar]
  8. Chang C., Martin R. G., Livingston D. M., Luborsky S. W., Hu C. P., Mora P. T. Relationship between T-antigen and tumor-specific transplantation antigen in simian virus 40-transformed cells. J Virol. 1979 Jan;29(1):69–75. doi: 10.1128/jvi.29.1.69-75.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chenciner N., Grossi M. P., Meneguzzi G., Corallini A., Manservigi R., Barbanti-Brodano G., Milanesi G. State of viral DNA in BK virus-transformed rabbit cells. Virology. 1980 May;103(1):138–148. doi: 10.1016/0042-6822(80)90132-4. [DOI] [PubMed] [Google Scholar]
  10. Chenciner N., Meneguzzi G., Corallini A., Grossi M. P., Grassi P., Barbanti-Brodano G., Milanesi G. Integrated and free viral DNA in hamster tumors induced by BK virus. Proc Natl Acad Sci U S A. 1980 Feb;77(2):975–979. doi: 10.1073/pnas.77.2.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Coleman D. V., Gardner S. D., Field A. M. Human polyomavirus infection in renal allograft recipients. Br Med J. 1973 Aug 18;3(5876):371–375. doi: 10.1136/bmj.3.5876.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Corallini A., Altavilla G., Cecchetti M. G., Fabris G., Grossi M. P., Balboni P. G., Lanza G., Barbanti-Brodano G. Ependymomas, malignant tumors of pancreatic islets, and osteosarcomas induced in hamsters by BK virus, a human papovavirus. J Natl Cancer Inst. 1978 Sep;61(3):875–883. [PubMed] [Google Scholar]
  13. Corallini A., Barbanti-Brodano G., Bortoloni W., Nenci I., Cassai E., Tampieri M., Portolani M., Borgatti M. High incidence of ependymomas induced by BK virus, a human papovavirus: brief communication. J Natl Cancer Inst. 1977 Nov;59(5):1561–1564. doi: 10.1093/jnci/59.5.1561. [DOI] [PubMed] [Google Scholar]
  14. Costa J., Yee C., Tralka T. S., Rabson A. S. Hamster ependymomas produced by intracerebral inoculation of a human papovavirus (MMV). J Natl Cancer Inst. 1976 Apr;56(4):863–864. doi: 10.1093/jnci/56.4.863. [DOI] [PubMed] [Google Scholar]
  15. Daya-Grosjean L., Monier R. Presence of free viral DNA in simian virus 40-transformed nonproducer cells. J Virol. 1978 Aug;27(2):307–312. doi: 10.1128/jvi.27.2.307-312.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dougherty R. M., DiStefano H. S. Isolation and characterization of a papovavirus from human urine. Proc Soc Exp Biol Med. 1974 Jun;146(2):481–487. doi: 10.3181/00379727-146-38131. [DOI] [PubMed] [Google Scholar]
  17. Duff R., Rapp F. Properties of hamster embryo fibroblasts transformed in vitro after exposure to ultraviolet-irradiated herpes simplex virus type 2. J Virol. 1971 Oct;8(4):469–477. doi: 10.1128/jvi.8.4.469-477.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gardner S. D. Prevalence in England of antibody to human polyomavirus (B.k.). Br Med J. 1973 Jan 13;1(5845):77–78. doi: 10.1136/bmj.1.5845.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gelb L. D., Kohne D. E., Martin M. A. Quantitation of Simian virus 40 sequences in African green monkey, mouse and virus-transformed cell genomes. J Mol Biol. 1971 Apr 14;57(1):129–145. doi: 10.1016/0022-2836(71)90123-9. [DOI] [PubMed] [Google Scholar]
  20. Greenlee J. E., Narayan O., Johnson R. T., Herndon R. M. Induction of brain tumors in hamsters with BK virus, a human papovavirus. Lab Invest. 1977 Jun;36(6):636–641. [PubMed] [Google Scholar]
  21. Howley P. M., Khoury G., Byrne J. C., Takemoto K. K., Martin M. A. Physical map of the BK virus genome. J Virol. 1975 Oct;16(4):959–973. doi: 10.1128/jvi.16.4.959-973.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kaplan J. C., Wilbert S. M., Collins J. J., Rakusanova T., Zamansky G. B., Black P. H. Isolation of simian virus 40-transformed inbred hamster cell lines heterogeneous for virus induction by chemicals or radiation. Virology. 1975 Nov;68(1):200–214. doi: 10.1016/0042-6822(75)90161-0. [DOI] [PubMed] [Google Scholar]
  23. Kaschka-Dierich C., Adams A., Lindahl T., Bornkamm G. W., Bjursell G., Klein G., Giovanella B. C., Singh S. Intracellular forms of Epstein-Barr virus DNA in human tumour cells in vivo. Nature. 1976 Mar 25;260(5549):302–306. doi: 10.1038/260302a0. [DOI] [PubMed] [Google Scholar]
  24. Lanford R. E., Butel J. S. Antigenic relationship of SV40 early proteins to purified large T polypeptide. Virology. 1979 Sep;97(2):295–306. doi: 10.1016/0042-6822(79)90341-6. [DOI] [PubMed] [Google Scholar]
  25. Law L. W., Takemoto K. K., Rogers M. J., Ting R. C. Induction of simian virus 40 (SV40) transplantation immunity in mice by SV40-transformed cells of various species. J Natl Cancer Inst. 1977 Nov;59(5):1523–1526. doi: 10.1093/jnci/59.5.1523. [DOI] [PubMed] [Google Scholar]
  26. MACPHERSON I., MONTAGNIER L. AGAR SUSPENSION CULTURE FOR THE SELECTIVE ASSAY OF CELLS TRANSFORMED BY POLYOMA VIRUS. Virology. 1964 Jun;23:291–294. doi: 10.1016/0042-6822(64)90301-0. [DOI] [PubMed] [Google Scholar]
  27. Pater M. M., Pater A., di Mayorca G. Comparative analysis of GS and BK virus genomes. J Virol. 1979 Oct;32(1):220–225. doi: 10.1128/jvi.32.1.220-225.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Purchio A. F., Fareed G. C. Transformation of human embryonic kidney cells by human papovarirus BK. J Virol. 1979 Feb;29(2):763–769. doi: 10.1128/jvi.29.2.763-769.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Reese J. M., Reissing M., Daniel R. W., Shah K. V. Occurrence of BK virus and BK virus-specific antibodies in the urine of patients receiving chemotherapy for malignancy. Infect Immun. 1975 Jun;11(6):1375–1381. doi: 10.1128/iai.11.6.1375-1381.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schmidt-Ullrich R., Kahn S. J., Thompson W. S., Wallach D. F. Host cell-modified T-antigen in membranes of simian virus 40-transformed hamster cells. J Natl Cancer Inst. 1980 Sep;65(3):585–593. [PubMed] [Google Scholar]
  31. Schmidt-Ullrich R., Wallach D. F., Davis F. D., 2nd Membranes of normal hamster lymphocytes and lymphoid cells neoplastically transformed by simian virus 40. I. High-yield purification of plasma membrane fragments. J Natl Cancer Inst. 1976 Nov;57(5):1107–1116. doi: 10.1093/jnci/57.5.1107. [DOI] [PubMed] [Google Scholar]
  32. Seif I., Khoury G., Dhar R. The genome of human papovavirus BKV. Cell. 1979 Dec;18(4):963–977. doi: 10.1016/0092-8674(79)90209-5. [DOI] [PubMed] [Google Scholar]
  33. Shah K. V., Daniel R. W., Strandberg J. D. Sarcoma in a hamster inoculated with BK virus, a human papovavirus. J Natl Cancer Inst. 1975 Apr;54(4):945–950. [PubMed] [Google Scholar]
  34. Soule H. R., Lanford R. E., Butel J. S. Antigenic and immunogenic characteristics of nuclear and membrane-associated simian virus 40 tumor antigen. J Virol. 1980 Feb;33(2):887–901. doi: 10.1128/jvi.33.2.887-901.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  36. Takemoto K. K., Linke H., Miyamura T., Fareed G. C. Persistent BK papovavirus infection of transformed human fetal brain cells. I. Episomal viral DNA in cloned lines deficient in T-antigen expression. J Virol. 1979 Mar;29(3):1177–1185. doi: 10.1128/jvi.29.3.1177-1185.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Takemoto K. K., Martin M. A. Transformation of hamster kidney cells by BK papovavirus DNA. J Virol. 1975 Jan;17(1):247–253. doi: 10.1128/jvi.17.1.247-253.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Takemoto K. K., Rabson A. S., Mullarkey M. F., Blaese R. M., Garon C. F., Nelson D. Isolation of papovavirus from brain tumor and urine of a patient with Wiskott-Aldrich syndrome. J Natl Cancer Inst. 1974 Nov;53(5):1205–1207. doi: 10.1093/jnci/53.5.1205. [DOI] [PubMed] [Google Scholar]
  39. Uchida S., Watanabe S., Aizawa T., Furuno A., Muto T. Polyoncogenicity and insulinoma-inducing ability of BK Virus, a human Papovavirus, in Syrian golden hamsters. J Natl Cancer Inst. 1979 Jul;63(1):119–126. [PubMed] [Google Scholar]
  40. Upcroft P., Skolnik H., Upcroft J. A., Solomon D., Khoury G., Hamer D. H., Fareed G. C. Transduction of a bacterial gene into mammalian cells. Proc Natl Acad Sci U S A. 1978 May;75(5):2117–2121. doi: 10.1073/pnas.75.5.2117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yogo Y., Furuno A., Watanabe S., Yoshiike K. Occurrence of free, defective viral DNA in a hamster tumor induced by human papovavirus BK. Virology. 1980 May;103(1):241–244. doi: 10.1016/0042-6822(80)90143-9. [DOI] [PubMed] [Google Scholar]
  43. ter Schegget J., Voves J., van Strien A., van der Noordaa J. Free viral DNA in BK virus-induced hamster tumor cells. J Virol. 1980 Aug;35(2):331–339. doi: 10.1128/jvi.35.2.331-339.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. van der Noordaa J. Infectivity, oncogenicity and transforming ability of BK virus and BK virus DNA. J Gen Virol. 1976 Mar;30(3):371–373. doi: 10.1099/0022-1317-30-3-371. [DOI] [PubMed] [Google Scholar]

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