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. 1969 Jul;4(1):75–93. doi: 10.1128/jvi.4.1.75-93.1969

Herpes-Type Virus of the Frog Renal Adenocarcinoma

I. Virus Development in Tumor Transplants Maintained at Low Temperature

Christopher W Stackpole 1,1
PMCID: PMC375840  PMID: 5808113

Abstract

Development of the herpes-type virus of the frog kidney tumor was investigated by electron microscopy and high-resolution autoradiography in eyechamber transplants of tumor maintained at 7.5 C for up to 27 weeks. Virus particles were first detected at 10 weeks in nuclei containing aggregates of dense granular material. The initial incorporation of a pulse of 3H-thymidine into these aggregates indicated that they contained newly synthesized viral deoxyribonucleic acid. Capsids enclosing doubleshelled cores were labeled with 3H-thymidine before capsids with dense cores, and intermediate core forms were observed, suggesting that the double-shelled core transforms into the dense core. Particles with dense cores were observed while being enveloped by budding through the inner membrane of the nuclear envelope, and subsequently while being unenveloped in passing through the outer membrane into the cytoplasm. Virus particles within the cytoplasm acquired fibrillar coats and budded into vesicles, from which they were released, in enveloped form, at the cell surface. Tubular forms and particles considerably smaller than virus particles were regularly encountered in infected nuclei, and the relationship of these forms to virus replication is discussed.

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Selected References

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  1. ARMSTRONG J. A., PEREIRA H. G., ANDREWES C. H. Observations on the virus of infectious bovine rhinotracheitis, and its affinity with the Herpesvirus group. Virology. 1961 Jun;14:276–285. doi: 10.1016/0042-6822(61)90204-5. [DOI] [PubMed] [Google Scholar]
  2. Ahmed M., Schidlovsky G. Electron microscopic localization of herpesvirus-type particles in Marek's disease. J Virol. 1968 Dec;2(12):1443–1457. doi: 10.1128/jvi.2.12.1443-1457.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BERNHARD W., FEBVRE H. L., CRAMER R. [Electron microscopic demonstration of a virus in cells infected in vitro by the polyoma agent]. C R Hebd Seances Acad Sci. 1959 Jul 20;249:483–485. [PubMed] [Google Scholar]
  4. CASPAR D. L., KLUG A. Physical principles in the construction of regular viruses. Cold Spring Harb Symp Quant Biol. 1962;27:1–24. doi: 10.1101/sqb.1962.027.001.005. [DOI] [PubMed] [Google Scholar]
  5. Darlington R. W., James C. Biological and morphological aspects of the growth of equine abortion virus. J Bacteriol. 1966 Jul;92(1):250–257. doi: 10.1128/jb.92.1.250-257.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Darlington R. W., Moss L. H., 3rd Herpesvirus envelopment. J Virol. 1968 Jan;2(1):48–55. doi: 10.1128/jvi.2.1.48-55.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. EPSTEIN M. A., HENLE G., ACHONG B. G., BARR Y. M. MORPHOLOGICAL AND BIOLOGICAL STUDIES ON A VIRUS IN CULTURED LYMPHOBLASTS FROM BURKITT'S LYMPHOMA. J Exp Med. 1965 May 1;121:761–770. doi: 10.1084/jem.121.5.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Epstein M. A., Achong B. G., Churchill A. E., Biggs P. M. Structure and development of the herpes-types virus of Marek's disease. J Natl Cancer Inst. 1968 Sep;41(3):805–820. [PubMed] [Google Scholar]
  9. FALKE D., SIEGERT R., VOGELL W. [Electron microscopic findings on the problem of double membrane formation in herpes simplex virus]. Arch Gesamte Virusforsch. 1959;9:484–496. [PubMed] [Google Scholar]
  10. FAWCETT D. W. Electron microscope observations on intracellular virus-like particles associated with the cells of the Lucké renal adenocarcinoma. J Biophys Biochem Cytol. 1956 Nov 25;2(6):725–741. doi: 10.1083/jcb.2.6.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. GRANBOULAN N., TOURNIER P., WICKER R., BERNHARD W. An electron microscope study of the development of SV40 virus. J Cell Biol. 1963 May;17:423–441. doi: 10.1083/jcb.17.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. HORNE R. W. The comparative structure of adenoviruses. Ann N Y Acad Sci. 1962 Nov 30;101:475–484. doi: 10.1111/j.1749-6632.1962.tb18888.x. [DOI] [PubMed] [Google Scholar]
  13. Henle W., Hummeler K., Henle G. Antibody coating and agglutination of virus particles separated from the EB3 line of Burkitt lymphoma cells. J Bacteriol. 1966 Jul;92(1):269–271. doi: 10.1128/jb.92.1.269-271.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jacob J. Involvement of the nucleolus in viral synthesis in the cells of primary renal tumors of Leopard frogs. Cancer Res. 1968 Oct;28(10):2126–2136. [PubMed] [Google Scholar]
  15. KAPLAN A. S., BEN-PORAT T. The pattern of viral and cellular DNA synthesis in pseudorabies virus-infected cells in the logarithmic phase of growth. Virology. 1963 Feb;19:205–214. doi: 10.1016/0042-6822(63)90010-2. [DOI] [PubMed] [Google Scholar]
  16. Lunger P. D., Darlington R. W., Granoff A. Cell-virus relationships in the Lucké renal adenocarcinoma: an ultrastructure study. Ann N Y Acad Sci. 1965 Aug 10;126(1):289–314. doi: 10.1111/j.1749-6632.1965.tb14281.x. [DOI] [PubMed] [Google Scholar]
  17. MAYOR H. D., JAMISON R. M., JORDAN L. E., VANMITCHELL M. REOVIRUSES. II. STRUCTURE AND COMPOSITION OF THE VIRION. J Bacteriol. 1965 Jun;89:1548–1556. doi: 10.1128/jb.89.6.1548-1556.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. MCGAVRAN M. H., SMITH M. G. ULTRASTRUCTURAL, CYTOCHEMICAL, AND MICROCHEMICAL OBSERVATIONS ON CYTOMEGALOVIRUS (SALIVARY GLAND VIRUS) INFECTION OF HUMAN CELLS IN TISSUE CULTURE. Exp Mol Pathol. 1965 Feb;76:1–10. doi: 10.1016/0014-4800(65)90019-5. [DOI] [PubMed] [Google Scholar]
  19. MORGAN C., ROSE H. M., HOLDEN M., JONES E. P. Electron microscopic observations on the development of herpes simplex virus. J Exp Med. 1959 Oct 1;110:643–656. doi: 10.1084/jem.110.4.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mayyasi S. A., Schidlovsky G., Bulfone L. M., Buscheck F. T. The coating reaction of the herpes-type virus isolated from malignant tissues with an antibody present in sera. Cancer Res. 1967 Nov;27(11):2020–2024. [PubMed] [Google Scholar]
  21. Mizell M., Stackpole C. W., Halperen S. Herpes-type virus recovery from "virus-free" frog kidney tumors. Proc Soc Exp Biol Med. 1968 Mar;127(3):808–814. doi: 10.3181/00379727-127-32809. [DOI] [PubMed] [Google Scholar]
  22. Nii S., Morgan C., Rose H. M. Electron microscopy of herpes simplex virus. II. Sequence of development. J Virol. 1968 May;2(5):517–536. doi: 10.1128/jvi.2.5.517-536.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Patrizi G., Middelkamp J. N., Reed C. A. Reduplication of nuclear membranes in tissue-culture cells infected with guinea-pig cytomegalovirus. Am J Pathol. 1967 May;50(5):779–790. [PMC free article] [PubMed] [Google Scholar]
  24. ROIZMAN B., ROANE P. R., Jr THE MULTIPLICATION OF HERPES SIMPLEX VIRUS. II. THE RELATION BETWEEN PROTEIN SYNTHESIS AND THE DUPLICATION OF VIRAL DNA IN INFECTED HEP-2 CELLS. Virology. 1964 Feb;22:262–269. doi: 10.1016/0042-6822(64)90011-x. [DOI] [PubMed] [Google Scholar]
  25. Rabin E. R., Jenson A. B. Electron microscopic studies of animal viruses with emphasis on in vivo infections. Prog Med Virol. 1967;9:392–450. [PubMed] [Google Scholar]
  26. Ruebner B. H., Hirano T., Slusser R., Osborn J., Medearis D. N., Jr Cytomegalovirus infection. Viral ultrastructure with particular reference to the relationship of lysosomes to cytoplasmic inclusions. Am J Pathol. 1966 Jun;48(6):971–989. [PMC free article] [PubMed] [Google Scholar]
  27. SALPETER M. M., BACHMANN L. AUTORADIOGRAPHY WITH THE ELECTRON MICROSCOPE. A PROCEDURE FOR IMPROVING RESOLUTION, SENSITIVITY, AND CONTRAST. J Cell Biol. 1964 Aug;22:469–477. doi: 10.1083/jcb.22.2.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. SECHAUD J., RYTER A., KELLENBERGER E. Considérations quantitatives sur des coupes ultraminces de bactéries infectées par un bactériophage. J Biophys Biochem Cytol. 1959 May 25;5(3):469–478. [PMC free article] [PubMed] [Google Scholar]
  29. SMITH K. O. RELATIONSHIP BETWEEN THE ENVELOPE AND THE INFECTIVITY OF HERPES SIMPLEX VIRUS. Proc Soc Exp Biol Med. 1964 Mar;115:814–816. doi: 10.3181/00379727-115-29045. [DOI] [PubMed] [Google Scholar]
  30. Shipkey F. H., Erlandson R. A., Bailey R. B., Babcock V. I., Southam C. M. Virus biographies. II. Growth of herpes simplex virus in tissue culture. Exp Mol Pathol. 1967 Feb;6(1):39–67. doi: 10.1016/0014-4800(67)90005-6. [DOI] [PubMed] [Google Scholar]
  31. Siegert R., Falke D. Elektronenmikroskopische Untersuchungen über die Entwicklung des Herpesvirus hominis in Kulturzellen. Arch Gesamte Virusforsch. 1966;19(2):230–249. [PubMed] [Google Scholar]
  32. Siminoff P., Menefee M. G. Normal and 5-bromodeoxyuridine-inhibited development of herpes simplex virus. An electron microscope study. Exp Cell Res. 1966 Nov-Dec;44(2):241–255. doi: 10.1016/0014-4827(66)90429-0. [DOI] [PubMed] [Google Scholar]
  33. Spring S. B., Roizman B., Schwartz J. Herpes simplex virus products in productive and abortive infection. II. Electron microscopic and immunological evidence for failure of virus envelopment as a cause of abortive infection. J Virol. 1968 Apr;2(4):384–392. doi: 10.1128/jvi.2.4.384-392.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stackpole C. W., Mizell M. Electron microscopic observations on herpes-type virus-related structures in the frog renal adenocarcinoma. Virology. 1968 Sep;36(1):63–72. doi: 10.1016/0042-6822(68)90117-7. [DOI] [PubMed] [Google Scholar]
  35. TOURNIER P., CATHALA F., BERNHARD W. Ultrastructure et développement intracellulaire du virus de la varicelle observé au microscope électronique. Presse Med. 1957 Jun 29;65(52):1229–1234. [PubMed] [Google Scholar]
  36. WATSON D. H., WILDY P., RUSSELL W. C. QUANTITATIVE ELECTRON MICROSCOPY STUDIES ON THE GROWTH OF HERPES VIRUS USING THE TECHNIQUES OF NEGATIVE STAINING AND ULTRAMICROTOMY. Virology. 1964 Dec;24:523–538. doi: 10.1016/0042-6822(64)90204-1. [DOI] [PubMed] [Google Scholar]
  37. WATSON D. H., WILDY P. SOME SEROLOGICAL PROPERTIES OF HERPES VIRUS PARTICLES STUDIED WITH THE ELECTRON MICROSCOPE. Virology. 1963 Sep;21:100–111. doi: 10.1016/0042-6822(63)90308-8. [DOI] [PubMed] [Google Scholar]
  38. Zambernard J., Vatter A. E., McKinnell R. G. The fine structure of nuclear and cytoplasmic inclusions in primary renal tumors of mutant leopard frogs. Cancer Res. 1966 Aug;26(8):1688–1700. [PubMed] [Google Scholar]

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