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Ultrastructural studies on the replication of herpes virus ateles-73 in owl monkey kidney cells

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Summary

The replicative cycle ofherpesvirus ateles, strain 73 (HVA-73), was examined in the electron microscope and compared to that of other herpesviruses known to be oncogenic. A relatively slow replicative cycle of HVA-73 in owl monkey kidney (OMK) cells allowed us to distinguish cytoplasmic and nuclear stages of replication, comprising virus uptake, transport, maturation, and extrusion. Virus uptake was observed within 10 hours of infection and occurred both as a result of fusion between virus and cell membranes and by phagocytosis. Morphologic evidence for the transfer of viral DNA from nuclecapsids to the nucleus at the nuclear membrane is presented. This is shown by the location of numerous empty capsids in front of nuclear pores early during infection. Towards the end of the eclipse phase, at about 48 hours after infection, two different types of nuclear inclusion bodies were observed. Progeny nucleocapsids were detected in the nucleus at the same time. The envelopment of nucleocapsids occurred both at the nuclear membrane and at proliferating Golgi lamellae in the cytoplasm. Each site of envelopment is associated with the maturation of a characteristic, morphologically distinguishable virus particle. The assembly of HVA-73 resembled that of other oncogenic herpesviruses.

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References

  1. Ablashi, D. V., Easton, J. M., Guegan, J. H.: Herpesviruses and cancer in man and subhuman primates. Biomedicine24, 286–305 (1976).

    Google Scholar 

  2. Ablashi, D. V., Easton, J. M.: Oncogenic DNA viruses: Experimental animals andin vitro systems for propagation, assay, transformation and tumor induction. Proc. Int. Symp. on Exptl. AnimalsIn Vitro Systems in Med. Microbiol., Munich, W. Germany, 106–160. Munich: Uni-Druck 1977.

    Google Scholar 

  3. Ablashi, D. V., Pearson, G., Rabin, H., Armstrong, G., Easton, J., Valerio, M., Cicmanec, J.: Experimental infection ofcallithrix jaccus marmosets withHerpesvirus saimiri, Herpesvirus ateles and Epstein-Barr virus. Biomedicine23, 7–10 (1978).

    Google Scholar 

  4. Ahmed, M., Schidlovsky, G.: Electron microscopic localization of herpesvirustype particles in Marek's disease. J. Virol.2, 1443–1457 (1968).

    Google Scholar 

  5. Cook, M. L., Stevens, J. G.: Labile Coat: Reason for noninfectious cell-free Varizella-Zoster virus in culture. J. Virol.2, 1458–1464 (1968).

    Google Scholar 

  6. Dalton, A. J.: A chrome osmium fixative for electron microscopy. Anat. Rec.121, 281 (1955).

    Google Scholar 

  7. Deinhardt, F., Falk, L., Wolfe, L.: Simian herpesviruses. Cancer Res.33, 1424–1426 (1973).

    Google Scholar 

  8. Falk, L., Wright, J., Wolfe, L., Deinhardt, F.:Herpesvirus ateles: transformationin vitro of marmoset splenic lymphocytes. Int. J. Cancer14, 244–251 (1974).

    Google Scholar 

  9. Falk, L. A., Nigida, S. M., Deinhardt, F., Wolfe, L. G., Cooper, R. W., Hernandez-Camacho, J. I.:Herpesvirus ateles: properties of an oncogenic herpesvirus isolated from circulating lymphocytes of spider monkeys (ateles sp.). Int. J. Cancer14, 473–482 (1974).

    Google Scholar 

  10. Friedman, A., Coward, J. E., Rosenkranz, H. S., Morgan, C.: Electron microscopic studies on the assembly of herpes simplex virus upon removal of hydroxy urea block. J. gen. Virol.26, 171–181 (1975).

    Google Scholar 

  11. Friedman, A., Coward, J. E., Morgan, C.: Electron microscopic study of the development ofherpesvirus saimiri. Virology69, 810–815 (1976).

    Google Scholar 

  12. Haguenau, F., Michelson-Fiske, S.: Cytomegalovirus: Nucleocapsid assembly and core structure. Intervirology5, 293–299 (1975).

    Google Scholar 

  13. Heine, U., Ablashi, D. V.: Morphological studies ofHerpesvirus saimiri in primate cell cultures. J. med. Primatology3, 18–26 (1974).

    Google Scholar 

  14. Heine, U., Ablashi, D. V., Armstrong, G. R.: Morphological studies onherpesvirus saimiri in subhuman and human cell cultures. Cancer Res.31, 1019–1029 (1971).

    Google Scholar 

  15. Heine, U., Cottler-Fox, M.: Electron microscopic observations on the composition of herpes-type virions. In:de Thé, G., Epstein, M. A., zur Hausen, H. (eds.), Oncogenesis and Herpesviruses II, Part I, 103–110. Lyon: IARDC 1975.

    Google Scholar 

  16. Heine, U. I., Dalton, A. J.: Ultrastructural analysis of herpes-type viruses. In: Molecular Studies in Viral Neoplasia (25th Ann. Symposium on Fundamental Cancer Research, 1972, The University of Texas M.D. Anderson Hospital and Tumor Institute at Houston), 63–96. Baltimore, Md.: The Williams and Wilkins Co. 1974.

    Google Scholar 

  17. Heine, U., Hinze, H. C.: Morphological studies onherpesvirus sylvilagus in rabbit kidney cell cultures. Cancer Res.32, 1340–1350 (1972).

    Google Scholar 

  18. Hummeler, K., Tomassini, N., Zajac, B.: Early events in herpes simplex virus infection: a radioautographic study. J. Virol.4, 67–74 (1969).

    Google Scholar 

  19. Hunt, R. D., Meléndez, L. V., King, N. W., Gilmore, C. E., Daniel, M. D., Williamson, M. E., Jones, T. C.: Morphology of a disease with features of malignant lymphoma in marmosets and owl monkeys inoculated withHerpesvirus saimiri. J. Natl. Cancer Inst.44, 447–465 (1970).

    Google Scholar 

  20. Luetzeler, J., Heine, U.: Nuclear accumulation of filamentous herpes simplex virus DNA late during the replicative cycle. Intervirology10, 289–299 (1978).

    Google Scholar 

  21. Melendez, L. V., Hunt, R. D., King, N. W., Barahone, H. H., Daniel, M. D., Fraser, C. E. O., Garcia, F. G.: A new lymphoma virus of monkeys:Herpesvirus ateles. Nature (New Biology)234, 182–184 (1972).

    Google Scholar 

  22. Miyamoto, K., Morgan, C.: Structure and development of viruses as observed in the electron microscope. XI. Entry and uncoating of herpes simplex virus. J. Virol.8, 910–918 (1971).

    Google Scholar 

  23. Morgan, C., Rose, H. M., Mednis, B.: Electron microscopy of herpes simplex virus. I. Entry. J. Virol.2, 507–516 (1968).

    Google Scholar 

  24. Morgan, G. D., Achong, B. G., Epstein, M. A.: Morphological observations on the replication ofherpesvirus saimiri in monkey cell cultures. J. gen. Virol.32, 461–470 (1976).

    Google Scholar 

  25. Nazerian, K., Lee, L. F., Witter, R. L., Burmester, B. R.: Ultrastructural studies of a herpesvirus of turkeys antigenically related to Marek's disease virus. Virology43, 442–452 (1971).

    Google Scholar 

  26. Perdue, M. L., Cohen, J. C., Randall, C. C., O'Callaghan, D. J.: Biochemical studies of the maturation of herpesvirus nucleocapsid species. Virology74, 194–208 (1976).

    Google Scholar 

  27. Seigneurin, J.-M., Vuillaume, M., Lenoir, G., de Thé, G.: Replication of Epstein-Barr virus: ultrastructural and immunofluorescent studies of P3HR1-super-infected Raji cells. J. Virol.24, 836–845 (1977).

    Google Scholar 

  28. Smith, J. D., de Harven, E.: Herpes simplex virus and human cytomegalovirus replication in WI38 cells. II. An ultrastructural study of viral penetration. J. Virol.14, 945–956 (1974).

    Google Scholar 

  29. Stackpole, C. W.: Herpestype virus of the frog renal adenocarcinoma. I. Virus development in tumor transplants maintained at low temperature. J. Virol.4, 75–93 (1969).

    Google Scholar 

  30. Tralka, T. S., Costa, J., Rabson, A.: Electron microscopic study ofherpesvirus saimiri. Virology80, 158–165 (1977).

    Google Scholar 

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Authors and Affiliations

  1. Immunopathology Section, University of Cologne, Germany

    J. Luetzeler

  2. Department of Otorhinolaryngology, University of Malaya, Kuala Lumpur, Malaysia

    U. Prasad

  3. Laboratory of Viral Carcinogenesis and Laboratory of DNA Tumor Viruses, National Cancer Institute, Bethesda, Maryland, USA

    J. Luetzeler, Ursula I. Heine, E. Wendel, U. Prasad & D. V. Ablashi

  4. Ultrastructural Studies Section, LVC, National Cancer Institute, National Institutes of Health, Building 37, Room 1C-15, 20014, Bethesda, MD, USA

    Ursula I. Heine

Authors
  1. J. Luetzeler
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  2. Ursula I. Heine
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  3. E. Wendel
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  4. U. Prasad
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  5. D. V. Ablashi
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Luetzeler, J., Heine, U.I., Wendel, E. et al. Ultrastructural studies on the replication of herpes virus ateles-73 in owl monkey kidney cells. Archives of Virology 60, 59–73 (1979). https://doi.org/10.1007/BF01318098

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  • DOI: https://doi.org/10.1007/BF01318098

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