Summary
The ultrastructural morphogenesis of squirrel monkey retrovirus (SMRV) and Mason-Pfizer monkey virus (MPMV) grown in cell culture were compared. Both viruses develop by a process that begins with the formation of intracytoplasmic A particles which are then enveloped at the plasma membrane during budding. SMRV also develops as a crescent-shaped nucleoid beneath a bulging plasma membrane, a development characteristic of type C oncornaviruses. Free extracellular mature SMRV was generally round with a centrally located electron-dense nucleoid enclosed by the viral envelope. In contrast, mature MPMV had a tubular-shaped nucleoid. Negative stained preparations of both viruses yielded head-tail forms with surface projections. By uranyl acetate/critical point drying, SMRV particles were usually round with an eccentric electron-dense nucleoid enclosed by the viral envelope, whereas MPMV particles were round and contained an electron-dense bar-shaped nucleoid. These morphological observations indicate that SMRV more closely resembles MPMV, presently the only member of genus oncornavirus type D, than other retroviruses species. However, since SMRV can be morphologically, biochemically, and immunologically distinguished from MPMV, it represents a new species within genus oncornavirus type D.
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References
Ahmed, M., Schidlovsky, G., Korol, W., Vidrine, G., Cicmanec, J. L.: Occurrence of Mason-Pfizer monkey virus in healthy rhesus monkeys. Cancer Res.34, 3504–3508 (1974).
Ahmed, M., Schidlovsky, G., Larson, D. L., Manousos, M., Mayyasi, S. A.: Detection of type C particles on Mason-Pfizer virus infected cell cultures. J. gen. Virol.30, 11–20 (1976).
Chopra, H. C.: An oncorna-type virus from monkey breast tumor. Prog. med. Virol.22, 104–122 (1976).
Chopra, H. C., Mason, M. M.: A new virus in a spontaneous mammary tumor of a rhesus monkey. Cancer Res.30, 2081–2086 (1970).
Chopra, H. C., Zelljadt, I., Jensen, E. M., Mason, M. M., Woodside, N. J.: Infectivity of cell cultures by a virus isolated from a mammary carcinoma of a rhesus monkey. J. Natl. Cancer Inst.46, 127–137 (1971).
Cohen, A. L., Marlow, D. P., Garner, G. E.: A rapid critical point method using fluorocarbons (“Freons”) as intermediate and transitional fluids. J. Microscopie7, 331–342 (1968).
Dalton, A. J.: Further analysis of the detailed structure of type B and C particles. J. Natl. Cancer Inst.48, 1095–1099 (1972).
Dalton, A. J., Melnick, J. L., Bauer, H., Beaudreau, G., Bentvelzen, P., Bolognesi, D., Gallo, R., Graffi, A., Haguenau, F., Heston, W., Huebner, R., Todaro, G., Heine, U. I.: The case for a family of reverse transcriptase viruses: Retraviridae. Intervirology4, 201–206 (1974).
De Harven, E., Beju, D., Evenson, D. P., Basu, S., Schidlovsky, G.: Structure of critical point dried oncornaviruses. Virology55, 535–540 (1973).
Fenner, F.: The classification and nomenclature of viruses. Intervirology6, 1–12 (1975/76).
Schochetman, G., Fine, D. L., Arthur, L. O., Gilden, R. V., Heberling, R. L.: Biochemical and immunological properties of squirrel monkey retravirus: A new virus isolated from a new world monkey. In:Weinhouse, S., Foti, M., Bergbauer, P. (eds.), 68th Meeting of the American Assoc. for Cancer Research, p. 110. Denver, Colorado, 1977.
Fine, D. L., Schochetman, G., Arthur, L. O., Hartsock, M. H.: Characterization of replication and persistent infection of Mason-Pfizer monkey virus in human rhabdomyosarcoma cells. Submitted (1977).
Giard, D., Aaronson, S. A., Todaro, G. J., Dosik, J. H., Parks, W. P.:In vitro cultivation of human tumors: Establishment of cell lines derived from a series of solid tumors. J. Natl. Cancer Inst.51, 1417–1423 (1973).
Gibbons, I. R., Grimstone, A. V.: On flagellar structure in certain flagellates. J. biophys. biochem. Cytol.7, 697–716 (1960).
Haguenau, F., Beard, J. W.: The avian sarcoma-leukosis complex, its biology and ultrastructure. In:Dalton, A. J., Haguenau, F. (eds.), Tumors Induced by Virus, 1–59. Ultrastructural Studies. New York: Academic Press 1962.
Heberling, R. L., Barker, S. T., Kalter, S. S., Smith, G., Helmke, R. J.: Oncornavirus: Isolation from a squirrel monkey(Saimiri sciureus) lung culture. Science195, 289–292 (1977).
Johnson, R. W., Perry, A., Robinson, O. R., Jr., Shibley, G. P.: Method for reproducible large-volume production and purification of Rauscher murine leukemia virus. Appl. environ. Microbiol.31, 182–188 (1976).
Kawakami, T., Huff, S. D., Buckley, P. M., Dungworth, D. L., Snyder, S. P., Gilden, R. V.: C-type virus associated with gibbon lymphosarcoma. Nature (New Biol.)235, 170–172 (1972).
Kawakami, T. G., Theilen, G. H., Dungworth, D. L., Mann, R. L., Beall, S. G.: “C” type viral particles in plasma of cats with feline leukemia. Science158, 1049–1050 (1967).
Rauscher, F. J.: A virus-induced disease of mice characterized by erythrocytopoesis and lymphoid leukemia. J. Natl. Cancer Inst.29, 515–543 (1962).
Reynolds, E. S.: The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J. Cell Biol.17, 208–212 (1963).
Schochetman, G., Fine, D. L., Arthur, L. O., Gilden, R. V., Heberling, R. L.: Characterization of a retrovirus isolated from squirrel monkeys. J. Virol.23, 384–393 (1977).
Stephens, R., Schidlovsky, G., Kuzmic, S.: The use of “microdiluter” and “ionized” carbon films for negative staining. In:Arcencaux, C. (ed.), Proc. Electron Microscop. Soc. Am., 124–125. Baton Rouge, La.: Claiters 1967.
Theilen, G. H., Gould, D., Fowler, M., Dungworth, D. L.: C-type virus in tumor tissue of a woolly monkey (Lagothrix spp.) with fibrosarcoma. J. Natl. Cancer Inst.47, 881–889 (1971).
Todaro, G. J., Lieber, M. M., Benveniste, R. E., Scherr, C. J., Gibbs, C. J., Gajdusek, D. C.: Infectious primate type C viruses: Three isolates belonging to a new subgroup from the brains of normal gibbons. Virology67, 335–343 (1975).
Todaro, G. J., Sherr, C. J., Benveniste, R. E.: Baboons and their close relatives are unusual among primates in their ability to release nondefective endogenous type C viruses. Virology72, 278–282 (1976).
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Gonda, M.A., Fine, D.L. & Gregg, M. Squirrel monkey retrovirus: Electron microscopy of a virus from new world monkeys and comparison with Mason-Pfizer monkey virus. Archives of Virology 56, 297–307 (1978). https://doi.org/10.1007/BF01315280
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DOI: https://doi.org/10.1007/BF01315280