1887

Abstract

Summary

Frog virus 3 (FV3) assembles in morphologically distinct assembly sites in the cytoplasm of infected cells. As the assembly sites form, the intermediate filaments (IF) aggregate, delimit the assembly sites, and remain so throughout infection. To determine the molecular basis of reorganization of IF, we analysed the vimentin of uninfected and FV3-infected cells by two-dimensional gel electrophoresis. The results showed that (i) the vimentin was more acidic in FV3-infected cells than in uninfected cells, (ii) the acidification of vimentin in FV3-infected cells was possibly due to a fourfold increase in phosphorylation, and (iii) the phosphorylation of vimentin preceded the reorganization of IF around virus assembly sites. A temperature-sensitive mutant of FV3 (9467), which at the non-permissive temperature neither reorganized IF nor formed assembly sites, failed to increase the phosphorylation of vimentin. Together, the above results suggest that changes in phosphorylation may modulate IF organization and that changes in IF organization are required for FV3 assembly site formation.

Keyword(s): assembly , FV3 and intermediate filaments
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-67-5-915
1986-05-01
2024-12-06
Loading full text...

Full text loading...

/deliver/fulltext/jgv/67/5/JV0670050915.html?itemId=/content/journal/jgv/10.1099/0022-1317-67-5-915&mimeType=html&fmt=ahah

References

  1. Aubin J., Osborn M., Franke W. W., Weber K. 1980; Intermediate filaments of the vimentin-type and the cytokeratin-type are distributed differently during mitosis. Experimental Cell Research 129:149–165
    [Google Scholar]
  2. Ben-Zeev A., Farmer S. R., Penman S. 1979; Mechanisms regulating tubulin synthesis in cultured mammalian cells. Cell 17:319–325
    [Google Scholar]
  3. Blose S. H. 1979; Ten-nanometer filaments and mitosis: maintenance of structural continuity in dividing endothelial cells. Proceedings of the National Academy of Sciences, U.S.A. 76:3372–3376
    [Google Scholar]
  4. Blose S. H., Chacko S. 1976; Rings of intermediate (100A) filament bundles in the perinuclear region of vascular endothelial cells. Journal of Cell Biology 70:459–466
    [Google Scholar]
  5. Brown S., Levinson W., Spudich J. A. 1976; Cytoskeletal elements of chick embryo fibroblasts revealed by detergent extraction. Journal of Supramolecular Structure 5:119–130
    [Google Scholar]
  6. Cabral F., Gottesman M. M. 1979; Phosphorylation of the 10 nm filament from Chinese hamster ovary cells. Journal of Biological Chemistry 254:6203–6206
    [Google Scholar]
  7. Darlington R. W., Granoff A., Breeze D. C. 1966; Viruses and renal carcinoma of Rana pipiens. II. Ultrastructural studies and sequential development of virus isolated from normal and tumor tissue. Virology 29:149–156
    [Google Scholar]
  8. Evans R. M., Fink L. M. 1982; An alteration in the phosphorylation of vimentin-type intermediate filaments is associated with mitosis in cultured mammalian cells. Cell 29:43–52
    [Google Scholar]
  9. Franke W. W., Schmid E., Osborn M., Weber K. 1978; Different intermediate-sized filaments distinguished by immunofluorescence microscopy. Proceedings of the National Academy of Sciences, V.S.A 75:5034–5038
    [Google Scholar]
  10. Gard D. L., Lazarides E. 1982; Cyclic AMP-modulated phosphorylation of intermediate filament proteins in cultured avian myogenic cells. Molecular and Cellular Biology 2:1104–1114
    [Google Scholar]
  11. Goldman R., Knipe D. 1973; The functions of cytoplasmic fibers in non-muscle cell motility. Cold Spring Harbor Symposia on Quantitative Biology 37:523–534
    [Google Scholar]
  12. Granger B., Lazarides E. 1978; The existence of an insoluble Z disc scaffold in chicken skeletal muscle. Cell 15:1253–1268
    [Google Scholar]
  13. Granger B., Lazarides E. 1979; Desmin and vimentin coexist at the periphery of the myofibril Z disc. Cell 18:1053–1063
    [Google Scholar]
  14. Hynes R. O., Destree A. T. 1978; 10 nm filaments in normal and transformed cells. Cell 13:151–163
    [Google Scholar]
  15. Krebs E. G., Beavo J. A. 1979; Phosphorylation-dephosphorylation of enzymes. Annual Review of Biochemistry 48:923–959
    [Google Scholar]
  16. Lazarides E. 1980; Intermediate filaments as mechanical integrators of cellular space. Nature, London 283:249–256
    [Google Scholar]
  17. Lazarides E. 1982; Intermediate filaments: a chemically heterogeneous, developmentally regulated class of proteins. Annual Review of Biochemistry 51:219–254
    [Google Scholar]
  18. Murti K. G., Goorha R. 1983; Interaction of frog virus 3 with the cytoskeleton. I. Altered organization of microtubules, intermediate filaments, and microfilaments. Journal of Cell Biology 96:1248–1257
    [Google Scholar]
  19. Murti K. G., Porter K. R., Goorha R., Ulrich M., Wray G. 1984; Interaction of frog virus 3 with the cytomatrix. II. Structure and composition of the virus assembly site. Experimental Cell Research 154:270–282
    [Google Scholar]
  20. Murti K. G., Chen M., Goorha R. 1985; Interaction of frog virus 3 with the cytomatrix. III. Role of microfilaments in virus release. Virology 142:317–325
    [Google Scholar]
  21. Naegele R. F., Granoff A. 1971; Viruses and renal carcinoma of Rana pipiens. XI. Isolation of FV3 temperature-sensitive mutants; complementation and genetic recombination. Virology 44:286–295
    [Google Scholar]
  22. O’connor C. M., Balzar D. R., Lazarides E. 1979; Phosphorylation of subunit proteins of intermediate filaments from chicken muscle and nonmuscle cells. Proceedings of the National Academy of Sciences, U. S. A 76:819–823
    [Google Scholar]
  23. O’Farrell P. H. 1975; High resolution two-dimensional electrophoresis of proteins. Journal of Biological Chemistry 250:4007–4021
    [Google Scholar]
  24. Robinson L. S., Nelkin B., Kaufmann S., Vogelstein B. 1981; Increased phosphorylation rate of intermediate filaments during mitotic arrest. Experimental Cell Research 133:445–449
    [Google Scholar]
  25. Silberstein H., August J. T. 1973; Phosphorylation of animal virus proteins by a virion protein kinase. Journal of Virology 12:511–522
    [Google Scholar]
  26. Silberstein H., August J. T. 1976; Characterization of virion protein kinase as a virus-specified enzyme. Journal of Biological Chemistry 251:3185–3190
    [Google Scholar]
  27. Spruill W. A., Steiner A. L., Tres L. L., Kierszenbaum A. 1983a; Follicle-stimulating hormone-dependent phosphorylation of vimentin in cultures of rat Sertoli cells. Proceedings of the National Academy of Sciences, U.S.A 80:993–997
    [Google Scholar]
  28. Spruill W. A., Zysk J. R., Tres L. L., Kierszenbaum A. 1983b; Calcium/calmodulin-dependent phosphorylation of vimentin in rat Sertoli cells. Proceedings of the National Academy of Sciences, U. S. A. 80:760–764
    [Google Scholar]
  29. Starger J., Goldman R. 1977; Isolation and preliminary characterization of 10 nm filaments from baby hamster kidney (BHK-21) cells. Proceedings of the National Academy of Sciences, U.S.A. 74:2422–2426
    [Google Scholar]
  30. Starger J. M., Brown W. E., Goldman A. E., Goldman R. D. 1978; Biochemical and immunological analysis of rapidly purified l0 nm filaments from baby hamster kidney (BHK-21) cells. Journal of Cell Biology 78:93–109
    [Google Scholar]
  31. Willis D. B., Goorha R., Granoff A. 1979; Macromolecular synthesis in cells infected by frog virus 3. XI. A ts mutant of frog virus 3 that is defective in late transcription. Virology 98:328–335
    [Google Scholar]
  32. Zieve G. W., Heidemann S. R., Mcintosh J. R. 1980; Isolation and partial characterization of a cage of filaments that surrounds the mammalian mitotic spindle. Journal of Cell Biology 87160–169
    [Google Scholar]
/content/journal/jgv/10.1099/0022-1317-67-5-915
Loading
/content/journal/jgv/10.1099/0022-1317-67-5-915
Loading

Data & Media loading...

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