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Autoregulation of tubulin synthesis in enucleated cells

Nature volume 317, pages 648–651 (1985)Cite this article

Abstract

The effects on tubulin messenger RNA levels and tubulin protein synthesis of treating cells with microtubule-depolymerizing drugs or directly microinjecting cells with tubulin have suggested that non-polymerized tubulin depresses its own synthesis1–4. The precise level of this control is unclear. It has been shown that enucleated cells, termed cytoplasts, retain many properties of the original cell, including maintenance of cell shape, pinocytic activity and locomotion5 as well as biosynthetic activities such as protein synthesis6,7 and replication of cytoplasmic viruses8. Furthermore, cytoplasts retain most of the components of the cytoskeleton including the centrioles5,9. If cytoplasmic activities alone are responsible for regulating tubulin biosynthesis, cytoplasts should contain the necessary components. To distinguish between regulation which would occur in the nucleus, that is, alterations in mRNA synthesis or modifications of the mRNA, from alterations in mRNA stability and/or translatability which would take place in the cytoplasm, we examined the autoregulation of tubulin synthesis in enucleated cells. Here, we report that enucleated mouse fibroblasts retain the ability to turn off tubulin protein synthesis in response to microtubule depolymerization, the reduction in tubulin synthesis being accompanied by a corresponding decrease in tubulin mRNA levels. Thus, transcription, processing and transport of tubulin mRNA from the nucleus are not likely to be the loci of regulation. Instead, tubulin must reduce, either directly or indirectly, the translatability of its own mRNA.

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References

  1. Ben-Ze'ev, A., Farmer, S. R. & Penman, S. Cell 17, 319–325 (1979).

    Article  CAS  Google Scholar 

  2. Cleveland, D. W., Lopata, M. A., Sherline, P. & Kirschner, M. W. Cell 25, 537–546 (1981).

    Article  CAS  Google Scholar 

  3. Caron, J. M., Jones, A. L. & Kirschner, M. W. J. Cell Biol. (in the press).

  4. Cleveland, D. W., Pittenger, M. F. & Feramisco, J. R. Nature 305, 738–740 (1983).

    Article  ADS  CAS  Google Scholar 

  5. Goldman, R. D., Pollack, R. & Hopkins, N. H. Proc. natn. Acad. Sci. U.S.A. 70, 750–754 (1973).

    Article  ADS  CAS  Google Scholar 

  6. Prescott, D. M., Meyerson, D. & Wallace, J. Expl Cell Res. 71, 480–485 (1972).

    Article  CAS  Google Scholar 

  7. Bruno, J. & Lucas, J. J. Cell Biol. int. Rep. 7, 651–659 (1983).

    Article  CAS  Google Scholar 

  8. Pollack, R. & Goldman, R. Science 179, 915–916 (1973).

    Article  ADS  CAS  Google Scholar 

  9. Karsenti, E., Kobayashi, S., Mitchison, T. & Kirschner, M. W. J. Cell Biol. 98, 1763–1776 (1984).

    Article  CAS  Google Scholar 

  10. Caron, J. M., Stimac, E. & Kirschner, M. W. J. Cell Biol. 99, 441a (1984).

    Google Scholar 

  11. Cleveland, D. W. & Havercroft, J. C. J. Cell Biol. 97, 919–924 (1983).

    Article  CAS  Google Scholar 

  12. Lau, J. T. Y., Pittenger, M. F. & Cleveland, D. W. Molec. cell. Biol. 5, 1611–1620 (1985).

    Article  CAS  Google Scholar 

  13. Rice, A. P. & Roberts, B. E. J. Virol. 47, 529–539 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Russell, M., Gold, L., Morrissett, H. & O'Farrell, P. Z. J. biol. Chem. 251, 7263–7270 (1976).

    Google Scholar 

  15. Fulford, W. & Model, P. J. molec. Biol. 173, 211–226 (1984).

    Article  CAS  Google Scholar 

  16. Fallon, A. M., Jinks, C. S., Strycharz, G. D. & Nomura, M. Proc. natn. Acad. Sci. U.S.A. 76, 3411–3415 (1979).

    Article  ADS  CAS  Google Scholar 

  17. Gourse, R. L., Takebe, Y., Sharrock, R. A. & Nomura, M. Proc. natn. Acad. Sci. U.S.A. 82, 1069–1073 (1985).

    Article  ADS  CAS  Google Scholar 

  18. Pearson, N. J., Fried, H. M. & Warner, J. R. Cell 29, 347–355 (1982).

    Article  CAS  Google Scholar 

  19. Warner, J. R. J. molec. Biol. 115, 315–333 (1977).

    Article  CAS  Google Scholar 

  20. Krauter, K. S., Soeiro, R. & Nadal-Ginard, B. J. molec. Biol. 142, 145–159 (1980).

    Article  CAS  Google Scholar 

  21. Osley, M. A. & Hereford, L. M. Cell 24, 377–384 (1981).

    Article  CAS  Google Scholar 

  22. Stimac, E., Groppi, V. E. & Coffino, P. Molec. cell. Biol. 4, 2082–2090 (1984).

    Article  CAS  Google Scholar 

  23. Luscher, B., Stauber, C., Schindler, R. & Schuperli, D. Proc. natn. Acad. Sci. U.S.A. 82, 4389–4393 (1985).

    Article  ADS  CAS  Google Scholar 

  24. Thimmappaya, B., Weinberger, C., Scheider, R. J. & Shenk, T. Cell 31, 543–551 (1982).

    Article  CAS  Google Scholar 

  25. Kaufman, R. J. Proc. natn. Acad. Sci. U.S.A. 82, 689–693 (1985).

    Article  ADS  CAS  Google Scholar 

  26. Lindquist, S. Nature 293, 311–314 (1981).

    Article  ADS  CAS  Google Scholar 

  27. Scott, M. P. & Pardue, M. L. Proc. natn. Acad. Sci. U.S.A. 78, 3353–3357 (1981).

    Article  ADS  CAS  Google Scholar 

  28. Kirk, M. M. & Kirk, D. L. Cell 41, 419–428 (1985).

    Article  CAS  Google Scholar 

  29. Cordell, B. et al. Cell 31, 531–542 (1982).

    Article  CAS  Google Scholar 

  30. Rosenthal, E. T., Brandhorst, B. P. & Ruderman, J. V. Devl Biol. 91, 215–220 (1982).

    Article  CAS  Google Scholar 

  31. Chirgwin, J. M., Przbyla, A. E., MacDonald, R. J. & Rutter, W. J. Biochemistry 18, 5294–5299 (1979).

    Article  CAS  Google Scholar 

  32. Rall, L. B. et al. Nature 313, 228–231 (1985).

    Article  ADS  CAS  Google Scholar 

  33. Cleveland, D. W. et al. Cell 20, 95–105 (1980).

    Article  CAS  Google Scholar 

  34. Spiegelman, B. M., Frank, M. & Green, H. J. biol. Chem. 258, 10083–10089 (1983).

    CAS  PubMed  Google Scholar 

  35. Boedtker, H. Biochim. biophys. Acta 240, 448–453 (1971).

    Article  CAS  Google Scholar 

  36. Thomas, P. S. Proc. natn. Acad. Sci. U.S.A. 77, 5201–5205 (1980).

    Article  ADS  CAS  Google Scholar 

  37. Lipsich, L. A., Lucas, J. J. & Kates, J. R. J. cell. Physiol. 97, 199–208 (1978).

    Article  CAS  Google Scholar 

  38. Firestone, G. L., Payvar, F. & Yamamoto, K. R. Nature 300, 221–225 (1982).

    Article  ADS  CAS  Google Scholar 

  39. Laemmli, U. K. Nature 227, 680–685 (1970).

    Article  ADS  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Intestinal Immunology Research Center, Cell Biology Section, 151E, Veterans Administration Medical Center, 4150 Clement Street, San Francisco, California, 94121

    Joan M. Caron, Albert L. Jones, Leslie B. Rall & M. W. Kirschner

  2. Departments of Medicine and Anatomy, University of California, San Francisco, 94143, USA

    Joan M. Caron & Albert L. Jones

  3. Department of Biochemistry, University of California, San Francisco, 94143, USA

    M. W. Kirschner

  4. Chiron Research Laboratories, Chiron Corporation, Emeryville, California, 94608, USA

    Leslie B. Rall

Authors
  1. Joan M. Caron
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  2. Albert L. Jones
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  3. Leslie B. Rall
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  4. M. W. Kirschner
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Caron, J., Jones, A., Rall, L. et al. Autoregulation of tubulin synthesis in enucleated cells. Nature 317, 648–651 (1985). https://doi.org/10.1038/317648a0

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