Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Translational control of InsP3-induced chromatin condensation during the early cell cycles of sea urchin embryos

Nature volume 332, pages 366–369 (1988)Cite this article

Abstract

The cycles of DNA synthesis and chromatin condensation in dividing cells are controlled by signals from the cytoplasm1–3. Changes in the concentration of free calcium (Cai) in the cytoplasm control a variety of cellular functions4 and it has thus been suggested that observed variations in Cai during the cell cycle may be the cytoplas-mic signal that co-ordinates nuclear and cytoplasmic division5–9. We show here that increases in Cai induced by the calcium-releasing second messenger inositol 1,4,5-triphosphate (Ins(l,4,5)P3), or by calcium buffers, cause premature chromatin condensation and breakdown of the nuclear envelope in sea urchin (Lytechinus pictus) early embryos. Both natural and induced chromatin condensation are prevented by calcium chelators. The nucleus becomes sensitive to the Cai signal 45 min after fertilization, but remains insensitive if protein synthesis is prevented. Our experiments demonstrate that Cai regulates the behaviour of the nucleus during the cell cycle, suggest that Ins(l,4,5)P3 is a cell cycle messenger and indicate that there is an interaction between the protein and ionic signals that control the state of chromatin during the cell cycle.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Gurdon, J. B. J. Embryol. exp. Morph. 20, 401–414 (1968).

    CAS  PubMed  Google Scholar 

  2. Rao, P. N. & Johnson, R. T. Nature 225, 159–164 (1970).

    Article  ADS  CAS  Google Scholar 

  3. Masui, H. & Markert, C. L. J. exp. Zool. 117, 129–146 (1971).

    Article  Google Scholar 

  4. Baker, P. F. & Metcalfe, J. C. Br. med. Bull. 42, 341 (1986).

    Article  Google Scholar 

  5. Poenie, M. & Steinhardt, R. A. in Calcium and Cellular Function Vol. 7 (ed. Cheung, M.) 133–157 (Academic, New York, 1987).

    Book  Google Scholar 

  6. Poenie, M., Alderton, J., Tsien, R. Y. & Steinhardt, R. A. Nature 315, 147–149 (1985).

    Article  ADS  CAS  Google Scholar 

  7. Steinhȧrdt, R. A. & Alderton, J. Nature 332, 364–366 (1988).

    Article  ADS  Google Scholar 

  8. Yoshimoto, Y., Iwamatsü, T. & Hiramoto, Y. Biomed. Res. 6, 387–394 (1985).

    Article  CAS  Google Scholar 

  9. Hafner, M. & Petzelt, C. Nature 330, 264–266 (1987).

    Article  ADS  CAS  Google Scholar 

  10. Arndt-Jovin, D. J. & Jovin, T. M. H. Histochem. Cytochem. 25, 585–589 (1977).

    Article  CAS  Google Scholar 

  11. Tsien, R. Y. Biochemistry 19, 2,396–2,404 (1980).

    Article  CAS  Google Scholar 

  12. Arslan, P., Di Virgilio, F., Beltrame, M., Tsien, R. Y. & Pozzan, T. J. biol. Chem. 260, 2,719–2,727 (1985).

    CAS  Google Scholar 

  13. Swann, K. & Whitaker, M. J. J. Cell Biol. 103, 2,333–2,342 (1986).

    Article  CAS  Google Scholar 

  14. Irvine, R. F. Br. med. Bull. 42, 369–374 (1986).

    Article  CAS  Google Scholar 

  15. Woods, N. M., Cuthbertson, K. S. R. & Cobbold, P. H. Nature 319, 600–602 (1986).

    Article  ADS  CAS  Google Scholar 

  16. Wagenaar, E. B. & Mazia, D. in Cell Reproduction (eds Dirksen, E., Prescott, D. & Fox, C. F.) 539–545 (Academic, New York, 1978).

    Book  Google Scholar 

  17. Wagenaar, E. B. Expl Cell Res. 144, 393–403 (1983).

    Article  CAS  Google Scholar 

  18. Grainger, J. L., von Brunn, A. & Winkler, M. M. Devl Biol. 114, 403–415 (1986).

    Article  CAS  Google Scholar 

  19. Evans, T., Rosenthal, E. T., Youngblom, J., Distel, D. & Hunt, T. Cell 33, 389–396 (1983).

    Article  CAS  Google Scholar 

  20. Swenson, K. I., Farell, K. M. & Ruderman, J. V. Cell 47, 861–870 (1986).

    Article  CAS  Google Scholar 

  21. Miake-Lye, R., Newport, J. & Kirschner, M. W. J. Cell Biol. 97, 81–91 (1983).

    Article  CAS  Google Scholar 

  22. Miake-Lye, R. & Kirschner, M. W. Cell 41, 165–175 (1985).

    Article  CAS  Google Scholar 

  23. Suprynowicz, F. A. & Gerace, L. J. Cell Biol. 103, 2,073–2,081 (1986).

    Article  CAS  Google Scholar 

  24. Picard, A. et al. Dev. Growth Different. 29, 93–103 (1987).

    Article  CAS  Google Scholar 

  25. Hutchison, C. J., Cos, R., Drepaul, R. S., Gomperts, B. D. & Ford, C. C. EMBO J. 6, 2,003–2,010 (1987).

    Article  CAS  Google Scholar 

  26. Newport, J. W. & Kirschner, M. W. Cell 37, 731–742 (1984).

    Article  CAS  Google Scholar 

  27. Grynkiewiicz, G., Poenie, M. & Tsien, R. Y. J. biol. Chem. 260, 3,440–3,450 (1985).

    Google Scholar 

Download references

Author information

Author notes

  1. Michael Whitaker: To whom correspondence should be addressed

Authors and Affiliations

  1. Department of Physiology, University College London, Gower Street, London, WC1E6BT, UK

    Jeremy Twigg, Rajnikant Patel & Michael Whitaker

Authors
  1. Jeremy Twigg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rajnikant Patel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Whitaker
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Twigg, J., Patel, R. & Whitaker, M. Translational control of InsP3-induced chromatin condensation during the early cell cycles of sea urchin embryos. Nature 332, 366–369 (1988). https://doi.org/10.1038/332366a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/332366a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing