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.

Involvement of caveolin-1 in meiotic cell-cycle progression in Caenorhabditis elegans

Nature Cell Biology volume 1, pages 127–129 (1999)Cite this article

Small invaginations called caveolae are present on the surface of many cells and are a form of glycosphingolipid- and cholesterol-enriched microdomains or rafts in the plasma membrane1,2. The main component of the caveolar coat is caveolin-1 (refs 3,4), a membrane protein of relative molecular mass (Mr) 21,000 (21K), which binds cholesterol5 and can form high-molecular-mass homo-oligomers resistant to sodium dodecyl sulphate (SDS)6,7. Caveolin-1 has been implicated in signal transduction, but its function remains unclear; whereas overactivation of the p42/44 MAP-kinase cascade was observed after downregulation of caveolin-1 (ref. 8), integrin-mediated activation of the Ras/extracellular-signal-regulated kinase (ERK) pathway9 or conversion of prostate cancer cells to an androgen-insensitive phenotype10 required expression of caveolin-1. To resolve the function of caveolin-1 in intact animals, we analysed caveolin-1 and glycosphingolipid/cholesterol-enriched rafts during the development of the nematode Caenorhabditis elegans. We show that C. elegans caveolin-1 (CAV-1) is expressed in the adult germ line and during embryonic development, and that CAV-1 is essential for Ras/MAP-kinase-dependent progression through the meiotic cell cycle. The function of CAV-1 is dependent on its association with cholesterol-rich membrane microdomains, providing a link between the membrane composition of germ cells and meiotic progression. Our results demonstrate that caveolin-1 and cholesterol-rich microdomains have an essential role in signal transduction in vivo and suggest a model for meiotic progression in the C. elegans germ line.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

Buy

All prices are NET prices.

Figure 1: Expression of CAV-1 in C. elegans.
Figure 2: CAV-1 regulates meiotic progression in C. elegans.

References

  1. Harder, T. & Simons, K. Curr. Opin. Cell Biol. 9, 534–542 (1997).

    Article  CAS  Google Scholar 

  2. Simons, K. & Ikonen, E. Nature 387, 569–572 (1997).

    Article  CAS  Google Scholar 

  3. Parton, R. G. Curr. Opin. Cell Biol. 8, 542–548 (1996).

    Article  CAS  Google Scholar 

  4. Anderson, R. G. W. Annu. Rev. Biochem. 67, 199–225 (1998).

    Article  CAS  Google Scholar 

  5. Murata, M. et al. Proc. Natl Acad. Sci. USA 92, 10339– 10343 (1995).

    Article  CAS  Google Scholar 

  6. Monier, S. et al. Mol. Biol. Cell 6, 911– 927 (1995).

    Article  CAS  Google Scholar 

  7. Sargiacomo, M. et al. Proc. Natl Acad. Sci. USA 92, 9407– 9411 (1995).

    Article  CAS  Google Scholar 

  8. Galbiati, F. et al. EMBO J. 17, 6633–6648 (1998).

    Article  CAS  Google Scholar 

  9. Wary, K. K., Mariotti, A., Zurzolo, C. & Giancotti, F. G. Cell 94, 625–634 ( 1998).

    Article  CAS  Google Scholar 

  10. Nasu, Y. et al. Nature Med. 4, 1062–1064 (1998).

    Article  CAS  Google Scholar 

  11. Tang, Z. et al. J. Biol. Chem. 272, 2437– 2445 (1997).

    Article  CAS  Google Scholar 

  12. Fire, A. et al. Nature 391, 806–811 (1998).

    Article  CAS  Google Scholar 

  13. Church, D. L., Guan, K. L. & Lambie, E. J. Development 121, 2525– 2535 (1995).

    CAS  Google Scholar 

  14. Gumienny, T. L., Lambie, E., Hartwieg, E., Horvitz, H. R. & Hengartner, M. O. Development 126, 1011– 1022 (1999).

    CAS  Google Scholar 

  15. Sternberg, P. W. & Han, M. Trends Genet. 14, 466–472 (1998).

    Article  CAS  Google Scholar 

  16. Friedrichson, T. & Kurzchalia, T. V. Nature 394, 802–805 (1998).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank K. Simons and G. Lewin for critically reading the manuscript; T. Schedl and F. Weth for discussions; and the Caenorhabditis Genetic Center (St Paul, Minnesota, USA) for providing strains.

Correspondence and requests for materials should be addressed to T.V.K.

Author information

Author notes

  1. Jochen Scheel

    Present address: Artemis Pharmaceuticals GmbH, Spemannstrasse 35, 72076, Tübingen, Germany

Authors and Affiliations

  1. Max Planck Institute for Developmental Biology, Spemannstrasse 35, Tübingen, 72076, Germany

    Jochen Scheel, Jagan Srinivasan & Ulrike Honnert

  2. Max Planck Institute for Molecular Cell Biology and Genetics, Dresden, Germany

    Teymuras V. Kurzchalia

  3. Department of Cell Biology, Max-Delbrück Centre for Molecular Medicine, Robert-Rössle Strasse 10, Berlin-Buch, 13092, Germany

    Annemarie Henske & Teymuras V. Kurzchalia

Authors
  1. Jochen Scheel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jagan Srinivasan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ulrike Honnert
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Annemarie Henske
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Teymuras V. Kurzchalia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Teymuras V. Kurzchalia.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Scheel, J., Srinivasan, J., Honnert, U. et al. Involvement of caveolin-1 in meiotic cell-cycle progression in Caenorhabditis elegans. Nat Cell Biol 1, 127–129 (1999). https://doi.org/10.1038/10100

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/10100

This article is cited by

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