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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.

The function of CAV-1 in C. elegans was studied by RNA interference (RNAi)12, a powerful method of obtaining phenocopies of C. elegans mutants by RNA injection into hermaphrodites. Treatment with RNAi for cav-1, after which CAV-1 is no longer detectable (data not shown), results in a burst of egg laying by the injected hermaphrodite. One hundred and twelve eggs (s.d. = 3) were laid by injected hermaphrodites ( n = 30) within 36 h after injection of late L4 larvae, compared with 46 eggs laid (s.d. = 2) by control animals (n = 30). Behaviour, morphology and lifespan of injected hermaphrodites are not affected. Embryonic or early larval lethality is observed in a small fraction of the progeny of the injected hermaphrodite 1 to 5 days after injection.

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

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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.

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  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

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  1. Jochen Scheel
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Correspondence to Teymuras V. Kurzchalia.

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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

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