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Regulation of cellular responsiveness to inductive signals in the developing C. elegans nervous system

Abstract

IN Caenorhabditis elegans, cell–cell communication is required to form a simple pattern of sensory ray neurons and cuticular structures (alae). The C. elegans pal-1 gene initiates one developmental pathway (ray lineages) simply by blocking a cell–cell interaction that induces an alternative pathway1. Here we show by mosaic analysis that pal-l+ acts by preventing specific cells from responding to inductive signals. The results indicate that although cell signals play a critical role in generating this pattern, they do not provide spatial information. Instead, signals are sent to many, if not all, of the precursor cells, and the ability to respond is spatially restricted. This patterning strategy thus differs from many well known models for pattern formation in which localized inductive signals influence a subset of cells within a field. We find that pal-1 encodes a homeodomain protein and so is likely to regulate transcription. The pal-l+ protein could block the response to cell signals either by repressing genes involved in signal transduction or by acting directly on downstream genes in a way that neutralizes the effects of the intercellular signals. Genetic experiments indicate that one candidate for such a downstream gene is the Antennapedia-like homeotic selector gene mab-5.

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References

  1. Waring, D. A. & Kenyon, C. Cell 60, 123–131 (1990).

    Article  CAS  Google Scholar 

  2. Sulston, J. & Horvitz, H. R. Devl. Biol. 56, 110–156 (1977).

    Article  CAS  Google Scholar 

  3. Sulston, J. & White, J. Devl. Biol. 78, 577–597 (1980).

    Article  CAS  Google Scholar 

  4. Kenyon, C. Cell 46, 477–487 (1986).

    Article  CAS  Google Scholar 

  5. Austin, J. & Kimble, J. Cell 51, 589–599 (1987).

    Article  CAS  Google Scholar 

  6. Costa, M., Weir, M., Coulson, A., Sulston, J. & Kenyon, C. Cell 55, 747–756 (1988).

    Article  CAS  Google Scholar 

  7. Horvitz, H., Sternberg, P., Greenwald, I., Fixsen, W. & Ellis, H. Cold Spring Harb. Symp. quant. Biol. 48, 453–463 (1983).

    Article  Google Scholar 

  8. Hedgecock, E., Culotti, J., Hall, D. & Stern, B. Development 100, 365–382 (1987).

    CAS  PubMed  Google Scholar 

  9. Sulston, J., Schierenberg, E., White, J. & Thomson, J. Devl. Biol. 100, 64–119 (1983).

    Article  CAS  Google Scholar 

  10. Rosenbluth, R., Cuddeford, C. & Baillie, D. Genetics 109, 493–511 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Burglin, T. R., Finney, M., Coulson, A. & Ruvkun, G. Nature 341, 239–243 (1989).

    Article  ADS  CAS  Google Scholar 

  12. Scott, M. P. & Carroll, S. B. Cell 51, 689–698 (1987).

    Article  CAS  Google Scholar 

  13. Fire, A. EMBO J. 5, 2673–2680 (1986).

    Article  CAS  Google Scholar 

  14. Krause, M. & Hirsh, D. Cell 49, 753–761 (1987).

    Article  CAS  Google Scholar 

Download references

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Waring, D., Kenyon, C. Regulation of cellular responsiveness to inductive signals in the developing C. elegans nervous system. Nature 350, 712–715 (1991). https://doi.org/10.1038/350712a0

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