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.

  • Review Article
  • Published:

Multiple intercellular signalling systems control the development of the Caenorhabditis elegans vulva

Abstract

Developmental, genetic and molecular studies indicate that multiple intercellular signalling systems interact to specify the types and spatial patterns of cells generated during the formation of the vulva of the nematode Caenorhabditis elegans. Two classes of evolutionary conserved transmembrane receptors and a Ras protein function in these signalling systems. The biology of vulval development provides a framework for understanding how cell interactions control the development of animals as diverse as nematodes, insects and mammals.

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

Access options

Buy this article

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

Similar content being viewed by others

References

  1. Wood, W. B. et al. in The Nematode Caenorhabditis elegans (Cold Spring Harbor Laboratory, New York, 1988).

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  4. Sternberg, P. W. & Horvitz, H. R. Cell 44, 761–772 (1986).

    Article  CAS  Google Scholar 

  5. Thomas, J., Stern, M. & Horvitz, H. R. Cell 62, 1041–1052 (1990).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. White, J. G. in The Nematode Caenorhabditis elegans (eds Wood, W. B. et al.) (Cold Spring Harbor Laboratory, New York, 1988).

    Google Scholar 

  8. Li, C. & Chalfie, M. Neuron 4, 681–695 (1990).

    Article  CAS  Google Scholar 

  9. Kimble, J. Devl Biol. 87, 286–300 (1981).

    Article  CAS  Google Scholar 

  10. Ferguson, E. & Horvitz, H. R. Genetics 110, 17–72 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Ferguson, E., Sternberg, P. W. & Horvitz, H. R. Nature 326, 259–267 (1987).

    Article  ADS  CAS  Google Scholar 

  12. Herman, R. K. & Hedgecock, E. M. Nature 348, 169–171 (1990).

    Article  ADS  CAS  Google Scholar 

  13. Herman, R. K. Genetics 108, 165–180 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Sternberg, P. W. Nature 335, 551–554 (1988).

    Article  ADS  CAS  Google Scholar 

  15. Han, M., Aroian, R. & Sternberg, P. W. Genetics 126, 899–913 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Horvitz, H. R. & Sulston, J. E. Genetics 96, 435–454 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Sulston, J. E. & Horvitz, H. R. Devl Biol. 82, 41–55 (1981).

    Article  CAS  Google Scholar 

  18. Greenwald, I. S., Sternberg, P. W. & Horvitz, H. R. Cell 34, 435–444 (1983).

    Article  CAS  Google Scholar 

  19. Ferguson, E. & Horvitz, H. R. Genetics 123, 109–121 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Kim, S. & Horvitz, H. R. Genes Dev. 4, 357–371 (1990).

    Article  CAS  Google Scholar 

  21. Beitel, G., Clark, S. & Horvitz, H. R. Nature 348, 503–509 (1990).

    Article  ADS  CAS  Google Scholar 

  22. Han, M. & Sternberg, P. W. Cell 63, 921–993 (1990).

    Article  CAS  Google Scholar 

  23. Barbacid, M. A. Rev. Biochem. 56, 779–827 (1987).

    Article  CAS  Google Scholar 

  24. Toda, T. et al. Cell 40, 27–36 (1985).

    Article  CAS  Google Scholar 

  25. Downward, J., Graves, J., Warne, P., Rayter, S. & Cantrell, D. Nature 346, 719–723 (1990).

    Article  ADS  CAS  Google Scholar 

  26. Bourne, H. R., Sanders, D. A. & McCormick, F. Nature 348, 125–132 (1990).

    Article  ADS  CAS  Google Scholar 

  27. Aroian, R., Koga, M., Mendel, J., Ohshima, Y. & Sternberg, P. W. Nature 348, 693–699 (1990).

    Article  ADS  CAS  Google Scholar 

  28. Ullrich, A. & Schlessinger, J. Cell 61, 203–212 (1990).

    Article  CAS  Google Scholar 

  29. Schupbach, T. Cell 49, 699–707 (1987).

    Article  CAS  Google Scholar 

  30. Price, J., Clifford, R. & Schupbach, T. Cell 56, 1085–1092 (1989).

    Article  CAS  Google Scholar 

  31. Schejter, E. & Shilo, B.-Z. Cell 56, 1093–1104 (1989).

    Article  CAS  Google Scholar 

  32. Baker, N. & Rubin, G. Nature 340, 150–153 (1989).

    Article  ADS  CAS  Google Scholar 

  33. Sternberg, P. W. & Horvitz, H. R. Cell 58, 679–693 (1989).

    Article  CAS  Google Scholar 

  34. Seydoux, G. & Greenwald, I. S. Cell 57, 1237–1245 (1989).

    Article  CAS  Google Scholar 

  35. Greenwald, L. S. Cell 43, 583–590 (1985).

    Article  CAS  Google Scholar 

  36. Yochem, J., Weston, K. & Greenwald, I. S. Nature 335, 547–550 (1988).

    Article  ADS  CAS  Google Scholar 

  37. Andrews, B. & Herskowitz, I. J. biol. Chem. 265, 14057–14060 (1990).

    CAS  PubMed  Google Scholar 

  38. Lux, S., John, K. & Bennett, W. Nature 344, 36–42 (1990).

    Article  ADS  CAS  Google Scholar 

  39. Greenwald, I. S. Trends Genet. 5, 237–241 (1989).

    Article  CAS  Google Scholar 

  40. Greenspan, R. New Biol. 2, 595–600 (1990).

    CAS  PubMed  Google Scholar 

  41. Coffmann, C., Harris, W. & Kintner, C. Science 249, 1438–1441 (1990).

    Article  ADS  Google Scholar 

  42. Kidd, S., Maylies, M., Gasic, G. & Young, M. Genes Dev. 3, 1113–1129 (1989).

    Article  CAS  Google Scholar 

  43. Fehon, R. et al. Cell 61, 523–534 (1990).

    Article  CAS  Google Scholar 

  44. Greenwald, I. S. & Seydoux, G. Nature 346, 197–199 (1990).

    Article  ADS  CAS  Google Scholar 

  45. Sternberg, P. W. & Horvitz, H. R. Devl Biol. 130, 67–73 (1988).

    Article  CAS  Google Scholar 

  46. Freyd, G., Kim, S. & Horvitz, H. R. Nature 344, 876–879 (1990).

    Article  ADS  CAS  Google Scholar 

  47. Way, J. & Chalfie, M. Cell 54, 5–16 (1988).

    Article  CAS  Google Scholar 

  48. Karlsson, O., Thor, S., Norberg, T., Ohlsson, H. & Edlund, T. Nature 344, 879–882 (1990).

    Article  ADS  CAS  Google Scholar 

  49. Rabbitts, T. & Boehm, T. Nature 348, 418 (1990).

    Article  ADS  Google Scholar 

  50. White, J. G., Southgate, E., Thomson, N. & Brenner, S. Phil. Trans. R. Soc. B 314, 1–340 (1986).

    Article  CAS  Google Scholar 

  51. Desai, C., Garriga, G., Mclntire, S. & Horvitz, H. R. Nature 336, 638–646 (1988).

    Article  ADS  CAS  Google Scholar 

  52. Shankland, M. Trends Genet. 3, 314–319 (1987).

    Article  Google Scholar 

  53. Doe, C. & Goodman, C. Devl Biol. 111, 206–219 (1985).

    Article  CAS  Google Scholar 

  54. Simpson, P. Development 109, 509–519 (1990).

    CAS  PubMed  Google Scholar 

  55. Nishida, H. & Satoh, N. Devl Biol. 132, 355–367 (1989).

    Article  CAS  Google Scholar 

  56. Lewis, J., Slack, M. & Wolpert, L. J. theor. Biol. 65, 575–590 (1977).

    Article  Google Scholar 

  57. Gurdon, J. Development 99, 285–306 (1987).

    CAS  PubMed  Google Scholar 

  58. Banerjee, U. & Zipursky, L. Neuron 4, 177–187 (1990).

    Article  CAS  Google Scholar 

  59. Weinberg, R. J. NIH Res. 3, 45–48 (1991).

    Google Scholar 

  60. Cantley, L. et al. Cell 64, 281–302 (1991).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Horvitz, H., Sternberg, P. Multiple intercellular signalling systems control the development of the Caenorhabditis elegans vulva. Nature 351, 535–541 (1991). https://doi.org/10.1038/351535a0

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/351535a0

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

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