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.

  • Article
  • Published:

Compartment boundaries and the control of Drosopfiffa limb pattern by hedgehog protein

Abstract

Drosophila limbs are subdivided into anterior and posterior compartments which derive from adjacent cell populations founded early in development. Evidence is now provided that posterior cells organize growth and cell patterning in both compartments by secreting hedgehog protein and that hedgehog protein acts indirectly by inducing neighbouring anterior cells to secrete decapentaplegic or wingless protein.

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. Garcia-Bellido, A., Ripoll, P. & Morata, G. Nature New Biol. 245, 251–253 (1973).

    Article  CAS  PubMed  Google Scholar 

  2. Crick, F. H. & Lawrence, P. A. Science 189, 340–347 (1975).

    Article  ADS  CAS  PubMed  Google Scholar 

  3. Garcia-Bellido, A. Genetic Control of Wing Disc Development in Drosophila (Associated Scientific Publishers, New York, 1975).

    Book  Google Scholar 

  4. Morata, G. & Lawrence, P. A. Nature 255, 614–617 (1975).

    Article  ADS  CAS  PubMed  Google Scholar 

  5. Lawrence, P. A. & Morata, G. Devl Biol. 50, 321–337 (1976).

    Article  CAS  Google Scholar 

  6. DiNardo, S., Kuner, J. M., Theis, J. & O'Farrell, P. H. Cell 43, 59–69 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kornberg, T., Siden, I., O'Farrell, P. H. & Simon, M. Cell 40, 45–53 (1985).

    Article  CAS  PubMed  Google Scholar 

  8. Hama, C., Ali, Z. & Kornberg, T. B. Genes Dev. 4, 1079–1093 (1990).

    Article  CAS  PubMed  Google Scholar 

  9. Moazed, D. & O'Farrell, P. H. Development 116, 805–810 (1992).

    CAS  PubMed  Google Scholar 

  10. Vincent, J. P. & O'Farrell, P. H. Cell 68, 923–931 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Lawrence, P. A. & Struhl, G. EMBO J. 1, 827–833 (1982).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Meinhardt, H. Devl Biol. 96, 375–385 (1983).

    Article  CAS  Google Scholar 

  13. Nüsslein-Volhard, C. & Wieschaus, E. Nature 287, 795–801 (1980).

    Article  ADS  PubMed  Google Scholar 

  14. Spencer, F. A., Hoffmann, F. M. & Gelbart, W. M. Cell 28, 451–461 (1982).

    Article  CAS  PubMed  Google Scholar 

  15. Sharma, R. P. & Chopra, V. L. Devl Biol. 48, 461–465 (1976).

    Article  CAS  Google Scholar 

  16. van-den-Heuvel, M., Nusse, R., Johnston, P. & Lawrence, P. A. Cell 59, 739–749 (1989).

    Article  CAS  PubMed  Google Scholar 

  17. Panganiban, G. E., Rashka, K. E., Neitzel, M. D. & Hoffmann, F. M. Molec. cell. Biol. 10, 2669–2677 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Panganiban, G. E., Reuter, R., Scott, M. P. & Hoffmann, F. M. Development 110, 1041–1050 (1990).

    CAS  PubMed  Google Scholar 

  19. Gonzalez, F., Swales, L., Bejsovec, A., Skaer, H. & Martinez-Arias, A. Mech. Dev. 35, 43–54 (1991).

    Article  CAS  PubMed  Google Scholar 

  20. Lee, J. J., von-Kessler, D. P., Parks, S. & Beachy, P. A. Cell 71, 33–50 (1992).

    Article  CAS  PubMed  Google Scholar 

  21. Taylor, A. M., Nakano, Y., Mohler, J. & Ingham, P. W. Mech. Dev. 43, 89–96 (1993).

    Article  Google Scholar 

  22. Baker, N. E. Devl Biol. 125, 96–108 (1988).

    Article  CAS  Google Scholar 

  23. DiNardo, S., Sher, E., Heemskerk, J. J., Kassis, J. A. & O'Farrell, P. H. Nature 332, 604–609 (1988).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  24. Martinez-Arias, A., Baker, N. E. & Ingham, P. W. Development 103, 157–170 (1988).

    CAS  PubMed  Google Scholar 

  25. Mohler, J. Genetics 120, 1061–1072 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Immerglück, K., Lawrence, P. A. & Bienz, M. Cell 62, 261–268 (1990).

    Article  PubMed  Google Scholar 

  27. Posakony, L. G., Raftery, L. A. & Gelbart, W. M. Mech. Dev. 33, 69–82 (1990).

    Article  CAS  PubMed  Google Scholar 

  28. Ingham, P. W., Taylor, A. M. & Nakano, Y. Nature 353, 184–187 (1991).

    Article  ADS  CAS  PubMed  Google Scholar 

  29. Ferguson, E. L. & Anderson, K. V. Cell 71, 451–461 (1992).

    Article  CAS  PubMed  Google Scholar 

  30. Heberlein, U., Wolff, T. & Rubin, G. M. Cell 75, 913–926 (1993).

    Article  CAS  PubMed  Google Scholar 

  31. Ingham, P. W. Nature 366, 560–562 (1993).

    Article  ADS  CAS  PubMed  Google Scholar 

  32. Ingham, P. W. & Hidalgo, A. Development 117, 283–291 (1993).

    CAS  PubMed  Google Scholar 

  33. Ma, C., Zhou, Y., Beachy, P. A. & Moses, K. Cell 75, 927–938 (1993).

    Article  CAS  PubMed  Google Scholar 

  34. Struhl, G. & Basler, K. Cell 72, 527–540 (1993).

    Article  CAS  PubMed  Google Scholar 

  35. Cabrera, C. V., Alonso, M. C., Johnston, P., Phillips, R. G. & Lawrence, P. A. Cell 50, 659–663 (1987).

    Article  CAS  PubMed  Google Scholar 

  36. Padgett, R. W., St Johnston, R. D. & Gelbart, W. M. Nature 325, 81–84 (1987).

    Article  ADS  CAS  PubMed  Google Scholar 

  37. Rijsewijk, F. et al. Cell 50, 649–657 (1987).

    Article  CAS  PubMed  Google Scholar 

  38. Riddle, R. D., Johnson, R. L., Laufer, E. & Tabin, C. Cell 76, 1401–1416 (1993).

    Article  Google Scholar 

  39. Krauss, S., Concordet, J.-P. & Ingham, P. W. Cell 76, 1431–1444 (1993).

    Article  Google Scholar 

  40. Echelard, Y. et al. Cell 76, 1417–1430 (1993).

    Article  Google Scholar 

  41. Mohler, J. & Vani, K. Development 115, 957–971 (1992).

    CAS  PubMed  Google Scholar 

  42. Tabata, T., Eaton, S. & Kornberg, T. B. Genes Dev. 6, 2635–2645 (1992).

    Article  CAS  PubMed  Google Scholar 

  43. Tashiro, S. et al. Gene 124, 183–189 (1993).

    Article  CAS  PubMed  Google Scholar 

  44. Masucci, J. D., Miltenberger, R. J. & Hoffmann, F. M. Genes Dev. 4, 2011–2023 (1990).

    Article  CAS  PubMed  Google Scholar 

  45. Blackman, R. K., Sanicola, M., Raftery, L. A., Gillevet, T. & Gelbart, W. M. Development 111, 657–666 (1991).

    CAS  PubMed  Google Scholar 

  46. Raftery, L. A., Sanicola, M., Blackman, R. K. & Gelbart, W. M. Development 113, 27–33 (1991).

    CAS  PubMed  Google Scholar 

  47. Couso, J. P., Bate, M. & Martinez-Arias, A. Science 259, 484–489 (1993).

    Article  ADS  CAS  PubMed  Google Scholar 

  48. Broach, J. R. & Hicks, J. B. Cell 21, 501–508 (1980).

    Article  CAS  PubMed  Google Scholar 

  49. Theurkauf, W. E., Baum, H., Bo, J. & Wensink, P. C. Proc. natn. Acad. Sci. U.S.A. 83, 8477–8481 (1986).

    Article  ADS  CAS  Google Scholar 

  50. Kassis, J. A., Noll, E., VanSickle, E. P., Odenwald, W. F. & Perrimon, N. Proc. natn. Acad. Sci. U.S.A. 89, 1919–1923 (1992).

    Article  ADS  CAS  Google Scholar 

  51. Lawrence, P. A., Johnston, P., Macdonald, P. & Struhl, G. Nature 328, 440–442 (1987).

    Article  ADS  CAS  PubMed  Google Scholar 

  52. Bejsovec, A. & Martinez-Arias, A. Development 113, 471–485 (1991).

    CAS  PubMed  Google Scholar 

  53. Heemskerk, J., DiNardo, S., Kostriken, R. & O'Farrell, P. H. Nature 352, 404–410 (1991).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  54. Peifer, M., Rauskolb, C., Williams, M., Riggleman, B. & Wieschaus, E. Development 11, 1029–1043 (1991).

    Google Scholar 

  55. Williams, J. A., Paddock, S. W. & Carroll, S. B. Development 117, 571–584 (1993).

    CAS  PubMed  Google Scholar 

  56. Steiner, E. Wilhelm Roux Arch. EntwMech. Org. 180, 9–30 (1976).

    Article  Google Scholar 

  57. Campbell, G., Weaver, T. & Tomlinson, A. Cell 74, 1113–1123 (1993).

    Article  CAS  PubMed  Google Scholar 

  58. Blair, S. S. Development 119, 339–351 (1993).

    CAS  PubMed  Google Scholar 

  59. Diaz-Benjumea, F. J. & Cohen, S. M. Cell 75, 741–752 (1993).

    Article  CAS  PubMed  Google Scholar 

  60. Ready, D. F., Hanson, T. E. & Benzer, S. Devl Biol. 53, 217–240 (1976).

    Article  CAS  Google Scholar 

  61. Anderson, R., Landry, M. & Muneoka, K. Development 117, 1421–1433 (1993).

    CAS  PubMed  Google Scholar 

  62. Niswander, L., Tickle, C., Vogel, A., Booth, I. & Martin, G. R. Cell 75, 579–587 (1993).

    Article  CAS  PubMed  Google Scholar 

  63. Placzek, M., Jessell, T. M. & Dodd, J. Development 117, 205–218 (1993).

    CAS  PubMed  Google Scholar 

  64. Vogel, A. & Tickle, C. Development 119, 199–206 (1993).

    CAS  PubMed  Google Scholar 

  65. Struhl, G. Devl Biol. 84, 372–385 (1981).

    Article  CAS  Google Scholar 

  66. Golic, K. Science 252, 958–961 (1991).

    Article  ADS  CAS  PubMed  Google Scholar 

  67. Xu, T. & Rubin, G. M. Development 117, 1223–1237 (1993).

    CAS  PubMed  Google Scholar 

  68. Morata, G. & Ripoll, P. Dev. Biol. 42, 211–221 (1975).

    Article  CAS  PubMed  Google Scholar 

  69. Patel, N. H. et al. Cell 58, 955–968 (1989).

    Article  CAS  PubMed  Google Scholar 

  70. Eaton, S. & Kornberg, T. B. Genes Dev. 4, 1068–1077 (1990).

    Article  CAS  PubMed  Google Scholar 

  71. Orenic, T. V., Slusarski, D. C., Kroll, K. L. & Holmgren, R. A. Genes Dev. 4, 1053–1067 (1990).

    Article  CAS  PubMed  Google Scholar 

  72. Tabata, T. & Kornberg, T. Cell 76, 89–102 (1994).

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Basler, K., Struhl, G. Compartment boundaries and the control of Drosopfiffa limb pattern by hedgehog protein. Nature 368, 208–214 (1994). https://doi.org/10.1038/368208a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/368208a0

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