Cofilin/ADF is required for cell motility during Drosophila ovary development and oogenesis (original) (raw)

Nature Cell Biology volume 3, pages 204–209 (2001)Cite this article

Abstract

The driving force behind cell motility is the actin cytoskeleton. Filopodia and lamellipodia are formed by the polymerization and extension of actin filaments towards the cell membrane1,2. This polymerization at the barbed end of the filament is balanced by depolymerization at the pointed end, recycling the actin in a 'treadmilling' process2,3. One protein involved in this process is cofilin/actin-depolymerizing factor (ADF), which can depolymerize actin filaments, allowing treadmilling to occur at an accelerated rate3,4. Cofilin/ADF is an actin-binding protein that is required for actin-filament disassembly, cytokinesis and the organization of muscle actin filaments4,5,6,7. There is also evidence that cofilin/ADF enhances cell motility3,8,9, although a direct requirement in vivo has not yet been shown. Here we show that Drosophila cofilin/ADF6,10, which is encoded by the twinstar (tsr) gene, promotes cell movements during ovary development and oogenesis. During larval development, cofilin/ADF is required for the cell rearrangement needed for formation of terminal filaments, stacks of somatic cells that are important for the initiation of ovarioles. It is also required for the migration of border cells during oogenesis. These results show that cofilin/ADF is an important regulator of actin-based cell motility during Drosophila development.

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

Access options

Subscribe to this journal

Receive 12 print issues and online access

$209.00 per year

only $17.42 per issue

Buy this article

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

Additional access options:

Similar content being viewed by others

References

  1. Mitchison, T. J. & Cramer, L. P. Cell 84, 371–379 (1996).
    Article CAS Google Scholar
  2. Carlier, M. F. Curr. Opin. Cell Biol. 10, 45–51 (1998).
    Article CAS Google Scholar
  3. Carlier, M. F. et al. J. Cell Biol. 136, 1307– 1322 (1997).
    Article CAS Google Scholar
  4. Bamburg, J. R. Annu. Rev. Cell Dev. Biol. 15, 185– 230 (1999).
    Article CAS Google Scholar
  5. Lappalainen, P. & Drubin, D. G. Nature 338, 78–82 (1997).
    Article Google Scholar
  6. Gunsalus, K. C. et al. J. Cell Biol. 131, 1243– 1259 (1995).
    Article CAS Google Scholar
  7. Ono, S., Baillie, D. L. & Benian, G. M. J. Cell Biol. 145, 491– 502 (1999).
    Article CAS Google Scholar
  8. Aizawa, H., Sutoh, K. & Yahara, I. J. Cell Biol. 132, 335– 344 (1996).
    Article CAS Google Scholar
  9. Loisel, T. P., Boujemaa, R., Pantaloni, D. & Carlier, M. F. Nature 401, 613–616 ( 1999).
    Article CAS Google Scholar
  10. Edwards, K. A. et al. Proc. Natl Acad. Sci. USA 91, 4589– 4593 (1994).
    Article CAS Google Scholar
  11. King, R. C. Ovarian Development in Drosophila melanogaster (Academic Press, New York, 1970).
    Google Scholar
  12. Spradling, A. in Development of Drosophila melanogaster (eds Bate, M. & Martinez-Arias, A.) 1–70 (Cold Spring Harbor Press, Cold Spring Harbor, New York, 1993).
    Google Scholar
  13. Lin, H. & Spradling, A. Dev. Biol. 159, 140–152 (1993).
    Article CAS Google Scholar
  14. Forbes, A., Lin, H., Ingham, P. & Spradling, A. Development 122, 1125–1135 ( 1996).
    CAS PubMed Google Scholar
  15. Godt, D. & Laski, F. A. Development 121, 173–187 (1995).
    CAS PubMed Google Scholar
  16. Sahut-Barnola, I., Godt, D., Laski, F. A. & Couderc, J. L. Dev. Biol. 170, 127–135 ( 1995).
    Article CAS Google Scholar
  17. Zollman, S., Godt, D., Prive, G. G., Couderc, J. L. & Laski, F. A. Proc. Natl Acad. Sci. USA 91, 10717–10721 (1994).
    Article CAS Google Scholar
  18. Torok, T., Tick, G., Alvarado, M. & Kiss, I. Genetics 135, 71–80 (1993).
    CAS PubMed PubMed Central Google Scholar
  19. Marlor, R. L., Parkhurst, S. M. & Corces, V. G. Mol. Cell. Biol. 6, 1129– 1134 (1986).
    Article CAS Google Scholar
  20. Verheyen, E. & Cooley, L. Development 120, 717–728 (1994).
    CAS PubMed Google Scholar
  21. Cant, K., Knowles, B., Mooseker, M. & Cooley, L. J. Cell Biol. 125, 369–380 (1994).
    Article CAS Google Scholar
  22. Hopmann, R., Cooper, J. A. & Miller, K. G. J. Cell Biol. 133, 1293– 1305 (1996).
    Article CAS Google Scholar
  23. Adams, A. E., Botstein, D. & Drubin, D. G. Nature 354, 404– 408 (1991).
    Article CAS Google Scholar
  24. Montell, D. J. Cell Biochem. Biophys. 31, 219–229 (1999).
    Article CAS Google Scholar
  25. Margolis, J. & Spradling, A. Development 121, 3797–3807 (1995).
    CAS PubMed Google Scholar
  26. Niewiadomska, P., Godt, D. & Tepass, U. J. Cell Biol. 144, 533– 547 (1999).
    Article CAS Google Scholar
  27. Yang, N. et al. Nature 393, 809–812 (1998).
    Article CAS Google Scholar
  28. Arber, S. et al. Nature 393, 805–809 (1998).
    Article CAS Google Scholar
  29. Spradling, A. et al. Proc. Natl Acad. Sci. USA 92, 10824 –10830 (1995).
    Article CAS Google Scholar
  30. Reed, B. H. & Orr-Weaver, T. L. Development 124 , 3543–3553 (1997).
    CAS PubMed Google Scholar

Download references

Acknowledgements

We thank H. D. Pham for excellent technical assistance, J. Pendelton, J. Peredo and T. Tran for their assistance in screening the 1,800 P-element lethal lines, and M. Bejar, J. Monroy and L. Ng for help with mapping tsr ntf. We also thank T. Orr-Weaver, P. Morcillo, the Bloomington Stock Center and T. Laverty (Berkeley Drosophila Genome Project) for stocks, and U. Tepass for critical reading of the manuscript. This work was supported by USPHS National Research Service Awards GM07185 and GM07617 (to J.C. and K.G., respectively). D.G. was supported by the Natural Science and Engineering Research Council of Canada. F.A.L. and M.G. were supported by NIH grants GM40451 and GM48430, respectively.

Author information

Authors and Affiliations

  1. Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, 90095, California, USA
    Jiong Chen & Frank A. Laski
  2. Molecular Biology Institute, University of California at Los Angeles, Los Angeles, 90095 , California, USA
    Frank A. Laski
  3. Department of Zoology, University of Toronto, Toronto, M5S 3G5, Ontario, Canada
    Dorothea Godt
  4. Department of Molecular Biology and Genetics, Cornell University, Ithaca, 14853, New York, USA
    Kris Gunsalus & Michael Goldberg
  5. Institute of Genetics, Hungarian Academy of Sciences , Szeged, H-6701, Hungary
    Istvan Kiss

Authors

  1. Jiong Chen
    You can also search for this author inPubMed Google Scholar
  2. Dorothea Godt
    You can also search for this author inPubMed Google Scholar
  3. Kris Gunsalus
    You can also search for this author inPubMed Google Scholar
  4. Istvan Kiss
    You can also search for this author inPubMed Google Scholar
  5. Michael Goldberg
    You can also search for this author inPubMed Google Scholar
  6. Frank A. Laski
    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toFrank A. Laski.

Supplementary information

Rights and permissions

About this article

Cite this article

Chen, J., Godt, D., Gunsalus, K. et al. Cofilin/ADF is required for cell motility during Drosophila ovary development and oogenesis.Nat Cell Biol 3, 204–209 (2001). https://doi.org/10.1038/35055120

Download citation

This article is cited by