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.

  • Brief Communication
  • Published:

Cofilin/ADF is required for cell motility during Drosophila ovary development and oogenesis

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

Buy this article

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

Figure 1: Diagram of terminal-filament formation and structure of the twinstar gene.
Figure 2: Formation of terminal filaments is disrupted in tsrntf mutant ovaries.
Figure 3: High levels of filamentous actin in a tsrntf mutant ovary.
Figure 4: Migration of border cells in wild-type and tsr-mutant egg chambers.

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 tsrntf. 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

Authors

Corresponding author

Correspondence to Frank A. Laski.

Supplementary information

Rights and permissions

Reprints 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

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35055120

This article is cited by

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