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:

Planar polarity and actin dynamics in the epidermis of Drosophila

Nature Cell Biology volume 4, pages 937–944 (2002)Cite this article

Abstract

Dorsal closure is a morphogenetic process involving the coordinated convergence of two epithelial sheets to enclose the Drosophila melanogaster embryo. Specialized populations of cells at the edges of each epithelial sheet, the dorsal-most epidermal cells, emit actin-based processes that are essential for the proper enclosure of the embryo. Here we show that actin dynamics at the leading edge is preceded by a planar polarization of the dorsal-most epidermal cells associated with a reorganization of the cytoskeleton. An important consequence of this planar polarization is the formation of actin-nucleating centres at the leading edge, which are important in the dynamics of actin. We show that Wingless (Wg) signalling and Jun amino-terminal kinase (JNK) signalling have overlapping but different roles in these events.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Temporal changes in protein localization during dorsal closure.
Figure 2: Structure of the DME cells during dorsal closure.
Figure 3: Polarity of the dorsal epidermis is not lost in hepR75 embryos.
Figure 4: The organization of DME cells is disrupted in wg mutants.
Figure 5: Differential rescue of hep mutant embryos by Wg signalling.
Figure 6: Rescue of polarity in wg mutants by ubiquitous expression of Wg.
Figure 7: Cellular events in the DME cells during dorsal closure.

Similar content being viewed by others

References

  1. Martinez Arias, A. in The Development of Drosophila (eds Bate, M. & Martinez Arias, A.) 517–608 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 1993).

    Google Scholar 

  2. Young, P. E., Richman, A. M., Ketchum, A. S. & Kiehart, D. P. Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 7, 29–41 (1993).

    Article  CAS  PubMed  Google Scholar 

  3. Jacinto, A., Martinez-Arias, A. & Martin, P. Mechanisms of epithelial fusion and repair. Nature Cell Biol. 3, E117–E123 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Noselli, S. & Agnes, F. Roles of the JNK signaling pathway in Drosophila morphogenesis. Curr. Opin. Genet. Dev. 9, 466–472. (1999).

    Article  CAS  PubMed  Google Scholar 

  5. Stronach, B. E. & Perrimon, N. Stress signaling in Drosophila. Oncogene 18, 6172–6182 (1999).

    Article  CAS  PubMed  Google Scholar 

  6. Ring, J. M. & Martinez Arias, A. puckered, a gene involved in position-specific cell differentiation in the dorsal epidermis of the Drosophila larva. Development (Suppl.) 251–259 (1993).

  7. Jacinto, A. et al. Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure. Curr. Biol. 10, 1420–1426 (2000).

    Article  CAS  PubMed  Google Scholar 

  8. Kiehart, D. P., Galbraith, C. G., Edwards, K. A., Rickoll, W. L. & Montague, R. A. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 149, 471–490 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Glise, B., Bourbon, H. & Noselli, S. hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83, 451–461 (1995).

    Article  CAS  PubMed  Google Scholar 

  10. Glise, B. & Noselli, S. Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev. 11, 1738–1747 (1997).

    Article  CAS  PubMed  Google Scholar 

  11. Harden, N., Loh, H. Y., Chia, W. & Lim, L. A dominant inhibitory version of the small GTP-binding protein Rac disrupts cytoskeletal structures and inhibits developmental cell shape changes in Drosophila. Development 121, 903–914 (1995).

    CAS  PubMed  Google Scholar 

  12. Hou, X. S., Goldstein, E. S. & Perrimon, N. Drosophila Jun relays the Jun amino-terminal kinase signal transduction pathway to the Decapentaplegic signal transduction pathway in regulating epithelial cell sheet movement. Genes Dev. 11, 1728–1737 (1997).

    Article  CAS  PubMed  Google Scholar 

  13. Kockel, L., Zeitlinger, J., Staszewski, L. M., Mlodzik, M. & Bohmann, D. Jun in Drosophila development: redundant and nonredundant functions and regulation by two MAPK signal transduction pathways. Genes Dev. 11, 1748–1758. (1997).

    Article  CAS  PubMed  Google Scholar 

  14. Riesgo-Escovar, J. R. & Hafen, E. Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP-1 transcription factor DJun during dorsal closure. Genes Dev. 11, 1717–1727 (1997).

    Article  CAS  PubMed  Google Scholar 

  15. Ricos, M. G., Harden, N., Sem, K. P., Lim, L. & Chia, W. Dcdc42 acts in TGF-beta signaling during Drosophila morphogenesis: distinct roles for the Drac1/JNK and Dcdc42/TGF-β cascades in cytoskeletal regulation. J. Cell Sci. 112, 1225–1235 (1999).

    CAS  PubMed  Google Scholar 

  16. Reed, B. H., Wilk, R. & Lipshitz, H. D. Downregulation of Jun kinase signaling in the amnioserosa is essential for dorsal closure of the Drosophila embryo. Curr. Biol. 11, 1098–1108 (2001).

    Article  CAS  PubMed  Google Scholar 

  17. Shimada, Y., Usui, T., Yanagawa, S., Takeichi, M. & Uemura, T. Asymmetric colocalization of Flamingo, a seven-pass transmembrane cadherin, and Dishevelled in planar cell polarization. Curr. Biol. 11, 859–863 (2001).

    Article  CAS  PubMed  Google Scholar 

  18. Adler, P. N. & Lee, H. Frizzled signaling and cell-cell interactions in planar polarity. Curr. Opin. Cell Biol. 13, 635–640 (2001).

    Article  CAS  PubMed  Google Scholar 

  19. Takahashi, K., Matsuo, T., Katsube, T., Ueda, R. & Yamamoto, D. Direct binding between two PDZ domain proteins Canoe and ZO-1 and their roles in regulation of the jun N-terminal kinase pathway in Drosophila morphogenesis. Mech. Dev. 78, 97–111 (1998).

    Article  CAS  PubMed  Google Scholar 

  20. Woods, D. F., Hough, C., Peel, D., Callaini, G. & Bryant, P. J. Dlg protein is required for junction structure, cell polarity, and proliferation control in Drosophila epithelia. J. Cell Biol. 134, 1469–1482 (1996).

    Article  CAS  PubMed  Google Scholar 

  21. Eaton, S., Wepf, R. & Simons, K. Roles for Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. J. Cell Biol. 135, 1277–1289 (1996).

    Article  CAS  PubMed  Google Scholar 

  22. Eaton, S. Planar polarization of Drosophila and vertebrate epithelia. Curr. Opin. Cell Biol. 9, 860–866 (1997).

    Article  CAS  PubMed  Google Scholar 

  23. Strutt, D. I., Weber, U. & Mlodzik, M. The role of RhoA in tissue polarity and Frizzled signalling. Nature 387, 292–295 (1997).

    Article  CAS  PubMed  Google Scholar 

  24. Boutros, M., Paricio, N., Strutt, D. I. & Mlodzik, M. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94, 109–118 (1998).

    Article  CAS  PubMed  Google Scholar 

  25. Craig, G. et al. Notch regulates actin cytoskeletal organisation and the activity of cellular protrusions during dorsal closure in Drosophila. (submitted).

  26. Stronach, B. & Perrimon, N. Activation of the JNK pathway during dorsal closure in Drosophila requires the mixed lineage kinase, slipper. Genes Dev. 16, 377–387 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Heisenberg, C. P. et al. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405, 76–81 (2000).

    Article  CAS  PubMed  Google Scholar 

  28. Tada, M. & Smith, J. C. Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127, 2227–2238 (2000).

    CAS  PubMed  Google Scholar 

  29. Wallingford, J. B. et al. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405, 81–85 (2000).

    Article  CAS  PubMed  Google Scholar 

  30. Yamanaka, H. et al. JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep. 3, 69–75 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. McEwen, D. G., Cox, R. T. & Peifer, M. The canonical Wg and JNK signaling cascades collaborate to promote both dorsal closure and ventral patterning. Development 127, 3607–3617 (2000).

    CAS  PubMed  Google Scholar 

  32. Snow, P. M., Bieber, A. J. & Goodman, C. S. Fasciclin III: a novel homophilic adhesion molecule in Drosophila. Cell 59, 313–323 (1989).

    Article  CAS  PubMed  Google Scholar 

  33. Perrimon, N. & Mahowald, A. P. Multiple functions of segment polarity genes in Drosophila. Dev. Biol. 119, 587–600 (1987).

    Article  CAS  PubMed  Google Scholar 

  34. Klein, T. & Arias, A. M. Different spatial and temporal interactions between Notch, wingless, and vestigial specify proximal and distal pattern elements of the wing in Drosophila. Dev. Biol. 194, 196–212 (1998).

    Article  CAS  PubMed  Google Scholar 

  35. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415 (1993).

    CAS  PubMed  Google Scholar 

  36. Axelrod, J. D., Miller, J. R., Shulman, J. M., Moon, R. T. & Perrimon, N. Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev. 12, 2610–2622 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. van de Wetering, M. et al. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88, 789–799 (1997).

    Article  CAS  PubMed  Google Scholar 

  38. Pai, L. M., Orsulic, S., Bejsovec, A. & Peifer, M. Negative regulation of Armadillo, a Wingless effector in Drosophila. Development 124, 2255–2266 (1997).

    CAS  PubMed  Google Scholar 

  39. Perrimon, N. The maternal effect of lethal(1)discs-large-1: a recessive oncogene of Drosophila melanogaster. Dev Biol 127, 392–407 (1988).

    Article  CAS  PubMed  Google Scholar 

  40. Zecchini, V., Brennan, K. & Martinez-Arias, A. An activity of Notch regulates JNK signalling and affects dorsal closure in Drosophila. Curr. Biol. 9, 460–469 (1999).

    Article  CAS  PubMed  Google Scholar 

  41. Fernandez, R. et al. The Drosophila shark tyrosine kinase is required for embryonic dorsal closure. Genes Dev. 14, 604–614 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Lu, Y. & Settleman, J. The Drosophila Pkn protein kinase is a Rho/Rac effector target required for dorsal closure during embryogenesis. Genes Dev. 13, 1168–1180 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Harden, N. et al. Drac1 and Crumbs participate in amnioserosa morphogenesis during dorsal closure in Drosophila. J.Cell Sci 115, 2119–2129 (2002).

    CAS  PubMed  Google Scholar 

  44. Magie, C. R., Meyer, M. R., Gorsuch, M. S. & Parkhurst, S. M. Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development. Development 126, 5353–5364 (1999).

    CAS  PubMed  Google Scholar 

  45. Hakeda-Suzuki, S. et al. Rac function and regulation during Drosophila development. Nature 416, 438–442 (2002).

    Article  CAS  PubMed  Google Scholar 

  46. Strutt, D. I. Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. Mol. Cell 7, 367–375 (2001).

    Article  CAS  PubMed  Google Scholar 

  47. Chou, T. B. & Perrimon, N. Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131, 643–653 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Ashburner, M. Drosophila: A Laboratory Manual. (Cold Spring Harbour Laboratory Press, Cold Spring Harbour, NY, 1989).

    Google Scholar 

  49. Lehmann, R. & Tautz, D. In situ hybridization to RNA. Methods Cell Biol. 44, 575–598 (1994).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank D. Bohman, P. J. Bryant, R. Karess, T. Uemura and D. Yamamoto for primary antibodies; D. Strutt for the Fz–GFP stock; J. Axelrod for the Dsh–GFP and UAS–Dsh stocks; and P. Martin for encouragement, tutorials and comments. This work was supported by The Wellcome Trust (J.K., N.L., A.P., T.B. and A.M.A.), the Association pour la Recherche sur le Cancer (V.M.) and the Fundação Ciência e Tecnologia (A.J. and B.G.F.).

Author information

Author notes

  1. Julia A. Kaltschmidt and Nicola Lawrence: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK

    Julia A. Kaltschmidt, Nicola Lawrence, Véronique Morel, Tina Balayo, Anne Pelissier & Alfonso Martinez Arias

  2. Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, Oeiras, 2780-156, Portugal

    Beatriz García Fernández & Antonio Jacinto

Authors
  1. Julia A. Kaltschmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicola Lawrence
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Véronique Morel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tina Balayo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Beatriz García Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anne Pelissier
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Antonio Jacinto
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alfonso Martinez Arias
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alfonso Martinez Arias.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary figures

Figure S1 Z sections taken through DME cells of wild type embryos (12 hour AEL) showing, from left to right, the relative distributions of FasIII, α-Catenin, ActinGFP, Canoe, Flamingo and Frizzled in the apico-basal axis of the cells. (PDF 1640 kb)

Figure S2 Addition of phalloidin to the fixation solution stabilises the actin cytoskeleton at the LE of wild type embryos and hep1 mutant embryos but not wingless mutant embryos. thin actin cable at the LE.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kaltschmidt, J., Lawrence, N., Morel, V. et al. Planar polarity and actin dynamics in the epidermis of Drosophila. Nat Cell Biol 4, 937–944 (2002). https://doi.org/10.1038/ncb882

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ncb882

This article is cited by

Search

Advanced 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