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.

  • Letter
  • Published:

Integrin-independent repression of cadherin transcription by talin during axis formation in Drosophila

Abstract

The Drosophila melanogaster anterior–posterior axis becomes polarized early during oogenesis by the posterior localization of the oocyte within the egg chamber. The invariant position of the oocyte is thought to be driven by an upregulation of the adhesion molecule DE-cadherin in the oocyte and the posterior somatic follicle cells, providing the first in vivo example of cell sorting that is specified by quantitative differences in cell–cell adhesion1,2. However, it has remained unclear how DE-cadherin levels are regulated. Here, we show that talin, known for its role in linking integrins to the actin cytoskeleton, has the unexpected function of specifically inhibiting DE-cadherin transcription. Follicle cells that are mutant for talin show a strikingly high level of DE-cadherin, due to elevated transcription of DE-cadherin. We demonstrate that this deregulation of DE-cadherin is sufficient to attract the oocyte to lateral and anterior positions. Surprisingly, this function of talin is independent of integrins. These results uncover a new role for talin in regulating cadherin-mediated cell adhesion.

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: Talin is required in the follicle cells for oocyte localization.
Figure 2: Follicle cells that lacked talin conserved their polarity and identity.
Figure 3: Integrins are not required for oocyte localization.
Figure 4: Follicle cells that lack talin overexpress DE-cadherin.
Figure 5: Talin regulates DE-cadherin transcription.

Similar content being viewed by others

References

  1. Godt, D. & Tepass, U. Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395, 387–391 (1998).

    Article  CAS  PubMed  Google Scholar 

  2. Gonzalez-Reyes, A. & St Johnston, D. The Drosophila AP axis is polarised by the cadherin-mediated positioning of the oocyte. Development 125, 3635–3644 (1998).

    CAS  PubMed  Google Scholar 

  3. Wheelock, M. J. & Johnson, K. R. Cadherins as modulators of cellular phenotype. Annu. Rev. Cell Dev. Biol. 19, 207–235 (2003).

    Article  CAS  PubMed  Google Scholar 

  4. Bokel, C. & Brown, N. H. Integrins in development: moving on, responding to, and sticking to the extracellular matrix. Dev. Cell 3, 311–321 (2002).

    Article  CAS  PubMed  Google Scholar 

  5. Hynes, R. O. Integrins: bidirectional, allosteric signaling machines. Cell 110, 673–687 (2002).

    Article  CAS  PubMed  Google Scholar 

  6. Avizienyte, E. et al. Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signalling. Nature Cell Biol. 4, 632–638 (2002).

    Article  CAS  PubMed  Google Scholar 

  7. Tepass, U., Godt, D. & Winklbauer, R. Cell sorting in animal development: signalling and adhesive mechanisms in the formation of tissue boundaries. Curr. Opin. Genet. Dev. 12, 572–582 (2002).

    Article  CAS  PubMed  Google Scholar 

  8. Nose, A., Nagafuchi, A. & Takeichi, M. Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54, 993–1001 (1988).

    Article  CAS  PubMed  Google Scholar 

  9. Steinberg, M. S. & Takeichi, M. Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc. Natl Acad. Sci. USA 91, 206–209 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Huynh, J. R. & St Johnston, D. The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr. Biol. 14, R438–R449 (2004).

    Article  CAS  PubMed  Google Scholar 

  11. Brown, N. H. et al. Talin is essential for integrin function in Drosophila. Dev. Cell 3, 569–579 (2002).

    Article  CAS  PubMed  Google Scholar 

  12. Garcia-Alvarez, B. et al. Structural determinants of integrin recognition by talin. Mol. Cell 11, 49–58 (2003).

    Article  CAS  PubMed  Google Scholar 

  13. Nayal, A., Webb, D. J. & Horwitz, A. F. Talin: an emerging focal point of adhesion dynamics. Curr. Opin. Cell Biol. 16, 94–98 (2004).

    Article  CAS  PubMed  Google Scholar 

  14. Cram, E. J. & Schwarzbauer, J. E. The talin wags the dog: new insights into integrin activation. Trends Cell Biol. 14, 55–57 (2004).

    Article  CAS  PubMed  Google Scholar 

  15. Cram, E. J., Clark, S. G. & Schwarzbauer, J. E. Talin loss-of-function uncovers roles in cell contractility and migration in C. elegans. J. Cell Sci. 116, 3871–3878 (2003).

    Article  CAS  PubMed  Google Scholar 

  16. Devenport, D. & Brown, N. H. Morphogenesis in the absence of integrins: mutation of both Drosophila β subunits prevents midgut migration. Development 131, 5405–5415 (2004).

    Article  CAS  PubMed  Google Scholar 

  17. Bateman, J., Reddy, R. S., Saito, H. & Van Vactor, D. The receptor tyrosine phosphatase Dlar and integrins organize actin filaments in the Drosophila follicular epithelium. Curr. Biol. 11, 1317–1327 (2001).

    Article  CAS  PubMed  Google Scholar 

  18. Struhl, G. & Basler, K. Organizing activity of wingless protein in Drosophila. Cell 72, 527–540 (1993).

    Article  CAS  PubMed  Google Scholar 

  19. Tepass, U. et al. shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev. 10, 672–685 (1996).

    Article  CAS  PubMed  Google Scholar 

  20. Balda, M. S. & Matter, K. Epithelial cell adhesion and the regulation of gene expression. Trends Cell Biol. 13, 310–318 (2003).

    Article  CAS  PubMed  Google Scholar 

  21. Gottardi, C. J. & Gumbiner, B. M. Adhesion signaling: how β-catenin interacts with its partners. Curr. Biol. 11, R792–R794 (2001).

    Article  CAS  PubMed  Google Scholar 

  22. Beckerle, M. C., Burridge, K., DeMartino, G. N. & Croall, D. E. Colocalization of calcium-dependent protease II and one of its substrates at sites of cell adhesion. Cell 51, 569–577 (1987).

    Article  CAS  PubMed  Google Scholar 

  23. Li, M. A., Alls, J. D., Avancini, R. M., Koo, K. & Godt, D. The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nature Cell Biol. 5, 994–1000 (2003).

    Article  CAS  PubMed  Google Scholar 

  24. Oda, H. & Tsukita, S. Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells. J. Cell Sci. 114, 493–501 (2001).

    CAS  PubMed  Google Scholar 

  25. Pacquelet, A., Lin, L. & Rorth, P. Binding site for p120/β-catenin is not required for Drosophila E-cadherin function in vivo. J. Cell Biol. 160, 313–319 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Prout, M., Damania, Z., Soong, J., Fristrom, D. & Fristrom, J. W. Autosomal mutations affecting adhesion between wing surfaces in Drosophila melanogaster. Genetics 146, 275–285 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Bunch, T. A. et al. Characterization of mutant alleles of myospheroid, the gene encoding the β subunit of the Drosophila PS integrins. Genetics 132, 519–528 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Chou, T. & 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 

  29. Luschnig, S., Krauss, J., Bohmann, K., Desjeux, I. & Nusslein-Volhard, C. The Drosophila SHC adaptor protein is required for signaling by a subset of receptor tyrosine kinases. Mol. Cell 5, 231–241 (2000).

    Article  CAS  PubMed  Google Scholar 

  30. Pignoni, F. & Zipursky, S. L. Induction of Drosophila eye development by decapentaplegic. Development 124, 271–278 (1997).

    CAS  PubMed  Google Scholar 

  31. Sanson, B., White, P. & Vincent, J. P. Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature 383, 627–630 (1996).

    Article  PubMed  Google Scholar 

  32. Gonzalez-Reyes, A. & St Johnston, D. Role of oocyte position in establishment of anterior-posterior polarity in Drosophila. Science 266, 639–642 (1994).

    Article  CAS  PubMed  Google Scholar 

  33. Wodarz, A., Ramrath, A., Grimm, A. & Knust, E. Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J. Cell Biol. 150, 1361–1374 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to A. Pacquelet and P. Rorth for the tubulin-cadherin–GFP line, U. Tepass for flies, and the DSHB (University of Iowa) for antibodies. We also wish to thank A. Guichet for the in situ hybridization. This work was supported by a fellowship from the Human Frontier Scientific Programme (G.T.), a Senior Fellowship from the Wellcome Trust (N.H.B.), the C.N.R.S and A.R.C. (J.A.L. and J.R.H.), the Ministère de la Recherche et de l'Education and A.R.C (I.E.B) and EMBO (J.R.H).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jean-René Huynh.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bécam, I., Tanentzapf, G., Lepesant, JA. et al. Integrin-independent repression of cadherin transcription by talin during axis formation in Drosophila. Nat Cell Biol 7, 510–516 (2005). https://doi.org/10.1038/ncb1253

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ncb1253

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