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:

Drosophila Stardust is a partner of Crumbs in the control of epithelial cell polarity

Nature volume 414, pages 638–643 (2001)Cite this article

Abstract

The polarized architecture of epithelial cells depends on the highly stereotypic distribution of cellular junctions and other membrane-associated protein complexes. In epithelial cells of the Drosophila embryo, three distinct domains subdivide the lateral plasma membrane. The most apical one comprises the subapical complex (SAC). It is followed by the zonula adherens (ZA) and, further basally, by the septate junction1. A core component of the SAC is the transmembrane protein Crumbs, the cytoplasmic domain of which recruits the PDZ-protein Discs Lost into the complex2,3. Cells lacking crumbs or the functionally related gene stardust fail to organize a continuous ZA and to maintain cell polarity4,5,6. Here we show that stardust provides an essential component of the SAC. Stardust proteins colocalize with Crumbs and bind to the carboxy-terminal amino acids of its cytoplasmic tail. We introduce two different Stardust proteins here: one MAGUK protein, characterized by a PDZ domain, an SH3 domain and a guanylate kinase domain; and a second isoform comprising only the guanylate kinase domain. The Stardust proteins represent versatile candidates as structural and possibly regulatory constituents of the SAC, a crucial element in the control of epithelial cell polarity.

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: Cuticle preparations of embryos.
Figure 2: Molecular analysis of the sdt locus.
Figure 3: Proteins predicted from the sdt locus.
Figure 4: Phenotypic characteristics of sdt mutant embryos.
Figure 5: Relationship between sdt and crb expression.

Similar content being viewed by others

References

  1. Müller, H. A. J. Genetic control of epithelial cell polarity: lessons from Drosophila. Dev. Dyn. 218, 52–67 (2000).

    Article  Google Scholar 

  2. Bhat, M. A. et al. Discs Lost, a novel multi-PDZ domain protein, establishes and maintains epithelial polarity. Cell 96, 833–845 (1999).

    Article  CAS  Google Scholar 

  3. Klebes, A. & Knust, E. A conserved motif in Crumbs is required for E-cadherin localisation and zonula adherens formation in Drosophila. Curr. Biol. 10, 76–85 (2000).

    Article  CAS  Google Scholar 

  4. Tepass, U. & Knust, E. Crumbs and stardust act in a genetic pathway that controls the organization of epithelia in Drosophila melanogaster. Dev. Biol. 159, 311–326 (1993).

    Article  CAS  Google Scholar 

  5. Grawe, F., Wodarz, A., Lee, B., Knust, E. & Skaer, H. The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions. Development 122, 951–959 (1996).

    Article  CAS  Google Scholar 

  6. Tepass, U. Crumbs, a component of the apical membrane, is required for zonula adherens formation in primary epithelia of Drosophila. Dev. Biol. 177, 217–225 (1996).

    Article  CAS  Google Scholar 

  7. Dimitratos, S. D., Woods, D. F., Stathakis, D. G. & Bryant, P. J. Signaling pathways are focused at specialized regions of the plasma membrane by scaffolding proteins of the MAGUK family. Bioessays 21, 912–921 (1999).

    Article  CAS  Google Scholar 

  8. Kamberov, E. et al. Molecular cloning and characterization of Pals, proteins associated with mLin-7. J. Biol. Chem. 275, 11425–11431 (2000).

    Article  CAS  Google Scholar 

  9. Müller, H. A. & Wieschaus, E. armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J. Cell Biol. 134, 149–163 (1996).

    Article  Google Scholar 

  10. Schober, M., Schaefer, M. & Knoblich, J. A. Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature 402, 548–551 (1999).

    Article  ADS  CAS  Google Scholar 

  11. Wodarz, A., Ramrath, A., Kuchinke, U. & Knust, E. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 402, 544–547 (1999).

    Article  ADS  CAS  Google Scholar 

  12. 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  Google Scholar 

  13. Petronczki, M. & Knoblich, J. A. DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila. Nature Cell Biol. 3, 43–49 (2001).

    Article  CAS  Google Scholar 

  14. Tepass, U., Theres, C. & Knust, E. crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 61, 787–799 (1990).

    Article  CAS  Google Scholar 

  15. McGee, A. W. & Bredt, D. S. Identification of an intramolecular interaction between the SH3 and guanylate kinase domains of PSD-95. J. Biol. Chem. 274, 17431–17436 (1999).

    Article  CAS  Google Scholar 

  16. Shin, H., Hsueh, Y.-I., Yang, F.-C., Kim, E. & Sheng, M. An intramolecular interaction between Src homology 3 domain and guanylate kinase-like domain required for channel clustering by postsynaptic density-95/SAP90. J. Neurosci. 20, 3580–3587 (2000).

    Article  CAS  Google Scholar 

  17. Wu, H. et al. Intramolecular interactions regulate SAP97 binding to GKAP. EMBO J. 19, 5740–5751 (2000).

    Article  CAS  Google Scholar 

  18. Nix, S. L., Chishti, A. H., Anderson, J. M. & Walther, Z. hCASK and hDlg associate in epithelia, and their Src homology 3 and guanylate kinase domains participate in both intramolecular and intermolecular interactions. J. Biol. Chem. 275, 41192–41200 (2000).

    Article  CAS  Google Scholar 

  19. Dimitratos, S. D., Woods, D. F. & Bryant, P. J. Camguk, Lin-2, and CASK: novel membrane-associated guanylate kinase homologs that also contain CaM kinase domains. Mech. Dev. 63, 127–130 (1997).

    Article  CAS  Google Scholar 

  20. Lammel, U. & Saumweber, H. X-linked loci of Drosophila melanogaster causing defects in the morphology of the embryonic salivary gland. Dev. Genes Evol. 10, 525–535 (2000).

    Article  Google Scholar 

  21. Rorth, P. A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proc. Natl Acad. Sci. USA 93, 12418–12422 (1996).

    Article  ADS  CAS  Google Scholar 

  22. Rubin, G. M. & Spradling, A. C. Vectors for P-element-mediated gene transfer in Drosophila. Nucleic Acids Res. 11, 6341–6351 (1983).

    Article  CAS  Google Scholar 

  23. Wodarz, A., Hinz, U., Engelbert, M. & Knust, E. Expression of Crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82, 67–76 (1995).

    Article  CAS  Google Scholar 

  24. Han, K. & Manley, J. L. Functional domains of the Drosophila Engrailed protein. EMBO J. 12, 2723–2733 (1993).

    Article  CAS  Google Scholar 

  25. Tower, J., Karpen, G. H., Craig, N. & Spradling, A. C. Preferential transposition of Drosophila P-elements to nearby chromosomal sites. Genetics 133, 347–359 (1993).

    Article  CAS  Google Scholar 

  26. Brown, N. H. & Kafatos, F. C. Functional cDNA libraries from Drosophila embryos. J. Mol. Biol. 203, 425–437 (1988).

    Article  CAS  Google Scholar 

  27. Hovemann, B. T., Dessen, E., Mechler, H. & Mack, E. Drosophila snRNP associated protein P11 which specifically binds to heat shock puff 93D reveals strong homology with hnRNP core protein A1. Nucleic Acids Res. 19, 4909–4914 (1991).

    Article  CAS  Google Scholar 

  28. Kennerdell, J. R. & Carthew, R. W. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the Wingless pathway. Cell 95, 1017–1026 (1998).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  30. Oda, H., Uemura, T., Harada, Y., Iwai, Y. & Takeichi, M. A Drosophila homolog of cadherin associated with armadillo and essential for embryonic cell–cell adhesion. Dev. Biol. 165, 716–726 (1994).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank N. Brown, B. Hovemann, M. Schäfer and C. M. Schuster for cDNA libraries, M. A. Bhat, D. Cavener and T. Uemura for antibodies, A. Ramrath for help with the yeast two-hybrid assay, and J. A. Campos-Ortega, K. Johnson, A. Müller and A. Wodarz for discussions and critical reading of the manuscript. The work was supported by the Deutsche Forschungsgemeinschaft and the Fonds der Chemischen Industrie.

Author information

Author notes

  1. Martina Schneider

    Present address: Department of Cell & Molecular Biology, Lund University, S-22184, Lund, Sweden

Authors and Affiliations

  1. Institut für Genetik, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, Düsseldorf, 40225, Germany

    André Bachmann, Martina Schneider, Eva Theilenberg, Ferdi Grawe & Elisabeth Knust

Authors
  1. André Bachmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martina Schneider
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eva Theilenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ferdi Grawe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elisabeth Knust
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elisabeth Knust.

Supplementary information

Figure 3.1

(JPG 175 KB)

Table 1. The MAGUK domain of Stardust binds to the cytoplasmic tail of Crumbs
Full size table
Table 2. Primer collection
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bachmann, A., Schneider, M., Theilenberg, E. et al. Drosophila Stardust is a partner of Crumbs in the control of epithelial cell polarity. Nature 414, 638–643 (2001). https://doi.org/10.1038/414638a

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/414638a

This article is cited by

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

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