Movatterモバイル変換

[0]ホーム
URL:

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.

Advertisement

Nature
  • Letter
  • Published:

Dishevelled controls cell polarity duringXenopus gastrulation

Naturevolume 405, pages81–85 (2000)Cite this article

Abstract

Although cell movements are vital for establishing the normal architecture of embryos, it is unclear how these movements are regulated during development in vertebrates. Inhibition ofXenopus Dishevelled (Xdsh) function disrupts convergent extension movements of cells during gastrulation, but the mechanism of this effect is unclear, as cell fates are not affected1. InDrosophila, Dishevelled controls both cell fate and cell polarity2,3,4, but whether Dishevelled is involved in controlling cell polarity in vertebrate embryos has not been investigated. Here we show, using time-lapse confocal microscopy, that the failure of cells lacking Xdsh function to undergo convergent extension results from defects in cell polarity. Furthermore, Xdsh mutations that inhibit convergent extension correspond to mutations in Drosophila Dishevelled that selectively perturb planar cell polarity. Finally, the localization of Xdsh at the membrane of normal dorsal mesodermal cells is consistent with Xdsh controlling cell polarity. Our results show that polarized cell behaviour is essential for convergent extension and is controlled by vertebrate Dishevelled. Thus, a vertebrate equivalent of the Drosophila planar cell polarity signalling cascade may be required for normal gastrulation.

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

Access options

Access through your institution

Subscription info for Japanese customers

We have a dedicated website for our Japanese customers. Please go tonatureasia.com to subscribe to this journal.

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

￥ 4,980

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

Figure 1: Methods and signalling pathways.
Figure 2: Analysis of cell behaviour and polarity in Keller explants.
Figure 3: Analysis of convergent extension in Keller explants.
Figure 4: Xdsh constructs and their effects in Wnt, PCP and convergent extension assays. ++, strongly active; +, weakly active; -, weakly inhibitory; --, strongly inhibitory; nt, not tested.
Figure 5: Xdsh is localized to the membrane in cells undergoing convergent extension.

Similar content being viewed by others

References

  1. Sokol,S. Y. Analysis of Dishevelled signalling pathways duringXenopus development.Curr. Biol.6, 1456–1467 (1996).

    Article CAS  Google Scholar 

  2. 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  Google Scholar 

  3. Boutros,M., Paricio,N., Strutt,D. I. & Mlodzik,M. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling.Cell94, 109– 118 (1998).

    Article CAS  Google Scholar 

  4. Boutros,M. & Mlodzik,M. Dishevelled: at the crossroads of divergent intracellular signaling pathways.Mech. Dev. 83, 27–37 (1999).

    Article CAS  Google Scholar 

  5. Vogt,W. Gestaltungsanalyse am amphibienkeim mit örtlicher vitalfärbung. II. Teil. Gastrulation und mesodermbildung bei urodelen und anuran.Wilhelm Roux Arch. EntwMech. Org.120, 384–706 (1929).

    Article  Google Scholar 

  6. Keller,R., Shih,J., Wilson,P. & Sater,A. K. in49th Symp. Soc. Develop. Biol. Cell–Cell Interactions in Early Development (ed. Gerhart, J.) 93–107 (Wiley, New York, 1991).

    Google Scholar 

  7. Keller,R., Shih,J. & Domingo,C. The patterning and functioning of protrusive activity during convergence and extension of theXenopus organiser.Development (Suppl.) 81–91 (1992).

  8. Shih,J. & Keller,R. Patterns of cell motility in the organizer and dorsal mesoderm ofXenopuslaevis.Development116, 915–930 ( 1992).

    CAS PubMed  Google Scholar 

  9. Shih,J. & Keller,R. Cell motility driving mediolateral intercalation in explants ofXenopus laevis.Development116, 901–914 ( 1992).

    CAS PubMed  Google Scholar 

  10. Cadigan,K. M. & Nusse,R. Wnt signaling: a common theme in animal development.Genes Dev.11, 3286– 3305 (1997).

    Article CAS  Google Scholar 

  11. Miller,J. R. et al. Establishment of the dorsal-ventral axis inXenopus embryos coincides with the dorsal enrichment of dishevelled that is dependent on cortical rotation.J. Cell Biol.146, 427–437 (1999).

    Article CAS  Google Scholar 

  12. Wallingford,J. B., Sater,A. K., Uzman,J. A. & Danilchik,M. V. Inhibition of morphogenetic movement duringXenopus gastrulation by injected sulfatase: implications for anteroposterior and dorsoventral axis formation. Dev. Biol.187, 224–235 (1997).

    Article CAS  Google Scholar 

  13. Pierce,S. B. & Kimelman,D. Regulation of Spemann organizer formation by the intracellular kinase Xgsk-3.Development 121, 755–765 (1995).

    CAS PubMed  Google Scholar 

  14. Rothbächer,U. et al. Dishevelled phosphorylation, subcellular localization and homomerization regulate its role in early embryogenesis.EMBO J.19, 1010–1022 ( 2000).

    Article  Google Scholar 

  15. Howard,J. E. & Smith,J. C. Analysis of gastrulation: different types of gastrulation movement are induced by different mesoderm-inducing factors inXenopus laevis.Mech. Dev.43, 37–48 (1993).

    Article CAS  Google Scholar 

  16. Li,L. et al. Dishevelled proteins lead to two signaling pathways. Regulation of LEF- 1 and c-Jun N-terminal kinase in mammalian cells.J. Biol. Chem.274, 129–134 ( 1999).

    Article CAS  Google Scholar 

  17. Moriyoshi,K., Richards,L. J., Akazawa,C., O'Leary,D. D. & Nakanishi,S. Labeling neural cells using adenoviral gene transfer of membrane-targeted GFP.Neuron16, 255–260 (1996).

    Article CAS  Google Scholar 

Download references

Acknowledgements

We thank T. Grammer, M. Dionne, A. Sater, D. Keys, K. Liu and D. Frank for discussions, reading the manuscript, and blind scoring; S. Sokol for the Xdsh and Xdd1 plasmids; and D. Turner for the memEGFP plasmid. This work was supported by the NIH, NIMH and the Beckman Institute. J.B.W. was supported by NIH/NIGMS and ACS postdoctoral fellowships; B.A.R. by a US Department of Defense Breast Cancer Research Program Grant to C. Larabell; and K.M.V. by the Nathan and Violet David Scholars program at UC Berkeley.

Author information

Author notes

  1. Ute Rothbächer

    Present address: Labouratoire de Genetique et Physiologie du Development, IBDM, Campus de Luminy, Marseille, France

Authors and Affiliations

  1. Department of Molecular and Cell Biology, 401 Barker Hall, University of California, Berkeley, 94720-3204, California, USA

    John B. Wallingford, Kevin M. Vogeli & Richard M. Harland

  2. Life Sciences Division (MS6-2100) Lawrence Berkeley National Laboratory, Berkeley, 94720, California , USA

    Brian A. Rowning

  3. Division of Biology and Beckman Institute California Institute of Technology, Pasadena, 91125, California , USA

    Ute Rothbächer & Scott E. Fraser

Authors
  1. John B. Wallingford
  2. Brian A. Rowning
  3. Kevin M. Vogeli
  4. Ute Rothbächer
  5. Scott E. Fraser
  6. Richard M. Harland

Corresponding author

Correspondence toRichard M. Harland.

Rights and permissions

About this article

Cite this article

Wallingford, J., Rowning, B., Vogeli, K.et al. Dishevelled controls cell polarity duringXenopus gastrulation .Nature405, 81–85 (2000). https://doi.org/10.1038/35011077

Download citation

This article is cited by

Access through your institution
Buy or subscribe

Advertisement

Search

Advanced search

Quick links

Nature Briefing

Sign up for theNature 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
[8]ページ先頭
©2009-2026 Movatter.jp