Skip to main content

Thank you for visiting 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.

Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation


Shaping a developing organ or embryo relies on the spatial regulation of cell division and shape. However, morphogenesis also occurs through changes in cell-neighbourhood relationships produced by intercalation1,2. Intercalation poses a special problem in epithelia because of the adherens junctions, which maintain the integrity of the tissue. Here we address the mechanism by which an ordered process of cell intercalation directs polarized epithelial morphogenesis during germ-band elongation, the developmental elongation of the Drosophila embryo. Intercalation progresses because junctions are spatially reorganized in the plane of the epithelium following an ordered pattern of disassembly and reassembly. The planar remodelling of junctions is not driven by external forces at the tissue boundaries but depends on local forces at cell boundaries. Myosin II is specifically enriched in disassembling junctions, and its planar polarized localization and activity are required for planar junction remodelling and cell intercalation. This simple cellular mechanism provides a general model for polarized morphogenesis in epithelial organs.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Polarized junction remodelling underlies planar intercalation.
Figure 2: Myosin II-polarized localization.
Figure 3: Myosin II is required for junction remodelling.
Figure 4: Role of Rok during intercalation.


  1. Wallingford, J. B., Fraser, S. E. & Harland, R. M. Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev. Cell 2, 695–706 (2002)

    Article  CAS  Google Scholar 

  2. Keller, R. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298, 1950–1954 (2002)

    Article  ADS  CAS  Google Scholar 

  3. Irvine, K. D. & Wieschaus, E. Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. Development 120, 827–841 (1994)

    CAS  PubMed  Google Scholar 

  4. Lecuit, T. & Wieschaus, E. Junctions as organizing centers in epithelial cells? A fly perspective. Traffic 3, 92–97 (2002)

    Article  CAS  Google Scholar 

  5. Knust, E. & Bossinger, O. Composition and formation of intercellular junctions in epithelial cells. Science 298, 1955–1959 (2002)

    Article  ADS  CAS  Google Scholar 

  6. Nelson, W. J. Adaptation of core mechanisms to generate cell polarity. Nature 422, 766–774 (2003)

    Article  ADS  CAS  Google Scholar 

  7. Adams, C. L. & Nelson, W. J. Cytomechanics of cadherin-mediated cell–cell adhesion. Curr. Opin. Cell Biol. 10, 572–577 (1998)

    Article  CAS  Google Scholar 

  8. 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 

  9. Rivera-Pomar, R. & Jackle, H. From gradients to stripes in Drosophila embryogenesis: filling in the gaps. Trends Genet. 12, 478–483 (1996)

    Article  CAS  Google Scholar 

  10. Small, S., Kraut, R., Hoey, T., Warrior, R. & Levine, M. Transcriptional regulation of a pair-rule stripe in Drosophila. Genes Dev. 5, 827–839 (1991)

    Article  CAS  Google Scholar 

  11. Costa, M., Wilson, E. T. & Wieschaus, E. A putative cell signal encoded by the folded gastrulation gene coordinates cell shape changes during Drosophila gastrulation. Cell 76, 1075–1089 (1994)

    Article  CAS  Google Scholar 

  12. Kiehart, D. P. Molecular genetic dissection of myosin heavy chain function. Cell 60, 347–350 (1990)

    Article  CAS  Google Scholar 

  13. Karess, R. E. et al. The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell 65, 1177–1189 (1991)

    Article  CAS  Google Scholar 

  14. 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  Google Scholar 

  15. Lecuit, T., Samanta, R. & Wieschaus, E. slam encodes a developmental regulator of polarized membrane growth during cleavage of the Drosophila embryo. Dev. Cell 2, 425–436 (2002)

    Article  CAS  Google Scholar 

  16. Stein, J. A., Broihier, H. T., Moore, L. A. & Lehmann, R. Slow as Molasses is required for polarized membrane growth and germ cell migration in Drosophila. Development 129, 3925–3934 (2002)

    CAS  PubMed  Google Scholar 

  17. 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  Google Scholar 

  18. Hutson, M. S. et al. Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300, 145–149 (2003)

    Article  ADS  CAS  Google Scholar 

  19. Wolf, W. A., Chew, T. L. & Chisholm, R. L. Regulation of cytokinesis. Cell. Mol. Life Sci. 55, 108–120 (1999)

    Article  CAS  Google Scholar 

  20. Glotzer, M. Animal cell cytokinesis. Annu. Rev. Cell Dev. Biol. 17, 351–386 (2001)

    Article  CAS  Google Scholar 

  21. Jordan, P. & Karess, R. Myosin light chain-activating phosphorylation sites are required for oogenesis in Drosophila. J. Cell Biol. 139, 1805–1819 (1997)

    Article  CAS  Google Scholar 

  22. Wheatley, S., Kulkarni, S. & Karess, R. Drosophila nonmuscle myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos. Development 121, 1937–1946 (1995)

    CAS  PubMed  Google Scholar 

  23. Winter, C. G. et al. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105, 81–91 (2001)

    Article  CAS  Google Scholar 

  24. Uehata, M. et al. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990–994 (1997)

    Article  ADS  CAS  Google Scholar 

  25. Narumiya, S., Ishizaki, T. & Uehata, M. Use and properties of ROCK-specific inhibitor Y-27632. Methods Enzymol. 325, 273–284 (2000)

    Article  CAS  Google Scholar 

  26. Royou, A., Sullivan, W. & Karess, R. Cortical recruitment of nonmuscle myosin II in early syncytial Drosophila embryos: its role in nuclear axial expansion and its regulation by Cdc2 activity. J. Cell Biol. 158, 127–137 (2002)

    Article  CAS  Google Scholar 

  27. Johansen, K. A., Iwaki, D. D. & Lengyel, J. A. Localized JAK/STAT signaling is required for oriented cell rearrangement in a tubular epithelium. Development 130, 135–145 (2003)

    Article  CAS  Google Scholar 

  28. Jazwinska, A., Ribeiro, C. & Affolter, M. Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein. Nature Cell Biol. 5, 895–901 (2003)

    Article  CAS  Google Scholar 

  29. Tree, D. R., Ma, D. & Axelrod, J. D. A three-tiered mechanism for regulation of planar cell polarity. Semin. Cell Dev. Biol. 13, 217–224 (2002)

    Article  CAS  Google Scholar 

Download references


We thank J. M. Philippe and J. Della Rovere for their technical help; A. Pelissier for the staining shown in Fig. 2c; R. Karess, D. Kiehart and H. Oda for sending key reagents; F. Pilot and C. Henderson for insights; F. Schweisguth for a useful suggestion; and S. Cohen, J. Ewbank, C. Henderson, S. Kerridge, F. Pilot, O. Pourquié and J. Pradel for comments on the manuscript. Research in the Lecuit laboratory is supported by an ATIP grant from the CNRS, by the Fondation pour la Recherche Médicale, the Association pour la Recherche contre le Cancer and the EMBO Young Investigator Programme.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Thomas Lecuit.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure 1

Cell intercalation is not controlled by posterior-midgut invagination. (JPG 136 kb)

Supplementary Movie

Time-lapse confocal images of an embryo expressing E-cadherin-GFP at low levels during cell intercalation. (MP4 186 kb)

Supplementary Figure & Movie Legends (DOC 21 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bertet, C., Sulak, L. & Lecuit, T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667–671 (2004).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


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.


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