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:

Calponin modulates the exclusion of Otx-expressing cells from convergence extension movements

Abstract

Otx2, a vertebrate homologue of the Drosophila orthodenticle gene, coordinates two processes in early embryonic development. Not only does it specify cell fate in the anterior regions of the embryo, it also prevents the cells that express it from participating in the convergence extension movements that shape the rest of the body axis. Here we show that, in Xenopus, this latter function is mediated by XclpH3, transcription of which is directly stimulated by Xotx2. XclpH3 is a Xenopus homologue of the mammalian calponin gene, the product of which binds both actin and myosin and prevents the generation of contractile force by actin filaments.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Phenotypes produced by ectopic expression of Xotx2 and XclpH3 , and pattern of XclpH3 expression.
Figure 2: XclpH3 is a direct target of Xotx2.
Figure 3: XclpH3 blocks convergence extension movements.
Figure 4: Rescue of the Xotx2 mutant phenotype with antisense XclpH3 mRNA, and post-translational modification of XclpH3 protein.

Similar content being viewed by others

References

  1. Lamb, T. M. et al. Neural induction by the secreted polypeptide noggin. Science 262, 713–718 ( 1993).

    Article  CAS  Google Scholar 

  2. Pannese, M. et al. The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. Development 121, 707–720 (1995).

    CAS  PubMed  Google Scholar 

  3. Blitz, I. L. & Cho, K. W. Y. Anterior neurectoderm is progressively induced during gastrulation: the role of the Xenopus homeobox gene orthodenticle. Development 121, 993– 1004 (1995).

    CAS  PubMed  Google Scholar 

  4. Boncinelli, E., Gulisano, M. & Broccoli, V. Emx and Otx homeobox genes in the developing mouse brain . J. Neurobiol. 24, 1356– 1366 (1993).

    Article  CAS  Google Scholar 

  5. Gammill, L. & Sive, H. Identification of otx2 target genes and restrictions in ectodermal competence during Xenopus cement gland formation. Development 124, 471– 481 (1997).

    CAS  PubMed  Google Scholar 

  6. Ang, S. L. et al. A targeted mouse Otx2 mutation leads to severe defects in gastrulation and formation of axial mesoderm and to deletion of rostral brain. Development 122, 243–252 (1996).

    CAS  PubMed  Google Scholar 

  7. Finkelstein, R., Smouse, D., Capaci, T. M., Spradling, A. C. & Perrimon, N. The orthodenticle gene encodes a novel homeodomain protein invovled in the development of the Drosophila nervous system and ocellar visual structures. Genes Dev. 4, 1516–1527 (1990).

    Article  CAS  Google Scholar 

  8. Finkelstein, R. & Perrimon, N. The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 346, 485–488 (1990).

    Article  CAS  Google Scholar 

  9. Keller, R. Early embryonic development of Xenopus laevis. Methods Cell Biol. 36, 61–113 ( 1991).

    Article  CAS  Google Scholar 

  10. Strasser, P., Gimona, M., Moessler, H., Herzog, M. & Small, V. J. Mammalian calponin: identification and expression of variants. FEBS Lett. 330, 13– 18 (1993).

    Article  CAS  Google Scholar 

  11. Shirinsky, V., Biryukov, K., Hettsch, J. & Sellers, J. Inhibition of the relative movement of actin and myosin by caldesmon and calponin . J. Biol. Chem., 306, 199– 204 (1992).

    Google Scholar 

  12. Andreazzoli, M., Pannese, M. & Boncinelli, E. Activating and repressing signals in head development: the role of Xotx1 and Xotx2. Development 124, 1733–1743 (1997).

    CAS  PubMed  Google Scholar 

  13. Keller, R., Shih, J. & Sater, A. The cellular basis of the convergence and extension of the Xenopus neural plate. Dev. Dyn. 193, 199– 217 (1992).

    Article  CAS  Google Scholar 

  14. Dale, L. & Slack, J. M. Fate map for the 32-cell stage of Xenopus laevis. Development 99, 527–551 (1987).

    CAS  PubMed  Google Scholar 

  15. Steinbeisser, H., Fainsod, A., Niehrs, C., Sasai, Y. & de Robertis, E. The role of gsc and BMP4 in dorsal-ventral patterning of the marginal zone in Xenopus: a loss-of-function study using antisense RNA. EMBO J. 14, 5230–5243 (1995).

    Article  CAS  Google Scholar 

  16. Ang, S. L. et al. A targeted mouse Otx2 mutation leads to severe defects in gastrulation and formation of axial mesoderm and to deletion of rostral brain . Development 122, 243– 252 (1996).

    CAS  PubMed  Google Scholar 

  17. El-Mezgueldi, M., Strasser, P., Fattoum, A. & Gimona, M. Expressing functional domains of mouse calponin: involvement of the region around alanine 145 in the actomyosin ATPase inhibitory activity of calponin . Biochemistry 35, 3654– 3661 (1996).

    Article  CAS  Google Scholar 

  18. Winder, S. J., Allen, B. G., Clement-Chomienne, O. & Walsh, M. P. Regulation of smooth muscle actin myosin interaction and force by calponin . Acta. Physiol. Scand. 164, 415– 426 (1998).

    Article  CAS  Google Scholar 

  19. Bhatia-Dey, N., Taira, M., Conti, M. A., Nooruddin, H. & Adelstein, R. S. Differential expression of non-muscle myosin heavy chain genes during Xenopus embryogenesis. Mech. Dev. 78, 33–36 (1998).

    Article  CAS  Google Scholar 

  20. Hardin, S. H., Carpenter, C. D., Hardin, P. E., Bruskin, A. M. & Klein, W. H. Structure of the Spec1 gene encoding a major calcium-binding protein in the embryonic ectoderm of the sea urchin, Strongylocentrotus purpuratus. J. Mol. Biol. 186, 243–255 ( 1985).

    Article  CAS  Google Scholar 

  21. Gan, L. et al. An orthodenticle-related protein from Strongylocentrotus purpuratus . Dev. Biol. 167, 517– 528 (1995).

    Article  CAS  Google Scholar 

  22. Mao, C. A. et al. Altering cell fates in sea urchin embryos by overexpressing SpOtx, and orthodenticle-related protein. Development 122, 1489–1498 (1996).

    CAS  PubMed  Google Scholar 

  23. Busse, U. & Seguin, C. Molecular analysis of the Wnt-1 proto-oncogene in Ambystoma mexicanum (axolotol) embryos. Differentiation 53, 7–15 (1993).

    Article  CAS  Google Scholar 

  24. Harland, R. M. In situ hybridization: an improved whole-mount method for Xenopus embryos . Methods Cell Biol. 36, 685– 695 (1991).

    Article  CAS  Google Scholar 

  25. Salisbury, J. R. & Watt, F. M. Lack of keratan sulphate in the human notochord. J. Anat. 157, 175–179 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Rokolya, A., Walsh, M. P. & Moreland, R. S. Calcium- and phorbol ester-dependent calponin phosphorylation in homogenates of swine cartoid artery. Am. J. Physiol. 271, H776–H783 (1996).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the EU training and mobility of researchers programme and the EU Biotech programme for supporting this research.

Correspondence and requests for materials should be addressed to R.M. The XclpH3 cDNA sequence has been deposited at GenBank under accession number AF081576.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Antony J. Durston.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morgan, R., Hooiveld, M., Pannese, M. et al. Calponin modulates the exclusion of Otx-expressing cells from convergence extension movements. Nat Cell Biol 1, 404–408 (1999). https://doi.org/10.1038/15635

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/15635

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