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Noggin and retinoic acid transform the identity of avian facial prominences

Nature volume 414, pages 909–912 (2001)Cite this article

Abstract

The signals that determine body part identity in vertebrate embryos are largely unknown, with some exceptions such as those for teeth and digits1,2. The vertebrate face is derived from small buds of tissue, facial prominences, that surround the embryonic oral cavity3. In chicken embryos, the skeleton of the upper beak is derived from the frontonasal mass and maxillary prominences4. Here we show that bone morphogenetic proteins (Bmps) and the vitamin A derivative, retinoic acid (RA), are used to specify the identity of the frontonasal mass and maxillary prominences. Implanting two beads adjacent to the stage-15 presumptive maxillary field, one soaked in the Bmp antagonist Noggin5 and one soaked in RA, induces a duplicate set of frontonasal mass skeletal elements in place of maxillary bones. We also show that the duplicated beak is due to transformation of the maxillary prominence into a second frontonasal mass and not due to ectopic migration of cells or splitting of the normal frontonasal mass. Thus the levels of Bmp and RA determine whether specific regions of the face form maxillary or frontonasal mass derivatives.

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Figure 1: Development of facial prominences and their derivatives.
Figure 2: Duplicated beak phenotype.
Figure 3: Ontogeny of the duplicated beak phenotype.
Figure 4: Increased Bmp7 and Bmp2 expression in treated maxillary prominences.

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References

  1. Tucker, A. S., Matthews, K. L. & Sharpe, P. T. Transformation of tooth type induced by inhibition of BMP signaling. Science 282, 1136–1138 (1998).

    Article  CAS  Google Scholar 

  2. Drossopoulou, G. et al. A model for anterioposterior patterning of the vertebrate limb based on sequential long- and short-range Shh signalling and Bmp signalling. Development 127, 1337–1348 (2000).

    CAS  PubMed  Google Scholar 

  3. Haeckel, E. H. P. A. The Evolution of Man. A Popular Exposition of the Principal Points of Human Ontogeny and Phylogeny (Appleton, New York, 1886).

    Google Scholar 

  4. Le Lièvre, C. S. Participation of neural crest-derived cells in the genesis of the skull in birds. J. Embryol. Exp. Morph. 47, 17–37 (1978).

    PubMed  Google Scholar 

  5. Zimmerman, L. B., De Jesus-Escobar, J. M. & Harland, R. M. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599–606 (1996).

    Article  CAS  Google Scholar 

  6. Noden, D. M. The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev. Biol. 96, 144–165 (1983).

    Article  CAS  Google Scholar 

  7. Couly, G., Grapin-Botton, A., Coltey, P., Ruhin, B. & Le Douarin, N. M. Determination of the identity of the derivatives of the cephalic neural crest: incompatibility between Hox gene expression and lower jaw development. Development 125, 3445–3459 (1998).

    CAS  PubMed  Google Scholar 

  8. Lumsden, A., Sprawson, N. & Graham, A. Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 113, 1281–1291 (1991).

    CAS  PubMed  Google Scholar 

  9. Mina, M. & Kollar, E. J. The induction of odontogenesis in non-dental mesenchyme combined with early murine mandibular arch epithelium. Arch. Oral Biol. 32, 123–127 (1987).

    Article  CAS  Google Scholar 

  10. Hamburger, V. & Hamilton, H. A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49–92 (1951).

    Article  CAS  Google Scholar 

  11. Richman, J. M. & Tickle, C. Epithelia are interchangeable between facial primordia of chick embryos and morphogenesis is controlled by the mesenchyme. Dev. Biol. 136, 201–210 (1989).

    Article  CAS  Google Scholar 

  12. Rodriguez-Esteban, C. et al. The T-box genes Tbx4 and Tbx5 regulate limb outgrowth and identity. Nature 398, 814–818 (1999).

    Article  CAS  Google Scholar 

  13. Takeuchi, J. K. et al. Tbx5 and Tbx4 genes determine the wing/leg identity of limb buds. Nature 398, 810–814 (1999).

    Article  CAS  Google Scholar 

  14. Francis-West, P. H., Tatla, T. & Brickell, P. Expression patterns of the bone morphogenetic protein genes Bmp-4 and Bmp-2 in the developing chick face suggest a role in the outgrowth of the primordia. Dev. Dyn. 201, 168–178 (1994).

    Article  CAS  Google Scholar 

  15. Wall, N. A. & Hogan, B. L. Expression of bone morphogenetic protein-4 (BMP-4), bone morphogenetic protein-7 (BMP-7), fibroblast growth factor-8 (FGF-8) and sonic hedgehog (SHH) during branchial arch development in the chick. Mech. Dev. 53, 383–392 (1995).

    Article  CAS  Google Scholar 

  16. Niederreither, K., Subbarayan, V., Dolle, P. & Chambon, P. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nature Genet. 21, 444–448 (1999).

    Article  CAS  Google Scholar 

  17. Schneider, R. A., Hu, D., Rubenstein, J. L., Maden, M. & Helms, J. A. Local retinoid signaling coordinates forebrain and facial morphogenesis by maintaining FGF8 and SHH. Development 128, 2755–2767 (2001).

    CAS  PubMed  Google Scholar 

  18. Barlow, A. J., Bogardi, J. P., Ladher, R. & Francis-West, P. H. Expression of chick Barx-1 and its differential regulation by FGF-8 and BMP signaling in the maxillary Primordia. Dev. Dyn. 214, 291–302 (1999).

    Article  CAS  Google Scholar 

  19. Shigetani, Y., Nobusada, Y. & Kuratani, S. Ectodermally derived FGF8 defines the maxillomandibular region in the early chick embryo: epithelial-mesenchymal interactions in the specification of the craniofacial ectomesenchyme. Dev. Biol. 228, 73–85 (2000).

    Article  CAS  Google Scholar 

  20. Brown, J. M. et al. Experimental analysis of the control of expression of the homeobox-gene Msx-1 in the developing limb and face. Development 119, 41–48 (1993).

    CAS  PubMed  Google Scholar 

  21. Hu, D. & Helms, J. A. The role of sonic hedgehog in normal and abnormal craniofacial morphogenesis. Development 126, 4873–4884 (1999).

    CAS  PubMed  Google Scholar 

  22. Eichele, G., Tickle, C. & Alberts, B. M. Microcontrolled release of biologically active compounds in chick embryos: Beads of 200-µm diameter for the local release of retinoids. Anal. Biochem. 142, 542–555 (1984).

    Article  CAS  Google Scholar 

  23. Fallon, J. F. et al. FGF-2: Apical ectodermal ridge growth signal for chick limb development. Science 264, 104–107 (1994).

    Article  CAS  Google Scholar 

  24. Barlow, A. J. & Francis-West, P. H. Ectopic application of recombinant BMP-2 and BMP-4 can change patterning and developing chick facial primordia. Development 124, 391–398 (1997).

    CAS  PubMed  Google Scholar 

  25. Shen, H. et al. Chicken transcription factor AP-2: Cloning, expression and its role in outgrowth of facial prominences and limb buds. Dev. Biol. 188, 248–266 (1997).

    Article  CAS  Google Scholar 

  26. Richman, J. M. & Tickle, C. Epithelial-mesenchymal interactions in the outgrowth of limb buds and facial primordia in chick embryos. Dev. Biol. 154, 299–308 (1992).

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank Regeneron for generously supplying Noggin protein, L. Niswander, C. Overall, C. Stern, T. Underhill, G. Hunter and V. Diewert for providing critical comments on the manuscript, C. Overall for stimulating discussions, M. A. Ashique for developing the enriching method of bead soaking and A. Wong for help with SEM. This work was funded by a CIHR grant to J.M.R. and salary support from Gyeongsang National University, Chinju, Korea for S.-H.L.

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Authors and Affiliations

  1. Department of Oral Health Science, Faculty of Dentistry, University of British Columbia, Vancouver, V6T 1Z3, British Columbia, Canada

    S.-H. Lee, K. K. Fu, J. N. Hui & J. M. Richman

  2. Department of Dentistry, Medical College, Gyeongsang National University, Chinju, Korea

    S.-H. Lee

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  1. S.-H. Lee
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  2. K. K. Fu
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  4. J. M. Richman
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Correspondence to J. M. Richman.

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Lee, SH., Fu, K., Hui, J. et al. Noggin and retinoic acid transform the identity of avian facial prominences. Nature 414, 909–912 (2001). https://doi.org/10.1038/414909a

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