Skip to main content
Log in

On a tissue interaction model for skin pattern formation

  • Published:
Journal of Nonlinear Science Aims and scope Submit manuscript

Summary

There is now sound biological evidence that dermal-epidermal communication is essential in the formation of skin organs. Recent experimental results suggest that cell adhesion molecules (CAMs) play an important role during skin pattern formation. We describe here a tissue interaction model for pattern morphogenesis in vertebrate skin which includes such CAMs. A mechanochemical mechanism is used to describe epithelial sheet motion, and a reaction-diffusion-chemotaxis mechanism is used to model the dermal cell movements. Neither of the mechanisms can independently generate spatial patterns in their respective layers. Tissue interaction is introduced using morphogens produced separately in the dermis and epithelium. These morphogens diffuse across the basal lamina, which separates the epidermis and dermis, and induce cell movements and deformation. Analysis of a simplified one-dimensional version shows that under certain conditions spatial patterns can be formed. A nonlinear analysis predicts the solution behavior which is in close agreement with the numerical results.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., & Watson, J. D. (1989).Molecular Biology of the Cell. 2nd ed., New York, London: Garland Publishing, Inc.

    Google Scholar 

  • Bentil, D. E., & Murray, J. D. (1991). Pattern selection in biological pattern formation mechanisms.Appl. Math. Lett. 4(3), 1–6.

    Article  MathSciNet  MATH  Google Scholar 

  • Berridge, M. J. (1988). Inositol lipids and calcium signalling.Proc. R. Soc. Lond. (Biol.) 234, 359–378.

    Article  Google Scholar 

  • Chuong, C.-M., & Edelman, G. M. (1985a). Expression of cell adhesion molecules in embryonic induction. I. Morphogenesis of nestling feathers.J. Cell Biol. 101, 1009–1026.

    Article  Google Scholar 

  • Chuong, C.-M., & Edelman, G. M. (1985b). Expression of cell adhesion molecules in embryonic induction. II. Morphogenesis of adult feathers.J. Cell Biol. 101, 1027–1043.

    Article  Google Scholar 

  • Davidson, D. (1983a). The mechanism of feather pattern development in the chick. I. The time determination of feather position.J. Embryol. exp. Morph. 74, 245–259.

    Google Scholar 

  • Davidson, D. (1983b). The mechanism of feather pattern development in the chick. II. Control of the sequence of pattern formation.J. Embryol. exp. Morph. 74, 261–273.

    Google Scholar 

  • Dhouailly, D. (1973). Dermo-epidermal interactions between birds and mammals: differentiation of cutaneous appendages.J. Embryol, exp. Morph. 30, 587–603.

    Google Scholar 

  • Dhouailly, D. (1975). Formation of cutaneous appendages in dermo-epidermal recombination between reptiles, birds and mammals.Wilhelm Roux Arc. EntwMech. Org. 177, 323–340.

    Article  Google Scholar 

  • Dhouailly, D., & Maderson, P. F. A. (1984). Ultrastructural observations on the embryonic development of the integument ofLacerta muralis (Lacertilia, Reptilia).J. Morph. 179, 203–228.

    Article  Google Scholar 

  • Edelman, G. M. (1984). Cell adhesion and morphogenesis: The regulator hypothesis.Proc. Natl. Acad. Sci. USA 81, 1460–1464.

    Article  Google Scholar 

  • Edelman, G. M. (1985). Cell adhesion and the molecular process of morphogenesis.Ann. Rev. Biochem. 54, 135–169.

    Article  Google Scholar 

  • Edelman, G. M. (1986). Cell adhesion molecules in the regulation of animal form and tissue pattern.Annu. Rev. Cell Biol. 2, 81–116.

    Article  Google Scholar 

  • Edelman, G. M. (1988). Morphoregulatory molecules.Biochemistry,27(10), 3533–3543.

    Article  Google Scholar 

  • Erikson, C. A. (1990). Cell migration and adult organism.Curr. Op. Cell. Biol. 2, 67–74.

    Google Scholar 

  • Gallin, W. J., Chuong, C.-M., Finkel, L. H., & Edelman, G. M. (1986). Antibodies to liver cell adhesion molecules perturb inductive interactions and alter feather pattern and structure.Proc. Natl. Acad. Sci. USA 83, 8235–8239.

    Article  Google Scholar 

  • Grumet, M., & Edelman, G. M. (1988). Neuron-glia cell adhesion molecules interacts with neurons and astroglia via different binding mechanisms.J. Cell Biol. 106, 487–503.

    Article  Google Scholar 

  • Hoffman, S., & Edelman, G. M. (1983). Kinetics of homophylic binding by embryonic and adult forms of the neural cell adhesion molecule.Proc. Natl. Acad. Sci. USA 80, 5762–5766.

    Article  Google Scholar 

  • Kolega, J. (1986). Effects of mechanical tension on protusive activity and microfilament and intermediate filaments organization in an epithelium moving in culture.J. Cell Biol. 102, 1400–1411.

    Article  Google Scholar 

  • Landau, L. D., & Lifshitz, E. M. (1970).Theory of Elasticity. 2nd ed., New York: Pergamon.

    Google Scholar 

  • Mooney, J. D., & Nagorcka, B. N. (1985). Spatial patterns produced by a reaction-diffusion system in primary hair follicles.J. Theor. Biol. 115, 229–317.

    MathSciNet  Google Scholar 

  • Murray, J. D. (1989).Mathematical Biology. Heidelberg: Springer Verlag.

    MATH  Google Scholar 

  • Murray, J. D., & Oster, G. F. (1984a). Cell traction models for generating pattern and form in morphogenesis.J. Math Biol. 19, 265–279.

    MathSciNet  MATH  Google Scholar 

  • Murray, J. D., & Oster, G. F. (1984b). Generation of biological pattern and form.IMA J. Maths Appl. Med. & Biol. 1, 51–75.

    MathSciNet  MATH  Google Scholar 

  • Murray, J. D., Oster, G. F., & Harris, A. K. (1983). A mechanical model for mesenchymal morphogenesis.J. Math Biol. 17, 125–129.

    Article  MATH  Google Scholar 

  • Nagorcka, B. N. (1984). Evidence for a reaction-diffusion system in the formation of hair fibres.Biosystems 16, 323–332.

    Article  Google Scholar 

  • Nagorcka, B. N. (1986). The role of a reaction-diffusion system in the initiation of skin organ primordia. I. The first wave of initiation.J. Theor. Biol. 121, 449–475.

    Google Scholar 

  • Nagorcka, B. N., Manorjan, V. S., & Murray, J. D. (1987). Complex spatial patterns from tissue interactions—an illustrative model.J. Theor. Biol. 128, 359–374.

    Google Scholar 

  • Nagorcka, B. N., & Mooney, J D. (1982). The role of a reaction-diffusion system in the formation of hair fibres.J. Theor. Biol. 98, 575–607.

    Article  MathSciNet  Google Scholar 

  • Nagorcka, B. N., & Mooney, J. D. (1985). The role of a reaction-diffusion system in the initiation of primary hair follicles.J. Theor. Biol. 114, 243–272.

    MathSciNet  Google Scholar 

  • Oster, G. F., & Murray, J. D (1989). Pattern formation models and developmental constraints.J. Exp. Zool. 251, 186–202.

    Article  Google Scholar 

  • Oster, G. F., Murray, J. D., & Harris, A. K. (1983). Mechanical aspects of mesenchymal morphogenesis.J. Embryol exp. Morph. 78, 83–125.

    Google Scholar 

  • Oster, G. F., & Odell, G. M. (1984). The mechanochemistry of cytogels.Physica 12D, 333–350.

    MathSciNet  Google Scholar 

  • Plickert, G. (1980). Mechanical induced stolon branching inEirene viridula (Thecata, Campanulinidae). In:Development and Cellular Biology of Coelenterates. (Eds. Tardent, P. & Tardent, R.). Amsterdam: Elsevier (North Holland).

    Google Scholar 

  • Rawles, M. (1963). Tissue interactions in scale and feather development as studied in dermal epidermal recombinations.J. Embryol. exp. Morph. 11, 765–789.

    Google Scholar 

  • Sengel, P. (1976).Morphogenesis of Skin, Cambridge: Cambridge University Press.

    Google Scholar 

  • Shaw, L. J., & Murray, J. D. (1990). Model for complex skin patterns.SIAM J. Appl. Math. 50(2), 628–648

    Article  MathSciNet  MATH  Google Scholar 

  • Turing, A. M. (1952). The chemical basis of morphogenesis.Phil. Trans. Roy. Soc. Lond. B237, 37–72.

    Google Scholar 

  • Wolpert, L. (1969). Positional information and the spatial pattern of cellular differentiation.J. Theor Biol. 25, 1–47.

    Google Scholar 

  • Wolpert, L. (1971). Positional information and pattern formation.Curr. Top. Dev. Biol. 6, 183–224.

    Article  Google Scholar 

  • Wolpert, L. (1981) Positional information and pattern formation.Phil. Trans. Roy Soc. Lond. B295, 441–450.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by Stephen Wiggins

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cruywagen, G.C., Murray, J.D. On a tissue interaction model for skin pattern formation. J Nonlinear Sci 2, 217–240 (1992). https://doi.org/10.1007/BF02429856

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02429856

Key words

Navigation