Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-05T11:00:17.009Z Has data issue: false hasContentIssue false

Stippling the Skin: Generation of Anatomical Periodicityby Reaction-Diffusion Mechanisms

Published online by Cambridge University Press:  11 July 2009

D. J. Headon*
Affiliation:
The Roslin Institute and Royal (Dick) School of Veterinary Studies University of Edinburgh, Midlothian, EH25 9PS, UK
K. J. Painter
Affiliation:
Department of Mathematics and Maxwell Institute for Mathematical Sciences, School of Mathematical and Computer Sciences, Heriot-Watt University, Edinburgh, EH14 4AS, UK
Get access

Abstract

During vertebrate development cells acquire different fates depending largely ontheir location in the embryo. The definition of a cell's developmentalfate relies on extensive intercellular communication that produces positionalinformation and ultimately generates an appropriately proportioned anatomy. Herewe place reaction-diffusion mechanisms in the context of general conceptsregarding the generation of positional information during development and thenfocus on these mechanisms as parsimonious systems for positioning anatomicalstructures relative to one another. In particular, we discuss the evidence forreaction-diffusion systems operating in the developing skin to yield theperiodic arrangements of hairs and feathers and discuss how best tobring together experimental molecular biology and numerical simulations to yielda more complete understanding of the mechanisms of development and naturalvariation.

Type
Research Article
Copyright
© EDP Sciences, 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abreu, J. G., Ketpura, N. I., Reversade, B., De Robertis, E. M.. Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta. Nat. Cell Biol., 4 (2002), 599604.
Akam, M.. Drosophila development: making stripes inelegantly. Nature, 341 (1989), 282283. CrossRef
Andl, T., Reddy, S. T., Gaddapara, T., Millar, S. E.. WNT signals are required for the initiation of hair follicle development. Dev. Cell, 2 (2002), 643653. CrossRef
Armstrong, N. J., Painter, K. J., Sherratt, J. A.. A continuum approach to modelling cell-cell adhesion. J. Theor. Biol., 243 (2006), 98113. CrossRef
Atit, R., Conlon, R. A., Niswander, L.. EGF signaling patterns the feather array by promoting the interbud fate. Dev. Cell, 4 (2003), 231240. CrossRef
Baker, R. E., Schnell, S., Maini, P. K.. A clock and wavefront mechanism for somite formation. Dev. Biol., 293 (2006), 116126. CrossRef
Balemans, W., Van Hul, W.. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol., 250 (2002), 231250. CrossRef
Cooke, J., Zeeman, E. C.. A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J. Theor. Biol., 58 (1976), 455476. CrossRef
Crampin, E. J., Gaffney, E. A., Maini, P. K.. Reaction and diffusion on growing domains: Scenarios for robust pattern formation. Bull. Math. Biol., 61 (1999), 10931120. CrossRef
Cui, Y., Hackenmiller, R., Berg, L., Jean, F., Nakayama, T., Thomas, G., Christian, J. L.. The activity and signaling range of mature BMP-4 is regulated by sequential cleavage at two sites within the prodomain of the precursor. Genes Dev., 15 (2001), 27972802.
Drew, C. F., Lin, C. M., Jiang, T. X., Blunt, G., Mou, C., Chuong, C. M., Headon, D. J.. The Edar subfamily in feather placode formation. Dev. Biol., 305 (2007), 232245. CrossRef
R. Dillon, P. K. Maini, H. G. Othmer Pattern formation in generalised Turing systems. I. Steady state patterns in systems with mixed boundary conditions. J. Math. Biol., 32 (1994), 345–393.
Eaton, S.. Release and trafficking of lipid-linked morphogens. Curr. Opin. Genet. Dev., 16 (2006), 1722. CrossRef
Gaffney, E. A., Monk, N. A.. Gene expression time delays and Turing pattern formation systems. Bull. Math. Biol., 68 (2006), 99130. CrossRef
Gierer, A., Meinhardt, H.. A theory of biological pattern formation. Kybernetik, 12 (1972), 3039. CrossRef
S.F. Gilbert. Developmental biology. Sinauer Associates, Sunderland, 2006.
Harding, K., Hoey, T., Warrior, R., Levine, M.. Autoregulatory and gap gene response elements of the even-skipped promoter of Drosophila. EMBO J., 8 (1989), 12051212.
Harris, M. P., Williamson, S., Fallon, J. F., Meinhardt, H., Prum, R. O.. Molecular evidence for an activator-inhibitor mechanism in development of embryonic feather branching. Proc. Natl. Acad. Sci. U.S.A., 102 (2005), 1173411739. CrossRef
Houghton, L., Lindon, C., Morgan, B. A.. The ectodysplasin pathway in feather tract development. Development, 132 (2005), 863872. CrossRefPubMed
Jiang, T. X., Jung, H. S., Widelitz, R. B., Chuong, C. M.. Self-organization of periodic patterns by dissociated feather mesenchymal cells and the regulation of size, number and spacing of primordia. Development, 126 (1999), 49975009. PubMed
Jiang, T. X., Widelitz, R. B., Shen, W. M., Will, P., Wu, D. Y., Lin, C. M., Jung, H. S., Chuong, C. M.. Integument pattern formation involves genetic and epigenetic controls: feather arrays simulated by digital hormone models. Int. J. Dev. Biol., 48 (2004), 117135. CrossRef
Jung, H. S., Francis-West, P. H., Widelitz, R. B., Jiang, T. X., Ting-Berreth, S., Tickle, C., Wolpert, L., Chuong, C. M.. Local inhibitory action of BMPs and their relationships with activators in feather formation: implications for periodic patterning. Dev. Biol., 196 (1998), 1123. CrossRef
Kashiwagi, M., Kuroki, T., Huh, N.. Specific inhibition of hair follicle formation by epidermal growth factor in an organ culture of developing mouse skin. Dev. Biol., 189 (1997), 2232. CrossRef
Keller, E. F., Segel, L. A.. Initiation of slime mold aggregation viewed as an instability. J. Theor. Biol., 26 (1970), 399415. CrossRef
Kondo, S.. The reaction-diffusion system: a mechanism for autonomous pattern formation in the animal skin. Genes Cells, 7 (2002), 535541. CrossRef
Laurikkala, J., Pispa, J., Jung, H. S., Nieminen, P., Mikkola, M., Wang, X., Saarialho-Kere, U., Galceran, J., Grosschedl, R., Thesleff, I.. Regulation of hair follicle development by the TNF signal ectodysplasin and its receptor Edar. Development, 129 (2002), 25412553. PubMed
Mandler, M., Neubüser, A.. FGF signaling is required for initiation of feather placode development. Development, 131 (2004), 33333343. CrossRefPubMed
H. Meinhardt. Models for positional signalling with application to the dorsoventral patterning of insects and segregation into different cell types. Development, 107 Suppl (2004), 169–180.
Mooney, J. R., Nagorcka, B. N.. Spatial patterns produced by a reaction-diffusion system in primary hair follicles. J. Theor. Biol., 115 (1985), 299317. CrossRef
Mou, C., Jackson, B., Schneider, P., Overbeek, P. A., Headon, D. J.. Generation of the primary hair follicle pattern. Proc. Natl. Acad. Sci. U.S.A., 103 (2006), 90759080. CrossRef
Murray, J. D.. Pattern formation in integrative biology–a marriage of theory and experiment. C. R. Acad. Sci. III, 323 (2000), 514. CrossRef
Murray, J. D.. On the mechanochemical theory of biological pattern formation with application to vasculogenesis. C. R. Biol., 326 (2003), 239252. CrossRef
Nagorcka, B. N., Mooney, J. R.. The role of a reaction-diffusion system in the initiation of primary hair follicles. J. Theor. Biol., 114 (1985), 243272. CrossRef
Narhi, K., Jarvinen, E., Birchmeier, W., Taketo, M. M., Mikkola, M. L., Thesleff, I.. Sustained epithelial beta-catenin activity induces precocious hair development but disrupts hair follicle down-growth and hair shaft formation. Development, 135 (2008), 10191028. CrossRefPubMed
Noramly, S., Freeman, A., Morgan, B. A.. beta-catenin signaling can initiate feather bud development. Development, 126 (1999), 35093521. PubMed
Noramly, S., Morgan, B. A.. BMPs mediate lateral inhibition at successive stages in feather tract development. Development, 125 (1998), 37753787. PubMed
Painter, K. J., Maini, P. K., Othmer, H. G.. Stripe formation in juvenile Pomacanthus explained by a generalized turing mechanism with chemotaxis. Proc. Natl. Acad. Sci. U.S.A., 96 (1999), 55495554. CrossRef
Patel, K., Makarenkova, H., Jung, H. S.. The role of long range, local and direct signalling molecules during chick feather bud development involving the BMPs, follistatin and the Eph receptor tyrosine kinase Eph-A4. Mech. Dev., 86 (1999), 5162. CrossRef
Paus, R., Cotsarelis, G.. The biology of hair follicles. N. Engl. J. Med., 341 (1999), 491497. CrossRef
Salazar-Ciudad, I., Jernvall, J., Newman, S. A.. Mechanisms of pattern formation in development and evolution. Development, 130 (2003), 20272037. CrossRefPubMed
Schmidt-Ullrich, R., Paus, R.. Molecular principles of hair follicle induction and morphogenesis. Bioessays, 27 (2005), 247261. CrossRef
P. Sengel. Morphogenesis of skin. CUP, Cambridge, 1976.
Sick, S., Reinker, S., Timmer, J., Schlake, T.. WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism. Science, 314 (2006), 14471450. CrossRef
Song, H., Wang, Y., Goetinck, P. F.. Fibroblast growth factor 2 can replace ectodermal signaling for feather development. Proc. Natl. Acad. Sci. U.S.A., 93 (1996), 1024610249. CrossRef
Teleman, A. A., Strigini, M., Cohen, S. M.. Shaping morphogen gradients. Cell, 105 (2001), 559562. CrossRef
Turing, A.M.. The chemical basis of morphogenesis. Phil. Trans. Roy. Soc. Lond. B, 237 (1952), 3772. CrossRef
Turk, G.. Generating textures on arbitrary surfaces using reaction-diffusion. Comp. Graphics, 25 (1991), 289298. CrossRef
Vincent, J.P., Briscoe, J.. Morphogens. Curr. Biol., 11 (2001), R851854. CrossRef
Widelitz, R. B., Jiang, T. X., Lu, J., Chuong, C. M.. beta-catenin in epithelial morphogenesis: conversion of part of avian foot scales into feather buds with a mutated beta-catenin. Dev. Biol., 219 (2000), 98114. CrossRef
L. Wolpert. Principles of development. OUP, Oxford, 2006.
Yamaguchi, M., Yoshimoto, E., Kondo, S.. Pattern regulation in the stripe of zebrafish suggests an underlying dynamic and autonomous mechanism. Proc. Natl. Acad. Sci. U.S.A., 104 (2007), 47904793. CrossRef
Yoshida, K., Munakata, H.. Connective tissue growth factor binds to fibronectin through the type I repeat modules and enhances the affinity of fibronectin to fibrin. Biochim. Biophys. Acta, 1770 (2007), 672680. CrossRef
Yu, M., Yue, Z., Wu, P., Wu, D. Y., Mayer, J. A., Medina, M., Widelitz, R. B., Jiang, T. X., Chuong, C. M.. The biology of feather follicles. Int. J. Dev. Biol., 48 (2004), 181191. CrossRef