1097-0177/asset/DVDY_left.gif?v=1&s=b87335326ab8ecd1f573539da0b5fa6abef26532)
Special Issue Research Article
You have full text access to this OnlineOpen article
Sharp developmental thresholds defined through bistability by antagonistic gradients of retinoic acid and FGF signaling
Article first published online: 11 MAY 2007
DOI: 10.1002/dvdy.21193
Copyright © 2007 Wiley-Liss, Inc.
Issue
Developmental Dynamics
Special Issue: Special Focus on Segmentation
Volume 236, Issue 6, pages 1495–1508, June 2007
Additional Information
How to Cite
Goldbeter, A., Gonze, D. and Pourquié, O. (2007), Sharp developmental thresholds defined through bistability by antagonistic gradients of retinoic acid and FGF signaling. Dev. Dyn., 236: 1495–1508. doi: 10.1002/dvdy.21193
Publication History
- Issue published online: 16 MAY 2007
- Article first published online: 11 MAY 2007
- Manuscript Accepted: 6 APR 2007
Funded by
- Fonds de la Recherche Scientifique Médicale. Grant Number: 3.4636.04
- European Union through the Network of Excellence BioSim. Grant Number: LSHB-CT-2004-005137
- Belgian Programme on Interuniversity Attraction Poles; Project: P6/22 BioMagnet
- National Institutes of Health. Grant Number: R01HD043158
- Defense Advanced Research Projects Agency (DARPA) FunBio Program. Grant Number: HR0011-05-1-0057
REFERENCES
- , , . 2002. MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science 297: 1018–1023.
- , , . 2003. Retinoic acid signalling centres in the avian embryo identified by sites of expression of synthesising and catabolising enzymes. Dev Dyn 227: 114–127.Direct Link:
- , , , , . 2005. Robust formation of morphogen gradients. Phys Rev Lett 94: 018103.
- , . 1996. Antagonistic interactions between wingless and decapentaplegic responsible for dorsal-ventral pattern in the Drosophila Leg. Science 273: 1373–1377.
- , . 2001. Patterning mechanisms controlling vertebrate limb development. Annu Rev Cell Dev Biol 17: 87–132.
- , . 2000. How to make a biological switch. J Theor Biol 203: 117–133.
- , , , . 1996. Pattern formation by lateral inhibition with feedback: a mathematical model of Delta-Notch intercellular signalling. J Theor Biol 183: 429–446.
- , . 1976. A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J Theor Biol 58: 455–476.
- , , , , . 2005. Control of the segmentation process by graded MAPK/ERK activation in the chick embryo. Proc Natl Acad Sci USA 102: 11343–11348.
- , , , , , , . 2006. A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science 314: 1595–1598.
- , . 1996. A common plan for dorsoventral patterning in Bilateria. Nature 380: 37–40.
- , . 2004. Opposing FGF and retinoid pathways: a signalling switch that controls differentiation and patterning onset in the extending vertebrate body axis. Bioessays 26: 857–869.Direct Link:
- , , , , , . 2003. Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40: 65–79.
- . 1981. AUTO: A program for the automatic bifurcation analysis of autonomous systems. (available at http://indy.cs.concordia.ca/auto/). Cong Numer 30:265–284.
- , . 2004. fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 427: 419–422.
- , , . 2001. FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106: 219–232.
- , , . 1989. A genetic switch, based on negative regulation, sharpens stripes in Drosophila embryos. Dev Genet 10: 124–142.Direct Link:
- , . 1987. Characterization of concentration gradients of a morphogenetically active retinoid in the chick limb bud. J Cell Biol 105: 1917–1923.
- 2002. Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr Opin Cell Biol 14: 140–148.
- , . 2002. Regulatory principles of developmental signaling. Annu Rev Cell Dev Biol 18: 515–539.
- , , . 2000. Construction of a genetic toggle switch in Escherichia coli. Nature 403: 339–342.
- , . 2000. Retinoid signalling and hindbrain patterning. Curr Opin Genet Dev 10: 380–386.
- , . 1990. Covalent modification of proteins as a threshold mechanism in development. J Theor Biol 142: 243–250.
- , , . 1998. Bistability in the isocitrate dehydrogenase reaction: an experimentally based theoretical study. Biophys J 74: 1229–1240.
- , , . 1991. The kinetics of mammalian gene expression. Bioessays 13: 667–674.Direct Link:
- , , . 2002. Establishment of developmental precision and proportions in the early Drosophila embryo. Nature 415: 798–802.
- , . 2005. Finding the center reliably: robust patterns of developmental gene expression. Phys Rev Lett 95: 208103.
- . 2004. Topology and robustness in the Drosophila segment polarity network. PLoS Biol 2: e123.
- , . 1996. Complementary and mutually exclusive activities of decapentaplegic and wingless organize axial patterning during Drosophila leg development. Cell 86: 401–409.
- . 1995. Model genetic circuits encoding autoregulatory transcription factors. J Theor Biol 172: 169–185.
- . 1997. Genes VI. Oxford, UK: Oxford University Press.
- . 2003. Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator. Curr Biol 13:1398–1408
- , , . 1977. Thresholds in development. J Theor Biol 65: 579–590.
- . 1985. A mechanism for memory storage insensitive to molecular turnover: a bistable autophosphorylating kinase. Proc Natl Acad Sci USA 82: 3055–3057.
- , , , . 1998. The distribution of endogenous retinoic acid in the chick embryo: implications for developmental mechanisms. Development 125: 4133–4144.
- , , . 2006. Embryonic pattern scaling achieved by oppositely directed morphogen gradients. Phys Biol 3: 107–120.
- , . 2000. Identification of human cytochrome P450 isoforms that contribute to all-trans-retinoic acid 4-hydroxylation. Biochem Pharmacol 60: 517–526.
- . 1982. Models of biological pattern formation. London: Academic Press.
- , , , . 2005. Threshold responses to morphogen gradients by zero-order ultrasensitivity. Mol Syst Biol 1: 2005.0028.
- , , . 1998. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet 18: 136–141.
- , . 1961. Teleonomic mechanisms in cellular metabolism, growth, and differentiation. Cold Spring Harb Symp Quant Biol 26: 389–401.
- , . 2004. Regulation of segmental patterning by retinoic acid signaling during Xenopus somitogenesis. Dev Cell 6: 205–218.
- , , , . 2005. The Mesp2 transcription factor establishes segmental borders by suppressing Notch activity. Nature 435: 354–359.
- , , , . 1999. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21: 444–448.
- , , , . 2003. A requirement for retinoic acid-mediated transcriptional activation in ventral neural patterning and motor neuron specification. Neuron 40: 81–95.
- , . 1989. Cell type and tissue distribution of the fibroblast growth factor receptor. J Cell Biochem 39: 443–454.Direct Link:
- , , , , . 2004. Multistability in the lactose utilization network of Escherichia coli. Nature 427: 737–740.
- , , , . 1997. Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesiss. Cell 91: 639–648.
- , , 2003. Building a cell cycle oscillator: hysteresis and bistability in the activation of Cdc2. Nat Cell Biol 5: 346–351.
- . 2003. The segmentation clock: converting embryonic time into spatial pattern. Science 301: 328–330.
- , , , , , . 2001. Fgf/MAPK signalling is a crucial positional cue in somite boundary formation. Development 128: 4873–4880.
- , . 2004. Endocytosis controls spreading and effective signaling range of Fgf8 protein. Curr Biol 14: 1834–1841.
- , , , , , , . 2003. Hysteresis drives cell-cycle transitions in Xenopus laevis egg extracts. Proc Natl Acad Sci USA 100: 975–980.
- , . 2004. Morphogens, their identification and regulation. Development 131: 703–712.
- , . 1990. Biological Feedback. Boca Raton, Fl: CRC Press.
- , . 2005. Retinoic acid coordinates somitogenesis and left-right patterning in vertebrate embryos. Nature 435: 215–220.
- , , , , , . 2005. Retinoic acid controls the bilateral symmetry of somite formation in the mouse embryo. Science 308: 563–566.
- , . 2002. Design and constraints of the Drosophila segment polarity module: robust spatial patterning emerges from intertwined cell state switches. J Exp Zool 294: 179–215.Direct Link:
- , . 2005. Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 434: 229–234.
- , 2003. A positive-feedback-based bistable 'memory module' that governs a cell fate decision. Nature 426: 460–465.
- , , , , , , , , . 2004. Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev Cell 6: 411–422.