Mutual regulation of decapentaplegic and hedgehog during the initiation of differentiation in the Drosophila retina.

Neuronal differentiation in the Drosophila retinal primordium, the eye imaginal disc, begins at the posterior tip of the disc and progresses anteriorly as a wave. The morphogenetic furrow (MF) marks the boundary between undifferentiated anterior cells and differentiating posterior cells. Anterior progression of differentiation is driven by Hedgehog, synthesized by cells located posterior to the MF. We report here that hedgehog (hh), which is expressed prior to the start of differentiation along the disc's posterior margin, also plays a crucial role in the initiation of differentiation. Using a temperature-sensitive allele we show that hh is normally required at the posterior margin to maintain the expression of decapentaplegic (dpp) and of the proneural gene atonal. In addition, we find that ectopic differentiation driven by ectopic dpp expression or loss of wingless function requires hh. Consistent with this is our observation that ectopic dpp induces the expression of hh along the anterior margin even in the absence of differentiation. Taken together, these data reveal a novel positive regulatory loop between dpp and hh that is essential for the initiation of differentiation in the eye disc.

[1]  U. Heberlein,et al.  Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. , 1997, Development.

[2]  N. Perrimon,et al.  Altering the insertional specificity of a Drosophila transposable element. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[3]  A. Tomlinson The cellular dynamics of pattern formation in the eye of Drosophila. , 1985, Journal of embryology and experimental morphology.

[4]  N. Perrimon,et al.  Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. , 1993, Development.

[5]  S. Zipursky,et al.  Induction of Drosophila eye development by decapentaplegic. , 1997, Development.

[6]  N. Patel,et al.  Differential splicing generates a nervous system—Specific form of drosophila neuroglian , 1990, Neuron.

[7]  A. Brand,et al.  Specificity of bone morphogenetic protein-related factors: cell fate and gene expression changes in Drosophila embryos induced by decapentaplegic but not 60A. , 1994, Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research.

[8]  M. Noll,et al.  The Drosophila smoothened Gene Encodes a Seven-Pass Membrane Protein, a Putative Receptor for the Hedgehog Signal , 1996, Cell.

[9]  K. Basler,et al.  Hedgehog signaling in Drosophila eye and limb development — conserved machinery, divergent roles? , 1997, Current Opinion in Neurobiology.

[10]  S. Zipursky,et al.  The Eye-Specification Proteins So and Eya Form a Complex and Regulate Multiple Steps in Drosophila Eye Development , 1997, Cell.

[11]  G. Rubin,et al.  cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in drosophila imaginal discs , 1995, Cell.

[12]  V. Hartenstein,et al.  The drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system , 1994, Neuron.

[13]  K. Basler,et al.  Hedgehog-dependent patterning in the Drosophila eye can occur in the absence of Dpp signaling. , 1996, Developmental biology.

[14]  D. Strutt,et al.  Hedgehog is an indirect regulator of morphogenetic furrow progression in the Drosophila eye disc. , 1997, Development.

[15]  U. Heberlein,et al.  Mechanisms of drosophila retinal morphogenesis: The virtues of being progressive , 1995, Cell.

[16]  C. Desplan,et al.  Eye Development: Governed by a Dictator or a Junta? , 1997, Cell.