Wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye.

In the developing Drosophila compound eye, a wave of pattern formation and cell-type determination sweeps across the presumptive eye epithelium. This 'morphogenetic furrow' coordinates the epithelial cells' division cycle, shape and gene expression to produce evenly spaced neural cell clusters that will eventually form the adult ommatidia. As these clusters develop, they rotate inwards to face the eye's equator and establish tissue polarity. We have found that wingless is strongly expressed in the dorsal margin of the presumptive eye field, ahead of the morphogenetic furrow. We have shown that inactivation of Wingless results in the induction of an ectopic furrow that proceeds ventrally from the dorsal margin. This ectopic furrow is normal in most respects, however the clusters formed by it fail to rotate, and we propose a two-vector model to account for normal rotation and tissue polarity in the retina. A second consequence of this inactivation of Wingless is that the dorsal head is largely deleted. We have also found that patched loss-of-function mosaic clones induce circular ectopic morphogenetic furrows (consistent with the observations of other workers with the hedgehog, and PKA genes). We use such patched induced furrows to test the two-vector model for cluster rotation and tissue polarity.

[1]  G. Struhl,et al.  Protein kinase A and hedgehog signaling in drosophila limb development , 1995, Cell.

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

[3]  Mary Ellen Lane,et al.  Function of protein kinase A in hedgehog signal transduction and Drosophila imaginal disc development , 1995, Cell.

[4]  S. Blair Hedgehog digs up an old friend , 1995, Nature.

[5]  D. Strutt,et al.  Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A , 1995, Nature.

[6]  T. J. Donohoe,et al.  Growth and differentiation in the Drosophila eye coordinated by hedgehog , 1995, Nature.

[7]  Susan M. Parkhurst,et al.  Signal transduction by cAMP-dependent protein kinase A in Drosophila limb patterning , 1995, Nature.

[8]  G. Rubin,et al.  dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. , 1994, Development.

[9]  M. Peifer,et al.  Phosphorylation of the Drosophila adherens junction protein Armadillo: roles for wingless signal and zeste-white 3 kinase. , 1994, Developmental biology.

[10]  Jean-Paul Vincent,et al.  It takes three to distalize , 1994, Nature.

[11]  A. M. Arias,et al.  Notch is required for wingless signaling in the epidermis of Drosophila , 1994, Cell.

[12]  S. Kunes,et al.  Pattern formation in the visual centers of the Drosophila brain: wingless acts via decapentaplegic to specify the dorsoventral axis , 1994, Cell.

[13]  S. Benzer,et al.  Rotation of photoreceptor clusters in the developing drosophila eye requires the nemo gene , 1994, Cell.

[14]  M. Scott,et al.  patched overexpression causes loss of wingless expression in Drosophila embryos. , 1994, Developmental biology.

[15]  S. Zipursky,et al.  Cell cycle progression in the developing Drosophila eye: roughex encodes a novel protein required for the establishment of G1 , 1994, Cell.

[16]  A. M. Arias Pathways of cell communication during development: signalling and epistases , 1994 .

[17]  I. Guerrero,et al.  Subcellular localization of the segment polarity protein patched suggests an interaction with the wingless reception complex in Drosophila embryos. , 1994, Development.

[18]  Norbert Perrimon,et al.  The genetic basis of patterned baldness in Drosophila , 1994, Cell.

[19]  H. Theisen,et al.  dishevelled is required during wingless signaling to establish both cell polarity and cell identity. , 1994, Development.

[20]  K. Moses,et al.  The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye , 1993, Cell.

[21]  Gerald M. Rubin,et al.  The TGFβ homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina , 1993, Cell.

[22]  D. Gubb Genes controlling cellular polarity in Drosophila. , 1993, Development (Cambridge, England). Supplement.

[23]  N. Perrimon,et al.  Cell patterning in the Drosophila segment: engrailed and wingless antigen distributions in segment polarity mutant embryos. , 1993, Development.

[24]  E. Wieschaus,et al.  Segment polarity gene interactions modulate epidermal patterning in Drosophila embryos. , 1993, Development.

[25]  C. Doe,et al.  Neuroblast specification and formation regulated by wingless in the Drosophila CNS. , 1993, Science.

[26]  J. Segall,et al.  Polarization of yeast cells in spatial gradients of alpha mating factor. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[27]  S. Di Nardo,et al.  Wingless: from embryo to adult. , 1993, Trends in genetics : TIG.

[28]  G. Rubin,et al.  Analysis of genetic mosaics in developing and adult Drosophila tissues. , 1993, Development.

[29]  Konrad Basler,et al.  Organizing activity of wingless protein in Drosophila , 1993, Cell.

[30]  P. Bryant,et al.  The polar coordinate model goes molecular. , 1993, Science.

[31]  P. Lawrence,et al.  The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo. , 1992, Development.

[32]  M. Peifer,et al.  Knowing your neighbors: Cell interactions determine intrasegmental patterning in Drosophila , 1992 .

[33]  Roel Nusse,et al.  Wnt genes , 1992, Cell.

[34]  R. Nusse,et al.  Isolation and expression of two novel Wnt/wingless gene homologues in Drosophila. , 1992, Development.

[35]  G. Rubin,et al.  Ellipse mutations in the Drosophila homologue of the EGF receptor affect pattern formation, cell division, and cell death in eye imaginal discs. , 1992, Developmental biology.

[36]  D. Lindsley,et al.  The Genome of Drosophila Melanogaster , 1992 .

[37]  P. Ingham,et al.  Boundaries and fields in early embryos , 1992, Cell.

[38]  C. Nüsslein-Volhard,et al.  The origin of pattern and polarity in the Drosophila embryo , 1992, Cell.

[39]  T. Wolff,et al.  The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. , 1991, Development.

[40]  P. Ingham,et al.  Role of the Drosophila patched gene in positional signalling , 1991, Nature.

[41]  A. Hidalgo Interactions between segment polarity genes and the generation of the segmental pattern in Drosophila , 1991, Mechanisms of Development.

[42]  K. White,et al.  Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. , 1991, Journal of neurobiology.

[43]  W. Gelbart,et al.  An extensive 3' cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-beta family in Drosophila. , 1991, Development.

[44]  G M Rubin,et al.  Spacing differentiation in the developing Drosophila eye: a fibrinogen-related lateral inhibitor encoded by scabrous. , 1990, Science.

[45]  G M Rubin,et al.  Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila. , 1990, Genes & development.

[46]  P. Ingham,et al.  The Drosophila segment polarity gene patched is involved in a position-signalling mechanism in imaginal discs. , 1990, Development.

[47]  M. Scott,et al.  The Drosophila patched gene encodes a putative membrane protein required for segmental patterning , 1989, Cell.

[48]  S. Lindquist,et al.  The FLP recombinase of yeast catalyzes site-specific recombination in the drosophila genome , 1989, Cell.

[49]  A. Taylor,et al.  A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched , 1989, Nature.

[50]  Gerald M. Rubin,et al.  The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells , 1989, Nature.

[51]  Gerald M. Rubin,et al.  Effect on eye development of dominant mutations in Drosophila homologue of the EGF receptor , 1989, Nature.

[52]  S. Carroll,et al.  The role of the hairy gene during Drosophila morphogenesis: stripes in imaginal discs , 1989 .

[53]  A. Tomlinson,et al.  Cellular interactions in the developing Drosophila eye. , 1988, Development.

[54]  N E Baker,et al.  Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. , 1988, Development.

[55]  G. Gibson,et al.  Head and thoracic transformations caused by ectopic expression of Antennapedia during Drosophila development , 1988 .

[56]  N. Baker Transcription of the segment-polarity gene wingless in the imaginal discs of Drosophila, and the phenotype of a pupal-lethal wg mutation. , 1988, Development.

[57]  Detlef Weigel,et al.  The Drosophila homology of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless , 1987, Cell.

[58]  N E Baker,et al.  Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila: the spatial distribution of a transcript in embryos , 1987, The EMBO journal.

[59]  D. Ready,et al.  Neuronal differentiation in Drosophila ommatidium. , 1987, Developmental biology.

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

[61]  G. Rubin,et al.  Transformation of white locus DNA in Drosophila: Dosage compensation, zeste interaction, and position effects , 1984, Cell.

[62]  S. Benzer,et al.  Development of the Drosophila retina, a neurocrystalline lattice. , 1976, Developmental biology.

[63]  O. Trujillo-Cenóz,et al.  The fine structure of the eye imagina disks in muscoid flies. , 1975, Journal of ultrastructure research.

[64]  C. H. Waddington,et al.  The ultra-structure of the developing eye of Drosophila , 1960, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[65]  Tsung-Ying Chen On the development of imaginal buds in normal and mutant Drosophila melanogaster , 1929 .

[66]  J. Krafka DEVELOPMENT OF THE COMPOUND EYE OF DROSOPHILA MELANOGASTER AND ITS BAR-EYED MUTANT , 1924 .

[67]  A. Martinez Arias Pathways of cell communication during development: signalling and epistases. , 1994, Trends in genetics : TIG.

[68]  S. Orsulic,et al.  A model system for cell adhesion and signal transduction in Drosophila. , 1993, Development.

[69]  N. Baker Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila. , 1988, Developmental biology.

[70]  W. Gehring,et al.  Redesigning the body plan of Drosophilaby ectopic expression of the homoeotic gene Antennapedia , 1987, Nature.