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JOURNAL ARTICLES
Wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye
C. Ma, K. Moses
Development 1995 121: 2279-2289;
C. Ma
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K. Moses
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Summary

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.

Reference

    1. Baker N. E.
    (1987) Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila: the spatial distribution of a transcript in embryos. EMBO J 6, 1765–1773
    OpenUrlPubMedWeb of Science
    1. Baker N. E.
    (1988) Transcription of the segment-polarity gene wingless in the imaginal discs of Drosophila, and the phenotype of a pupal-lethal wg mutation. Development 102, 489–497
    OpenUrlAbstract
    1. Baker N. E.
    (1988) Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila. Dev. Biol 125, 96–108
    OpenUrlCrossRefPubMedWeb of Science
    1. Baker N. E.,
    2. Mlodzik M.,
    3. Rubin G. M.
    (1990) Spacing differentiation in the developing Drosophila eye: a fibrinogen-related lateral inhibitor encoded by scabrous. Science 250, 1370–1377
    OpenUrlAbstract/FREE Full Text
    1. Baker N. E.,
    2. Rubin G. M.
    (1989) Effect on eye development of dominant mutations in Drosophila homologue of the EGF receptor. Nature 340, 150–153
    OpenUrlCrossRefPubMed
    1. Baker N. E.,
    2. Rubin G. M.
    (1992) Ellipse mutations in the Drosophila homologue of the EGF receptor affect pattern formation, cell division, and cell death in eye imaginal discs. Dev. Biol 150, 381–396
    OpenUrlCrossRefPubMedWeb of Science
    1. Bejsovec A.,
    2. Wieschaus E.
    (1993) Segment polarity gene interactions modulate epidermal patterning in Drosophila embryos. Development 119, 501–517
    OpenUrlAbstract
    1. Blackman R. K.,
    2. Sanicola M.,
    3. Raferty L. A.,
    4. Gillevet T.,
    5. Gelbart W. M.
    (1991) An extensive 3cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-family in Drosophila. Development 111, 657–665
    OpenUrlAbstract
    1. Blair S. S.
    (1995) Hedgehog digs up an old friend. Nature 373, 656–657
    OpenUrlCrossRefPubMedWeb of Science
    1. Bryant P. J.
    (1993) The polar coordinate model goes molecular. Science 259, 471–472
    OpenUrlFREE Full Text
    1. Capdevila J.,
    2. Pariente F.,
    3. Sampedro J.,
    4. Alonso J. L.,
    5. Guerrero I.
    (1994) Subcellular localization of the segment polarity protein patched suggests an interaction with the wingless reception complex in Drosophila embryos. Development 120, 987–998
    OpenUrlAbstract
    1. Carroll S. B.,
    2. Whyte J. S.
    (1989) The role of the hairy gene during Drosophila morphogenesis: stripes in imaginal discs. Genes Dev 3, 905–916
    OpenUrlAbstract/FREE Full Text
    1. Choi K.-W.,
    2. Benzer S.
    (1994) Rotation of photoreceptor clusters in the developing Drosophila eye requires the nemo gene. Cell 78, 125–136
    OpenUrlCrossRefPubMedWeb of Science
    1. Chu-LaGraff Q.,
    2. Doe C. Q.
    (1993) Neuroblast specification and formation regulated by wingless in the Drosophila CNS. Science 261, 1594–1597
    OpenUrlAbstract/FREE Full Text
    1. Cohen S. M.,
    2. Di Nardo S.
    (1993) wingless: from embryo to adult. Trends Genet 9, 189–192
    OpenUrlCrossRefPubMed
    1. Couso J. P.,
    2. Martinez Arias A.
    (1994) Notch is required for wingless signaling in the epidermis of Drosophila. Cell 79, 259–272
    OpenUrlCrossRefPubMedWeb of Science
    1. Gibson G.,
    2. Gehring W. J.
    (1988) Head and thoracic transformations caused by ectopic expression of Antennapedia during Drosophila development. Development 102, 657–675
    OpenUrlAbstract/FREE Full Text
    1. Golic K. G.,
    2. Lindquist S.
    (1989) The Flp recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499–509
    OpenUrlCrossRefPubMedWeb of Science
    1. Gubb D.
    (1993) Genes controlling cellular polarity in Drosophila. Development 1993, 269–277
    1. Hazelrigg T.,
    2. Levis R.,
    3. Rubin G. M.
    (1984) Transformation of white locus DNA in Drosophila: dosage compensation, zeste interaction, and position effects. Cell 36, 469–481
    OpenUrlCrossRefPubMedWeb of Science
    1. Heberlein U.,
    2. Singh C. M.,
    3. Luk A. Y.,
    4. Donohoe T. J.
    (1995) Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373, 709–711
    OpenUrlCrossRefPubMed
    1. Heberlein U.,
    2. Wolff T.,
    3. Rubin G. M.
    (1993) The TGFhomolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 75, 913–926
    OpenUrlCrossRefPubMedWeb of Science
    1. Hidalgo A.
    (1991) Interactions between segment polarity genes and the generation of the segmental pattern in Drosophila. Mech. Dev 35, 77–87
    OpenUrlCrossRefPubMedWeb of Science
    1. Hooper J. E.,
    2. Scott M. P.
    (1989) The Drosophilapatched gene encodes a putative membrane protein required for segmental patterning. Cell 59, 751–765
    OpenUrlCrossRefPubMedWeb of Science
    1. Ingham P. W.,
    2. Martinez-Arias A.
    (1992) Boundaries and fields in early embryos. Cell 68, 221–235
    OpenUrlCrossRefPubMedWeb of Science
    1. Ingham P. W.,
    2. Taylor A. M.,
    3. Nakano Y.
    (1991) Role of the Drosophila patched gene in positional signaling. Nature 353, 184–186
    OpenUrlCrossRefPubMed
    1. Jiang J.,
    2. Struhl G.
    (1995) Protein kinase A and hedgehog signaling in Drosophila limb development. Cell 80, 563–572
    OpenUrlCrossRefPubMedWeb of Science
    1. Kaphingst K.,
    2. Kunes S.
    (1994) Pattern formation in the visual centers of the Drosophila brain: wingless acts via decapentaplegic to specify the dorsoventral axis. Cell 78, 437–448
    OpenUrlCrossRefPubMedWeb of Science
    1. Lepage T.,
    2. Cohen S. M.,
    3. Diaz-Benjumea F. J.,
    4. Parkhurst S. M.
    (1995) Signal transduction by cAMP-dependent protein kinase A in Drosophila limb patterning. Nature 373, 711–715
    OpenUrlCrossRefPubMedWeb of Science
    1. Li W.,
    2. Ohlmeyer J. T.,
    3. Lane M. E.,
    4. Kalderon D.
    (1995) Function of protein kinase A in Hedgehog signal transduction and Drosophila imaginal disc development. Cell 80, 553–562
    OpenUrlCrossRefPubMedWeb of Science
    1. Ma C.,
    2. Zhou Y.,
    3. Beachy P. A.,
    4. Moses K.
    (1993) The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell 75, 927–938
    OpenUrlCrossRefPubMedWeb of Science
    1. Mardon G.,
    2. Solomon N. M.,
    3. Rubin G. M.
    (1994) dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120, 3473–3486
    OpenUrlAbstract
    1. Martinez Arias A.
    (1994) Pathways of cell communication during development: signaling and epistases. Trends Genet 10, 219–222
    OpenUrlCrossRefPubMed
    1. Martinez-Arias A.,
    2. Baker N. E.,
    3. Ingham P. W.
    (1988) Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. Development 103, 157–170
    OpenUrlAbstract
    1. Melamed J.,
    2. Trujillo-Cenoz O.
    (1975) The fine structure of the eye imaginal disks in Muscoid flies. J. Ultrastr. Res 51, 79–93
    OpenUrlCrossRefPubMedWeb of Science
    1. Mlodzik M.,
    2. Baker N. E.,
    3. Rubin G. M.
    (1990) Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila. Genes Dev 4, 1848–1861
    OpenUrlAbstract/FREE Full Text
    1. Moses K.,
    2. Ellis M. C.,
    3. Rubin G. M.
    (1989) The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells. Nature 340, 531–536
    OpenUrlCrossRefPubMed
    1. Nakano Y.,
    2. Guerrero I.,
    3. Hidalgo A.,
    4. Taylor A.,
    5. Whittle J. R. S.,
    6. Ingham P. W.
    (1989) A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched. Nature 341, 508–512
    OpenUrlCrossRefPubMed
    1. Noordermeer J.,
    2. Johnston P.,
    3. Rijsewijk F.,
    4. Nusse R.,
    5. Lawrence P. A.
    (1992) The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo. Development 116, 711–719
    OpenUrlAbstract
    1. Nusse R.,
    2. Varmus H. E.
    (1992) Wnt genes. Cell 69, 1073–1087
    OpenUrlCrossRefPubMedWeb of Science
    1. Pan D.,
    2. Rubin G. M.
    (1995) cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal discs. Cell 80, 543–552
    OpenUrlCrossRefPubMedWeb of Science
    1. Peifer M.,
    2. Bejsovec A.
    (1992) Knowing your neighbors: cell interactions determine intrasegmental patterning in Drosophila. Trends Genet 8, 243–249
    1. Peifer M.,
    2. Orsulic S.,
    3. Pai L.-M.,
    4. Loureiro J.
    (1993) A model system for cell adhesion and signal transduction in Drosophila. Development 1993, 163–176
    1. Peifer M.,
    2. Pai L.-M.,
    3. Casey M.
    (1994) Phosphorylation of the Drosophila adherens junction protein Armadillo: roles for Wingless signal and Zeste-white 3 kinase. Dev. Biol 166, 543–556
    OpenUrlCrossRefPubMedWeb of Science
    1. Perrimon N.
    (1994) The genetic basis of patterned baldness in Drosophila. Cell 76, 781–784
    OpenUrlCrossRefPubMedWeb of Science
    1. Phillips R. G.,
    2. Roberts I. J. H.,
    3. Ingham P. W.,
    4. Whittle J. R. S.
    (1990) The Drosophila segment polarity gene patched is involved in a position-signaling mechanism in imaginal discs. Development 110, 105–114
    OpenUrlAbstract
    1. Ready D. F.,
    2. Hanson T. E.,
    3. Benzer S.
    (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol 53, 217–240
    OpenUrlCrossRefPubMedWeb of Science
    1. Rijsewijk F.,
    2. Schuermann M.,
    3. Wagenaar E.,
    4. Parren P.,
    5. Weigel D.,
    6. Nusse R.
    (1987) The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50, 649–657
    OpenUrlCrossRefPubMedWeb of Science
    1. Robinow S.,
    2. White K.
    (1991) Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol 22, 443–461
    OpenUrlCrossRefPubMedWeb of Science
    1. Russell J.,
    2. Gennissen A.,
    3. Nusse R.
    (1992) Isolation and expression of two novel Wnt/wingless gene homologues in Drosophila. Development 115, 475–485
    OpenUrlAbstract
    1. Schneuwly S.,
    2. Klemenz R.,
    3. Gehring W. J.
    (1987) Redesigning the body plan of Drosophila by ectopic expression of the homoeotic gene Antennapedia. Nature 325, 816–818
    OpenUrlCrossRefPubMedWeb of Science
    1. Schuske K.,
    2. Hooper J. E.,
    3. Scott M. P.
    (1994) patched overexpression causes loss of wingless expression in Drosophila embryos. Dev. Biol 164, 300–311
    OpenUrlCrossRefPubMed
    1. Segall J. E.
    (1993) Polarization of yeast cells in spatial gradients ofmating factor. Proc. Natl. Acad. Sci. USA 90, 8332–8336
    OpenUrlAbstract/FREE Full Text
    1. St. Johnston D.,
    2. Nusslein-Volhard C.
    (1992) The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–219
    OpenUrlCrossRefPubMedWeb of Science
    1. Struhl G.,
    2. Basler K.
    (1993) Organizing activity of wingless protein in Drosophila. Cell 72, 527–540
    OpenUrlCrossRefPubMedWeb of Science
    1. Strutt D. I.,
    2. Wiersdorff V.,
    3. Mlodzik M.
    (1995) Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A. Nature 373, 705–709
    OpenUrlCrossRefPubMed
    1. Tautz D.,
    2. Pfeifle C.
    (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Tearle R.,
    2. Nusslein-Volhard
    (1987) Tubingen mutants and stocklist. Dros. Inf. Serv 66, 209–269
    OpenUrl
    1. Theisen H.,
    2. Purcell J.,
    3. Bennett M.,
    4. Kansagara D.,
    5. Syed A.,
    6. Marsh J. L.
    (1994) disheveled is required during wingless signaling to establish both cell polarity and cell identity. Development 120, 347–360
    OpenUrlAbstract
    1. Thomas B. J.,
    2. Gunning D. A.,
    3. Cho J.,
    4. Zipursky S. L.
    (1994) Cell cycle progression in the developing Drosophila eye: roughex encodes a novel protein required for the establishment of G1. Cell 77, 1003–1014
    OpenUrlCrossRefPubMedWeb of Science
    1. Tomlinson A.
    (1985) The cellular dynamics of pattern formation in the eye of Drosophila. J. Embryol. Exp. Morph 89, 313–331
    OpenUrlPubMedWeb of Science
    1. Tomlinson A.
    (1988) Cellular interactions in the developing Drosophila eye. Development 104, 183–193
    OpenUrlPubMedWeb of Science
    1. Tomlinson A.,
    2. Ready D. F.
    (1987) Neuronal differentiation in the Drosophila ommatidium. Dev. Biol 120, 366–376
    OpenUrlCrossRefPubMedWeb of Science
    1. van den Heuvel M.,
    2. Klingensmith J.,
    3. Perrimon N.,
    4. Nusse R.
    (1993) Cell patterning in the Drosophila segment: engrailed and wingless antigen distributions in segment polarity mutant embryos. Development 1993, 105–114
    1. Vincent J.-P.,
    2. Lawrence P. A.
    (1994) It takes three to distalize. Nature 372, 132–133
    OpenUrlCrossRefPubMed
    1. Waddington C. H.,
    2. Perry M. M.
    (1960) The ultra-structure of the developing eye of Drosophila. Proc. Roy. Soc. Lond. B 153, 155–178
    OpenUrlAbstract/FREE Full Text
    1. Wolff T.,
    2. Ready D. F.
    (1991) The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113, 841–850
    OpenUrlAbstract
    1. Xu T.,
    2. Rubin G. M.
    (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223–1237
    OpenUrlAbstract
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JOURNAL ARTICLES
Wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye
C. Ma, K. Moses
Development 1995 121: 2279-2289;
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JOURNAL ARTICLES
Wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye
C. Ma, K. Moses
Development 1995 121: 2279-2289;

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