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JOURNAL ARTICLES
frizzled regulates mirror-symmetric pattern formation in the Drosophila eye
L. Zheng, J. Zhang, R.W. Carthew
Development 1995 121: 3045-3055;

Summary

Coordinated morphogenesis of ommatidia during Drosophila eye development establishes a mirror-image symmetric pattern across the entire eye bisected by an anteroposterior equator. We have investigated the mechanisms by which this pattern formation occurs and our results suggest that morphogenesis is coordinated by a graded signal transmitted bidirectionally from the presumptive equator to the dorsal and ventral poles. This signal is mediated by frizzled, which encodes a cell surface transmembrane protein. Mosaic analysis indicates that frizzled acts non-autonomously in an equatorial to polar direction. It also indicates that relative levels of frizzled in photoreceptor cells R3 and R4 of each ommatidium affect their positional fate choices such that the cell with greater frizzled activity becomes an R3 cell and the cell with less frizzled activity becomes an R4 cell. Moreover, this bias affects the choice an ommatidium makes as to which direction to rotate. Equator-outwards progression of elav expression and expression of the nemo gene in the morphogenetic furrow are regulated by frizzled, which itself is dynamically expressed about the morphogenetic furrow. We propose that frizzled mediates a bidirectional signal emanating from the equator.

Reference

    1. Adler P. N.,
    2. Vinson C.,
    3. Park W. J.,
    4. Conover S.,
    5. Klein L.
    (1990) Molecular structure of frizzled, a Drosophila tissue polarity gene. Genetics 126, 401–416
    OpenUrlAbstract/FREE Full Text
    1. Carthew R. W.,
    2. Rubin G. M.
    (1990) seven in absentia, a gene required for specification of R7 cell fate in the Drosophila eye. Cell 63, 561–577
    OpenUrlCrossRefPubMedWeb of Science
    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. Diaz-Benjumea F. J.,
    2. Cohen S. M.
    (1993) Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75, 741–752
    OpenUrlCrossRefPubMedWeb of Science
    1. Fischer-Vize J. A.,
    2. Rubin G. M.,
    3. Lehmann R.
    (1992) The fat facets gene is required for Drosophila eye and embryo development. Development 116, 985–1000
    OpenUrlAbstract/FREE Full Text
    1. Freeman M.,
    2. Klämbt C.,
    3. Goodman C. S.,
    4. Rubin G. M.
    (1992) The argos gene encodes a diffusuble factor that regulates cell fate decisions in the Drosophila eye. Cell 69, 963–975
    OpenUrlCrossRefPubMedWeb of Science
    1. Gierer A.
    (1974) Molecular models and combinatorial principles in cell differentiation and morphogenesis. Cold Spring Harbor Symp. Quant. Biol 38, 951–961
    OpenUrlAbstract/FREE Full Text
    1. Gubb D.
    (1993) Genes controlling cellular polarity in Drosophila. Development 1993, 269–277
    1. Gubb D.,
    2. Garcia-Bellido A.
    (1982) A genetic analysis of the determination of cuticular polarity during development of Drosophila melanogaster. J. Embryol. Exp. Morphol 68, 37–57
    OpenUrlPubMedWeb of Science
    1. Hay B. A.,
    2. Wolff T.,
    3. Rubin G. M.
    (1994) Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121–2129
    OpenUrlAbstract
    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
    OpenUrlCrossRefPubMedWeb of Science
    1. Heitzler P.,
    2. Simpson P.
    (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64, 1083–1092
    OpenUrlCrossRefPubMedWeb of Science
    1. Kimmel B. E.,
    2. Heberlein U.,
    3. Rubin G. M.
    (1990) The homeodomain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype. Genes Dev 4, 712–727
    OpenUrlAbstract/FREE Full Text
    1. Krasnow R. E.,
    2. Adler P. N.
    (1994) A single frizzled protein has a dual function in tissue polarity. Development 120, 1883–1893
    OpenUrlAbstract
    1. Lawrence P. A.
    (1966) Gradients in the insect segment: the orientation of hairs in the milkweed bug Oncopeltus fasciatus. J. Exp. Biol 44, 607–620
    OpenUrlAbstract/FREE Full Text
    1. Lawrence P. A.,
    2. Crick F. H. C.,
    3. Munro M.
    (1972) A gradient of positional information in an insect, Rhodnius. J. Cell Sci 11, 815–853
    OpenUrlAbstract/FREE Full Text
    1. Lawrence P. A.,
    2. Shelton P. M. J.
    (1975) The determination of polarity in the developing insect retina. J. Embryol. Exp. Morph 33, 471–486
    OpenUrlPubMedWeb of Science
    1. Locke M.
    (1959) The cuticular pattern in an insect, Rhodnius prolixus Stål. J. Exp. Biol 36, 459–477
    OpenUrlAbstract
    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. Rubin G. M.
    (1991) glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes Dev 5, 583–593
    OpenUrlAbstract/FREE Full Text
    1. Park W. J.,
    2. Liu J.,
    3. Adler P. N.
    (1994) The frizzled gene of Drosophila encodes a membrane protein with an odd number of transmembrane domains. Mech. Dev 45, 127–137
    OpenUrlCrossRefPubMed
    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. 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. Theisen H.,
    2. Purcell J.,
    3. Bennett M.,
    4. Kansagara D.,
    5. Syed A.,
    6. Marsh J. L.
    (1994) dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development 120, 347–360
    OpenUrlAbstract
    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. Vinson C. R.,
    2. Adler P. N.
    (1987) Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila. Nature 329, 549–551
    OpenUrlCrossRefPubMed
    1. Vinson C. R.,
    2. Conover S.,
    3. Adler P. N.
    (1989) A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature 338, 263–264
    OpenUrlCrossRefPubMed
    1. Williams J. A.,
    2. Paddock S. W.,
    3. Carroll S. B.
    (1993) Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions. Development 117, 571–584
    OpenUrlAbstract
    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. Wolff T.,
    2. Ready D. F.
    (1991) Cell death in normal and rough eye mutants of Drosophila. Development 113, 825–839
    OpenUrlAbstract
    1. Xu T.,
    2. Rubin G. M.
    (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223–1237
    OpenUrlAbstract
    1. Zipursky S. L.,
    2. Rubin G. M.
    (1994) Determination of neuronal cell fate: lessons from the R7 neuron of Drosophila. Annu. Rev. Neurosci 17, 373–397
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
frizzled regulates mirror-symmetric pattern formation in the Drosophila eye
L. Zheng, J. Zhang, R.W. Carthew
Development 1995 121: 3045-3055;
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