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Mad acts downstream of Dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye
V. Wiersdorff, T. Lecuit, S. M. Cohen, M. Mlodzik
Development 1996 122: 2153-2162;

Summary

Decapentaplegic (Dpp), a member of the TGF-betta family of cytokines, has been implicated in many patterning processes in Drosophila, including the initial steps of pattern formation in the developing eye. We show that the Mothers against dpp (Mad) gene is required for dpp signaling during eye development. Clonal analysis demonstrates a cell-autonomous function for Mad and genetic interactions indicate that Mad is an essential component of the signal transduction pathway downstream of the Dpp receptors in responding cells. Mad-mediated dpp signaling is absolutely required for the initiation of the morphogenetic furrow in the eye, but has only a minor role in its subsequent propagation across the eye

Reference

    1. Arora K.,
    2. Dai H.,
    3. Kazuko S. G.,
    4. Jamal J.,
    5. O'Connor M. B.,
    6. Letsou A.,
    7. Warrior R.
    (1995) The Drosophila schnurri gene acts in the Dpp/TGF-signaling pathway and encodes a transcription factor homologous to the human MBP family. Cell 81, 781–790
    OpenUrlCrossRefPubMedWeb of Science
    1. Attisano L.,
    2. Wrana J. L.,
    3. Lopez-Casillas F.,
    4. Massague J.
    (1994) TGF-receptors and actions. Biochim. Biophys. Acta 1222, 71–80
    OpenUrlPubMed
    1. Blackman R. K.,
    2. Sanicola M.,
    3. Raftery L. A.,
    4. Gillevet T.,
    5. Gelbart W. M.
    (1991) An extensive 3 cis -regulatory region directs the imaginal disc expression of decapentaplegic, a member of the TGF-family in Drosophila. Development 111, 657–666
    OpenUrlAbstract
    1. Capdevila J.,
    2. Guerrero I.
    (1994) Targeted expression of the signalling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J 13, 4459–4468
    OpenUrlPubMedWeb of Science
    1. Chanut F.,
    2. Heberlein U.
    (1995) Role of the morphogenetic furrow in establishing polarity in the Drosophila eye. Development 121, 4085–4094
    OpenUrlAbstract
    1. Diaz-Benjumea F. J.,
    2. Cohen B.,
    3. Cohen S. M.
    (1994) Cell interaction between compartments establishes the proximal-distal axis of Drosophila limbs. Nature 372, 175–179
    OpenUrlCrossRefPubMed
    1. Ellis M. C.,
    2. Weber U.,
    3. Wiersdorff V.,
    4. Mlodzik M.
    (1994) Confrontation of scabrous expressing and non-expressing cells is essential for normal ommatidial spacing in the Drosophila eye. Development 120, 1959–1969
    OpenUrlAbstract
    1. Ferguson E. L.,
    2. Anderson K. V.
    (1992) decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71, 451–461
    OpenUrlCrossRefPubMedWeb of Science
    1. Grieder N. C.,
    2. Nellen D.,
    3. Burke R.,
    4. Basler K.,
    5. Affolter M.
    (1995) schnurri is required for Drosophila Dpp signaling and encodes a zinc finger protein similar to the mammalian transcription factor PRDII-BF1. Cell 81, 791–800
    OpenUrlCrossRefPubMedWeb of Science
    1. Hahn S. A.,
    2. Schutte M.,
    3. Shamsul Hoque A. T. M.,
    4. Moskaluk C. A.,
    5. da Costa L. T.,
    6. Rozenblum E.,
    7. Weinstein C. L.,
    8. Fischer A.,
    9. Yeo C. J.,
    10. Hruban R. H.,
    11. Kern S. E.
    (1996). DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271, 350–353
    OpenUrlAbstract
    1. Hay B.,
    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. Moses K.
    (1995) Mechanisms of Drosophila retinal morphogenesis: the virtues of being progressive. Cell 81, 987–990
    OpenUrlCrossRefPubMedWeb of Science
    1. Heberlein U.,
    2. Singh C. M.,
    3. Luk A. Y.,
    4. Donohue T. J.
    (1995) Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373, 709–711
    OpenUrlCrossRefPubMedWeb of Science
    1. Heberlein U.,
    2. Wolff T.,
    3. Rubin G. M.
    (1993) The TGFhomolog dpp and the segment polarity gene hedgehog are required for the propagation of a morphogenetic wave in the Drosophila retina. Cell 75, 913–926
    OpenUrlCrossRefPubMedWeb of Science
    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. 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 pattern. Nature 373, 711–715
    OpenUrlCrossRefPubMedWeb of Science
    1. Letsou A.,
    2. Arora K.,
    3. Wrana J. L.,
    4. Simin K.,
    5. Twombly V.,
    6. Jamal J.,
    7. Staeheling-Hampton K.,
    8. Hofmann F. M.,
    9. Gelbart W. M.,
    10. Massague J.,
    11. O'Connor M. B.
    (1995) Drosophila Dpp signaling is mediated by the punt gene product: a dual ligand-binding type II receptor of the TGF-receptor family. Cell 80, 899–908
    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. Moses K.
    (1995) wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye. Development 121, 2279–2289
    OpenUrlAbstract
    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. Massague J.
    (1992) Receptors for the TGF-family. Cell 69, 1067–1070
    OpenUrlCrossRefPubMedWeb of Science
    1. Masucci J. D.,
    2. Miltenberger R. J.,
    3. Hoffmann F. M.
    (1990) Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal discs is regulated by 3 cis -regulatory elements. Genes Dev 4, 2011–2023
    OpenUrlAbstract/FREE Full Text
    1. Mlodzik M.,
    2. Hiromi Y.,
    3. Weber U.,
    4. Goodman C. S.,
    5. Rubin G. M.
    (1990) The Drosophilaseven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell 60, 211–224
    OpenUrlCrossRefPubMedWeb of Science
    1. Nellen D.,
    2. Affolter M.,
    3. Basler K.
    (1994) Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell 78, 225–237
    OpenUrlCrossRefPubMedWeb of Science
    1. Newfeld S. J.,
    2. Chartoff E. H.,
    3. Graff J. M.,
    4. Melton D. A.,
    5. Gelbart W. M.
    (1996) Mothers against dpp encodes a conserved cytoplasmic protein required in DPP/TGF-responsive cells. Development 122, 2099–2108
    OpenUrlAbstract
    1. Padgett R. W.,
    2. Wozney J. M.,
    3. Gelbart W. M.
    (1993) Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 90, 2905–2909
    OpenUrlAbstract/FREE Full Text
    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. Raftery L. A.,
    2. Twombly V.,
    3. Wharton K.,
    4. Gelbart W. M.
    (1995) Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila. Genetics 139, 241–254
    OpenUrlAbstract/FREE Full Text
    1. Ready D. F.
    (1989) A multifaceted approach to neural development. Trends Neurosci 12, 102–110
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruberte E.,
    2. Marty T.,
    3. Nellen D.,
    4. Affolter M.,
    5. Basler K.
    (1995) An absolute requirement for both the type II and type I receptors, punt and thickveins, for Dpp signaling in vivo. Cell 80, 889–897
    OpenUrlCrossRefPubMedWeb of Science
    1. Sampath T. K.,
    2. Rashka K. E.,
    3. Doctor J. S.,
    4. Tucker R. F.,
    5. Hoffmann F. M.
    (1993) Drosophila TGF-superfamily proteins induce endochondrial bone formation in mammals. Proc. Natl. Acad. Sci. USA 90, 6004–6008
    OpenUrlAbstract/FREE Full Text
    1. Savage C.,
    2. Das P.,
    3. Finelli A. L.,
    4. Townsend S. R.,
    5. Sun C.-Y.,
    6. Baird S. E.,
    7. Padgett R. W.
    (1996) C. elegans genes sma-2, sma-3, and sma-4 define a conserved family of transforming growth factorpathway components. Proc. Natl. Acad. Sci. USA 93, 790–794
    OpenUrlAbstract/FREE Full Text
    1. Sekelsky J. J.,
    2. Newfeld S. J.,
    3. Raftery L. A.,
    4. Chartoff E. H.,
    5. Gelbart W. M.
    (1995) Genetic characterization and cloning of Mothers against dpp, a gene required for decapentaplegic function in Drosophilamelanogaster. Genetics 139, 1347–1358
    OpenUrlAbstract/FREE Full Text
    1. Spradling A. C.,
    2. Rubin G. M.
    (1982) Transposition of cloned P-elements into Drosophila germ line chromosomes. Science 218, 341–347
    OpenUrlAbstract/FREE Full Text
    1. Strutt D. I.,
    2. Mlodzik M.
    (1995) Ommatidial polarity in the Drosophila eye is determined by the direction of furrow progression and local interactions. Development 121, 4247–4256
    OpenUrlAbstract
    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. 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) Cell fate in the Drosophila Ommatidium. Dev. Biol 123, 264–275
    OpenUrlCrossRefPubMedWeb of Science
    1. Török T.,
    2. Tick G.,
    3. Alvarado M.,
    4. Kiss I.
    (1993) P-lacW insertional mutagenesis on the second chromosome of Drosophilamelanogaster: isolation of lethals with different overgrowth phenotypes. Genetics 135, 71–80
    OpenUrlAbstract/FREE Full Text
    1. Treisman J. E.,
    2. Lai Z.-C.,
    3. Rubin G. M.
    (1995) shortsighted acts in the decapentaplegic pathway in Drosophila eye development and has homology to a mouse TGF-responsive gene. Development 121, 2835–2845
    OpenUrlAbstract
    1. Treisman J. E.,
    2. Rubin G. M.
    (1995) wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121, 3519–3527
    OpenUrlAbstract
    1. Vincent J.-P.,
    2. Girdham C. H.,
    3. O'Farrell P. H.
    (1994) A cell-autonomous, ubiquitous marker for the analysis of Drosophila genetic mosaics. Dev. Biol 164, 328–331
    OpenUrlCrossRefPubMedWeb of Science
    1. Wall N. A.,
    2. Hogan B. L. M.
    (1994) TGFrelated genes in development. Curr. Opin. Genet. Dev 4, 517–522
    OpenUrlCrossRefPubMed
    1. Wehrli M.,
    2. Tomlinson A.
    (1995) Epithelial planar polarity in the developing Drosophila eye. Development 121, 2451–2459
    OpenUrlAbstract
    1. Wharton K. A.,
    2. Ray R. P.,
    3. Gelbart W. M.
    (1993) An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 117, 807–822
    OpenUrlAbstract
    1. Wieser R.,
    2. Wrana J.,
    3. Massague J.
    (1995) GS domain mutants that constitutively activate TR-1, the downstream signaling component in the TGF-b receptor complex. EMBO J 14, 2199–2208
    OpenUrlPubMedWeb of Science
    1. Wrana J. L.,
    2. Attisano L.,
    3. Wieser R.,
    4. Ventura F.,
    5. Massague J.
    (1994) Mechanism of activation of the TGF-receptor. Nature 370, 341–347
    OpenUrlCrossRefPubMedWeb of Science
    1. Xu T.,
    2. Rubin G. M.
    (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223–1237
    OpenUrlAbstract
    1. Zecca M.,
    2. Basler K.,
    3. Struhl G.
    (1995) Sequential organising activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121, 2265–2278
    OpenUrlAbstract
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JOURNAL ARTICLES
Mad acts downstream of Dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye
V. Wiersdorff, T. Lecuit, S. M. Cohen, M. Mlodzik
Development 1996 122: 2153-2162;
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