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JOURNAL ARTICLES
The role of segment polarity genes during early oogenesis in Drosophila
A.J. Forbes, A.C. Spradling, P.W. Ingham, H. Lin
Development 1996 122: 3283-3294;
A.J. Forbes
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A.C. Spradling
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P.W. Ingham
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H. Lin
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Summary

In the Drosophila ovary, hedgehog (hh) signaling from cells near the apical tip of the germarium stimulates the proliferation and specification of somatic cells in region 2 of the germarium, 2–5 cells away from the hh-expressing cells (A. J. Forbes, H. Lin, P. Ingham and A. Spradling (1996) Development 122, 1125–1135). This report examines the role during early oogenesis of several genes that are known to function in hh-mediated signaling during embryonic and larval development (P. Ingham (1995) Current Opin. Genetics Dev. 5, 528–534). As in imaginal discs, engrailed (en) is co-expressed with hh in the germarium, while patched (ptc) and cubitus interruptus (ci) are expressed in somatic cells throughout the germarium and in developing egg chambers, with ptc expression being elevated within 10 cell diameters of the source of the hh signal. Moreover, the somatic cell overproliferation caused by ectopic hh expression is accompanied by elevated levels of ptc and is phenocopied in ptc- somatic clones. These analyses suggest that ptc and ci are components of the hh signaling pathway in the germarium. However, unlike embryos and imaginal discs, neither wingless (wg) nor decapentaplegic (dpp) appear to mediate the ovarian hh signal. wg is expressed in ‘cap cells,’ a subset of hh-expressing cells located adjacent to germ-line stem cells, but is unaffected by ectopic hh expression. Nor does the ectopic expression of wg or dpp mimic the effect of ectopic hh expression. We propose that Hh diffuses from apical cells, including cap cells, and regulates the proliferation of nearby ovarian somatic cells by antagonizing the negative effects of ptc on ci activity in these cells, thereby allowing the transcription of ci-dependent genes, including ptc itself.

Reference

    1. Basler K.,
    2. Struhl. G.
    (1994) Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208–214
    OpenUrlCrossRefPubMedWeb of Science
    1. Cadigan K. M.,
    2. Grossniklaus U.,
    3. Gehring W. J.
    (1994) Localized expression of sloppy paired maintains the polarity of the Drosophila parasegment. Genes Dev 8, 899–913
    OpenUrlAbstract/FREE Full Text
    1. Capdevila J.,
    2. Estrada M. P.,
    3. Sanchez-Herrero E.,
    4. Guerrero I.
    (1994) The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. EMBO J 13, 71–82
    OpenUrlPubMedWeb of Science
    1. Couso J. P.,
    2. Bishop S. A.,
    3. Martinez-Arias A.
    (1994) The wingless signalling pathway and the patterning of the wing margin in Drosophila. Development 120, 621–636
    OpenUrlAbstract
    1. DiNardo S.,
    2. Heemskerk J.
    (1990) Molecular and cellular interactions responsible for intrasegmental patterning during Drosophila embryogenesis. Semin. Cell Biol 1, 173–83
    OpenUrlPubMed
    1. Eaton S.,
    2. Kornberg T. B.
    (1990) Repression of ci-D in posterior compartments of Drosophila by engrailed. Genes Dev 4, 1068–1077
    OpenUrlAbstract/FREE Full Text
    1. Forbes A. J.,
    2. Lin H.,
    3. Ingham P.,
    4. Spradling A.
    (1996) hedgehog is required for the proliferation and specification of somatic cells during egg chamber assembly in Drosophila oogenesis. Development 122, 1125–1135
    OpenUrlAbstract
    1. Golic K.,
    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. 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. Donohoe T. J.
    (1995) Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373, 709–711
    OpenUrlCrossRefPubMedWeb of Science
    1. Heemskerk J.,
    2. DiNardo S.,
    3. Kostriken R.,
    4. O'Farrell P. H.
    (1991) Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature 352, 404–10
    OpenUrlCrossRefPubMedWeb of Science
    1. Hooper J. E.,
    2. Scott M. P.
    (1989) The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell 59, 751–765
    OpenUrlCrossRefPubMedWeb of Science
    1. Ingham P. W.
    (1993) Localized hedgehog activity controls spatially restricted transcription of wingless in the Drosophila embryo. Nature 366, 560–562
    OpenUrlCrossRefPubMedWeb of Science
    1. Ingham P. W.,
    2. Feitz M.
    (1995) Quantitative effects of hedgehog and decapentaplegic activity on the pattering of the Drosophila wing. Current Biology 5, 432–440
    OpenUrlCrossRefPubMedWeb of Science
    1. Ingham P. W.,
    2. Hidalgo A.
    (1993) Regulation of wingless transcription in the Drosophila embryo. Development 117, 283–291
    OpenUrlAbstract/FREE Full Text
    1. Ingham. P. W.,
    2. Taylor A. M.,
    3. Nakano Y.
    (1991) Role of the Drosophila patched gene in positional signaling. Nature 353, 184–187
    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. Johnson R.,
    2. Tabin C.
    (1995) The long and short of hedgehog signaling. Cell 81, 313–316
    OpenUrlCrossRefPubMedWeb of Science
    1. Karpen G.,
    2. Spradling A.
    (1992) Analysis of subtelomeric heterochromatin in a Drosophila minichromosome by single P element insertional mutagenesis. Genetics 133, 737–753
    OpenUrlAbstract/FREE Full Text
    1. Kirkpatrick C.,
    2. Peifer M.
    (1995) Not just glue: cell-cell junctions as cellular signaling centers. Curr. Opin. Genet. Dev 5, 56–65
    OpenUrlCrossRefPubMed
    1. Koch E.,
    2. King R.
    (1966) The origin and early differentiation of the egg chamber of Drosophilamelanogaster. J. Morph 119, 283–304
    OpenUrlCrossRefPubMed
    1. Lane M. E.,
    2. Kalderon D.
    (1994) RNA localization along the anteroposterior axis of the Drosophila oocyte requires PKA-mediated signal transduction to direct normal microtubule organization. Genes Dev 8, 2986–2995
    OpenUrlAbstract/FREE Full Text
    1. Lane M. E.,
    2. Kalderon D.
    (1995) Localization and function of protein kinase A during Drosophila oogenesis. Mech Develop 49, 191–200
    OpenUrlCrossRefPubMed
    1. Lee J. J.,
    2. von Kessler D. P.,
    3. Parks S.,
    4. Beachy P. A.
    (1992) Secretion and localized transcription suggests a role in positional signaling for products of the segmentation gene hedgehog. Cell 71, 777–789
    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. Lin H.,
    2. Spradling A.
    (1993) Germline stem cell division and egg chamber development in transplanted Drosophila germaria. Dev. Biol 159, 140–152
    OpenUrlCrossRefPubMedWeb of Science
    1. Lin H.,
    2. Spradling A.
    (1995) Fusome asymmetry and oocyte determination in Drosophila. Dev. Genetics 16, 6–12
    OpenUrlCrossRefPubMedWeb of Science
    1. Lin H.,
    2. Yue L.,
    3. Spradling A.
    (1994) The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120, 947–956
    OpenUrlAbstract
    1. Margolis J.,
    2. Spradling A.
    (1995) Identification and behavior of epithelial stem cells in the Drosophila ovary. Development 121, 3797–3807
    OpenUrlAbstract
    1. Martinez-Arias A.,
    2. Baker N.,
    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. Mohler E.,
    2. Vani K.
    (1992) Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterns of Drosophila. Development 115, 957–971
    OpenUrlAbstract
    1. Motzny C. K.,
    2. Holmgren R.
    (1995) The Drosophila cubitus interruptus protein and its role in the wingless and hedgehog signal transduction pathways. Mech. Dev 52, 137–50
    OpenUrlCrossRefPubMedWeb of Science
    1. Nakano Y.,
    2. Guerrero I.,
    3. Hidalgo A.,
    4. Taylor A.,
    5. Whittle R.,
    6. Ingham P. W.
    (1989) A protein with several possible membrane spanning domains encoded by the Drosophila segment polarity gene patched. Nature 341, 508–513
    OpenUrlCrossRefPubMedWeb of Science
    1. Noordermeer J.,
    2. Johnston P.,
    3. Rijsewijk F.,
    4. Nusse R.,
    5. Lawrence P.
    (1992) The consequences of ubiquitous expression of the wingless gene in the Drosophila ovary. Development 116, 711–9
    OpenUrlAbstract
    1. Pan D.,
    2. Rubin G. M.
    (1995) cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal disks. Cell 80, 543–552
    OpenUrlCrossRefPubMedWeb of Science
    1. Patel N.,
    2. Martin-Blanco E.,
    3. Coleman K.,
    4. Poole S. J.,
    5. Ellis M. C.,
    6. Korngerg T. B.,
    7. Goodman C. S.
    (1989) Expression of engrailed proteins in arthropods, annelids and chordates. Cell 58, 955–968
    OpenUrlCrossRefPubMedWeb of Science
    1. Peifer M.,
    2. Orsulic S.,
    3. Sweeton D.,
    4. Wieschaus E.
    (1993) A role for the Drosophila segment polarity genes armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development 118, 1191–1207
    OpenUrlAbstract/FREE Full Text
    1. Perrimon N.
    (1994) The genetic basis of baldness in Drosophila. Cell 6, 781–784
    1. Perrimon N.
    (1995) Hedgehog and beyond. Cell 80, 517–520
    OpenUrlCrossRefPubMedWeb of Science
    1. Pesacreta T. C.,
    2. Byers T. J.,
    3. Dubreuil R.,
    4. Kiehart D. P.,
    5. Branton D.
    (1989) Drosophila spectrin: the membrane skeleton during embryogenesis. J. Cell Biol 121, 1697–1709
    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 positional signaling in imaginal discs. Development 110, 105–114
    OpenUrlAbstract
    1. Riggleman B.,
    2. Schedl P.,
    3. Wieschaus E.
    (1990) Spatial expression of the segment polarity gene armadillo is post transcriptionally regulated by wingless. Cell 63, 549–560
    OpenUrlCrossRefPubMedWeb of Science
    1. Roberts D. J.,
    2. Johnson R. L.,
    3. Burke A. C.,
    4. Nelson C. E.,
    5. Morgan B. A.,
    6. Tabin C.
    (1995) Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 121, 3163–3174
    OpenUrlAbstract
    1. Ruohola-Baker H.,
    2. Jan L. Y.,
    3. Jan Y. N.
    (1994) The role of gene cassettes in axis formation during oogenesis. Trends in Genetics 10, 89–94
    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. Tabata T.,
    2. Kornberg T.
    (1994) Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell 76, 89–102
    OpenUrlCrossRefPubMedWeb of Science
    1. Tabata T.,
    2. Eaton S.,
    3. Kornberg T. B.
    (1992) The Drosophilahedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev 6, 2635–2645
    OpenUrlAbstract/FREE Full Text
    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. Twombly V.,
    2. Blackman R. K.,
    3. Jin H.,
    4. Graff J. M.,
    5. Padgett R. W.,
    6. Gelbart W. M.
    (1996) The TGF-β signaling pathway is essential for Drosophila oogenesis. Development 122, 1555–1565
    OpenUrlAbstract
    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. Yanagawa S.,
    2. van Leeuwen F.,
    3. Wodarz A.,
    4. Klingensmith J.,
    5. Nusse R.
    (1995) The dishevelled protein is modified by wingless signaling in Drosophila. Genes Dev 9, 1087–97
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
The role of segment polarity genes during early oogenesis in Drosophila
A.J. Forbes, A.C. Spradling, P.W. Ingham, H. Lin
Development 1996 122: 3283-3294;
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JOURNAL ARTICLES
The role of segment polarity genes during early oogenesis in Drosophila
A.J. Forbes, A.C. Spradling, P.W. Ingham, H. Lin
Development 1996 122: 3283-3294;

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