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Expression of constitutively active Notch arrests follicle cells at a precursor stage during Drosophila oogenesis and disrupts the anterior-posterior axis of the oocyte
M.K. Larkin, K. Holder, C. Yost, E. Giniger, H. Ruohola-Baker
Development 1996 122: 3639-3650;

Summary

During early development, there are numerous instances where a bipotent progenitor divides to give rise to two progeny cells with different fates. The Notch gene of Drosophila and its homologues in other metazoans have been implicated in many of these cell fate decisions. It has been argued that the role of Notch in such instances may be to maintain cells in a precursor state susceptible to specific differentiating signals. This has been difficult to prove, however, due to a lack of definitive markers for precursor identity. We here perform molecular and morphological analyses of the roles of Notch in ovarian follicle cells during Drosophila oogenesis. These studies show directly that constitutively active Notch arrests cells at a precursor stage, while the loss of Notch function eliminates this stage. Expression of moderate levels of activated Notch leads to partial transformation of cell fates, as found in other systems, and we show that this milder phenotype correlates with a prolonged, but still transient, precursor stage. We also find that expression of constitutively active Notch in follicle cells at later stages leads to a defect in the anterior-posterior axis of the oocyte.

Reference

    1. Artavanis-Tsakonas S.,
    2. Matsuno K.,
    3. Fortini M. E.
    (1995) Notch signaling. Science 268, 225–232
    OpenUrlAbstract/FREE Full Text
    1. Austin C. P.,
    2. Feldman D. E.,
    3. Ida J. A., Jr.,
    4. Cepko C. L.
    (1995) Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development 121, 3637–3650
    OpenUrlAbstract
    1. Bier E.,
    2. Vaessin H.,
    3. Shepherd S.,
    4. Lee K.,
    5. McCall K.,
    6. Barbel S.,
    7. Ackerman L.,
    8. Carretto R.,
    9. Uemura T.,
    10. Grell E.,
    11. et al.
    (1989) Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev 3, 1273–1287
    OpenUrlAbstract/FREE Full Text
    1. Brand A. H.,
    2. Perrimon N.
    (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415
    OpenUrlAbstract
    1. Brand A. H.,
    2. Perrimon N.
    (1994) Raf acts downstream of the EGF receptor to determine dorsoventral polarity during Drosophila oogenesis. Genes Dev 8, 629–639
    OpenUrlAbstract/FREE Full Text
    1. Brand A.
    (1995) GFP in Drosophila. Trends in Gen 11, 324–325
    OpenUrlCrossRefPubMedWeb of Science
    1. Clark I.,
    2. Giniger E.,
    3. Ruohola-Baker H.,
    4. Jan L. Y.,
    5. Jan Y. N.
    (1994) Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Current Biology 4, 289–300
    OpenUrlCrossRefPubMedWeb of Science
    1. Coffman C. R.,
    2. Skoglund P.,
    3. Harris W. A.,
    4. Kintner C. R.
    (1993) Expression of extracellular deletion of Xotch diverts cell fate in Xenopus embryos. Cell 73, 659–671
    OpenUrlCrossRefPubMedWeb of Science
    1. Driever W.,
    2. Siegel V.,
    3. Nusslein-Volhard C.
    (1990) Autonomous determination of anterior structures in the early Drosophila embryo by the bicoid morphogen. Development 109, 811–820
    OpenUrlAbstract/FREE Full Text
    1. Ephrussi A.,
    2. Dickinson L. K.,
    3. Lehmann R.
    (1991) Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66, 37–50
    OpenUrlCrossRefPubMedWeb of Science
    1. Ellisen L. W.,
    2. Bird J.,
    3. West D. C.,
    4. Soreng A. L.,
    5. Reynolds T. C.,
    6. Smith S. D.,
    7. Sklar J.
    (1991) TAN-1, the human homolog of the Drosophila Notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66, 649–661
    OpenUrlCrossRefPubMedWeb of Science
    1. Forbes A. J.,
    2. Lin H.,
    3. Ingham P. W.,
    4. Spradling A. C.
    (1996) Hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila. Development 122, 1125–1135
    OpenUrlAbstract
    1. Fortini M. E.,
    2. Rebay I.,
    3. Caron L. A.,
    4. Artavanis-Tsakonas S.
    (1993) An activated Notch receptor blocks cell fate commitment in the developing Drosophila eye. Nature 365, 555–557
    OpenUrlCrossRefPubMedWeb of Science
    1. Gillespie D. E.,
    2. Berg C. A.
    (1995) Homeless is required for RNA localization in Drosophila oogenesis and encodes a new member of the DE-H family of RNA-dependent ATPases. Genes Dev 9, 2495–2508
    OpenUrlAbstract/FREE Full Text
    1. Gonzales-Reyes A.,
    2. Elliot H.,
    3. St Johnston D.
    (1995) Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375, 654–658
    OpenUrlCrossRefPubMedWeb of Science
    1. Gutzeit H. O.,
    2. Koppa R.
    (1982) Time-lapse film analysis of cytoplasmic streaming during late oogenesis of Drosophila. J. Embryol. Exp. Morph 67, 101–111
    OpenUrlWeb of Science
    1. Hartenstein V.,
    2. Posakony J. W.
    (1990) A dual function of the Notch gene in Drosophila sensillum development. Dev. Biol 142, 13–30
    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. Kim-Ha J.,
    2. Smith J. L.,
    3. Macdonald P. M.
    (1991) Oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66, 23–35
    OpenUrlCrossRefPubMedWeb of Science
    1. Kopan R.,
    2. Schroeter E. H.,
    3. Weintraub H.,
    4. Nye J. S.
    (1996) Signal transduction by activated mNotch: Importance of proteolytic processing and its regulation by the extracellular domain. Proc. Natl. Acad. Sci.USA 93, 1683–1688
    OpenUrlAbstract/FREE Full Text
    1. Lane M. E.,
    2. Kalderon D.
    (1994) RNA localization along the anteroposterior axis of Drosophila oocyte requires PKA-mediated signal transduction to direct normal microtubule organization. Genes Dev 8, 2986–2995
    OpenUrlAbstract/FREE Full Text
    1. Lieber T.,
    2. Kidd S.,
    3. Alcamo E.,
    4. Corbin V.,
    5. Young M. W.
    (1993) Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal tranduction and may point to a novel function for Notch in nuclei. Genes Dev 7, 1949–1965
    OpenUrlAbstract/FREE Full Text
    1. Lyman D.,
    2. Young M. W.
    (1993) Further evidence for function of the Drosophila Notch protein as a transmembrane receptor. Proc. Natl. Acad. Sci.USA 90, 10395–10399
    OpenUrlAbstract/FREE Full Text
    1. Margolis J.,
    2. Spradling A.
    (1995) Identification and behavior of epithelial stem cells in the Drosophila ovary. Development 121, 3797–3807
    OpenUrlAbstract
    1. Markussen F.-H.,
    2. Michon A.-M.,
    3. Breitwieser W.,
    4. Ephrussi A.
    (1995) Translational control of oskar generates Short OSK, the isoform that induces pole plasm assembly. Development 121, 3723–3732
    OpenUrlAbstract
    1. Muskavitch M. A.
    (1994) Delta-Notch signaling and Drosophila cell fate choice. Dev. Biol 166, 415–430
    OpenUrlCrossRefPubMedWeb of Science
    1. Nusslein-Volhard C.,
    2. Frohnhofer H. G.,
    3. Lehmann R.
    (1987) Determination of anteroposterior polarity in Drosophila. Science 238, 1675–1681
    OpenUrlAbstract/FREE Full Text
    1. Pokrywka N. J.,
    2. Stephenson E. C.
    (1991) Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis. Development 113, 55–66
    OpenUrlAbstract
    1. Poulson D. F.
    (1940) The effects of certain X-chromosome deficiencies on the embryonic development of Drosophila melanogaster. J. Exp. Zool 83, 271–325
    OpenUrlCrossRefWeb of Science
    1. Rebay I.,
    2. Fehon R. G.,
    3. Artavanis-Tsakonas S.
    (1993) Specific truncations of Drosophila Notch define dominant activated and dominant negative forms of the receptor. Cell 74, 319–329
    OpenUrlCrossRefPubMedWeb of Science
    1. Roehl H.,
    2. Kimble J.
    (1993) Control of cell fate in C. elegans by a GLP-1 peptide consisting primarily of ankyrin repeats. Nature 364, 632–635
    OpenUrlCrossRefPubMed
    1. Rongo C.,
    2. Lehmann R.
    (1996) Regulated synthesis, transport and assembly of the Drosophila germ plasm. Trends in Gen 12, 102–109
    OpenUrlCrossRefPubMedWeb of Science
    1. Roth S.,
    2. Neuman-Silberberg F. S.,
    3. Barcelo G.,
    4. Schupbach T.
    (1995) Cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 81, 967–978
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruohola H.,
    2. Bremer K. A.,
    3. Baker D.,
    4. Swedlow J. R.,
    5. Jan L. Y.,
    6. Jan Y. N.
    (1991) Role of neurogenic genes in establishment of follicle cell fate and ooctye polarity during oogenesis in Drosophila. Cell 66, 433–449
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruohola-Baker H.,
    2. Jan L.,
    3. Jan Y. N.
    (1994) The role of gene cassettes in axis formation during Drosophila oogenesis. Trends in Gen 10, 89–94
    OpenUrlCrossRefPubMedWeb of Science
    1. St Johnston D.,
    2. Beuchle D.,
    3. Nusslein-Volhard C.
    (1991) Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51–63
    OpenUrlCrossRefPubMedWeb of Science
    1. St Johnston D.,
    2. Driever W.,
    3. Berleth T.,
    4. Richstein S.,
    5. Nusslein-Volhard C.
    (1989) Multiple steps in localization of Bicoid mRNA to the anterior pole of the Drosophila oocyte. Development 107, 13–19
    1. Struhl G.,
    2. Fitzgerald K.,
    3. Greenwald I.
    (1993) Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74, 331–345
    OpenUrlCrossRefPubMedWeb of Science
    1. Theurkauf W.,
    2. Smiley S.,
    3. Wong M.,
    4. Alberts B.
    (1992) Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development 115, 923–936
    OpenUrlAbstract
    1. Theurkauf W.
    (1994) Premature microtubule-dependent cytoplasmic streaming in cappuccino and spire mutant oocytes. Science 265, 2093–2096
    OpenUrlAbstract/FREE Full Text
    1. Xu T.,
    2. Caron L. A.,
    3. Fehon R. G.,
    4. Artavanis-Tsakonas S.
    (1992) The involvement of the Notch locus in Drosophila oogenesis. Development 115, 913–922
    OpenUrlAbstract
    1. Zipursky S. L.,
    2. Venkatesh T. R.,
    3. Teplow D. B.,
    4. Benzer S.
    (1984) Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 36, 15–26
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Expression of constitutively active Notch arrests follicle cells at a precursor stage during Drosophila oogenesis and disrupts the anterior-posterior axis of the oocyte
M.K. Larkin, K. Holder, C. Yost, E. Giniger, H. Ruohola-Baker
Development 1996 122: 3639-3650;
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