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JOURNAL ARTICLES
The Serrate locus of Drosophila and its role in morphogenesis of the wing imaginal discs: control of cell proliferation
S.A. Speicher, U. Thomas, U. Hinz, E. Knust
Development 1994 120: 535-544;

Summary

The Drosophila gene Serrate encodes a transmembrane protein with 14 EGF-like repeats in its extracellular domain. Here we show that loss-of-function mutations in this gene lead to larval lethality. Homozygous mutant larvae fail to differentiate the anterior spiracles, exhibit poorly developed mouth-hooks and show a severe reduction in the size of the wing and haltere primordia, which is not due to cell death. The few homozygous mutant escapers that pupariate develop into pharate adults that almost completely lack wings and halteres. Clonal analysis in the adult epidermis demonstrates a requirement for Serrate during wing and haltere development. Targeted ectopic expression of Serrate in the imaginal discs using the yeast transcriptional activator Gal4 results in regionally restricted induction of cell proliferation, e.g. the ventral tissues in the case of the wings and halteres. The results suggest that the wild-type function of Serrate is required for the control of position-specific cell proliferation during development of meso- and metathoracic dorsal discs, which in turn exerts a direct effect on morphogenesis.

REFERENCES

    1. Bate M.,
    2. Martinez Arias A.
    (1991) The embryonic origin of imaginal discs in Drosophila. Development 112, 755–759
    OpenUrlAbstract
    1. Brand A.,
    2. Perrimon N.
    (1993) Targeted expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415
    OpenUrlAbstract
    1. Bryant P. J.
    (1975) Pattern formation in the imaginal wing disc of Drosophila melanogaster. J. Exp. Zool 192, 49–78
    OpenUrl
    1. Bryant P. J.
    (1993) The polar coordinate model goes molecular. Nature 259, 471–472
    1. Bryant P. J.,
    2. Huettner B.,
    3. Held L. I.,
    4. Ryerse J.,
    5. Szidonya J.
    (1988) Mutations at the fat locus interfere with cell proliferation control and epithelial morphogenesis in Drosophila. Dev. Biol 129, 541–554
    OpenUrlCrossRefPubMedWeb of Science
    1. Bryant P. J.,
    2. Levinson P.
    (1985) Intrinsic growth control in the imaginal primordia of Drosophila, and the autonomous action of a lethal mutation causing overgrowth. Dev. Biol 107, 355–363
    OpenUrlCrossRefPubMedWeb of Science
    1. Bunch T. A.,
    2. Grunblat Y.,
    3. Goldstein L. S. B.
    (1988) Characterization and use of the Drosophila melanogaster metallothionein promoter in cultured Drosophila melanogaster cells. Nucl. Acids Res 16, 1043–1061
    OpenUrlAbstract/FREE Full Text
    1. Carroll S. B.,
    2. Laughon A.,
    3. Thalley B. S.
    (1988) Expression, function, and regulation of the hairy segmentation protein in the Drosophila embryo. Genes Dev 2, 883–890
    OpenUrlAbstract/FREE Full Text
    1. Cohen B.,
    2. MacGuffin E.,
    3. Pfeifle C.,
    4. Segal D.,
    5. Cohen S. M.
    (1992) apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genes Dev 6, 715–729
    OpenUrlAbstract/FREE Full Text
    1. Couso J. P.,
    2. Bate M.,
    3. Martinez-Arias A.
    (1993) A wingless -dependent polar coordinate system in Drosophila imaginal discs. Science 259, 484–489
    OpenUrlAbstract/FREE Full Text
    1. de Celis J. F.,
    2. Barrio R.,
    3. del Arco A.,
    4. Garcia-Bellido A.
    (1993) Genetic and molecular characterization of a Notch mutation in its Delta-and Serrate-binding domain in Drosophila. Proc. Natl. Acad. Sci. USA 90, 4037–4041
    OpenUrlAbstract/FREE Full Text
    1. Ellisen L. W.,
    2. Bird J.,
    3. West D. C.,
    4. Soreng A. L.,
    5. Reynolds T. C.,
    6. Smith D. S.,
    7. Sklar J.
    (1991) TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocation in T lymphoblastic neoplasms. Cell 66, 649–661
    OpenUrlCrossRefPubMedWeb of Science
    1. Fleming R. J.,
    2. Scottgale T. N.,
    3. Diederich R. J.,
    4. Artavanis-Tsakonas S.
    (1990) The gene Serrate encodes a putative EGF-like transmembrane protein essential for proper ectodermal development in Drosophila melanogaster. Genes Dev 4, 2188–2201
    OpenUrlAbstract/FREE Full Text
    1. French V.,
    2. Bryant P. J.,
    3. Bryant S. V.
    (1976) Pattern regulation in epimorphic fields. Science 193, 969–981
    OpenUrlAbstract/FREE Full Text
    1. Fristrom D.
    (1969) Cellular degeneration in the production of some mutant phenotypes in Drosophila melanogaster. Molec. Gen. Genetics 103, 363–379
    OpenUrlCrossRefPubMed
    1. Garcia-Bellido A.,
    2. de Celis J. F.
    (1992) developmental genetics of the venation pattern of Drosophila. Ann. Rev. Genetics 26, 277–304
    OpenUrlCrossRefPubMedWeb of Science
    1. Garcia-Bellido A.,
    2. Merriam J. R.
    (1971) Parameters of the wing imaginal disc development of Drosophila melanogaster. Dev. Biol 24, 61–87
    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. Hooper K. L.,
    2. Parkhust S. M.,
    3. Ish-Horowicz D.
    (1989) Spatial control of hairy protein expression during embryogenesis. Development 107, 489–504
    OpenUrlAbstract
    1. Jhappan C.,
    2. Gallahan D.,
    3. Stahle C.,
    4. Chu E.,
    5. Smith G. H.,
    6. Merlino G.,
    7. Callahan R.
    (1992) Expression of an activated Notch -related int-3 transgene interferes with cell differentiation and induces neoplastic transformation im mammary and salivary glands. Genes Dev 6, 345–355
    OpenUrlAbstract/FREE Full Text
    1. Kidd S.,
    2. Kelley M. R.,
    3. Young M. W.
    (1986) Sequence of the Notch locus of Drosophila melanogaster: Relationship of the encoded protein to mammalian clotting and growth factors. Molec. Cell. Biol 6, 3094–3108
    OpenUrlAbstract/FREE Full Text
    1. Kopczynski C. C.,
    2. Alton A. K.,
    3. Fechtel K.,
    4. Kooh P. J.,
    5. Muskavitch M. A. T.
    (1988) Delta, a Drosophila neurogenic gene, is transcriptionally complex and encodes a protein related to blood coagulation factors and epidermal growth factor of vertebrates. Genes Dev 2, 1723–1735
    OpenUrlAbstract/FREE Full Text
    1. Laski F. A.,
    2. Rio D. C.,
    3. Rubin G. M.
    (1986) Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell 44, 7–19
    OpenUrlCrossRefPubMedWeb of Science
    1. Mahoney P. A.,
    2. Weber U.,
    3. Onofrechuk P.,
    4. Biessmann H.,
    5. Bryant P. J.,
    6. Goodman C. S.
    (1991) The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamiliy. Cell 67, 853–868
    OpenUrlCrossRefPubMedWeb of Science
    1. Martin P.,
    2. Martin A.,
    3. Shearn A.
    (1977) Studies of l(3)c43hs1 -a polyphasic, temperature-sensitive mutant of Drosophila melanogster with a variety of imaginal discs defects. Dev. Biol 55, 213–232
    OpenUrlCrossRefPubMed
    1. Martinez Arias A.
    (1989) A cellular basis for pattern formation in the insect epidermis. Trends Genet 5, 262–267
    OpenUrlCrossRefPubMedWeb of Science
    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, 508–513
    OpenUrlCrossRefPubMed
    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-signalling mechanism in imaginal discs. Development 110, 105–114
    OpenUrlAbstract
    1. Posakony L. G.,
    2. Raftery L. A.,
    3. Gelbart W. M.
    (1991) Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior-posterior compartment boundary. Mech. Dev 33, 69–82
    OpenUrl
    1. Rebay I.,
    2. Fleming R. J.,
    3. Fehon R. G.,
    4. Cherbas L.,
    5. Cherbas P.,
    6. Artavanis-Tsakonas S.
    (1991) Specific EGF repeats of Notch mediate interactions with Delta and Serrate: Implications for Notch as a multifunctional receptor. Cell 67, 687–699
    OpenUrlCrossRefPubMedWeb of Science
    1. Rothberg J. M.,
    2. Hartley D. A.,
    3. Walter Z.,
    4. Artavanis-Tsakonas S.
    (1988) slit: an EGF-homologous locus of Drosophila melanogaster involved in the development of the embryonic central nervous system. Cell 55, 1047–1059
    OpenUrlCrossRefPubMedWeb of Science
    1. Rothberg J. M.,
    2. Jacobs J. R.,
    3. Goodman C. S.,
    4. Artavanis-Tsakonas S.
    (1990) slit: an extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGF and LRR domains. Genes Dev 4, 2169–2187
    OpenUrlAbstract/FREE Full Text
    1. Sharma R. P.,
    2. Chopra V. L.
    (1976) Effects of wingless (wg1) mutation on wing and haltere development in Drosohila melanogaster. Dev. Biol 48, 461–465
    OpenUrlCrossRefPubMedWeb of Science
    1. Shellenbarger D. L.,
    2. Mohler J. D.
    (1978) Temperature-sensitive periods and autonomy of pleiotropic effects of l(1)Nts1, a conditional Notch lethal of Drosophila. Dev. Biol 62, 432–446
    OpenUrlCrossRefPubMedWeb of Science
    1. Tepaβ U.,
    2. Theres C.,
    3. Knust E.
    (1990) The Drosophila gene crumbs encodes an EGF-like protein, expressed on apical membranes of epithelial cells and required for organization of epithelia. Cell 61, 787–799
    OpenUrlCrossRefPubMedWeb of Science
    1. Thomas U.,
    2. Speicher S. A.,
    3. Knust E.
    (1991) The Drosophila gene Serrate encodes an EGF-like transmembrane protein with a complex expression pattern in embryos and wing discs. Development 111, 749–761
    OpenUrlAbstract
    1. Vässin H.,
    2. Bremer K. A.,
    3. Knust E.,
    4. Campos-Ortega J. A.
    (1987) The neurogenic locus Delta of Drosophila melanogaster is expressed in neurogenic territories and encodes a putative transmembrane protein with EGF-like repeats. EMBO J 6, 3431–3440
    OpenUrlPubMedWeb of Science
    1. Wharton K. A.,
    2. Johansen K. M.,
    3. Xu T.,
    4. Artavanis-Tsakonas S.
    (1985) Nucleotide sequence from the neurogenic locus Notch implies a gene product that shares homology with proteins containing EGF-like repeats. Cell 43, 567–581
    OpenUrlCrossRefPubMedWeb of Science
    1. Whittle J. R. S.
    (1990) Pattern formation in imaginal discs. Seminars in Cell Biology 1, 241–252
    OpenUrlPubMed
    1. Williams J. A.,
    2. Bell J. B.,
    3. Carroll S. B.
    (1991) Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev 5, 2481–2495
    OpenUrlAbstract/FREE Full Text
    1. Williams J. A.,
    2. Carroll S. B.
    (1993) the origin, patterning and evolution of insect appendages. BioEssays 15, 567–577
    OpenUrlCrossRefWeb of Science
    1. Williams J. A.,
    2. Paddock S. W.,
    3. Carroll S. B.
    (1993) Pattern formation in a secondary field: a hierarchy of regulatory genes subdiviedes the developing Drosophila wing disc into discrete subregions. Development 117, 571–584
    OpenUrlAbstract
    1. Wilson T. G.
    (1981) Expression of phenotypes in a temperature-sensitive allele of the apterous mutation in Drosophila melanogaster. Dev. Biol 85, 425–433
    OpenUrlCrossRefPubMed
    1. Woods D. F.,
    2. Bryant P. J.
    (1991) The Discs-large tumour suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66, 451–464
    OpenUrlCrossRefPubMedWeb of Science
    1. Yochem J.,
    2. Greenwald I.
    (1989) glp-1 and lin-12, genes implicated in distinct cell-cell interactions in C. elegans, encode similar transmembrane proteins. Cell 58, 553–563
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
The Serrate locus of Drosophila and its role in morphogenesis of the wing imaginal discs: control of cell proliferation
S.A. Speicher, U. Thomas, U. Hinz, E. Knust
Development 1994 120: 535-544;
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