Advertisement
JOURNAL ARTICLES
The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo
J. Noordermeer, P. Johnston, F. Rijsewijk, R. Nusse, P.A. Lawrence
Development 1992 116: 711-719;

Summary

The segment polarity gene wingless has an essential function in cell-to-cell communication during various stages of Drosophila development. The wingless gene encodes a secreted protein that affects gene expression in surrounding cells but does not spread far from the cells where it is made. In larvae, wingless is necessary to generate naked cuticle in a restricted part of each segment. To test whether the local accumulation of wingless is essential for its function, we made transgenic flies that express wingless under the control of a hsp70 promoter (HS-wg flies). Uniform wingless expression results in a complete naked cuticle, uniform armadillo accumulation and broadening of the engrailed domain. The expression patterns of patched, cubitus interruptus Dominant and Ultrabithorax follow the change in engrailed. The phenotype of heatshocked HS-wg embryos resembles the segment polarity mutant naked, suggesting that embryos that overexpress wingless or lack the naked gene enter similar developmental pathways. The ubiquitous effects of ectopic wingless expression may indicate that most cells in the embryo can receive and interpret the wingless signal. For the development of the wild-type pattern, it is required that wingless is expressed in a subset of these cells.

REFERENCES

    1. Babu P.
    (1977) Early developmental subdivisions of the wing disk in Drosophila. Mol. Gen. Genet 151, 289–294
    OpenUrlCrossRefPubMed
    1. Baker N. E.
    (1987) Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila: The spatial distribution of a transcript in embryos. EMBO J 6, 1765–1773
    OpenUrlPubMedWeb of Science
    1. Baumgartner S.,
    2. Bopp D.,
    3. Burri M.,
    4. Noll M.
    (1987) Structure of two genes at the gooseberry locus related to the paired gene and their spatial expression during Drosophila embryogenesis. Genes Dev 1, 1247–1267
    OpenUrlAbstract/FREE Full Text
    1. Bejsovec A.,
    2. Martinez Arias A.
    (1991) Roles of wingless in patterning the larval epidermis of Drosophila. Development 113, 471–485
    OpenUrlAbstract
    1. Bourouis M.,
    2. Moore P.,
    3. Puel L.,
    4. Grau Y.,
    5. Heitzler P.,
    6. Simpson P.
    (1990) An early embryonic product of the gene shaggy encodes aserine/threonine protein kinase related to CDC28/cdc2+ subfamily. EMBO J 9, 2877–2884
    OpenUrlPubMedWeb of Science
    1. Bradley R. S.,
    2. Brown A. M.
    (1990) The proto-oncogene int-1 encodes a secreted protein associated with the extracellular matrix. EMBO J 9, 1569–1575
    OpenUrlPubMedWeb of Science
    1. DiNardo S.,
    2. Sher E.,
    3. Heemskerk-Jorgens J.,
    4. Kassis J.,
    5. O'Farrell P.
    (1988) Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis. Nature 332, 604–609
    OpenUrlCrossRefPubMed
    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. Fjose A.,
    2. McGinnis W. J.,
    3. Gehring W. J.
    (1985) Isolation of a homeobox-containing gene from the engrailed region of Drosophila and the spatial distribution of its transcript. Nature 313, 284–289
    OpenUrlCrossRefPubMed
    1. González F.,
    2. Swales L.,
    3. Bejsovec A.,
    4. Skaer H.,
    5. Arias A. M.
    (1991) Secretion and movement of wingless protein in the epidermis of the Drosophila embryo. Mech. Dev 35, 43–54
    OpenUrlCrossRefPubMedWeb of Science
    1. Hama C.,
    2. Ali Z.,
    3. Kornberg T. B.
    (1990) Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev 4, 1079–1093
    OpenUrlAbstract/FREE Full Text
    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, 404–410
    OpenUrlCrossRefPubMedWeb of Science
    1. Hidalgo A.,
    2. Ingham P.
    (1990) Cell patterning in the Drosophila segment: spatial regulation of the segment polarity gene patched. Development 110, 291–301
    OpenUrlAbstract
    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.,
    2. Taylor A. M.,
    3. Nakano Y.
    (1991) Role of the Drosophila patched gene in positional signalling. Nature 353, 184–187
    OpenUrlCrossRefPubMed
    1. Jue S.,
    2. Bradley R.,
    3. Rudnicki J.,
    4. Varmus H.,
    5. Brown A.
    (1992) The mouse Wnt-1 gene can act as a paracrine mechanism in transformation of mammary epithelial cells. Mol. Cell. Biol 12, 321–328
    OpenUrlAbstract/FREE Full Text
    1. Kornberg T.,
    2. Siden I.,
    3. O'Farrell P.,
    4. Simon M.
    (1985) The engrailed locus of Drosophila: in situ localization of transcripts reveals compartment-specific expression. Cell 40, 45–56
    OpenUrlCrossRefPubMedWeb of Science
    1. Krämer H.,
    2. Cagan R. L.,
    3. Zipursky S. L.
    (1991) Interaction of bride of sevenless membrane-bound ligand and the sevenless tyrosine-kinase receptor. Nature 352, 207–212
    OpenUrlCrossRefPubMed
    1. Lawrence P. A.,
    2. Johnston P.,
    3. Macdonald P.,
    4. Struhl G.
    (1987) Borders of parasegments in Drosophila embryos are delimited by the fushi tarazu and even-skipped genes. Nature 328, 440–442
    OpenUrlCrossRefPubMed
    1. Lohs-Schardin M.,
    2. Cremer C.,
    3. Nusslein-Volhard C.
    (1979) A fate map for the larval epidermis of Drosophila melanogaster: localized cuticle defects following irradiation of the blastoderm with an ultraviolet laser microbeam. Dev. Biol 73, 239–255
    OpenUrlCrossRefPubMedWeb of Science
    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. Martinez-Arias A.,
    2. White R. A. H.
    (1988) Ultrabithorax and engrailed expression in Drosophila embryos mutant for segmentation genes of the pair-rule class. Development 102, 325–338
    OpenUrlAbstract
    1. Martinez-Arias A.,
    2. Lawrence P. A.
    (1985) Parasegments and compartments in the Drosophila embryo. Nature 313, 639–642
    OpenUrlCrossRefPubMedWeb of Science
    1. McCrea P. D.,
    2. Turck C. W.,
    3. Gumbiner B.
    (1991) A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science 254, 1359–1361
    OpenUrlAbstract/FREE Full Text
    1. Moran L.,
    2. Mirault M.-E.,
    3. Tissieres A.,
    4. Lis J.,
    5. Schedl P.,
    6. Artavanis-Tsakonas S.,
    7. Gehring W. J.
    (1979) Physical map of two D. melanogaster DNA segments containing sequences coding for the 70,000 dalton heat shock protein. Cell 17, 1–8
    OpenUrlCrossRefPubMedWeb of Science
    1. Morata G.,
    2. Lawrence P. A.
    (1977) The development of wingless, a homeotic mutation of Drosophila. Dev. Biol 56, 227–240
    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) The Drosophila segment polarity gene patched encodes a protein with multiple potential membrane spanning domains. Nature 341, 508–513
    OpenUrlCrossRefPubMed
    1. Nusse R.,
    2. Varmus H. E.
    (1992) Wnt genes. Cell 69, 1073–1087
    OpenUrlCrossRefPubMedWeb of Science
    1. Nusslein-Volhard C.,
    2. Wieschaus E.
    (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287, 795–801
    OpenUrlCrossRefPubMedWeb of Science
    1. Orenic T. V.,
    2. Slusarski C.,
    3. Kroll K. L.,
    4. Holmgren R. A.
    (1990) Cloning and characterization of the segment polarity gene cubitus interruptus Dominant of Drosophila. Genes Dev 4, 1053–1067
    OpenUrlAbstract/FREE Full Text
    1. Papkoff J.,
    2. Schryver B.
    (1990) Secreted int-1 protein is associated with the cell surface. Mol. Cell Biol 10, 2723–2730
    OpenUrlAbstract/FREE Full Text
    1. Peifer M.,
    2. Wieschaus E.
    (1990) The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell 63, 1167–1178
    OpenUrlCrossRefPubMedWeb of Science
    1. Perrimon N.,
    2. Smouse D.
    (1989) Multiple functions of a Drosophila homeotic gene, zeste-white 3, during segmentation and neurogenesis. Dev. Biol 135, 287–305
    OpenUrlCrossRefPubMed
    1. Preat T.,
    2. Therond P.,
    3. Lamour-Isnard C.,
    4. Limbourg-Bouchon B.,
    5. Tricoire H.,
    6. Erk I.,
    7. Mariol M.-C.,
    8. Busson D.
    (1990) A putative serine/threonine protein kinase encoded by the segment-polarity fused gene of Drosophila. Nature 347, 87–89
    OpenUrlCrossRefPubMed
    1. Riggleman B.,
    2. Schedl P.,
    3. Wieschaus E.
    (1990) Spatial expression of the Drosophila segment polarity gene armadillo is post-transcriptionally regulated by wingless. Cell 63, 549–560
    OpenUrlCrossRefPubMedWeb of Science
    1. Riggleman B.,
    2. Wieschaus E.,
    3. Schedl P.
    (1989) Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene. Genes Dev 3, 96–113
    OpenUrlAbstract/FREE Full Text
    1. Rijsewijk F.,
    2. Schuermann M.,
    3. Wagenaar E.,
    4. Parren P.,
    5. Weigel D.,
    6. Nusse R.
    (1987) The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50, 649–57
    OpenUrlCrossRefPubMedWeb of Science
    1. Sharma R. P.,
    2. Chopra V. L.
    (1976) Effect of the wingless (wg1) mutation on wing and haltere development in Drosophila melanogaster. Dev. Biol 48, 461–465
    OpenUrlCrossRefPubMedWeb of Science
    1. Siegfried E.,
    2. Perkins L. A.,
    3. Capaci T. M.,
    4. Perrimon N.
    (1990) Putative protein kinase product of the Drosophila segment-polarity gene zeste-white3. Nature 345, 825–829
    OpenUrlCrossRefPubMedWeb of Science
    1. Simcox A.,
    2. Roberts I.,
    3. Hersperger E.,
    4. Gribbin C.,
    5. Shearn A.,
    6. Whittle R.
    (1989) Imaginal discs can be removed from cultured embryos mutant for the segment polarity genes engrailed, naked and patched, but not from wingless. Development 107, 715–722
    OpenUrlAbstract/FREE Full Text
    1. Stein D.,
    2. Roth S.,
    3. Vogelsang E.,
    4. Nusslein-Volhard C.
    (1991) The polarity of the dorsoventral axis in the Drosophila embryo is defined by an extracellular signal. Cell 65, 725–735
    OpenUrlCrossRefPubMedWeb of Science
    1. Stevens L. M.,
    2. Frohnhöfer H. G.,
    3. Klingler M.,
    4. Nusslein-Volhard C.
    (1990) Localized requirement for torso -like expression in follicle cells for development of terminal anlagen of the Drosophila embryo. Nature 346, 660–663
    OpenUrlCrossRefPubMed
    1. Tautz D.,
    2. Pfeiffle C.
    (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Török I.,
    2. Karch F.
    (1980) Nucleotide sequences of heat shock activated genes in Drosophila melanogaster. I. Sequences in regions of the 5and 3 ends of the hsp 70 gene in the hybrid plasmid 56H8. Nucl. Acids Res 8, 3105–3123
    OpenUrlAbstract/FREE Full Text
    1. van den Heuvel M.,
    2. Nusse R.,
    3. Johnston P.,
    4. Lawrence P. A.
    (1989) Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell 59, 739–749
    OpenUrlCrossRefPubMedWeb of Science
    1. White R. A. H.,
    2. Wilcox M.
    (1985) Distribution of Ultra-bithorax proteins in Drosophila. EMBO J 4, 2035–2043
    OpenUrlPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo
J. Noordermeer, P. Johnston, F. Rijsewijk, R. Nusse, P.A. Lawrence
Development 1992 116: 711-719;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

A new society for regenerative biologists

Kenneth Poss and Elly Tanaka announce the launch of the International Society for Regenerative Biology (ISRB), which will promote research and education in the field of regenerative biology.

Upcoming special issue: call for papers

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

The special issue welcomes Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

An interview with Cagney Coomer

Over a virtual chat, we spoke to Cagney Coomer about her experiences in the lab, the classroom and the community centre, and why she thinks outreach and role models are vital to science.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.