Advertisement
JOURNAL ARTICLES
wingless acts through the shaggy/zeste-white 3 kinase to direct dorsal-ventral axis formation in the Drosophila leg
F.J. Diaz-Benjumea, S.M. Cohen
Development 1994 120: 1661-1670;

Summary

The secreted glycoproteins encoded by Wnt genes are thought to function as intercellular signaling molecules which convey positional information. Localized expression of Wingless protein is required to specify the fate of ventral cells in the developing Drosophila leg. We report here that Wingless acts through inactivation of the shaggy/zeste white 3 protein kinase to specify ventral cell fate in the leg. Ectopic expression of Wingless outside its normal ventral domain has been shown reorganize the dorsal-ventral axis of the leg in a non-autonomous manner. Using genetic mosaics, we show that cells that lack shaggy/zeste white 3 activity can influence the fate of neighboring cells to reorganize dorsal-ventral pattern in the leg, in the same manner as Wingless-expressing cells. Therefore, clones of cells that lack shaggy/zeste white 3 activity exhibit all of the organizer activity previously attributed to Wingless-expressing cells, but do so without expressing wingless. We also show that the organizing activity of ventral cells depends upon the location of the clone along the dorsal-ventral axis. These findings suggest that Wingless protein does not function as a morphogen in the dorsal-ventral axis of the leg.

REFERENCES

    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, 1765–1774
    OpenUrlPubMedWeb of Science
    1. Baker N. E.
    (1988) Transcription of the segment-polarity gene wingless in the imaginal discs of Drosophila and the phenotype of a pupal lethal wg mutation. Development 102, 489–497
    OpenUrlAbstract
    1. Baker N. E.
    (1988) Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila. Dev. Biol 125, 96–108
    OpenUrlCrossRefPubMedWeb of Science
    1. Bate M.,
    2. Martinez Arias A.
    (1991) The embryonic origin of imaginal discs in Drosophila. Development 112, 755–761
    OpenUrlAbstract
    1. Bejsovec A.,
    2. Martinez Arias A.
    (1991) Roles of wingless in patterning of the larval epidermis of Drosophila. Development 113, 471–485
    OpenUrlAbstract
    1. Bohn H.
    (1972) The origin of the epidermis in the supernumerary regenerates of triple legs in cockroaches (Blattaria). J. Embryol. Exp. Morph 28, 185–208
    OpenUrlPubMedWeb of Science
    1. Bourouis M.,
    2. Moore P.,
    3. Ruel L.,
    4. Grau Y.,
    5. Heitzler P.,
    6. Simpson P.
    (1990) An early embryonic product of the gene shaggy encodes a serine/threonine protein kinase related to the 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. Campbell G.,
    2. Weaver T.,
    3. Tomlinson A.
    (1993) Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 74, 1113–1123
    OpenUrlCrossRefPubMedWeb of Science
    1. Cohen B.,
    2. Simcox A. A.,
    3. Cohen S. M.
    (1993) Allocation of the thoracic imaginal disc primordia in the Drosophila embryo. Development 117, 597–608
    OpenUrlAbstract
    1. Cohen B.,
    2. Wimmer E. A.,
    3. Cohen S. M.
    (1991) Early development of leg and wing primordia in the Drosophila embryo. Mech. Devel 33, 229–240
    OpenUrlCrossRefPubMedWeb of Science
    1. Cohen S. M.
    (1990) Specification of limb development in the Drosophila embryo by positional cues from segmentation genes. Nature 343, 173–177
    OpenUrlCrossRefPubMed
    1. Cohen S. M.,
    2. DiNardo S.
    (1993) wingless: from embryo to adult. Trends Genet 9, 189–192
    OpenUrlCrossRefPubMed
    1. Couso J. P.,
    2. Bate M.,
    3. Martinez Arias A.
    (1993) A wingless- dependent polar coordinate system in the imaginal discs of Drosophila. Science 259, 484–489
    OpenUrlAbstract/FREE Full Text
    1. Couso J. P.,
    2. Gonzalez-Gaitan M.
    (1993) Embryonic limb development in Drosophila. Trends Genet 9, 371–373
    OpenUrlCrossRefPubMed
    1. Cumberledge S.,
    2. Krasnow M. A.
    (1993) Intercellular signaling in Drosophila segment formation reconstructed in vitro. Nature 363, 549–552
    OpenUrlCrossRefPubMed
    1. Diaz-Benjumea F. J.,
    2. Cohen S. M.
    (1993) Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75, 741–752
    OpenUrlCrossRefPubMedWeb of Science
    1. DiNardo S.,
    2. Sher E.,
    3. Heemskerk J. J.,
    4. Kassis J. A.,
    5. O'Farrell P. H.
    (1988) Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis. Nature 332, 604–609
    OpenUrlCrossRefPubMed
    1. Dougan S.,
    2. DiNardo S.
    (1992) Drosophila wingless generates cell type diversity among engrailed expressing cells. Nature 360, 347–349
    OpenUrlCrossRefPubMed
    1. Echelard Y.,
    2. Epstein D. J.,
    3. St-Jaques B.,
    4. Shen L.,
    5. Mohler J.,
    6. McMahon J. A.,
    7. McMahon A. P.
    (1993) Sonic Hedgehog, a member of a family of putative signalling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417–1430
    OpenUrlCrossRefPubMedWeb of Science
    1. Ferrus A.
    (1975) Parameters of mitotic recombination in Minute mutants of Drosophila melanogaster. Genetics 79, 589–599
    OpenUrlAbstract/FREE Full Text
    1. French V.
    (1976) Leg regeneration in the cockroach, Blatella germanica. II. Regeneration from a non-congruent tibial host/graft junction. J. Embryol. Exp. Morph 35, 267–301
    OpenUrlPubMedWeb of Science
    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. González F.,
    2. Swales L.,
    3. Bejsovec A.,
    4. Skaer H.,
    5. Martinez Arias A.
    (1991) Secretion and movement of the wingless protein in the epidermis of the Drosophila embryo. Mech. Dev 35, 43–54
    OpenUrlCrossRefPubMedWeb of Science
    1. Greenwald I.,
    2. Rubin G.
    (1992) Making a difference: the role of cell-cell interactions in establishing separate identities for equivalent cells. Cell 68, 271–281
    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, 404–410
    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. Ingham P. W.,
    2. Martinez Arias A.
    (1992) Boundaries and fields in early embryos. Cell 68, 221–235
    OpenUrlCrossRefPubMedWeb of Science
    1. Jessell T. M.,
    2. Melton D. A.
    (1992) Diffusible factors in vertebrate embryonic induction. Cell 68, 257–270
    OpenUrlCrossRefPubMedWeb of Science
    1. Jue S. F.,
    2. Bradley R. S.,
    3. Rudnicki J. A.,
    4. Varmus H. E.,
    5. Brown A. M.
    (1992) The mouse Wnt-1 gene can act via a paracrine mechanism in transformation of mammary epithelial cells. Mol. Cell. Biol 12, 321–8
    OpenUrlAbstract/FREE Full Text
    1. Krauss S.,
    2. Concordet J.-P.,
    3. Ingham P. W.
    (1993) A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431–1444
    OpenUrlCrossRefPubMedWeb of Science
    1. Martinez Arias A.,
    2. Baker N. E.,
    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. McMahon A. P.,
    2. Moon R. T.
    (1989) Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis. Cell 58, 1075–1084
    OpenUrlCrossRefPubMedWeb of Science
    1. Meinhardt H.
    (1983) Cell determination boundaries as organizing regions for secondary embryonic fields. Dev. Biol 96, 375–385
    OpenUrlCrossRefPubMedWeb of Science
    1. Morata G.,
    2. Ripoll P.
    (1975) Minutes: mutants of Drosophila autonomously affecting cell division rate. Dev. Biol 42, 211–221
    OpenUrlCrossRefPubMedWeb of Science
    1. Noordermeer J.,
    2. Johnston P.,
    3. Rijswijk F.,
    4. Nusse R.,
    5. Lawrence P. A.
    (1992) The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo. Development 116, 711–719
    OpenUrlAbstract
    1. Nusse R.,
    2. Varmus H.
    (1992) Wnt genes. Cell 69, 1073–1087
    OpenUrlCrossRefPubMedWeb of Science
    1. Papkoff J.
    (1989) Inducible overexpression and secretion of int-1 protein. Mol. Cell. Biol 9, 3377–3384
    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. Parkin N. T.,
    2. Kitajewski J.,
    3. Varmus H. E.
    (1993) Activity of Wnt-1 as a transmembrane protein. Genes Dev 7, 2181–2193
    OpenUrlAbstract/FREE Full Text
    1. Peifer M.,
    2. Rauskolb C.,
    3. Williams M.,
    4. Riggleman B.,
    5. Wieschaus E.
    (1991) The segment polarity gene armadillo Interacts with the wingless signaling pathway in both embryonic and adult pattern formation. Development 111, 1029–1043
    OpenUrlAbstract/FREE Full Text
    1. Riddle R. D.,
    2. Johnson R. L.,
    3. Laufer E.,
    4. Tabin C.
    (1993) sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401–1416
    OpenUrlCrossRefPubMedWeb of Science
    1. Rijsewijk F.,
    2. Schuermann M.,
    3. Wagenaar E.,
    4. Parren P.,
    5. Weigel D.,
    6. Nusse R.
    (1987) The Drosophila homologue of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50, 649–657
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruel L.,
    2. Pantesco V.,
    3. Lutz Y.,
    4. Simpson P.,
    5. Bourouis M.
    (1993) Functional significance of a family of protein kinases encoded at the shaggy locus in Drosophila. EMBO J 12, 1657–1669
    OpenUrlPubMedWeb of Science
    1. Ruel L.,
    2. Bourouis M.,
    3. Heitzler P.,
    4. Pantesco V.,
    5. Simpson P.
    (1993) Drosophila shaggy kinase and rat glycogen synthase kinase-3 have conserved activities and act downstream of Notch. Nature 362, 557–560
    OpenUrlCrossRefPubMedWeb of Science
    1. Sampedro J.,
    2. Johnston P.,
    3. Lawrence P. A.
    (1993) A role for wingless in the segmental gradient of Drosophila. Development 117, 677–687
    OpenUrlAbstract
    1. Siegfried E.,
    2. Chou T.-B.,
    3. Perrimon N.
    (1992) wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell 71, 1167–1179
    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-white 3. Nature 345, 825–829
    OpenUrlCrossRefPubMedWeb of Science
    1. Simcox A. A.,
    2. Roberts I. J. H.,
    3. Hersperger E.,
    4. Gribbin M. C.,
    5. Shearn A.,
    6. Whittle J. R. S.
    (1989) Imaginal discs can be recovered 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. Smith W. C.,
    2. Harland R. M.
    (1991) Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 67, 753–765
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith W. C.,
    2. Harland R. M.
    (1992) Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70, 829–840
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith J. C.,
    2. Slack J. M. W.
    (1983) Dorsalization and neural induction: properties of the organiser in Xenopus laevis. J. Embryol. Exp. Morph 78, 299–317
    OpenUrlPubMedWeb of Science
    1. Sokol S.,
    2. Christian J. L.,
    3. Moon R.,
    4. Melton D.
    (1991) Injected Wnt RNA induces a complete body axis in Xenopus embryos. Cell 67, 741–752
    OpenUrlCrossRefPubMedWeb of Science
    1. Struhl G.,
    2. Basler K.
    (1993) Organizing activity of wingless protein in Drosophila. Cell 72, 527–540
    OpenUrlCrossRefPubMedWeb of Science
    1. Thaller C.,
    2. Eichele G.
    (1987) Identification and spatial distribution of retinoids in the developing chick limb bud. Nature 327, 625–628
    OpenUrlCrossRefPubMed
    1. Tickle C.,
    2. Alberts B.,
    3. Wolpert L.,
    4. Lee J.
    (1982) Local application of retinoic acid to the limb bud mimics action of the polarizing region. Nature 296, 564–565
    OpenUrlCrossRefPubMed
    1. Tickle C.,
    2. Summerbell D.,
    3. Wolpert L.
    (1975) Positional signalling and specification of digits in chick limb morphogenesis. Nature 254, 199–202
    OpenUrlCrossRefPubMedWeb of Science
    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. Wolpert L.
    (1969) Positional information and the spatial pattern of cellular differentiation. J. Theoret. Biol 25, 1–47
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
wingless acts through the shaggy/zeste-white 3 kinase to direct dorsal-ventral axis formation in the Drosophila leg
F.J. Diaz-Benjumea, S.M. Cohen
Development 1994 120: 1661-1670;
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

Interviews — Bénédicte Sanson and Kate Storey

Bénédicte Sanson and Kate Storey

Hear from Bénédicte Sanson, winner of the BSDB’s Cheryll Tickle medal, and Kate Storey, winner of the BSDB’s Waddington Medal, as they discuss their research, the future of the field and the importance of collaboration.

Review Commons launches

We're excited to be an affiliate journal for Review Commons, the ASAPbio/EMBO platform for high-quality journal-independent peer-review in the life sciences, which went live on 09 December.

Early-career researchers can apply for up to £2,500 to offset the cost of travel and expenses to make collaborative visits to other labs around the world. Read about Peter’s experience in Switzerland, where he joined forces with the Lutolf lab to refine a protocol for producing gastruloids.

Publishing peer review reports

To continue working towards transparency around the editorial process, Development now publishes a ‘Peer review history file’ alongside published papers. Read more about the policy and see the reports for yourself in one the first papers to publish the reports (under the ‘Info & metrics’ tab).

Development at a glance — Cell interactions in collective cell migration

Extract from the poster showing specific cell-cell interactions in metastasis.

Take a look at the latest poster and accompanying article by Denise Montell and her colleagues from the University of California, where they describe a sampling of both known and new cells that migrate collectively in vivo.