Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in
  • Log out

Search

  • Advanced search
Development
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Development

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube 

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
JOURNAL ARTICLES
Shaggy and dishevelled exert opposite effects on Wingless and Decapentaplegic expression and on positional identity in imaginal discs
T.R. Heslip, H. Theisen, H. Walker, J.L. Marsh
Development 1997 124: 1069-1078;
T.R. Heslip
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
H. Theisen
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
H. Walker
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
J.L. Marsh
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Info & metrics
  • PDF
Loading

Summary

The finding that Wingless (WG) and Decapentaplegic (DPP) suppress each others transcription provides a mechanism for creating developmental territories in fields of cells. Here, we address the mechanism of that antagonism. The dishevelled (dsh) and shaggy (sgg) genes encode intracellular proteins generally thought of as downstream of WG signaling. We have investigated the effects of changing either DSH or SGG activity on both cell fate and wg and dpp expression. At the level of cell fate in discs, DSH antagonizes SGG activity. At the level of gene expression, SGG positively regulates dpp expression and negatively regulates wg expression while DSH activity suppresses dpp expression and promotes wg expression. Sharp borders of gene expression correlating precisely with clone boundaries suggest that the effects of DSH and SGG on transcription of wg and dpp are not mediated by secreted factors but rather act through intracellular effectors. The interactions described here suggest a model for the antagonism between WG and DPP that is mediated via SGG. The model incorporates autoactivation and lateral inhibition, which are properties required for the production of stable patterns. The regulatory interactions described exhibit extensive ability to organize new pattern in response to manipulation or injury.

REFERENCES

    1. Abbot L. C.,
    2. Karpen G. H.,
    3. Schubiger G.
    (1981) Compartmental restrictions and blastema formation during pattern regulation in Drosophila imaginal discs. Dev. Biol 87, 64–75
    OpenUrlCrossRefPubMed
    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. 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. Blair S. S.
    (1995) Compartments and appendage development in Drosophila. BioEssays 17, 299–309
    OpenUrlCrossRefPubMedWeb of Science
    1. Brook W. J.,
    2. Cohen S. M.
    (1996) Antagonistic interactions between Wingless and Decapentaplegic responsible for dorsal-ventral pattern in the Drosophila leg. Science 273, 1373–1377
    OpenUrlAbstract
    1. Bryant S. V.,
    2. French V.,
    3. Bryant P. J.
    (1981) Distal Regeneration and Symmetry. Science 212, 993–1002
    OpenUrlAbstract/FREE Full Text
    1. Campbell G.,
    2. Tomlinson A.
    (1995) Initiation of the proximodistal axis in insect legs. Development 121, 619–628
    OpenUrlAbstract
    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. Chou T. B.,
    2. Perrimon N.
    (1992) Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131, 643–53
    OpenUrlAbstract/FREE Full Text
    1. Diaz-Benjumea F. J.,
    2. Cohen S. M.
    (1994) wingless acts through shaggy/zeste-white 3 kinase to direct dorsal-ventral axis formation in the Drosophila leg. Development 120, 1661–1670
    OpenUrlAbstract
    1. Dominguez M.,
    2. Brunner M.,
    3. Hafen E.,
    4. Basler K.
    (1996) Sending and receiving the Hedgehog signal: control by the Drosophila Gli protein Cubitus interruptus. Science 272, 1621–1625
    OpenUrlAbstract
    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. Girton J. R.
    (1981) Pattern triplications produced by a cell-lethal mutation in Drosophila. Dev. Biol 84, 164–172
    OpenUrlCrossRefPubMed
    1. Hannah-Alava A.
    (1958) Morphology and chaetotaxy of the legs of Drosophila melanogaster. J. Morph 103, 281–310
    OpenUrlCrossRef
    1. Heberlein U.,
    2. Wolff T.,
    3. Rubin G.
    (1993) The TGFhomolog dpp and the segment polarity gene hedgehog are required for propagation of the morphogenetic wave in the Drosophila retina. Cell 75, 913–926
    OpenUrlCrossRefPubMedWeb of Science
    1. Ingham P. W.
    (1996) Signaling by hedgehog family proteins in Drosophila and vertebrate development. Curr. Opin. Genet. Dev 5, 492–498
    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. Jiang J.,
    2. Struhl G.
    (1996) Complementary and mutually exclusive activities of decapentaplegic and wingless organize axial patterning during Drosophila leg development. Cell 86, 401–409
    OpenUrlCrossRefPubMedWeb of Science
    1. Johnson R. J.,
    2. Grenier J. K.,
    3. Scott M. P.
    (1995) patched overexpression alters wing disc size and pattern: transcriptional and post-transcriptional effects on hedgehog targets. Development 121, 4161–4170
    OpenUrlAbstract
    1. Johnston L. A.,
    2. Schubiger G.
    (1996) Ectopic expression of wingless in imaginal discs interferes with decapentaplegic expression and alters cell determination. Development 122, 3519–3529
    OpenUrlAbstract
    1. Kassis J. A.,
    2. Noll E.,
    3. VanSickle E. P.,
    4. Odenwald W. F.,
    5. Perrimon N.
    (1992) Altering the insertional specificity of a Drosophila transposable element. Proc. Natl Acad. Sci. USA 89, 1919–23
    OpenUrlAbstract/FREE Full Text
    1. Klingensmith J.,
    2. Nusse R.,
    3. Perrimon N.
    (1994) The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wg signal. Genes Dev 8, 118–130
    OpenUrlAbstract/FREE Full Text
    1. Lecuit T.,
    2. Brook W. J.,
    3. Ng M.,
    4. Calleja M.,
    5. Sun H.,
    6. Cohen S. M.
    (1996) Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381, 387–393
    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. Ma C.,
    2. Moses K.
    (1995) wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye. Development 121, 2279–2289
    OpenUrlAbstract
    1. Ma C.,
    2. Zhou Y.,
    3. Beachy P. A.,
    4. Moses K.
    (1993) The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell 75, 927–938
    OpenUrlCrossRefPubMedWeb of Science
    1. Masucci J. D.,
    2. Miltenberger R. J.,
    3. Michael H. F.
    (1990) Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal discs is regulated by 3′ cis regulatory elements. Genes Dev 4, 2011–2023
    OpenUrlAbstract/FREE Full Text
    1. Maves L.,
    2. Schubiger G.
    (1995) wingless induces transdetermination in developing Drosophila imaginal discs. Development 121, 1263–1272
    OpenUrlAbstract
    1. Meinhardt H.
    (1983) Cell determination boundaries as organizing regions for secondary embryonic fields. Dev. Biol 96, 375–385
    OpenUrlCrossRefPubMedWeb of Science
    1. Morimura S.,
    2. Maves L.,
    3. Chen Y.,
    4. Hoffmann F. M.
    (1996) decapentaplegic Overexpression Affects Drosophila Wing and Leg Imaginal Disc Development and wingless Expression. Dev. Biol 177, 136–151
    OpenUrlCrossRefPubMedWeb of Science
    1. Nellen D.,
    2. Burke R.,
    3. Struhl G.,
    4. Basler K.
    (1996) Direct and long-range action of a DPP morphogen gradient. Cell 85, 357–368
    OpenUrlCrossRefPubMedWeb of Science
    1. Peifer M.
    (1993) The product of the Drosophila segment polarity gene armadillo is part of a multi-protein complex resembling the vertebrate adherens junction. J. Cell Sci 105, 993–1000
    OpenUrlAbstract/FREE Full Text
    1. Peifer M.,
    2. Orsulic S.,
    3. Sweeton D.,
    4. Wieschaus E.
    (1993) A model system for cell adhesion and signal transduction in Drosophila. Development 1993, 163–176
    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, 1029–43
    OpenUrlAbstract/FREE Full Text
    1. Peifer M.,
    2. Sweeton D.,
    3. Casey M.,
    4. Wieschaus E.
    (1994) wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo. Development 120, 369–380
    OpenUrlAbstract
    1. Penton A.,
    2. Hoffmann M.
    (1996) Decapentaplegic restricts the domain of wingless during limb patterning. Nature 382, 162–165
    OpenUrlCrossRefPubMed
    1. Phillips R. G.,
    2. Roberts I. G. H.,
    3. Ingham P. W.,
    4. Whittle J. R. S.
    (1990) The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. Development 110, 105–114
    OpenUrlAbstract
    1. Raftery L. A.,
    2. Sanicola M.,
    3. Blackman R. K.,
    4. Gelbart W. M.
    (1991) The relationship of decapentaplegic and engrailed expression in Drosophila imaginal discs: do these genes mark the anterior-posterior compartment boundary?. Development 113, 27–33
    OpenUrlAbstract
    1. Riggleman B.,
    2. Schedl P.,
    3. Wieschaus E.
    (1990) Spatial expression of the Drosophila segment polarity gene armadillo is posttranscriptionally regulated by wingless. Cell 63, 549–60
    OpenUrlCrossRefPubMedWeb of Science
    1. Rothbacher U.,
    2. Laurent M. N.,
    3. Blitz I. L.,
    4. Watabe T.,
    5. Marsh J. L.,
    6. Cho K. W. Y.
    (1995) Functional conservation of the Wnt signaling pathway revealed by ectopic expression of Drosophila dishevelled in Xenopus. Dev. Biol 170, 717–21
    OpenUrlCrossRefPubMedWeb of Science
    1. Royet J.,
    2. Finkelstein R.
    (1996) hedgehog, wingless and orthodenticle specify adult head development in Drosophila. Development 122, 1849–58
    OpenUrlAbstract
    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, 557–60
    OpenUrlCrossRefPubMedWeb of Science
    1. Rulifson E. J.,
    2. Blair S. S.
    (1995) Notch regulates wingless expression and is not required for reception of the paracrine wingless signal during wing margin neurogenesis in Drosophila. Development 121, 2813–2824
    OpenUrlAbstract
    1. Schubiger G.
    (1971) Regeneration, duplication and transdetermination in fragments of the leg disc of Drosophilamelanogaster. Dev. Biol 26, 277–295
    OpenUrlCrossRefPubMedWeb of Science
    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, 1167–79
    OpenUrlCrossRefPubMedWeb of Science
    1. Siegfried E.,
    2. Wilder E. L.,
    3. Perrimon N.
    (1994) Components of wingless signalling in Drosophila. Nature 367, 76–80
    OpenUrlCrossRefPubMedWeb of Science
    1. Spencer F. A.,
    2. Hoffmann F. M.,
    3. Gelbart W. M.
    (1982) Decapentaplegic: A gene complex affecting morphogenesis in Drosophila Melanogaster. Cell 28, 451–461
    OpenUrlCrossRefPubMedWeb of Science
    1. Struhl G.
    (1981) A blastoderm fate map of compartments and segments of the Drosophila head. Dev. Biol 84, 386–396
    OpenUrlCrossRefPubMed
    1. Struhl G.,
    2. Basler K.
    (1993) Organizing activity of wingless protein in Drosophila. Cell 72, 527–40
    OpenUrlCrossRefPubMedWeb of Science
    1. Theisen H.,
    2. Haerry E.,
    3. O'Connor M. B.,
    4. Marsh J. L.
    (1996) Developmental territories created by mutual antagonism between WG and DPP. Development 122, 3939–3948
    OpenUrlAbstract
    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. Tickle C.
    (1995) Vertebrate limb development. Curr. Opin. Genet. Dev 5, 478–484
    OpenUrlCrossRefPubMedWeb of Science
    1. Treisman J. E.,
    2. Rubin G. M.
    (1995) wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121, 3519–3527
    OpenUrlAbstract
    1. Wilder E. L.,
    2. Perrimon N.
    (1995) Dual functions of wingless in the Drosophila imaginal disc. Development 121, 477–488
    OpenUrlAbstract
    1. Wolpert L.
    (1969) Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol 25, 1–47
    OpenUrlCrossRefPubMedWeb of Science
    1. Xu T.,
    2. Rubin G. M.
    (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223–37
    OpenUrlAbstract
    1. Zecca M.,
    2. Basler K.,
    3. Struhl G.
    (1995) Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121, 2265–2278
    OpenUrlAbstract
Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

 Download PDF

Email

Thank you for your interest in spreading the word on Development.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Shaggy and dishevelled exert opposite effects on Wingless and Decapentaplegic expression and on positional identity in imaginal discs
(Your Name) has sent you a message from Development
(Your Name) thought you would like to see the Development web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
JOURNAL ARTICLES
Shaggy and dishevelled exert opposite effects on Wingless and Decapentaplegic expression and on positional identity in imaginal discs
T.R. Heslip, H. Theisen, H. Walker, J.L. Marsh
Development 1997 124: 1069-1078;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
JOURNAL ARTICLES
Shaggy and dishevelled exert opposite effects on Wingless and Decapentaplegic expression and on positional identity in imaginal discs
T.R. Heslip, H. Theisen, H. Walker, J.L. Marsh
Development 1997 124: 1069-1078;

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • even skipped is required to produce a trans-acting signal for larval neuroblast proliferation that can be mimicked by ecdysone
  • Groucho augments the repression of multiple Even skipped target genes in establishing parasegment boundaries
  • Axial skeletal patterning in mice lacking all paralogous group 8 Hox genes
Show more JOURNAL ARTICLES

Similar articles

Other journals from The Company of Biologists

Journal of Cell Science

Journal of Experimental Biology

Disease Models & Mechanisms

Biology Open

Advertisement

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.


Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.


Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.


Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

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

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.


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. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights

Articles

  • Accepted manuscripts
  • Issue in progress
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Sign up for alerts

About us

  • About Development
  • About the Node
  • Editors and board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists

For authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Biology Open transfer

Journal info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact Development
  • Subscriptions
  • Advertising
  • Feedback

 Twitter   YouTube   LinkedIn

© 2021   The Company of Biologists Ltd   Registered Charity 277992