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
The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis
F. Agnes, M. Suzanne, S. Noselli
Development 1999 126: 5453-5462;
F. Agnes
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
M. Suzanne
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
S. Noselli
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Info & metrics
  • PDF
Loading

Summary

In Drosophila, the Jun-N-terminal Kinase-(JNK) signaling pathway is required for epithelial cell shape changes during dorsal closure of the embryo. In the absence of JNK pathway activity, as in the DJNKK/hemipterous (hep) mutant, the dorsolateral ectodermal cells fail both to elongate and move toward the dorsal midline, leading to dorsally open embryos. We show here that hep and the JNK pathway are required later in development, for correct morphogenesis of other epithelia, the imaginal discs. During metamorphosis, the imaginal discs undergo profound morphological changes, giving rise to the adult head and thoracic structures, including the cuticle and appendages. hep mutant pupae and pharate adults show severe defects in discs morphogenesis, especially in the fusion of the two lateral wing discs. We show that these defects are accompanied by a loss of expression of puckered (puc), a JNK phosphatase-encoding gene, in a subset of peripodial cells that ultimately delineates the margins of fusing discs. In further support of a role of puc in discs morphogenesis, pupal and adult hep phenotypes are suppressed by reducing puc function, indicative of a negative role of puc in disc morphogenesis. Furthermore, we show that the small GTPase Dcdc42, but not Drac1, is an activator of puc expression in a hep-dependent manner in imaginal discs. Altogether, these results demonstrate a new role for the JNK pathway in epithelial morphogenesis, and provide genetic evidence for a role of the peripodial membrane in disc morphogenesis. We discuss a general model whereby the JNK pathway regulates morphogenesis of epithelia with differentiated edges.

Reference

    1. Agnes F.,
    2. Noselli S.
    (1999) Dorsal closure in Drosophila. A genetic model for wound healing?. C. R. Acad. Sci. III 322, 5–13
    OpenUrlPubMed
    1. Andres A.,
    2. Fletcher J. C.,
    3. Karim F. D.,
    4. Thummel C. S.
    (1993) Molecular analysis of the initiation of insect metamorphosis: a comparative study of Drosophila ecdysteroid-regulated transcritption. Dev. Biol 160, 388–404
    OpenUrlCrossRefPubMedWeb of Science
    1. Bainbridge S. P.,
    2. Bownes M.
    (1981) Staging the metamorphosis of Drosophila melanogaster. J. Embryol. Exp. Morphol 66, 57–80
    OpenUrlPubMedWeb of Science
    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. Capdevila J.,
    2. Guerrero I.
    (1994) Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J 13, 4459–4468
    OpenUrlPubMedWeb of Science
    1. Chen Y.,
    2. Riese M. J.,
    3. Killinger M. A.,
    4. Hoffmann F. M.
    (1998) A genetic screen for modifiers of Drosophila decapentaplegic signaling identifies mutations in punt, Mothers against dpp and the BMP-7 homologue, 60A. Development 125, 1759–1768
    OpenUrlAbstract
    1. DiBello P. R.,
    2. Withers D. A.,
    3. Bayer C. A.,
    4. Fristrom J. W.,
    5. Guild G. M.
    (1991) The Drosophila Broad-Complex encodes a family of related proteins containing zinc fingers. Genetics 129, 385–397
    OpenUrlAbstract/FREE Full Text
    1. Duffy J. B.,
    2. Harrison D. A.,
    3. Perrimon N.
    (1998) Identifying loci required for follicular patterning using directed mosaics. Development 125, 2263–2271
    OpenUrlAbstract
    1. Eaton S.,
    2. Auvinen P.,
    3. Luo L.,
    4. Jan Y. N.,
    5. Simons K.
    (1995) CDC42 and Rac1 control different actin-dependent processes in the Drosophila wing disc epithelium. J. Cell Biol 131, 151–164
    OpenUrlAbstract/FREE Full Text
    1. Fristrom J.,
    2. Fristrom D.,
    3. Kekete E.,
    4. Kuniyuki A.
    (1977) The mechanisms of evagination of imaginal discs of Drosophila melanogaster. Am. Zool 17, 671–684
    OpenUrl
    1. Gibson M. C.,
    2. Schubiger G.
    (1999) Hedgehog is required for activation of engrailed during regeneration of fragmented drosophila imaginal discs. Development 126, 1591–1599
    OpenUrlAbstract
    1. Glise B.,
    2. Bourbon H.,
    3. Noselli S.
    (1995) hemipterous encodes a novel Drosophila Map kinase kinase, required for epithelial cell sheet movement. Cell 83, 451–461
    OpenUrlCrossRefPubMedWeb of Science
    1. Glise B.,
    2. Noselli S.
    (1997) Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev 11, 1738–1747
    OpenUrlAbstract/FREE Full Text
    1. Goberdhan D. C.,
    2. Wilson C.
    (1998) JNK, cytoskeletal regulator and stress response kinase? A Drosophila perspective. BioEssays 20, 1009–1019
    OpenUrlCrossRefPubMedWeb of Science
    1. Han S. J.,
    2. Choi K. Y.,
    3. Brey P. T.,
    4. Lee W. J.
    (1998) Molecular cloning and characterization of a Drosophila p38 mitogen-activated protein kinase. J. Biol. Chem 273, 369–374
    OpenUrlAbstract/FREE Full Text
    1. Han Z. S.,
    2. Enslen H.,
    3. Hu X.,
    4. Meng X.,
    5. Wu I. H.,
    6. Barrett T.,
    7. Davis R. J.,
    8. Ip Y. T.
    (1998) A conserved p38 mitogen-activated protein kinase pathway regulates Drosophila immunity gene expression. Mol. Cell. Biol 18, 3527–3539
    OpenUrlAbstract/FREE Full Text
    1. Harden N.,
    2. Lee J.,
    3. Loh H. Y.,
    4. Ong Y. M.,
    5. Tan I.,
    6. Leung T.,
    7. Manser E.,
    8. Lim L.
    (1996) A Drosophila homolog of the Rac-and Cdc42-activated serine/threonine kinase PAK is a potential focal adhesion and focal complex protein that colocalizes with dynamic actin structures. Mol. Cell Biol 16, 1896–908
    OpenUrlAbstract/FREE Full Text
    1. Harden N.,
    2. Ricos M.,
    3. Ong Y. M.,
    4. Chia W.,
    5. Lim L.
    (1999) Participation of small GTPases in dorsal closure of the Drosophila embryo: distinct roles for Rho subfamily proteins in epithelial morphogenesis. J Cell Sci 112, 273–284
    OpenUrlAbstract/FREE Full Text
    1. Hou X. S.,
    2. Goldstein E. S.,
    3. Perrimon N.
    (1997) Drosophila Jun relays the Jun amino-terminal kinase signal transduction pathway to the Decapentaplegic signal transduction pathway in regulating epithelial cell sheet movement. Genes Dev 11, 1728–1737
    OpenUrlAbstract/FREE Full Text
    1. Hudson J. B.,
    2. Podos S. D.,
    3. Keith K.,
    4. Simpson S. L.,
    5. Ferguson E. L.
    (1998) The Drosophila Medea gene is required downstream of dpp and encodes a functional homolog of human Smad4. Development 125, 1407–1420
    OpenUrlAbstract
    1. Ip Y. T.,
    2. Davis R. J.
    (1998) Signal transduction by the c-Jun N-terminal kinase (JNK)—from inflammation to development. Curr. Opin. Cell Biol 10, 205–219
    OpenUrlCrossRefPubMedWeb of Science
    1. Kockel L.,
    2. Zeitlinger J.,
    3. Staszewski L. M.,
    4. Mlodzik M.,
    5. Bohmann D.
    (1997) Jun in Drosophila development: redundant and nonredundant functions and regulation by two MAPK signal transduction pathways. Genes Dev 11, 1748–1758
    OpenUrlAbstract/FREE Full Text
    1. Liu H.,
    2. Su Y. C.,
    3. Becker E.,
    4. Treisman J.,
    5. Skolnik E. Y.
    (1999) A Drosophila TNF-receptor-associated factor (TRAF) binds the ste20 kinase Misshapen and activates Jun kinase. Curr. Biol 9, 101–104
    OpenUrlCrossRefPubMedWeb of Science
    1. Lu Y.,
    2. Settleman J.
    (1999) The Drosophila pkn protein kinase is a Rho/Rac effector target required for dorsal closure during embryogenesis. Genes Dev 13, 1168–1180
    OpenUrlAbstract/FREE Full Text
    1. Luo L.,
    2. Liao Y. J.,
    3. Jan L. Y.,
    4. Jan Y. N.
    (1994) Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 8, 1787–1802
    OpenUrlAbstract/FREE Full Text
    1. Martin P.
    (1997) Wound healing—aiming for perfect skin regeneration. Science 276, 75–81
    OpenUrlAbstract/FREE Full Text
    1. Martin-Blanco E.,
    2. Gampel A.,
    3. Ring J.,
    4. Virdee K.,
    5. Kirov N.,
    6. Tolkovsky A. M.,
    7. Martinez-Arias A.
    (1998) puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev 12, 557–570
    OpenUrlAbstract/FREE Full Text
    1. Milner M. J.
    (1977) The eversion and differentiation of Drosophila melanogaster leg and wing imaginal discs cultured in vitro with an optimal concentration of beta-ecdysone. J. Embryol. Exp. Morphol 37, 105–117
    OpenUrlPubMedWeb 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. Noselli S.
    (1998) JNK signaling and morphogenesis in Drosophila. Trends Genet 14, 33–38
    OpenUrlCrossRefPubMedWeb of Science
    1. Noselli S.,
    2. Agnes F.
    (1999) Roles of the JNK signaling pathway in Drosophila morphogenesis. Curr. Opin. Genet. Dev 9, 466–472
    OpenUrlCrossRefPubMedWeb of Science
    1. Ramirez-Weber F. A.,
    2. Kornberg T. B.
    (1999) Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 97, 599–607
    OpenUrlCrossRefPubMedWeb of Science
    1. Ricos M. G.,
    2. Harden N.,
    3. Sem K. P.,
    4. Lim L.,
    5. Chia W.
    (1999) Dcdc42 acts in TGF-signaling during Drosophila morphogenesis: distinct roles for the Drac1/JNK and Dcdc42/TGF- cascades in cytoskeletal regulation. J. Cell Sci 112, 1225–1235
    OpenUrlAbstract/FREE Full Text
    1. Riesgo-Escovar J. R.,
    2. Hafen E.
    (1997) Common and distinct roles of DFos and DJun during Drosophila development. Science 278, 669–672
    OpenUrlAbstract/FREE Full Text
    1. Riesgo-Escovar J. R.,
    2. Hafen E.
    (1997) Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP-1 transcription factor DJun during dorsal closure. Genes Dev 11, 1717–1727
    OpenUrlAbstract/FREE Full Text
    1. Riesgo-Escovar J. R.,
    2. Jenni M.,
    3. Fritz A.,
    4. Hafen E.
    (1996) The Drosophila Jun-N-terminal kinase is required for cell morphogenesis but not for DJun-dependent cell fate specification in the eye. Genes Dev 10, 2759–2768
    OpenUrlAbstract/FREE Full Text
    1. Simin K.,
    2. Bates E. A.,
    3. Horner M. A.,
    4. Letsou A.
    (1998) Genetic analysis of punt, a type II Dpp receptor that functions throughout the Drosophila melanogaster life cycle. Genetics 148, 801–813
    OpenUrlAbstract/FREE Full Text
    1. Sluss H. K.,
    2. Davis R. J.
    (1997) Embryonic morphogenesis signaling pathway mediated by JNK targets the transcription factor JUN and the TGF-beta homologue decapentaplegic. J. Cell Biochem 67, 1–12
    OpenUrlCrossRefPubMedWeb of Science
    1. Sluss H. K.,
    2. Han Z.,
    3. Barrett T.,
    4. Davis R. J.,
    5. Ip Y. T.
    (1996) A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev 10, 2745–2758
    OpenUrlAbstract/FREE Full Text
    1. Su Y. C.,
    2. Treisman J. E.,
    3. Skolnik E. Y.
    (1998) The Drosophila Ste20-related kinase misshapen is required for embryonic dorsal closure and acts through a JNK MAPK module on an evolutionarily conserved signaling pathway. Genes Dev 12, 2371–2380
    OpenUrlAbstract/FREE Full Text
    1. Suzanne M.,
    2. Irie K.,
    3. Glise B.,
    4. Agnes F.,
    5. Mori E.,
    6. Matsumoto K.,
    7. Noselli S.
    (1999) The drosophila p38 MAPK pathway is required during oogenesis for egg asymmetric development. Genes Dev 13, 1464–1474
    OpenUrlAbstract/FREE Full Text
    1. Takahashi K.,
    2. Matsuo T.,
    3. Katsube T.,
    4. Ueda R.,
    5. Yamamoto D.
    (1998) Direct binding between two PDZ domain proteins Canoe and ZO-1 and their roles in regulation of the jun N-terminal kinase pathway in Drosophila morphogenesis. Mech. Dev 78, 97–111
    OpenUrlCrossRefPubMedWeb of Science
    1. Williams-Masson E. M.,
    2. Malik A. N.,
    3. Hardin J.
    (1997) An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis. Development 124, 2889–2901
    OpenUrlAbstract
    1. Young P. E.,
    2. Richman A. M.,
    3. Ketchum A. S.,
    4. Kiehart D. P.
    (1993) Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev 7, 29–41
    OpenUrlAbstract/FREE Full Text
    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
    1. Zeitlinger J.,
    2. Kockel L.,
    3. Peverali F. A.,
    4. Jackson D. B.,
    5. Mlodzik M.,
    6. Bohmann D.
    (1997) Defective dorsal closure and loss of epidermal decapentaplegic expression in Drosophila fos mutants. EMBO J 16, 7393–7401
    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.
The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis
(Your Name) has sent you a message from Development
(Your Name) thought you would like to see the Development web site.
Share
JOURNAL ARTICLES
The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis
F. Agnes, M. Suzanne, S. Noselli
Development 1999 126: 5453-5462;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
JOURNAL ARTICLES
The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis
F. Agnes, M. Suzanne, S. Noselli
Development 1999 126: 5453-5462;

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

  • A BAC transgenic analysis of the Mrf4/Myf5 locus reveals interdigitated elements that control activation and maintenance of gene expression during muscle development
  • Visualization and functional characterization of the developing murine cardiac conduction system
  • Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo
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

The people behind the papers – George Britton and Aryeh Warmflash

George and Aryeh

First author George Britton and his supervisor Aryeh Warmflash discuss their new Development paper in which they apply advanced in vitro culturing techniques to investigate embryonic ectoderm patterning.


Travelling Fellowship – New imaging approach unveils a bigger picture

Highlights from Travelling Fellowship trips

Find out how Pamela Imperadore’s Travelling Fellowship grant from The Company of Biologists took her to Germany, where she used new imaging techniques to investigate the cellular machinery underlying octopus arm regeneration. Don’t miss the next application deadline for 2020 travel, coming up on 29 November. Where will your research take you?


Primer – Principles and applications of optogenetics in developmental biology

Schematic demonstrating the approaches to controlling protein activity using optogenetics.

Protein function can be controlled by light using optogenetic techniques. In their new Primer, Stefano De Renzis and his colleagues in Heidelberg provide an overview of the most commonly used optogenetic tools and their application in developmental biology.


preLights – Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Sundar Naganathan

preLighter Sundar Naganathan explains his selected preprint by Vikas Trivedi, Benjamin Steventon and their co-workers on pescoids, a new in vitro model system to study early zebrafish embryogenesis.


Spotlight – Can laboratory model systems instruct human limb regeneration?

An extract from a schematic demonstrating the possible pipeline for how discovery in lab model systems can influence applications for regenerative therapies.

One of the most challenging objectives of tissue regeneration research is regrowth of a lost or amputated limb. Here, Ben Cox, Maximina Yun and Kenneth Poss outline the research avenues yet to be explored to move closer to this capstone achievement.


Articles of interest in our sister journals

Tox4 modulates cell fate reprogramming

Lotte Vanheer, Juan Song, Natalie De Geest, Adrian Janiszewski, Irene Talon, Caterina Provenzano, Taeho Oh, Joel Chappell, Vincent Pasque
Journal of Cell Science

Drosophila melanogaster: a simple system for understanding complexity

Stephanie E. Mohr, Norbert Perrimon
Disease Models & Mechanisms

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

© 2019   The Company of Biologists Ltd   Registered Charity 277992