Advertisement
JOURNAL ARTICLES
Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo
A.M. Queenan, A. Ghabrial, T. Schupbach
Development 1997 124: 3871-3880;

Summary

The Drosophila gene torpedo/Egfr (top/Egfr) encodes a homolog of the vertebrate Epidermal Growth Factor receptor. This receptor is required several times during the life cycle of the fly for the transmisson of developmental cues. During oogenesis, Top/Egfr activation is required for the establishment of the dorsal/ventral axis of the egg and the embryo. To examine how ectopic Top/Egfr activation affects cell fate determination, we constructed an activated version of the protein. Expression of this activated form (lambda top) in the follicle cells of the ovary induces dorsal cell fates in both the follicular epithelium and the embryo. Different levels of expression resulted in different dorsal follicle cell fates. These dorsal cell fates were expanded in the anterior, but not the posterior, of the egg, even in cases where all the follicle cells covering the oocyte expressed lambda top. The expression of genes known to respond to top/Egfr activation, argos (aos), kekkon1 (kek 1) and rhomboid (rho), was also expanded in the presence of the lambda top construct. When lambda top was expressed in all the follicle cells covering the oocyte, kek 1 and argos expression was induced in follicle cells all along the anterior/posterior axis of the egg chamber. In contrast, rho RNA expression was only activated in the anterior of the egg chamber. These data indicate that the response to Top/Egfr signaling is regulated by an anterior/posterior prepattern in the follicle cells. Expression of lambda top in the entire follicular epithelium resulted in an embryo dorsalized along the entire anterior/posterior axis. Expression of lambda top in anterior or posterior subpopulations of follicle cells resulted in regionally autonomous dorsalization of the embryos. This result indicates that subpopulations of follicle cells along the anterior/posterior axis can respond to Top/Egfr activation independently of one another.

REFERENCES

    1. Baker N. E.,
    2. Rubin G. M.
    (1992) Ellipse mutations in the Drosophila homologue of the EGF receptor affect pattern formation, cell division, and cell death in eye imaginal discs. Dev. Biol 150, 381–396
    OpenUrlCrossRefPubMedWeb of Science
    1. Basler K.,
    2. Christen B.,
    3. Hafen E.
    (1991) Ligand-independent activation of the sevenless receptor tyrosine kinase changes the fate of cells in the developing Drosophila eye. Cell 64, 1069–1081
    OpenUrlCrossRefPubMedWeb of Science
    1. Bier E.,
    2. Jan L. Y.,
    3. Jan Y. N.
    (1990) rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev 4, 190–203
    OpenUrlAbstract/FREE Full Text
    1. Brand A.,
    2. Perrimon N.
    (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415
    OpenUrlAbstract
    1. Brand A. H.,
    2. Perrimon N.
    (1994) Raf acts downstream of the EGFreceptor to determine dorsoventral polarity during Drosophila oogenesis. Genes Dev 8, 629–639
    OpenUrlAbstract/FREE Full Text
    1. Brunner D.,
    2. Oellers N.,
    3. Szabad J.,
    4. Biggs III W. H.,
    5. Zipursky S. L.,
    6. Hafen E.
    (1994) A gain-of-function mutation in Drosophila MAP kinase activates multiple receptor tyrosine kinase signaling pathways. Cell 76, 875–888
    OpenUrlCrossRefPubMedWeb of Science
    1. Clifford R. J.,
    2. Schupbach T.
    (1989) Coordinately and differentially mutable activities of torpedo, the Drosophila melanogaster homolog of the vertebrate EGF receptor gene. Genetics 123, 771–787
    OpenUrlAbstract/FREE Full Text
    1. Diaz-Benjumea F. J.,
    2. Garcia-Bellido A.
    (1990) Behaviour of cells mutant for an EGF receptor homologue of Drosophila in genetic mosaics. Proc. R. Soc. Lond. B, 242, 36–44
    OpenUrlPubMed
    1. Duffy J. B.,
    2. Perrimon N.
    (1996) Recent advances in understanding signal transduction pathways in worms and flies. Current Opinion in Cell Biology 8, 231–238
    OpenUrlCrossRefPubMed
    1. Fantl W. J.,
    2. Johnson D. E.,
    3. Williams L. T.
    (1993) Signalling by receptor tyrosine kinases. Annu. Rev. Biochem 62, 453–481
    OpenUrlCrossRefPubMedWeb of Science
    1. Freeman M.
    (1997) Cell determination strategies in the Drosophila eye. Development 124, 261–270
    OpenUrlAbstract
    1. Freeman M.,
    2. Klämbt C.,
    3. Goodman C. S.,
    4. Rubin G. M.
    (1992) The argos gene encodes a diffusible factor that regulates cell fate decisions in the Drosophila Eye. Cell 69, 963–975
    OpenUrlCrossRefPubMedWeb of Science
    1. Golembo M.,
    2. Schweitzer R.,
    3. Freeman M.,
    4. Shilo B.-Z.
    (1996) argos transcription is induced by the Drosophila EGF receptor pathway to form an inhibitory feedback loop. Development 122, 223–230
    OpenUrlAbstract
    1. Gonzalez-Reyes A.,
    2. Elliott H.,
    3. St Johnston D.
    (1995) Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375, 654–658
    OpenUrlCrossRefPubMedWeb of Science
    1. Harrison D. A.,
    2. Binari R.,
    3. Nahreini T. S.,
    4. Gilman M.,
    5. Perrimon N.
    (1995) Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. EMBO J 14, 2857–2865
    OpenUrlPubMedWeb of Science
    1. Hsu T.,
    2. Bagni C.,
    3. Sutherland J. D.,
    4. Kafatos F. C.
    (1996) The transcription factor CF2 is a mediator of EGF-R-activated dorsoventral patterning in Drosophila oogenesis. Genes Dev 10, 1411–1421
    OpenUrlAbstract/FREE Full Text
    1. Hunter T.
    (1997) Oncoprotein Networks. Cell 88, 333–346
    OpenUrlCrossRefPubMedWeb of Science
    1. Kammermeyer K. L.,
    2. Wadsworth S. C.
    (1987) Expression of Drosophila epidermal growth factor receptor homologue in mitotic cell populations. Development 100, 201–210
    OpenUrlAbstract/FREE Full Text
    1. Lee T.,
    2. Hacohen N.,
    3. Krasnow M.,
    4. Montell D.
    (1996) Regulated breathless receptor tyrosine kinase activity required to pattern cell migration and branching in the Drosophila tracheal system. Genes Dev 10, 2912–2921
    OpenUrlAbstract/FREE Full Text
    1. Livneh E.,
    2. Glazer L.,
    3. Segal D.,
    4. Schlessinger J.,
    5. Shilo B.-Z.
    (1985) The Drosophila EGF receptor gene homolog: conservation of both hormone binding and kinase domains. Cell 40, 599–607
    OpenUrlCrossRefPubMedWeb of Science
    1. Morimoto A. M.,
    2. Jordan K. C.,
    3. Tietze K.,
    4. Britton J. S.,
    5. O'Neill E. M.,
    6. Ruohola-Baker H.
    (1996) Pointed, an ETS domain transcription factor, negatively regulates the EGF receptor pathway in Drosophila oogensis. Development 122, 3745–3754
    OpenUrlAbstract
    1. Morisato D.,
    2. Anderson K.
    (1995) Signaling pathways that establish the dorsal-ventral pattern of the Drosophila embryo. Annu. Rev. Genetics 29, 371–399
    OpenUrlCrossRefPubMedWeb of Science
    1. Musacchio M.,
    2. Perrimon N.
    (1996) The Drosophila kekkon genes: novel members of both the leucine-rich repeat and immunoglobulin superfamilies expressed in the CNS. Dev. Biol 178, 63–76
    OpenUrlCrossRefPubMedWeb of Science
    1. Neuman-Silberberg F. S.,
    2. Schupbach T.
    (1993) The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGF-like protein. Cell 75, 165–174
    OpenUrlCrossRefPubMedWeb of Science
    1. Price J. V.,
    2. Clifford R. J.,
    3. Schupbach T.
    (1989) The maternal ventralizing locus torpedo is allelic to faint little ball, an embryonic lethal, encodes the Drosophila EGF receptor homolog. Cell 56, 1085–1092
    OpenUrlCrossRefPubMed
    1. Ray R. P.,
    2. Schupbach T.
    (1996) Intercellular signaling and the polarization of body axes during Drosophila oogenesis. Genes Dev 10, 1711–1723
    OpenUrlFREE Full Text
    1. Raz E.,
    2. Schejter E. D.,
    3. Shilo B.-Z.
    (1991) Interallelic complementation among DER/flb alleles: implications for the mechanism of signal transduction by receptor tyrosine kinases. Genetics 129, 191–201
    OpenUrlAbstract/FREE Full Text
    1. Roth S.,
    2. Neuman-Silberberg F. S.,
    3. Barcelo G.,
    4. Schupbach T.
    (1995) cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 81, 967–978
    OpenUrlCrossRefPubMedWeb of Science
    1. Roth S.,
    2. Stein D.,
    3. Nusslein-Volhard C.
    (1989) A gradient of nuclearlocalization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo. Cell 59, 1189–1202
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruohola-Baker H.,
    2. Grell E.,
    3. Chou T.-B.,
    4. Baker D.,
    5. Jan L. Y.,
    6. Jan Y. N.
    (1993) Spatially localized rhomboid is required for establishment of the dorsal-ventral axis in Drosophila oogenesis. Cell 73, 953–965
    OpenUrlCrossRefPubMedWeb of Science
    1. Schejter E. D.,
    2. Shilo B.-Z.
    (1989) The Drosophila EGF receptor homolog (DER) gene is allelic to faint little ball, a locus essential for embryonic development. Cell 56, 1093–1104
    OpenUrlCrossRefPubMedWeb of Science
    1. Schlessinger J.,
    2. Ullrich A.
    (1992) Growth factor signaling by receptor tyrosine kinases. Neuron 9, 383–391
    OpenUrlCrossRefPubMedWeb of Science
    1. Schupbach T.
    (1987) Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster. Cell 49, 699–707
    OpenUrlCrossRefPubMedWeb of Science
    1. Schweitzer R.,
    2. Shilo B.-Z.
    (1997) A thousand and one roles for the Drosophila EGF receptor. Trends in Genetics 13, 191–196
    OpenUrlCrossRefPubMedWeb of Science
    1. Tautz D.,
    2. Pfeifle 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. Twombly V.,
    2. Blackman R. K.,
    3. Jin H.,
    4. Graff J. M.,
    5. Padgett R. W.,
    6. Gelbart W. M.
    (1996) The TGF-signaling pathway is essential for Drosophila oogenesis. Development 122, 1555–1565
    OpenUrlAbstract
    1. Wadsworth S. C.,
    2. Vincent III W. S.,
    3. Bilodeau-Wentworth D.
    (1985) A Drosophila genomic sequence with homology to the human epidermal growth factor receptor. Nature 314, 178–180
    OpenUrlCrossRefPubMed
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo
A.M. Queenan, A. Ghabrial, T. Schupbach
Development 1997 124: 3871-3880;
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

An interview with Swathi Arur

Swathi Arur joined the team at Development as an Academic Editor in 2020. Her lab uses multidisciplinary approaches to understand female germline development and fertility. We met with her over Zoom to hear more about her life, her career and her love for C. elegans.

Jim Wells and Hanna Mikkola join our team of Editors

We are pleased to welcome James (Jim) Wells and Hanna Mikkola to our team of Editors. Jim joins us a new Academic Editor, taking over from Gordan Keller, and Hanna joins our team of Associate Editors. Find out more about their research interests and areas of expertise.

New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.

Read & Publish participation continues to grow

“I’d heard of Read & Publish deals and knew that many universities, including mine, had signed up to them but I had not previously understood the benefits that these deals bring to authors who work at those universities.”

Professor Sally Lowell (University of Edinburgh) shares her experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – 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. Here, Brandon Carpenter talks about how inherited histone methylation defines the germline versus soma decision in C. elegans. 

Sign up to join our next session:

10 March
Time: TBC
Chaired by: Thomas Lecuit