Advertisement
JOURNAL ARTICLES
Post-transcriptional regulation of gurken by encore is required for axis determination in Drosophila
N.C. Hawkins, C. Van Buskirk, U. Grossniklaus, T. Schupbach
Development 1997 124: 4801-4810;

Summary

Establishment of anterior-posterior and dorsal-ventral polarity within the Drosophila egg chamber requires signaling between the germline and the somatic cells of the ovary. The gene gurken (grk) encodes a TGFalpha-like protein that is localized within the developing oocyte and is thought to locally activate torpedo/Egfr (top/Egfr), the Drosophila homolog of the EGF receptor, which is expressed throughout the follicular epithelium surrounding the oocyte. grk-Egfr signaling is required early in oogenesis for specification of posterior follicle cell fate and later in oogenesis for dorsal follicle cell fate determination, thus establishing the axes of the egg shell and embryo. Previous studies have shown that these patterning processes are highly sensitive to changes in the levels and localization of grk mRNA. Here we show that post-transcriptional regulation of Grk protein levels is required for correct pattern formation. encore (enc), a gene that functions in the regulation of germline mitosis and maintenance of oocyte identity, is also required for the accumulation of Grk protein during oogenesis. We present evidence that enc regulates Grk post-transcriptionally to ensure adequate levels of signaling for establishment of the anterior-posterior and dorsal-ventral axes.

REFERENCES

    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 Drosophilamelanogaster. Genes Dev 4, 190–203
    OpenUrlAbstract/FREE Full Text
    1. Christerson L. B.,
    2. McKearin D. M.
    (1994) orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis. Genes Dev 8, 614–628
    OpenUrlAbstract/FREE Full Text
    1. Gonzales-Reyes A.,
    2. Elliott H.,
    3. St. Johnston R. D.
    (1995) Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375, 654–658
    OpenUrlCrossRefPubMedWeb of Science
    1. Grossniklaus U.,
    2. Bellen H. J.,
    3. Wilson C.,
    4. Gehring W. J.
    (1989) P-element mediated enhancer trap detection applied to the study of oogenesis in Drosophila. Development 107, 189–200
    OpenUrlAbstract
    1. Haenlin M.,
    2. McDonald W. F.,
    3. Cibert C.,
    4. Mohier E.
    (1995) The angle of the dorsoventral axis with respect to the anteroposterior axis in the Drosophila embryo is controlled by the distribution of gurken mRNA in the oocyte. Mech. Dev 49, 97–106
    OpenUrlCrossRefPubMed
    1. Hake L. E.,
    2. Richter J. D.
    (1994) CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell 79, 617–627
    OpenUrlCrossRefPubMedWeb of Science
    1. Hawkins N. C.,
    2. Thorpe J.,
    3. Schupbach T.
    (1996) encore, a gene required for the regulation of germ line mitosis and oocyte differentiation during Drosophila oogenesis. Development 122, 281–290
    OpenUrlAbstract
    1. Kammermeyer K. L.,
    2. Wadsworth S. C.
    (1987) Expression of the Drosophila epidermal growth factor homolog in mitotic cell populations. Development 100, 201–210
    OpenUrlAbstract/FREE Full Text
    1. Kim-Ha J.,
    2. Kerr K.,
    3. Macdonald P.
    (1995) Translational regulation of oskar mRNA by Bruno, an ovarian RNA binding protein, is essential. Cell 81, 403–412
    OpenUrlCrossRefPubMedWeb of Science
    1. Kulkarni S. J.,
    2. Newby L. M.,
    3. Jackson F. R.
    (1994) Drosophila GABAergic systems. II. Mutational analysis of chromosomal segment 64AB, a region containing the glutamic acid decarboxylase gene. Mol. Gen. Genet 243, 555–564
    OpenUrlCrossRefPubMedWeb of Science
    1. Lantz V.,
    2. Chang J. S.,
    3. Horabin J. I.,
    4. Bopp D.,
    5. Schedl P.
    (1994) The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev 8, 598–613
    OpenUrlAbstract/FREE Full Text
    1. Mach J.,
    2. Lehmann R.
    (1997) An Egalitarian-BicaudalD complex is essential for oocyte specification and axis determination in Drosophila. Genes Dev 11, 423–435
    OpenUrlAbstract/FREE Full Text
    1. McKearin D. M.,
    2. Spradling A. C.
    (1990) bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev 4, 2242–2251
    OpenUrlAbstract/FREE Full Text
    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. Neuman-Silberberg F. S.,
    2. Schupbach T.
    (1994) Dorsoventral axis formation in Drosophila depends on the correct dosage of the gene gurken. Development 120, 2457–2463
    OpenUrlAbstract/FREE Full Text
    1. Neuman-Silberberg F. S.,
    2. Schupbach T.
    (1996) The Drosophila TGF-like protein Gurken: expression and cellular localization during Drosophila oogenesis. Mech. Dev 59, 105–113
    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, and encodes the Drosophila EGF receptor homolog. Cell 56, 1985–1092
    OpenUrl
    1. Ray R. P.,
    2. Arora K.,
    3. Nusslein-Volhard C.,
    4. Gelbart W.
    (1991) The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development 113, 35–54
    OpenUrlAbstract
    1. Roth S.,
    2. Stein D.,
    3. Nusslein-Volhard C.
    (1989) A gradient of nuclear localization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo. Cell 59, 1189–1202
    OpenUrlCrossRefPubMedWeb of Science
    1. Roth S.,
    2. Schupbach T.
    (1994) The relationship between ovarian and embryonic dorsoventral patterns of the Drosophila embryo. Development 120, 2245–2257
    OpenUrlAbstract
    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. 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, 1903–1104
    OpenUrl
    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. Schupbach T.,
    2. Wieschaus E.
    (1991) Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129, 1119–1136
    OpenUrlAbstract/FREE Full Text
    1. Serano T. L.,
    2. Karlin-McGinness M.,
    3. Cohen R. S.
    (1995) The role of fs(1)K10 in the localization of the mRNA of the TGFhomolog gurken within the Drosophila oocyte. Mech. Dev 51, 183–192
    OpenUrlCrossRefPubMed
    1. St Johnston D.,
    2. Gelbart W. M.
    (1987) Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J 6, 2785–2791
    OpenUrlPubMedWeb of Science
    1. Swan A.,
    2. Suter B.
    (1996) Role of Bicaudal-D in patterning the Drosophila egg chamber in mid-oogenesis. Development 122, 3577–3586
    OpenUrlAbstract
    1. Tautz D.,
    2. Pfeifle C.
    (1989) A non radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals a translational control of the segmentation gene hunchback. Chromosoma 98, 81–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Thisse B.,
    2. Stoetzel C.,
    3. Gorostiza-Thisse C.,
    4. Perrin-Schmitt F.
    (1988) Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J 7, 2175–2183
    OpenUrlPubMedWeb of Science
    1. Wilson J. E.,
    2. Connell J. E.,
    3. Macdonald P. M.
    (1996) aubergine enhances oskar translation in the Drosophila ovary. Development 122, 1631–1639
    OpenUrlAbstract
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Post-transcriptional regulation of gurken by encore is required for axis determination in Drosophila
N.C. Hawkins, C. Van Buskirk, U. Grossniklaus, T. Schupbach
Development 1997 124: 4801-4810;
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