Advertisement
JOURNAL ARTICLES
The Notch signalling pathway is required for Enhancer of split bHLH protein expression during neurogenesis in the Drosophila embryo
B. Jennings, A. Preiss, C. Delidakis, S. Bray
Development 1994 120: 3537-3548;

Summary

The Enhancer of split locus is required during many cell-fate decisions in Drosophila, including the segregation of neural precursors in the embryo. We have generated monoclonal antibodies that recognise some of the basic helix-loop-helix proteins encoded by the Enhancer of split locus and have used them to examine expression of Enhancer of split proteins during neurogenesis. The proteins are expressed in a dynamic pattern in the ventral neurogenic region and are confined to those ectodermal cells that surround a neuroblast in the process of delaminating. There is no staining in the neuroblasts themselves. We have also examined the relationship between Enhancer of split protein accumulation and the Notch signalling pathway. Protein expression is abolished in a number of neurogenic mutant backgrounds, including Notch, but is increased as a result of expressing a constitutively active Notch product. We conclude that Notch signalling activity is directly responsible for the accumulation of basic helix-loop-helix proteins encoded by the Enhancer of split locus.

REFERENCES

    1. Alonso M.,
    2. Cabrera C. V.
    (1988) The achaete-scute gene complex of Drosophilamelanogaster comprises four homologous genes. EMBO J 7, 2585–2591
    OpenUrlPubMedWeb of Science
    1. Artavanis-Tsakonas S.,
    2. Simpson P.
    (1991) Choosing a cell fate: a view from the Notch locus. Trends Genet 7, 403–408
    OpenUrlCrossRefPubMedWeb of Science
    1. Bray S. J.,
    2. Burke B.,
    3. Brown N. H.,
    4. Hirsh J.
    (1989) Embryonic expression pattern of a family of Drosophila proteins that interact with a central nervous system regulatory element. Genes Dev 3, 1130–1145
    OpenUrlAbstract/FREE Full Text
    1. Bray S. J.,
    2. Kafatos F. C.
    (1991) Developmental function of Elf-1: an essential transcription factor during embryogenesis in Drosophila. Genes Dev 5, 1672–1683
    OpenUrlAbstract/FREE Full Text
    1. Busseau I.,
    2. Diederich R. J.,
    3. Xu T.,
    4. Artavanis-Tsakonas S.
    (1994) A member of the Notch group of interacting loci, deltex encodes a cytoplasmic basic protein. Genetics 136, 585–596
    OpenUrlAbstract/FREE Full Text
    1. Cagan R. L.,
    2. Ready D. F.
    (1989) Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev 3, 1099–1112
    OpenUrlAbstract/FREE Full Text
    1. Campuzano S.,
    2. Modollel J.
    (1992) Patterning of the Drosophila nervous system-the achaete - scute gene complex. Trends Genet 8, 202–208
    OpenUrlCrossRefPubMedWeb 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, 643–653
    OpenUrlAbstract/FREE Full Text
    1. Coffman C.,
    2. Harris W.,
    3. Kintner C.
    (1990) Xotch, the Xenopus homolog of Drosophila Notch. Science 249, 1438–1441
    OpenUrlAbstract/FREE Full Text
    1. Coffman C. R.,
    2. Skoglund P.,
    3. Harris W. A.,
    4. Kintner C.
    (1993) Expression of an extracellular deletion of Xotch diverts cell fate in Xenopus embryos. Cell 73, 659–671
    OpenUrlCrossRefPubMedWeb of Science
    1. Corbin V.,
    2. Michelson A. M.,
    3. Abmayr S. M.,
    4. Neel B.,
    5. Alcamo E.,
    6. Maniatis T.,
    7. Young M. W.
    (1991) A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell 67, 311–323
    OpenUrlCrossRefPubMedWeb of Science
    1. de la Concha A.,
    2. Dietrich U.,
    3. Weigel D.,
    4. Campos-Ortega J. A.
    (1988) Functional interactions of neurogenic genes of Drosophila melanogaster. Genetics 118, 499–508
    OpenUrlAbstract/FREE Full Text
    1. Del Amo F. F.,
    2. Smith D. E.,
    3. Swiatek P. J.,
    4. Gendron-Maguire M.,
    5. Greenspan R. J.,
    6. McMahon A. P.,
    7. Gridley T.
    (1992) Expression pattern of Motch, a mouse homolog of DrosophilaNotch, suggests an impotant role in early postimplantation mouse development. Development 115, 737–744
    OpenUrlAbstract/FREE Full Text
    1. Delidakis C.,
    2. Artavanis-Tsakonas S.
    (1992) The Enhancer of Split [E(spl)] locus of Drosophila encodes seven independent helix-loop-helix proteins. Proc. Natl. Acad. Sci. USA 89, 8731–8735
    OpenUrlAbstract/FREE Full Text
    1. Delidakis C.,
    2. Preiss A.,
    3. Hartley D. A.,
    4. Artavanis-Tsakonas S.
    (1991) Two genetically and molecularly distinct functions involved in early neurogenesis reside within the Enhancer of split locus of Drosophila melanogaster. Genetics 129, 803–823
    OpenUrlAbstract/FREE Full Text
    1. Diederich R. J.,
    2. Matsuno K.,
    3. Hing H.,
    4. Artavanis-Tsakonas S.
    (1994) Cytosolic interaction between deltex and Notch ankyrin repeats implicates deltex in the Notch signal. Development 120, 473–481
    OpenUrlAbstract
    1. Doe C.
    (1992) Molecular markers for identified neuroblasts and ganglionmother cells in the Drosophila central nervous system. Development 116, 855–863
    OpenUrlAbstract/FREE Full Text
    1. Ellisen L. W.,
    2. Bird J.,
    3. West D. C.,
    4. Soreng A. L.,
    5. Reynolds T. C.,
    6. Smith S. D.,
    7. Sklar J.
    (1991) TAN-1, the human homolog of the Drosophila Notch gene, is broken by chromosomal translocations in T lymphoblstic neoplasms. Cell 66, 649–661
    OpenUrlCrossRefPubMedWeb of Science
    1. Fehon R. G.,
    2. Kooh P. J.,
    3. Rebay I.,
    4. Regan C. L.,
    5. Xu T.,
    6. Muskavitch M. A. T.,
    7. Artavanis-Tsakonas S.
    (1990) Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell 61, 523–534
    OpenUrlCrossRefPubMedWeb of Science
    1. Fortini M. E.,
    2. Artavanis-Tsakonas S.
    (1993) Notch: neurogenesis is only part of the picture. Cell 75, 1245–1247
    OpenUrlCrossRefPubMedWeb of Science
    1. Fortini M. E.,
    2. Rebay I.,
    3. Caron L. A.,
    4. Artavanis-Tsakonas S.
    (1993) An activated Notch receptor blocks cell fate commitment in the developing Drosophila eye. Nature 365, 555–557
    OpenUrlCrossRefPubMedWeb of Science
    1. Godt D.,
    2. Schrons H.,
    3. Guth S.,
    4. Campos-Ortega J. A.
    (1991) The distribution of transcripts of neurogenic genes in neurogenic mutants of Drosophila melanogaster. J. Neurogenetics 7, 241–252
    OpenUrlPubMed
    1. Greenwald I.,
    2. Rubin G. M.
    (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. Hart A. C.,
    2. Kramer H.,
    3. Van Vactor D. L., Jr.,
    4. Paidhungat M.,
    5. Zipursky S. L.
    (1990) Induction of cell fate in the Drosophila retina: the bride of sevenless protein is predicted to contain a large extracellular domain and seven transmembrane segments. Genes Dev 4, 1835–1847
    OpenUrlAbstract/FREE Full Text
    1. Hartenstein A.,
    2. Rugendoff A.,
    3. Tepass U.,
    4. Hartenstein V.
    (1992) The function of neurogenic genes during epithelium formation in the Drosophila embryo. Development 116, 1203–1220
    OpenUrlAbstract/FREE Full Text
    1. Hartley D. A.,
    2. Preiss A.,
    3. Artavanis-Tsakonas
    (1988) A deduced gene product from the Drosophila neurogenic locus, Enhancer of split, shows homology to mammalian G-protein b subunit. Cell 55, 785–795
    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. Hoppe P. E.,
    2. Greenspan R. J.
    (1990) The Notch locus is required in epidermal cells for epidermal development. Development 109, 875–885
    OpenUrlAbstract/FREE Full Text
    1. Kidd S.,
    2. Kelley M. R.,
    3. Young M. W.
    (1989) Sequence of the Notch locus of Drosophila: Relationship of the encoded protein to mammalian clotting and growth factors. Mol. Cell. Biol 6, 3094–3108
    OpenUrl
    1. Kidd S.,
    2. Lockett T. J.,
    3. Young M. W.
    (1983) The Notch locus of Drosophila melanogaster. Cell 34, 421–433
    OpenUrlCrossRefPubMedWeb of Science
    1. Klämbt C.,
    2. Knust E.,
    3. Tietze K.,
    4. Campos-Ortega J. A.
    (1989) Closely related transcripts encoded by the neurogenic gene complex Enhancer of split of Drosophila melanogaster. EMBO J 8, 203–210
    OpenUrlPubMedWeb of Science
    1. Knust E.,
    2. Schrons H.,
    3. Grawe F.,
    4. Campos-Ortega J. A.
    (1992) Seven Genes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics 132, 505–518
    OpenUrlAbstract/FREE Full Text
    1. Lieber T.,
    2. Kidd S.,
    3. Alcamo E.,
    4. Corbin V.,
    5. Young M. W.
    (1993) Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei. Genes Dev 7, 1949–1965
    OpenUrlAbstract/FREE Full Text
    1. Martin-Bermudo M. D.,
    2. Martinez C.,
    3. Rodriguez I.,
    4. Jimenez F.
    (1991) Distribution and function of the lethal of scute gene product during early neurogenesis in Drosophila. Development 113, 445–454
    OpenUrlAbstract
    1. Preiss A.,
    2. Hartley D. A.,
    3. Artavanis-Tsakonas S.
    (1988) The molecular genetics of E(spl), a gene required for early embryonic neural development in Drosophila melanogaster. EMBO J 7, 3917–3927
    OpenUrlPubMedWeb of Science
    1. Rebay I.,
    2. Fehon R. G.,
    3. Artavanis-Tsakonas S.
    (1993) Specific truncations of Drosophila Notch define dominant activated and dominant negative forms of the receptor. Cell 74, 319–329
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruiz-Gomez M.,
    2. Ghysen A.
    (1993) The expression and role of a proneural gene, acheate, in the development of the larval nervous system of Drosophila. EMBO J 12, 1121–1130
    OpenUrlPubMedWeb of Science
    1. Ruohola H.,
    2. Bremer K. A.,
    3. Baker D.,
    4. Swedlow J. R.,
    5. Jan L. Y.,
    6. Jan Y. N.
    (1991) Role of neurogenic genes in establishment of folicle cell fate and oocyte polarity during oogenesis in Drosophila. Cell 66, 433–439
    OpenUrlCrossRefPubMedWeb of Science
    1. Schrons H.,
    2. Knust E.,
    3. Campos-Ortega J. A.
    (1992) The Enhancer of split complex and adjacent genes in the 96F region of Drosophila melanogaster are required for segregation of neural and epidermal progenitor cells. Genetics 132, 481–503
    OpenUrlAbstract/FREE Full Text
    1. Schweisguth F.,
    2. Posakony J. W.
    (1994) Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis. Development 120, 1433–1441
    OpenUrlAbstract
    1. Shepard S. B.,
    2. Boverman S. A.,
    3. Muskavitch M. A. T.
    (1989) A tripartite interaction among alleles of Notch, Delta and Enhancer of split during imaginal development of Drosophila melanogaster. Genetics 122, 429–438
    OpenUrlAbstract/FREE Full Text
    1. Shermoen A. W.,
    2. O'Farrell P. H.
    (1991) Progreesion of the Cell Cycle through mitosis leads to abortion of nascent transcripts. Cell 67, 303–310
    OpenUrlCrossRefPubMedWeb of Science
    1. Skeath J.,
    2. Carroll S.
    (1992) Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo. Development 114, 939–946
    OpenUrlAbstract
    1. Struhl G.,
    2. Fitzgerald K.,
    3. Greenwald I.
    (1993) Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74, 331–345
    OpenUrlCrossRefPubMedWeb of Science
    1. Tata F.,
    2. Hartley D. A.
    (1993) The role of the Enhancer of split complex during cell fate determination in Drosophila. Development 1993, 139–148
    1. Technau G. M.,
    2. Campos-Ortega J. A.
    (1987) Cell autonomy of expression of neurogenic genes of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 84, 4500–4504
    OpenUrlAbstract/FREE Full Text
    1. Vässin H.,
    2. Campos-Ortega J. A.
    (1987) Genetic analysis of Delta, a neurogenic gene of Drosophila melanogaster. Genetics 116, 433–445
    OpenUrlAbstract/FREE Full Text
    1. Vässin H.,
    2. Vielmetter J.,
    3. Campos-Ortega J. A.
    (1985) Genetic interactions in early neurogenesis of Drosophila melanogaster. J. Neurogenetics 2, 291–308
    OpenUrlCrossRefPubMedWeb of Science
    1. Weinmaster G.,
    2. Roberts V. J.,
    3. Lemke G.
    (1991) A homologue of DrosophilaNotch expressed during mammalian development. Development 113, 199–205
    OpenUrlAbstract
    1. Welshons W. J.
    (1956) Dosage sensitive interactions with split mutations in the presence of an enhancer of split. Drosophila Inf. Service 30
    1. Wharton K. A.,
    2. Johansen K. M.,
    3. Xu T.,
    4. Artavanis-Tsakonas S.
    (1985). Nucleotide sequence from the neurogenic locus Notch implies a gene product that shares homology with proteins containing EGF-repeats. Cell 49, 177–184
    OpenUrlAbstract
    1. Xu T.,
    2. Caron L. A.,
    3. Rehon R. G.,
    4. Artavanis-Tsakonas S.
    (1992) The involvement of the Notch locus in Drosophila oogenesis. Development 115, 913–922
    OpenUrlAbstract/FREE Full Text
    1. Xu T.,
    2. Rebay I.,
    3. Fleming R. J.,
    4. Scottgale T. N.,
    5. Artavanis-Tsakonas S.
    (1990) The Notch locus and genetic circuitry involved in early Drosophila neurogenesis. Genes Dev 4, 464–475
Back to top

 Download PDF

Email
JOURNAL ARTICLES
The Notch signalling pathway is required for Enhancer of split bHLH protein expression during neurogenesis in the Drosophila embryo
B. Jennings, A. Preiss, C. Delidakis, S. Bray
Development 1994 120: 3537-3548;
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.