Advertisement
JOURNAL ARTICLES
Neuroectodermal transcription of the Drosophila neurogenic genes E(spl) and HLH-m5 is regulated by proneural genes
B. Kramatschek, J.A. Campos-Ortega
Development 1994 120: 815-826;

Summary

The Enhancer of split gene complex (E(SPL)-C) of Drosophila comprises seven genes encoding bHLH proteins, which are required by neuroectodermal cells for epidermal development. Using promoter and gene fusions with the lacZ gene, we determined the location of cis-acting sequences necessary for normal expression of two of the genes of the E(SPL)-C, E(spl) and HLH-m5. About 0.46 kb of E(spl) and 1.9 kb of HLH-m5 upstream sequences are necessary to reproduce the normal transcription pattern of these genes. The gene products of achaete, scute and lethal of scute, together with that of ventral nervous system condensation defective, act synergistically to specify the neuroectodermal E(spl) and HLH-m5 expression domains. Negative cross- and autoregulatory interactions of the E(SPL)-C on E(spl) contribute, directly or indirectly, to this regulation. Interactions involve DNA binding, since mutagenesis of binding sites for bHLH proteins in the E(spl) promoter abolishes neuroectodermal expression and activates ectopic expression in neuroblasts. A model for activation and repression of E(spl) in the neuroectoderm and neuroblasts, respectively, is proposed.

REFERENCES

    1. Alonso M. C.,
    2. Cabrera C. V.
    (1988) The achaete-scute gene complex of Drosophila melanogaster comprises four homologous genes. EMBO J 7, 2585–2591
    OpenUrlPubMedWeb of Science
    1. Cabrera C. V.
    (1990) Lateral inhibition and cell fate during neurogenesis in Drosophila, the interaction between scute, Notch, and Delta. Development 109, 733–742
    OpenUrlAbstract
    1. Cabrera C. V.,
    2. Martinez Arias A.,
    3. Bate M.
    (1987) The expression of three members of the achaete-scute gene complex correlates with neuroblast segregation in Drosophila. Cell 50, 425–433
    OpenUrlCrossRefPubMedWeb of Science
    1. Caudy M.,
    2. Vässin H.,
    3. Brand M.,
    4. Tuma R.,
    5. Jan L. Y.,
    6. Jan Y. N.
    (1988) daughterless, a gene essential for both neurogenesis and sex determination in Drosophila, has sequence similarities to myc and the achaete-scute complex. Cell 55, 1061–1067
    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. 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. Doe C. Q.
    (1992) Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116, 855–863
    OpenUrlAbstract/FREE Full Text
    1. Garcia-Bellido A.
    (1979) Genetic analysis of the achaete-scute system of Drosophila melanogaster. Genetics 91, 491–520
    OpenUrlAbstract/FREE Full Text
    1. Garcia-Bellido A.,
    2. Santamaria P.
    (1978) Developmental analysis of the achaete-scute system of Drosophila melanogaster. Genetics 88, 469–486
    OpenUrlAbstract/FREE Full Text
    1. Ghysen A.,
    2. Dambly-Chaudiere C.
    (1989) Genesis of the Drosophila periheral nervous system. Trends Genet 5, 251–255
    OpenUrlCrossRefPubMedWeb of Science
    1. Ghysen A.,
    2. Dambly-Chaudiere C.,
    3. Jan L. Y.,
    4. Jan Y.-N.
    (1993) Cell interactions and gene interactions in peripheral neurogenesis. Genes Dev 7, 723–733
    OpenUrlFREE Full Text
    1. González F.,
    2. Romani S.,
    3. Cubas P.,
    4. Modolell J.,
    5. Campuzano S.
    (1989) Molecular analysis of asense, a member of the achaete-scute complex of Drosophila melanogaster, and its novel role in optic lobe development. EMBO J., 8, 3553–3562
    OpenUrlPubMedWeb of Science
    1. Hart A. C.,
    2. Krämer H.,
    3. Van Vactor D. L., Jr.,
    4. Paidhungat M.,
    5. Zipursky S. L.
    (1990) Induction of cell fate in the Drosophila retina, thebride 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. Hinz U.,
    2. Giebel B.,
    3. Campos-Ortega J. A.
    (1994) The basic-helix-loop-helix domain of the Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 76, 77–87
    OpenUrlCrossRefPubMedWeb of Science
    1. Hinz U.,
    2. Wolk A.,
    3. Renkawitz-Pohl R.
    (1992) Ultrabithorax is a regulator of3 tubulin expression in the Drosophila visceral mesoderm. Development 116, 543–554
    OpenUrlAbstract
    1. Jan Y. N.,
    2. Jan L. Y.
    (1990) Genes required for specifying cell fates in Drosophila embryonic sensory nervous system. Trends Neurosci 13, 493–498
    OpenUrlCrossRefPubMedWeb of Science
    1. Jimenez F.,
    2. Campos-Ortega J. A.
    (1979) A region of the Drosophila genome ncessary for CNS development. Nature 282, 310–312
    OpenUrlCrossRefPubMed
    1. Jimenez F.,
    2. Campos-Ortega J. A.
    (1987) Genes in subdivision 1B of the Drosophila melanogaster X-chromosome and their influence on neuronal development. J. Neurogenet 4, 179–200
    OpenUrlPubMedWeb of Science
    1. Jimenez F.,
    2. Campos-Ortega J. A.
    (1990) Defective neuroblast commitment in mutants of the achaete - scute complex and adjacent genes of Drosophila melanogaster. Neuron 5, 81–89
    OpenUrlCrossRefPubMedWeb of Science
    1. Jones T. R.,
    2. Cole M. D.
    (1987) Rapid cytoplasmic turnover of c-myc mRNA. Requirement of the 3untranslated sequences. Mol. Cell. Biol 7, 4513–4521
    OpenUrlAbstract/FREE Full Text
    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. Bremer K. A.,
    3. Vässin H.,
    4. Ziemer A.,
    5. Tepass U.,
    6. Campos-Ortega J. A.
    (1987) The Enhancer of split locus and neurogenesis in Drosophila melanogaster. Dev. Biol 122, 262–273
    OpenUrlCrossRefPubMedWeb of Science
    1. Knust E.,
    2. Tietze K.,
    3. Campos-Ortega J. A.
    (1987) Molecular analysis of the neurogenic locus Enhancer of split of Drosophila melanogaster. EMBO J 6, 4113–4123
    OpenUrlPubMedWeb of Science
    1. Knust E.,
    2. Schrons H.,
    3. Grawe F.,
    4. Campos-Ortega J. A.
    (1992) Sevengenes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics 132, 505–518
    OpenUrlAbstract/FREE Full Text
    1. Laski F. A.,
    2. Rio D. C.,
    3. Rubin G. M.
    (1986) Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell 44, 7–19
    OpenUrlCrossRefPubMedWeb of Science
    1. Martin-Bermudo M. D.,
    2. Martinez C.,
    3. Rodriguez A.,
    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. Mason J. M.,
    2. Voelker R. A.,
    3. Rosen D.,
    4. Campos A. R.,
    5. White K.,
    6. Lim J. K.
    (1986) Localization of terminal deficiency breakpoints on the X chromosome. Drosophila Inform. Serv 63, 164–165
    OpenUrl
    1. Molsberger G.,
    2. Schäfer U.,
    3. Schäfer M.
    (1988) A new set of lacZ fusion vectors, pUCPlac, for studying gene expression in Drosophila by P-mediated transformation. Gene 3, 147–151
    1. Murre C.,
    2. Schonleber McCaw P.,
    3. Baltimore D.
    (1989) The amphipathic helix-loop-helix, a new DNA-binding and dimerization motif in immunglobulin enhancer binding, daughterless, MyoD and myc proteins. Cell 56, 777–783
    OpenUrlCrossRefPubMedWeb of Science
    1. Patel N.,
    2. Martin-Blanco E.,
    3. Coleman K. G.,
    4. Poole S. J.,
    5. Ellis M. C.,
    6. Kornberg T. B.,
    7. Goodman C. S.
    (1989) Expression of engrailed proteins in arthropods, annelids and chordates. Cell 58, 955–968
    OpenUrlCrossRefPubMedWeb of Science
    1. Romani S.,
    2. Campuzano S.,
    3. Modolell J.
    (1987) The achaete-scute complex is expressed in neurogenic regions of Drosophila embryos. EMBO J 6, 2085–2092
    OpenUrlPubMedWeb of Science
    1. Romani S.,
    2. Campuzano S.,
    3. Macagno E. R.,
    4. Modolell J.
    (1989) Expression of achaete and scute genes in Drosophila imaginal discs and their function in sensory organ development. Genes Dev 3, 997–100
    OpenUrlAbstract/FREE Full Text
    1. Rubin G. M.,
    2. Spradling A. C.
    (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218, 348–353
    OpenUrlAbstract/FREE Full Text
    1. Ruiz-Gomez M.,
    2. Ghysen A.
    (1993) The expression and role of a proneural gene, achaete, in the development of the larval nervous system of Drosophila. EMBO J 12, 1121–1130
    OpenUrlPubMedWeb of Science
    1. Schrons H.,
    2. Knust E.,
    3. Campos-Ortega J. A.
    (1992) The Enhancer of split complex and adjacent genes in the 96 F region of Drosophila melanogaster are required for segregation of neural and epidermal progenitor cells. Genetics 132, 481–503
    OpenUrlAbstract/FREE Full Text
    1. Shaw G.,
    2. Kamen R.
    (1986) A conserved AU sequence from the 3untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46, 659–667
    OpenUrlCrossRefPubMedWeb of Science
    1. Shyu A.-B.,
    2. Greenberg M. E.,
    3. Belasco J. G.
    (1989) The c-fos transcript is targeted for rapid decay by two distinct mRNA degradation pathways. Genes Dev 3, 60–72
    OpenUrlAbstract/FREE Full Text
    1. Simpson P.
    (1990) Lateral inhibition and the development of the sensory bristles of the adult peripheral nervous system of Drosophila. Development 109, 509–519
    OpenUrlAbstract
    1. Skeath J. B.,
    2. Carroll S. B.
    (1992) Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo. Development 114, 939–946
    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 translational control of the segmentation gene hunchback. Chromosoma 98, 81–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Tietze K.,
    2. Oellers N.,
    3. Knust E.
    (1992) Enhancer of splitD, a dominant mutation of Drosophila and its use in the study of functional domains of a helix-loop-helix protein. Proc. Natl Acad. Sci. USA 89, 6152–6156
    OpenUrlAbstract/FREE Full Text
    1. Villares R.,
    2. Cabrera C. V.
    (1987) The achaete-scute gene complex of Drosophila melanogaster: conserved domains in a subset of genes required for neurogenesis and their homology to myc. Cell 50, 415–424
    OpenUrlCrossRefPubMedWeb of Science
    1. White K.
    (1980) Defective neural development in Drosophila melanogaster embryos deficient for the tip of the X-chromosome. Dev. Biol 80, 322–344
    1. White K.,
    2. Decelles N. L.,
    3. Enlow T. C.
    (1983) Genetic and developmental analysis of the locus vnd in Drosophila melanogaster. Genetics 104, 433–488
    OpenUrlAbstract/FREE Full Text
Back to top

 Download PDF

Email
Neuroectodermal transcription of the Drosophila neurogenic genes E(spl) and HLH-m5 is regulated by proneural genes
B. Kramatschek, J.A. Campos-Ortega
Development 1994 120: 815-826;
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

A new Editor-in-Chief for Development

http://dev.biologists.org/sites/default/files/Snippet/0318_News.jpg

“I'm very keen that Development continues to innovate and support our community.”

We're delighted to announce the appointment of James Briscoe, Group Leader at The Francis Crick Institute, London, as our new Editor-in-Chief. Read our interview with James to find out his career and research interests, the importance of interdisciplinary thinking in developmental biology, and his views on the current state and future opportunities in scientific publishing. Also, check out the Editorial from Sarah Bray, Kate Storey and Katherine Brown to learn more about the announcement, and about our recent community consultation.

Review – Developing in 3D: the role of CTCF in cell differentiation

In this Review, Rodrigo G. Arzate-Mejía, Félix Recillas-Targa and Victor G. Corces discuss evidence linking CTCF to the control of developmental processes in various cell and tissue types through 3D organization of the genome.

From stem cells to human development ­– meeting reporter competition

In September, Development is hosting our next meeting focusing on human developmental biology. We are excited to announce a competition for a reporter to cover the meeting for the Node. The winner will get free registration to the meeting, and it’s a fantastic opportunity to practice your science communication skills - find out more here.

Spotlight ­– Susan Strome

“I realised that I could think it through on my own – I didn't require that my advisor tell me what to do or how to do it”

Recently appointed an editor at Development, we caught up with Susan to discuss her early career switch from prokaryotes to worms, her experiences of small and big science, and why teaching is so important to her.

On the Node – The people behind the papers

Development and homeostasis depend crucially on the maintenance of cell identity, and in gamete-producing tissues the somatic/germline distinction is paramount. A recent paper in Development explores how cell identity is secured in the Drosophila ovary by studying the function of the conserved tumour suppressor L(3)mbt. To find out more about the story, the Node caught up with first author Rémi-Xavier Coux and his supervisor Ruth Lehmann of the Skirball Institute at New York University School of Medicine.  

Santa Cruz Developmental Biology Meeting

Development is a proud sponsor of the upcoming Santa Cruz Developmental Biology Meeting, which takes place 11-15 August 2018 at the University of California, Santa Cruz . Registration for this meeting is now open!

Articles of interest in our sister journals

Rap1, Canoe and Mbt cooperate with Bazooka to promote zonula adherens assembly in the fly photoreceptor
Rhian F. Walther, Mubarik Burki, Noelia Pinal, Clare Rogerson, Franck Pichaud. J Cell Sci 2018 131: jcs207779.

H2AFX and MDC1 promote maintenance of genomic integrity in male germ cells
Erika Testa, Daniela Nardozi, Cristina Antinozzi, Monica Faieta, Stefano Di Cecca, Cinzia Caggiano, Tomoyuki Fukuda, Elena Bonanno, Lou Zhenkun, Andros Maldonado, Ignasi Roig, Monica Di Giacomo, Marco Barchi. J Cell Sci 2018 131: jcs214411.