Abstract
The E(spl) locus is thought to participate in a cell interaction mechanism that controls the choice of many cell fates during Drosophila development, including the segregation of neural precursors. Previous studies have demonstrated that E(spl) is defined by two groups of closely related transcripts, (i) a cluster of three transcripts encoding proteins bearing a helix-loop-helix (HLH) motif and (ii) a single-copy gene encoding a nuclear protein containing repeated motifs first identified in the beta subunit of guanine nucleotide-binding proteins. Both groups interact genetically with the Notch locus, which codes for a transmembrane protein. We report the structure of four additional HLH-encoding genes that reside in the E(spl) complex and provide evidence that we have now identified all the remaining members of the E(spl) HLH cluster.
Full text
PDF




Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alonso M. C., Cabrera C. V. The achaete-scute gene complex of Drosophila melanogaster comprises four homologous genes. EMBO J. 1988 Aug;7(8):2585–2591. doi: 10.1002/j.1460-2075.1988.tb03108.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Artavanis-Tsakonas S., Delidakis C., Fehon R. G. The Notch locus and the cell biology of neuroblast segregation. Annu Rev Cell Biol. 1991;7:427–452. doi: 10.1146/annurev.cb.07.110191.002235. [DOI] [PubMed] [Google Scholar]
- Artavanis-Tsakonas S., Simpson P. Choosing a cell fate: a view from the Notch locus. Trends Genet. 1991 Nov-Dec;7(11-12):403–408. doi: 10.1016/0168-9525(91)90264-q. [DOI] [PubMed] [Google Scholar]
- Benezra R., Davis R. L., Lockshon D., Turner D. L., Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 1990 Apr 6;61(1):49–59. doi: 10.1016/0092-8674(90)90214-y. [DOI] [PubMed] [Google Scholar]
- Blackwood E. M., Eisenman R. N. Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc. Science. 1991 Mar 8;251(4998):1211–1217. doi: 10.1126/science.2006410. [DOI] [PubMed] [Google Scholar]
- Brown N. H., Kafatos F. C. Functional cDNA libraries from Drosophila embryos. J Mol Biol. 1988 Sep 20;203(2):425–437. doi: 10.1016/0022-2836(88)90010-1. [DOI] [PubMed] [Google Scholar]
- Cabrera C. V., Alonso M. C. Transcriptional activation by heterodimers of the achaete-scute and daughterless gene products of Drosophila. EMBO J. 1991 Oct;10(10):2965–2973. doi: 10.1002/j.1460-2075.1991.tb07847.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cabrera C. V. Lateral inhibition and cell fate during neurogenesis in Drosophila: the interactions between scute, Notch and Delta. Development. 1990 Sep;110(1):733–742. [PubMed] [Google Scholar]
- Carroll S. B., Laughon A., Thalley B. S. Expression, function, and regulation of the hairy segmentation protein in the Drosophila embryo. Genes Dev. 1988 Jul;2(7):883–890. doi: 10.1101/gad.2.7.883. [DOI] [PubMed] [Google Scholar]
- Cubas P., de Celis J. F., Campuzano S., Modolell J. Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc. Genes Dev. 1991 Jun;5(6):996–1008. doi: 10.1101/gad.5.6.996. [DOI] [PubMed] [Google Scholar]
- Davis R. L., Cheng P. F., Lassar A. B., Weintraub H. The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell. 1990 Mar 9;60(5):733–746. doi: 10.1016/0092-8674(90)90088-v. [DOI] [PubMed] [Google Scholar]
- Delidakis C., Preiss A., Hartley D. A., Artavanis-Tsakonas S. Two genetically and molecularly distinct functions involved in early neurogenesis reside within the Enhancer of split locus of Drosophila melanogaster. Genetics. 1991 Nov;129(3):803–823. doi: 10.1093/genetics/129.3.803. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doe C. Q., Goodman C. S. Early events in insect neurogenesis. II. The role of cell interactions and cell lineage in the determination of neuronal precursor cells. Dev Biol. 1985 Sep;111(1):206–219. doi: 10.1016/0012-1606(85)90446-4. [DOI] [PubMed] [Google Scholar]
- Ellis H. M., Spann D. R., Posakony J. W. extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins. Cell. 1990 Apr 6;61(1):27–38. doi: 10.1016/0092-8674(90)90212-w. [DOI] [PubMed] [Google Scholar]
- Fehon R. G., Kooh P. J., Rebay I., Regan C. L., Xu T., Muskavitch M. A., Artavanis-Tsakonas S. Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell. 1990 May 4;61(3):523–534. doi: 10.1016/0092-8674(90)90534-l. [DOI] [PubMed] [Google Scholar]
- Garrell J., Modolell J. The Drosophila extramacrochaetae locus, an antagonist of proneural genes that, like these genes, encodes a helix-loop-helix protein. Cell. 1990 Apr 6;61(1):39–48. doi: 10.1016/0092-8674(90)90213-x. [DOI] [PubMed] [Google Scholar]
- Ghysen A., Dambly-Chaudière C. From DNA to form: the achaete-scute complex. Genes Dev. 1988 May;2(5):495–501. doi: 10.1101/gad.2.5.495. [DOI] [PubMed] [Google Scholar]
- Hart A. C., Krämer H., Van Vactor D. L., Jr, Paidhungat M., Zipursky S. L. 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. 1990 Nov;4(11):1835–1847. doi: 10.1101/gad.4.11.1835. [DOI] [PubMed] [Google Scholar]
- Hartley D. A., Preiss A., Artavanis-Tsakonas S. A deduced gene product from the Drosophila neurogenic locus, enhancer of split, shows homology to mammalian G-protein beta subunit. Cell. 1988 Dec 2;55(5):785–795. doi: 10.1016/0092-8674(88)90134-1. [DOI] [PubMed] [Google Scholar]
- Ingham P. W., Pinchin S. M., Howard K. R., Ish-Horowicz D. Genetic Analysis of the Hairy Locus in DROSOPHILA MELANOGASTER. Genetics. 1985 Nov;111(3):463–486. doi: 10.1093/genetics/111.3.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jan Y. N., Jan L. Y. Genes required for specifying cell fates in Drosophila embryonic sensory nervous system. Trends Neurosci. 1990 Dec;13(12):493–498. doi: 10.1016/0166-2236(90)90083-m. [DOI] [PubMed] [Google Scholar]
- Jiménez F., Campos-Ortega J. A. Defective neuroblast commitment in mutants of the achaete-scute complex and adjacent genes of D. melanogaster. Neuron. 1990 Jul;5(1):81–89. doi: 10.1016/0896-6273(90)90036-f. [DOI] [PubMed] [Google Scholar]
- Klämbt C., Knust E., Tietze K., Campos-Ortega J. A. Closely related transcripts encoded by the neurogenic gene complex enhancer of split of Drosophila melanogaster. EMBO J. 1989 Jan;8(1):203–210. doi: 10.1002/j.1460-2075.1989.tb03365.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knust E., Tietze K., Campos-Ortega J. A. Molecular analysis of the neurogenic locus Enhancer of split of Drosophila melanogaster. EMBO J. 1987 Dec 20;6(13):4113–4123. doi: 10.1002/j.1460-2075.1987.tb02757.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martín-Bermudo M. D., Martínez C., Rodríguez A., Jiménez F. Distribution and function of the lethal of scute gene product during early neurogenesis in Drosophila. Development. 1991 Oct;113(2):445–454. doi: 10.1242/dev.113.2.445. [DOI] [PubMed] [Google Scholar]
- Murre C., McCaw P. S., Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell. 1989 Mar 10;56(5):777–783. doi: 10.1016/0092-8674(89)90682-x. [DOI] [PubMed] [Google Scholar]
- Murre C., McCaw P. S., Vaessin H., Caudy M., Jan L. Y., Jan Y. N., Cabrera C. V., Buskin J. N., Hauschka S. D., Lassar A. B. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell. 1989 Aug 11;58(3):537–544. doi: 10.1016/0092-8674(89)90434-0. [DOI] [PubMed] [Google Scholar]
- Preiss A., Hartley D. A., Artavanis-Tsakonas S. The molecular genetics of Enhancer of split, a gene required for embryonic neural development in Drosophila. EMBO J. 1988 Dec 1;7(12):3917–3927. doi: 10.1002/j.1460-2075.1988.tb03278.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reed K. C., Mann D. A. Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res. 1985 Oct 25;13(20):7207–7221. doi: 10.1093/nar/13.20.7207. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rogers S., Wells R., Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science. 1986 Oct 17;234(4774):364–368. doi: 10.1126/science.2876518. [DOI] [PubMed] [Google Scholar]
- Rushlow C. A., Hogan A., Pinchin S. M., Howe K. M., Lardelli M., Ish-Horowicz D. The Drosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N-myc. EMBO J. 1989 Oct;8(10):3095–3103. doi: 10.1002/j.1460-2075.1989.tb08461.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simpson P. Lateral inhibition and the development of the sensory bristles of the adult peripheral nervous system of Drosophila. Development. 1990 Jul;109(3):509–519. doi: 10.1242/dev.109.3.509. [DOI] [PubMed] [Google Scholar]
- Skeath J. B., Carroll S. B. Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev. 1991 Jun;5(6):984–995. doi: 10.1101/gad.5.6.984. [DOI] [PubMed] [Google Scholar]
- Van Doren M., Ellis H. M., Posakony J. W. The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes. Development. 1991 Sep;113(1):245–255. doi: 10.1242/dev.113.1.245. [DOI] [PubMed] [Google Scholar]
- Voronova A., Baltimore D. Mutations that disrupt DNA binding and dimer formation in the E47 helix-loop-helix protein map to distinct domains. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4722–4726. doi: 10.1073/pnas.87.12.4722. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weintraub H., Dwarki V. J., Verma I., Davis R., Hollenberg S., Snider L., Lassar A., Tapscott S. J. Muscle-specific transcriptional activation by MyoD. Genes Dev. 1991 Aug;5(8):1377–1386. doi: 10.1101/gad.5.8.1377. [DOI] [PubMed] [Google Scholar]