Advertisement
JOURNAL ARTICLES
Characterization of Star and its interactions with sevenless and EGF receptor during photoreceptor cell development in Drosophila
A.L. Kolodkin, A.T. Pickup, D.M. Lin, C.S. Goodman, U. Banerjee
Development 1994 120: 1731-1745;

Summary

Loss-of-function mutations in Star impart a dominant rough eye phenotype and, when homozygous, are embryonic lethal with ventrolateral cuticular defects. We have cloned the Star gene and show that it encodes a novel protein with a putative transmembrane domain. Star transcript is expressed in a dynamic pattern in the embryo including in cells of the ventral midline. In the larval eye disc, Star is expressed first at the morphogenetic furrow, then in the developing R2, R5, and R8 cells as well as in the posterior clusters of the disc in additional R cells. Star interacts with Drosophila EGF receptor in the eye and mosaic analysis of Star in the larval eye disc reveals that homozygous Star patches contain no developing R cells. Taken together with the expression pattern at the morphogenetic furrow, these results demonstrate an early role for Star in photoreceptor development. Additionally, loss-of-function mutations in Star act as suppressors of R7 development in a sensitized genetic background involving the Son of sevenless (Sos) locus, and overexpression of Star enhances R7 development in this genetic background. Based on the genetic interactions with Sos, we suggest that Star also has a later role in photoreceptor development including the recruitment of the R7 cell through the sevenless pathway.

REFERENCES

    1. Altschul S. F.,
    2. Gish W.,
    3. Miller W.,
    4. Myers E. W.,
    5. Lipman D. J.
    (1990) Basic local alignment search tool. J. Mol. Biol 215, 403–410
    OpenUrlCrossRefPubMedWeb of Science
    1. Baker N. E.,
    2. Rubin G. M.
    (1989) Effect on eye development of dominant mutations in Drosophila homologue of EGF-receptor. Nature 340, 150–153
    OpenUrlCrossRefPubMed
    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. Banerjee U.,
    2. Renfranz P. J.,
    3. Pollock J. A.,
    4. Benzer S.
    (1987) Molecular characterization and expression of sevenless, a gene involved in neuronal pattern formation in the Drosophila eye. Cell 49, 281–291
    OpenUrlCrossRefPubMedWeb of Science
    1. Banerjee U.,
    2. Renfranz P. J.,
    3. Hinton D. R.,
    4. Rabin B. A.,
    5. Benzer S.
    (1987) The Sevenless+protein is expressed apically in cell membranes of developing Drosophila retina; it is not restricted to cell R7. Cell 51, 151–158
    OpenUrlCrossRefPubMedWeb of Science
    1. Banerjee U.,
    2. Zipursky S. L.
    (1990) The role of cell-cell interaction in the development of the Drosophila visual system. Neuron 4, 177–187
    OpenUrlCrossRefPubMedWeb of Science
    1. Bier E.,
    2. Jan L. Y.,
    3. Jan Y. N.
    (1990) rhomboid, a gene required for the dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev 4, 190–203
    OpenUrlAbstract/FREE Full Text
    1. Bonfini L.,
    2. Karlovich C. A.,
    3. Dasgupta C.,
    4. Banerjee U.
    (1992) The Son of sevenless gene product: a putative activator of Ras. Science 255, 603–606
    OpenUrlAbstract/FREE Full Text
    1. Cagan R. L.,
    2. Kramer H.,
    3. Hart A. C.
    (1992) The Bride of sevenless and Sevenless interaction: Internalization of a Transmembrane Ligand. Cell 69, 393–399
    OpenUrlCrossRefPubMedWeb of Science
    1. Dalbey R. E.
    (1990) Positively charged residues are important determinants of membrane protein topology. Trends Biochem 15, 253–257
    OpenUrlCrossRefPubMedWeb of Science
    1. Dickson B.,
    2. Sprenger F.,
    3. Morrison D.,
    4. Hafen E.
    (1993) Raf functions downstream of Ras1 in the Sevenless signal transduction pathway. Nature 360, 600–603
    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. Freeman M.,
    2. Kimmel B. E.,
    3. Rubin G. M.
    (1992) Identifying targets of the rough homeobox gene of Drosophila: evidence that rhomboid functions in eye development. Development 116, 335–346
    OpenUrlAbstract/FREE Full Text
    1. Franceschini N.,
    2. Kirshfeld K.
    (1971) Pseudopupil phenomena in the compound eye of Drosophila. Kybernetik 9, 159–182
    OpenUrlCrossRefPubMedWeb of Science
    1. Gaul U.,
    2. Mardon G.,
    3. Rubin G. M.
    (1992) A putative Ras GTPase activating protein acts as a negative regulator of signaling by the Sevenless receptor tyrosine kinase. Cell 68, 1007–19
    OpenUrlCrossRefPubMedWeb of Science
    1. Golic K.
    (1991) Site specific recombination between homologous chromosomes in Drosophila. Science 252, 958–961
    OpenUrlAbstract/FREE Full Text
    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. Hafen E.,
    2. Basler K.,
    3. Edstroem J. E.,
    4. Rubin G. M.
    (1987) sevenless, a cell-specific homeotic gene of Drosophila, encodes a putative transmembrane receptor. Science 236, 55–63
    OpenUrlAbstract/FREE Full Text
    1. Hart A. C.,
    2. Kramer H.,
    3. Van Vactor D. L.,
    4. Paidhungat M.,
    5. Zipursky S. L.
    (1990) Induction of cell fate in 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. Hashimoto C.,
    2. Hudson K. L.,
    3. Anderson K. V.
    (1988) The Toll gene of Drosophila required for dorso-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 52, 269–279
    OpenUrlCrossRefPubMedWeb of Science
    1. Heberlein U.,
    2. Rubin G. M.
    (1991) Star is required in a subset of photoreceptor cells in the developing Drosophila retina and displays dosage sensitive interactions with rough. Dev. Biol 144, 353–361
    OpenUrlCrossRefPubMedWeb of Science
    1. Heberlein U.,
    2. Hariharan I.,
    3. Rubin G. M.
    (1993) Star is required for neuronal differentiation in the Drosophila retina and displays dosage-sensitive interactions with Ras 1. Dev. Biol 160, 51–63
    OpenUrlCrossRefPubMedWeb of Science
    1. Kim S. H.,
    2. Crews S. T.
    (1993) Influence of Drosophila ventral epidermal development by the CNS midline cells and spitz class genes. Development 118, 1–9
    OpenUrlAbstract
    1. Klämbt C.,
    2. Jacobs R.,
    3. Goodman C. S.
    (1991) The midline of the Drosophila CNS: A model system for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 64, 801–815
    OpenUrlCrossRefPubMedWeb of Science
    1. Kohl N. E.,
    2. Legony E.,
    3. DePinho R. A.,
    4. Nisen P. E.,
    5. Smith R. K.,
    6. Gee C. E.,
    7. Alt F. W.
    (1986) Human N-myc is closely related in organisation and nucleotide sequence to C-myc. Nature 319, 73–77
    OpenUrlCrossRefPubMed
    1. Kopczynski C. C.,
    2. Muskavitch M. A.
    (1992) Introns excised from the Delta primary transcript are localized near sites of Delta transcription. J.Cell Biol 119, 503–12
    OpenUrlAbstract/FREE Full Text
    1. Kramer H.,
    2. Cagan R. L.,
    3. Zipursky S. L.
    (1991) Interaction of Bride of sevenless membrane-bound ligand and the Sevenless tyrosine-kinase receptor. Nature 352, 207–212
    OpenUrlCrossRefPubMedWeb of Science
    1. Landschultz W.,
    2. Johnson P. F.,
    3. McKnight S. L.
    (1988) The leucine zipper: A hypothetical structure common to a new class of DNA binding proteins. Science 245, 1759–1764
    OpenUrl
    1. Lewis E.
    (1945) The relation of repeats to position effect in Drosophila melanogaster. Genetics 30, 137–166
    OpenUrlFREE Full Text
    1. Mayer U.,
    2. Nusslein-Volhard C.
    (1988) A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo. Genes Dev 2, 1496–1511
    OpenUrlAbstract/FREE Full Text
    1. Reinke R.,
    2. Zipursky S. L.
    (1988) Cell-cell interaction in the Drosophila retina: The bride of sevenless gene is required in cell R8 for R7 cell development. Cell 55, 321–330
    OpenUrlCrossRefPubMedWeb of Science
    1. Robertson H. M.,
    2. Prestion C. R.,
    3. Phillis R. W.,
    4. Johnson-Schlitz D. M.,
    5. Benz W. K.,
    6. Engels W. R.
    (1988) A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461–470
    OpenUrlAbstract/FREE Full Text
    1. Rogers S.,
    2. Wells M.,
    3. Rechsteiner M.
    (1986) Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234, 364–368
    OpenUrlAbstract/FREE Full Text
    1. Rogge R. D.,
    2. Karlovich C. A.,
    3. Banerjee U.
    (1991) Genetic dissection of a neurodevelopmental pathway: Son of sevenless functions downstream of the sevenless and EGF receptor tyrosine kinases. Cell 64, 39–48
    OpenUrlCrossRefPubMedWeb of Science
    1. Rogge R. D.,
    2. Cagan R. L.,
    3. Majumdar A.,
    4. Dulaney T.,
    5. Banerjee U.
    (1992) Neuronal development in the Drosophila retina: the sextra gene defines an inhibitory component in the developmental pathway of R7 photoreceptor cells. Proc. Natn. Acad. Sci. USA 89, 5271–5275
    OpenUrlAbstract/FREE Full Text
    1. Rubin G. M.
    (1991) Signal transduction and the fate of the R7 photoreceptor in Drosophila. Trends Genet 7, 372–377
    OpenUrlCrossRefPubMedWeb of Science
    1. Rutledge B. J.,
    2. Zhang K.,
    3. Bier E.,
    4. Jan Y. N.,
    5. Perrimon N.
    (1992) The Drosophilaspitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis. Genes Dev 6, 1503–1517
    OpenUrlAbstract/FREE Full Text
    1. Sanger F.,
    2. Nicklen S.,
    3. Coulson A. R.
    (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463–5467
    OpenUrlAbstract/FREE Full Text
    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. Schneuwly S.,
    2. Klemenz R.,
    3. Gehring W. J.
    (1987) Redesigning the body plan of Drosophila by ectopic expression of the homeotic gene Antennapedia. Nature 325, 816–818
    OpenUrlCrossRefPubMedWeb of Science
    1. Simon M. A.,
    2. Bowtell D. D. L.,
    3. Dodson G. S.,
    4. Laverty T. R.,
    5. Rubin G. M.
    (1991) Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the Sevenless protein tyrosine kinase. Cell 67, 701–716
    OpenUrlCrossRefPubMedWeb of Science
    1. Spiess M.,
    2. Lodish H. F.
    (1986) An internal signal sequence: the asialoglycoprotein receptor membrane anchor. Cell 44, 177–185
    OpenUrlCrossRefPubMedWeb of Science
    1. Sturtevant M.,
    2. Roark M.,
    3. Bier E.
    (1993) Localized expression of the Drosophila rhomboid gene directs wing vein formation. Genes Dev 7, 961–973
    OpenUrlAbstract/FREE Full Text
    1. Tomlinson A.,
    2. Bowtell D. D. L.,
    3. Hafen E.,
    4. Rubin G. M.
    (1987) Localization of the sevenless protein, a putative receptor for positional information, in the eye imaginal disc of Drosophila. Cell 51, 143–150
    OpenUrlCrossRefPubMedWeb of Science
    1. Tomlinson A.,
    2. Ready D. F.
    (1987) Neuronal differentiation in the Drosophila ommatidium. Dev. Biol 120, 366–376
    OpenUrlCrossRefPubMedWeb of Science
    1. Van Vactor D. L.,
    2. Cagan R. L.,
    3. Kramer H.,
    4. Zipursky S. L.
    (1991) Induction in the developing compound eye of Drosophila: Multiple mechanisms restrict R7 induction to a single retinal precursor cell. Cell 67, 1145–1156
    OpenUrlCrossRefPubMedWeb of Science
    1. Wolff T.,
    2. Ready D. F.
    (1991) The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113, 841–850
    OpenUrlAbstract
    1. Zak N. B.,
    2. Shilo B.-Z.
    (1992) Localization of DER and the pattern of cell divisions in wild type and Ellipse eye imaginal discs. Dev. Biol 149, 448–456
    OpenUrlCrossRefPubMedWeb of Science
    1. Zinn K.,
    2. McAllister L.,
    3. Goodman C. S.
    (1988) Sequence analysis and neuronal expression of fasciclin I in grasshopper and Drosophila. Cell 53, 577–587
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Characterization of Star and its interactions with sevenless and EGF receptor during photoreceptor cell development in Drosophila
A.L. Kolodkin, A.T. Pickup, D.M. Lin, C.S. Goodman, U. Banerjee
Development 1994 120: 1731-1745;
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 society for regenerative biologists

Kenneth Poss and Elly Tanaka announce the launch of the International Society for Regenerative Biology (ISRB), which will promote research and education in the field of regenerative biology.

Upcoming special issue: call for papers

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

The special issue welcomes Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

An interview with Cagney Coomer

Over a virtual chat, we spoke to Cagney Coomer about her experiences in the lab, the classroom and the community centre, and why she thinks outreach and role models are vital to science.

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, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.