Article
Full Access
Characterization of IMP-E3, A gene active during imaginal disc morphogenesis in Drosophila melanogaster
John T. Moore,
Dianne Fristrom,
Ann S. Hammonds,
James W. Fristrom,
John T. Moore
Division of Genetics, Department of Molecular and Cell Biology, University of California, Berkeley
Search for more papers by this authorDianne Fristrom
Division of Genetics, Department of Molecular and Cell Biology, University of California, Berkeley
Search for more papers by this authorAnn S. Hammonds
Division of Genetics, Department of Molecular and Cell Biology, University of California, Berkeley
Search for more papers by this authorCorresponding Author
James W. Fristrom
Division of Genetics, Department of Molecular and Cell Biology, University of California, Berkeley
589 Life Science Addition, University of California, Berkeley, CA 94720Search for more papers by this authorJohn T. Moore,
Dianne Fristrom,
Ann S. Hammonds,
James W. Fristrom,
John T. Moore
Division of Genetics, Department of Molecular and Cell Biology, University of California, Berkeley
Search for more papers by this authorDianne Fristrom
Division of Genetics, Department of Molecular and Cell Biology, University of California, Berkeley
Search for more papers by this authorAnn S. Hammonds
Division of Genetics, Department of Molecular and Cell Biology, University of California, Berkeley
Search for more papers by this authorCorresponding Author
James W. Fristrom
Division of Genetics, Department of Molecular and Cell Biology, University of California, Berkeley
589 Life Science Addition, University of California, Berkeley, CA 94720Search for more papers by this authorAbstract
The steroid hormone 20-hydroxyecdysone (20-HE) induces imcainol discs to form adult appendages in Drosophila. We have isolated a set of six ecdysone-responsive genes that apparently encode disc cell-surface or secreted proteins. Transcripts from one of these genes, IMP-E3, accumulate rapidly within 1–2 h in response to hormone. Developmentally,IMP-E3 transcripts reach maximum levels during the first stages of metamorphosis (white prepupae, WPP) and are primarily limited to imaginal tissues. Transcripts are also present during embryogenesis (0–3 h and 12–18 h). Two different-sized transcripts (1.2 and 1.4 kb) result from differential polyadenylation, with the larger transcript predominating in WPP. The conceptual IMP-E3 protein contains a signal peptide, an RGD sequence, and a potential glycosylphosphatidylinositol anchor. We speculate that the protein provides a transient cue important for imaginal disc morphogenesis.
References
- Barnes WM, Bevan M, Son PH (1983): Kilo-sequencing: Creation of an ordered nest of asymmetric deletions across a large target sequence carried on phage M13. Methods Enzymol 101: 98–122.
- Brawerman G (1989): mRNA Decay: Finding the Right Targets. Cell 57: 9, 10.
-
Chirgwin JM,
Przybyla AE,
MacDonald RJ,
Rutter WJ
(1979):
Isolation of biologically active nucleic acid from sources enriched in ribonucleases.
Biochemistry
24: 5294–5299.
10.1021/bi00591a005 Google Scholar
- Condic ML, Firstrom D, Fristrom JW: Atical cell shape changes during Drosophila imaginal leg disc elongation: A novel morphogenetic mechanism. Submitted.
- Cox KH, DeLeon DV, Angerer L, Angerer RC (1984): Detection of mRNAs in sea urchin embryos by in situ hybridization using asymmetric RNA probes. Dev Biol 101: 485–502.
- Demerec M (1950): “ The Biology of Drosophila.” New York: John Wiley and Sons.
- Denhardt DT (1966): A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun 23: 641–646.
- Edelman GM (1986): Cell adhesion molecules in the regulation of animal form and tissue pattern. Annu Rev Cell Biol 2: 81–116.
-
Eugene OE,
Yund MA,
Fristrom JW
(1979):
Preparative isolation and short-term organ culture of imaginal discs of Drosophila melanogaster.
Tissue Cult Assoc Man
5: 1055–1062.
10.1007/BF00919788 Google Scholar
- Fechtel K, Fristrom DK, Fristrom JW (1989): Prepupal differentiation in Drosophila: distinct cell types elaborate a shared structure, the pupal cuticle, but accumulate transcripts in unique patterns. Development 106: 649–656.
- Ferguson MAJ, Williams AF (1988): Cell-surface anchoring of proteins via glycosylphosphatidylinositol structures. Annu Rev Biochem 57: 285–320.
- Fristrom DK (1976): The mechanism of evagination of imaginal discs of Drosophila melanogaster. III Evidence for cell rearrangement. Dev Biol 54: 163–171.
- Fristrom D, Fristrom JW (1975): The mechanism of evagination of imaginal discs of Drosophila melanogaster I. General considerations. Dev Biol 43: 1–23.
- Fristrom JW, Doctor J, Fristrom D, Logan WR, Silvert DJ (1982): The formation of the pupal cuticle by Drosophila imaginal discs in vitro. Dev Biol 91: 337–350.
- Gough JA, Murray NE (1983): Sequence diversity among related genes for recognition of specific targets in DNA molecules. J Mol Biol 166: 1–19.
- Hafen E, Levine M, Garber RL, Gehring WJ (1983): An improved in situ hybridization method for the detection of cellular RNAs in Drosophila tissue sections and its application for localizing transcripts of the homeotic Antennopedia gene complex. EMBO J 2: 617–623.
- Hodgetts RB, Sage B, O'Connor JD (1977): Ecdysone titers during post-embryonic development of Drosophila melanogaster. Dev Biol 60: 310–317.
- Hynes RO (1987): Integrins: a family of cell surface receptors. Cell 48: 549–554.
- Lehrach H, Diamond D, Wozney JM, Boedtker H (1977): RNA molecular weight determinations by gel electrophoresis using denaturing conditions: A critical re-examination. Biochemistry 16: 4743–4751.
- Leptin M, Boghart T, Lahmann R, Wilcox M (1989): The function of PS integrins during Drosophila morphogenesis. Cell 56: 401–408.
- Maniatis T, Fritsch EF, Sambrook J (1982): “ Molecular Cloning: A Laboratory Manual.” Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
- Maroy P, Dennis R, Beckers C, Sage BA, O'Connor JD (1978): Demonstration of an ecdysteroid receptor in a cultured cell line of Drosophila melanogaster. Proc Natl Acad Sci USA 75: 6035–6038.
- Maruyama T, Gojobori T, Aota S, Ikemura T (1986): Codon usage tabulated from Genbank genetic sequence data. Nucleic Acids Res [Suppl] 14: 151–197.
- Melton DA, Kreig PA, Rebagliati MR, Maniatis T, Zinn K, Green MR (1984): Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res 12: 7035–7056.
- Messing J (1983): New M13 vectors for cloning. Methods Enzymol 101: 21–99.
- Milner MJ, Bleaseby AJ, Pyott O (1983): The role of the peripodial membrane in the morphogenesis of the eye-antennal disc of Drosophila melanogaster. Wilhelm Rouxs Arch 192: 164–170.
- Milner MJ, Bleaseby AJ, Pyott O (1984): Cell interactions during the fusion in vitro of Drosophila eye-antennal discs. Wilhelm's Rouxs Arch 193: 406–413.
- Mizusawa S, Nishimura S, Seela F (1986): Improvement of the dideoxy chain termination method of DNA sequencing by use of deoxy-7-deazaguanosine triphosphate in place ofdGTP. Nucleic. Acids Res 14: 1319–1324.
- Natzle JE, McCarthy BJ (1984): Regulation of Drosophila α and β-tubulin genes during development. Dev Biol 104: 187–198.
- Natzle JE, Hammonds AS, Fristrom JW (1986): Isolation of genes active during hormone-induced morphogenesis in Drosophila imaginal discs. J Biol Chem 261: 5575–5588.
- Natzle JE, Fristrom JW, Fristrom DK, Moore JT, Osterbur D, Paine-Saunders S, Withers D (1987): Properties of genes expressed during ecdysone-induced imaginal disc morphogenesis in Drosophila Imaginal discs. Monsanto-UCLA Symposium, Molecular Entomology, pp 151–164.
- Natzle JE, Fristrom DK, Fristrom JW (1988): Genes expressed during imaginal disc morphogenesis: IMP-E1, a gene associated with epithelial cell rearrangement. Dev Biol 129: 428–438.
- Osterbur DL, Fristrom DK, Natzle JE, Tojo SJ, Fristrom JW (1988): Genes expressed during imaginal disc morphogenesis: IMP-L2, a gene expressed during imaginal disc and imaginal histoblast morphogenesis. Dev Biol 129: 439–448.
- Perlman D, Halvorson HO (1983): A putative signal peptidase recognition site and sequence in eucaryotic and procarytoic signal peptides. J Mol Biol 167: 391–409.
- Pirrotta V, Manet E, Hardon E, Bickel SE, Benson M (1987): Structure and sequence of the Drosophila zeste gene. EMBO J 6: 791–9.
- Ready DF, Hanson TE, and Benzer S (1976): Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53: 217–240.
- Rickoll WL, Fristrom JW (1983): The effects of 20-hydroxyecdysone on the metabolic labeling of membrane proteins in Drosophila imaginal discs. Dev Biol 95: 275–287.
- Robb J (1969): Maintenance of imaginal discs of Drosophila melanogaster in chemically defined media. J Cell Biol 41: 876–884.
- Ruoslahti E, Pierschbacher MD (1986): Arg-Gly-Asp: A versatile cell recognition signal. Cell 44: 517, 518.
- Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KM, Ehrlich HA (1988): Primer directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491.
- Sanger F, Nicklen S, Coulsen AR (1977): DNA sequencing with chainterminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467.
- Shaw G, Kamen R (1986): A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46: 659–667.
- Takeichi M (1988): The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102: 639–655.
- Tomlinson A (1985): The cellular dynamics of pattern formation in the eye of Drosophila. J Embryol Exp Morphol 89: 313–331.
- von Heinje G (1985): Signal sequences: the limits of variation. J Mol Biol 184: 99–105.
- Yund MA, King DS, Fristrom JW (1978): Ecdysteroid receptors in imaginal discs of Drosophila melanogaster. Proc Natl Acad Sci USA 75: 6039–6043.
