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Genetics. Mar 1996; 142(3): 893–906.
PMCID: PMC1207026

The Drosophila Engrailed and Invected Genes: Partners in Regulation, Expression and Function

Abstract

We isolated and characterized numerous engrailed and invected alleles. Among the deficiencies we isolated, a mutant lacking invected sequences was viable and phenotypically normal, a mutant lacking engrailed was an embryo lethal and had slight segmentation defects, and a mutant lacking both engrailed and invected was most severely affected. In seven engrailed alleles, mutations caused translation to terminate prematurely in the central or C-terminal portion of the coding sequence, resulting in embryonic lethality and segmentation defects. Both engrailed and invected expression declined prematurely in these mutant embryos. In wild-type embryos, engrailed and invected are juxtaposed and are expressed in essentially identical patterns. A breakpoint mutant that separates the engrailed and invected transcription units parceled different aspects of the expression pattern to engrailed or invected. We also found that both genes cause similar defects when expressed ectopically and that the protein products of both genes act to repress transcription in cultured cells. We propose that the varied phenotypes of the engrailed alleles can be explained by the differential effects these mutants have on the combination of engrailed and invected activities, that engrailed and invected share a regulatory region, and that they encode redundant functions.

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Selected References

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  • Atkins JF, Weiss RB, Gesteland RF. Ribosome gymnastics--degree of difficulty 9.5, style 10.0. Cell. 1990 Aug 10;62(3):413–423. [PubMed]
  • Baumgartner S, Bopp D, Burri M, Noll M. Structure of two genes at the gooseberry locus related to the paired gene and their spatial expression during Drosophila embryogenesis. Genes Dev. 1987 Dec;1(10):1247–1267. [PubMed]
  • Busturia A, Morata G. Ectopic expression of homeotic genes caused by the elimination of the Polycomb gene in Drosophila imaginal epidermis. Development. 1988 Dec;104(4):713–720. [PubMed]
  • Cadigan KM, Grossniklaus U, Gehring WJ. Functional redundancy: the respective roles of the two sloppy paired genes in Drosophila segmentation. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6324–6328. [PMC free article] [PubMed]
  • Coleman KG, Poole SJ, Weir MP, Soeller WC, Kornberg T. The invected gene of Drosophila: sequence analysis and expression studies reveal a close kinship to the engrailed gene. Genes Dev. 1987 Mar;1(1):19–28. [PubMed]
  • Dente L, Cesareni G, Cortese R. pEMBL: a new family of single stranded plasmids. Nucleic Acids Res. 1983 Mar 25;11(6):1645–1655. [PMC free article] [PubMed]
  • Eaton S, Kornberg TB. Repression of ci-D in posterior compartments of Drosophila by engrailed. Genes Dev. 1990 Jun;4(6):1068–1077. [PubMed]
  • Goldsborough AS, Kornberg TB. Allele-specific quantification of Drosophila engrailed and invected transcripts. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12696–12700. [PMC free article] [PubMed]
  • González-Gaitán M, Rothe M, Wimmer EA, Taubert H, Jäckle H. Redundant functions of the genes knirps and knirps-related for the establishment of anterior Drosophila head structures. Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8567–8571. [PMC free article] [PubMed]
  • Grossniklaus U, Pearson RK, Gehring WJ. The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev. 1992 Jun;6(6):1030–1051. [PubMed]
  • Hama C, Ali Z, Kornberg TB. Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev. 1990 Jul;4(7):1079–1093. [PubMed]
  • Heemskerk J, DiNardo S, Kostriken R, O'Farrell PH. Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature. 1991 Aug 1;352(6334):404–410. [PMC free article] [PubMed]
  • Hopmann R, Duncan D, Duncan I. Transvection in the iab-5,6,7 region of the bithorax complex of Drosophila: homology independent interactions in trans. Genetics. 1995 Feb;139(2):815–833. [PMC free article] [PubMed]
  • Hui CC, Matsuno K, Ueno K, Suzuki Y. Molecular characterization and silk gland expression of Bombyx engrailed and invected genes. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):167–171. [PMC free article] [PubMed]
  • Jaynes JB, O'Farrell PH. Active repression of transcription by the engrailed homeodomain protein. EMBO J. 1991 Jun;10(6):1427–1433. [PMC free article] [PubMed]
  • Karr TL, Ali Z, Drees B, Kornberg T. The engrailed locus of D. melanogaster provides an essential zygotic function in precellular embryos. Cell. 1985 Dec;43(3 Pt 2):591–601. [PubMed]
  • Kornberg T. Engrailed: a gene controlling compartment and segment formation in Drosophila. Proc Natl Acad Sci U S A. 1981 Feb;78(2):1095–1099. [PMC free article] [PubMed]
  • Krasnow MA, Saffman EE, Kornfeld K, Hogness DS. Transcriptional activation and repression by Ultrabithorax proteins in cultured Drosophila cells. Cell. 1989 Jun 16;57(6):1031–1043. [PubMed]
  • Lawrence PA, Morata G. Compartments in the wing of Drosophila: a study of the engrailed gene. Dev Biol. 1976 Jun;50(2):321–337. [PubMed]
  • Lawrence PA, Struhl G. Further studies of the engrailed phenotype in Drosophila. EMBO J. 1982;1(7):827–833. [PMC free article] [PubMed]
  • Li X, Noll M. Evolution of distinct developmental functions of three Drosophila genes by acquisition of different cis-regulatory regions. Nature. 1994 Jan 6;367(6458):83–87. [PubMed]
  • Patel NH, Martin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Kornberg TB, Goodman CS. Expression of engrailed proteins in arthropods, annelids, and chordates. Cell. 1989 Sep 8;58(5):955–968. [PubMed]
  • Poole SJ, Kauvar LM, Drees B, Kornberg T. The engrailed locus of Drosophila: structural analysis of an embryonic transcript. Cell. 1985 Jan;40(1):37–43. [PubMed]
  • Poole SJ, Kornberg TB. Modifying expression of the engrailed gene of Drosophila melanogaster. Development. 1988;104 (Suppl):85–93. [PubMed]
  • Rothe M, Nauber U, Jäckle H. Three hormone receptor-like Drosophila genes encode an identical DNA-binding finger. EMBO J. 1989 Oct;8(10):3087–3094. [PMC free article] [PubMed]
  • Rothe M, Pehl M, Taubert H, Jäckle H. Loss of gene function through rapid mitotic cycles in the Drosophila embryo. Nature. 1992 Sep 10;359(6391):156–159. [PubMed]
  • Ruden DM, Jäckle H. Mitotic delay dependent survival identifies components of cell cycle control in the Drosophila blastoderm. Development. 1995 Jan;121(1):63–73. [PubMed]
  • Rushlow C, Doyle H, Hoey T, Levine M. Molecular characterization of the zerknüllt region of the Antennapedia gene complex in Drosophila. Genes Dev. 1987 Dec;1(10):1268–1279. [PubMed]
  • Schwartz C, Locke J, Nishida C, Kornberg TB. Analysis of cubitus interruptus regulation in Drosophila embryos and imaginal disks. Development. 1995 Jun;121(6):1625–1635. [PubMed]
  • Serrano N, Brock HW, Demeret C, Dura JM, Randsholt NB, Kornberg TB, Maschat F. polyhomeotic appears to be a target of engrailed regulation in Drosophila. Development. 1995 Jun;121(6):1691–1703. [PubMed]
  • Simmonds AJ, Brook WJ, Cohen SM, Bell JB. Distinguishable functions for engrailed and invected in anterior-posterior patterning in the Drosophila wing. Nature. 1995 Aug 3;376(6539):424–427. [PubMed]
  • Tabata T, Eaton S, Kornberg TB. The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev. 1992 Dec;6(12B):2635–2645. [PubMed]
  • Weir MP, Kornberg T. Patterns of engrailed and fushi tarazu transcripts reveal novel intermediate stages in Drosophila segmentation. Nature. 1985 Dec 5;318(6045):433–439. [PubMed]

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