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Spatial and temporal expression of an Antennapedia/lac Z gene construct integrated into the endogenous Antennapedia gene of Drosophila melanogaster

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Summary

In order to study the regulation of spatial and temporal expression of the homeotic gene Antennapedia (Antp) in Drosophila melanogaster, we have constructed fusion genes which contain Antp sequences linked to the reporter gene lac Z of Escherichia coli. In one case of P-element transformation, a fusion gene construct integrated into the endogenous Antp gene close to one of the two promoters (P1). The spatial expression from the reporter gene in this transformant line, as analysed by the detection of β-galactosidase activity, was found to exactly mimic the normal expression from the P1 promoter of the Antp gene. We have used this unique transformant as a tool for studying the expression of the P1 promoter in embryonic, larval and adult development. Parallel lines transformed with the same fusion gene construct did not confer a correct P1 pattern of expression. The position in the genome was, therefore, crucial for the expression pattern of the reporter gene. Experiments aiming at the detection of autoregulatory control of Antp gene expression were designed. The results did not, however, support models of positive or negative autoregulation of P1 expression by Amp protein.

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References

  • Abbott MK, Kaufman TK (1986) The relationship between the functional complexity and the molecular organization of the Antennapedia locus of Drosophila melanogaster. Genetics 114:919–942

    Google Scholar 

  • Bermingham JJ, Scott MP (1988) Developmentally regulated alternative splicing of transcripts from the Drosophila homeotic gene Antennapedia can produce four different proteins. EMBO J 7:3211–3222

    Google Scholar 

  • Bermingham JJ, Martinez-Arias A, Petitt MG, Scott MP (1990) Different patterns of transcription from the two Antennapedia promoters during Drosophila embryogenesis. Development 109:553–566

    Google Scholar 

  • Bienz M, Tremml G (1988) Domain of Ultrabithorax expression in Drosophila visceral mesoderm from autoregulation and exclusion. Nature 333:576–578

    Google Scholar 

  • Boulet AM, Scott MP (1988) Control elements of the P2 promoter of the Antennapedia gene. Genes Dev 2:1600–1614

    Google Scholar 

  • Brower DL, Lawrence PA, Wilcox M (1981) Clonal analysis of the undifferentiated wing disk of Drosophila. Dev Biol 86:448–455

    Google Scholar 

  • Bryant PJ (1975) Pattern formation in the imaginal wing disc of Drosophila melanogaster. J Exp Zool 193:49–78

    Google Scholar 

  • Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin Heidelberg New York Tokyo

    Google Scholar 

  • Carroll SB, Laymon RA, McCutcheon MA, Riley PD, Scott MP (1986) The localization and regulation of Antennapedia protein expression in Drosophila melanogaster. Cell 47:113–122

    Google Scholar 

  • Cohen SM, Jürgens G (1989a) Proximal-distal pattern formation in Drosophila cell autonomous requirement for Distal-less gene activity in limb development. EMBO J 8:2045–2055

    Google Scholar 

  • Cohen SM, Jürgens G (1989b) Proximal-distal pattern formation in Drosophila: graded requirement for Distal-less gene activity during limb development. Roux's Arch Dev Biol 198:157–169

    Google Scholar 

  • Cohen SM, Brönner G, Kilttner F, Jürgens G, Jäckle H (1989) Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature 338:432–434

    Google Scholar 

  • Duncan I (1987) The Bithorax Complex. Ann Rev Genet 21:285–320

    Google Scholar 

  • Engels WR (1988) P-elements in Drosophila. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington, pp 437–484

    Google Scholar 

  • Frischer LE, Hagen FS, Garber RL (1986) An inversion that disrupts the Antennapedia gene causes abnormal structure and localization of RNAs. Cell 47:1017–1023

    Google Scholar 

  • Garber RL, Kuroiwa A, Gehring WJ (1983) Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J 2:2027–2036

    Google Scholar 

  • Gehring WJ (1987) Homeoboxes in the study of development. Science 236:1245–1252

    Google Scholar 

  • Gehring WJ, Hiromi Y (1986) Homeotic genes and the homeobox. Ann Rev Genet 20:147–173

    Google Scholar 

  • Gibson G, Gehring WJ (1988) Head and thoracic transformations caused by ectopic expression of Antennapedia during Drosophila development. Development 102:657–675

    Google Scholar 

  • Hafen E, Levine M (1986) The localization of RNAs in Drosophila tissue sections by in situ hybridization. In: Roberts DB (ed) Drosophila: A practical approach. IRL Press, pp 138–158

  • Hafen E, Levine M, Gehring WJ (1984) Regulation of Antennapedia transcript distribution by the bithorax complex in Drosophila. Nature 307:287–289

    Google Scholar 

  • Hama C, Ali Z, Kornberg TB (1990) Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev 4:1079–1093

    Google Scholar 

  • Hiromi Y, Gehring WJ (1987) Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell 50:963–974

    Google Scholar 

  • Hiromi Y, Kuroiwa A, Gehring WJ (1985) Control elements of the Drosophila segmentation gene fushi tarazu. Cell 43:603–614

    Google Scholar 

  • Ingham PW (1988) The molecular genetics of embryonic pattern formation in Drosophila. Nature 335:25–34

    Google Scholar 

  • Ingham PW, Martinez-Arias A (1986) The correct activation of Antennapedia and bithorax complex genes requires the fushi tarazu gene. Nature 324:592–597

    Google Scholar 

  • Irish VF, Martinez-Arias A, Akam M (1989) Spatial regulation of the Antennapedia and Ultrabithorax homeotic genes during Drosophila early development. EMBO J 8:1527–1537

    Google Scholar 

  • Johnson PF, McKnight PF (1989) Eukaryotic transcriptional regulatory proteins. Ann Rev Biochem 58:799–839

    Google Scholar 

  • Jorgensen EM, Garber RL (1987) Function and misfunction of the two promoters of the Drosophila Antennapedia gene. Genes Dev 1:544–555

    Google Scholar 

  • Karess RE, Rubin GM (1984) Analysis of P transposable element functions in Drosophila. Cell 38:135–146

    Google Scholar 

  • Kankel DR, Ferrus A, Garen SH, Harte PJ, Lewis PE (1980) The structure and development of the nervous system. In: Ashburner M, Wright TRF (eds) The genetics and biology of Drosophila. (Vol 2d). Academic Press, London, pp 295–368

    Google Scholar 

  • Kaufman TC, Lewis R, Wakimoto B (1980) Cytogenetic analysis of chromosome 3 in Drosophila melanogaster: the homoeotic gene complex in polytene chromosome interval 84A,B. Genetics 94:115–133

    Google Scholar 

  • Knipple DC, McIntyre RJ (1984) Cytogenetic mapping and isolation of mutants of the β-Gal-1 locus of Drosophila melanogaster. Mol Gen Genet 198:75–83

    Google Scholar 

  • Kuziora MA, McGinnis W (1988) Autoregulation of a Drosophila homeotic selector gene. Cell 55:477–485

    Google Scholar 

  • Laughon A, Boulet AM, Bermingham JR, Laymon RA, Scott MP (1986) Structure of transcripts from the homeotic Antennapedia gene of Drosophila melanogaster: Two promoters control the major protein-coding region. Mol Cell Biol 6:4676–4689

    Google Scholar 

  • Levine M, Hafen E, Garber RL, Gehring WJ (1983) Spatial distribution of Antennapedia transcripts during Drosophila development. EMBO J 2:2037–2046

    Google Scholar 

  • Lewis EB (1978) A gene complex controlling segmentation. Nature 276:565–570

    Google Scholar 

  • Lindsley D, Grell E (1968) Genetic variations of Drosophila melanogaster. Carnegie Inst Washington Publ 627

  • Martinez-Arias A (1986) The Antennapedia gene is required and expressed in parasegments 4 and 5 of the Drosophila embryo. EMBO J 5:135–141

    Google Scholar 

  • Merriam J (1991) Published electronically on the Internet, available via anonymous ftp from ftp.bio.indiana.edu. in the directory archive/fly/P-by-location

  • Merriam J (1991) Drosophila information from the network: Genmaps database; P-by-location

  • Miller A (1965) The internal anatomy and histology of the imago of Drosophila melanogaster. In: Demerec M (ed) Biology of Drosophila. Hafner Publishing Company, New York London, pp 420–531

    Google Scholar 

  • Milner MJ, Bleasby AJ, Kelly SL (1984) The role of the peripodial membrane of leg and wing imaginal discs of Drosophila melanogaster during evagination and differentiation in vitro. Roux's Arch Dev Biol 193:180–186

    Google Scholar 

  • Nayak SV, Singh RN (1983) Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 12:273–291

    Google Scholar 

  • O'Kane CJ, Gehring WJ (1987) Detection in situ of genomic regulatory elements in Drosophila. Proc Natl Acad Sci USA 84:9123–9127

    Google Scholar 

  • Okamoto H, Hiromi Y, Ishikawa E, Yamada T, Isoda K, Mackawa H, Hotta Y (1986) Molecular characterization of mutant actin genes which induce heat-shock proteins in Drosophila flight muscles. EMBO J 5:589–596

    Google Scholar 

  • Otting G, Qian YQ, Billeter M, Müller M, Affolter M, Gehring WJ, Wütrich K (1990) Protein-DNA contacts in the structure of a homeodomain-DNA complex determined by nuclear magnetic resonance spectroscopy in solution. EMBO J 9:3085–3092

    Google Scholar 

  • Paro R (1990) Imprinting a determined state into the chromatin of Drosophila. Trend Genet 6:416–421

    Google Scholar 

  • Reuter R, Scott MP (1990) Expression and function of the homoeotic genes Antennapedia and Sex combs reduced in the embryonic midgut of Drosophila. Development 109:289–303

    Google Scholar 

  • Rubin GM, Spradling AC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218:348–353

    Google Scholar 

  • Rubin GM, Spradling AC (1983) Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res 11:6341–6351

    Google Scholar 

  • Schedl P, Artavanis-Tsakonas S, Steward R, Gehring WJ, Mirault M-E, Goldschmidt-Clermont M, Moran L, Tissières A (1978) Two hybrid plasmids with D. melanogaster DNA sequences complementary to mRNA coding for the major heat shock protein. Cell 14:921–929

    Google Scholar 

  • Schneuwly S, Kuroiwa A, Baumgartner P, Gehring WJ (1986) Structural organization and sequence of the homeotic gene Antennapedia of Drosophila melanogaster. EMBO J 5:733–740

    Google Scholar 

  • Schneuwly S, Klemenz R, Gehring WJ (1987a) Redesigning the body plan of Drosophila by ectopic expression of the homoeotic gene Antennapedia. Nature 325:816–818

    Google Scholar 

  • Schneuwly S, Kuroiwa A, Gehring WJ (1987b) Molecular analysis of the dominant homeotic Antennapedia phenotype. EMBO J 6:201–206

    Google Scholar 

  • Scott MP, Tamkun JW, Hartzell GW (1989) The structure and function of the homeodomain. BBA Rev Cancer 989:25–48

    Google Scholar 

  • Scott MP, Weiner AJ, Hazelrigg TI, Polisky BA, Pirrotta V, Scalenghe F, Kaufman TC (1983) The molecular organization of the Antennapedia locus of Drosophila. Cell 35:763–766

    Google Scholar 

  • Shapira SK, Chou J, Richaud FV, Casadaban MJ (1983) New versatile plasmid vectors for the expression of hybrid proteins coded by a cloned gene fused to lacZ gene sequences encoding an enzymatically active carboxy-terminal portion of β-galactosidase. Gene 25:71–82

    Google Scholar 

  • Simon JA, Sutton CA, Lobell RB, Glaser RL, Lis JT (1985) Determinants of heat shock-induced chromosome puffing. Cell 40:805–817

    Google Scholar 

  • Steller H, Fischbach K-F, Rubin GM (1987) disconnected: A locus required for neuronal pathway formation in the visual system of Drosophila. Cell 50:1139–1153

    Google Scholar 

  • Stocker RF, Schorderet M (1981) Cobalt filling of sensory projections from internal and external mouthparts in Drosophila. Cell Tissue Res 216:513–523

    Google Scholar 

  • Stroeher VL, Jorgensen EM, Garber RL (1986) Multiple transcripts from the Antennapedia gene of Drosophila melanogaster. Mol Cell Biol 6:4667–4675

    Google Scholar 

  • Wirz J, Fessler LI, Gehring WJ (1986) Localization of the Antennapedia protein in Drosophila embryos and imaginal discs. EMBO J 5:3327–3334

    Google Scholar 

  • Zink B, Engström Y, Gehring WJ, Paro R (1991) Direct interaction of the Polycomb protein with Antennapedia regulatory sequences in polytene chromosomes of Drosophila melanogaster. EMBO J 10:153–162

    Google Scholar 

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Authors and Affiliations

  1. Department of Molecular Biology, University of Stockholm, S-106 91, Stockholm, Sweden

    Ylva Engström

  2. Institut für Genetik und Mikrobiologie der Universität Würzburg, Röntgenring 11, D-8700, Würzburg, Germany

    Stephan Schneuwly

  3. Department of Cell Biology, Biozentrum, Klingelbergstrasse 70, CH-4056, Basel, Switzerland

    Walter Jakob Gehring

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  1. Ylva Engström
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  2. Stephan Schneuwly
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  3. Walter Jakob Gehring
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Engström, Y., Schneuwly, S. & Gehring, W.J. Spatial and temporal expression of an Antennapedia/lac Z gene construct integrated into the endogenous Antennapedia gene of Drosophila melanogaster . Roux's Arch Dev Biol 201, 65–80 (1992). https://doi.org/10.1007/BF00420417

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