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Genetics. Mar 1994; 136(3): 1025–1038.
PMCID: PMC1205860

Unusual Properties of Regulatory DNA from the Drosophila Engrailed Gene: Three ``pairing-Sensitive'' Sites within a 1.6-Kb Region


We have previously shown that a 2-kb fragment of engrailed DNA can suppress expression of a linked marker gene, white, in the P element vector CaSpeR. This suppression is dependent on the presence of two copies of engrailed DNA-containing P elements (P[en]) in proximity in the Drosophila genome (either in cis or in trans). In this study, the 2-kb fragment was dissected and found to contain three fragments of DNA which could mediate white suppression [called ``pairing-sensitive sites'' (PS)]. A PS site was also identified in regulatory DNA from the Drosophila escargot gene. The eye colors of six different P[en] insertions in the escargot gene suggest an interaction between P[en]-encoded and genome-encoded PS sites. I hypothesize that white gene expression from P[en] is repressed by the formation of a protein complex which is initiated at the engrailed PS sites and also requires interactions with flanking genomic DNA. Genes were sought which influence the function of PS sites. Mutations in some Polycomb and trithorax group genes were found to affect the eye color from some P[en] insertion sites. However, different mutations affected expression from different P[en] insertion sites and no one mutation was found to affect expression from all P[en] insertion sites examined. These results suggest that white expression from P[en] is not directly regulated by members of the Polycomb and trithorax group genes, but in some cases can be influenced by them. I propose that engrailed PS sites normally act to promote interactions between distantly located engrailed regulatory sites and the engrailed promoter.

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Selected References

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  • Bellen HJ, Vaessin H, Bier E, Kolodkin A, D'Evelyn D, Kooyer S, Jan YN. The Drosophila couch potato gene: an essential gene required for normal adult behavior. Genetics. 1992 Jun;131(2):365–375. [PMC free article] [PubMed]
  • Bier E, Vaessin H, Shepherd S, Lee K, McCall K, Barbel S, Ackerman L, Carretto R, Uemura T, Grell E, et al. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 1989 Sep;3(9):1273–1287. [PubMed]
  • Biggin MD, Bickel S, Benson M, Pirrotta V, Tjian R. Zeste encodes a sequence-specific transcription factor that activates the Ultrabithorax promoter in vitro. Cell. 1988 Jun 3;53(5):713–722. [PubMed]
  • Chen JD, Pirrotta V. Stepwise assembly of hyperaggregated forms of Drosophila zeste mutant protein suppresses white gene expression in vivo. EMBO J. 1993 May;12(5):2061–2073. [PMC free article] [PubMed]
  • Chung JH, Whiteley M, Felsenfeld G. A 5' element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell. 1993 Aug 13;74(3):505–514. [PubMed]
  • DeCamillis M, Cheng NS, Pierre D, Brock HW. The polyhomeotic gene of Drosophila encodes a chromatin protein that shares polytene chromosome-binding sites with Polycomb. Genes Dev. 1992 Feb;6(2):223–232. [PubMed]
  • Gubb D, Roote J, McGill S, Shelton M, Ashburner M. Interactions between WHITE Genes Carried by a Large Transposing Element and the ZESTE Allele in DROSOPHILA MELANOGASTER. Genetics. 1986 Mar;112(3):551–575. [PMC free article] [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]
  • Hayashi S, Hirose S, Metcalfe T, Shirras AD. Control of imaginal cell development by the escargot gene of Drosophila. Development. 1993 May;118(1):105–115. [PubMed]
  • Hazelrigg T, Levis R, Rubin GM. Transformation of white locus DNA in drosophila: dosage compensation, zeste interaction, and position effects. Cell. 1984 Feb;36(2):469–481. [PubMed]
  • Hazelrigg T, Petersen S. An unusual genomic position effect on Drosophila white gene expression: pairing dependence, interactions with zeste, and molecular analysis of revertants. Genetics. 1992 Jan;130(1):125–138. [PMC free article] [PubMed]
  • Karess RE, Rubin GM. Analysis of P transposable element functions in Drosophila. Cell. 1984 Aug;38(1):135–146. [PubMed]
  • Kassis JA. Spatial and temporal control elements of the Drosophila engrailed gene. Genes Dev. 1990 Mar;4(3):433–443. [PubMed]
  • Kassis JA, VanSickle EP, Sensabaugh SM. A fragment of engrailed regulatory DNA can mediate transvection of the white gene in Drosophila. Genetics. 1991 Aug;128(4):751–761. [PMC free article] [PubMed]
  • Kennison JA. Transcriptional activation of Drosophila homeotic genes from distant regulatory elements. Trends Genet. 1993 Mar;9(3):75–79. [PubMed]
  • Kennison JA, Tamkun JW. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8136–8140. [PMC free article] [PubMed]
  • Kuner JM, Nakanishi M, Ali Z, Drees B, Gustavson E, Theis J, Kauvar L, Kornberg T, O'Farrell PH. Molecular cloning of engrailed: a gene involved in the development of pattern in Drosophila melanogaster. Cell. 1985 Aug;42(1):309–316. [PMC free article] [PubMed]
  • Laney JD, Biggin MD. zeste, a nonessential gene, potently activates Ultrabithorax transcription in the Drosophila embryo. Genes Dev. 1992 Aug;6(8):1531–1541. [PubMed]
  • Mansukhani A, Crickmore A, Sherwood PW, Goldberg ML. DNA-binding properties of the Drosophila melanogaster zeste gene product. Mol Cell Biol. 1988 Feb;8(2):615–623. [PMC free article] [PubMed]
  • Moazed D, O'Farrell PH. Maintenance of the engrailed expression pattern by Polycomb group genes in Drosophila. Development. 1992 Nov;116(3):805–810. [PMC free article] [PubMed]
  • Müller HP, Schaffner W. Transcriptional enhancers can act in trans. Trends Genet. 1990 Sep;6(9):300–304. [PubMed]
  • Pirrotta V. Vectors for P-mediated transformation in Drosophila. Biotechnology. 1988;10:437–456. [PubMed]
  • Pirrotta V. Transvection and long-distance gene regulation. Bioessays. 1990 Sep;12(9):409–414. [PubMed]
  • Pirrotta V. The genetics and molecular biology of zeste in Drosophila melanogaster. Adv Genet. 1991;29:301–348. [PubMed]
  • Rastelli L, Chan CS, Pirrotta V. Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function. EMBO J. 1993 Apr;12(4):1513–1522. [PMC free article] [PubMed]
  • Robertson HM, Preston CR, Phillis RW, Johnson-Schlitz DM, Benz WK, Engels WR. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. [PMC free article] [PubMed]
  • Simon JA, Lis JT. A germline transformation analysis reveals flexibility in the organization of heat shock consensus elements. Nucleic Acids Res. 1987 Apr 10;15(7):2971–2988. [PMC free article] [PubMed]
  • Thummel CS, Boulet AM, Lipshitz HD. Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene. 1988 Dec 30;74(2):445–456. [PubMed]
  • Whiteley M, Noguchi PD, Sensabaugh SM, Odenwald WF, Kassis JA. The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes. Mech Dev. 1992 Feb;36(3):117–127. [PubMed]
  • Wu CT. Transvection, nuclear structure, and chromatin proteins. J Cell Biol. 1993 Feb;120(3):587–590. [PMC free article] [PubMed]
  • Wu CT, Goldberg ML. The Drosophila zeste gene and transvection. Trends Genet. 1989 Jun;5(6):189–194. [PubMed]
  • Wu CT, Jones RS, Lasko PF, Gelbart WM. Homeosis and the interaction of zeste and white in Drosophila. Mol Gen Genet. 1989 Sep;218(3):559–564. [PubMed]
  • Zink B, Paro R. In vivo binding pattern of a trans-regulator of homoeotic genes in Drosophila melanogaster. Nature. 1989 Feb 2;337(6206):468–471. [PubMed]

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