Abstract
There is ample evidence that the enhancers of a promoterless yellow locus in one homologous chromosome can activate the yellow promoter in the other chromosome where the enhancers are inactive or deleted, which is indicative of a high specificity of the enhancer–promoter interaction in yellow. In this paper, we have found that the yellow sequence from −100 to −69 is essential for stimulation of the heterologous eve (TATA-containing) and white (TATA-less) promoters by the yellow enhancers from a distance. However, the presence of this sequence is not required when the yellow enhancers are directly fused to the heterologous promoters or are activated by the yeast GAL4 activator. Unexpectedly, the same promoter proximal region defines previously described promoter-specific, long-distance repression of the yellow promoter by the gypsy insulator on the mod(mdg4) u1 background. These finding suggest that proteins bound to the −100 to −69 sequence are essential for communication between the yellow promoter and upstream regulatory elements.
Similar content being viewed by others
References
Ashburner M (1989) Drosophila: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
Biessmann H, Mason JM (1988) Progressive loss of DNA sequences from terminal chromosome deficiencies in Drosophila melanogaster. EMBO J 7(4):1081–1086
Blackwood EM, Kadonaga JT (1998) Going the distance: a current view of enhancer action. Science 281:60–63
Bondarenko VA, Liu YV, Jiang YI, Studitsky VM (2003) Communication over a large distance: enhancers and insulators. Biochem Cell Biol 81:241–251
Brasset E, Vaury C (2005) Insulators are fundamental components of the eukaryotic genomes. Heredity 94:571–576
Buchner K, Roth P, Schotta G, Krauss V, Saumweber H, Reuter G, Dorn R (2000) Genetic and molecular complexity of the position effect variegation modifier mod(mdg4) in Drosophila. Genetics 155:141–157
Cai H, Levine M (1997) The gypsy insulator can function as a promoter-specific silencer in the Drosophila embryo. EMBO J 16:1732–1741
Calhoun VC, Levine M (2003) Long-range enhancer–promoter interactions in the Scr−Antp interval of the Drosophila Antennapedia complex. Proc Natl Acad Sci USA 100:9878–9883
Calhoun VC, Stathopoulos A, Levine M (2002) Promoter-proximal tethering elements regulate enhancer−promoter specificity in the Drosophila Antennapedia complex. Proc Natl Acad Sci USA 99:9243–9247
Capelson M, Corces VG (2004) Boundary elements and nuclear organization. Biol Cell 96:617–629
Carter D, Chakalova L, Osborne CS, Dai YF, Fraser P (2002) Long-range chromatin regulatory interactions in vivo. Nat Genet 32:623–626
Chambeyron S, Bickmore WA (2004) Does looping and clustering in the nucleus regulate gene expression? Curr Opin Cell Biol 16:256–262
Chen J-L, Huisinga KL, Viering MM, Ou SA, Wu C-T, Geyer PK (2002) Enhancer action in trans is permitted throughout the Drosophila genome. Proc Natl Acad Sci USA 95:3723–3728
De Laat W, Grosveld F (2003) Spatial organization of gene expression: the active chromatin hub. Chromosome Res 11:447–459
Dillon N, Sabbattini P (2000) Functional gene expression domains: defining functional unit of eukaryotic gene regulation. BioEssays 22:657–665
Dorsett D (1990) Potentiation of a polyadenylation site by a downstream protein DNA interaction. Proc Natl Acad Sci USA 87:4373–4377
Dorsett D (1999) Distant liaisons: long-range enhancer−promoter interactions in Drosophila. Curr Opin Genet Dev 9:505–514
Duncan IW (2002) Transvection effects Drosophila. Annu Rev Genet 36:521–556
Gause M, Morcillo P, Dorsett D (2001) Insulation of enhancer−promoter communication by a gypsy transposon insert in the Drosophila cut gene: cooperation between suppressor of Hairy-wing and modifier of mdg4 proteins. Mol Cell Biol 21:4807–4817
Gdula DA, Corces VG (1997) Characterization of functional domains of the su(Hw) protein that mediate the silencing effect of mod(mdg4) mutations. Genetics 145:153–161
Georgiev P, Kozycina M (1996) Interaction between mutations in the suppressor of Hairy wing and modifier of mdg4 genes of Drosophila melanogaster affecting the phenotype of gypsy-induced mutations. Genetics 142:425–436
Gerasimova TI, Gdula DA, Gerasimov DV, Simonova O, Corces VG (1995) A Drosophila protein that imparts directionality on a chromatin insulator is an enhancer of position-effect variegation. Cell 82:587–597
Geyer PK, Clark I (2002) Protecting against promiscuity: the regulatory role of insulators. Cell Mol Life Sci 59:2112–2127
Geyer PK, Corces VG (1987) Separate regulatory elements are responsible for the complex pattern of tissue-specific and developmental transcription of the yellow locus in Drosophila melanogaster. Genes Dev 1:996–1004
Geyer PK, Corces VG (1992) DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev 6:1865–1873
Geyer PK, Spana C, Corces VG (1986) On the molecular mechanism of gypsy-induced mutations at the yellow locus of Drosophila melanogaster. EMBO J 5:2657–2662
Geyer PK, Green MM, Corces VG (1990) Tissue-specific transcriptional enhancers may act in trans on the gene located in the homologous chromosome: the molecular basis of transvection in Drosophila. EMBO J 9:2247–2256
Ghosh D, Gerasimova TI, Corces VG (2001) Interactions between the Su(Hw) and Mod(mdg4) proteins required for gypsy insulator function. EMBO J 20:2518–2527
Golic KG, Lindquist S (1989) The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59:499–509
Golovnin A, Gause M, Georgieva S, Gracheva E, Georgiev P (1999) Su(Hw) insulator can disrupt enhancer–promoter interactions when located more than 20 kilobases away from the Drosophila achaete-scute complex. Mol Cell Biol 19:3443–3456
Golovnin A, Melnick E, Mazur A, Georgiev P (2005) Drosophila Su(Hw) insulator can stimulate transcription of a weakened yellow promoter over a distance. Genetics 170:1133–1142
Gomez-Skarmeta JL, Rodriguez I, Martinez C, Culi J, Ferres-Marco D, Beamonte D, Modolell J (1995) Cis-regulation of achaete and scute: shared enhancer-like elements drive their coexpression in proneural clusters of the imaginal discs. Genes Dev 9:1869–1882
Hagstrom K, Muller M, Schedl P (1996) Fab-7 functions as a chromatin domain boundary to ensure proper segment specification by the Drosophila bithorax complex. Genes Dev 10:3202–3215
Holdridge C, Dorsett D (1991) Repression of hsp70 heat shock gene transcription by the suppressor of Hairy-wing protein of Drosophila melanogaster. Mol Cell Biol 11:1894–1900
Kares RE, Rubin GM (1984) Analysis of P transposable element functions in Drosophila. Cell 38:135–146
Kennison JA, Southworth JW (2002) Transvection in Drosophila. Adv Genet 46:399–420
Kutach AK, Kadonaga JT (2000) The downstream promoter element DPE appears to be as widely used as the TATA box in Drosophila core promoters. Mol Cell Biol 20:4754–4764
Lagrange T, Kapanidis AN, Tang H, Reinberg D, Ebright RH (1998) New core promoter element in RNA polymerase II-dependent transcription: sequence-specific DNA binding by transcription factor IIB. Genes Dev 12:34–44
Lee A, Wu C-T (2006) Enhancer–promoter communication at the yellow gene in Drosophila melanogaster: diverse promoters participate in and regulate trans- interactions. Genetics 174:1867–1880
Levine M, Tjian R (2003) Transcription regulation and animal diversity. Nature 424:147–150
Lewis EB (1954) The theory and application of a new method of detecting chromosomal rearrangements in Drosophila melanogaster. Am Nat 88:225–239
Lindsley DL, Zimm GG (1992) The Genome of Drosophila melanogaster. Academic, New York
Macdonald PM, Ingham P, Struhl G (1986) Isolation, structure, and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeo box. Cell 47:721–734
Mahmoudi T, Katsani KR, Verrijzer CP (2002) GAGA can mediate enhancer function in trans by linking two separate DNA molecules. EMBO J 21:1775–1781
Martin M, Meng YB, Chia W (1989) Regulatory elements involved in the tissue-specific expression of the yellow gene of Drosophila. Mol Gen Genet 218:118–126
Martinez-Laborda A, Gonzales-Reyes A, Morata G (1992) Trans-regulation in the Ultrabithorax gene of Drosophila: alterations in the promoter enhance transvection. EMBO J 11:3645–3652
Merli C, Bergstrom DE, Cygan JA, Blackman RK (1996) Promoter specificity mediates the independent regulation of neighboring genes. Genes Dev 10:1260–1270
Morris JR, Chen J-L, Geyer PK, Wu C-T (1998) Two modes of transvection: enhancer action in trans and bypass of a chromatin insulator in cis. Proc Natl Acad Sci USA 95:10740–10745
Morris JR, Chen J-L, Filandrinos ST, Dunn RC, Fisk R, Geyer P, Wu C-T (1999a) An analysis of transvection at the yellow locus of Drosophila melanogaster. Genetics 151:633–651
Morris JR, Geyer PK, Wu C-T (1999b) Core promoter elements can regulate transcription on a separate chromosome in trans. Genes Dev 13:253–258
Morris JR, Petrov DA, Lee AM, Wu C-T (2004) Enahncer choice in cis and in trans in Drosophila melanogaster: role of the promoter. Genetics 167:1739–1747
Muravyova E, Golovnin A, Gracheva E, Parshikov A, Belenkaya T, Pirrotta V, Georgiev P (2001) Loss of insulator activity by paired Su(Hw) chromatin insulators. Science 291:495–498
Nash WG, Yarkin RJ (1974) Genetic regulation and pattern formation: a study of the yellow locus in Drosophila melanogaster. Genet Res 24:19–26
Pai CY, Lei EP, Ghosh D, Corces VG (2004) The centrosomal protein CP190 is a component of the gypsy chromatin insulator. Mol Cell 16:737–748
Parkhurst S, Corces VG (1986) Interactions among the gypsy element and the yellow and suppressor of Hairy-wing loci in Drosophila melanogaster. Mol Cell Biol 6:47–53
Patrinos GP, de Krom M, de Boer E, Langeveld A, Imam AM, Strouboulis J, de Laat W, Grosveld FG (2004) Multiple interactions between regulatory regions are required to stabilize an active chromatin hub. Genes Dev 18:1495–1509
Petrascheck M, Escher D, Mahmoudi T, Verrijzer CP, Schaffner W, Barberis A (2005) DNA looping induced by a transcriptional enhancer in vivo. Nucleic Acids Res 33:3743–3750
Pirrotta V (1999) Transvection and chromosomal trans-interaction effects. Biochim Biophys Acta 1424:M1–M8
Ptashne M, Gann A (2002) Genes and signals. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
Qian S, Varjavand B, Pirrotta V (1992) Molecular analysis of the zeste-white interaction reveals a promoter-proximal element essential for distant enhancer−promoter communication. Genetics 131:79–90
Rubin GM, Spradling AC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218:348–353
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
Savitsky M, Kahn T, Pomerantseva E, Georgiev P (2003) Transvection at the end of the truncated chromosome in Drosophila melanogaster. Genetics 163:1375–1387
Scott KS, Taubman AD, Geyer PK (1999) Enhancer blocking by the Drosophila gypsy insulator depends upon insulator anatomy and enhancer strength. Genetics 153:787–798
Sipos L, Gyurkovics H (2005) Long-distance interactions between enhancers and promoters. The case of the Abd-B domain of the Drosophila bithorax complex. FEBS J 272:3253–3259
Sipos L, Mihaly J, Karch F, Schedl P, Gausz J, Gyurkovics H (1998) Transvection in the Drosophila Abd-B domain: extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter. Genetics 149:1031–1050
Spana C, Corces VG (1990) DNA bending is a determinant of binding specificity for a Drosophila zinc finger protein. Genes Dev 4:1505–1515
Spradling AC, Rubin GM (1982) Transposition of cloned P elements into germline chromosomes. Science 218:341–347
Su W, Jackson S, Tjian R, Echols H (1991) DNA looping between sites for transcriptional activation: self-association of DNA-bound Sp1. Genes Dev 5:820–826
Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W (2002) Looping and interaction between hypersensitive sites in the active β-globin locus. Mol Cell 10:1453–1465
Vakoc CR, Letting DL, Gheldof N, Sawado T, Bender MA, Groudine M, Weiss MJ, Dekker J, Blobel GA (2005) Proximity among \distant regulatory elements at the β-globin locus requires GATA-1 and FOG-1. Mol Cell 17:453–462
Walter MF, Black BC, Afshar G, Kermabon AY, Wright TR, Biessmann H (1991) Temporal and spatial expression of the yellow gene in correlation with cuticle formation and dopa decarboxylase activity in Drosophila development. Dev Biol 147:32–45
West AG, Fraser P (2005) Remote control of gene transcription. Hum Mol Genet 14:R101–R111
West AG, Gaszner M, Felsenfeld G (2002) Insulators: many functions, many mechanisms. Genes Dev 16:271–288
Wu C-T, Morris JR (1999) Transvection and other homology effects. Curr Opin Genet Dev 9:237–246
Acknowledgement
We are grateful to C.-T. Wu and A. Lee for providing us with fly lines and for scientific collaboration. This study was supported by the Russian Foundation for Basic Research (project no. 06-04-48350), by Russian program for young scientists (project no. 15/2006–2009 to M.K.) and an International Research Scholar Award from the Howard Hughes Medical Institute (to P.G.).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E.A. Nigg
Rights and permissions
About this article
Cite this article
Melnikova, L., Kostuchenko, M., Silicheva, M. et al. Drosophila gypsy insulator and yellow enhancers regulate activity of yellow promoter through the same regulatory element. Chromosoma 117, 137–145 (2008). https://doi.org/10.1007/s00412-007-0132-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-007-0132-6