Identification of engrailed promoter elements essential for interactions with a stripe enhancer in Drosophila embryos

Minako, Orihara; Hosono, Chie; Kojima, Takao; Saigo, Kaoru

doi:10.1046/j.1365-2443.1999.00254.x

Cited by 15 publications

(13 citation statements)

References 67 publications

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“…42 The GAF sites in the engrailed promoter are essential for enhancer-dependent activation. 43 The stage-specific activity of GAF is supported by the observation that the eve promoter in embryos possesses intrinsic insulator properties that are critically dependent on GAF function. 44 In all these cases, however, GAF may well play only an auxiliary role by facilitating the binding of other transcription factors involved in the above activities.…”

Section: Discussionmentioning

confidence: 99%

Drosophila BTB/POZ Domains of “ttk Group” Can Form Multimers and Selectively Interact with Each Other

Bonchuk

Denisov

Georgiev

et al. 2011

Journal of Molecular Biology

103

109

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Edited by M. GottesmanKeywords: GAGA; BTB domain; Mod(mdg4); CP190; chromatin insulatorThe BTB (bric-a-brac, tramtrack and broad complex)/POZ (poxvirus and zinc finger) domain is a conserved protein-protein interaction motif contained in a variety of transcription factors involved in development, chromatin remodeling, insulator activity, and carcinogenesis. All wellstudied mammalian BTB domains form obligate homodimers and, rarely, tetramers. Only the BTB domain of the Drosophila GAGA factor (GAF) has been shown to exist as higher-order multimers. The BTB domain of GAF belongs to the "ttk group" that contains several highly conserved sequences not found in other BTB domains. Here, we have shown by size-exclusion chromatography, chemical cross-linking, and nondenaturing PAGE that four additional BTB domains of the ttk group-Batman, Mod(mdg4), Pipsqueak, and Tramtrack-can form multimers, like GAF. Interestingly, the BTB domains of GAF and Batman have formed a wide range of complexes and interacted in the yeast two-hybrid assay with other BTB domains tested. In contrast, the BTB domains of Mod(mdg4), Pipsqueak, and Tramtrack have formed stable high-order multimer complexes and failed to interact with each other. The BTB domain of Drosophila CP190 protein does not belong to the ttk group. This BTB domain has formed stable dimers and has not interacted with domains of the ttk group. Previously, it was suggested that GAF oligomerization into higher-order complexes facilitates long-range activation by providing a protein bridge between an enhancer and a promoter. Unexpectedly, experiments in the Drosophila model system have not supported the role of GAF in organization of longdistance interaction between the yeast GAL4 activator and the white promoter.© 2011 Elsevier Ltd. All rights reserved. IntroductionThe BTB (bric-a-brac, tramtrack and broad complex) domain [also known as the POZ (poxvirus and zinc finger) domain] is a versatile protein-protein interaction motif that participates in a wide range of cellular functions, including transcription regulation (for review, see Ref. 1 ). Transcription factors with a BTB domain at the N-terminus comprise a large important class of molecules involved in development and carcinogenesis. As shown in crystallographic studies,

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Section: Discussionmentioning

confidence: 99%

Drosophila BTB/POZ Domains of “ttk Group” Can Form Multimers and Selectively Interact with Each Other

Bonchuk

Denisov

Georgiev

et al. 2011

Journal of Molecular Biology

103

109

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“…Second, both promoters have binding sites for the transcription factor GAGA, which are located just upstream of the transcription start site. GAGA-binding sites greatly increase the activity of the en promoter (Orihara et al, 1999). Third, both have Polycomb response elements (PREs) located very close to the promoters (Nègre et al, 2006;DeVido et al, 2008) (Cunningham, Brown and Kassis, unpublished).…”

Section: Discussionmentioning

confidence: 99%

Enhancer-promoter communication at theDrosophila engrailedlocus

et al. 2009

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Enhancers are often located many tens of kilobases away from the promoter they regulate, sometimes residing closer to the promoter of a neighboring gene. How do they know which gene to activate? We have used homing P[en]constructs to study the enhancer-promoter communication at the engrailed locus. Here we show that engrailed enhancers can act over large distances, even skipping over other transcription units,choosing the engrailed promoter over those of neighboring genes. This specificity is achieved in at least three ways. First, early acting engrailed stripe enhancers exhibit promoter specificity. Second, a proximal promoter-tethering element is required for the action of the imaginal disc enhancer(s). Our data suggest that there are two partially redundant promoter-tethering elements. Third, the long-distance action of engrailed enhancers requires a combination of the engrailedpromoter and sequences within or closely linked to the promoter proximal Polycomb-group response elements. These data show that multiple mechanisms ensure proper enhancer-promoter communication at the Drosophila engrailed locus.

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“…Like the Mod(mdg4) proteins, GAGA factor is a group of BTB/POZ-containing trxG proteins that can also both aid activation and help insulate (44,45). GAGA factor binds proximal to several promoters and potentiates activation of the engrailed promoter by a distal enhancer (46). We speculate, as shown with the promoter on the right, that when BTB/POZ proteins such as GAGA bind just upstream of a promoter, they anchor activators close to the promoter and thereby aid activation.…”

Section: Discussionmentioning

confidence: 99%

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

Gause

Morcillo

Dorsett

2001

Molecular and Cellular Biology

123

126

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The Drosophila mod(mdg4) gene products counteract heterochromatin-mediated silencing of the white gene and help activate genes of the bithorax complex. They also regulate the insulator activity of the gypsy transposon when gypsy inserts between an enhancer and promoter. The Su(Hw) protein is required for gypsymediated insulation, and the Mod(mdg4)-67.2 protein binds to Su(Hw). The aim of this study was to determine whether Mod(mdg4)-67.2 is a coinsulator that helps Su(Hw) block enhancers or a facilitator of activation that is inhibited by Su(Hw). Here we provide evidence that Mod(mdg4)-67.2 acts as a coinsulator by showing that some loss-of-function mod(mdg4) mutations decrease enhancer blocking by a gypsy insert in the cut gene. We find that the C terminus of Mod(mdg4)-67.2 binds in vitro to a region of Su(Hw) that is required for insulation, while the N terminus mediates self-association. The N terminus of Mod(mdg4)-67.2 also interacts with the Chip protein, which facilitates activation of cut. Mod(mdg4)-67.2 truncated in the C terminus interferes in a dominant-negative fashion with insulation in cut but does not significantly affect heterochromatin-mediated silencing of white. We infer that multiple contacts between Su(Hw) and a Mod(mdg4)-67.2 multimer are required for insulation. We theorize that Mod(mdg4)-67.2 usually aids gene activation but can also act as a coinsulator by helping Su(Hw) trap facilitators of activation, such as the Chip protein.

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Identification of engrailed promoter elements essential for interactions with a stripe enhancer in Drosophila embryos

Cited by 15 publications

References 67 publications

Drosophila BTB/POZ Domains of “ttk Group” Can Form Multimers and Selectively Interact with Each Other

Drosophila BTB/POZ Domains of “ttk Group” Can Form Multimers and Selectively Interact with Each Other

Enhancer-promoter communication at theDrosophila engrailedlocus

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

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