Structure of DRE, a retrotransposable element which integrates with position specificity upstream of Dictyostelium discoideum tRNA genes.

Marschalek, Rolf; Hofmann, Jörg; Schumann, Gerald G.; Gösseringer, R; Dingermann, Theodor

doi:10.1128/mcb.12.1.229

Cited by 37 publications

(40 citation statements)

References 32 publications

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“…Ty3 insertion occurs with a strong preference near the tRNA gene transcription initiation site (13,14), and it seems possible that this insertion preference developed because of a regulatory advantage conferred by the neighboring placement on the chromosome. A very similar close association with tRNA genes has been found for the DRE retrotransposons from Dictyostelium discoideum (69,70).…”

supporting

confidence: 51%

tRNA genes as transcriptional repressor elements.

Hull¹,

Erickson²,

Johnston³

et al. 1994

Mol. Cell. Biol.

120

129

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Eukaryotic genomes frequently contain large numbers of repetitive RNA polymerase III (pol III) promoter elements interspersed between and within RNA pol II transcription units, and in several instances a regulatory relationship between the two types of promoter has been postulated. In the budding yeast Saccharomyces cerevisiae, tRNA genes are the only known interspersed pol III promoter-containing repetitive elements, and we find that they strongly inhibit transcription from adjacent pol II promoters in vivo. This inhibition requires active transcription of the upstream tRNA gene but is independent of its orientation and appears not to involve simple steric blockage of the pol II upstream activator sites. Evidence is presented that different pol II promoters can be repressed by different tRNA genes placed upstream at varied distances in both orientations.To test whether this phenomenon functions in naturally occurring instances in which tRNA genes and pol II promoters are juxtaposed, we examined the sigma and Ty3 elements. This class of retrotransposons is always found integrated immediately upstream of different tRNA genes. Weakening tRNA gene transcription by means of a temperature-sensitive mutation in RNA pol III increases the pheromone-inducible expression of sigma and Ty3 elements up to 60-fold.Many eukaryotic genomes contain families of moderately to highly repeated DNA elements containing RNA polymerase III (pol III) promoters (reviewed in references 74 and 75). Frequently these elements resemble the intragenic pol III promoter class found in tRNA and 7SL RNA genes, which consist of consensus A-box and B-box sequences downstream from the transcription start sites. These elements can be found either dispersed as individual copies or as highly reiterated tandem copies, especially in heterochromatic regions. The pol III elements are not generally transcribed into stable RNA commensurate with their copy number in vivo, although they can usually be transcribed in vitro, and there are numerous reports of condition-specific or development-specific activation in vivo (10,27,61,90,95,97,101). Several hypotheses have been put forward regarding possible functions for these sequences, but one particularly interesting suggestion is that dispersed RNA pol III promoters might exert either a positive or negative influence on the transcriptional activity of overlapping or nearby RNA pol II promoters (11,12,15,89,90,96). In some cases, cryptic pol III promoter elements directly interfere with factor binding sites in the pol II promoter upstream region or with the pol II initiation site itself. In at least one report, however, repression was achieved by an Alu repetitive element, in which case there was no obvious steric overlap with the neighboring pol II promoter (96).In this report, the question of whether RNA pol III promoters can exert negative transcriptional regulation on neighboring DNA has been approached by studying the budding yeast Saccharomyces cerevisiae. Although this yeast does not appear to have any Alu-ty...

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supporting

confidence: 51%

tRNA genes as transcriptional repressor elements.

Hull¹,

Erickson²,

Johnston³

et al. 1994

Mol. Cell. Biol.

120

129

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“…They are characterized by the sequence and by the nucleotides of the prototype DRE (31 307 within the oligo(dA) stretch separating the A and B modules of the left TR, and it terminated at coordinate 5274 inside the B module of the 3' TR. This cDNA (clone a) ended with the DRE nucleotides ...AAAGAAAAA but contained no poly(A) tail, strongly suggesting that it was generated by oligo(dT) priming at an internal A-rich sequence (Fig.…”

Section: Methodsmentioning

confidence: 99%

“…Retrotransposable Dictyostelium repetitive elements (DREs) are present in approximately 150 to 200 copies in the genomes of different Dictyostelium discoideum strains (28)(29)(30)(31).…”

mentioning

confidence: 99%

Internally located and oppositely oriented polymerase II promoters direct convergent transcription of a LINE-like retroelement, the Dictyostelium repetitive element, from Dictyostelium discoideum.

Schumann¹,

Zündorf²,

Hofmann³

et al. 1994

Mol. Cell. Biol.

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The Dictyostelium discoideum NC4 genome harbors approximately 150 individual copies of a retrotransposable element called the Dictyostelium repetitive element (DRE). This element contains nonidentical terminal repeats (TRs) consisting of conserved building blocks A and B in the left TR and B and C in the right TR. Seven different-sized classes of RNA transcripts from these elements were resolved by Northern (RNA) blot analysis, but their combined abundance was very low. When D. discoideum cells were grown in the presence of the respiratory chain blocker antimycin A, steady-state concentrations of these RNA species increased 10-to 20-fold. The D. discoideum genome contains two DRE subtypes, the full-length 5.7-kb DREa and the internally deleted 2.4-kb DREb. Both subtypes are transcribed, as confirmed by analysis of cloned cDNA. Primary transcripts from the sense strand originate at nucleotide +1 and terminate at two dominant sites, located 21 or 28 nucleotides upstream from the 3' end of the elements. The activity of a reasonably strong polymerase II promoter in the 5'-terminal A module is slightly upregulated by the tRNA gene located 50 ± 4 nucleotides upstream and drastically reduced by the adjacent B module of the DRE. Transcripts from the opposite DNA strand (complementary-sense transcripts) were also detected, directed by an internally located polymerase II promoter residing within the C module. This latter transcription was initiated at multiple sites within the oligo(dA12) stretch which terminates DREs.Retrotransposable Dictyostelium repetitive elements (DREs) are present in approximately 150 to 200 copies in the genomes of different Dictyostelium discoideum strains (28-31).Most remarkably, this element always integrates at a distance of 50 ± 4 nucleotides upstream from tRNA genes but in the opposite transcriptional orientation. Upon integration, a 14 + 2-nucleotide target site duplication is created (29). The 5.7-kb DREs contain an internal coding portion with two open reading frames (ORFs) which is flanked by nonidentical terminal repeats (TRs) (see Fig. IA). These TRs are composed of three distinct modules, termed A, B, and C. The 5' TR consists of one or several A modules followed by a 290-bp B module which provides the AUG translation initiation codon. The 3' TR consists of a B module followed by a terminal C module.Approximately half of the DREs in NC4-derived strains show a variant organization (30). They are only 2.4 kb long and are termed DREbs, as opposed to the 5.7-kb DREas (Fig. IA). DREbs carry an extensive internal deletion encompassing nearly the entire ORF2. They also contain several small deletions within the right TR and a variant A module (termed Ab), which always differs from the Aa module of the 5.7-kb DREas by the same three distinct point mutations (30). A similar situation has been described for jockey elements of Drosophila melanogaster, which occur as full-size (5-kb) copies

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“…These include DRE I [1], a nonLTR retrotransposon from Dictyostelium discoideum, and the Tyl and Ty2 copialike and Ty3 gypsylike LTR retrotransposons from Saccharomyces cerevisiae (reviewed in [2]). DRE I elements are close to position -50 nt relative to tRNA gene sequence.…”

Section: Introductionmentioning

confidence: 99%

RNA polymerase III interferes with Ty3 integration

Connolly

Sandmeyer

1997

FEBS Letters

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Ty3, a gypsylike retrotransposon of budding yeast, integrates at the transcription initiation site of genes transcribed by RNA polymerase III (pol III). It was previously shown that integration in vitro requires intact promoter elements and the pol III transcription factors TFIIIB and TFIIIC. In order to test the effect of pol III on integration, increasing amounts of a pol Illcontaining fraction were added to Ty3 in vitro integration reactions. The pol Ill-containing fraction was inhibitory to integration. These results are consistent with a model where the Ty3 integration complex and pol III recognize similar features of the stable transcription complex and compete with each other for access to the transcription initiation site.

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Structure of DRE, a retrotransposable element which integrates with position specificity upstream of Dictyostelium discoideum tRNA genes.

Cited by 37 publications

References 32 publications

tRNA genes as transcriptional repressor elements.

tRNA genes as transcriptional repressor elements.

Internally located and oppositely oriented polymerase II promoters direct convergent transcription of a LINE-like retroelement, the Dictyostelium repetitive element, from Dictyostelium discoideum.

RNA polymerase III interferes with Ty3 integration

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