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Chapter 27 : Ty3, a Position-Specific, Gypsy-Like Element in Saccharomyces cerevisiae

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Abstract:

Ty3 is one of five types of long terminal repeat (LTR) retrotransposons (Ty1 to Ty5) in . These elements are classified in the family . The Ty elements of yeast provide useful model systems for understanding the retrovirus life cycle and the diversities of retroelement functions. The other LTR elements in are copialike elements in the genus . The similarity of Ty3 reverse transcriptase (RT) to retroviral RT, the nature of the minus- and plus-strand primer features, and the existence of minus- and plus-strand reverse transcription intermediates all argue that Ty3 replication is similar to that of retroviruses. In cells activated for Ty1 transposition, Ty3 insertions are readily detectable. These results argue that Ty3 insertion is highly specific for pol III-transcribed genes. One of the objectives of studying yeast retrotransposons is the identification of host factors that are involved in the life cycles of retroelements including retroviruses. Ty1 and Ty3 both rely on frameshifting for protein expression, but use distinct mechanisms. Development of varied and quantitative assays for transposition is facilitating use of the genomic resources in a high-throughput format. The combined use of these resources will make this an exciting time to realize the potential of the yeast elements as model systems for understanding the complex interactions between retroelements and their hosts.

Citation: Sandmeyer S, Aye M, Menees T. 2002. Ty3, a Position-Specific, Gypsy-Like Element in Saccharomyces cerevisiae, p 663-683. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch27

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Figure 1

The Ty3 life cycle. (A) Replication of the Ty3 element. The integrated Ty3 DNA is 5351 bp in length. The upstream and downstream LTRs are divided into repeat regions present at the 5′and 3′ends of the RNA (R) and regions present uniquely (downstream and upstream of R) at the 5′and 3′ends (U5 and U3, respectively). The RNA primes minus-strand reverse transcription from tRNA(i), which is predicted to bind to a 5′-3′bipartite split between the upstream and U3 regions of the transcript. The first template switch occurs so that the minus-strand strong stop anneals to the 3′end of the genomic RNA. Plus-strand reverse transcription is primed, after RNaseHcleavage at the end of the polypurine tract (PPT), just upstream of the U3 region and templated from the nascent minus-strand cDNA. A second template switch transfers the plus-strand strong-stop DNA to the 5′end of the genomic RNA. Experimental data support the existence of the bipartite PBS, minusstrand and plus-strand species, and priming positions of the minus and plus strands, and are described in the text. Other aspects of the model are based on retrovirus replication. After replication, the extrachromosomal Ty3 is 2 bp longer at each end. As in retroviruses, the Ty3 DNA is processed by IN so that 2 nt are removed from each 3′end (indicated by arrowheads). These ends are transferred to positions 5 nt apart in the target DNA, resulting after repair in the characteristic 5-bp repeat at both ends of the insertion. (B) Ty3 proteins. The Ty3 RNA is first translated into Ty3 polyproteins. The inferred position of translation initiation is indicated by AUG. The inferred position of termination of translation of the ORF is indicated by UAA. Most ribosomes terminate at the end of the reading frame. A percentage, however, frameshift at the sequence GCGAGUU and proceed into the reading frame to produce a Gag3-Pol3p fusion protein. Gag3p and Gag3-Pol3p polyproteins are processed by Ty3 PR into the structural and catalytic proteins that support Ty3 replication (as indicated in panel B, top). The amino-terminal processing sites of NC, PR, RT, and IN have been inferred from the amino-terminal sequences of these proteins ( ) and are shown in the right portion of the bottom panel. A protein domain, J, of about 10 kDa is inferred to occur between the PR and RT domains. It has not been detected.

Citation: Sandmeyer S, Aye M, Menees T. 2002. Ty3, a Position-Specific, Gypsy-Like Element in Saccharomyces cerevisiae, p 663-683. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch27
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Image of Figure 2
Figure 2

Assays for Ty3 transposition. (A) Ty3 Helper mobilization of a donor Ty3. In this assay, the Ty3 donor element is genetically marked. This can be with a gene that is expressed in the donor context or which is silent in the donor context and activated during transposition. If the marker gene, such as is expressed from the donor plasmid, then after transposition the plasmid must be counter selected to distinguish cells that have acquired a genomic copy of An example of the latter assay is the use of the gene containing an artificial intron () first used to study Ty1 transposition ( ). In this case is in the antisense orientation relative to Ty3 and is disrupted by a sense intron, which is spliced from the Ty3 transcript, rendering the gene active after reverse transcription and integration. In cases where the marker renders the marked element incompetent for transposition, the defect is complemented in vivo by the expression of Ty3 proteins from a transposition-competent helper Ty3. (B) Suppressor activation. This assay exploits the target specificity of Ty3 for selection of retrotransposition events. After induction of Ty3 expression, Ty3 cDNA integrates into the target plasmid containing divergent tRNA genes. Because of the closeness of the two tRNA genes, assembly of transcription initiation complex on one gene interferes with the other. Ty3 integration into the intergenic region activates expression of the suppressor tRNA gene (). This expression is detected on the selective medium as the suppression of nonsense ochre alleles of and (C) PCR amplification of integrated element DNA. This assay relies on one primer in the internal domain of Ty3 and one primer on the target plasmid. Insertion of Ty3 into the plasmid or genomic locus creates a template for PCR that results in amplification of a fragment diagnostic of a joined element and test target sequence.

Citation: Sandmeyer S, Aye M, Menees T. 2002. Ty3, a Position-Specific, Gypsy-Like Element in Saccharomyces cerevisiae, p 663-683. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch27
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Figure 3

Ty3 integration targets. Ty3 insertions occur close to the transcription initiation sites of genes transcribed by pol III. This has been demonstrated for tRNA, 5S, and U6 genes. (A) A tRNA gene (tDNA) target of Ty3 integration. Internal promoter elements box A and box B are shown. Bent arrow indicates the site of transcription initiation used for integration. TFIIIC is composed of six subunits and is shown binding over the A and B boxes of the tDNA. TFIIIC loads the initiation factor TFIIIB onto a position upstream of the transcription initiation site. TFIIIB is composed of three subunits (described in the text). Brf and TBP comprise the B′factor. In vitro TFIIIC and TFIIIB are required for Ty3 integration. (B) SNR6 target of Ty3 integration. TATA box, internal box A, and downstream box B promoter elements are shown. In vivo TFIIIC binds through contacts at the B and A boxes and loads TFIIIB (46). In vitro, in reactions with recombinant proteins, TFIIIB can bind and mediate transcription by pol III or integration by Ty3.

Citation: Sandmeyer S, Aye M, Menees T. 2002. Ty3, a Position-Specific, Gypsy-Like Element in Saccharomyces cerevisiae, p 663-683. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch27
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