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The Ty1 LTR-Retrotransposon of Budding Yeast,

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  • Authors: M. Joan Curcio1, Sheila Lutz2, Pascale Lesage3
  • Editors: Suzanne Sandmeyer4, Nancy Craig5
    Affiliations: 1: Laboratory of Molecular Genetics, Wadsworth Center, and Department of Biomedical Sciences, University at Albany-SUNY; Center for Medical Sciences, 150 New Scotland Avenue, Albany, NY, 12208; 2: Laboratory of Molecular Genetics, Wadsworth Center, and Department of Biomedical Sciences, University at Albany-SUNY; Center for Medical Sciences, 150 New Scotland Avenue, Albany, NY, 12208; 3: Université Paris Diderot, Sorbonne Paris Cité, Institut Universitaire d'Hématologie, Hôpital St. Louis, Institut National de la Santé et de la Recherche Médicale (INSERM) UMR 944, Centre National de la Recherche Scientifique (CNRS) UMR 7212, Paris cedex 10, France; 4: University of California, Irvine, CA; 5: Johns Hopkins University, Baltimore, MD
  • Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014
  • Received 08 September 2014 Accepted 22 January 2015 Published 19 March 2015
  • Joan Curcio, [email protected]
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  • Abstract:

    Long-terminal repeat (LTR)-retrotransposons generate a copy of their DNA (cDNA) by reverse transcription of their RNA genome in cytoplasmic nucleocapsids. They are widespread in the eukaryotic kingdom and are the evolutionary progenitors of retroviruses. The Ty1 element of the budding yeast was the first LTR-retrotransposon demonstrated to mobilize through an RNA intermediate, and not surprisingly, is the best studied. The depth of our knowledge of Ty1 biology stems not only from the predominance of active Ty1 elements in the genome but also the ease and breadth of genomic, biochemical, and cell biology approaches available to study cellular processes in yeast. This review describes the basic structure of Ty1 and its gene products, the replication cycle, the rapidly expanding compendium of host cofactors known to influence retrotransposition, and the nature of Ty1's elaborate symbiosis with its host. Our goal is to illuminate the value of Ty1 as a paradigm to explore the biology of LTR-retrotransposons in multicellular organisms, where the low frequency of retrotransposition events presents a formidable barrier to investigations of retrotransposon biology.

  • Citation: Curcio M, Lutz S, Lesage P. 2015. The Ty1 LTR-Retrotransposon of Budding Yeast, . Microbiol Spectrum 3(2):MDNA3-0053-2014. doi:10.1128/microbiolspec.MDNA3-0053-2014.


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Long-terminal repeat (LTR)-retrotransposons generate a copy of their DNA (cDNA) by reverse transcription of their RNA genome in cytoplasmic nucleocapsids. They are widespread in the eukaryotic kingdom and are the evolutionary progenitors of retroviruses. The Ty1 element of the budding yeast was the first LTR-retrotransposon demonstrated to mobilize through an RNA intermediate, and not surprisingly, is the best studied. The depth of our knowledge of Ty1 biology stems not only from the predominance of active Ty1 elements in the genome but also the ease and breadth of genomic, biochemical, and cell biology approaches available to study cellular processes in yeast. This review describes the basic structure of Ty1 and its gene products, the replication cycle, the rapidly expanding compendium of host cofactors known to influence retrotransposition, and the nature of Ty1's elaborate symbiosis with its host. Our goal is to illuminate the value of Ty1 as a paradigm to explore the biology of LTR-retrotransposons in multicellular organisms, where the low frequency of retrotransposition events presents a formidable barrier to investigations of retrotransposon biology.

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Structure of the Ty1 element relative to the simple retrovirus, avian leukemia virus (ALV). Ty1 consists of long terminal repeats (LTRs; boxed arrowheads) flanking a central coding region that contains two overlapping ORFs, () and (), which are analogous to retroviral and genes, respectively. Separate functional domains of that are conserved in LTR-retrotransposons and retroviruses and are synthesized as part of the Gag-Pol polyprotein and cleaved into separate proteins posttranslationally include protease (PR), reverse transcriptase-RNase H (RT-RH), and integrase (IN). The retroviral envelope gene () is not present in Ty1.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014
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Ty1 replication cycle. The major steps in replication of Ty1, which results in the introduction of a new copy of Ty1 into the host genome, are illustrated. A Ty1 element in the host genome (blue double helix) is transcribed and the Ty1 RNA (wavy teal lines) is exported to the cytoplasm. The RNA is translated into Gag and Gag-Pol proteins and associates with these proteins to form Ty1 RNPs, also known as retrosomes. Ty1 RNPs give rise to virus-like particles (VLPs) that encapsidate a dimer of Ty1 RNA and tRNA . Within the VLP, Gag and Pol proteins are cleaved by protease (PR) (maroon ball) to form mature Gag, PR, integrase (IN), and reverse transcriptase (RT) proteins. Following VLP maturation, Ty1 RNA is reverse transcribed into cDNA by RT (blue ball) using tRNA as a primer. The cDNA is bound by IN (purple ball) to form the preintegation complex, which is imported into the nucleus. IN integrates Ty1 cDNA into the yeast genome.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014
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Assay for Ty1 retromobility using a retrotranscript indicator gene (RIG). A chromosomal Ty1 element tagged with the RIG gives rise to Ty1 cDNA bearing a functional gene. The cDNA can enter the host genome (represented by a blue double helix) by two retromobility pathways. Retrotransposition occurs when Ty1 integrase (IN) mediates the integration of cDNA into the genome, while cDNA recombination occurs when the cDNA recombines homologously with an endogenous Ty1 element. The dashed lines represent the low frequency of Ty1 cDNA recombination in wild-type cells. Cells that sustain a Ty1 retromobility event give rise to His colonies. Other RIGs used in yeast include , which is selectable with G418 and , which is selectable by adenine prototrophy ( 268 , 269 ).

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014
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Helper-donor assay for separation of mRNA and gRNA functions. In this assay, expression of both Ty1 elements is driven from the promoter in a strain, which lacks endogenous Ty1 expression. The helper-Ty1 encodes a functional mRNA with and ORFs and silent mutations at the 5′ end of (indicated by an asterisk) that disrupt -acting signals required for reverse transcription. The absence of a 3′ long terminal repeat (LTR) also precludes the use of the helper-Ty1 RNA as a template for reverse transcription. The donor-Ty1 RNA encodes a functional gRNA that lacks ORFs but contains -acting signals for dimerization, packaging, and reverse transcription. The RIG is also contained in this element to detect retromobility of mini-Ty1 cDNA. The minimal donor element capable of retromobility is depicted.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014
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Ty1 transcription. (A) Sense and antisense RNAs transcribed from Ty1. The Ty1 sense-strand transcript starts at the U3/R junction of the 5′ LTR and ends at the R/U5 junction of the 3′ LTR. The 5 kb Ty1 RNA species is detected in mutants. Ty1AS RNA 5′ and 3′ extremities have been mapped by RACE to positions 661 ( 68 ) and 760 ( 33 ) of Ty1-H3 and to positions 136 and 178 of Ty1-H3 ( 33 ), respectively. (B) Organization of the Ty1 promoter. Ty1 contains two TATA boxes, T and T (at positions 159 to 165 and 167 to 173, respectively) and two termination sequences TS (5,776 to 5,781) and TS (5,837 to 5,842). The arrow and lollipop indicate sites of transcription initiation and termination, respectively. The Ty1 promoter extends over 1 kb including the 5′ LTR and part of the ORF. The positions of the Ty1 activator binding sites are: Gcn4 (five binding sites: 12 to 17, 79 to 84, 98 to 103, 155 to 160, and 318 to 323), Gcr1 (115 to 119), Ste12 (395 to 401), Tec1 (418 to 422), Tye7 (three binding sites: 463 to 468, 661 to 666, and 727 to 732), Mcm1 (833 to 848), Tea1/Ibf1 (884 to 899), and Rap1 (911 to 923). The filamentous response element (FRE) comprises Ste12 and Tec1 binding sites, while MIR comprises Mcm1, Tea1/Ibf1, and Rap1 binding sites. The positions of the Ty1 repressor binding sites are: Mot3 (several binding sites in the 5′ LTR; higher affinity site at positions 147 to 150) and a1/α2 (832 to 863). Positions are given relative to Ty1-H3 sequence ( 10 ).

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014
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Expression of individual endogenous Ty1 elements. Relative transcriptional activities of 31 Ty1 elements present in the S288C strain (adapted from Morillon et al. [ 56 ]). Ty1/Ty2 hybrid elements are indicated by black filled bars and Ty′ elements are indicated by gray filled bars.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014
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Secondary structure model of the 5′ end of Ty1 RNA. (Reproduced from Purzycka et al. [ 74 ].) Full-length Ty1 RNA within virus-like particles (VLPs) () was analyzed to determine the SHAPE reactivities of nucleotides 1 to 1,482, which are individually represented by a color-coded ball. The color is indicative of the reactivity of that nucleotide to the SHAPE reagent, N-methyisatoic anhydride (NMIA). The secondary structure model in which regions predicted to be based-paired (illustrated as bars linking balls) and regions predicted to be single stranded are shown was obtained from the SHAPE reactivities using RNAstructure 4.6 software ( 270 ). Nucleotide positions at which SHAPE reactivities changed when the proteins were gently stripped away from VLP-associated Ty1 RNA () are marked with blue diamonds (increased reactivity) or gray diamonds (decreased reactivity). Annotated regions include the following: PAL1, PAL2, and PAL3 motifs, at which the differences in nucleotide reactivity versus suggest that the Ty1 RNA pairs with a second molecule of Ty1 RNA to form a dimer; the AUG codon of (nucleotides 54 to 57); CYC5, a region that hybridizes to the CYC3 domain near the 3′ end of Ty1 RNA; primer binding sequence (PBS), Box 0, and Box 1, where the tRNA primer (shown in gray) hybridizes to Ty1 RNA to initiate reverse transcription; and the Gag-Pol frameshift site at nucleotides 1,356 to 1,362.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014
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The Ty1 retrosome. Retrosomes are cytoplasmic foci in which Gag and retrotransposon RNA colocalize, as visualized by fluorescence microscopy. Ty1 retrosomes are detected in fixed cells after fluorescence hybridization and immunofluorescence. Ty1 RNA is detected using a DNA oligomer end-labeled with Cy3, and Gag is detected using anti-VLP antibodies that are bound by a secondary antibody coupled to Alexa Fluor® 488 (Life Technologies, Grand Island, NY)

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014
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Steps in reverse transcription of Ty1 cDNA. Details of each step are provided in the text. Gag and protease (PR) have nucleic acid chaperone activities required for reverse transcription and integrase (IN) facilitates the reverse transcription reaction carried out by reverse transcriptase/RNase H (RT/RH). In this schematic, minus-strand strong-stop (msss) cDNA is shown being transferred to the second Ty1 RNA in the VLP for minus strand cDNA synthesis. However, it is formally possible that msss cDNA transfers to the 3′ end of the first Ty1 RNA, as long as this RNA, following RNAse H-mediated degradation, contains a remnant of R-U5 sequence to template minus-strand cDNA synthesis so that minus-strand cDNA can hybridize to plus-strand strong-stop (psss) cDNA in the final step of the RT reaction. Single strands of cDNA are represented by thin green lines; the presence of an arrowhead indicates strands being extended by reverse transcription. Blue wavy line, Ty1 RNA; short blue squiggles, polypurine tracts of Ty1 RNA, cPPT and PPT, remaining after RNase H endonucleolytic activity; blue pacman shape, RNase H activity of RT/RH; LTR, long terminal repeat; PBS, primer binding sequence.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014
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Integrase and the integration target region. (A) Schematic representation of Ty1 integrase domains. Amino acid residues in the zinc binding motif (ZBD) and the catalytic core domain that are conserved in retroviral integrases, or residues in the C-terminal domain that are conserved in the family of long terminal repeat-retrotransposons are indicated. Identical clusters of basic residues that define the bipartite nuclear localization signal (NLS) are also indicated. (B) Plot of Ty1 insertions upstream of tRNA genes. (Reproduced from Bridier-Nahmias and Lesage [ 271 ].) The blue curve above the midline represents Ty1 insertions in tandem with the tRNA genes and that below the midline represents elements inserted in inverted orientation.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014
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List of verified host factors that regulate Ty1 retromobility

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0053-2014

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