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The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of

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  • Authors: Caroline Esnault1, Henry L. Levin2
  • Editors: Suzanne Sandmeyer3, Nancy Craig4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Section on Eukaryotic Transposable Elements, Program in Cellular Regulation and Metabolism, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892; 2: Section on Eukaryotic Transposable Elements, Program in Cellular Regulation and Metabolism, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892; 3: University of California, Irvine, CA; 4: Johns Hopkins University, Baltimore, MD
  • Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0040-2014
  • Received 03 July 2014 Accepted 20 October 2014 Published 23 July 2015
  • Henry Levin, henry_levin@nih.gov
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  • Abstract:

    The long terminal repeat (LTR) retrotransposons Tf1 and Tf2 of are active mobile elements of the Ty3/gypsy family. The mobilization of these retrotransposons depends on particle formation, reverse transcription and integration, processes typical of other LTR retrotransposons. However, Tf1 and Tf2 are distinct from other LTR elements in that they assemble virus-like particles from a single primary translation product, initiate reverse transcription with an unusual self-priming mechanism, and, in the case of Tf1, integrate with a pattern that favors specific promoters of RNA pol II-transcribed genes. To avoid the chromosome instability and genome damage that results from increased copy number, applies a variety of defense mechanisms that restrict Tf1 and Tf2 activity. The mRNA of the Tf elements is eliminated by an exosome-based pathway when cells are in favorable conditions whereas nutrient deprivation triggers an RNA interference-dependent pathway that results in the heterochromatization of the elements. Interestingly, Tf1 integrates into the promoters of stress-induced genes and these insertions are capable of increasing the expression of adjacent genes. These properties of Tf1 transposition raise the possibility that Tf1 benefits cells with specific insertions by providing resistance to environmental stress.

  • Citation: Esnault C, Levin H. 2015. The Long Terminal Repeat Retrotransposons Tf1 and Tf2 of . Microbiol Spectrum 3(4):MDNA3-0040-2014. doi:10.1128/microbiolspec.MDNA3-0040-2014.

Key Concept Ranking

DNA Synthesis
0.7059078
Long Terminal Repeat Retrotransposons
0.5591921
Transcription Start Site
0.5180187
0.7059078

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/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0040-2014
2015-07-23
2017-02-19

Abstract:

The long terminal repeat (LTR) retrotransposons Tf1 and Tf2 of are active mobile elements of the Ty3/gypsy family. The mobilization of these retrotransposons depends on particle formation, reverse transcription and integration, processes typical of other LTR retrotransposons. However, Tf1 and Tf2 are distinct from other LTR elements in that they assemble virus-like particles from a single primary translation product, initiate reverse transcription with an unusual self-priming mechanism, and, in the case of Tf1, integrate with a pattern that favors specific promoters of RNA pol II-transcribed genes. To avoid the chromosome instability and genome damage that results from increased copy number, applies a variety of defense mechanisms that restrict Tf1 and Tf2 activity. The mRNA of the Tf elements is eliminated by an exosome-based pathway when cells are in favorable conditions whereas nutrient deprivation triggers an RNA interference-dependent pathway that results in the heterochromatization of the elements. Interestingly, Tf1 integrates into the promoters of stress-induced genes and these insertions are capable of increasing the expression of adjacent genes. These properties of Tf1 transposition raise the possibility that Tf1 benefits cells with specific insertions by providing resistance to environmental stress.

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FIGURE 1

Tf1 transposition in . Full-length Tf1 (blue rectangles) is transcribed and translated. The polyprotein assembles into particle precursors and PR processes the protein into Gag (pink), protease (PR), reverse transcriptase (RT) (orange), and integrase (IN) (orange). The mature virus-like particles (VLP) contain the processed proteins and two copies of mRNA (blue wavy lines). The RT reverse-transcribes the mRNA into double-stranded cDNA that associates with IN. Once transported into the nucleus (above dotted line), the IN integrates the cDNA at a new position in the genome. The long terminal repeats are symbolized by triangles. The protein coding sequences are represented by rectangles. doi:10.1128/microbiolspec.MDNA3-0040-2014.f1

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0040-2014
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Image of FIGURE 2
FIGURE 2

Reverse transcription of Tf1 is initiated by a self-priming mechanism. (A) The 5′ end of the Tf1 mRNA anneals to the primer binding site (PBS). The first 11 nucleotides (red) are cleaved from the Tf1 mRNA (black) and prime reverse transcription towards the 5′ end of the mRNA. The scissors indicate the position of cleavage. The arrow indicates the direction of reverse transcription. (B) The 5′ end of the Tf1 mRNA folds into a complex duplex structure. The scissors indicate the position of the cleavage that liberates the self-primer (red). The position of the U5-IR stem-loop is indicated. doi:10.1128/microbiolspec.MDNA3-0040-2014.f2

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0040-2014
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FIGURE 3

Distribution of the distance from Tf1 integration to the nearest open reading frame (ORF). A collection of 800,723 independent integration events was positioned according to the distance to the nearest ORF (red) ( 57 ). The -axis represents the distance from the 5′ end and 3′ end of ORFs in bins that are 100 bp wide; distances within ORFs are divided into 15 bins of equal proportion. The -axis represents the percentage of independent integration events positioned within the bins. The majority of integration events are located near the 5′ end of ORFs, 3.8% of all integration events targeted coding sequences. Figure reproduced with permission from ref. ( 57 ). doi:10.1128/microbiolspec.MDNA3-0040-2014.f3

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0040-2014
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FIGURE 4

Impact of Tf elements on gene expression. Tf element integration can activate the expression of adjacent genes. (A) Tf2 long terminal repeat (LTR) (blue) possesses a motif ATCGTACCAT bound by the transcription factor Sre1 (green), which activates the transcription of oxygen-dependent genes such as . Pol II (pink); RNA polymerase II. (B) Sequences within the Tf1 LTR substitute for the elements in the promoter that are disrupted by Tf1 integration. Tf1 integration results in a 2.1- to 3.6-fold increase in expression. TF (grey): transcription factor. (C) Tf1 integration near the heat shock gene acts as an enhancer of transcription, through a mechanism that may involve the transcription activation factor Atf1 (red). A motif TGACGT similar to the sequence bound by Atf1 is within the Tf1 LTR (blue). doi:10.1128/microbiolspec.MDNA3-0040-2014.f4

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0040-2014
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Tables

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TABLE 1

Features and content in transposable elements of the genome

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0040-2014
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TABLE 2

Sizes of transposable elements and the molecular weights of their components in

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0040-2014
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TABLE 3

Host factors that restrict transposable element activity

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MDNA3-0040-2014

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