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Review
. 2017 Jul 19;9(7):192.
doi: 10.3390/v9070192.

Drosophila: Retrotransposons Making up Telomeres

Elena Casacuberta  1
Affiliations
Review

Drosophila: Retrotransposons Making up Telomeres

Elena Casacuberta. Viruses. .

Abstract

Drosophila and extant species are the best-studied telomerase exception. In this organism, telomere elongation is coupled with targeted retrotransposition of Healing Transposon (HeT-A) and Telomere Associated Retrotransposon (TART) with sporadic additions of Telomere Associated and HeT-A Related (TAHRE), all three specialized non-Long Terminal Repeat (non-LTR) retrotransposons. These three very special retroelements transpose in head to tail arrays, always in the same orientation at the end of the chromosomes but never in interior locations. Apparently, retrotransposon and telomerase telomeres might seem very different, but a detailed view of their mechanisms reveals similarities explaining how the loss of telomerase in a Drosophila ancestor could successfully have been replaced by the telomere retrotransposons. In this review, we will discover that although HeT-A, TART, and TAHRE are still the only examples to date where their targeted transposition is perfectly tamed into the telomere biology of Drosophila, there are other examples of retrotransposons that manage to successfully integrate inside and at the end of telomeres. Because the aim of this special issue is viral integration at telomeres, understanding the base of the telomerase exceptions will help to obtain clues on similar strategies that mobile elements and viruses could have acquired in order to ensure their survival in the host genome.

Keywords: telomere integration, HeT-A, TART, TAHRE, Drosophila, telomere targeting.

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Conflict of interest statement

The authors declare they do not have any conflicts of interest.

Figures

Figure 1
Figure 1
The telomeric retrotransposons of Drosophila. (A) The telomere retrotransposons. Figure 1 depicts the telomeric retrotransposons Healing Transposon (HeT-A), Telomere Associated and HeT-A Related (TAHRE) and Telomere Associated Retrotransposon (TART) from Drosophila melanogaster and a canonical non-Long Terminal Repeat (non-LTR) retrotransposon for comparing the unusual features of the telomere retrotransposons. Figure 1 is drawn approximately to scale. Dotted grey lines show conserved regions of TAHRE and HeT-A DNA sequences. Bright Grey: non-coding 5′ and 3′ untranslated regions (UTRs) sequences. White: Gag open reading frames (ORF). Dark Grey: Pol ORF domains; EN, endonuclease, RT, reverse-transcriptase. White arrows in TART indicate the Perfect Non-Terminal Repeats (PNTRs); (A)n, 3′ oligo A. Black Arrows: indicate approximate location of the sense and antisense promoter. (B) The HeT-A telomere retrotransposon resembles an intermediate between a non-LTR and a LTR retrotransposon. Representation of a Drosophila melanogaster telomere. The array of HeT-A elements shows how from sense to sense promoter its analogous to an LTR retrotransposon. See legend in A) for schematic representation.
Figure 2
Figure 2
Life cycle of the telomeric retrotransposons in Drosophila. Black lines represent: division between nucleus and cytoplasm (curved), steps of the life cycle (arrows) and zoom in of the TPRT at the end of the chromosome (square). Small blue lines represent HeT-A mRNA and transcription from the telomeres. AAA poly A tail. For simplicity only HeT-A is represented. Blue arrows represent the elements at the HTT array, the telomeres in Drosophila. HeT-A Gag protein drawn as purple spheres. Red circles represent the ribosome and the red rectangle represents host DNA polymerase for second strand synthesis. 3′ hydroxyl group that primes the reverse transcription reaction is indicated. RT, reverse transcriptase (of still of unknown source). Moi, Tea, and Ver (MTV) are part of the capping complex that binds the ssDNA strand at the telomeres MTV, and is involved in formation of the spheres of HeT-A Gag containing HeT-A mRNA at the moment of telomere replication and elongation. See text for detail description of each step.
Figure 3
Figure 3
Schematic representation of different mechanisms of telomere integration. (A) Non-LTR retrotransposons containing Apurinic/Apyrimidinic (APE) endonucleases. SART and TRAS telomeric retrotransposons from Bombyx mori. Strand and nucleotide specificity of their respective endonucleases indicated. Telomere repeats in black. Blue lines: mRNA of SART and TRAS. RT indicates reverse transcriptase, and AAA poly A tail. (B) Penelope-like elements and endonuclease defective LINE L1 elements. Representation of telomeres by black lines. 3′ hydroxyl group that primes the reverse transcription reaction is indicated. Blue spheres indicate Orfp1 with structural properties, and RT, reverse transcriptase. Blue line represents retrotransposon mRNA (figuring PLE or L1) and AAA poly A tail. (C) Targeting host factors; Ty5 as an example. In blue, transposition intermediate of the LTR yeast retrotransposon Ty5. Integrase protein in green at the ends of the intermediate with red dots representing phosphorylation. Black and thick double arrow, Sir4P, the chromatin host factor that targets Ty5 towards subtelomeres. Black arrow on the right side of the figure indicates direction from telomere towards centromere applying to the entire figure.
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