TAHRE, a Novel Telomeric Retrotransposon from Drosophila melanogaster, Reveals the Origin of Drosophila Telomeres

Abad, José P.; Pablos, Beatriz de; Osoegawa, Kazutoyo; Jong, Pieter J. de; Martin-Gallardo, Antonia; Villasanté, Alfredo

doi:10.1093/molbev/msh180

Cited by 116 publications

(126 citation statements)

References 35 publications

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“…44,45 The 5'UTR, ORF1 and 3'UTR of TAHRE are very similar to the corresponding sequences of HeT-A, and its ORF2 encodes a RT that has some similarity to the RT of TART. 31 These structural data, together with the phylogenetic analyses of HeT-A, TART and TAHRE, suggest that HeT-A derived from an ancestral TAHRE element that lost its ORF2. 31 The HeT-A promoter, as well as the TAHRE promoter, is located at the 3' end of the element and drive transcription of the adjacent downstream element.…”

Section: Three Retrotransposons Maintain Telomeres In Drosophila Melamentioning

confidence: 80%

“…29 HeT-A and TAHRE are, respectively, the more and less abundant elements. In the y; cn bw sp strain of D. melanogaster a unique complete copy of TAHRE has been found, 31 whereas several elements from four HeT-A subfamilies and various elements of one TART subfamily were found. 29 The analysis of TART elements in different strains allowed the identification of three TART subfamilies.…”

Section: Three Retrotransposons Maintain Telomeres In Drosophila Melamentioning

confidence: 99%

“…[37][38][39][40][41][42][43] TART and TAHRE have the two open reading frames typical of non-LTR retrotransposons; the ORF1 encodes a putative RNA binding protein and the ORF2 encodes a protein with domains related to both reverse transcriptase (RT) and endonuclease. 31,32 Per contra, HeT-A is an atypical element because it lacks ORF2, so the RT for its transposition must be produced in trans. This type of non-autonomous elements has been described in several species.…”

Section: Three Retrotransposons Maintain Telomeres In Drosophila Melamentioning

confidence: 99%

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Telomere maintenance in Drosophila: Rapid transposon evolution at chromosome ends

Villasanté

Pablos²,

Méndez-Lago³

et al. 2008

Cell Cycle

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The maintenance of terminal sequences is an important role of the telomere, since it prevents the loss of internal regions that encode essential genes. In most eukaryotes, this is accomplished by the telomerase. However, telomere length can also be maintained by other mechanisms, such as homologous recombination and transposition of telomeric retrotransposons to the chromosome ends. A remarkable situation is the case of Drosophila, where telomerase was lost, and thus telomeres managed to be maintained by occasional retrotransposition of telomeric elements to the receding ends. In the recent analysis of 12 Drosophila genomes, the multiplicity of autonomous and non-autonomous telomere-specific retrotransposons has revealed extensive and rapid evolution of telomeric DNA. The phylogenetic relationship among these telomeric retrotransposons is congruent with the species phylogeny, suggesting that they have been vertically transmitted from a common ancestor. In this review, we also suggest that the formation of a non-canonical DNA structure at Drosophila telomeres could be the way to protect the ends.

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Section: Three Retrotransposons Maintain Telomeres In Drosophila Melamentioning

confidence: 80%

Section: Three Retrotransposons Maintain Telomeres In Drosophila Melamentioning

confidence: 99%

Section: Three Retrotransposons Maintain Telomeres In Drosophila Melamentioning

confidence: 99%

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Telomere maintenance in Drosophila: Rapid transposon evolution at chromosome ends

Villasanté

Pablos²,

Méndez-Lago³

et al. 2008

Cell Cycle

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“…For example, Drosophila lacks a formal telomerase and relies on three retrotransposons (HetA, TART, and TAHRE) to maintain its telomeres (61)(62)(63)(64)(65). Interestingly, TART and TAHRE have an apparent APE domain, suggesting that, unlike ENi L1 retrotransposition, this putative endonuclease may be important for telomere localization (66).…”

Section: Discussionmentioning

confidence: 99%

Similarities between long interspersed element-1 (LINE-1) reverse transcriptase and telomerase

Kopera¹,

Moldovan²,

Morrish³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Long interspersed element-1 (LINE-1 or L1) retrotransposons encode two proteins (ORF1p and ORF2p) that contain activities required for conventional retrotransposition by a mechanism termed target-site primed reverse transcription. Previous experiments in XRCC4 or DNA protein kinase catalytic subunit-deficient CHO cell lines, which are defective for the nonhomologous endjoining DNA repair pathway, revealed an alternative endonuclease-independent (ENi) pathway for L1 retrotransposition. Interestingly, some ENi retrotransposition events in DNA protein kinase catalytic subunit-deficient cells are targeted to dysfunctional telomeres. Here we used an in vitro assay to detect L1 reverse transcriptase activity to demonstrate that wild-type or endonuclease-defective L1 ribonucleoprotein particles can use oligonucleotide adapters that mimic telomeric ends as primers to initiate the reverse transcription of L1 mRNA. Importantly, these ribonucleoprotein particles also contain a nuclease activity that can process the oligonucleotide adapters before the initiation of reverse transcription. Finally, we demonstrate that ORF1p is not strictly required for ENi retrotransposition at dysfunctional telomeres. Thus, these data further highlight similarities between the mechanism of ENi L1 retrotransposition and telomerase.L ong interspersed element-1 sequences (LINE-1s or L1s) are abundant non-long terminal repeat (non-LTR) retrotransposons that constitute approximately one-sixth (i.e., ≈17%) of human nuclear DNA (1). An estimated 80-100 full-length, retrotransposition competent L1s (RC-L1s) are present in a typical diploid human genome, and a small number, termed "hot L1s" exhibit high retrotransposition efficiencies in cultured human cells (2). Human RC-L1s are ≈6 kb (3, 4) and encode two proteins (ORF1p and ORF2p) required for retrotransposition (5). ORF1p is a 40-kDa protein (6) with RNA binding (7-12) and nucleic acid chaperone activities (13-15). ORF2p is a 150-kDa protein (16, 17) with endonuclease (EN) (18,19) and reverse transcriptase (RT) (20, 21) activities.The mobilization of RC-L1s can be mutagenic (22); germ line and, less often, somatic L1 insertions have led to ≈65 sporadic cases of disease in humans (reviewed in ref. 23). ORF1p and/or ORF2p also can act in trans to mobilize short interspersed elements [e.g., Alu (24) and SINE-VNTR-Alu (25) elements], certain noncoding RNAs [e.g., U6 snRNA and small nucleolar RNAs (24, 26-29)], and some cellular mRNAs, which leads to the formation of processed pseudogenes (30-32). In total, these trans retrotransposition events account for at least an additional 10% of human DNA (1). Moreover, several recent studies have further demonstrated that L1-mediated retrotransposition events are responsible for a significant proportion of interindividual genetic variation in the human population (33-39) and may cause intraindividual variation in the mammalian nervous system (40, 41). L1 retrotransposition likely occurs by a mechanism termed target-site primed reverse transcription (TPRT) (42)...

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“…melanogaster maintains its telomeres by occasional targeted transposition of three telomere-specific non-LTR retrotransposons (HeT-A, TART and TAHRE) to chromosome ends 54,55 and not by the more common mechanism of telomerase-generated G-rich repeats 56 . Multiple telomeric retrotransposons have originated within the genus, where they now maintain telomeres, and recurrent loss of most of the ORF2 from telomeric retrotransposons (for example, TAHRE) has given rise to half-telomeric-retrotransposons (for example, HeT-A) during Drosophila evolution 57 .…”

Section: Gelbart Personal Communication) (Supplementary Information mentioning

confidence: 99%

Evolution of genes and genomes on the Drosophila phylogeny

Clark¹,

Eisen²,

Smith³

et al. 2007

Nature

1,826

1,041

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Comparative analysis of multiple genomes in a phylogenetic framework dramatically improves the precision and sensitivity of evolutionary inference, producing more robust results than single-genome analyses can provide. The genomes of 12 Drosophila species, ten of which are presented here for the first time (sechellia, simulans, yakuba, erecta, ananassae, persimilis, willistoni, mojavensis, virilis and grimshawi), illustrate how rates and patterns of sequence divergence across taxa can illuminate evolutionary processes on a genomic scale. These genome sequences augment the formidable genetic tools that have made Drosophila melanogaster a pre-eminent model for animal genetics, and will further catalyse fundamental research on mechanisms of development, cell biology, genetics, disease, neurobiology, behaviour, physiology and evolution. Despite remarkable similarities among these Drosophila species, we identified many putatively non-neutral changes in protein-coding genes, non-coding RNA genes, and cis-regulatory regions. These may prove to underlie differences in the ecology and behaviour of these diverse species.

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TAHRE, a Novel Telomeric Retrotransposon from Drosophila melanogaster, Reveals the Origin of Drosophila Telomeres

Cited by 116 publications

References 35 publications

Telomere maintenance in Drosophila: Rapid transposon evolution at chromosome ends

Telomere maintenance in Drosophila: Rapid transposon evolution at chromosome ends

Similarities between long interspersed element-1 (LINE-1) reverse transcriptase and telomerase

Evolution of genes and genomes on the Drosophila phylogeny

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