Features of the mammal mar1 transposons in the human, sheep, cow, and mouse genomes and implications for their evolution

Demattei, Marie-Véronique; Augé-Gouillou, Corrine; Pollet, Nicolas; Hamelin, Marie‐Hélène; Meunier–Rotival, Michèle; Bigot, Yves

doi:10.1007/s003350010204

Cited by 10 publications

(5 citation statements)

References 16 publications

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“…The probabilities for the P167S substitution predicted from the human and the chimpanzee trees were 0.9 and 0.7, respectively. Other Hsmar1-like sequences for alignments were Hydra littoralis mar1 (AAB61385), acrobat ant mar 29.3 (42), and Bos taurus mar1 (Btmar1) (6). The Ornithorhynchus anatinus mar1 (Oamar1) sequence found in public databases is available upon request.…”

Section: Methodsmentioning

confidence: 99%

The Ancient mariner Sails Again: Transposition of the Human Hsmar1 Element by a Reconstructed Transposase and Activities of the SETMAR Protein on Transposon Ends

Miskey

Papp

Mátés

et al. 2007

Molecular and Cellular Biology

112

136

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Hsmar1, one of the two subfamilies of mariner transposons in humans, is an ancient element that entered the primate genome lineage ϳ50 million years ago. Although Hsmar1 elements are inactive due to mutational damage, one particular copy of the transposase gene has apparently been under selection. This transposase coding region is part of the SETMAR gene, in which a histone methylatransferase SET domain is fused to an Hsmar1 transposase domain. A phylogenetic approach was taken to reconstruct the ancestral Hsmar1 transposase gene, which we named Hsmar1-Ra. The Hsmar1-Ra transposase efficiently mobilizes Hsmar1 transposons by a cut-and-paste mechanism in human cells and zebra fish embryos. Hsmar1-Ra can also mobilize short inverted-repeat transposable elements (MITEs) related to Hsmar1 (MiHsmar1), thereby establishing a functional relationship between an Hsmar1 transposase source and these MITEs. MiHsmar1 excision is 2 orders of magnitude more efficient than that of long elements, thus providing an explanation for their high copy numbers. We show that the SETMAR protein binds and introduces single-strand nicks into Hsmar1 invertedrepeat sequences in vitro. Pathway choices for DNA break repair were found to be characteristically different in response to transposon cleavage mediated by Hsmar1-Ra and SETMAR in vivo. Whereas nonhomologous end joining plays a dominant role in repairing excision sites generated by the Hsmar1-Ra transposase, DNA repair following cleavage by SETMAR predominantly follows a homology-dependent pathway. The novel transposon system can be a useful tool for genome manipulations in vertebrates and for investigations into the transpositional dynamics and the contributions of these elements to primate genome evolution.

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Section: Methodsmentioning

confidence: 99%

The Ancient mariner Sails Again: Transposition of the Human Hsmar1 Element by a Reconstructed Transposase and Activities of the SETMAR Protein on Transposon Ends

Miskey

Papp

Mátés

et al. 2007

Molecular and Cellular Biology

112

136

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“…1C), a subfamily typified by the original mos1 element active in Drosophila mauritiana (Hartl et al 1997;Robertson 2002). We could not detect any members of the irritans or cecropia subfamilies of mariner in M. lucifugus using protein queries representing these lineages, although these two lineages have been identified in a broad range of mammals (Demattei et al 2000;Robertson 2002;Waterston et al 2002;Sinzelle et al 2006), including other bat species (see below).…”

Section: Tc1/mariner Superfamilymentioning

confidence: 99%

Multiple waves of recent DNA transposon activity in the bat, Myotis lucifugus

Ray¹,

Feschotte²,

Pagán³

et al. 2008

Genome Res.

150

163

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DNA transposons, or class 2 transposable elements, have successfully propagated in a wide variety of genomes. However, it is widely believed that DNA transposon activity has ceased in mammalian genomes for at least the last 40 million years. We recently reported evidence for the relatively recent activity of hAT and Helitron elements, two distinct groups of DNA transposons, in the lineage of the vespertilionid bat Myotis lucifugus. Here, we describe seven additional families that have also been recently active in the bat lineage. Early vespertilionid genome evolution was dominated by the activity of Helitrons, mariner-like and Tc2-like elements. This was followed by the colonization of Tc1-like elements, and by a more recent explosion of hAT-like elements. Finally, and most recently, piggyBac-like elements have amplified within the Myotis genome and our results indicate that one of these families is probably still expanding in natural populations. Together, these data suggest that there has been tremendous recent activity of various DNA transposons in the bat lineage that far exceeds those previously reported for any mammalian lineage. The diverse and recent populations of DNA transposons in genus Myotis will provide an unprecedented opportunity to study the impact of this class of elements on mammalian genome evolution and to better understand what makes some species more susceptible to invasion by genomic parasites than others.

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“…This type of element makes up 3% of our genome (Lander et al 2001), yet only a limited number of studies have focused on DNA transposons in any mammalian genomes (Auge-Gouillou et al 1995;Morgan 1995;Oosumi et al 1995;Robertson 1996;Smit and Riggs 1996;Robertson and Martos 1997;Robertson and Zumpano 1997;Demattei et al 2000). In contrast, the evolutionary history and genomic impact of mammalian retrotransposons has been the subject of intensive investigation (for examples, see Smit et al 1995;Kapitonov and Jurka 1996;Szak et al 2002;Xing et al 2003;Price et al 2004;Khan et al 2006; for review, see Deininger et al 2003).…”

mentioning

confidence: 99%

The evolutionary history of human DNA transposons: Evidence for intense activity in the primate lineage

2007

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Class 2, or DNA transposons, make up ∼3% of the human genome, yet the evolutionary history of these elements has been largely overlooked and remains poorly understood. Here we carried out the first comprehensive analysis of the activity of human DNA transposons over the course of primate evolution using three independent computational methods. First, we conducted an exhaustive search for human DNA transposons nested within L1 and Alu elements known to be primate specific. Second, we assessed the presence/absence of 794 human DNA transposons at orthologous positions in 10 mammalian species using sequence data generated by The ENCODE Project. These two approaches, which do not rely upon sequence divergence, allowed us to classify DNA transposons into three different categories: anthropoid specific (40-63 My), primate specific (64-80 My), and eutherian wide (81-150 My). Finally, we used this data to calculate the substitution rates of DNA transposons for each category and refine the age of each family based on the average percent divergence of individual copies to their consensus. Based on these combined methods, we can confidently estimate that at least 40 human DNA transposon families, representing ∼98,000 elements (∼33 Mb) in the human genome, have been active in the primate lineage. There was a cessation in the transpositional activity of DNA transposons during the later phase of the primate radiation, with no evidence of elements younger than ∼37 My. This data points to intense activity of DNA transposons during the mammalian radiation and early primate evolution, followed, apparently, by their mass extinction in an anthropoid primate ancestor.

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Features of the mammal mar1 transposons in the human, sheep, cow, and mouse genomes and implications for their evolution

Cited by 10 publications

References 16 publications

The Ancient mariner Sails Again: Transposition of the Human Hsmar1 Element by a Reconstructed Transposase and Activities of the SETMAR Protein on Transposon Ends

The Ancient mariner Sails Again: Transposition of the Human Hsmar1 Element by a Reconstructed Transposase and Activities of the SETMAR Protein on Transposon Ends

Multiple waves of recent DNA transposon activity in the bat, Myotis lucifugus

The evolutionary history of human DNA transposons: Evidence for intense activity in the primate lineage

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