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Site-specific non-LTR retrotransposons

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  • Author: Haruhiko Fujiwara1
  • Editors: Alan Lambowitz2, Nancy Craig3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Kashiwa 277-8562, Japan; 2: University of Texas, Austin, TX; 3: Johns Hopkins University, Baltimore, MD
  • Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0001-2014
  • Received 13 July 2014 Accepted 16 July 2014 Published 12 March 2015
  • Haruhiko Fujiwara, haruh@k.u-tokyo.ac.jp
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  • Abstract:

    Although most of non-long terminal repeat (non-LTR) retrotransposons are incorporated in the host genome almost randomly, some non-LTR retrotransposons are incorporated into specific sequences within a target site. On the basis of structural and phylogenetic features, non-LTR retrotransposons are classified into two large groups, restriction enzyme-like endonuclease (RLE)-encoding elements and apurinic/apyrimidinic endonuclease (APE)-encoding elements. All clades of RLE-encoding non-LTR retrotransposons include site-specific elements. However, only two of more than 20 APE-encoding clades, Tx1 and R1, contain site-specific non-LTR elements. Site-specific non-LTR retrotransposons usually target within multi-copy RNA genes, such as rRNA gene (rDNA) clusters, or repetitive genomic sequences, such as telomeric repeats; this behavior may be a symbiotic strategy to reduce the damage to the host genome. Site- and sequence-specificity are variable even among closely related non-LTR elements and appeared to have changed during evolution. In the APE-encoding elements, the primary determinant of the sequence- specific integration is APE itself, which nicks one strand of the target DNA during the initiation of target primed reverse transcription (TPRT). However, other factors, such as interaction between mRNA and the target DNA, and access to the target region in the nuclei also affect the sequence-specificity. In contrast, in the RLE-encoding elements, DNA-binding motifs appear to affect their sequence-specificity, rather than the RLE domain itself. Highly specific integration properties of these site-specific non-LTR elements make them ideal alternative tools for sequence-specific gene delivery, particularly for therapeutic purposes in human diseases.

  • Citation: Fujiwara H. 2015. Site-specific non-LTR retrotransposons. Microbiol Spectrum 3(2):MDNA3-0001-2014. doi:10.1128/microbiolspec.MDNA3-0001-2014.

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RNA Polymerase II
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/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0001-2014
2015-03-12
2017-11-18

Abstract:

Although most of non-long terminal repeat (non-LTR) retrotransposons are incorporated in the host genome almost randomly, some non-LTR retrotransposons are incorporated into specific sequences within a target site. On the basis of structural and phylogenetic features, non-LTR retrotransposons are classified into two large groups, restriction enzyme-like endonuclease (RLE)-encoding elements and apurinic/apyrimidinic endonuclease (APE)-encoding elements. All clades of RLE-encoding non-LTR retrotransposons include site-specific elements. However, only two of more than 20 APE-encoding clades, Tx1 and R1, contain site-specific non-LTR elements. Site-specific non-LTR retrotransposons usually target within multi-copy RNA genes, such as rRNA gene (rDNA) clusters, or repetitive genomic sequences, such as telomeric repeats; this behavior may be a symbiotic strategy to reduce the damage to the host genome. Site- and sequence-specificity are variable even among closely related non-LTR elements and appeared to have changed during evolution. In the APE-encoding elements, the primary determinant of the sequence- specific integration is APE itself, which nicks one strand of the target DNA during the initiation of target primed reverse transcription (TPRT). However, other factors, such as interaction between mRNA and the target DNA, and access to the target region in the nuclei also affect the sequence-specificity. In contrast, in the RLE-encoding elements, DNA-binding motifs appear to affect their sequence-specificity, rather than the RLE domain itself. Highly specific integration properties of these site-specific non-LTR elements make them ideal alternative tools for sequence-specific gene delivery, particularly for therapeutic purposes in human diseases.

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FIGURE 1

Two types of genomic insertion of non-LTR elements. doi:10.1128/microbiolspec.MDNA3-0001-2014.f1

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0001-2014
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FIGURE 2

Schematic structure of each clade of site-specific non-LTR retrotransposons. The ORF1 in APE-encoding elements is shown as a short rectangle. An ORF2 in APE-encoding elements or ORF in RLE-encoding elements is shown as a long rectangle. A ZF-like structure is shown as a vertical bold line. A ZF-like structure in ORF1 of APE-encoding elements is shown as a zinc knuckle: Cx2Cx4Hx4Cx5-8Cx2Cx3Hx4C. In R2 clade elements, some elements have an additional ZF-like structure shown as a dotted vertical line. Myb-like (Myb) domains are found in R2 clade-elements and in TRAS families in the R1-clade. doi:10.1128/microbiolspec.MDNA3-0001-2014.f2

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0001-2014
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FIGURE 3

rDNA-specific-elements (R-elements) and telomere-specific-elements. Locations and insertion sites of rDNA-specific non-LTR elements (A) and telomere-specific non-LTR elements (B) are shown schematically. Arrows indicate the 5′ to 3′ orientation of non-LTR element insertion. Three telomere-specific elements, TART, HeT-A, and TAHRE, in are located at extreme ends of chromosome (their locations are in random order). doi:10.1128/microbiolspec.MDNA3-0001-2014.f3

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0001-2014
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FIGURE 4

Evolution of target sequences in R1-clade elements. The phylogeny is constructed on the basis of data in K. K. Kojima and H. Fujiwara ( 16 ). Nonsequence-specific elements are shown as dotted lines and asterisks. Target and flanking sequences of each site-specific element are shown on the right. In the TPRT model, the bottom strand is first nicked and then the top strand is cleaved. The SART and TRAS elements target the same (TTAGG/CCATT) telomeric repeats. However, TRAS first cut the TTAGG bottom strand, whereas SART first cut the CCTAA strand. The bottom-to-top strand cleavage in each target sequence is represented by bent lines. Arrows indicate variation of top-strand cleavage. Broken lines between the top and bottom strands, in TRAS, SART, Waldo, and Mino, indicate unidentified exact cleavage sites because they target the tandem repeats TTAGG and ACAY (or AC). Broken boxes indicate homologous sequences near cleavage sites among RT and R7. doi:10.1128/microbiolspec.MDNA3-0001-2014.f4

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0001-2014
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FIGURE 5

Evolution of telomere and TERT structure in higher insects. X in indicates the loss of a TERT gene from the genome. In the silkworm () and the flour beetle (), introns and GQ domains are lost from TERT genes (see text). The phylogenetic tree was constructed based on recent reports ( 71 , 72 ). doi:10.1128/microbiolspec.MDNA3-0001-2014.f5

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0001-2014
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FIGURE 6

Structures of the silkworm TERT gene. (A) The position of upstream ATG in several TERT genes. The numbers of upstream ATG in each 5′ UTR of TERT are shown on the right. (B) Polyadenylation site of TERT. Poly (A) sequences at the 3′ ends of the TERT gene in genomic DNA and cDNA (corresponding to the mRNA sequence) are shown in bold. (C) The schematic model for the generation of a processed TERT gene from the original TERT with introns by reverse transcription. Four exons are shown as Ex-A to Ex-D. doi:10.1128/microbiolspec.MDNA3-0001-2014.f6

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0001-2014
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FIGURE 7

Schematic model for interaction between mRNA of a site-specific non-LTR element and target DNA at the 3′ junction. (A) Interaction between the read-through transcript of a non-LTR element (from copy1) and the target site DNA at the 3′ junction of copy 3. (B) Annealing of R2Ol mRNA with the target DNA (28S rDNA) at the 3′ junction. -transcribed R2Ol with 4 bp of the 28S target sequence at its 3′ end showed the accurate and efficient retrotransposition in the zebrafish embryo. However, the R2Ol mRNA with 3 bp of the 28S target sequence showed insufficient retrotransposition (39%) (H. Mizuno and H. Fujiwara, unpublished data). These observations indicate that annealing of the read-though product of R2Ol to the target DNA at the 3′ junction seems important for its efficient and accurate retrotransposition. doi:10.1128/microbiolspec.MDNA3-0001-2014.f7

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0001-2014
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FIGURE 8

Main factors involved in the target-site selection of site-specific APE-encoding elements. Four main steps of the retrotransposition of non-LTR elements in the cells (transcription, translation, RNP formation, and nuclear import) are shown schematically. Three factors involved in the target-site selection are indicated. doi:10.1128/microbiolspec.MDNA3-0001-2014.f8

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0001-2014
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Tables

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TABLE 1

Targets of site-specific non-LTR retrotransposons

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0001-2014

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