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Chapter 36 : Telomeres and Transposable Elements

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Abstract:

This chapter describes what is known about the two telomere-specific retrotransposons, and . Although is the only organism in which the telomerase-telomere is known to be completely replaced by retrotransposons, there are now a few examples of other retrotransposons that associate specifically with telomerase-telomeres. These telomere-associated retrotransposons are also discussed. Phylogenetic analysis of the reverse transcriptase (RT) and endonuclease domains of places it in the Jockey clade of arthropod non-LTR elements. In summary, studies of argue that and are converging on their telomere specialization, rather than diverging from a common ancestor. Their primary shared characters are the gag coding sequence and the telomere targeting. This suggests that the gag protein may have a role in delivering the elements to chromosome ends, a hypothesis that is being actively investigated. Although is the only organism known to have retrotransposon-telomeres instead of telomerase-telomeres, retrotransposons with a special relationship to telomerase-telomeres have been described for several organisms. Elements transposing as DNA have not been reported in terminal sequences, although DNA transposons are found in subtelomeric satellite regions. The amplified telomere sequences solve the problem of chromosome shortening. In most organisms, the length of telomeric arrays is much greater than needed to replace end erosion, and these sequences seem to have additional roles. The evidence suggesting relationships between telomeres and cell life span, tumorigenesis, and cell cycle checkpoints hints that these roles are important.

Citation: Pardue M, Debaryshe P. 2002. Telomeres and Transposable Elements, p 870-888. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch36

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Figures

Image of Figure 1
Figure 1

telomere retrotransposons. Elements are diagrammed as their putative RNA transposition intermediates. The 5′ noncoding regions (5′-UTR), open reading frames (ORFs), and 3′ noncoding regions (3′-UTR) are indicated. AAAAA indicates the poly(A) tail on the RNA (and the [dA/T] region joining each element to the more proximal region of the chromosome in the DNA copy). The question mark at the 5′ end of indicates that the 5′ end of this element has not yet been completely defined. The black bar running through the 5′-UTRand extending into ORF1 indicates a sequence that is perfectly repeated at the site of the second black bar in the 3′-UTR. Each subfamily of has a pair of these perfect nonterminal repeats (see “What is the relationship between and ?” in the text).

Citation: Pardue M, Debaryshe P. 2002. Telomeres and Transposable Elements, p 870-888. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch36
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Image of Figure 2
Figure 2

Diagram summarizing the current picture of the ends of chromosomes. The large solid arrows represent and elements intermixed on the end of each chromosome. Each element is attached to the chromosome by its poly(A) end (depicted by an arrowhead), producing a polarized array. The hatched bar at right represents the subtelomeric region of the chromosome, which extends to the right. Poly(A)transcripts of and shown below the chromosome end serve as both mRNAs and as templates for reverse transcription onto the extreme end of the chromosome.

Citation: Pardue M, Debaryshe P. 2002. Telomeres and Transposable Elements, p 870-888. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch36
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Image of Figure 3
Figure 3

Comparison of the mechanism by which telomerase extends chromosome ends with the mechanism proposed for telomeres. (Top) The protein components of telomerase (gray) associate with the end of the chromosomal DNA molecule. The RNA component of telomerase (black) is aligned with the 3′end of the DNA and a short sequence in the center of this RNA (AACCCCAAC, in this case) is copied repeatedly into DNA attached to the chromosome. A, C, G, and T refer to free dNTPs. (Bottom) In RNA becomes associated with reverse transcriptase (gray). (This RNA is drawn as a black line with an arrowhead to indicate that the total length of the transposition intermediate is not shown here.) The 3′-poly(A) of RNA is aligned with the end of the chromosomal DNA and the rest of the RNA is copied into DNA to extend the chromosome by a mechanism analogous to the one used by telomerase. Telomerase and reverse transcriptase both extend only one strand of DNA. Presumably, the second strand of DNA is then replicated by DNA polymerase (from reference , reprinted with permission from Elsevier Science).

Citation: Pardue M, Debaryshe P. 2002. Telomeres and Transposable Elements, p 870-888. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch36
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Image of Figure 4
Figure 4

Dot matrix analysis showing the regularly spaced regions of A-rich segments of the 3′-UTRof from The nucleotide sequence of element 23Zn-1 is compared with itself at a stringency of ∼60%. (The element is compared with itself because this is the only element for which the complete sequence is available. A similar picture is found when any of the partial sequences of other elements are used.) The regular patterns of clusters flanking the major diagonal in the 5′-UTRand 3′-UTRmark the locations of the A-rich regions. Comparisons of 3′-UTRsequence from different subfamilies are shown in Figs. 5 and 6 . All comparisons were done with Dotty Plotter (Version 1.0, D. Gilbert) with a window of 25 and a stringency of 15.

Citation: Pardue M, Debaryshe P. 2002. Telomeres and Transposable Elements, p 870-888. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch36
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Figure 5

Dot matrix analysis comparing the nucleotide sequences of elements from and The comparison is done at a stringency of 60%. The coding regions have 64% identity. Identical nucleotides are spread relatively evenly and thus give a nearly continuous major diagonal line over the entire region. The 5′-UTR and 3′-UTR have only 48% identity. This identity is most pronounced in the most 3′ sequences (upper right), and a diagonal line is detected there; however, throughout most of these regions sequence identity is too low to yield a line on the major diagonal. Despite this sequence change, the regular pattern of A-rich sequences is conserved, as indicated by the off-diagonal clusters. All comparisons were done with use of Dotty Plotter with a window of 25 and a stringency of 15.

Citation: Pardue M, Debaryshe P. 2002. Telomeres and Transposable Elements, p 870-888. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch36
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Image of Figure 6
Figure 6

Dot matrix analysis comparing the nucleotide sequences from 3′-UTRs of different subfamilies. The 3′-UTR of element 23Zn-1 (2,586 bp) is compared with the 3′-UTR of element RT473 (2,456 bp) (A) and element 44P (2,336 bp) (B). Breaks in the diagonal line of identity indicate large insertions or deletions. Where sequence can be compared, 23Zn-1 has 80.5% identity with RT473 and 93.1% identity with 44P. All comparisons show marked patterns of off-diagonal clusters indicating A-rich repeats. Note particularly the close-packed array of three repeated clusters in 23Zn-1, four repeated clusters in 44P, and five repeated clusters in RT473.

Citation: Pardue M, Debaryshe P. 2002. Telomeres and Transposable Elements, p 870-888. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch36
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Image of Figure 7
Figure 7

The 3′ promoter of has features of a proto-LTR. Two tandem elements are depicted with the DNA diagrammed as in Fig. 1 . The region of the upstream element with maximal promoter activity is outlined by an arrowhead, and the equivalent region of the element being transcribed is similarly marked to indicate the formal similarity to an LTR. The start of transcription within the upstream element is indicated. In the RNA transcript diagrammed below the two elements, the darker segments on either end indicate terminal redundancy produced because transcription starts in the upstream element, which adds a short sequence identical with the 3′ end of the downstream element.

Citation: Pardue M, Debaryshe P. 2002. Telomeres and Transposable Elements, p 870-888. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch36
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Image of Figure 8
Figure 8

The retrotransposable element, may have evolved from components of telomerase. This figure suggests one possible way in which the evolution could have occurred. (From reference , reprinted with permission from Springer.)

Citation: Pardue M, Debaryshe P. 2002. Telomeres and Transposable Elements, p 870-888. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch36
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Tables

Generic image for table
Table 1

Base compositions of 3' noncoding regions of elements

Citation: Pardue M, Debaryshe P. 2002. Telomeres and Transposable Elements, p 870-888. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch36

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