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Chapter 37 : IS91 Rolling-Circle Transposition

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Abstract:

This chapter reviews a class of insertion sequence (IS) elements, the IS family, that occupies a definite genetic niche, probably as a consequence of a rather peculiar transposition mechanism. It encompasses and summarizes the results obtained in our study of rolling circle (RC) transposition. The analysis is mainly based on IS, the family prototype and the element studied in greatest detail. The fact that different family members, such as IS and IS, appeared close to each other in association with virulence genes suggests that they are particularly adapted to move about this type of sequence. In summary, two conclusions can be drawn from analysis of the reported BLAST hits. Most if not all of the observed hits correspond to partial IS-like elements, starting precisely at one or the other terminus (or ) and ending up at widely variable positions within the element, and most of the hits are adjacent to functional bacterial virulence genes harbored in known virulence plasmids (and not in antibiotic resistance plasmids). The search was complicated by the fact that the conserved motifs are also present in Rep proteins of rolling-circle (RC)-replication plasmids and phages, and these are ubiquitous. Hairpin structures remind one of RC phage and plasmid replication origins. The authors say that a more detailed analysis is in progress that will define the commonalities and specificities of each of the family elements.

Citation: Garcillán-Barcia M, Bernales I, Mendiola M, De La Cruz F. 2002. IS91 Rolling-Circle Transposition, p 891-904. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch37

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Figures

Image of Figure 1
Figure 1

ISgenetic structure ( ). The top drawing represents the complete IS element, pointing out the coding frames, the termini (arrowheads), and the target CTTG or GTTC sequences, which are always adjacent to IR. The two central drawings are a close-up to the extended termini, and (see also Fig. 3 ). Thick black arrows represent inverted repeat sequences thought to be functionally important. The two bottom drawings focus on the DNA sequences at the ends of the element. The thin arrows below the sequences point out the short interrupted inverted repeat at the termini.

Citation: Garcillán-Barcia M, Bernales I, Mendiola M, De La Cruz F. 2002. IS91 Rolling-Circle Transposition, p 891-904. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch37
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Image of Figure 2
Figure 2

Alignment of IS-like transposases. The figure shows the amino acid sequences of eight IS-like transposases around five conserved motifs, which are also shared by RC-replication plasmids and ssDNA phages (the amino acid sequence of ϕX174 gpA protein around motifs II to V is shown for comparison. The most conserved segments are underlined). See Table 2 for reference to the transposase names. TnpA_Fusne and TnpA_Psepa represent partial sequences that are missing motifs I and II. Invariant residues are boxed. Conserved residues are shown on a gray background. Sequences were aligned using the CLUSTALW global alignment algorithm.

Citation: Garcillán-Barcia M, Bernales I, Mendiola M, De La Cruz F. 2002. IS91 Rolling-Circle Transposition, p 891-904. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch37
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Image of Figure 3
Figure 3

DNA sequence comparisons among the termini of IS IS and IS Asterisks point out residues conserved with respect to IS The CTTG sequences shown in brackets do not belong to the IS elements. Horizontal arrows point out inverted repeat sequences (sometimes imperfect), (A) regions, (B) regions.

Citation: Garcillán-Barcia M, Bernales I, Mendiola M, De La Cruz F. 2002. IS91 Rolling-Circle Transposition, p 891-904. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch37
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Image of Figure 4
Figure 4

Structural and sequence similarities between and RC-replication origin of plasmid pC194. The DNA sequences at and ( Fig. 2 ) are drawn to show their palindromic sequences for a better comparison to pC194 Nick points to the cleavage site used for initiation of replication or transposition. See Espinosa et al. ( ) for a discussion of the roles of the different pC194 structural elements in pC194 function.

Citation: Garcillán-Barcia M, Bernales I, Mendiola M, De La Cruz F. 2002. IS91 Rolling-Circle Transposition, p 891-904. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch37
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Image of Figure 5
Figure 5

A concerted RC-transposition model (modified from Mendiola et al. [ ]). For each step of the reaction, both strands of the donor (top lines) and recipient (bottom lines) DNAs are shown as linear DNAs, with arrowheads pointing to the 3′ends of the molecules. Thick continuous lines represent preexisting IS sequences, dotted lines represent newly synthesized IS sequences, and thin lines represent nontransposon sequences. A single transposase monomer (irregular shape) binds to both donor and recipient DNAs. A first cleavage reaction (3′of the CTTG sequence) covalently joins one tyrosyl residue (Y1) to the 5′end of the cleavage site at (step b). A second cleavage reaction covalently joins the second tyrosyl residue (Y2) to the target DNA (3′of a CTTG sequence in the target DNA). The displaced 3′-hydroxyl of the target DNA attacks the DNA-Y1 bond, causing the strand-transfer reaction that covalently binds donor and recipient DNAs (step c). The resulting DNA complex could be worked upon by a variety of replication/recombination/repair systems in the bacterial cell. By analogy with RC-replication phages, we assume that a DNA helicase (ellipse) helps unwind the DNA with a 5′to 3′polarity, and this allows recruitment of the DNA polymerase holoenzyme (large shaded circle) and leading-strand DNA synthesis by RC replication (step d). The displaced strand is progressively coated by SSB (small circles). Upon arrival to the transposase catalyzes a second strand-transfer reaction. Y1 cleaves the 3′end of and becomes covalently linked to the 5′end of the nick. The resulting free 3′-hydroxyl in turn attacks the Y2-target DNA bond, covalently linking to the target DNA and freeing the transposase from it. The overall result of the transposition reaction is the transfer of a single preexisting strand of IS to the target site of the recipient DNA (step e). The bacterial replication machinery can passively replicate this looped DNA.

Citation: Garcillán-Barcia M, Bernales I, Mendiola M, De La Cruz F. 2002. IS91 Rolling-Circle Transposition, p 891-904. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch37
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Tables

Generic image for table
Table 1

Database sequences related to ISfamily elements

Citation: Garcillán-Barcia M, Bernales I, Mendiola M, De La Cruz F. 2002. IS91 Rolling-Circle Transposition, p 891-904. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch37
Generic image for table
Table 2

Protein sequences related to IStransposase

Citation: Garcillán-Barcia M, Bernales I, Mendiola M, De La Cruz F. 2002. IS91 Rolling-Circle Transposition, p 891-904. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch37

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