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Chapter 10 : Serine Resolvases

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Abstract:

The serine resolvases are a group of recombinases that, in their native contexts, resolve large fused replicons into smaller separated ones ( ). Serine resolvases and the closely related invertases were the first serine recombinases to be studied in detail, and much of our understanding of the serine recombinase mechanism is owed to those early studies. Resolvases and invertases have also served as paradigms for understanding how DNA topology can be harnessed to regulate recombination reactions ( ). Like other serine recombinases, the resolvases have a largely modular structure. In the resolvase case, the conserved catalytic domain is followed by a DNA-binding domain that is a simple helix-turn-helix similar to that found in many prokaryotic repressors ( ). This modularity, combined with a wealth of structural and biochemical data, has made them good targets for engineering chimeric recombinases with designer sequence specificity ( ).

Citation: Rice P. 2015. Serine Resolvases, p 237-252. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0045-2014

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Figures

Image of Figure 1
Figure 1

Cartoon of serine resolvase-mediated strand exchange. The wild-type protein initially binds crossover sites as an inactive dimer. Upon activation (see text), the catalytic domains (labeled “Cat.”) form a tetramer that synapses the two partner sites. Within the tetramer, the active site serines (red dots) attack the DNA, creating double strand breaks with 5′ phosphoserine linkages and 2-nucleotide 3′ overhangs. Two subunits and the DNA segments covalently linked to them can then rotate relative to the other two. A 180° rotation aligns the broken ends for re-ligation in the recombinant configuration. Much of both the dimer and tetramer interface is contributed by helix E. doi:10.1128/microbiolspec.MDNA3-0045-2014.f1

Citation: Rice P. 2015. Serine Resolvases, p 237-252. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0045-2014
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Image of Figure 2
Figure 2

Biological roles for resolvases. (A) Some resolvases (e.g., γδ and Tn3) are encoded by replicative transposons. Their transposition creates a branched intermediate (center panel) that is processed by the host replication and repair machinery (new DNA strands are in blue) to yield a “cointegrate” (fourth panel) in which both the donor and recipient replicons are fused. Resolvase action at a site within the transposon (yellow) resolves the cointegrate into the original donor and the recipient that now carries a copy of the transposon. (B) Some resolvases (e.g., β and Sin) are encoded by plasmids. Rescue of a stalled replication fork by a homologous recombination-mediated pathway can lead to a Holliday Junction (HJ) behind the rescued fork (second panel). Depending on which pair of strands is cut to resolve the Holliday Junction, replication results in two daughter circles (upper branch) or in a plasmid dimer (lower branch). Action of the plasmid-encoded resolvase at a site (yellow) converts this dimer into two daughter circles. In both examples, the product circles are initially linked as catenanes (not shown for simplicity; see Figure 3 ) that are later separated by a host type II topoisomerase. doi:10.1128/microbiolspec.MDNA3-0045-2014.f2

Citation: Rice P. 2015. Serine Resolvases, p 237-252. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0045-2014
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Image of Figure 3
Figure 3

sites and the topology of the synaptosome. (A) Examples of serine resolvase sites. Specific recognition sequences (∼12 bp each) for individual resolvase subunits are shown as colored boxes: green for the crossover site (always an inverted repeat), purple for accessory sites that form direct repeats, and yellow for accessory sites that form inverted repeats. The recombinase dimers bound to the accessory sites are catalytically inactive, and these sites always differ from the crossover site in the length of their central spacers and/or the relative orientation of their half-sites. Sin and related resolvases require a DNA bending protein as well as additional recombinase subunits. The coding sequence for the resolvase protein is usually adjacent to its cognate site. Figure adapted from reference ( ) with permission. (B) Resolvase synaptosomes trap 3 supercoiling nodes. The resolvase and accessory proteins (if any) bound to each of the cognate sites form a complex (the “synaptosome”) that traps 3 dsDNA-over-dsDNA crossings and juxtaposes the two site Is. Synaptosome formation activates the site I-bound resolvase subunits, which then introduce double-strand breaks. A 180° rotation of the bottom two subunits (as drawn) realigns the broken ends, which are then re-ligated. In a negatively supercoiled substrate a right-handed rotation is favored because it introduces a + supercoiling node (ΔLk = +1) that cancels one of the pre-existing (–) nodes trapped in the synaptosome and because it allows rewinding of each duplex by a half turn (ΔTw for each = +½). The remaining two crossings trapped by the synaptosome are no longer intramolecular and instead catenate the two daughter circles (which can be separated by a host type II topoisomerase). doi:10.1128/microbiolspec.MDNA3-0045-2014.f3

Citation: Rice P. 2015. Serine Resolvases, p 237-252. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0045-2014
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Image of Figure 4
Figure 4

Serine resolvase structures. (A) Wild-type γδ resolvase bound to crossover site (or “site I”) DNA. The active site serine residues are marked with red spheres (PDBid 1gdt; ( )). (B) Activated mutant γδ resolvase with crossover site DNA in the covalent protein–DNA intermediate state. Note that each catalytic domain has undergone major conformational changes in the transition from dimer to tetramer (PDBid 2gm4; ( )). (C) The same structure as in B, rotated by ∼90° about a horizontal axis. (D) Activated Sin resolvase tetramer catalytic domain tetramer. Sulfate ions that mark the binding pockets for the scissile phosphate are shown as sticks (PDBid 3pkz) ( ). doi:10.1128/microbiolspec.MDNA3-0045-2014.f4

Citation: Rice P. 2015. Serine Resolvases, p 237-252. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0045-2014
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Image of Figure 5
Figure 5

Intramolecular conformational changes upon activation. (A) Superposition, using the E-helices as guides, of one subunit from an activated, DNA-bound γδ resolvase tetramer (green) in a post-cleavage state with one from an inactive wild-type γδ dimer (light green) (PDBids 2gm4 and 2rsl ( )). Red spheres mark the α carbons of the active site serines (S10 for γδ, S9 for Sin); green and blue spheres those of the probable general acid R71 (γδ)/R69 (Sin). (B) Similar superposition of the same activated γδ subunit as in (A), and one subunit from an activated Sin tetramer that appeared to be in the cleavage-ready state (PDBid 3pkz, ( )). doi:10.1128/microbiolspec.MDNA3-0045-2014.f5

Citation: Rice P. 2015. Serine Resolvases, p 237-252. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0045-2014
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Image of Figure 6
Figure 6

Structures of serine recombinase tetramers in three different rotational states. Colors are as in Figure 4 , except that the E-helices are highlighted in yellow (green subunits) and magenta (blue subunits). (A) Activated γδ resolvase tetramer; (B) activated Sin resolvase tetramer; (C) activated Gin invertase tetramer. PDBids 2gm4, 3pkz, and 3uj3, respectively ( ). doi:10.1128/microbiolspec.MDNA3-0045-2014.f6

Citation: Rice P. 2015. Serine Resolvases, p 237-252. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0045-2014
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Image of Figure 7
Figure 7

Modeling the Sin synaptosome. (A) Two orthogonal views of the structure of a tetramer of WT Sin resolvase bound to its cognate site II. In the left panel, the catalytic domains of the lower dimer are oriented in a similar way to those of wild-type γδ resolvase in Figure 4(A) . The dimer–dimer contacts are mediated by the DNA-binding domains (PDBid 2r0q ( )). Yellow arrows show the orientations of the individual monomer-binding sites in the DNA. (B) Model for the synaptosome, created by rigid-body docking together of a symmetrized version of an activated γδ resolvase tetramer–DNA structure (blue and green proteins), two copies of an IHF–DNA complex structure (pink proteins), and the Sin–site II structure (purple proteins). The DNAs are shown as smoothed green and blue surfaces. The view is the same as for the right hand panel of (A). PDBids 1zr4, 1ihf, and 2r0q were used ( ). (C) Cartoon similar to that in Figure 3B showing the expected synaptosome topology. Yellow arrows mark the orientations of the half-sites within each dimer-binding site. (D) Second view of the synaptosome model, rotated 90° about a horizontal axis. doi:10.1128/microbiolspec.MDNA3-0045-2014.f7

Citation: Rice P. 2015. Serine Resolvases, p 237-252. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0045-2014
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Image of Figure 8
Figure 8

Interdimer contacts within the synaptosome may affect the dimer–tetramer equilibrium. A wild-type Sin dimer (yellow) is superimposed on two subunits from the activated Sin tetramer (blue). Red spheres mark the α carbons of the catalytic serines, and other spheres mark the positions of side chains whose mutation interferes with interdimer contacts in Sin and γδ resolvases and with catalytic domain–DNA contacts in the related Hin invertase ( ). doi:10.1128/microbiolspec.MDNA3-0045-2014.f8

Citation: Rice P. 2015. Serine Resolvases, p 237-252. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0045-2014
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Image of Figure 9
Figure 9

Details of the Sin active site. (A) Stereo view of one subunit from an activated Sin tetramer (PDBid 3pkz ( )). A sulfate ion marks the scissile-phosphate binding pocket, and side chains important for catalysis are shown as sticks. Those residues whose mutation had the most deleterious effect on the rate of DNA cleavage by Tn3 resolvase are shown in magenta, shading to white for those whose mutation had more moderate effects ( ). (B) Stereo view of one subunit from a site II-bound wild-type Sin dimer (PDBid 2r0q ( )). The same side chains are shown, similarly shaded from a dark color to white. doi:10.1128/microbiolspec.MDNA3-0045-2014.f9

Citation: Rice P. 2015. Serine Resolvases, p 237-252. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0045-2014
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Image of Figure 10
Figure 10

Superposition of all currently published serine resolvase catalytic domain structures, aligned using their E helices as guides. Each structure is shaded from blue (N-ter) to red (end of catalytic domain), and all unique copies from the asymmetric unit for each structure were used (two to four per structure). Colored spheres mark the positions of the active site serines. From right to left (roughly), they are: light blue, wild-type (WT) Sin from the Sin–site II structure (PDBid 2r0q); dark blue, WT γδ determined without DNA (PDBid 2rsl); green, WT γδ from the γδ–site I complex structure (PDBid 1gdt); yellow, activated γδ from a structure without DNA (PDBid 2gm5); orange and red, two different activated variants of γδ from structures with covalently linked crossover site DNA (PDBids 1zr4 and 2gm4, respectively), and pink, activated Sin tetramer (determined without DNA; PDBid 1pkz). Black and Gray spheres mark the Cα positions of the probable general acid R71 (γδ)/R69 (Sin). Those that cluster towards the left are in structures of activated mutants, whereas those that cluster towards the right are from WT structures. doi:10.1128/microbiolspec.MDNA3-0045-2014.f10

Citation: Rice P. 2015. Serine Resolvases, p 237-252. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0045-2014
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