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Chapter 19 : Overview of Homologous Recombination and Repair Machines

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Abstract:

The study of homologous recombination between plasmids, or between a plasmid and the chromosome, revealed that the RecFOR pathway is less of a poor cousin than first thought. When the exquisite sensitivity to DNA damage of the first recombination-deficient mutants was found, it became clear that homologous recombination might be the only way to repair certain DNA lesions. Generally, the stronger the defect in homologous recombination, the higher the sensitivity to DNA damage. In , chromosomal lesions are repaired by homology-guided strand exchange between sister chromatids. The evidence in support of this notion comes in three forms. First, physical connections between parental and daughter strands, associated with lesion repair, can be detected. Second, repair of chromosomal lesions is not observed in mutants. Third, DNA damage stimulates homologous recombination although the structure of chromosomal lesions in this case is unspecified. Single-stranded DNA-binding protein (SSB) complexes single-stranded DNA (ssDNA), facilitating its subsequent use in replication and in degradation and repair pathways of DNA metabolism. Chromosomal dimerization in creates a chromosomal lesion, because it prevents segregation of the replicated chromosomes into daughter cells. The understanding of the formation of replication-dependent chromosomal lesions is still primitive. There is one in vivo study on the structure of stalled replication forks, a report documenting replication fork reversal in vivo, as well as a few reports of replication fork reversal in vitro, likely to be an artifact of DNA isolation.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 1

Basic types of merozygotes to detect homologous recombination in bacteria. See text for explanation.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 2

Genetic pathways for homologous recombination in E. coli. See text for explanation.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 3

The idea of recombinational repair. (A) Two homologous chromosomes: the top one has a two-strand DNA lesion, and the bottom one is intact. (B) Homologous pairing and strand exchange between the two homologues, leading to conversion of the two-strand DNA lesion into a pair of one-strand DNA lesions in the hybrid DNA segments, bracketed by the double Holliday junction. One of two possible directions of the junction resolution is indicated by small arrows. (C) Holliday junction resolution breaks the joint molecule apart. (D) Excision repair removes the one-strand lesions. Open double line, the intact duplex; filled double line, the duplex with DNA lesions; lollipops in the filled strands, one-strand DNA lesions.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 4

Configuration of chromosomal lesions.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 5

Formation of a daughter-strand gap during replication fork passage over a noncoding lesion. (A) A replication fork approaching a pyrimidine dimer. (B) The replication fork is traversing the pyrimidine dimer. (C) The stalled replisome is released, while the fork recruits a new replisome to reinitiate downstream from the lesion. (D) The replication fork moves away, leaving behind a daughter-strand gap. T=T, pyrimidine dimer (a noncoding lesion).

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 6

Replication fork collapse at a single-strand interruption in template DNA. (A) A replication fork. (B) The replication fork is approaching a single-strand interruption. (C) The replication fork has reached the interruption and come apart (collapsed). (D) The single-strand interruption in the full-length chromosome is repaired, while the detached double-strand end awaits its fate.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 7

Replication fork collapse as a chromosomal lesion. (A) A theta-replicating chromosome. (B) As a result of collapse of the right replication fork, the chromosome starts replicating as a sigmastructure. (C) Collapse of the second replication fork terminates sigma-replication. (D) Collapse of the second replication fork linearizes the chromosome.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 8

Regression of a stalled replication fork with subsequent resetting or breakage. The shaded circle indicates a protein tightly bound to the template DNA. (A) A replication fork approaches a block in the downstream template. (B) The replication fork stalls at the block. (C) The replication fork regresses from the block, forming a Holliday junction and extruding the newly replicated strands in a duplex of their own. (D) The regressed replication fork is reset and the block is removed. (E) A nuclease degrades the extruded fourth arm, recreating the replication fork structure. (F) Resolution of the Holliday junction leads to replication fork breakage. (G) Closure of the nicks completes the formation of a chromosomal lesion, in this case a double-strand end.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 9

Locking and unlocking of a replication fork stalled at a small palindrome: a hypothesis. (A) A replication fork approaches a block in the downstream template, which happens to be near a small palindrome. (B) The replication fork is stalled at the block; one strand of the palindrome is replicated, while the opposite strand is complexed with SSB and remains single stranded. (C) The replication fork regresses from the block, extruding the newly replicated strand. The possibility of homologous pairing between the single-strand regions is shown by arrows. (D) Template switching due to the annealing of the complementary strands. (E) DNA synthesis, primed by the switched end, locks the replication fork. (F) Further regression of the locked replication fork extrudes the palindrome into a hairpin. (G) Hairpin degradation by SbcCD regenerates a replication fork structure. Shaded circle, a protein tightly bound to the template DNA; black and white arrows, palindrome (a black arrow forms a duplex with a codirectional white arrow).

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 10

The two hypothetical pathways of recombinational repair. A scheme for daughter-strand gap repair, catalyzed by RecFOR and RecA, is shown on the left; a scheme for double-strand-end repair, catalyzed by RecBCD and RecA, is shown on the right. T=T, pyrimidine dimer (a noncoding lesion).

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 11

Holliday junction processing by the RuvABC resolvasome. (A) A Holliday junction in the folded conformation (difficult to process but preferred in physiological conditions). The arrow indicates the 1808 rotation required to convert the folded conformation into the square planar one. (B) A Holliday junction in the square planar conformation (easy to process, observed in the absence of Mg2þ ions). (C) RuvA tetramers bind Holliday junctions under physiological conditions and isomerize them into the square planar conformation. (D) RuvB hexamers are shown as washers on opposite arms of the Holliday junction; they interact with RuvA and “pump” DNA through their central openings (the direction of DNA movement is shown by arrows). At this stage of the Holliday junction processing, two RuvA tetramers assemble around the junction in a turtle-shell configuration (not shown). (E) One of the RuvA tetramers is replaced with a RuvC dimer (two circles), while the RuvC consensus resolution sequences (diamonds) are drawn into the junction by RuvB pumping. (F) RuvC symmetrically cuts at the resolution consensus sequences, resolving the joint molecule (RuvABC proteins are not shown). The two original duplexes, forming a joint molecule, are shown as either open or filled double lines.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 12

The two ways of restoring theta-replication to a circular chromosome that suffered replication fork collapse. (A) A theta-replicating chromosome. (B) The right fork of the replication bubble has collapsed, shifting chromosome replication into sigma-mode. (C) RecBCD- and RecA-catalyzed strand exchange restores replication fork structure, returning the chromosome to theta-replication. (D) RecBCD-catalyzed degradation of the linear tail makes theta-replication possible again without repairing the collapsed replication fork.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Figure 13

A hypothetical, RecG-dependent way of Holliday junction processing. (A) An end-invasion intermediate, with the 3′ end being extended by DNA pol I. (B) DNA pol I cleaves the displaced strand and starts nick-translating. (C) DNA ligase seals the nick, while RecG helicase binds to the side of the Holliday junction opposite the side bound by the RecA filament. (D) RecG translocates the Holliday junction toward the DNA end, dispersing the RecA filament and restoring replication fork structure. Rectangle with rounded corners, RecA filament; gray oval, RecG; open circles, RecA monomers; small arrow, the position of DNA strand cleavage; one-sided arrow, the 3′end used by DNA pol I.

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
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Tables

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Table 1

Viability of homologous recombination mutants and their sensitivity to different kinds of DNA-damaging treatments

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19
Generic image for table
Table 2

The pageant of homologous recombination enzymes of E. coli

Citation: Kuzminov A, Stahl F. 2005. Overview of Homologous Recombination and Repair Machines, p 349-368. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch19

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