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Chapter 21 : Homologous Recombination by the RecBCD and RecF Pathways

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Homologous Recombination by the RecBCD and RecF Pathways, Page 1 of 2

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Abstract:

Interaction with χ affects the helicase activity of RecBCD enzyme. Recognition of χ causes the enzyme to pause briefly at χ and to resume translocation after the χ site, but at a rate that is reduced by approximately twofold. In response to χ the RecBCD enzyme accomplishes both tasks essential for initiation of homologous recombination: (i) it recesses the double-strand break (DSB) to produce an ssDNA-tailed duplex DNA with χ at its terminus, and (ii) it catalyzes formation of the RecA nucleoprotein filament on the ssDNA produced. Interestingly, the efficiency of conjugational and transductional recombination by the RecF pathway in the recBC sbcBC cells is similar to that of the RecBCD pathway in wild-type cells, showing that the machinery of this pathway can be as productive as that of the RecBCD pathway. The loading of RecA protein is an essential aspect of recombination in the RecBCD pathway. On the other hand, recB recF double mutants are deficient in recombination between chromosomal direct repeats, suggesting that both RecBCD and RecF pathways play major roles in recombination. Homologous recombination can be initiated at either DSBs or single-strand DNA gap (SSG) in duplex DNA. Two major pathways are responsible for homologous recombination in wild-type : The RecBCD pathway is specific for the recombinational repair of DSBs, and in the wild-type cells, the RecF pathway is primarily used for recombination that initiates at SSGs.

Citation: Spies M, Kowalczykowski S. 2005. Homologous Recombination by the RecBCD and RecF Pathways, p 389-403. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch21

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Genetic Recombination
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DNA Synthesis
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Nucleotide Excision Repair
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Cellular Processes
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Escherichia coli
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Figures

Image of Figure 1.
Figure 1.

Recombinational repair of DNA damage. The DNA strands that are used as templates for the leading strand synthesis are shown in black, and the strands used as templates for the lagging strand synthesis are shown in gray. Arrows indicate the direction of DNA synthesis. (A) Recombinational repair of directly induced DSBs. A DSB, which occurs in newly synthesized DNA, can be repaired by completion of the following steps. First, the DSB is processed to produce 3′-terminated ssDNA. Then, one of the ssDNA tails can invade the homologous dsDNA daughter, displacing one of the resident strands to form a D-loop. This structure can be used as a template for DNA synthesis, ultimately resulting in the formation of a Holliday junction. Upon resolution of the Holliday junction, the replication fork is restored to its original form. When a DSB occurs in a part of the chromosome that is not yet replicated, there is no homologous DNA to serve as a template, and such a DSB can be lethal. (B) Recombinational repair of replication-dependent DSBs. DSBs can be produced by replication through a single-strand DNA break. The source of the replication-dependent DSBs is a nick or an ssDNA gap in one of the strands of the replicated DNA molecule. Replication through the strand discontinuity results in the formation of one intact and one broken DNA molecule. The end of the broken chromosome is processed to form a 3′-terminated ssDNA tail, which invades the intact homologous DNA to form a D-loop, which can then be used to restore a normal replication fork. (C) Recombinational repair of replication-dependent SSGs. SSGs can be produced when synthesis of only one DNA strand is halted by an encounter of a noncoding lesion in that DNA strand. After DNA strand exchange of the ssDNA in the gap with a strand in the intact daughter homologue, the displaced DNA strand can be used as a template for DNA synthesis, resulting in the restoration of the replication fork. Upon completion of replication, one of the DNA molecules will still contain the original DNA damage. If this damage is not repaired by the appropriate repair system, then an SSG will be formed again by the next round of DNA replication.

Citation: Spies M, Kowalczykowski S. 2005. Homologous Recombination by the RecBCD and RecF Pathways, p 389-403. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch21
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Image of Figure 2.
Figure 2.

DSBs can be produced as a result of Holliday junction cleavage. Reversal of a stalled DNA replication fork results in the formation of a regressed replication fork, which is a four-way (Holliday) junction that contains a dsDNA end. There are two potential fates for this regressed replication fork: it can be degraded by the recombination machinery to produce a three-way junction that resembles a replication fork, or the Holliday junction can be cleaved to produce a DSB that is repaired by a DSB repair pathway.

Citation: Spies M, Kowalczykowski S. 2005. Homologous Recombination by the RecBCD and RecF Pathways, p 389-403. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch21
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Image of Figure 3.
Figure 3.

Interstrand cross-links are converted into DSBs and SSGs. Schematic representation for the incision-recombination mechanism of interstrand DNA cross-link repair. The repair of an interstrand cross-link depends on both the nucleotide excision repair (NER) and recombination machineries. The NER enzymes make an incision on either side of the lesion on one DNA strand and also displace the cross-link-containing oligonucleotide to produce an SSG; this SSG can be repaired by an SSG repair pathway. However, the incised oligonucleotide remains cross-linked to the second DNA strand. If this lesion is recognized by NER machinery prior to the completion of SSG repair of the top strand, then the subsequent incisions on the second strand convert the interstrand cross-link into a DSB, which is then repaired by a DSB repair pathway.

Citation: Spies M, Kowalczykowski S. 2005. Homologous Recombination by the RecBCD and RecF Pathways, p 389-403. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch21
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Image of Figure 4.
Figure 4.

Initiation of homologous recombination at DSBs by the RecBCD pathway. Schematic representation of the early enzymatic steps of RecBCD pathway of recombinational repair. (a and a′) RecBCD (or RecBC) enzyme binds to the blunt or nearly blunt dsDNA end. (b) RecBCD enzyme uses the energy of ATP hydrolysis to translocate along and to unwind the dsDNA. The associated nuclease activity degrades the newly produced ssDNA. (c) Interaction with χ results in the attenuation of the RecBCD nuclease activity and production of ssDNA terminated with the χ sequence at its 3′ end. (d) The χ-modified enzyme loads RecA protein onto the χ-containing ssDNA to the exclusion of SSB protein, forming a RecA nucleoprotein filament. (e and e′) The RecA-ssDNA nucleoprotein filament invades homologous dsDNA. (b′) The RecBC enzyme (i.e., lacking the RecD subunit) behaves as a constitutively w-modified RecBCD enzyme that can load RecA protein without the need for χ interaction. The RecBC enzyme lacks nuclease activity that is compensated for by the action of the RecJ nuclease.

Citation: Spies M, Kowalczykowski S. 2005. Homologous Recombination by the RecBCD and RecF Pathways, p 389-403. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch21
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Image of Figure 5.
Figure 5.

Initiation of homologous recombination at DSBs by the RecF pathway. Schematic representation of the early enzymatic steps of the RecF pathway. (a, b, and c) The combined action of RecQ helicase and RecJ nuclease converts a DSB into an ssDNA-dsDNA junction with 3′-terminated ssDNA overhang; this ssDNA is complexed with SSB protein. (d and e) The RecF, RecO, and RecR proteins form a complex at the junction and facilitate RecA nucleoprotein filament assembly on the SSB-coated ssDNA. (f) The RecA-ssDNA nucleoprotein filament invades homologous dsDNA.

Citation: Spies M, Kowalczykowski S. 2005. Homologous Recombination by the RecBCD and RecF Pathways, p 389-403. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch21
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Image of Figure 6.
Figure 6.

SSG repair by the RecF pathway. The SSG has several potential fates. The RecFOR proteins can bind to the 5′ end of the ssDNA-dsDNA junction (a), the SSG can be cleaved to produce a DSB (b), or the ssDNA region can be expanded by the combined activities of the RecQ helicase and RecJ nuclease (c and d). (e) RecFOR proteins facilitate RecA protein loading onto the SSB-coated ssDNA. (f) Growth of the RecA nucleoprotein filament beyond the ssDNA region is prevented by the RecFR complex bound to the ssDNA-dsDNA junction containing a free 3′ end. (g) The RecA nucleoprotein filament invades homologous dsDNA and catalyzes DNA strand exchange. (h) DNA heteroduplex expansion results in the formation of two Holliday junctions. (i) RuvABC proteins facilitate branch migration and Holliday junction resolution to produce repaired recombinant molecules. (j) Translesion DNA synthesis by DNA polymerase (UmuD′C) can also repair the SSG due to direct interaction of the polymerase with the RecA nucleoprotein filament.

Citation: Spies M, Kowalczykowski S. 2005. Homologous Recombination by the RecBCD and RecF Pathways, p 389-403. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch21
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