Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda.

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Authors A Kuzminov - University of Oregon. Although homologous recombination and DNA repair phenomena in bacteria were initially extensively studied without regard to any relationship between the two, it is now appreciated that DNA repair and homologous recombination are related through DNA replication. In Escherichia coli, two-strand DNA damage, generated mostly during replication on a template DNA containing one-strand damage, is repaired by recombination with a homologous intact duplex, usually the sister chromosome.

The two major types recombinational repair of dna damage in escherichia coli and bacteriophage lambda two-strand DNA lesions are channeled into two distinct pathways of recombinational repair: The phage lambda recombination system is simpler in that its major reaction is to link two double-stranded DNA ends by using overlapping homologous sequences.

The remarkable progress in understanding the mechanisms of recombinational repair in E. Putting our knowledge about recombinational repair in the broader context of DNA replication will guide future experimentation.

Publication citations Citation Count is the number of times that this paper has been cited by other published papers in the database.

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In nucleotide excision repair, damaged nucleotides i. The patch is then joined to the main strand by DNA ligase. This process is very accurate, and does not produce mutations.

The sheer volume of publications on "cut and patch" nucleotide excision repair e. Quite to the contrary, recombinational DNA repair is critical for the survival of UV radiation-damaged cells. The first indication that nucleotide excision repair "cut and patch" is NOT the only mechanism by which cells repair damage to their DNA, was the observation that bacterial cells deficient in nucleotide excision repair i.

A double mutant uvrA recA , however, is much more sensitive to UV irradiation than either of the single mutants Figure 1. From the most fundamental principles of radiation biology and genetics, these data argue that, a these two systems, i.

These studies led to the discovery of postreplication repair see below. The uvrA6 mutation blocks nucleotide excision repair, and the recA13 mutation blocks recombinational DNA repair.

Note that the double mutant, uvrA6 recA13 is very much more sensitive to UV radiation than either of the single mutants, indicating that the two single mutants are involved in separate pathways of DNA repair. Since the two single mutants have about the same sensitivity, it indicates that nucleotide excision repair and recombinational DNA repair are of about equal importance to the survival of UV irradiated E.

Schematic of DNA replication in E. The problems and opportunity for recombinational DNA repair in these two regions of the chromosome are markedly different. Postreplication Repair The DNA synthesized immediately after UV irradiation in excision repair-deficient cells and also wild-type cells; see below of E. The mean length of newly synthesized DNA approximates the distance between pyrimidine dimers in the parental strand. With further incubation of the cells, however, these discontinuities disappear, and the DNA approximates the molecular size of that from unirradiated control cells Rupp and Howard-Flanders, ; Howard-Flanders et al.

The exchanges envisioned by this type of repair resemble those involved in genetic recombination Rupp et al. This prediction has been verified by demonstrating that recA cells are deficient in the production of normal length DNA from the small pieces of DNA synthesized immediately after UV irradiation Smith and Meun, ; Sedgwick, When DNA synthesis proceeds along a damaged template, synthesis halts at the site of a non-coding lesion, and then resumes downstream from the lesion i.

The fact that photoreactivation after UV irradiation in a uvrA strain stimulated gap filling, is taken as further evidence that a large proportion of the DNA daughter-strand gaps are opposite pyrimidine dimers Bridges and Sedgwick, Only after the gaps are filled by sister-strand exchanges will the dimers again be subject to excision repair. These gaps in the daughter strands, which average nucleotides in length Iyer and Rupp, , are subsequently repaired in recombination proficient strains by transferring the appropriate sections of DNA from the parental strands into the daughter strands.

This transfer of parental strands into daughter strands has been confirmed by direct measurement Rupp et al. Although most studies on postreplication repair have been performed in excision repair deficient cells, this type of repair is fully operative in wild-type cells Smith and Meun, ; Rupp, Iyer and Zipser, ; Howard-Flanders and Rupp, Although postreplication repair i.

However, the recB gene is known to function in the repair of DNA double-strand breaks that are formed metabolically after UV irradiation in E. In fact, unrepaired DNA double-strand breaks appear to be the major cause of lethality in UV-irradiated wild-type bacteria Bonura and Smith, a,b. The repair of metabolically-produced DNA double-strand breaks constitutes a second type of recombination repair that is distinct from the repair of DNA daughter-strand gaps, i.

Much of postreplication repair is constitutive Ganesan and Smith, ; Sedgwick, , but a portion i. Each of these pathways is recBC -independent Smith and Meun, The involvement of the recF gene suggests that the recF pathway of homologous recombination may be involved in this repair process.

The repair of daughter-strand gaps by the recF -dependent and the recF -independent process see below is accompanied by the transfer of DNA lesions from the parental strand to the daughter strand Ganesan, ; Wang and Smith, The fact that a uvrB recF stain is not as deficient in the repair of daughter-strand gaps as is a uvrB recA strain suggested that a second pathway must exist for the repair of daughter-strand gaps Wang and Smith, This conclusion was supported by studies using an insertion mutation of recF recF Tn3 to ensure that the earlier results were not due to leakiness in the original recF mutation.

The recF -independent pathway is also independent of the recBC genes, and is constitutive Sharma and Smith, Studies using polA mutants, indicate that the polA gene DNA polymerase l plays a major role in the recF -independent repair of daughter-strand gaps.

Studies on different polA mutants i. Furthermore, since DNA polymerase is known to be involved in the joining of Okazaki fragments synthesized in the lagging strand of unirradiated cells, this raises the possibility that the daughter-strand gaps formed in the lagging strand of UV irradiated cells may be selectively repaired by the recF -independent, polA -dependent pathway, while the daughter-strand gaps formed in the leading strand i.

Since a uvrA polA recF strain is not quite as deficient in the repair of daughter-strand gaps as is a uvrA recA strain Sharma and Smith, , it suggests that a third pathway must exist for the repair of daughter-strand gaps.

Consistent with this observation, a small fraction of the repair of daughter-strand gaps is dependent upon the umuC gene, but is independent of the recF and recBC genes Wang and Smith, A uvrA polA recF umuC strain has not yet been tested to see if it as deficient as a uvrA recA strain in the repair of daughter-strand gaps. This is consistent with the fact that umuC controls all of UV radiation mutagenesis Kato and Shinoura, A umuC mutation, however, has only a partial effect on spontaneous mutagenesis Sargentini and Smith, , and on X-ray mutagenesis Sargentini and Smith, One pathway is DNA polymerase l dependent, growth medium independent i.

The second excision repair process, long-patch excision repair, which requires two DNA duplexes, is largely ignored by reviewers e. Nevertheless, this excision repair pathway does exist, and it has been confirmed by other authors e. It is dependent upon the recA gene, it is growth medium dependent i. Long-patch excision repair also requires the recF gene Hanawalt et al. The early repair seems to be short-patch excision repair, which occurs immediately after UV irradiation, and is controlled by DNA polymerase l Cooper and Hanawalt, a , while the induced repair appears to be the long-patch system that is controlled by recA Cooper, Additional copies of the UvrA protein Kenyon and Walker, and the UvrB protein Schendel, Fogliano, and Strausbaugh, are synthesized after UV irradiation, and may be relevant to the inducible long-patch excision repair process.

The excision repair that occurs in cells that contain completely replicated chromosomes, i. In this situation, classical nucleotide excision repair occurs, i.

The excision repair that functions in the part of the chromosome that was replicated before UV irradiation i. The similarities between the genetic requirements for long-patch excision repair and the repair of DNA daughter-strand gaps, i. The only significant difference between these two processes is the manner in which the gaps in the sister duplexes are formed, i.

For a discussion of excision repair in mammalian cells, see the module Nucleotide Excision Repair in Human Cells. Furthermore, most reviewers make no distinction between the repair events that take place in the two different parts of the chromosome, i. Clearly the problems and the opportunities for DNA repair are quite different in these two regions of the chromosome.

Enzymatic production of deoxyribonucleic acid double-strand breaks after ultraviolet irradiation of Escherichia coli K Bonura T, Smith KC. Effect of photoreactivation on the filling of gaps in deoxyribonucleic acid synthesized after exposure of Escherichia coli to ultraviolet light. Characterization of long patch excision repair of DNA in ultraviolet-irradiated Escherichia coli: Mol Gen Genet Role of DNA polymerase l and the rec system in excision-repair in Escherichia coli.

Heterogeneity of patch size in repair replicated DNA in Escherichia coli. J Mol Biol Persistence of pyrimidine dimers during post-replication repair in ultraviolet light-irradiated Escherichia coli K Requirement for protein synthesis in rec -dependent repair of deoxyribonucleic acid in Escherichia coli after ultraviolet or X irradiation. Controlling the efficiency of excision repair. Repair replication schemes in bacteria and human cells. Repair responses to DNA damage: J Cell Biochem DNA repair and genetic recombination: Radiat Res Suppl 6: Recombination repair in UV-irradiated Escherichia coli , In: Measurement of postreplication repair in prokaryotes, In: Marcel Dekker, New York p DNA replication and recombination after UV irradiation.

Usefulness of benzoylated naphthoylated DEAE-cellulose to distinguish and fractionate double-stranded DNA bearing different extents of single-stranded regions. Biochim Biophys Acta Sensitivity to ultraviolet light of single- and double-stranded DNA. Effects of chloramphenicol and caffeine on postreplication repair in uvrAumuC and uvrArecF strains of Escherichia coli K Kato T, Shinoura Y. Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light.

Expression of the E. Recombinational repair of DNA damage in Escherichia coli and bacteriophage. Microbiol Mol Biol Rev DNA damage-dependent recruitment of nucleotide excision repair and transcription proteins to Escherichia coli inner membranes. Nucleic Acids Res Effect of RecF protein on reactions catalyzed by RecA protein. Petit C, Sancar A. Discontinuities in the DNA synthesized in an excision-defective strain of Escherichia coli following ultraviolet irradiation.

The reconstitution of chromosomal DNA in irradiated cells by post-replication recombinational repair, In: Advances in Radiation Research: Exchanges between DNA strands in ultraviolet-irradiated Escherichia coli.

Much of spontaneous mutagenesis in Escherichia coli is due to error-prone DNA repair: Implications for spontaneous carcinogenesis.