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¹ Institute of Medical Science, Medinet, Tamagawadai 2-2-8, Setagaya-ku, Tokyo 158-0096, Japan
² Fundamental Research Laboratory, G & G Science, Yokohama Leading Venture Plaza 503, Ono-cho 75-1, Tsurumi-ku, Yokohama 230-0046, Japan

	Abstract

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To study roles of Rep helicase in short-homology-dependent illegitimate recombination, we examined the effect of a rep mutation on illegitimate recombination and found that the frequency of spontaneous illegitimate recombination is enhanced by the rep mutation. In addition, illegitimate recombination was synergistically enhanced by the rep mutation and UV irradiation, showing that Rep helicase plays a role in suppression of spontaneous as well as UV-induced illegitimate recombination. The defect in RecQ helicase also has a synergistic effect on the increased illegitimate recombination in the rep mutant. It was also found that the illegitimate recombination induced by the rep mutation is independent of the RecA function with or without UV irradiation. Nucleotide sequence analyses of the recombination junctions showed that the illegitimate recombination induced by the rep mutation mostly takes place between short homologous sequences. Based on the fact that the defect of Rep helicase induces replication arrest during replication, resulting in the formation of DNA double-strand breaks, we propose a model for illegitimate recombination, in which double-strand breaks caused by defect of Rep helicase promotes illegitimate recombination via short-homology-dependent-end-joining. In addition, the mechanism of synergistic action between the rep mutation and UV irradiation on illegitimate recombination is discussed.

	Introduction

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DNA helicases, which catalyze ATP-dependent unwinding of DNA, are involved in various aspects of DNA metabolism and at least 11 helicases have been identified in E. coli (Matson et al. 1994). DnaB and PriA are involved in DNA replication (Scott & Kornberg 1978; LeBowitz & McMacken 1986; Lee & Marians 1987; Lee & Kornberg 1991). RecBCD, RecQ, and HelD participate in recombination (Taylor & Smith 1980; Umezu et al. 1990; Mendonca et al. 1993). UvrAB and UvrD helicases play roles in recombination and repair (Oh & Grossman 1987; Modrich 1989; Orren et al. 1992). Among them, Rep helicase is required for replication of single-stranded DNA phages X174 and fd, and is also required for the growth of double-stranded DNA phage P2 (Takahashi et al. 1978). rep mutations do not affect cell viability but they reduce the rate of replication fork progression and increase the number of replication forks in the replicating E. coli chromosome (Lane & Denhardt 1975), and the large overproduction of the Rep protein is lethal to E. coli (Lohman et al. 1989). rep mutations also cause constitutive expression of the SOS functions (Ossanna & Mount 1989). DNA double-strand breaks upon arrest of replication forks occur due to a defect in Rep helicase (Michel et al. 1997). RecA-independent homologous recombination is enhanced in a rep mutant (Bierne et al. 1997). However, the role of Rep helicase on illegitimate recombination is unknown.

Illegitimate recombination takes place between sequences having little or no homology, and results in DNA rearrangements such as deletions, translocations or insertions of the chromosomes. Illegitimate recombination usually occurs at a low frequency but is greatly enhanced by UV irradiation or other DNA-damaging agents (Ikeda et al. 1995; Onda et al. 1999). Illegitimate recombination can be classified into two classes, short-homology-dependent illegitimate recombination (SHDIR) and short-homology-independent illegitimate recombination (SHIIR) (Shimizu et al. 1995, 1997). SHIIR occurs between sequences with entirely no homology and is mediated by DNA topoisomerases I and DNA gyrase (Ikeda et al. 1981; Bierne et al. 1997; Shimizu et al. 1997; Ashizawa et al. 1999). SHDIR occurs spontaneously or is induced, by UV light or other DNA-damaging agents, and requires short regions of homology between recombination sites. These regions usually contain 4–13 bp of homologous sequences (Yamaguchi et al. 1995; Ukita & Ikeda 1996). It has been shown that RecJ exonuclease promotes UV-induced SHDIR, but RecQ helicase suppresses it (Ukita & Ikeda 1996; Hanada et al. 1997). A temperature-sensitive dnaB mutation reduces SHDIR at a semipermissive temperature under UV irradiation (Hanada et al. 2001). On the other hand, overproduction of DnaB enhanced SHDIR without DNA damage (Yamashita et al. 1999), suggesting a relationship between SHDIR and DNA replication.

To examine the roles of Rep helicase in SHDIR, we measured the frequency of illegitimate recombination between phage and bacterial genomes during prophage induction and found that the defect of Rep helicase enhances the frequency of spontaneous and UV-induced illegitimate recombination. The Rep-overexpression strain also reduces the frequency of spontaneous and UV-induced illegitimate recombination, compared to wild-type strain. In addition, the RecQ function plays a role in the suppression of the illegitimate recombination enhanced by the rep mutation without UV-irradiation. A model for roles of Rep helicase in illegitimate recombination is discussed.

	Results

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Effect of a rep mutation on spontaneous and UV-induced illegitimate recombination

To study the role of Rep helicase on illegitimate recombination, we examined the effect of the rep mutation on the recombination detected as the formation of bio transducing phages during prophage induction. bio transducing phages are formed by illegitimate recombination between bacterial and phage DNAs, lack both the red and gam genes and can be distinguished from normal phage on the basis of a Spi^– (sensitive to P2 interference) phenotype. These recombinant phages, which are called Spi^– phages, can be positively detected as phages that grow in P2 lysogen of E. coli (Ikeda et al. 1995). On the other hand, normal phages cannot grow in P2 lysogen. Therefore, the frequency of illegitimate recombination can be calculated as a ratio of the number of Spi^– phages to the number of total phages in a given lysate. When E. coli HI2051 wild-type lysogen was induced by high temperature, the frequency of Spi^– phages was low. On the other hand, in E. coli HI3303 lysogen carrying a rep mutation, the frequency of Spi^– phage was nine-fold higher than that in the wild-type strain without UV irradiation (Table 1). This result indicated that Rep helicase plays a role in the suppression of spontaneous illegitimate recombination.

Effect of over-expression of Rep helicase on the frequency of Spi^– phage

Next, we examined the effect of over-expression of Rep helicase on illegitimate recombination. The plasmid, pRepO, is a derivative of pKC30 and contains the rep⁺ gene under control of the phage P_L promotor. We introduced the pRepO plasmid into the rep mutant. Using these strains, we measured the frequency of Spi^– phage after prophage induction and found that it is reduced by the introduction of pRepO into rep mutant with or without UV irradiation, compared to the introduction of pKC30 into rep mutant (Table 2). Surprisingly, the frequency of Spi^– phage was reduced in the wild-type strain with pRepO, compared to the wild-type with pKC30, under UV irradiation (Table 2). These results indicated that Rep helicase is required for the decrease of frequencies of spontaneous and UV-mediated illegitimate recombination. This indicates that the frequency of Spi^– phage depends on the concentration of Rep protein in the cell, probably because the increased Rep activity reduces the replication arrest with or without UV damage.

Since the effect of the rep mutation on illegitimate recombination is similar to that of the recQ mutation (Hanada et al. 1997), we examined the functional relationship between Rep and RecQ helicases in illegitimate recombination. We measured the frequency of Spi^– phage in the recQ rep double mutation without UV irradiation and found that illegitimate recombination enhanced by the rep mutation is further enhanced by a recQ mutation in the absence of UV-irradiation (Table 3). The result suggests that Rep and RecQ work in the same pathway in spontaneous illegitimate recombination, but they act on different steps. On the other hand, the frequency of illegitimate recombination in the recQ rep double mutant was comparable to that of the recQ single mutant under UV irradiation (Table 3). It may imply that Rep works in a different pathway from RecQ in UV-induced illegitimate recombination.

We determined the distribution of recombination junction of Spi^– phage isolated from the rep mutant with or without UV irradiation. Since illegitimate recombination takes place between E. coli bio-uvrB genes and git-gam regions as shown in Fig. 1A, the segments containing recombination junctions were amplified by PCR with several primer oligonucleotide sets, followed by agarose gel electrophoresis analysis. In a previous report, we determined the sequences of the recombination junction in the wild-type at Hotspot I, Hotspot II, Hotspot III and some sequences at non-hotspots and found that most of the illegitimate recombination occurs at Hotspot I (Yamaguchi et al. 1995; Hanada et al. 1997). In the phages formed in the rep mutant with or without UV-irradiation, the frequencies at Hotspot I were 77% and 70%, respectively (Table 4), indicating that illegitimate recombination induced by the rep mutation mostly takes place at Hotspot I with or without UV irradiation.

View larger version (39K): [in this window] [in a new window]   Figure 1  Nucleotide sequences of the recombination junctions of bio transducing phages isolated from the rep mutant. (A) Schematic representation of the recombination sites in this assay. (B) (i)(a) Hotspot I detected at the recombination junctions of bio transducing phages UR2 and UR36, which were isolated without UV irradiation, and bio transducing phages REV8 and REV11, which were isolated under UV irradiation. The sequences shown in bold indicate homology at the recombination sites. Map coordinates for phage and bacterial sequences are indicated. (i)(b) Sequences of Hotspot II detected at the recombination junctions of bio transducing phages UR5 and UR11, which were isolated without UV irradiation, and bio transducing phages REV36 and REV39, which were isolated under UV irradiation. (i)(c) Sequences of Hotspot III detected in the recombination junctions of bio transducing phages REV39 and REY60, which were isolated under UV irradiation. (ii)(d–f) Sequences of non-hotspot sites detected in the recombination junctions of bio transducing phages derived from the rep mutant without UV irradiation. (iii)(g,h) Sequences of non-hotspot sites derived from the rep mutant under UV irradiation.

View this table: [in this window] [in a new window]   Table 4 Distribution of recombination sites of bio transducing phages formed following with or without UV irradiation

	Discussion

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We found that the rep mutation enhances spontaneous illegitimate recombination between bacterial and phage DNA during prophage induction, indicating that Rep helicase plays a role in suppression of spontaneous illegitimate recombination. rep mutants exhibited a slower movement of replication forks, thus resulting in a reduced replication rate (Lane & Denhardt 1975). It has been found that the rep mutations increase expression of the SOS response in the absence of DNA damage (Ossanna & Mount 1989). Since Rep has an ability to displace DNA-bound protein in vitro, it has been postulated that Rep may have a role to remove proteins during replication fork progression (Yancey-Wrona & Matson 1992; Matson et al. 1994). It has also been shown that rep recBTS recCTS mutants accumulate linear DNA upon incubation at the restrictive temperature, showing the occurrence of spontaneous double-strand breaks (DSBs) in rep mutants (Michel et al. 1997). Furthermore, the formation of DSBs is mediated by the action of RuvABC protein (Seigneur et al. 1998). They postulated the replication fork reversal model, in which replication pause initiates the formation of a Holiday junction via reannealing of template strands and pairing of newly synthesized strands, resulting in the RuvABC-mediated resolution of the Holliday junction. Based on these observations, it is suggested that these DSBs induced by the rep mutation may cause illegitimate recombination via short-homology-dependent-end-joining reaction.

Bierne et al. (1997) found that RecA-independent recombination is enhanced in a rep mutant and suggested that replication pausing induced the rep mutation that may facilitate slippage at duplicated sequences, leading to the formation of deletion mutation. It is possible that the illegitimate recombination induced by the rep mutation also takes place by the slippage mechanism. The slipped replication and mispairing at the duplicated sequences may then lead to the production of bio-transducing phage. It is, however, unlikely that slipped mispairing takes place between the short homologous sequences detected in this study, because they are separated by the length of a prophage and it is hard to imagine slippage between such a long distance. Even if the slippage is successful, it would result in formation of di-lysogen or non-lysogen but not excision of the prophage.

Next, we found that the illegitimate recombination is synergistically enhanced by the rep mutation and UV irradiation. This indicates that Rep helicase somehow suppresses illegitimate recombination induced by the UV irradiation. It is thought that UV irradiation induces DNA damages on DNA, which then cause replication fork arrest when damages are not repaired. In the absence of Rep, not only DNA-bound protein but also the encounter of UV-induced DNA damages may cause frequent replication arrest, resulting in formation of DSBs followed by illegitimate recombination. How does Rep helicase play a role in overcoming the unrepaired DNA damage? In addition to the Rep function to stabilize the replication fork during normal DNA synthesis, Rep is known to function in the PriC-dependent pathway of replication fork restart (Sandler 2000). It is therefore possible that Rep protein plays roles not only on normal progression of replication fork but also on avoidance of the replication fork arrest induced by DNA damages. This interpretation is consistent with the observation that the rep mutant is hypersensitive to UV light (Denhardt et al. 1967).

E. coli UmuC protein is an error-prone DNA polymerase (Pol V), which is activated by UmuD', RecA, and SSB, and is required for translesion synthesis followed by DNA damage-induced mutagenesis (Reuven et al. 1999; Tang et al. 1999). DinB protein is also a DNA polymerase (Pol IV), which is regulated by the SOS stress response and is required for the untargeted mutagenesis (Wagner et al. 1999). The function of Rep protein in suppression of UV-induced illegitimate recombination may be explained by involvement of Rep in translesion synthesis. But this is not the case because illegitimate recombination induced by the rep mutation is RecA-independent.

Next, we showed that RecQ suppresses illegitimate recombination induced by the rep mutation without UV-irradiation. Based on the 3'-to-5' DNA helicase activity of RecQ, we have previously postulated that the RecQ helicase may unwind a hydrogen-bonded intermediate of the DNA end-joining reaction which is formed by annealing of DNA ends with short homologies, thus exhibiting the suppression of recombination (Hanada et al. 1997). Spontaneous illegitimate recombination induced by the rep mutation may be suppressed by the helicase activity of RecQ in a way similar to the mechanism previously proposed. Therefore, RecQ and Rep helicases have similar roles important for suppression of illegitimate recombination, but they may work at different steps in the same recombination pathway.

Hotspot I and subhotspots were observed among the recombination sites of the rep mutant with or without UV irradiation. The recombination at Hotspot I accounts for 77% or 70% of total bio transducing phages induced by the rep mutation with or without UV irradiation, respectively. We have previously shown that Hotspot I was seen in the illegitimate recombination induced by UV irradiation or spontaneously, which constituted 57% or 77% of total bio transducing phages, respectively (Yamaguchi et al. 1995). The hotspot sites on E. coli and DNAs shared a short homology of 9 bp. In addition, we found direct repeat sequences of average 9 bp within and near both of the bio and hotspots in the recombination junctions induced by the rep mutation. The results therefore indicated that the illegitimate recombination induced by the rep mutation with or without UV irradiation takes place in a short-homology-dependent manner.

In the illegitimate recombination between and E. coli bio DNAs, it was previously found that RecJ exonuclease promotes short-homology-dependent illegitimate recombination (Ukita & Ikeda 1996). RecJ may modify 5' protruding ends, which are produced by DSBs, to form blunt ends. Furthermore, it was found that the co-expression of RecE and RecT enhances the frequencies of spontaneous and UV-induced illegitimate recombination, suggesting that RecE digests the 5' single-strand of the blunt end, producing a 3' overhang (Shiraishi et al. 2002). A temperature-sensitive mutation in the DNA ligase gene reduced the frequency of bio-transducing phage production compared to that of the wild type, whereas over-expression of DNA ligase enhances it, showing that DNA ligase is required for short-homology-dependent illegitimate recombination (Onda et al. 2001). The involvement of DNA ligase strongly supports the postulated DNA double-strand-break and join model. Rep and RecQ may play important roles in suppression of illegitimate recombination mediated by the break and join mechanism.

	Experimental procedures

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Bacterial strains and media

E. coli strains used in this study are described in Table 5. Plasmid pKC30 were supplied by Dr P. Modrich (Cheng et al. 1984). All strains in this work are derivatives of E. coli K-12. YP broth contained 10 g of Bacto Tryptone (Difco), 1 g of yeast extract (Difco), 2.5 g of NaCl, and 1.5 g of Na₂HPO₄, and 0.18 g of MgSO₄ in 1 liter of water and was used for growth of bacteria and phage. agar plate and trypticase agar plate were described in Ikeda et al. (1995) and was used for measuring bacterial colony and Spi^– phage, respectively.

Measurement of frequency of bio transducing phage formed spontaneously or by UV-irradiation during prophage induction

E. colicI857 or its derivatives were grown at 30 °C in YP broth. Strains were grown in YP broth at 30 °C to 1 x 10⁸ cells/mL. If necessary, 2 mL of the culture was irradiated with a UV lamp (15W) with a wavelength of 253.6 nm at a distance of 40 cm. Thermal induction of prophage was carried out by incubation at 42 °C for 15 min. The culture was then incubated at 37 °C for 2 h. The titer of Spi^– phages was measured on a lawn of E. coli WL95 (P2). The number of total phages was measured on a lawn of E. coli Ymel. The frequency of bio transducing phage was calculated by dividing the number of Spi^– phages by the total number of phages (Ikeda et al. 1995).

Independent isolation of bio transducing phage induced spontaneously or by UV irradiation

E. coli lysogen was irradiated with UV as described above, if necessary. The culture was then divided into 60 test tubes. Each tube containing 2 mL of the culture was then incubated at 42 °C for 15 min. The cultures were then incubated at 37 °C for 2 h. Phage lysates were plated on a lawn of E. coli WL95. A plaque derived from each tube was picked, suspended in M9 buffer, and plated on lawn of Ymel to isolate a single clone.

Determination of locations and nucleotide sequences of recombination junctions in bio transducing phage

bio transducing phage was identified by PCR with a mixture of several sets of primers. Locations of recombination junctions were also determined through PCR by using multiple combinations of primers (Ukita & Ikeda 1996). The recombination junctions were then sequenced and analyzed with an ABI PRISM 310 genetic analyzer (Applied Biosystems).

	Acknowledgements

 
We thank Drs T. M. Lohman, P. Modrich, and B. Michel for providing plasmids or E. coli strains and Dr K. Egawa for encouragement.

	Footnotes

 
Communicated by: Fumio Hanaoka

²Present address: Fundamental Research Laboratory, G & G Science, Yokohama Leading Venture Plaza 503, Ono-cho 75-1, Tsurumi-ku, Yokoyama 230-0046

^* Correspondence: E-mail: ikeda{at}gandgscience.co.jp

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Received: 24 June 2005
Accepted: 15 August 2005

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