Browse > Article
http://dx.doi.org/10.4014/jmb.0907.07005

Unbalanced Restriction Impairs SOS-induced DNA Repair Effects  

Katna, Anna (Department of Microbiology, University of Gdansk)
Boratynski, Robert (Department of Microbiology, University of Gdansk)
Furmanek-Blaszk, Beata (Department of Microbiology, University of Gdansk)
Zolcinska, Natalia (Department of Microbiology, University of Gdansk)
Sektas, Marian (Department of Microbiology, University of Gdansk)
Publication Information
Journal of Microbiology and Biotechnology / v.20, no.1, 2010 , pp. 30-38 More about this Journal
Abstract
The contribution of a type II restriction-modification system (R-M system) to genome integrity and cell viability was investigated. We established experimental conditions that enabled the achievement of hemimethylated and unmethylated states for the specific bases of the recognition sequences of the host's DNA. To achieve this, we constructed the MboII R-M system containing only one (i.e., M2.MboII) out of two functional MboII methyltransferases found in Moraxella bovis. Using the incomplete R-M system, we were able to perturb the balance between methylation and restriction in an inducible manner. We demonstrate that upon the SOS-induced DNA repair in mitomycin C treated cells, restriction significantly reduces cell viability. Similar results for the well-studied wild-type EcoRI R-M system, expressed constitutively in Escherichia coli, were obtained. Our data provide further insights into the benefits and disadvantages of maintaining of a type II R-M system, highlighting its impact on host cell fitness.
Keywords
Restriction endonuclease; DNA methyltransferase; type II R-M systems; SOS induction;
Citations & Related Records

Times Cited By Web Of Science : 1  (Related Records In Web of Science)
연도 인용수 순위
  • Reference
1 Aras, R. A., A. J. Small, T. Ando, and M. J. Blaser. 2002. Helicobacter pylori interstrain restriction-modification diversity prevents genome subversion by chromosomal DNA from competing strain. Nucleic Acids Res. 30: 5391-5397.   DOI
2 Bocklage, H., K. Heeger, and B. Muller-Hill. 1991. Cloning and characterization of the MboII restriction-modification system. Nucleic Acids Res. 19: 1007-1013.   DOI   ScienceOn
3 Cerritelli, S., S. S. Springhorn, and S. A. Lacks. 1989. DpnA, a methylase for single-strand DNA in the DpnII restriction system and its biological function. Proc. Natl. Acad. Sci. U.S.A. 86: 9223-9227.   DOI   ScienceOn
4 Taylor, J. D., A. J. Goodall, C. L. Vermote, and S. E. Halford. 1990. Fidelity of DNA recognition by the EcoRV restriction/modification system in vivo. Biochemistry 29: 10727-10733.   DOI   ScienceOn
5 Courcelle, J., A. Khodursky, B. Peter, P. O. Brown, and P. C. Hanawalt. 2001. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158: 41-64.
6 Blakely, G. W. and N. E. Murray. 2006. Control of the endonuclease activity of type I restriction-modification systems is required to maintain chromosome integrity following homologous recombination. Mol. Microbiol. 60: 883-893.   DOI   ScienceOn
7 Blattner, F. R., G. Plunkett III, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, et al. 1997. The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1462.   DOI   ScienceOn
8 Chang, A. C. Y. and S. N. Cohen. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from P15A cryptic miniplasmid. J. Bacteriol. 134: 1141-1156.
9 Fomenkov, A., J. P. Xiao, D. Dila, E. Raleigh, and S. Y. Xu. 1994. The "endo-blue method" for direct cloning of restriction endonuclease genes in E. coli. Nucleic Acids Res. 22: 2399-2403.   DOI   ScienceOn
10 Heitman, J., T. Ivanenko, and A. Kiss. 1999. DNA nicks inflicted by restriction endonucleases are repaired by a RecA- and RecB-dependent pathway in Escherichia coli. Mol. Microbiol. 33: 1141-1151.
11 Heitman, J., N. D. Zinder, and P. Model. 1989. Repair of the Escherichia coli chromosome after in vivo scission by the EcoRI endonuclease. Proc. Natl. Acad. Sci. U.S.A. 86: 2281-2285.   DOI   ScienceOn
12 Quillardet, P., O. Huisman, R. D'Ari, and M. Hofnung. 1982. SOS chromotest, a direct assay of induction of an SOS function in Escherichia coli K-12 to measure genotoxicity. Proc. Natl. Acad. Sci. U.S.A. 79: 5971-5975.   DOI   ScienceOn
13 Kobayashi, I. 2004. Restriction-modification systems as minimal forms of life, pp. 19-62. In A. Pingoud (ed.). Nucleic Acids and Molecular Biology, Vol. 14. Restriction Endonucleases. Springer-Verlag, Berlin Heidelberg.
14 Kumar, S., R. Lipman, and M. Tomasz. 1992. Recognition of specific DNA sequences by mitomycin C for alkylation. Biochemistry 31: 1399-1407.   DOI   ScienceOn
15 Merkiene, E., G. Vilkaitis, and S Klimasauskas. 1998. A pair of single-strand and double-strand DNA cytosine-N4 methyltransferases from Bacillus centrosporus. Biol. Chem. 379: 569-571.
16 Roberts, R. J., T. Vincze, J. Posfai, and D. Macelis. 2007. REBASE: Restriction enzymes and DNA methyltransferases. Nucleic Acids Res. 33: D230-D232.
17 Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual, 2nd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
18 Surby, M. A. and N. O. Reich. 1996. Facilitated diffusion of the EcoRI DNA methyltransferase is described by a novel mechanism. Biochemistry 35: 2209-2217.   DOI   ScienceOn
19 Yoshimori, R., D. Roulland-Dussoix, and H. W. Boyer. 1972. R-Factor-controlled restriction and modification of deoxyribonucleic acid: Restriction mutants. J. Bacteriol. 112: 1275-1279.
20 Handa, N., A. Ichige, K. Kusano, and I. Kobayashi. 2000. Cellular responses to postsegregational killing by restriction-modification genes. J. Bacteriol. 182: 2218-2229.   DOI   ScienceOn
21 McClelland, M., M. Nelson, and C. R. Cantor. 1985. Purification of MboII methylase (GAAGmA) from Moraxella bovis: Site specific cleavage of DNA at nine and ten base pair sequences. Nucleic Acids Res. 13: 7171-7182.   DOI   ScienceOn
22 Naito, Y., K. Kusano, and I. Kobayashi, I. 1995. Selfish behavior of restriction-modification systems. Science 267: 897-899.   DOI
23 Boyer, H. and D. Roulland-Dussoix. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41: 459-472.   DOI
24 Ichige, A. and I. Kobayashi. 2005. Stability of EcoRI restriction-modification enzymes in vivo differentiates the EcoRI restriction-modification system from other postsegregational cell killing system. J. Bacteriol. 187: 6612-6621.   DOI   ScienceOn
25 Kaczorowski, T., M. Sektas, P. Skowron, and A. Podhajska. 1999. The FokI methyltransferase from Flavobacterium okeanokoites: Purification and characterization of the enzyme and its truncated derivatives. Mol. Biotechnol. 13: 1-15.   DOI   ScienceOn
26 Lin, L. F., J. Posfai, R. J. Roberts, and H. Kong. 2001. Comparative genomics of the restriction-modification systems in Helicobacter pylori. Proc. Natl. Acad. Sci. U.S.A. 98: 2740-2745.   DOI   ScienceOn
27 Aras, R. A., T. Takata, T. Ando, A. var der Ende, and M. J. Blaser. 2001. Regulation of the HpyII restriction-modification system of Helicobacter pylori by gene deletion and horizontal reconstitution. Mol. Microbiol. 42: 369-382.   DOI   ScienceOn
28 Nobusato, A., I. Uchiyama, S. Ohashi, and I. Kobayashi. 2000. Insertion with target duplication: A mechanism for gene mobility suggested from comparison of two related bacterial genomes. Gene 259: 99-108.   DOI
29 Nagornykh, M. O., E. S. Bogdanova, A. S. Protsenko, A. S. Solonin, M. V. Zakharova, and K. V. Severinov. 2008. Regulation of gene expression in a type II restriction-modification system. Russ. J. Genetics 44: 523-532.   DOI   ScienceOn
30 Posfai, G., M. Koob, Z. Hradecna, N. Hasan, M. Filutowicz, and W. Szybalski. 1994. In vivo excision and amplification of large segments of the Escherichia coli genome. Nucleic Acids Res. 22: 2392-2398.   DOI   ScienceOn
31 Kelleher, J. E. and E. A. Raleigh. 1994. Response to UV damage by four Escherichia coli K-12 restriction systems. J. Bacteriol. 176: 5888-5896.
32 Bolivar, F., R. L. Rodriguez, M. C. Betlach, and H. W. Boyer. 1977. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2: 95-113.   DOI
33 Cromie, G. A. and D. R. F. Leach. 2001. Recombinational repair of chromosomal DNA double-strand breaks generated by a restriction endonuclease. Mol. Microbiol. 4: 873-883.
34 Guzman, L. M., D. Belin, M. J. Carson, and J. Beckwith. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose $P_{BAD}$ promoter. J. Bacteriol. 177: 4121-4130.
35 Handa, N. and I. Kobayashi. 1999. Post-segregational killing by restriction modification gene complexes: Observations of individual cell deaths. Biochimie 81: 931-938.   DOI   ScienceOn
36 Tock, M. R. and D. T. F. Dryden. 2005. The biology of restriction and anti-restriction. Curr. Opin. Microbiol. 8: 466-472.   DOI   ScienceOn
37 Furmanek-Blaszk, B., R. Boratynski, N. Zolcinska, and M. Sektas. 2009. M1.MboII and M2.MboII type IIS methyltransferases: Different specificities, the same target. Microbiology 155: 1111-1121.   DOI
38 Cheng, S. C., R. Kim, K. King, S. H. Kim, and P. Modrich. 1984. Isolation of gram quantities of EcoRI restriction and modification enzymes from an overproducing strain. J. Biol. Chem. 259: 11571-11575.
39 Mruk, I. and R. M. Blumenthal. 2008. Real-time kinetics of restriction-modification gene expression after entry into a new host cell. Nucleic Acids Res. 36: 2581-2593.   DOI   ScienceOn
40 Khil, P. P. and R. D. Camerini-Otero. 2002. Over 1000 genes are involved in the DNA damage response of Escherichia coli. Mol. Microbiol. 44: 89-105.   DOI   ScienceOn
41 Nakayama, Y. and I. Kobayashi. 1998. Restriction-modification gene complexes as selfish gene entities: Roles of a regulatory system in their establishment, maintenance, and apoptotic mutual exclusion. Proc. Natl. Acad. Sci. U.S.A. 95: 6442-6447.   DOI   ScienceOn
42 Spira, B. and T. Ferenci. 2008. Alkaline phosphatase as a reporter of sigma(S) levels and rpoS polymorphisms in different E. coli strains. Arch. Microbiol. 189: 43-47.
43 Handa, N., A. Ichige, and I. Kobayashi. 2009. Contribution of RecFOR machinery of homologous recombination to cell survival after loss of a restriction-modification gene complex. Microbiology 155: 2320-2332.   DOI   ScienceOn
44 Hasan, N., M. Koob, and W. Szybalski. 1994. Escherichia coli genome targeting. I. Cre-lox-mediated in vitro generation of ori-plasmids and their in vivo chromosomal integration and retrieval. Gene 150: 51-56.   DOI   ScienceOn
45 Thoms, B. and W. Wackernagel. 1982. UV-induced alleviation of $\lambda$ restriction in Escherichia coli K12: Kinetics of induction and specificity of this SOS function. Mol. Gen. Genet. 186: 111-117.   DOI   ScienceOn
46 Cohen, S. N., A. C. Y. Chang, H. W. Boyer, and R. B. Helling. 1973. Construction of biologically functional bacterial plasmids in vitro. Proc. Natl. Acad. Sci. U.S.A. 70: 3240-3244.   DOI   ScienceOn
47 Miller, J. H. 1972. Experiments in Molecular Genetics, p. 439. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48 Surby, M. A. and N. O. Reich. 1996. Contribution of facilitated diffusion and processive catalysis to enzyme efficiency: Implications for the EcoRI restriction-modification system. Biochemistry 35: 2201-2208.   DOI   ScienceOn
49 Yanisch-Perron, C., J Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: Nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33: 103-119.   DOI   ScienceOn
50 Makovets, S., V. A. Doronina, and N. E. Murray. 1999. Regulation of endonuclease activity by proteolysis prevents breakage of unmodified bacterial chromosomes by type I restriction enzymes. Proc. Natl. Acad. Sci. U.S.A. 96: 9757-9762.   DOI   ScienceOn
51 Dronkert, M. L. G. and R. Kanaar. 2001. Repair of DNA interstrand cross-links. Mutat. Res. 486: 217-247.   DOI   ScienceOn