Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Unbalanced Restriction Impairs SOS-induced DNA Repair Effects

  • Published : 2010.01.31
Download PDF
⟨ Previous Next ⟩

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

References

  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. https://doi.org/10.1093/nar/gkf686
  2. 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. https://doi.org/10.1046/j.1365-2958.2001.02637.x
  3. 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. https://doi.org/10.1111/j.1365-2958.2006.05144.x
  4. 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. https://doi.org/10.1126/science.277.5331.1453
  5. Bocklage, H., K. Heeger, and B. Muller-Hill. 1991. Cloning and characterization of the MboII restriction-modification system. Nucleic Acids Res. 19: 1007-1013. https://doi.org/10.1093/nar/19.5.1007
  6. 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. https://doi.org/10.1016/0378-1119(77)90000-2
  7. 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. https://doi.org/10.1016/0022-2836(69)90288-5
  8. 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. https://doi.org/10.1073/pnas.86.23.9223
  9. 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.
  10. 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.
  11. 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. https://doi.org/10.1073/pnas.70.11.3240
  12. 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.
  13. 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.
  14. Dronkert, M. L. G. and R. Kanaar. 2001. Repair of DNA interstrand cross-links. Mutat. Res. 486: 217-247. https://doi.org/10.1016/S0921-8777(01)00092-1
  15. 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. https://doi.org/10.1093/nar/22.12.2399
  16. 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. https://doi.org/10.1099/mic.0.025023-0
  17. 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.
  18. 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. https://doi.org/10.1099/mic.0.026401-0
  19. Handa, N., A. Ichige, K. Kusano, and I. Kobayashi. 2000. Cellular responses to postsegregational killing by restriction-modification genes. J. Bacteriol. 182: 2218-2229. https://doi.org/10.1128/JB.182.8.2218-2229.2000
  20. Handa, N. and I. Kobayashi. 1999. Post-segregational killing by restriction modification gene complexes: Observations of individual cell deaths. Biochimie 81: 931-938. https://doi.org/10.1016/S0300-9084(99)00201-1
  21. 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. https://doi.org/10.1016/0378-1119(94)90856-7
  22. 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.
  23. 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. https://doi.org/10.1073/pnas.86.7.2281
  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. https://doi.org/10.1128/JB.187.19.6612-6621.2005
  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. https://doi.org/10.1385/MB:13:1:1
  26. 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. https://doi.org/10.1046/j.1365-2958.2002.02878.x
  27. 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.
  28. 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.
  29. Kumar, S., R. Lipman, and M. Tomasz. 1992. Recognition of specific DNA sequences by mitomycin C for alkylation. Biochemistry 31: 1399-1407. https://doi.org/10.1021/bi00120a016
  30. 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. https://doi.org/10.1073/pnas.051612298
  31. 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. https://doi.org/10.1073/pnas.96.17.9757
  32. 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. https://doi.org/10.1093/nar/13.20.7171
  33. 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.
  34. Miller, J. H. 1972. Experiments in Molecular Genetics, p. 439. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
  35. 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. https://doi.org/10.1093/nar/gkn097
  36. 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. https://doi.org/10.1134/S1022795408050037
  37. Naito, Y., K. Kusano, and I. Kobayashi, I. 1995. Selfish behavior of restriction-modification systems. Science 267: 897-899. https://doi.org/10.1126/science.7846533
  38. 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. https://doi.org/10.1073/pnas.95.11.6442
  39. 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. https://doi.org/10.1016/S0378-1119(00)00456-X
  40. 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. https://doi.org/10.1093/nar/22.12.2392
  41. 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. https://doi.org/10.1073/pnas.79.19.5971
  42. Roberts, R. J., T. Vincze, J. Posfai, and D. Macelis. 2007. REBASE: Restriction enzymes and DNA methyltransferases. Nucleic Acids Res. 33: D230-D232.
  43. 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.
  44. 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.
  45. 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. https://doi.org/10.1021/bi951883n
  46. 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. https://doi.org/10.1021/bi951884f
  47. 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. https://doi.org/10.1021/bi00500a003
  48. 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. https://doi.org/10.1007/BF00422921
  49. Tock, M. R. and D. T. F. Dryden. 2005. The biology of restriction and anti-restriction. Curr. Opin. Microbiol. 8: 466-472. https://doi.org/10.1016/j.mib.2005.06.003
  50. 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. https://doi.org/10.1016/0378-1119(85)90120-9
  51. 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.

Cited by

  1. Conflicts Targeting Epigenetic Systems and Their Resolution by Cell Death: Novel Concepts for Methyl-Specific and Other Restriction Systems vol.17, pp.6, 2010, https://doi.org/10.1093/dnares/dsq027
  2. Natural C-independent expression of restriction endonuclease in a C protein-associated restriction-modification system vol.44, pp.6, 2016, https://doi.org/10.1093/nar/gkv1331
  3. Restriction endonuclease triggered bacterial apoptosis as a mechanism for long time survival vol.45, pp.14, 2010, https://doi.org/10.1093/nar/gkx576
  4. Controller protein of restriction–modification system Kpn2I affects transcription of its gene by acting as a transcription elongation roadblock vol.46, pp.20, 2010, https://doi.org/10.1093/nar/gky880
  5. Natural tuning of restriction endonuclease synthesis by cluster of rare arginine codons vol.9, pp.None, 2010, https://doi.org/10.1038/s41598-019-42311-w
  6. Low-level expression of the Type II restriction–modification system confers potent bacteriophage resistance in Escherichia coli vol.27, pp.1, 2020, https://doi.org/10.1093/dnares/dsaa003