Some aspects of the SOS response system - A critical survey.

• Authors: Celina Janion
• Languages of publication: EN

Abstracts

EN

The SOS system and SOS mutagenesis are frequently studied, or exploited to obtain an increase in mutagenicity of bacteria. Here a short survey is made of the phenomenon of SOS response with special attention to latest and less discussed data, especially the induction of the SOS system in response to cell starvation or mutation of certain genes and the role of inducible DNA polymerases.

Keywords

EN

SOS response; error-prone DNA polymerases; chronic SOS induction; DNA-repair; adaptive mutations; DNA mutations

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2001
• Volume: 48
• Issue: 3
• Pages: 599-610

Dates

published

2001

received

2001-03-12

revised

2001-05-14

accepted

2001-06-6

Contributors

author

Celina Janion

• Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warszawa, Poland

References

• 1. Weigle, J.J. (1953) Induction of mutation in a bacterial virus. Proc. Natl. Acad. Sci. U.S.A. 39, 628-636.
• 2. Radman, M. (1974) Phenomenology of an inducible mutagenic DNA repair pathway in Escherichia coli: SOS repair hypothesis; in Molecular and Environmental Aspects of Mutagenesis (Sherman, S., Miller, M., Lawrence, C. & Tabor, W.H., eds.) pp. 128-142, Charles C. Thomas Publisher, Springfield.
• 3. Herman, L. & Luria, S.E. (1967) Transduction studies on the role of rec+ gene in the ultraviolet induction of prophage lambda. J. Mol. Biol. 23, 117-133.
• 4. Green, M.H., Greenberg, J. & Donch, J. (1969) Effect of a recA gene on cell division and capsular polysaccharide production in a lon strain of Escherichia coli. Genet. Res. 14, 159-162.
• 5. Witkin, E. (1969) Ultraviolet induced mutation and DNA repair. Annu. Rev. Microbiol. 23, 487-514.
• 6. Defais, M., Fauquet, P., Radman, M. & Errera, M. (1971) Ultraviolet reactivation and ultraviolet mutagenesis of λ in different genetic systems. Virology 43, 495-503.
• 7. Witkin, E.M. (1989) Ultraviolet mutagenesis and the SOS response in Escherichia coli: A personal perspective. Environ. Mol. Mutagen. 14, 30-34.
• 8. Roberts, J.W. & Roberts, C.W. (1975) Proteolytic cleavage of bacteriophage lambda repressor in induction. Proc. Natl. Acad. Sci. U.S.A. 72, 147-151.
• 9. Gudas, L.J. & Pardee, A.B. (1975) Model for regulation of Escherichia coli DNA repair functions. Proc. Natl. Acad. Sci. U.S.A. 72, 2330-2334.
• 10. Roberts, J.W., Roberts, C.W. & Craig, N.L. (1978) Escherichia coli recA gene product inactivates phage lambda repressor. Proc. Natl. Acad. Sci. U.S.A. 75, 4714-4718.
• 11. Little, J.W., Edmiston, S.H., Pacelli, L.Z. & Mount, D.W. (1980) Cleavage of Escherichia coli LexA protein by RecA protease. Proc. Natl. Acad. Sci. U.S.A. 77, 3225-3229.
• 12. Walker, G.C. (1984) Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol. Rev. 48, 60-93.
• 13. Little, J.W. & Mount, D.W. (1982) The SOS regulatory system of Escherichia coli. Cell 29, 11-22.
• 14. Suzuki, K., Miyaki, M., Ono, T., Mori, H., Moriya, H. & Kato, T. (1983) UV-induced imbalance of the deoxyribonucleoside triphosphate pool in E. Coli. Mutat. Res. 122, 293-298.
• 15. Barbe, J., Villaverde, A. & Guerrero, R. (1983) Evolution of cellular ATP concentration after UV-mediated induction of SOS system in Escherichia coli. Biochem. Biophys. Res. Commun. 117, 556-561.
• 16. Guerrero, R., Liagostera, M., Villaverde, A. & Barbe, J. (1984) Changes in ATP concentration in Escherichia coli during induction of the SOS system by mitomycin C and bleomycin. J. Gen. Microbiol. 130, 2247-2251.
• 17. Dahan-Grobgeld, E., Livneh, Z., Maretzek, F., Polak-Charcon, S., Eichenbaum, Z. & Degani, H. (1998) Reversible induction of ATP synthesis by DNA damage and repair in Escherichia coli. In vivo NMR studies. J. Biol. Chem. 273, 30232-30238.
• 18. Kenyon, C.J. & Walker, G.C. (1980) DNA damaging agents stimulate gene expression at specific loci in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 77, 2819-2823.
• 19. Walker, G.C., Kenyon, C.J., Baggs, A., Elledge, S.J., Parry, K.L. & Shanabruch, W.G. (1982) Regulation and functions of Escherichia coli genes induced by DNA damage; in Molecular and Cellular Mechanism of Mutagenesis (Lemont, J.F. & Generoso, W.M., eds.) pp. 43-63, Plenum Publishing Corp. New York.
• 20. Casadaban, M.J. & Cohen, S.N. (1979) Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc. Natl. Acad. Sci. U.S.A. 76, 4530-4533.
• 21. Quillardet, P., Bellecombe, C. & Hofnung, M. (1985) The SOS chromotest, a colorimetric bacterial assay for genotoxins: Validation study with 83 compounds. Mutat. Res. 147, 79-95.
• 22. Lewis, L.K., Harlow, G.R., Gregg-Jolly, R.A. & Mount, D.W. (1994) Identification of high affinity binding sites for LexA which define new DNA damage inducible genes in Escherichia coli. J. Mol. Biol. 241, 507-523.
• 23. Kuzminov, A. (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage λ. Microbiol. Mol. Biol. Rev. 63, 751-813.
• 24. Fernandez de Henestrosa, A., Ogi, T., Aoyagi, S., Chafin, D., Hayes, J.J., Ohmori, H. & Woodgate, R. (2000) Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol. Microbiol. 35, 1560-1572.
• 25. Yasuda, T., Morimatsu, K., Horii, T., Nagata, T. & Ohmori, H. (1998) Inhibition of Escherichia coli RecA coprotease by Din I. EMBO J. 17, 3207-3216.
• 26. Bonner, C.A., Stukenberg, P.T., Rajagopalan, M., Eritja, R., O'Donnell, M., McEntee, K., Echols, H. & Goodman, M.F. (1988) Processive DNA synthesis by DNA polymerase II mediated by DNA polymerase III accessory proteins. J. Biol. Chem. 267, 11431-11438.
• 27. Rangarajan, S., Woodgate, R. & Goodman, M.F. (1999) A phenotype for enigmatic DNA polymerase II in replication restart in UV-irradiated Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 96, 9224-9229.
• 28. Asai, T., Bates, D.B. & Kogoma, T. (1994) DNA replication triggered by double-strand breaks in E. coli; Dependence on homologous recombination functions. Cell 78, 1051-1061.
• 29. Kowalczykowski, S.C., Dixon, D.A., Eggleston, A.K., Lauder, S.D. & Rehrauer, W.M. (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol. Rev. 58, 401-465.
• 30. Picksley, S.M., Attfield, P.V. & Lloyd, R.G. (1984) Repair of DNA double-strand breaks in Escherichia coli K12 requires a functional recN product. Mol. Gen. Genet. 195, 267-274.
• 31. Kowalczykowski, S.C. (2000) Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci. 25, 156-165.
• 32. Clark, A.J. & Margulies, A.D. (1965) Isolation and characterisation of recombination-deficient mutant of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 53, 451-459.
• 33. Tang, M., Shen, X., Frank, E.G., O'Donnell, M., Woodgate, R. & Goodman, M.F. (1999) UmuD'2C is an error-prone DNA polymerase, Escherichia coli pol V. Proc. Natl. Acad. Sci. U.S.A. 96, 8919-8924.
• 34. Robison, K., McGuire, A.M. & Church, G.M. (1998) A comprehensive library of DNA-binding site matrices for 55 proteins applied to the complete Escherichia coli K-12 genome. J. Mol. Biol. 284, 241-254.
• 35. Dri, A.M. & Moreau, P.L. (1994) Control of the LexA regulon by pH: Evidence for a reversible inactivation of the LexA repressor during the growth cycle of Escherichia coli. Mol. Microbiol. 12, 621-629.
• 36. Taddei, F., Matic, I. & Radman, M. (1995) cAMP-dependent SOS induction and mutagenesis in resting bacterial populations. Proc. Natl. Acad. Sci. U.S.A. 92, 11736-11740.
• 37. Koch, W.H. & Woodgate, R. (1998) The SOS response; in DNA Damage and Repair, vol. 1, DNA Repair in Prokaryotes and Lower Eukaryotes (Nickoloff, J.A. & Hoekstra, M.F., eds.) pp. 107-134, Humana Press Inc., Totova.
• 38. MacPhee, D.G. (1993) Directed mutation: Paradigm postponed. Mutat. Res. 285, 109- 116.
• 39. Ambrose, M. & MacPhee, D.G. (1998) Glucose and related catabolite repressors are powerful inhibitors of pKM101-enhanced UV mutagenesis in Escherichia coli. Mutat. Res. 422, 107-112.
• 40. Cairns, J., Overbaugh, J. & Miller, S. (1988) The origin of mutants. Nature 335, 142-145.
• 41. Hall, B.G. (1998) Adaptive mutagenesis: A process that generates almost exclusively beneficial mutations. Genetica 102-103, 109-125.
• 42. Bridges, B.A. (1998) The role of DNA damage in stationary phase (adaptive) mutation. Mutat. Res. 408, 1-9.
• 43. Foster, P.L. (1999) Mechanism of stationary phase mutation: A decade of adaptive mutation. Annu. Rev. Genet. 33, 57-88.
• 44. Janion, C. (2000) A new look at adaptive mutations in bacteria. Acta Biochim. Polon. 47, 451-457.
• 45. Costa de Oliviera, R., Laval, J. & Boiteux, S. (1986) Induction of SOS and adaptive responses by alkylating agents in Escherichia coli mutants deficient in 3-methyladenine- DNA glycosylase activities. Mutat. Res. 183, 11-20.
• 46. Peterson, K.R., Wertman, K.F. & Mount, D.W. & Marinus, M.G. (1985) Viability of Escherichia coli K-12 DNA adenine methylase (dam) mutants requires increased expression of specific genes in the SOS regulon. Mol. Gen. Genet. 201, 14-19.
• 47. Bębenek, K. & Janion, C. (1985) Ability of base analogs to induce the SOS response: Effect of a dam mutation and mismatch repair system. Mol. Gen. Genet. 201, 519-524.
• 48. Peterson, K.R., Ossana, N., Thliveris, T, Ennis, D.G. & Mount, D.W. (1998) Derepression of specific genes promotes DNA repair mutagenesis in Escherichia coli. J. Bacteriol. 170, 1-4..
• 49. Peterson, K.R. & Mount, D.W. (1993) Analysis of the genetic requirements for viability of Escherichia coli K-12 DNA adenine methylase mutants. J. Bacteriol. 175, 7505-7508.
• 50. Condra, J.H. & Pauling, C.J. (1982) Induction of the SOS system by DNA ligase-deficient growth of Escherichia coli. J. Gen. Microbiol. 128, 613-621..
• 51. Bates, H., Randall, S.K., Rayssiguier, C., Bridges, B.A., Goodman, M.F. & Radman, M. (1989) Spontaneous and UV-induced mutations in Escherichia coli K-12 strains with altered or absent DNA polymerase I. J. Bacteriol. 171, 2480-2484.
• 52. Ossana, N. & Mount, D.W. (1989) Mutations in uvrD induce the SOS response in Escherichia coli. J. Bacteriol. 171, 303-307.
• 53. SaiSree, L., Reddy, M. & Gowrishankar, J. (2000) lon incompatibility associated with mutations causing SOS induction: null uvrD alleles induce an SOS response in Escherichia coli. J. Bacteriol. 182, 3151-3157.
• 54. Slater, S.C., Lifsics, M.R., O'Donnell, M. & Maurer, R. (1994) holE, the gene coding for teta subunit of DNA polymerase III of Escherichia coli: Characterization of a holE mutant and comparison with a dnaQ (ε subunit) mutant. J. Bacteriol. 176, 815-821.
• 55. Nurse, P., Zavitz, K.H. & Marians, K.J. (1991) Inactivation of the Escherichia coli PriA DNA replication protein induces the SOS response. J. Bacteriol. 173, 6686-6693.
• 56. Dunman, P.M., Ren, L., Rahman, M.S., Palejwala, V.A., Murphy, H.S., Volkert, M.R. & Humayun, M.Z. (2000) Escherichia coli cells defective for the recN gene display constitutive elevation of mutagenesis at 3,N(4)-ethenocytosine via an SOS-induced mechanism. Mol. Microbiol. 37, 680-686.
• 57. Marinus, M.G. (1984) Methylation of prokaryotic DNA; in DNA Methylation (Razin, A., Cedar, H. & Riggs, A.D., eds.) pp. 81-109, Springer Series in Molecular Biology, Springer-Verlag New York Inc.
• 58. Modrich, P. & Lahue, R. (1996) Mismatch repair in replication fidelity, genetic reccombination and cancer biology. Annu. Rev. Biochem. 65, 101-133.
• 59. Kornberg, A. & Baker, T.A. (1992) DNA replication. W.H. Freeman & Co., New York.
• 60. Lijungquist, S. (1997) A new endonuclease from Escherichia coli acting at apurinic sites in DNA. J. Biol. Chem. 252, 2808-2814.
• 61. Weiss, B. (1976) Endonuclease II of Escherichia coli is exonuclease III. J. Biol. Chem. 251, 1896-1901.
• 62. Katcher, H.L. & Wallas, S.S. (1983) Characterization of the Escherichia coli X-ray endonuclease, endonuclease III. Biochemistry 22, 4071-4081.
• 63. Moll, C.D., Hosfield, D.J. & Tainer, H.A. (2000) Abasic site recognition by two apurinic/apyrimidinic endonuclease families in DNA base excision repair: The 3' ends, justify the means. Mutat. Res. 460, 211-229.
• 64. Miller, J.H. (1998) Mutators in Escherichia coli. Mutat. Res. 409, 99-106.
• 65. Horst, J.P., Wu, T.H. & Marinus, M.G. (1999) Escherichia coli mutator genes. Trends Microbiol. 7, 29-36.
• 66. Kato, T. & Shinoura, Y. (1977) Isolation and characterisation of mutant of Escherichia coli deficient in induction of mutation by ultraviolet light. Mol. Gen. Genet. 156, 121-131.
• 67. Bridges, B.A. & Woodgate, R. (1985) Mutagenic repair in Escherichia coli: Products of the recA gene and of the umuD and umuC genes act at different steps in UV-induced mutagenesis. Proc. Natl. Acad. Sci. U.S.A. 82, 4193- 4197.
• 68. Nohmi, T., Battista, J.R., Dodson, L.A. & Walker, G.C. (1988) RecA-mediated cleavage activates UmuD for mutagenesis: Mechanistic relationship between transcriptional derepression and posttranslational activation. Proc. Natl. Acad. Sci. U.S.A. 85, 1816-1820.
• 69. Smith, B.T. & Walker, G.C. (1998) Mutagenesis and more: umuDC and the Escherichia coli SOS response. Genetics 148, 1599-1610.
• 70. Goodman, M.F. (2000) Coping with replication train wrecks in Escherichia coli using Pol V, Pol II and Rec A proteins. Trends Biochem. Sci. 25, 189-195.
• 71. Goodman, M.F & Tippin, B. (2000) Sloppier copier DNA polymerases involved in genome repair. Curr. Opin. Genet. Dev. 10, 162-168.
• 72. Tang, M., Pham, P., Shen, X., Taylor, J.S., O'Donnell, M., Woodgate, R. & Goodman, M.F. (2000) Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis. Nature 404, 1014-1018.
• 73. Maor-Shoshani, A., Reuven, N.B., Tomer, G. & Livneh, Z. (2000) Highly mutagenic replication by DNA polymerase V (UmuC) provides a mechanistic basis for SOS untargeted mutagenesis. Proc. Natl. Acad. Sci. U.S.A. 97, 565-570.
• 74. Napolitano, R., Janel-Bintz, R., Wagner, J. & Fuchs, R.P.P. (2000) All three SOS-inducible DNA polymerases (Pol II, Pol IV and Pol V) are involved in induced mutagenesis. EMBO J. 19, 6259-6265.
• 75. Courcelle, J., Khodursky, A., Peter, B., Brown, P.O. & Hanawalt, P.C. (2001) Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158, 41-64 (reference added in proof).