Preferences help
enabled [disable] Abstract
Number of results
2003 | 50 | 4 | 921-939
Article title

UV- and MMS-induced mutagenesis of lO(am)8 phage under nonpermissive conditions for phage DNA replication.

Title variants
Languages of publication
Mutagenesis in Escherichia coli, a subject of many years of study is considered to be related to DNA replication. DNA lesions nonrepaired by the error-free nucleotide excision repair (NER), base excision repair (BER) and recombination repair (RR), stop replication at the fork. Reinitiation needs translesion synthesis (TLS) by DNA polymerase V (UmuC), which in the presence of accessory proteins, UmuD', RecA and ssDNA-binding protein (SSB), has an ability to bypass the lesion with high mutagenicity. This enables reinitiation and extension of DNA replication by DNA polymerase III (Pol III). We studied UV- and MMS-induced mutagenesis of λO(am)8 phage in E. coli 594 sup+ host, unable to replicate the phage DNA, as a possible model for mutagenesis induced in nondividing cells (e.g. somatic cells). We show that in E. coli 594 sup+ cells UV- and MMS-induced mutagenesis of λO(am)8 phage may occur. This mutagenic process requires both the UmuD' and C proteins, albeit a high level of UmuD' and low level of UmuC seem to be necessary and sufficient. We compared UV-induced mutagenesis of λO(am)8 in nonpermissive (594 sup+) and permissive (C600 supE) conditions for phage DNA replication. It appeared that while the mutagenesis of λO(am)8 in 594 sup+ requires the UmuD' and C proteins, which can not be replaced by other SOS-inducible protein(s), in C600 supE their functions may be replaced by other inducible protein(s), possibly DNA polymerase IV (DinB). Mutations induced under nonpermissive conditions for phage DNA replication are resistant to mismatch repair (MMR), while among those induced under permissive conditions, only about 40% are resistant.
Physical description
  • Institute of Biochemistry and Biophysics, Department of Molecular Biology, Polish Academy of Sciences, Warszawa, Poland
  • Institute of Biochemistry and Biophysics, Department of Molecular Biology, Polish Academy of Sciences, Warszawa, Poland
  • Institute of Biochemistry and Biophysics, Department of Molecular Biology, Polish Academy of Sciences, Warszawa, Poland
  • Institute of Biochemistry and Biophysics, Department of Molecular Biology, Polish Academy of Sciences, Warszawa, Poland
  • Appleyard RK. (1953) Segregation of lambda lysogenicity during bacterial recombination in E.coli K12. Cold Spring Harb Symp Quant Biol.; 18: 95-7.
  • Becherel OJ, Fuchs RP, Wagner J. (2002) Pivotal role of beta clamp in translesion synthesis and mutagenesis in E.coli cells. DNA Repair (Amst).; 1: 703-8.
  • Boorstein RJ, Hilbert TP, Cunningham RP, Teebor GW. (1990) Formation and stability of repairable pyrimidine photohydrates in DNA. Biochemistry.; 29: 10455-60.
  • Boudsocq F, Ling H, Yang W, Woodgate R. (2002) Structure-based interpretation of missence mutations in Y-family DNA polymerases and their implications for polymerase function and lesion bypass. DNA Repair (Amst).; 1: 343-58.
  • Brotcorne-Lannoye A, Maenhaut-Michel G. (1986) Role of RecA protein in untargeted UV mutagenesis of bacteriophage lambda: evidence for the requirement for the dinB gene. Proc Natl Acad Sci U S A.; 83: 3904-08.
  • Campbell A. (1961) Sensitive mutants of bacteriophage lambda. Virology.; 14: 22-32.
  • Cohen-Fix O, Livneh Z. (1992) Biochemical analysis of UV mutagenesis in Escherichia coli by using a cell-free reaction coupled to a bioassay: identification of a DNA repair-dependent, replication-independent pathway. Proc Natl Acad Sci U S A.; 89: 3300-04.
  • Demple B, Linn S. (1980) DNA N-glycosylases and UV repair. Nature.; 287: 203-8.
  • Demple B, Linn S. (1982) 5,6-Saturated thymine lesions in DNA: production by ultraviolet light or hydrogen peroxide. Nucleic Acids Res.; 10: 3781-9.
  • Dodson M, McMacken R, Echols H. (1989) Specialized nucleoprotein structures at the origin of replication of bacteriophage lambda protein association and disassociation reactions responsible for localized initiation of replication. J Biol Chem.; 264: 10719-25.
  • Doetsch PW, Zastawny TH, Martin AM, Dizdaroglu M. (1995) Monomeric base damage products from adenine, guanine, and thymine induced by exposure of DNA to ultraviolet radiation. Biochemistry.; 34: 737-42.
  • Doyle N, Strike P. (1995) The spectra of base substitutions induced by the impCAB mucAB and umuDC error-prone DNA repair operons differ following exposure to methyl methanesulfonate. Mol Gen Genet.; 247: 735-41.
  • Ebisuzaki K, Dewey CL, Behme MT. (1975) Pathways of DNA repair in T4 phage. I. Methyl methanesulfonate sensitive mutant. Virology.; 64: 330-8.
  • Fijalkowska IJ, Schaaper RM. (1995) Effects of Escherichia coli dnaE antimutator alleles in a proofreading-deficient mutD5. J Bacteriol.; 177: 5979-86.
  • Fisher GJ, Johns HE. (1976) Pyrimidine hydrates. In Photochemistry and photobiology of nucleic acids. Wang SY, ed, vol 1, pp 169-294. Academic Press Inc New York.
  • Frank EG, Cheng N, Do CC, Cerritelli ME, Bruck I, Goodman MF, Egelman EH, Woodgate R, Steven AC. (2000) Visualization of two binding sites for the Escherichia coli UmuD'(2)C complex (DNA pol V) on RecA-ssDNA filaments. J Mol Biol.; 297: 585-97.
  • Friedberg EC, Walker GC, Siede W. (1995) DNA repair and mutagenesis. American Society for Microbiology Press, Washington DC.
  • Goodman MF, Tippin B. (2000) The expanding polymerase universe. Nat Rev Mol Cell Biol.; 1: 101-9.
  • Goodman MF. (2002) Error-prone repair DNA polymerase in prokaryotes and eukaryotes. Annu Rev Biochem.; 71: 17-50.
  • Grzesiuk E, Janion C. (1996) MMS-induced mutagenesis and DNA repair in Escherichia coli dnaQ49: contribution of UmuD' to DNA repair. Mutat Res.; 362: 147-54.
  • Horiuchi T, Maki H, Sekiguchi M. (1978) A new conditional lethal mutator (dnaQ49) in Escherichia coli K12. Mol Gen Genet.; 163: 277-83.
  • Kim SR, Maenhaut-Michel G, Yamada M, Yamamoto Y, Matsui K, Sofuni T, Nohmi T, Ohmori H. (1997) Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA. Proc Natl Acad Sci U S A.; 94: 13792-7.
  • Kim SR, Matsui K, Yamada M, Gruz P, Nohmi T. (2001) Roles of chromosomal and episomal dinB genes encoding DNA polIV in targeted and untargeted mutagenesis in Escherichia coli. Mol Genet Genomics.; 266: 207-15.
  • Kobayashi S, Valentine MR, Pham P, O'Donnell M, Goodman MF. (2002) Fidelity of Escherichia coli DNA polymerase IV. J Biol Chem.; 277: 34198-207.
  • Koch WH, Woodgate R. (1998) The SOS response. In DNA damage and repair. Nickoloff A, Hoekstra MF, eds, vol 1, pp 107-134. Humana Press Inc, New York.
  • Kow YW. (2002) Repair of deaminated bases in DNA. Free Radic Biol Med.; 33: 886-93.
  • Livneh Z. (2001) DNA damage control by novel DNA polymerases: translesion replication and mutagenesis. J Biol Chem.; 276: 25639-42.
  • Loeb LA, Preston BD. (1986) Mutagenesis by apurinic/apyrimidinic sites. Annu Rev Genet.; 20: 201-30.
  • Maor-Shoshani A, Reuven NB, 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: 565-70.
  • Miller JH. (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor New York.
  • Miura A, Tomizawa J. (1970) Mutation and recombination of bacteriophage lambda: effect of ultraviolet radiation. Proc Natl Acad Sci U S A.; 67: 1722-6.
  • Modrich P, Lahue RS. (1996) Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem.; 65: 101-33.
  • Napolitano R, Janel-Bintz R, Wagner J, Fuchs RP. (2000) All three SOS-inducible DNA polymerases (Pol II Pol IV and Pol V) are involved in induced mutagenesis. EMBO J.; 19: 6259-65.
  • Nohmi T, Battista JR, Dodson LA, Walker GC. (1988) RecA-mediated cleavage activates UmuD for mutagenesis: mechanistic relationship between transcriptional derepression and posttranslational activation. Proc Natl Acad Sci U S A.; 85: 1816-20.
  • Ogawa T, Tomizawa J. (1968) Replication of bacteriophage DNA. I. Replication of DNA of lambda phage defective in early functions. J Mol Biol.; 38: 217-25.
  • Opperman T, Murli S, Walker GC. (1996) The genetic requirements for UmuDC-mediated cold sensitivity are distinct from those for SOS mutagenesis. J Bacteriol.; 178: 4400-11.
  • Otoshi E, Yagi T, Mori T, Matsunaga T, Nikaido O, Kim S-T, Hitomi K, Ikenaga M, Todo T. (2000) Respective roles of cyclobutane pyrimidine dimers (6-4)photoproducts, and minor photoproducts in ultraviolet mutagenesis of repair-deficient xeroderma pigmentosum A cells. Cancer Res.; 60: 1729-35.
  • Piechocki R, Kupper D, Quinones A, Langhammer R. (1986) Mutational specificity of a proof-reading defective Escherichia coli dnaQ49 mutator. Mol Gen Genet.; 202: 162-8.
  • Pietrzykowska I. (1973) On the mechanism of bromouracil-induced mutagenesis. Mutat Res.; 19: 1-9.
  • Pietrzykowska I, Felczak M. (1991) Considerations on the mechanisms of UV-induced mutagenesis. In Light in biology and medicine. Douglas RH, Moan J, Ronto G, eds, 2: 485-94.
  • Rajagopalan M, Lu C, Woodgate R, O'Donnell M, Goodman MF, Echols H. (1992) Activity of the purified mutagenesis proteins UmuC UmuD' and RecA in replicative bypass of an abasic DNA lesion by DNA polymerase III. Proc Natl Acad Sci U S A.; 89: 10777-81.
  • Rasmussen LJ, Samson L, Marinus MG. (1998) Dam-directed DNA mismatch repair. In DNA damage and repair: DNA repair in Prokaryotes and Lower Eukaryotes Nickoloff JA, Hoekstra MF, eds, vol 1, pp 205-28. Humana Press Inc, Totowo.
  • Reuven NB, Arad G, Maor-Shoshani A, Livneh Z. (1999) The mutagenesis protein UmuC is a DNA polymerase activated by UmuD' RecA and SSB and is specialized for translesion replication. J Biol Chem.; 274: 31763-6.
  • Reuven NB, Arad G, Stasiak AZ, Stasiak A, Livneh Z. (2001) Lesion bypass by the Escherichia coli polymerase V requires assembly of a RecA nucleoprotein filament. J Biol Chem.; 276: 5511-7.
  • Rothwell DG, Hickson ID. (1997) Repair of apurinic/apyrimidinic (AP) sites in DNA by AP endonucleases In Base excision repair of DNA damage. Hicson ID, ed, pp 67-80. Landes Bioscience Austin T X.
  • Sambrook J, Fritsch EF, Maniatis T. (1989) Molecular Cloning. In A laboratory manual. Cold Spring Harbor, Laboratory Press Cold Spring Harbor New York.
  • Shuster RC, Weissbach A. (1969) Genetic mapping of an endonuclease synthesized by bacteriophage lambda. Nature.; 223: 852-3.
  • Sinha RP, Hader DP. (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci.; 1: 225-36.
  • Stary A, Kannouche P, Lehmann AR, Sarasin A. (2003) Role of DNA polymerase eta in the UV mutation spectrum in human cells. J Biol Chem.; 278: 18767-75.
  • Stephens KM, McMacken R. (1997) Functional properties of replication fork assemblies established by bacteriophage lambdaO and lambdaP replication proteins. J Biol Chem.; 272: 28800-13.
  • Sutton MD, Walker GC. (2001) Managing DNA polymerases: coordinating DNA replication, DNA repair, DNA recombination. Proc Natl Acad Sci U S A.; 98: 8342-9.
  • Sutton MD, Smith BT, Godoy VG, Walker GC. (2000) The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu Rev Genet.; 34: 479-97.
  • Sutton MD, Farrow MF, Burton BM, Walker GC. (2001) Genetic interaction between the Escherichia coli umuDC gene products and the beta processivity clamp of the replicative DNA polymerase. J Bacteriol.; 183: 2897-909.
  • Sutton MD, Guzzo A, Narumi I, Costanzo M, Altenbach C, Ferentz AE, Hubbell WL, Walker GC. (2002) A model for the structure of the Escherichia coli SOS-regulated UmuD2 protein. DNA Repair (Amst).; 1: 77-93.
  • Tang M, Bruck I, Eritja R, Turner J, Frank EG, Woodgate R, O'Donnell M, Goodman MF. (1998) Biochemical basis of SOS-induced mutagenesis in Escherichia coli: reconstitution of in vitro lesion bypass dependent on the UmuD'2C mutagenic complex and RecA protein. Proc Natl Acad Sci U S A.; 95: 9755-60.
  • Tang M, Shen X, Frank EG, O'Donnell M, Woodgate R, Goodman MF. (1999) UmuD'(2)C is an error-prone DNA polymerase Escherichia coli pol V. Proc Natl Acad Sci U S A.; 96: 8919-24.
  • Tang M, Pham P, Shen X, Taylor J-S, O'Donnell M, Woodgate R, Goodman MF. (2000) Roles of E coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis. Nature.; 404: 1014-18.
  • Taylor J-S. (2002) New structural and mechanistic insight into the A-rule and the instructional and non-instructional behaviour of DNA photoproducts and other lesions. Mutat Res.; 510: 55-70.
  • Wagner J, Gruz P, Kim SR, Yamada M, Matsui K, Fuchs RP, Nohmi T. (1999) The dinB gene encodes a novel E coli DNA polymerase DNA pol IV involved in mutagenesis. Mol Cell.; 4: 281-6.
  • Wagner J, Etienne H, Janel-Bintz R, Fuchs RPP. (2002) Genetics of mutagenesis in E.coli: various combinations of translesion polymerases (PolII, IV and V) deal with lesion/sequence context diversity. DNA Repair (Amst).; 1: 159-67.
  • Wang Z. (2001) Translesion synthesis by the UmuC family of DNA polymerases. Mutation Res.; 486: 59-70.
  • Woodgate R. (1992) Construction of a umuDC operon substitution mutation in Escherichia coli. Mutat Res.; 281: 221-5.
  • Woodgate R. (1999) A plethora of lesion-replicating DNA polymerases. Genes Dev.; 13: 2191-5.
  • Woodgate R. (2001) Evolution of the two-step model for UV-mutagenesis. Mutat Res.; 485: 83-92.
  • Woodgate R, Levine AS. (1996) Damage inducible mutagenesis: recent insights into the activities of the Umu family of mutagenesis proteins. Cancer Surv.; 28: 117-40.
  • Woodgate R, Singh M, Kulaeva OI, Frank EG, Levine AS, Koch WH. (1994) Isolation and characterization of novel plasmid-encoded umuC mutants. J Bacteriol.; 176: 5011-21.
  • Wyatt WM, Inokuchi H. (1974) Stability of lambda O and P replication functions. Virology.; 58: 313-15.
  • Yamane T, Wyluda BJ, Shulman RG. (1967) Dihydrothymine from UV-irradiated DNA. Proc Natl Acad Sci U S A.; 58: 439-42.
  • Zhao X, Taylor J-S. (1996) Mutation spectra of TA*, the major photoproduct of thymidylyl-(3'-5')-deoxyadenine, in Escherichia coli under SOS condition. Nucleic Acids Res.; 24: 1561-5.
  • Zylicz M, Ang D, Liberek K, Jamamoto T, Georgopulos C. (1988) Initiation of lambda DNA replication reconstituted with purified lambda and Escherichia coli replication proteins. Biochim Biophys Acta.; 951: 344-50.
  • Zylicz M, Gorska I, Taylor K, Georgopulos C. (1984) Bacteriophage lambda replication proteins: forming of a mixed oilgomer and binding to the origin of lambda DNA. Mol Gen Genet.; 196: 401-6.
Document Type
Publication order reference
YADDA identifier
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.