A New Model for SOS-induced Mutagenesis: How RecA Protein Activates DNA Polymerase V

Overview

Journal Crit Rev Biochem Mol Biol

Publisher Informa Healthcare

Specialties Biochemistry
Molecular Biology

Date 2010 May 6

PMID 20441441

Citations 63

Authors

Meghna Patel

Qingfei Jiang

Roger Woodgate

Michael M Cox

Myron F Goodman

Affiliations

Soon will be listed here.

Abstract

In Escherichia coli, cell survival and genomic stability after UV radiation depends on repair mechanisms induced as part of the SOS response to DNA damage. The early phase of the SOS response is mostly dominated by accurate DNA repair, while the later phase is characterized with elevated mutation levels caused by error-prone DNA replication. SOS mutagenesis is largely the result of the action of DNA polymerase V (pol V), which has the ability to insert nucleotides opposite various DNA lesions in a process termed translesion DNA synthesis (TLS). Pol V is a low-fidelity polymerase that is composed of UmuD'(2)C and is encoded by the umuDC operon. Pol V is strictly regulated in the cell so as to avoid genomic mutation overload. RecA nucleoprotein filaments (RecA*), formed by RecA binding to single-stranded DNA with ATP, are essential for pol V-catalyzed TLS both in vivo and in vitro. This review focuses on recent studies addressing the protein composition of active DNA polymerase V, and the role of RecA protein in activating this enzyme. Based on unforeseen properties of RecA*, we describe a new model for pol V-catalyzed SOS-induced mutagenesis.

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References

Silvian L, Toth E, Pham P, Goodman M, Ellenberger T . Crystal structure of a DinB family error-prone DNA polymerase from Sulfolobus solfataricus. Nat Struct Biol. 2001; 8(11):984-9. DOI: 10.1038/nsb1101-984. View

Woodgate R . Construction of a umuDC operon substitution mutation in Escherichia coli. Mutat Res. 1992; 281(3):221-5. DOI: 10.1016/0165-7992(92)90012-7. View

Tang M, Shen X, Frank E, ODonnell M, Woodgate R, Goodman M . UmuD'(2)C is an error-prone DNA polymerase, Escherichia coli pol V. Proc Natl Acad Sci U S A. 1999; 96(16):8919-24. PMC: 17708. DOI: 10.1073/pnas.96.16.8919. View

Yang W, Woodgate R . What a difference a decade makes: insights into translesion DNA synthesis. Proc Natl Acad Sci U S A. 2007; 104(40):15591-8. PMC: 2000391. DOI: 10.1073/pnas.0704219104. View

Pham P, Bertram J, ODonnell M, Woodgate R, Goodman M . A model for SOS-lesion-targeted mutations in Escherichia coli. Nature. 2001; 409(6818):366-70. DOI: 10.1038/35053116. View

Clark A, Sandler S . Homologous genetic recombination: the pieces begin to fall into place. Crit Rev Microbiol. 1994; 20(2):125-42. DOI: 10.3109/10408419409113552. View

Sweasy J, WITKIN E, Sinha N . RecA protein of Escherichia coli has a third essential role in SOS mutator activity. J Bacteriol. 1990; 172(6):3030-6. PMC: 209104. DOI: 10.1128/jb.172.6.3030-3036.1990. View

Joo C, McKinney S, Nakamura M, Rasnik I, Myong S, Ha T . Real-time observation of RecA filament dynamics with single monomer resolution. Cell. 2006; 126(3):515-27. DOI: 10.1016/j.cell.2006.06.042. View

Register 3rd J, Griffith J . The direction of RecA protein assembly onto single strand DNA is the same as the direction of strand assimilation during strand exchange. J Biol Chem. 1985; 260(22):12308-12. View

10.

Shinagawa H, Iwasaki H, Kato T, Nakata A . RecA protein-dependent cleavage of UmuD protein and SOS mutagenesis. Proc Natl Acad Sci U S A. 1988; 85(6):1806-10. PMC: 279868. DOI: 10.1073/pnas.85.6.1806. View

11.

Rajagopalan M, Lu C, Woodgate R, ODonnell M, Goodman M, Echols H . 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. 1992; 89(22):10777-81. PMC: 50425. DOI: 10.1073/pnas.89.22.10777. View

12.

Fujii S, Gasser V, Fuchs R . The biochemical requirements of DNA polymerase V-mediated translesion synthesis revisited. J Mol Biol. 2004; 341(2):405-17. DOI: 10.1016/j.jmb.2004.06.017. View

13.

Yu X, Egelman E . Direct visualization of dynamics and co-operative conformational changes within RecA filaments that appear to be associated with the hydrolysis of adenosine 5'-O-(3-thiotriphosphate). J Mol Biol. 1992; 225(1):193-216. DOI: 10.1016/0022-2836(92)91036-o. View

14.

Steinborn G . Uvm mutants of Escherichia coli K12 deficient in UV mutagenesis. II. Further evidence for a novel function in error-prone repair. Mol Gen Genet. 1979; 175(2):203-8. DOI: 10.1007/BF00425537. View

15.

Weinstock G, McEntee K, Lehman I . Hydrolysis of nucleoside triphosphates catalyzed by the recA protein of Escherichia coli. Steady state kinetic analysis of ATP hydrolysis. J Biol Chem. 1981; 256(16):8845-9. View

16.

Clark A, MARGULIES A . ISOLATION AND CHARACTERIZATION OF RECOMBINATION-DEFICIENT MUTANTS OF ESCHERICHIA COLI K12. Proc Natl Acad Sci U S A. 1965; 53:451-9. PMC: 219534. DOI: 10.1073/pnas.53.2.451. View

17.

Gonzalez M, Rasulova F, Maurizi M, Woodgate R . Subunit-specific degradation of the UmuD/D' heterodimer by the ClpXP protease: the role of trans recognition in UmuD' stability. EMBO J. 2000; 19(19):5251-8. PMC: 302103. DOI: 10.1093/emboj/19.19.5251. View

18.

Skoneczna A, McIntyre J, Skoneczny M, Policinska Z, Sledziewska-Gojska E . Polymerase eta is a short-lived, proteasomally degraded protein that is temporarily stabilized following UV irradiation in Saccharomyces cerevisiae. J Mol Biol. 2007; 366(4):1074-86. DOI: 10.1016/j.jmb.2006.11.093. View

19.

Pugh B, Cox M . Stable binding of recA protein to duplex DNA. Unraveling a paradox. J Biol Chem. 1987; 262(3):1326-36. View

20.

Kurumizaka H, Shibata T . Homologous recognition by RecA protein using non-equivalent three DNA-strand-binding sites. J Biochem. 1996; 119(2):216-23. DOI: 10.1093/oxfordjournals.jbchem.a021224. View