Translesion DNA polymerases remodel the replisome and alter the speed of the replicative helicase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 15, 2009, Pages 6031-6038

  Indiani, Chiara ^a   Langston, Lance D ^a   Yurieva, Olga ^a   Goodman, Myron F ^b   O'Donnell, Mike ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

DNA repair; DNA replication; Replication fork; Replisome sliding clamp

Indexed keywords

DNA B; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE BETA; DNA DIRECTED DNA POLYMERASE GAMMA; DNA POLYMERASE; HELICASE; REPLISOME; BACTERIAL DNA; DNA DIRECTED DNA POLYMERASE;

ARTICLE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA STRUCTURE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; BACTERIAL CHROMOSOME; BIOSYNTHESIS; ENZYMOLOGY; GENETICS; METABOLISM; TIME;

ESCHERICHIA COLI;

CHROMOSOMES, BACTERIAL; DNA DAMAGE; DNA HELICASES; DNA REPLICATION; DNA, BACTERIAL; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; TIME FACTORS;

EID: 65549153598     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0901403106     Document Type: Article

References (32)

1. Kornberg A, Baker TA (1992) DNA replication. DNA Replication (Freeman Press, New York), 2nd ed, p 931.
2. Johnson A, O'Donnell M (2005) Cellular DNA replicases: Components and dynamics at the replication fork. Annu Rev Biochem 74:283-315.
3. Kim S, Dallmann HG, McHenry CS, Marians KJ (1996) Coupling of a replicative poly-merase and helicase: A tau-DnaB interaction mediates rapid replication fork movement. Cell 84:643-650.
4. Courcelle J, Khodursky A, Peter B, Brown PO, Hanawalt PC (2001) Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli . Genetics 158:41-64.
5. 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 19:6259-6265.
6. Kobayashi S, Valentine MR, Pham P, O'Donnell M, Goodman MF (2002) Fidelity of Escherichia coli DNA polymerase IV. Preferential generation of small deletion mutations by dNTP-stabilized misalignment. J Biol Chem 277:34198-34207.
7. Tang M, et al. (2000) Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis. Nature 404:1014-1018.
8. Cai H, Yu H, McEntee K, Kunkel TA, Goodman MF (1995) Purification and properties of wild-type and exonuclease-deficient DNA polymerase II from Escherichia coli . J Biol Chem 270:15327-15335.
9. Bonner CA, Hays S, McEntee K, Goodman MF (1990) DNA polymerase II is encoded by the DNA damage-inducible dinA gene of Escherichia coli. Proc Natl Acad Sci USA 87:7663-7667.
10. Kim SR, Matsui K, Yamada M, Gruz P, Nohmi T (2001) Roles of chromosomal and episomal dinB genes encoding DNA pol IV in targeted and untargeted mutagenesis in Escherichia coli . Mol Genet Genomics 266:207-215.
11. Qiu Z, Goodman MF (1997) The Escherichia coli polB locus is identical to dinA, the structural gene for DNA polymerase II. Characterization of Pol II purified from a polB mutant. J Biol Chem 272:8611-8617.
12. Woodgate R, Ennis DG (1991) Levels of chromosomally encoded Umu proteins and requirements for in vivo UmuD cleavage. Mol Gen Genet 229:10-16.
13. Woodgate R, Levine AS (1996) Damage inducible mutagenesis: Recent insights into the activities of the Umu family of mutagenesis proteins. Cancer Surv 28:117-140.
14. Indiani C, McInerney P, Georgescu R, Goodman MF, O'Donnell M (2005) A sliding-clamp toolbelt binds high- and low-fidelity DNA polymerases simultaneously. Mol Cell 19:805-815.
15. Yang J, Zhuang Z, Roccasecca RM, Trakselis MA, Benkovic SJ (2004) The dynamic processivity of the T4 DNA polymerase during replication. Proc Natl Acad Sci USA 101:8289-8294.
16. Furukohri A, Goodman MF, Maki H (2008) A dynamic polymerase exchange with Escherichia coli DNA polymerase IV replacing DNA polymerase III on the sliding clamp. J Biol Chem 283:11260-11269.
17. Fujii S, Fuchs RP (2004) Defining the position of the switches between replicative and bypass DNA polymerases. EMBO J 23:4342-4352.
18. Higuchi K, et al. (2003) Fate of DNA replication fork encountering a single DNA lesion during oriC plasmid DNA replication in vitro. Genes Cells 8:437-449.
19. Pages V, Fuchs RP (2003) Uncoupling of leading- and lagging-strand DNA replication during lesion bypass in vivo. Science 300:1300-1303.
20. McInerney P, O'Donnell M (2004) Functional uncoupling of twin polymerases: Mechanism of polymerase dissociation from a lagging-strand block. J Biol Chem 279:21543-21551.
21. Uchida K, et al. (2008) Overproduction of Escherichia coli DNA polymerase DinB (Pol IV) inhibits replication fork progression and is lethal. Mol Microbiol 70:608-622.
22. Duigou S, Ehrlich SD, Noirot P, Noirot-Gros MF (2004) Distinctive genetic feature sexhibited by the Y-family DNA polymerases in Bacillus subtilis. Mol Microbiol 54:439-451.
23. Lee J, Chastain PD, 2nd, Kusakabe T, Griffith JD, Richardson CC (1998) Coordinated leading and lagging strand DNA synthesis on a minicircular template. Mol Cell 1:1001-1010.
24. Bonner CA, et al. (1992) Processive DNA synthesis by DNA polymerase II mediated by DNA polymerase III accessory proteins. J Biol Chem 267:11431-11438.
25. Wagner J, Fujii S, Gruz P, Nohmi T, Fuchs RP (2000) The β -clamp targets DNA polymerase IV to DNA and strongly increases its processivity. EMBO Rep 1:484-488.
26. Gao D, McHenry CS (2001) tau binds and organizes Escherichia coli replication proteins through distinct domains. Domain IV, located within the unique C terminus of tau, binds the replication fork, helicase, DnaB. J Biol Chem 276:4441-4446.
27. Dalrymple BP, Kongsuwan K, Wijffels G, Dixon NE, Jennings PA (2001) A universal protein-protein interaction motif in the eubacterial DNA replication and repair systems. Proc Natl Acad Sci USA 98:11627-11632.
28. Lenne-Samuel N, Wagner J, Etienne H, Fuchs RP (2002) The processivity factor β controls DNA polymerase IV traffic during spontaneous mutagenesis and translesion synthesis in vivo. EMBO Rep 3:45-49.
29. Rangarajan S, Woodgate R, Goodman MF (1999) A phenotype for enigmatic DNA polymerase II: A pivotal role for pol II in replication restart in UV-irradiated Escherichia coli . Proc Natl Acad Sci USA 96:9224-9229.
30. Courcelle CT, Belle JJ, Courcelle J (2005) Nucleotide excision repair or polymerase V-mediated lesion bypass can act to restore UV-arrested replication forks in Escherichia coli . J Bacteriol 187:6953-6961.
31. Little JW, Mount DW, Yanisch-Perron CR (1981) Purified lexA protein is a repressor of the recA and lexA genes. Proc Natl Acad Sci USA 78:4199-4203.
32. Heller RC, Marians KJ (2006) Replication fork reactivation downstream of a blocked nascent leading strand. Nature 439:557-562.