DNA polymerase IV mediates efficient and quick recovery of replication forks stalled at N2-dG adducts

Nucleic Acids Research

Volumn 42, Issue 13, 2014, Pages 8461-8472

  Ikeda, Mio ^a   Furukohri, Asako ^a   Philippin, Gaelle ^b   Loechler, Edward ^c   Akiyama, Masahiro Tatsumi ^a   Katayama, Tsutomu ^d   Fuchs, Robert P ^b   Maki, Hisaji ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b AIX MARSEILLE UNIVERSITY   (France)

^c USA   (United States)

^d KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE GAMMA; DNA POLYMERASE; DNA POLYMERASE IV; DOUBLE STRANDED DNA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CHROMOSOME; CHROMOSOME REPLICATION; CONTROLLED STUDY; DNA ADDUCT; DNA DAMAGE; DNA REPLICATION; DNA TEMPLATE; DOWN REGULATION; ESCHERICHIA COLI; IN VITRO STUDY; PRIORITY JOURNAL; REPLISOME; UPREGULATION;

BENZOPYRENES; DEOXYGUANOSINE; DNA; DNA ADDUCTS; DNA POLYMERASE BETA; DNA POLYMERASE III; DNA REPLICATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS;

EID: 84905589877     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku547     Document Type: Article

References (48)

1. Friedberg, E.C., Walker, G.C., Siede, W, Wood, R.D., Schultz, R.A., and Ellenberger, T.2nd edn Friedberg, E.C., Walker, G.C., Siede, W, Wood, R.D., Schultz, R.A., and Ellenberger, T. (2006) In: DNA Repair and Mutagenesis, ASM Press, Washington, DC..
2. Michel, B., Boubakri, H., Baharoglu, Z., LeMasson, M., and Lestini, R. Michel, B., Boubakri, H., Baharoglu, Z., LeMasson, M., and Lestini, R. (2007) Recombination proteins and rescue of arrested replication forks. DNA Repair (Amst.), 6, 967-980.
3. Gabbai, C.B. and Marians, K.J. Gabbai, C.B. and Marians, K.J. (2010) Recruitment to stalled replication forks of the PriA DNA helicase and replisome-loading activities is essential for survival. DNA Repair (Amst.), 9, 202-209.
4. Costes, A. and Lambert, S.A. ECostes, A. and Lambert, S.A.E (2013) Homologous recombination as a replication fork escort: fork-protection and recovery. Biomolecules, 3, 39-71.
5. Higuchi, K., Katayama, T., Iwai, S., Hidaka, M., Horiuchi, T., and Maki, H. Higuchi, K., Katayama, T., Iwai, S., Hidaka, M., Horiuchi, T., and Maki, H. (2003) Fate of DNA replication fork encountering a single DNA lesion during oriC plasmid DNA replication in vitro. Genes Cells, 8, 437-449.
6. Pages, V. and Fuchs, R.P. Pages, V. and Fuchs, R.P. (2003) Uncoupling of leading- and lagging-strand DNA replication during lesion bypass in vivo. Science, 300, 1300-1303.
7. Yeeles, J.T. and Marians, K.J. Yeeles, J.T. and Marians, K.J. (2011) The Escherichia coli replisome is inherently DNA damage tolerant. Science, 334, 235-238.
8. Sutton, M.D. Sutton, M.D. (2010) Coordinating DNA polymerase traffic during high and low fidelity synthesis. Biochim. Biophys. Acta, 1804, 1167-1179.
9. Sale, J.E., Lehmann, A.R., and Woodgate, R. Sale, J.E., Lehmann, A.R., and Woodgate, R. (2012) Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat. Rev. Mol. Cell Biol., 13, 141-152.
10. Pages, V., Mazon, G., Naiman, K., Philippin, G., and Fuchs, R.P. Pages, V., Mazon, G., Naiman, K., Philippin, G., and Fuchs, R.P. (2012) Monitoring bypass of single replication-blocking lesions by damage avoidance in the escherichia coli chromosome. Nucleic Acids Res., 40, 9036-9043.
11. Izhar, L., Ziv, O., Cohen, I.S., Geacintov, N.E., and Livneh, Z. Izhar, L., Ziv, O., Cohen, I.S., Geacintov, N.E., and Livneh, Z. (2013) Genomic assay reveals tolerance of DNA damage by both translesion DNA synthesis and homology-dependent repair in mammalian cells. Proc. Natl. Acad. Sci. U.S.A., 110, E1462-E1469.
12. Fuchs, R.P. and Fujii, S. Fuchs, R.P. and Fujii, S. (2013) Translesion synthesis and mutagenesis in prokaryotes. Cold Spring Harb. Perspect. Biol., 5, a012682.
13. Wagner, J., Gruz, P., Kim, S.R., Yamada, M., Matsui, K., Fuchs, R.P., and Nohmi, T. Wagner, J., Gruz, P., Kim, S.R., Yamada, M., Matsui, K., Fuchs, R.P., and Nohmi, T. (1999) The dinB gene encodes a novel E. Coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol. Cell, 4, 281-286.
14. Ohmori, H., Friedberg, E.C., Fuchs, R.P., Goodman, M.F., Hanaoka, F., Hinkle, D., Kunkel, T.A., Lawrence, C.W., Livneh, Z., and Nohmi, T. et al. Ohmori, H., Friedberg, E.C., Fuchs, R.P., Goodman, M.F., Hanaoka, F., Hinkle, D., Kunkel, T.A., Lawrence, C.W., Livneh, Z., and Nohmi, T. (2001) The Y-family of DNA polymerases. Mol. Cell, 8, 7-8.
15. Kim, S., Dallmann, H.G., McHenry, C.S., and Marians, K.J. Kim, S., Dallmann, H.G., McHenry, C.S., and Marians, K.J. (1996) Coupling of a replicative polymerase and helicase: a tau-DnaB interaction mediates rapid replication fork movement. Cell, 84, 643-650.
16. Napolitano, R., Janel-Bintz, R., Wagner, J., and Fuchs, R.P. Napolitano, R., Janel-Bintz, R., Wagner, J., and Fuchs, R.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.
17. Shen, X., Sayer, J.M., Kroth, H., Ponten, I., O'Donnell, M., Woodgate, R., Jerina, D.M., and Goodman, M.F. Shen, X., Sayer, J.M., Kroth, H., Ponten, I., O'Donnell, M., Woodgate, R., Jerina, D.M., and Goodman, M.F. (2002) Efficiency and accuracy of SOS-induced DNA polymerases replicating benzo[a]pyrene-7, 8-diol 9, 10-epoxide A and G adducts. J. Biol. Chem., 277, 5265-5274.
18. Seo, K.Y., Nagalingam, A., Miri, S., Yin, J., Chandani, S., Kolbanovskiy, A., Shastry, A., and Loechler, E.L. Seo, K.Y., Nagalingam, A., Miri, S., Yin, J., Chandani, S., Kolbanovskiy, A., Shastry, A., and Loechler, E.L. (2006) Mirror image stereoisomers of the major benzo[a]pyrene N2-dG adduct are bypassed by different lesion-bypass DNA polymerases in E. Coli. DNA Repair (Amst.), 5, 515-522.
19. Jarosz, D.F., Godoy, V.G., Delaney, J.C., Essigmann, J.M., and Walker, G.C. Jarosz, D.F., Godoy, V.G., Delaney, J.C., Essigmann, J.M., and Walker, G.C. (2006) A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates. Nature, 439, 225-228.
20. Kumari, A., Minko, I.G., Harbut, M.B., Finkel, S.E., Goodman, M.F., and Lloyd, R.S. Kumari, A., Minko, I.G., Harbut, M.B., Finkel, S.E., Goodman, M.F., and Lloyd, R.S. (2008) Replication bypass of interstrand cross-link intermediates by Escherichia coli DNA polymerase IV. J. Biol. Chem., 283, 27433-27437.
21. Minko, I.G., Yamanaka, K., Kozekov, I.D., Kozekova, A., Indiani, C., O'Donnell, M.E., Jiang, Q., Goodman, M.F., Rizzo, C.J., and Lloyd, R.S. Minko, I.G., Yamanaka, K., Kozekov, I.D., Kozekova, A., Indiani, C., O'Donnell, M.E., Jiang, Q., Goodman, M.F., Rizzo, C.J., and Lloyd, R.S. (2008) Replication bypass of the acrolein-mediated deoxyguanine DNA-peptide cross-links by DNA polymerases of the DinB family. Chem. Res. Toxicol., 21, 1983-1990.
22. Yuan, B., Cao, H., Jiang, Y., Hong, H., and Wang, Y. Yuan, B., Cao, H., Jiang, Y., Hong, H., and Wang, Y. (2008) Efficient and accurate bypass of N2-(1-carboxyethyl)-2'-deoxyguanosine by DinB DNA polymerase in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A., 105, 8679-8684.
23. Bjedov, I., Dasgupta, C.N., Slade, D., Le Blastier, S., Selva, M., and Matic, I. Bjedov, I., Dasgupta, C.N., Slade, D., Le Blastier, S., Selva, M., and Matic, I. (2007) Involvement of Escherichia coli DNA polymerase IV in tolerance of cytotoxic alkylating DNA lesions in vivo. Genetics, 176, 1431-1440.
24. Indiani, C., McInerney, P., Georgescu, R., Goodman, M.F., and O'Donnell, M. Indiani, C., McInerney, P., Georgescu, R., Goodman, M.F., and O'Donnell, M. (2005) A sliding-clamp toolbelt binds highand low-fidelity DNA polymerases simultaneously. Mol. Cell, 19, 805-815.
25. Furukohri, A., Goodman, M.F., and Maki, H. Furukohri, A., Goodman, M.F., and 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.
26. Bunting, K.A., Roe, S.M., and Pearl, L.H. Bunting, K.A., Roe, S.M., and Pearl, L.H. (2003) Structural basis for recruitment of translesion DNA polymerase pol IV/DinB to the beta-clamp. EMBO J., 22, 5883-5892.
27. Burnouf, D.Y., Olieric, V., Wagner, J., Fujii, S., Reinbolt, J., Fuchs, R.P., and Dumas, P. Burnouf, D.Y., Olieric, V., Wagner, J., Fujii, S., Reinbolt, J., Fuchs, R.P., and Dumas, P. (2004) Structural and biochemical analysis of sliding clamp/ligand interactions suggest a competition between replicative and translesion DNA polymerases. J. Mol. Biol., 335, 1187-1197.
28. Heltzel, J.M., Maul, R.W., Wolff, D.W., and Sutton, M.D. Heltzel, J.M., Maul, R.W., Wolff, D.W., and Sutton, M.D. (2012) Escherichia coli DNA polymerase IV (pol IV), but not pol II, dynamically switches with a stalled pol III replicase. J. Bacteriol., 194, 3589-3600.
29. Wagner, J., Etienne, H., Fuchs, R.P., Cordonnier, A., and Burnouf, D. Wagner, J., Etienne, H., Fuchs, R.P., Cordonnier, A., and Burnouf, D. (2009) Distinct beta-clamp interactions govern the activities of the Y family PolIV DNA polymerase. Mol. Microbiol., 74, 1143-1151.
30. Godoy, V.G., Jarosz, D.F., Simon, S.M., Abyzov, A., Ilyin, V., and Walker, G.C. Godoy, V.G., Jarosz, D.F., Simon, S.M., Abyzov, A., Ilyin, V., andWalker, G.C. (2007) UmuD and RecA directly modulate the mutagenic potential of the Y family DNA polymerase DinB. Mol. Cell, 28, 1058-1070.
31. Cafarelli, T.M., Rands, T.J., Benson, R.W., Rudnicki, P.A., Lin, I., and Godoy, V.G. Cafarelli, T.M., Rands, T.J., Benson, R.W., Rudnicki, P.A., Lin, I., and Godoy, V.G. (2013) A single residue unique to DinB-like proteins limits formation of the polymerase IV multiprotein complex in Escherichia coli. J. Bacteriol., 195, 1179-1193.
32. Funnell, B.E., Baker, T.A., and Kornberg, A. Funnell, B.E., Baker, T.A., and Kornberg, A. (1986) Complete enzymatic replication of plasmids containing the origin of the Escherichia coli chromosome. J. Biol. Chem., 261, 5616-5624.
33. Maki, H., Maki, S., and Kornberg, A. Maki, H., Maki, S., and Kornberg, A. (1988) DNA polymerase III holoenzyme of Escherichia coli. IV. the holoenzyme is an asymmetric dimer with twin active sites. J. Biol. Chem., 263, 6570-6578.
34. Sugaya, Y., Ihara, K., Masuda, Y., Ohtsubo, E., and Maki, H. Sugaya, Y., Ihara, K., Masuda, Y., Ohtsubo, E., and Maki, H. (2002) Hyper-processive and slower DNA chain elongation catalysed by DNA polymerase III holoenzyme purified from the dnaE173 mutator mutant of Escherichia coli. Genes Cells, 7, 385-399.
35. Koehl, P., Burnouf, D., and Fuchs, R.P. Koehl, P., Burnouf, D., and Fuchs, R.P. (1989) Construction of plasmids containing a unique acetylaminofluorene adduct located within a mutation hot spot. A new probe for frameshift mutagenesis. J. Mol. Biol., 207, 355-364.
36. Lenne-Samuel, N., Janel-Bintz, R., Kolbanovskiy, A., Geacintov, N.E., and Fuchs, R.P. Lenne-Samuel, N., Janel-Bintz, R., Kolbanovskiy, A., Geacintov, N.E., and Fuchs, R.P. (2000) The processing of a benzo(a)pyrene adduct into a frameshift or a base substitution mutation requires a different set of genes in Escherichia coli. Mol. Microbiol., 38, 299-307.
37. Wagner, J., Fujii, S., Gruz, P., Nohmi, T., and Fuchs, R.P. Wagner, J., Fujii, S., Gruz, P., Nohmi, T., and Fuchs, R.P. (2000) The beta clamp targets DNA polymerase IV to DNA and strongly increases its processivity. EMBO Rep., 1, 484-488.
38. Friedman, K.L. and Brewer, B.J. Friedman, K.L. and Brewer, B.J. (1995) Analysis of replication intermediates by two-dimensional agarose gel electrophoresis. Methods Enzymol., 262, 613-627.
39. Kurth, I. and O'Donnell, M. Kurth, I. and O'Donnell, M. (2013) New insights into replisome fluidity during chromosome replication. Trends Biochem. Sci., 38, 195-203.
40. Maki, H. and Furukohri, A. Lennarz, W.J. and Lane, M.D. Eds. Maki, H. and Furukohri, A. InedsVolMaki, H. and Furukohri, A. (2013) DNA polymerase III, bacterial. In: The Encyclopedia of Biological Chemistry, Lennarz, W.J. and Lane, M.D. Eds. Academic Press, Waltham, MA. pp. 92-95.
41. Marians, K.J. Marians, K.J. (1992) Prokaryotic DNA replication. Annu. Rev. Biochem., 61, 673-719.
42. Heltzel, J.M., Maul, R.W., Scouten Ponticelli, S.K., and Sutton, M.D. Heltzel, J.M., Maul, R.W., Scouten Ponticelli, S.K., and Sutton, M.D. (2009) A model for DNA polymerase switching involving a single cleft and the rim of the sliding clamp. Proc. Natl. Acad. Sci. U.S.A., 106, 12664-12669.
43. Ozawa, K., Horan, N.P., Robinson, A., Yagi, H., Hill, F.R., Jergic, S., Xu, Z.Q., Loscha, K.V., Li, N., and Tehei, M. et al. Ozawa, K., Horan, N.P., Robinson, A., Yagi, H., Hill, F.R., Jergic, S., Xu, Z.Q., Loscha, K.V., Li, N., and Tehei, M. (2013) Proofreading exonuclease on a tether: the complex between the E. Coli DNA polymerase III subunits alpha, epsilon, theta and beta reveals a highly flexible arrangement of the proofreading domain. Nucleic Acids Res., 41, 5354-5367.
44. Toste Rego, A., Holding, A.N., Kent, H., and Lamers, M.H. Toste Rego, A., Holding, A.N., Kent, H., and Lamers, M.H. (2013) Architecture of the pol III-clamp-exonuclease complex reveals key roles of the exonuclease subunit in processive DNA synthesis and repair. EMBO J., 32, 1334-1343.
45. Jasti, V.P., Das, R.S., Hilton, B.A., Weerasooriya, S., Zou, Y., and Basu, A.K. Jasti, V.P., Das, R.S., Hilton, B.A., Weerasooriya, S., Zou, Y., and Basu, A.K. (2011) (5'S)-8, 5'-cyclo-2'-deoxyguanosine is a strong block to replication, a potent pol V-dependent mutagenic lesion, and is inefficiently repaired in escherichia coli. Biochemistry, 50, 3862-3865.
46. Yuan, B., Wang, J., Cao, H., Sun, R., and Wang, Y. Yuan, B., Wang, J., Cao, H., Sun, R., and Wang, Y. (2011) High-throughput analysis of the mutagenic and cytotoxic properties of DNA lesions by next-generation sequencing. Nucleic Acids Res., 39, 5945-5954.
47. Ippoliti, P.J., Delateur, N.A., Jones, K.M., and Beuning, P.J. Ippoliti, P.J., Delateur, N.A., Jones, K.M., and Beuning, P.J. (2012) Multiple strategies for translesion synthesis in bacteria. Cells, 1, 799-831.
48. McInerney, P. and O'Donnell, M. McInerney, P. and O'Donnell, M. (2004) Functional uncoupling of twin polymerases: Mechanism of polymerase dissociation from a lagging-strand block. J. Biol. Chem., 279, 21543-21551.