Toxicological Research

Korean Society of Toxicology & Korea Environmental Mutagen Society (한국독성학회)
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Chronological Switch from Translesion Synthesis to Homology-Dependent Gap Repair In Vivo

  • Fujii, Shingo (DNA Damage Tolerance CNRS) ;
  • Isogawa, Asako (DNA Damage Tolerance CNRS) ;
  • Fuchs, Robert P. (DNA Damage Tolerance CNRS)
  • Received : 2018.07.30
  • Accepted : 2018.08.30
  • Published : 2018.10.15
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Abstract

Cells are constantly exposed to endogenous and exogenous chemical and physical agents that damage their genome by forming DNA lesions. These lesions interfere with the normal functions of DNA such as transcription and replication, and need to be either repaired or tolerated. DNA lesions are accurately removed via various repair pathways. In contrast, tolerance mechanisms do not remove lesions but only allow replication to proceed despite the presence of unrepaired lesions. Cells possess two major tolerance strategies, namely translesion synthesis (TLS), which is an error-prone strategy and an accurate strategy based on homologous recombination (homology-dependent gap repair [HDGR]). Thus, the mutation frequency reflects the relative extent to which the two tolerance pathways operate in vivo. In the present paper, we review the present understanding of the mechanisms of TLS and HDGR and propose a novel and comprehensive view of the way both strategies interact and are regulated in vivo.

Keywords

References

  1. Howard-Flanders, P. and Theriot, L. (1966) Mutants of Escherichia coli K-12 defective in DNA repair and in genetic recombination. Genetics, 53, 1137-1150.
  2. Courcelle, J. and Hanawalt, P.C. (2003) RecA-dependent recovery of arrested DNA replication forks. Annu. Rev. Genet., 37, 611-646. https://doi.org/10.1146/annurev.genet.37.110801.142616
  3. Rupp, W.D. and Howard-Flanders, P. (1968) Discontinuities in the DNA synthesized in an excision-defective strain of Escherichia coli following ultraviolet irradiation. J. Mol. Biol., 31, 291-304. https://doi.org/10.1016/0022-2836(68)90445-2
  4. Rudolph, C.J., Upton, A.L. and Lloyd, R.G. (2007) Replication fork stalling and cell cycle arrest in UV-irradiated Escherichia coli. Genes Dev., 21, 668-681. https://doi.org/10.1101/gad.417607
  5. Yeeles, J.T.P. and Marians, K.J. (2013) Dynamics of leadingstrand lesion skipping by the replisome. Mol. Cell, 52, 855-865. https://doi.org/10.1016/j.molcel.2013.10.020
  6. Pages, V. and Fuchs, RP. (2003) Uncoupling of leading- and lagging-strand DNA replication during lesion bypass in vivo. Science, 300, 1300-1303. https://doi.org/10.1126/science.1083964
  7. Rupp, W.D., Wilde, C.E., Reno, D.L. and Howard-Flanders, P. (1971) Exchanges between DNA strands in ultravioletirradiated Escherichia coli. J. Mol. Biol., 61, 25-44. https://doi.org/10.1016/0022-2836(71)90204-X
  8. Lehmann, A.R. and Fuchs, R.P. (2006) Gaps and forks in DNA replication: rediscovering old models. DNA Repair (Amst.), 5, 1495-1498. https://doi.org/10.1016/j.dnarep.2006.07.002
  9. Lopes, M., Foiani, M. and Sogo, J.M. (2006) Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell, 21, 15-27. https://doi.org/10.1016/j.molcel.2005.11.015
  10. Daigaku, Y., Davies, A.A. and Ulrich, H.D. (2010) Ubiquitin-dependent DNA damage bypass is separable from genome replication. Nature, 465, 951-955. https://doi.org/10.1038/nature09097
  11. Courcelle, C.T., Chow, K.-H., Casey, A. and Courcelle, J. (2006) Nascent DNA processing by RecJ favors lesion repair over translesion synthesis at arrested replication forks in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A., 103, 9154-9159. https://doi.org/10.1073/pnas.0600785103
  12. Cerda-Olmedo, E., Hanawalt, P.C. and Guerola, N. (1968) Mutagenesis of the replication point by nitrosoguanidine: map and pattern of replication of the Escherichia coli chromosome. J. Mol. Biol., 33, 705-719. https://doi.org/10.1016/0022-2836(68)90315-X
  13. Higgins, N.P., Kato, K. and Strauss, B. (1976) A model for replication repair in mammalian cells. J. Mol. Biol., 101, 417-425. https://doi.org/10.1016/0022-2836(76)90156-X
  14. Lehmann, A.R., Kirk-Bell, S., Arlett, C.F., Paterson, M.C., Lohman, P.H., de Weerd-Kastelein, E.A. and Bootsma, D. (1975) Xeroderma pigmentosum cells with normal levels of excision repair have a defect in DNA synthesis after UVirradiation. Proc. Natl. Acad. Sci. U.S.A., 72, 219-223. https://doi.org/10.1073/pnas.72.1.219
  15. Branzei, D. and Szakal, B. (2016) DNA damage tolerance by recombination: Molecular pathways and DNA structures. DNA Repair (Amst.), 44, 68-75. https://doi.org/10.1016/j.dnarep.2016.05.008
  16. 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 https://doi.org/10.1073/pnas.1216894110
  17. Coulon, S., Ramasubramanyan, S., Alies, C., Philippin, G., Lehmann, A. and Fuchs, R.P. (2010) Rad8Rad5/Mms2-Ubc13 ubiquitin ligase complex controls translesion synthesis in fission yeast. EMBO J., 29, 2048-2058. https://doi.org/10.1038/emboj.2010.87
  18. Fuchs, R.P. (2016) Tolerance of lesions in E. coli: Chronological competition between translesion synthesis and damage avoidance. DNA Repair (Amst.), 44, 51-58. https://doi.org/10.1016/j.dnarep.2016.05.006
  19. Goodman, M.F. (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu. Rev. Biochem., 71, 17-50. https://doi.org/10.1146/annurev.biochem.71.083101.124707
  20. Masutani, C., Kusumoto, R., Yamada, A., Dohmae, N., Yokoi, M., Yuasa, M., Araki, M., Iwai, S., Takio, K. and Hanaoka, F. (1999) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature, 399, 700-704. https://doi.org/10.1038/21447
  21. Johnson, R.E., Kondratick, C.M., Prakash, S. and Prakash, L. (1999) hRAD30 mutations in the variant form of xeroderma pigmentosum. Science, 285, 263-265. https://doi.org/10.1126/science.285.5425.263
  22. 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. https://doi.org/10.1093/emboj/19.22.6259
  23. Tang, M., Shen, X., Frank, E.G., O'Donnell, M., Woodgate, R. and Goodman, M.F. (1999) UmuD'(2)C is an error-prone DNA polymerase, Escherichia coli pol V. Proc. Natl. Acad. Sci. U.S.A., 96, 8919-8924. https://doi.org/10.1073/pnas.96.16.8919
  24. Fuchs, R.P., Fujii, S. and Wagner, J. (2004) Properties and functions of Escherichia coli: Pol IV and Pol V. Adv. Protein Chem., 69, 229-264.
  25. Kato, T. and Shinoura, Y. (1977) Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light. Mol. Gen. Genet., 156, 121-131.
  26. Steinborn, G. (1978) Uvm mutants of Escherichia coli K12 deficient in UV mutagenesis. I. Isolation of uvm mutants and their phenotypical characterization in DNA repair and mutagenesis. Mol. Gen. Genet., 165, 87-93. https://doi.org/10.1007/BF00270380
  27. Blanco, M., Herrera, G., Collado, P., Rebollo, J.E. and Botella, L.M. (1982) Influence of RecA protein on induced mutagenesis. Biochimie, 64, 633-636. https://doi.org/10.1016/S0300-9084(82)80102-8
  28. Dutreix, M., Moreau, P.L., Bailone, A., Galibert, F., Battista, J.R., Walker, G.C. and Devoret, R. (1989) New recA mutations that dissociate the various RecA protein activities in Escherichia coli provide evidence for an additional role for RecA protein in UV mutagenesis. J. Bacteriol., 171, 2415-2423. https://doi.org/10.1128/jb.171.5.2415-2423.1989
  29. Sweasy, J.B., Witkin, E.M., Sinha, N. and Roegner-Maniscalco, V. (1990) RecA protein of Escherichia coli has a third essential role in SOS mutator activity. J. Bacteriol., 172, 3030-3036. https://doi.org/10.1128/jb.172.6.3030-3036.1990
  30. Becherel, O.J., Fuchs. R.P.P. and Wagner, J. (2002) Pivotal role of the beta-clamp in translesion DNA synthesis and mutagenesis in E. coli cells. DNA Repair (Amst.), 1, 703-708. https://doi.org/10.1016/S1568-7864(02)00106-4
  31. Fujii, S., Gasser, V. and Fuchs, R.P. (2004) The biochemical requirements of DNA polymerase V-mediated translesion synthesis revisited. J. Mol. Biol., 341, 405-417. https://doi.org/10.1016/j.jmb.2004.06.017
  32. Fujii, S. and Fuchs, R.P. (2009) Biochemical basis for the essential genetic requirements of RecA and the beta-clamp in Pol V activation. Proc. Natl. Acad. Sci. U.S.A., 106, 14825-14830. https://doi.org/10.1073/pnas.0905855106
  33. Schlacher, K., Cox, M.M., Woodgate, R. and Goodman, M.F. (2006) RecA acts in trans to allow replication of damaged DNA by DNA polymerase V. Nature, 442, 883-887. https://doi.org/10.1038/nature05042
  34. Jiang, Q., Karata, K., Woodgate, R., Cox, M.M. and Goodman. M.F. (2009) The active form of DNA polymerase V is UmuD'(2)C-RecA-ATP. Nature, 460, 359-363. https://doi.org/10.1038/nature08178
  35. Fuchs, R.P. and Fujii, S. (2007) Translesion synthesis in Escherichia coli: lessons from the NarI mutation hot spot. DNA Repair (Amst.), 6,1032-1041. https://doi.org/10.1016/j.dnarep.2007.02.021
  36. Fuchs, R.P. and Fujii, S. (2013) Translesion DNA synthesis and mutagenesis in prokaryotes. Cold Spring Harb. Perspect. Biol., 5, a012682. https://doi.org/10.1101/cshperspect.a012682
  37. Fujii, S. and Fuchs, R.P. (2004) Defining the position of the switches between replicative and bypass DNA polymerases. EMBO J., 23, 4342-4352. https://doi.org/10.1038/sj.emboj.7600438
  38. Gon, S., Napolitano, R., Rocha, W., Coulon, S. and Fuchs, R.P. (2011) Increase in dNTP pool size during the DNA damage response plays a key role in spontaneous and induced-mutagenesis in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A., 108, 19311-19316. https://doi.org/10.1073/pnas.1113664108
  39. Isogawa, A., Ong, J.L., Potapov, V., Fuchs, R.P. and Fujii, S. (2018) Pol V-mediated translesion synthesis elicits localized untargeted mutagenesis during post-replicative gap repair. Cell Rep., 24, 1290-1300. https://doi.org/10.1016/j.celrep.2018.06.120
  40. 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. https://doi.org/10.1046/j.1365-2443.2003.00646.x
  41. 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. https://doi.org/10.1093/nar/gks675
  42. Veaute, X. and Fuchs, R.P. (1993) Greater susceptibility to mutations in lagging strand of DNA replication in Escherichia coli than in leading strand. Science, 261, 598-600. https://doi.org/10.1126/science.8342022
  43. Naiman, K., Philippin, G., Fuchs, R.P. and Pages, V. (2014) Chronology in lesion tolerance gives priority to genetic variability. Proc. Natl. Acad. Sci. U.S.A., 111, 5526-5531. https://doi.org/10.1073/pnas.1321008111
  44. Courcelle, J., Donaldson, J.R., Chow, K.-H. and Courcelle, C.T. (2003) DNA damage-induced replication fork regression and processing in Escherichia coli. Science, 299, 1064-1067. https://doi.org/10.1126/science.1081328
  45. Adikesavan, A.K., Katsonis, P., Marciano, D.C., Lua, R., Herman, C. and Lichtarge, O. (2011) Separation of recombination and SOS response in Escherichia coli RecA suggests LexA interaction sites. PLoS Genet., 7, e1002244. https://doi.org/10.1371/journal.pgen.1002244
  46. Naiman, K., Pages, V. and Fuchs, R.P. (2016) A defect in homologous recombination leads to increased translesion synthesis in E. coli. Nucleic Acids Res., 44, 7691-7699. https://doi.org/10.1093/nar/gkw488