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Article

The Preference for Error-Free or Error-Prone Postreplication Repair in Saccharomyces cerevisiae Exposed to Low-Dose Methyl Methanesulfonate Is Cell Cycle Dependent

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Pages 1515-1527 | Received 15 Oct 2012, Accepted 30 Jan 2013, Published online: 21 Mar 2023

REFERENCES

  • Lazzaro F, Giannattasio M, Puddu F, Granata M, Pellicioli A, Plevani P, Muzi-Falconi M. 2009. Checkpoint mechanisms at the intersection between DNA damage and repair. DNA Repair 8:1055–1067.
  • Drabløs F, Feyzi E, Aas PA, Vaagbø CB, Kavli B, Bratlie MS, Peña-Diaz J, Otterlei M, Slupphaug G, Krokan HE. 2004. Alkylation damage in DNA and RNA-repair mechanisms and medical significance. DNA Repair 3:1389–1407.
  • Lindahl T. 1993. Instability and decay of the primary structure of DNA. Nature 362:709–715.
  • Hishida T, Kubota Y, Carr AM, Iwasaki H. 2009. RAD6-RAD18-RAD5-pathway-dependent tolerance to chronic low-dose ultraviolet light. Nature 457:612–615.
  • Tercero JA, Longhese MP, Diffley JF. 2003. A central role for DNA replication forks in checkpoint activation and response. Mol. Cell 11:1323–1336.
  • Murakami-Sekimata A, Huang D, Piening BD, Bangur C, Paulovich AG. 2010. The Saccharomyces cerevisiae RAD9, RAD17 and RAD24 genes are required for suppression of mutagenic post-replicative repair during chronic DNA damage. DNA Repair 9:824–834.
  • Shulman LN. 1993. The biology of alkylating-agent cellular injury. Hematol. Oncol. Clin. North Am. 7:325–335.
  • Broomfield S, Chow BL, Xiao W. 1998. MMS2, encoding an ubiquitin-conjugating-enzyme-like protein, is a member of the yeast error-free postreplication repair pathway. Proc. Natl. Acad. Sci. U. S. A. 95:5678–5683.
  • Prakash L, Prakash S. 1977. Isolation and characterization of MMS-sensitive mutants of Saccharomyces cerevisiae. Genetics 86:33–55.
  • Prakash S, Prakash L. 1977. Increased spontaneous mitotic segregation in MMS-sensitive mutants of Saccharomyces cerevisiae. Genetics 87:229–236.
  • Tercero JA, Diffley JF. 2001. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412:553–557.
  • Andersen PL, Xu F, Xiao W. 2008. Eukaryotic DNA damage tolerance and translesion synthesis through covalent modifications of PCNA. Cell Res. 18:162–173.
  • Ulrich HD, Walden H. 2010. Ubiquitin signaling in DNA replication and repair. Nat. Rev. Mol. Cell Biol. 11:479–489.
  • Ulrich HD. 2011. Timing and spacing of ubiquitin-dependent DNA damage bypass. FEBS Lett. 585:2861–2867.
  • Nelson JR, Lawrence CW, Hinkle DC. 1996. Thymine-thymine dimer bypass by yeast DNA polymerase zeta. Science 272:1646–1649.
  • Blastyák A, Pintér L, Unk I, Prakash L, Prakash S, Haracska L. 2007. Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol. Cell 28:167–175.
  • Longtine MS, McKenzie AIII, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953–961.
  • Reid RJD, Sunjevaric I, Keddache M, Rothstein R. 2002. Efficient PCR-based gene disruption in Saccharomyces strains using intergenic primers. Yeast 19:319–328.
  • Tong AH, Boone C. 2006. Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol. Biol. 313:171–192.
  • Paulovich AG, Margulies RU, Garvik BM, Hartwell LH. 1997. RAD9, RAD17, and RAD24 are required for S phase regulation in Saccharomyces cerevisiae in response to DNA damage. Genetics 145:45–62.
  • Pellicioli A, Lucca C, Liberi G, Marini F, Lopes M, Plevani P, Romano A, Di Fiore PP, Foiani M. 1999. Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J. 18:6561–6572.
  • Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685.
  • Chang M, Bellaoui M, Boone C, Brown GW. 2002. A genome-wide screen for methyl methanesulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage. Proc. Natl. Acad. Sci. U. S. A. 99:16934–16939.
  • Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Bussey H, Chu AM, Connelly C, Davis K, Dietrich F, Dow SW, El Bakkoury M, Foury F, Friend SH, Gentalen E, Giaever G, Hegemann JH, Jones T, Laub M, Liao H, Liebundguth N, Lockhart DJ, Lucau-Danila A, Lussier M, M'Rabet N, Menard P, Mittmann M, Pai C, Rebischung C, Revuelta JL, Riles L, Roberts CJ, Ross-MacDonald P, Scherens B, Snyder M, Sookhai-Mahadeo S, Storms RK, Véronneau S, Voet M, Volckaert G, Ward TR, Wysocki R, Yen GS, Yu K, Zimmermann K, Philippsen P, Johnston M, Davis RW. 1999. Functional characterization of the Saccharomyces cerevisiae genome by gene deletion and parallel analysis. Science 285:901–906.
  • Grunenfelder B, Winzeler EA. 2002. Treasures and traps in genome-wide data sets: case examples from yeast. Nat. Rev. Genet. 3:653–661.
  • Hughes TR, Roberts CJ, Dai H, Jones AR, Meyer MR, Slade D, Burchard J, Dow S, Ward TR, Kidd MJ, Friend SH, Marton MJ. 2000. Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet. 25:333–337.
  • Barbour L, Ball LG, Zhang K, Xiao W. 2006. DNA damage checkpoints are involved in postreplication repair. Genetics 174:1789–1800.
  • Daigaku Y, Davies AA, Ulrich HD. 2010. Ubiquitin-dependent DNA damage bypass is separable from genome replication. Nature 465:951–955.
  • Barbour L, Xiao W. 2003. Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: a yeast model. Mutat. Res. 532:137–155.
  • Gangavarapu V, Prakash S, Prakash L. 2007. Requirement of RAD52 group genes for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 27:7758–7764.
  • Paulovich AG, Hartwell LH. 1995. A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82:841–847.
  • Lopes M, Foiani M, Sogo JM. 2006. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell 21:15–27.
  • Prakash L. 1981. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol. Gen. Genet. 184:471–478.
  • Geigl EM, Eckardt-Schupp F. 1991. The repair of double-strand breaks and S1 nuclease-sensitive sites can be monitored chromosome-specifically in Saccharomyces cerevisiae using pulse-field gel electrophoresis. Mol. Microbiol. 5:1615–1620.
  • Ma W, Panduri V, Sterling JF, Van Houten B, Gordenin DA, Resnick MA. 2009. The transition of closely opposed lesions to double-strand breaks during long-patch base excision repair is prevented by the coordinated action of DNA polymerase δ and Rad27/Fen1. Mol. Cell. Biol. 29:1212–1221.
  • Chu G, Vollrath D, Davis RW. 1986. Separation of large DNA molecules by contour-clamped homogeneous electric fields. Science 234:1582–1585.
  • Karras GI, Jentsch S. 2010. The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell 141:255–267.
  • Giannattasio M, Follonier C, Tourrière H, Puddu F, Lazzaro F, Pasero P, Lopes M, Plevani P, Muzi-Falconi M. 2010. Exo1 competes with repair synthesis, converts NER intermediates to long ssDNA gaps, and promotes checkpoint activation. Mol. Cell 40:50–62.
  • Pfander B, Moldovan GL, Sacher M, Hoege C, Jentsch S. 2005. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436:428–433.
  • Hishida T, Hirade Y, Haruta N, Kubota Y, Iwasaki H. 2010. Srs2 plays a critical role in reversible G2 arrest upon chronic and low doses of UV irradiation via two distinct homologous recombination-dependent mechanisms in postreplication repair-deficient cells. Mol. Cell. Biol. 30:4840–4850.
  • Liu J, Renault L, Veaute X, Fabre F, Stahlberg H, Heyer WD. 2011. Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature 479:245–248.
  • Zhang H, Lawrence CW. 2005. The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination. Proc. Natl. Acad. Sci. U. S. A. 102:15954–15959.
  • Waters LS, Walker GC. 2006. The critical mutagenic translesion DNA polymerase Rev1 is highly expressed during G(2)/M phase rather than S phase. Proc. Natl. Acad. Sci. U. S. A. 103:8971–8976.
  • Broomfield S, Hryciw T, Xiao W. 2001. DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae. Mutat. Res. 486:167–184.
  • Toczyski DP, Galgoczy DJ, Hartwell LH. 1997. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90:1097–1106.
  • Segurado M, Diffley JF. 2008. Separate roles for the DNA damage checkpoint protein kinases in stabilizing DNA replication forks. Genes Dev. 22:1816–1827.
  • Claus EB, Calvocoressi L, Bondy ML, Schildkraut JM, Wiemels JL, Wrensch M. 2012. Dental X-rays and risk of meningioma. Cancer 118:4530–4537.
  • Longstreth WTJr, Phillips LE, Drangsholt M, Koepsell TD, Custer BS, Gehrels JA, van Belle G. 2004. Dental X-rays and the risk of intracranial meningioma: a population-based case-control study. Cancer 100:1026–1034.
  • Nguyen PK, Wu JC. 2011. Radiation exposure from imaging tests: is there an increased cancer risk? Expert Rev. Cardiovasc. Ther. 9:177–183.
  • Brenner DJ. 2009. Extrapolating radiation-induced cancer risks from low doses to very low doses. Health Phys. 97:505–509.
  • Goodhead DT. 2010. New radiobiological, radiation risk and radiation protection paradigms. Mutat. Res. 687:13–16.
  • Mullenders L, Atkinson M, Paretzke H, Sabatier L, Bouffler S. 2009. Assessing cancer risks of low-dose radiation. Nat. Rev. Cancer 9:596–604.
  • Preston DL, Pierce DA, Shimizu Y, Cullings HM, Fujita S, Funamoto S, Kodama K. 2004. Effect of recent changes in atomic bomb survivor dosimetry on cancer mortality risk estimates. Radiat. Res. 162:377–389.
  • Preston DL, Ron E, Tokuoka S, Funamoto S, Nishi N, Soda M, Mabuchi K, Kodama K. 2007. Solid cancer incidence in atomic bomb survivors: 1958–1998. Radiat. Res. 168:1–64.
  • Baerlocher MO, Detsky AS. 2010. Discussing radiation risks associated with CT scans with patients. JAMA 304:2170–2171.
  • Brenner DJ, Hall EJ. 2007. Computed tomography—an increasing source of radiation exposure. N. Engl. J. Med. 357:2277–2284.

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