Skip to main content
SpringerLink
Log in

DNA Damage Tolerance in the Yeast Saccharomyces cerevisiae

  • REVIEWS AND THEORETICAL ARTICLES
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

In eukaryotes, DNA damage tolerance (DDT) can be achieved through two mechanisms. One mechanism is mediated by the homologous recombination repair proteins. The other is under control of the RAD6 epistatic group genes and is divided into two more pathways, including error-free and error-prone ones. The error-prone mechanism, termed translesion DNA synthesis (TLS), is carried out with the participation of specialized TLS DNA polymerases. TLS is an important source of mutational changes in DNA. On the contrary, upon the realization of RAD6-dependent error-free DDT mechanism, relatively higher accuracy of DNA synthesis is provided by the use of intact sister chromatid or a homologous chromosome as a template to continue replication. In this case, after the replication fork stalling at the site of damage, the 3' end of the synthesized strand is transferred to an intact homologous DNA molecule, the synthesis continues for some length on a new template, and then the elongated strand is transferred back to the original chromatid. Inactivation of most genes that control the error-free DDT mechanism either does not affect the level of UV-induced mutagenesis or decreases it. Exceptions include genes belonging to the HSM3 epistatic group. Mutations in the genes of this group lead to a considerable increase in the frequency of UV-induced mutagenesis. This review focuses on the error-free DDT pathway, and attempts to substantiate the role of the HSM3 epistatic group genes in a series of molecular events that lead to the error-free bypass of replication-blocking lesions in budding yeast are made.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Lindahl, T., Instability and decay of the primary structure of DNA, Nature, 1993, vol. 362, pp. 709—715. https://doi.org/10.1038/362709a0

    Google Scholar 

  2. Freidberg, E.C., Walker, G.C., Siede, W., et al., DNA Repair and Mutagenesis, Washington: ASM Press, 2006, 2nd ed.

    Google Scholar 

  3. Prakash, L., Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations, Mol. Gen. Genet., 1981, vol. 184, no. 3, pp. 471—478. https://doi.org/10.1007/bf00352525

    Google Scholar 

  4. Bridges, B.A. and Munson, R.J., Mutagenesis in Escherichia coli: evidence for the mechanism of base change mutation by ultraviolet radiation in a strain deficient in excision-repair, Proc. R. Soc. B, 1968, vol. 171, pp. 213—226. https://doi.org/10.1098/rspb.1968.0065

    Google Scholar 

  5. Ganesan, A.K., Persistence of pyrimidine dimers during post-replication repair in ultraviolet light-irradiated Escherichia coli K12, J. Mol. Biol., 1974, vol. 87, pp. 103—119. https://doi.org/10.1016/0022-2836(74)90563-4

    Google Scholar 

  6. Lopes, M., Foiani, M., and Sogo, J.M., Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions, Mol. Cell, 2006, vol. 21, pp. 15—27. https://doi.org/10.1016/j.molcel.2005.11.015

    Google Scholar 

  7. Daigaku, Y., Davies, A.A., and Ulrich, H.D., Ubiquitin-dependent DNA damage bypass is reparable from genome replication, Nature, 2010, vol. 465, pp. 951—955. https://doi.org/10.1038/nature09097

    Google Scholar 

  8. Karras, GI. and Jentsch, S., The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase, Cell, 2010, vol. 141, no. 2, pp. 255—267. https://doi.org/10.1016/j.cell.2010.02.028

    Google Scholar 

  9. Andersen, P., Xu, F., and Xiao, W., Eykaryotic DNA damage tolerance and translesion synthesis through covalent modifications of PCNA, Cell Res., 2008, vol. 18, pp. 162—173. https://doi.org/10.1038/cr.2007.114

    Google Scholar 

  10. Pages, V. and Fuchs, R.P., Uncoupling of leading- and lagging-strand DNA replication during lesion bypass in vivo, Science, 2003, vol. 300, pp. 1300—1303. https://doi.org/10.1126/science.1083964

    Google Scholar 

  11. Yang, K., Gong, P., Gokhale, P., and Zhuang, Z., Chemical protein polyubiquitination reveals the role of a noncanonical polyubiquin chain in DNA damage tolerance, ACS Chem. Biol., 2014, vol. 9, no. 8, pp. 1685—1691. https://doi.org/10.1021/cb500133k

    Google Scholar 

  12. Choe, K.N. and Moldovan, G.-L., Forging ahead through darkness: PCNA, still the principal conductor at the replication fork, Mol. Cell, 2017, vol. 65, no. 3, pp. 380—392. https://doi.org/10.1016/j.molcel.2016.12.020

    Google Scholar 

  13. Amara, F., Colombo, R., Cazzaniga, P., et al., In vivo and in silico analysis of PCNA ubiquitylation in the activation of the post replication repair pathway in S. cerevisiae, BMC Syst. Biol., 2013, vol. 7, no. 24. https://doi.org/10.1186/1752-0509-7-24

  14. Majka, J., Binz, S.K., Wold, M.S., and Burgers, P.M.J., Replication protein A directs loading of the DNA damage checkpoint clamp to 5'-DNA junctions, JBC, 2006, vol. 281, pp. 27855—27861. https://doi.org/10.1074/jbc.M605176200

    Google Scholar 

  15. Pardo, B., Crabbe, L., and Pasero, P., Signaling pathways of replication stressing yeast, FEMS Yeast Res., 2017, vol. 17, no. 2. https://doi.org/10.1093/femsyr/fow101

  16. Goodman, M.F. and Woodgate, R., Translesion DNA polymerases, Cold Spring Harb. Perspect. Biol., 2013, vol. 5, no. 10. https://doi.org/10.1101/cshperspect.a010363

  17. Zou, L., Liu, D., and Elledge, S.J., Replication protein A-mediated recruitment and activation of Rad17 complexes, Proc. Natl. Acad. Sci. U.S.A., 2003, vol. 100, pp. 13827—13832. https://doi.org/10.1073/pnas.2336100100

    Google Scholar 

  18. Johnson, R.E., Prakash, S., and Prakash, L., Efficient bypass of a thymine—thymine dimer by yeast DNA polymerase Polη, Science, 1999, vol. 283, pp. 1001—1004. https://doi.org/10.1126/science.283.5404.1001

    Google Scholar 

  19. Nelson, J.R., Lawrence, C.W., and Hinkle, D.C., Thymine—thymine dimer bypass by yeast DNA polymerase zeta, Science, 1996, vol. 272, pp. 1646—1649. https://doi.org/10.1126/science.272.5268.1646

    Google Scholar 

  20. Torres-Ramos, C., Prakash, S., and Prakash, L., Requirement of RAD5 and MMS2 for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae, Mol. Cell. Biol., 2002, vol. 22, pp. 2419—2426. https://doi.org/10.1128/MCB.22.7.2419-2426.2002

    Google Scholar 

  21. Gangavarapu, V., Prakash, S., and Prakash, L., Requirement of RAD52 group genes for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae, Mol. Cell. Biol., 2007, vol. 27, pp. 7758—7764. https://doi.org/10.1128/MCB.01331-07

    Google Scholar 

  22. Bailly, V., Lamb, J., Sung, P., et al., Specific complex formation between yeast RAD6 and RAD18 proteins: a potential mechanism for targeting RAD6 ubiquitin-conjugating activity to DNA damage sites, Genes Dev., 1994, vol. 8, pp. 811—820. https://doi.org/10.1101/gad.8.7.811

    Google Scholar 

  23. Broomfield, S., Hryciw, T., and Xiao, W., DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae, Mutat. Res., 2001, vol. 486, pp. 167—184. https://doi.org/10.1016/s0921-8777(01)00091-x

    Google Scholar 

  24. Bienko, M., Green, C.M., Crosetto, N., et al., Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis, Science, 2005, vol. 310, pp. 1821—1824. https://doi.org/10.1126/science.1120615

    Google Scholar 

  25. Garg, P. and Burgers, P.M., Ubiquitinated proliferating cell nuclear antigen activates translesion DNA polymerases η and REV1, Proc. Natl. Acad. Sci. U.S.A., 2005, vol. 102, pp. 18361—18366. https://doi.org/10.1073/pnas.0505949102

    Google Scholar 

  26. Biertümpfel, C., Zhao, Y., Kondo, Y., et al., Structure and mechanism of human DNA polymerase eta, Nature, 2010, vol. 465, no. 7301, pp. 1044—1048. https://doi.org/10.1038/nature09196

    Google Scholar 

  27. McDonald, J.P., Levine, A.S., and Woodgate, R., The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism, Genetics, 1997, vol. 147, pp. 1557—1568.

    Google Scholar 

  28. Stary, A., Kannouche, P., Lehmann, A.R., and Sarasin, A., Role of DNA polymerase η in the UV mutation spectrum in human cells, J. Biol. Chem., 2003, vol. 278, pp. 18767—18775. https://doi.org/10.1074/jbc.M211838200

    Google Scholar 

  29. Johnson, R.E., Kondratick, C.M., Prakash, S., and Prakash, L., hRAD30 mutations in the variant form of xeroderma pigmentosum, Science, 1999, vol. 285, pp. 263—265. https://doi.org/10.1126/science.285.5425.263

    Google Scholar 

  30. Masutani, C., Kusumoto, R., Yamada, A., et al., The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η, Nature, 1999, vol. 399, pp. 700—704. https://doi.org/10.1038/21447

    Google Scholar 

  31. Johnson, R.E., Haracska, L., Prakash, S., and Prakash, L., Role of DNA polymerase η in the bypass of a (6-4) TT photoproduct, Mol. Cell. Biol., 2001, vol. 21, pp. 3558—3563. https://doi.org/10.1128/MCB.21.10.3558-3563.2001

    Google Scholar 

  32. Johnson, R.E., Washington, M.T., Haracska, L., et al., Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions, Nature, 2000, vol. 406, pp. 1015—1019. https://doi.org/10.1038/35023030

    Google Scholar 

  33. Kuang, L., Kou, H., Xie, Z., et al., A non-catalytic function of Rev1 in translesion DNA synthesis and mutagenesis is mediated by its stable interaction with Rad5, DNA Repair, 2013, vol. 12, pp. 27—37. https://doi.org/10.1016/j.dnarep.2012.10.003

    Google Scholar 

  34. Blastyák, A., Pintér, L., Unk, I., et al., Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression, Mol. Cell, 2007, vol. 28, pp. 167—175. https://doi.org/10.1016/j.molcel.2007.07.030

    Google Scholar 

  35. Eddins, M.J., Carlile, C.M., Gomez, K.M., et al., Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation, Nat. Struct. Mol. Biol., 2006, vol. 13, pp. 915—920. https://doi.org/10.1038/nsmb1148

    Google Scholar 

  36. Hofmann, R.M. and Pickart, C.M., Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair, Cell, 1999, vol. 96, pp. 645—653. https://doi.org/10.1016/s0092-8674(00)80575-9

    Google Scholar 

  37. Van Demark, A.P., Hofmann, R.M., Tsui, C., et al., Molecular insights into polyubiquitin chain assembly: crystal structure of the Mms2/Ubc13 heterodimer, Cell, 2001, vol. 105, pp. 711—720. https://doi.org/10.1016/s0092-8674(01)00387-7

    Google Scholar 

  38. Broomfield, S., Chow, B.L., and Xiao, W., MMS2, encoding a ubiquitin-conjugating-enzyme-like protein, is a member of the yeast error-free postreplication repair pathway, Proc. Natl. Acad. Sci. U.S.A., 1998, vol. 95, pp. 5678—5683. https://doi.org/10.1073/pnas.95.10.5678

    Google Scholar 

  39. McKenna, S., Spyracopoulos, L., Moraes, T., et al., Noncovalent interaction between ubiquitin and the human DNA repair protein Mms2 is required for Ubc13-mediated polyubiquitination, J. Biol. Chem., 2001, vol. 276, pp. 40120—40126. https://doi.org/10.1074/jbc.M102858200

    Google Scholar 

  40. Moraes, T.F., Edwards, R.A., McKenna, S., et al., Crystal structure of the human ubiquitin conjugating enzyme complex, hMms2-hUbc13, Nat. Struct. Biol., 2001, vol. 8, pp. 669—673. https://doi.org/10.1038/90373

    Google Scholar 

  41. Ulrich, H.D. and Jentsch, S., Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair, EMBO J., 2000, vol. 19, pp. 3388—3397. https://doi.org/10.1093/emboj/19.13.3388

    Google Scholar 

  42. Hoege, C., Pfander, B., Moldovan, G.L., et al., RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO, Nature, 2002, vol. 419, pp. 135—141. https://doi.org/10.1038/nature00991

    Google Scholar 

  43. Ulrich, H.D., Protein—protein interactions within an E2–RING finger complex: implications for ubiquitin-dependent DNA damage repair, J. Biol. Chem., 2003, vol. 278, pp. 7051—7058. https://doi.org/10.1074/jbc.M212195200

    Google Scholar 

  44. Carlile, C.M., Pickart, C.M., Matunis, M.J., and Cohen, R.E., Synthesis of free and proliferating cell nuclear antigen-bound polyubiquitin chains by the RING E3 ubiquitin ligase Rad5, J. Biol. Chem., 2009, vol. 284, pp. 29326—29334. https://doi.org/10.1074/jbc.M109.043885

    Google Scholar 

  45. Parker, J.L. and Ulrich, H.D., Mechanistic analysis of PCNA poly-ubiquitylation by the ubiquitin protein ligases Rad18 and Rad5, EMBO J., 2009, vol. 28, pp. 3657—3666. https://doi.org/10.1038/emboj.2009.303

    Google Scholar 

  46. Zhang, W., Qin, Z., Zhang, X., and Xiao, W., Roles of sequential ubiquitination of PCNA in DNA-damage tolerance, FEBS Lett., 2011, vol. 585, pp. 2786—2794. https://doi.org/10.1016/j.febslet.2011.04.044

    Google Scholar 

  47. Trenz, K., Smith, E., Smith, S., and Costanzo, V., ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks, EMBO J., 2006, vol. 25, pp. 1764—1774. https://doi.org/10.1038/sj.emboj.7601045

    Google Scholar 

  48. Bentsen, I.B., Nielsen, I., Lisby, M., et al., MRX protects fork integrity at protein-DNA barriers, and its absence causes checkpoint activation dependent on chromatin context, Nucleic Acids Res., 2013, vol. 41, pp. 3173—3189. https://doi.org/10.1093/nar/gkt051

    Google Scholar 

  49. Hashimoto, Y., Chaudhuri, A.R., Lopez, M., and Costanzo, V., Rad51 protects nascent DNA from Mre11 dependent degradation and promotes continuous DNA synthesis, Nat. Struct. Mol. Biol., 2010, vol. 17, pp. 1305—1311. https://doi.org/10.1038/nsmb.1927

    Google Scholar 

  50. Garcia-Rodrigues, N., Wong, R.P., and Ulrich, H.D., The helicase Pif1 functions in the template switching pathway of DNA damage bypass, Nucleic Acids Res., 2018, vol. 46, no. 16. https://doi.org/10.1093/nar/gky648

  51. Liberi, G., Maffioletti, G., Lucca, C., et al., Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase, Genes Dev., 2005, vol. 19, pp. 339—350. https://doi.org/10.1101/gad.322605

    Google Scholar 

  52. Branzei, D., Sollier, J., Liberi, G., et al., Ubc9- and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks, Cell, 2006, vol. 127, pp. 509—522. https://doi.org/10.1016/j.cell.2006.08.050

    Google Scholar 

  53. Minca, E.C. and Kowalski, D., Multiple Rad5 activities mediate sister chromatid recombination to bypass DNA damage at stalled replication forks, Mol. Cell, 2010, vol. 38, pp. 649—661. https://doi.org/10.1016/j.molcel.2010.03.020

    Google Scholar 

  54. Ball, L.G., Zhang, K., Cobb, J.A., et al., The yeast Shu complex couples error-free post-replication repair to homologous recombination, Mol. Microbiol., 2009, vol. 73, pp. 89—102. https://doi.org/10.1111/j.1365-2958.2009.06748.x

    Google Scholar 

  55. Gonzalez-Huici, V., Szakal, B., Urulangodi, M., et al., DNA bending facilitates the error-free DNA damage tolerance pathway and upholds genome integrity, EMBO J., 2014, vol. 33, pp. 327—340. https://doi.org/10.1002/embj.201387425

    Google Scholar 

  56. Kamau, E., Bauerle, K.T., and Grove, A., The Saccharomyces cerevisiae high mobility group box protein HMO1 contains two functional DNA binding domains, J. Biol. Chem., 2004, vol. 279, pp. 55234—55240. https://doi.org/10.1074/jbc.M409459200

    Google Scholar 

  57. Shor, E., Weinstein, J., and Rothstein, R., A genetic screen for top3 suppressors in Saccharomyces cerevisiae identifies SHU1SHU2PSY3 and CSM2: four genes involved in error-free DNA repair, Genetics, 2005, vol. 169, pp. 1275—1289. https://doi.org/10.1534/genetics.104.036764

    Google Scholar 

  58. Mankouri, H.W., Ngo, H.P., and Hickson, I.D., Shu proteins promote the formation of homologous recombination intermediates that are processed by Sgs1–Rmi1–Top3, Mol. Biol. Cell, 2007, vol. 18, pp. 4062—4073. https://doi.org/10.1091/mbc.e07-05-0490

    Google Scholar 

  59. Xu, X., Ball, L., Chen, W., et al., The yeast Shu complex utilizes homologous recombination machinery for error-free lesion bypass via physical interaction with a Rad51 paralogue, PLoS One, 2013, vol. 8, no. 12. https://doi.org/10.1371/journal.pone.0081371

  60. Godin, S., Wier, A., Kabbinavar, F., et al., The Shu complex interacts with Rad51 through the Rad51 paralogues Rad55—Rad57 to mediate error-free recombination, Nucleic Acids Res., 2013, vol. 41, pp. 4525–4534. https://doi.org/10.1093/nar/gkt138

    Google Scholar 

  61. Scheller, J., Schurer, A., Rudolph, C., et al., MPH1, a yeast gene encoding a DEAH protein, plays a role in protection of the genome from spontaneous and chemically induced damage, Genetics, 2000, vol. 155, pp. 1069—1081.

    Google Scholar 

  62. Prakash, R., Krejci, L., Van Komen, S., et al., Saccharomyces cerevisiae MPH1 gene, required for homologous recombination-mediated mutation avoidance, encodes a 3' to 5' DNA helicase, J. Biol. Chem., 2005, vol. 280, no. 9, pp. 7854—7860. https://doi.org/10.1074/jbc.M413898200

    Google Scholar 

  63. Prakash, R., Satory, D., Dray, E., et al., Yeast Mph1 helicase dissociates Rad-51made D-loop: implications for crossingover control in mitotic recombination, Genes Dev., 2009, vol. 23, pp. 67—79. https://doi.org/10.1101/gad.1737809

    Google Scholar 

  64. Ivanov, E.L., Kovaltzova, S.V., and Korolev, V.G., Saccharomyces cerevisiae mutants with enhanced induced mutation and altered mitotic gene conversion, Mutat. Res., 1989, vol. 213, pp. 105—115. https://doi.org/10.1016/0027-5107(89)90141-3

    Google Scholar 

  65. Blackwell, Jr., Wilkinson, S.T., Mosammaparast, N., and Pemberton, L.F., Mutational analysis of H3 and H4 N termini reveals distinct roles in nuclear import, J. Biol. Chem., 2007, vol. 282, pp. 20142—20150.

    Google Scholar 

  66. Ivanov, E.L., Fedorova, I.V., and Kovaltsova, S.V., Isolation and characterization of new Saccharomyces cerevisiae mutants with increased spontaneous mutability, Genetica (Moscow), 1992, vol. 28, no. 1, pp. 47—55.

    Google Scholar 

  67. Fedorova, I.V., and Kovaltsova, S.V., and Ivanov, E.L., Effect of hms mutations increasing spontaneous mutability on induced mutagenesis and mitotic recombination in the yeast Saccharomyces cerevisiae, Genetica (Moscow), 1992, vol. 28, no. 1, pp. 54—65.

    Google Scholar 

  68. Alekseev, S.Yu., Kovaltzova, S.V., Fedorova, I.V., et al., HSM2 (HMO1) gene participates in mutagenesis control in yeast Saccharomyces cerevisiae, DNA Repair, 2002, vol. 1, pp. 287—297.

    Google Scholar 

  69. Kelberg, E.P., Kovaltsova, S.V., Alekseev, S.Y., et al., HIM1, a new yeast Saccharomyces cerevisiae gene playing a role in control of spontaneous and induced mutagenesis, Mutat. Res., 2005, vol. 578, pp. 64—78. https://doi.org/10.1016/j.mrfmmm.2005.03.003

    Google Scholar 

  70. Gracheva, L.M, Evstyukhina, T.A., Kovaltsova, S.V., et al., Mutator genes of the Saccharomyces cerevisiae yeast: I. Repair of artificial heteroduplexes in mutants him and hsm, Genetica (Moscow), 1996, vol. 32, no. 7, pp. 801—804.

    Google Scholar 

  71. Fedorova, I.V., Gracheva, L.M., Kovaltzova, S.V., et al., The yeast HSM3 gene acts in one of the mismatch repair pathways, Genetics, 1998, vol. 148, pp. 963—973.

    Google Scholar 

  72. Inbar, O., Liefshitz, B., Bitan, G., and Kupiec, M., The relationship between homology length and crossing over during the repair of a broken chromosome, J. Biol. Chem., 2000, vol. 275, pp. 30833—30838. https://doi.org/10.1074/jbc.C000133200

    Google Scholar 

  73. Ge, Z., Wang, H., and Parthun, M.R., Nuclear Hat1p complex (NuB4) components participate in DNA repair-linked chromatin reassembly, J. Biol. Chem., 2011, vol. 286, pp. 16790—16799.

    Google Scholar 

  74. Le Tallec, B., Barrault, M.-B., Guerois, R., et al., Hsm3/S5b participates in the assembly pathway of the 19S regulatory particle of the proteasome, Mol. Cell, 2009, vol. 33, pp. 389—399.

    Google Scholar 

  75. Funakoshi, M., Tomko, R.J., Jr., Kobayashi, H., and Hochstrasser, M., Multiple assembly chaperones govern biogenesis of the proteasome regulatory particle base, Cell, 2009, vol. 137, pp. 887—899.

    Google Scholar 

  76. Chernenkov, A.Y., Ivanova, S.V., Kovaltzova, S.V., et al., Genetic analysis of the Hsm3 protein domain structure in yeast Saccharomyces cerevisiae, Russ. J. Genet., 2010, vol. 46, no. 6, pp. 652—658. https://doi.org/10.1134/S1022795410060037

    Google Scholar 

  77. Gadal, C., Labarre, S., Djschiero, C., and Thuriaux, P., Hmo1, an HMG-box protein, belongs to the yeast ribosomal DNA transcription system, EMBO J., 2002, vol. 21, pp. 5498—5507.

    Google Scholar 

  78. Chernenkov, A.Yu., Fedorov, D.V., Gracheva, L.M., et al., Interactions of the HSM gene with genes initiating homologous recombination repair in yeast Saccharomyces cerevisiae, Russ. J. Genet., 2012, vol. 48, no. 3, pp. 284—290. https://doi.org/10.1134/S1022795412020056

    Google Scholar 

  79. Fedorov, D.V., Kovaltsova, S.V., Evstuhina, T.A., et al., HSM6 gene is identical to PSY4 gene in Saccharomyces cerevisiae yeasts, Russ. J. Genet., 2013, vol. 49, no. 3, pp. 286—293. https://doi.org/10.1134/S1022795413020063

    Google Scholar 

  80. Alekseeva, E.A., Evstyukhina, T.A., Peshekhonov, V.T., and Korolev, V.G., Interaction of the Saccharomyces cerevisiae yeast HIM1 gene product with Srs2 (RadH) and Mph1 helicases, Tsitilogiya, 2018, vol. 60, no. 7, pp. 555—557. https://doi.org/10.31116/tsitol.2018.07.13

    Google Scholar 

  81. Xiao, L., Williams, A.M., and Grove, A., The C-terminal domain of yeast high mobility group protein HMO1 mediates lateral protein accretion and in-phase DNA bending, Biochemistry, 2010, vol. 49, pp. 4051—4059. https://doi.org/10.1021/bi1003603

    Google Scholar 

  82. Bernstein, K.A., Reid, R.J.D., Sunjevaric, I., et al., The Shu complex, which contains Rad51 paralogues, promotes DNA repair through inhibition of the Srs2 anti-recombinase, Mol. Biol. Cell, 2011, vol. 22, pp. 1599—1607.

    Google Scholar 

  83. Kovaltsova, S.V., Gracheva, L.M., Evstyukhina, T.A., et al., Mutator genes of the Saccharomyces cerevisiae yeast: II. Interaction between the genes him and hsm, Genetica (Moscow), 1996, vol. 32, no. 7, pp. 805—810.

    Google Scholar 

  84. Stafa, A., Donnianni, R.A., Timashev, L.A., et al., Template switching during break-induced replication is promoted by the Mph1 helicase in Saccharomyces cerevisiae, Genetics, 2014, vol. 196, pp. 1017—1028. https://doi.org/10.1534/genetics.114.162297

    Google Scholar 

  85. Zheng, X.-F., Prakash, R., Saro, D., et al., Processing of DNA structures via DNA unwinding and branch migration by the S. cerevisiae Mph1 protein, DNA Repair (Amsterdam), 2011, vol. 10, no. 10, pp. 1034—1043. https://doi.org/10.1016/j.dnarep.2011.08.002

    Google Scholar 

  86. Dohrmann, P.R. and Sclafani, R.A., Novel role for checkpoint Rad53 protein kinase in the initiation of chromosomal DNA replication in Saccharomyces cerevisiae, J. Genet. Soc. Am., 2006, no. 174, pp. 87—99. https://doi.org/10.1534/genetics.106.060236

  87. Chabes, A., Georgieva, B., Domkin, V., et al., Survival of DNA damage in yeast directly depends on increased dNTP levels allowed by relaxed feedback inhibition of ribonucleotide reductase, Cell, 2003, vol. 112, pp. 391—401. https://doi.org/10.1016/s0092-8674(03)00075-8

Download references

Funding

This study was supported by the Russian Foundation for Basic Research (grant no. 18-34-00540 mol_a) and the Genome Research Center development program “Kurchatov Genome Center–PNPI” (Agreement no. 075-15-2019-1663).

Author information

Authors and Affiliations

  1. Konstantinov Petersburg Nuclear Physics Institute, National Research Center Kurchatov Institute, 188300, Gatchina, Leningrad oblast, Russia

    E. A. Alekseeva & V. G. Korolev

Authors
  1. E. A. Alekseeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. G. Korolev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. A. Alekseeva.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by N. Maleeva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alekseeva, E.A., Korolev, V.G. DNA Damage Tolerance in the Yeast Saccharomyces cerevisiae . Russ J Genet 57, 379–389 (2021). https://doi.org/10.1134/S1022795421040025

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795421040025

Keywords:

Search

Navigation