Current Genetics

, Volume 46, Issue 6, pp 317–330 | Cite as

How heterologously expressed Escherichia coli genes contribute to understanding DNA repair processes in Saccharomyces cerevisiae

  • Jela BrozmanováEmail author
  • Viera Vlčková
  • Miroslav Chovanec
Review Article


DNA-damaging agents constantly challenge cellular DNA; and efficient DNA repair is therefore essential to maintain genome stability and cell viability. Several DNA repair mechanisms have evolved and these have been shown to be highly conserved from bacteria to man. DNA repair studies were originally initiated in very simple organisms such as Escherichia coli and Saccharomyces cerevisiae, bacteria being the best understood organism to date. As a consequence, bacterial DNA repair genes encoding proteins with well characterized functions have been transferred into higher organisms in order to increase repair capacity, or to complement repair defects, in heterologous cells. While indicating the contribution of these repair functions to protection against the genotoxic effects of DNA-damaging agents, heterologous expression studies also highlighted the role of the DNA lesions that are substrates for such processes. In addition, bacterial DNA repair-like functions could be identified in higher organisms using this approach. We heterologously expressed three well characterized E. coli repair genes in S. cerevisiae cells of different genetic backgrounds: (1) the ada gene encoding O6-methylguanine DNA-methyltransferase, a protein involved in the repair of alkylation damage to DNA, (2) the recA gene encoding the main recombinase in E. coli and (3) the nth gene, the product of which (endonuclease III) is responsible for the repair of oxidative base damage. Here, we summarize our results and indicate the possible implications they have for a better understanding of particular DNA repair processes in S. cerevisiae.


DNA repair Heterologous expression Saccharomyces cerevisiae Escherichia coli 



The authors thank Dr. G.P. Margison and Dr. Z. Dudášová for critical reading of the manuscript. Work in the authors’ laboratory is supported by the VEGA Grant Agency of the Slovak Republic (grants 2/3091/23, 1/0043/03) and by project 2003 SP 51 028 08 00/028 08 01 in the national program Use of Cancer Genomics to Improve the Human Population Health.


  1. Aas PA, Otterlei M, Falnes PO, Vagbo CB, Skorpen F, Akbari M, Sundheim O, Bjørås M, Slupphaug G, Seeberg E, Krokan HE (2003) Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421:859–863CrossRefPubMedGoogle Scholar
  2. Aboussekhra A, Chanet R, Adjiri A, Fabre F (1992) Semidominant suppressors of Srs2 helicase mutations of Saccharomyces cerevisiae map in the RAD51 gene, whose sequence predicts a protein with similarities to procaryotic RecA proteins. Mol Cell Biol 12:3224–3234PubMedGoogle Scholar
  3. Alseth I, Eide L, Pirovano M, Rognes T, Seeberg E, Bjørås M (1999) The Saccharomyces cerevisiae homologues of endonuclease III from Escherichia coli, Ntg1 and Ntg2, are both required for efficient repair of spontaneous and induced oxidative DNA damage in yeast. Mol Cell Biol 19:3779–3787PubMedGoogle Scholar
  4. Asahara H, Wistort PM, Bank JF, Bakerian RH, Cunningham RP (1989) Purification and characterization of Escherichia coli endonuclease III from the cloned nth gene. Biochemistry 28:4444–4449PubMedGoogle Scholar
  5. Augeri L, Lee YM, Barton AB, Doetsch PW (1997) Purification, characterization, gene cloning, and expression of Saccharomyces cerevisiae redoxyendonuclease, a homolog of Escherichia coli endonuclease III. Biochemistry 36:721–729CrossRefPubMedGoogle Scholar
  6. Aylon Y, Kupiec M (2004) New insights into the mechanism of homologous recombination in yeast. Mutat Res 566:231–248PubMedGoogle Scholar
  7. Bailly V, Verly WG (1987) Escherichia coli endonuclease III is not an endonuclease but a beta-elimination catalyst. Biochem J 242:565–572PubMedGoogle Scholar
  8. Basile G, Aker M, Mortimer RK (1992) Nucleotide sequence and transcriptional regulation of the yeast recombinational repair gene RAD51. Mol Cell Biol 12:3235–3246PubMedGoogle Scholar
  9. Baumann P, West SC (1998) Role of the human RAD51 protein in homologous recombination and double-stranded-break repair. Trends Biochem Sci 23:247–251CrossRefPubMedGoogle Scholar
  10. Beranek DT, Weis CC, Swenson DH (1980) A comprehensive quantitative analysis of methylated and ethylated DNA using high pressure liquid chromatography. Carcinogenesis 1:595–606PubMedGoogle Scholar
  11. Bi B, Rybalchenko N, Golub EI, Radding CM (2004) Human and yeast Rad52 proteins promote DNA strand exchange. Proc Natl Acad Sci USA 101:9568–9572CrossRefPubMedGoogle Scholar
  12. Bianco PR, Tracy RB, Kowalczykowski SC (1998) DNA strand exchange proteins: a biochemical and physical comparison. Front Biosci 3:D570–D603PubMedGoogle Scholar
  13. Boiteux S (1993) Properties and biological functions of the NTH and FPG proteins of Escherichia coli: two DNA glycosylases that repair oxidative damage in DNA. J Photochem Photobiol B 19:87–96CrossRefPubMedGoogle Scholar
  14. Breimer LH, Lindahl T (1984) DNA glycosylase activities for thymine residues damaged by ring saturation, fragmentation, or ring contraction are functions of endonuclease III in Escherichia coli. J Biol Chem 259:5543–5548PubMedGoogle Scholar
  15. Brendel M, Grey M, Maris AF, Hietkamp J, Fesus Z, Pich CT, Dafre AL, Schmidt M, Eckardt-Schupp F, Henriques JA (1998) Low glutathione pools in the original pso3 mutant of Saccharomyces cerevisiae are responsible for its pleiotropic sensitivity phenotype. Curr Genet 33:4–9CrossRefPubMedGoogle Scholar
  16. Brendel M, Henriques JA (2001) The pso mutants of Saccharomyces cerevisiae comprise two groups: one deficient in DNA repair and another with altered mutagen metabolism. Mutat Res 489:79–96PubMedGoogle Scholar
  17. Brendel M, Bonatto D, Strauss M, Revers LF, Pungartnik C, Saffi J, Henriques JA (2003) Role of PSO genes in repair of DNA damage of Saccharomyces cerevisiae. Mutat Res 544:179–193PubMedGoogle Scholar
  18. Brennand J, Margison GP (1986) Reduction of the toxicity and mutagenicity of alkyklation agents in mammalian cells harbouring the E. coli alkyltransferase gene. Proc Natl Acad Sci USA 83:6292–6296PubMedGoogle Scholar
  19. Brozmanová J, Kleibl K, Vlčková V, Škorvaga M, Černáková L, Margison GP (1990) Expression of the E. coli ada gene in yeast protects against the toxic and mutagenic effects of N-methyl-N′-nitro-N-nitrosoguanidine. Nucleic Acids Res 18:331–335PubMedGoogle Scholar
  20. Brozmanová J, Černáková L, Vlčková V, Duraj J, Fridrichová I (1991) The Escherichia coli recA gene increases resistance of the yeast Saccharomyces cerevisiae to ionizing and ultraviolet radiation. Mol Gen Genet 227:473–480CrossRefPubMedGoogle Scholar
  21. Brozmanová J, Vlčková V, Chovanec M, Černáková L, Škorvaga M, Margison GP (1994) Expression of the E. coli ada gene in S. cerevisiae provides cellular resistance to N-methyl-N′-nitro-N-nitrosoguanidine in rad6 but not in rad52 mutants. Nucleic Acids Res 22:5717–5722PubMedGoogle Scholar
  22. Brozmanová J, Dudáš A, Henriques JA (2001a) Repair of oxidative DNA damage—an important factor reducing cancer risk. Neoplasma 48:85–93PubMedGoogle Scholar
  23. Brozmanová J, Vlčková V, Farkašová E, Dudáš A, Vlasáková D, Chovanec M, Mikulovská Ž, Fridrichová I, Saffi J, Henriques JA (2001b) Increased DNA double strand breakage is responsible for sensitivity of the pso3-1 mutant of Saccharomyces cerevisiae to hydrogen peroxide. Mutat Res 485:345–355PubMedGoogle Scholar
  24. Bruner SD, Nash HM, Lane WS, Verdine GL (1998) Repair of oxidatively damaged guanine in Saccharomyces cerevisiae by an alternative pathway. Curr Biol 8:393–403CrossRefPubMedGoogle Scholar
  25. Burgess S, Jaruga P, Dodson ML, Dizdaroglu M, Lloyd RS (2002) Determination of active site residues in Escherichia coli endonuclease VIII. J Biol Chem 277:2938–2944CrossRefPubMedGoogle Scholar
  26. Camerini-Otero RD, Hsieh P (1995) Homologous recombination proteins in prokaryotes and eukaryotes. Annu Rev Genet 29:509–552CrossRefPubMedGoogle Scholar
  27. Chenevert JA, Naumovski L, Schultz RA, Friedberg EC (1986) Partial complementation of the UV sensitivity of E. coli and yeast excision repair mutants by the cloned denV gene of bacteriophage T4. Mol Gen Genet 203:163–171PubMedGoogle Scholar
  28. Cheng SC, Tarn WY, Tsao TY, Abelson J (1993) PRP19: a novel spliceosomal component. Mol Cell Biol 13:1876–1882PubMedGoogle Scholar
  29. Clark AJ, Margulies AD (1965) Isolation and characterization of recombination-deficient mutants of Escherichia coli K12. Proc Natl Acad Sci USA 53:451–459PubMedGoogle Scholar
  30. Clarke ND, Kvaal M, Seeberg E (1984) Cloning of Escherichia coli genes encoding 3-methyladenine DNA glycosylases I and II. Mol Gen Genet 197:368–372PubMedGoogle Scholar
  31. Cooper AJ, Waters R (1987) A complex pattern of sensitivity to simple monofunctional alkylating agents exists amongst the rad mutants of Saccharomyces cerevisiae. Mol Gen Genet 209:142–148PubMedGoogle Scholar
  32. Cunningham RP, Weiss B (1985) Endonuclease III (nth) mutants of Escherichia coli. Proc Natl Acad Sci USA 82:474–478PubMedGoogle Scholar
  33. Cunningham RP, Asahara H, Bank JF, Scholes CP, Salerno JC, Surerus K, Munck E, McCracken J, Peisach J, Emptage MH (1989) Endonuclease III is an iron–sulfur protein. Biochemistry 28:4450–4455PubMedGoogle Scholar
  34. Cunningham RP, Ahern H, Xing D, Thayer MM, Tainer JA (1994) Structure and function of Escherichia coli endonuclease III. Ann NY Acad Sci 726:215–222PubMedGoogle Scholar
  35. Černáková L, Fridrichová I, Piršel M, Kleibl K, Duraj J, Brozmanová J (1991) Expression of the Escherichia coli recA gene in the yeast Saccharomyces cerevisiae. Biochimie 73:285–288CrossRefPubMedGoogle Scholar
  36. de Andrade HH, Marques EK, Schenberg AC, Henriques JA (1989) The PSO4 gene is responsible for an error-prone recombinational DNA repair pathway in Saccharomyces cerevisiae. Mol Gen Genet 217:419–426PubMedGoogle Scholar
  37. Demple B, Linn S (1980) DNA N-glycosylases and UV repair. Nature 287:203–208PubMedGoogle Scholar
  38. Demple B, Harrison L (1994) Repair of oxidative damage to DNA: enzymology and biology. Annu Rev Biochem 63:915–948CrossRefPubMedGoogle Scholar
  39. Dizdaroglu M (2003) Substrate specificities and excision kinetics of DNA glycosylases involved in base-excision repair of oxidative DNA damage. Mutat Res 531:109–126PubMedGoogle Scholar
  40. Doetsch PW, Morey NJ, Swanson RL, Jinks-Robertson S (2001) Yeast base excision repair: interconnections and networks. Prog Nucleic Acid Res Mol Biol 68:29–39PubMedGoogle Scholar
  41. Dudáš A, Marková E, Vlasáková D, Kolman A, Bartošová Z, Brozmanová J, Chovanec M (2003) The Escherichia coli RecA protein complements recombination defective phenotype of the Saccharomyces cerevisiae rad52 mutant cells. Yeast 20:389–396CrossRefPubMedGoogle Scholar
  42. Dudáš A, Chovanec M (2004) DNA double-strand break repair by homologous recombination. Mutat Res 566:131–167PubMedGoogle Scholar
  43. Eide L, Bjørås M, Pirovano M, Alseth I, Berdal KG, Seeberg E (1996) Base excision of oxidative purine and pyrimidine DNA damage in Saccharomyces cerevisiae by a DNA glycosylase with sequence similarity to endonuclease III from Escherichia coli. Proc Natl Acad Sci USA 93:10735–10740CrossRefPubMedGoogle Scholar
  44. Erdemir T, Bilican B, Oncel D, Goding CR, Yavuzer U (2002) DNA damage-dependent interaction of the nuclear matrix protein C1D with Translin-associated factor X (TRAX). J Cell Sci 115:207–216PubMedGoogle Scholar
  45. Falnes PO, Johansen RF, Seeberg E (2002) AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 419:178–182CrossRefPubMedGoogle Scholar
  46. Farkašová E, Chovanec M, Vlasáková D, Vlčková V, Margison GP, Brozmanová J (2000) Effect of stable integration of the Escherichia coli ada gene on the sensitivity of Saccharomyces cerevisiae to the toxic and mutagenic effects of alkylating agents. Environ Mol Mutagen 35:66–69CrossRefPubMedGoogle Scholar
  47. Fridrichová I, Kovařík A, Rosskopfová O (1992) Immunological quantification of RecA protein in cell extracts of E. coli after exposure to chemical mutagens or UV radiation. Folia Microbiol 37:24–30Google Scholar
  48. Friedberg EC (1988) Deoxyribonucleic acid repair in the yeast Saccharomyces cerevisiae. Microbiol Rev 52:70–102PubMedGoogle Scholar
  49. Friedberg EC (1991) Eukaryotic DNA repair: glimpses through the yeast Saccharomyces cerevisiae. Bioessays 13:91–95Google Scholar
  50. Friedberg EC, Siede W, Cooper AJ (1992) Cellular responses to DNA damage in yeast. In: Broach JR (ed) The molecular and cellular biology of the yeast Saccharomyces: genome dynamics, protein synthesis, and energetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., pp 147–192Google Scholar
  51. Friedberg EC (2000) Biological responses to DNA damage: a perspective in the new millennium. Cold Spring Harb Symp Quant Biol 65:593–602PubMedGoogle Scholar
  52. Game JC (2000) The Saccharomyces repair genes at the end of the century. Mutat Res 451:277–293PubMedGoogle Scholar
  53. Girard PM, Boiteux S (1997) Repair of oxidized DNA bases in the yeast Saccharomyces cerevisiae. Biochimie 79:559–566CrossRefPubMedGoogle Scholar
  54. Gossett J, Lee K, Cunningham RP, Doetsch PW (1988) Yeast redoxyendonuclease, a DNA repair enzyme similar to Escherichia coli endonuclease III. Biochemistry 27:2629–2634PubMedGoogle Scholar
  55. Goth-Goldstein R, Johnson PL (1990) Repair of alkylation damage in Saccharomyces cerevisiae. Mol Gen Genet 221:353–357CrossRefPubMedGoogle Scholar
  56. Gotzmann J, Gerner C, Meissner M, Holzmann K, Grimm R, Mikulitz W, Sauermann G (2000) hNMP 200: a novel human common nuclear matrix protein combining structural and regulatory functions. Exp Cell Res 261:166–179CrossRefPubMedGoogle Scholar
  57. Grey M, Dusterhoft A, Henriques JA, Brendel M (1996) Allelism of PSO4 and PRP19 links pre-mRNA processing with recombination and error-prone DNA repair in Saccharomyces cerevisiae. Nucleic Acids Res 24:4009–4014CrossRefPubMedGoogle Scholar
  58. Gros L, Saparbaev MK, Laval J (2002) Enzymology of the repair of free radicals-induced DNA damage. Oncogene 21:8905–8925CrossRefPubMedGoogle Scholar
  59. Harrison L, Škorvaga M, Cunningham RP, Hendry JH, Margison GP (1992) Transfection of the Escherichia coli nth gene into radiosensitive Chinese hamster cells: effects on sensitivity to radiation, hydrogen peroxide and bleomycine sulfate. Radiat Res 132: 30–39PubMedGoogle Scholar
  60. Hays SL, Firmenich AA, Berg P (1995) Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins. Proc Natl Acad Sci USA 92:6925–6929PubMedGoogle Scholar
  61. Henriques JA, Vicente EJ, Leandro da Silva KV, Schenberg AC (1989) PSO4: a novel gene involved in error-prone repair in Saccharomyces cerevisiae. Mutat Res 218:111–124PubMedGoogle Scholar
  62. Henriques JA, Brendel M (1990) The role of PSO and SNM genes in DNA repair of the yeast Saccharomyces cerevisiae. Curr Genet 18:387–393PubMedGoogle Scholar
  63. Henriques JA, Brozmanová J, Brendel M (1997) Role of PSO genes in the repair of photoinduced interstrand cross-links and photooxidative damage in the DNA of the yeast Saccharomyces cerevisiae. J Photochem Photobiol B 39:185–196CrossRefPubMedGoogle Scholar
  64. Hoeijmakers JH (2001) Genome maintenance mechanisms for preventing cancer. Nature 411:366–374CrossRefGoogle Scholar
  65. Jazayeri A, Jackson SP (2002) Screening the yeast genome for new DNA-repair genes. Genome Biol 3:1009CrossRefGoogle Scholar
  66. Jiang D, Hatahet Z, Melamede RJ, Kow YW, Wallace SS (1997) Characterization of Escherichia coli endonuclease VIII. J Biol Chem 272:32230–32239CrossRefPubMedGoogle Scholar
  67. Jimenez-Sanchez A, Cerda-Olmedo E (1975) Mutation and DNA replication in Escherichia coli treated with low concentrations of N-methyl-N′-nitro-N-nitrosoguanidine. Mutat Res 28:337–345PubMedGoogle Scholar
  68. Karlin S, Brocchieri L (1996) Evolutionary conservation of recA genes in relation to protein structure and function. J Bacteriol 178:1881–1894PubMedGoogle Scholar
  69. Kat A, Thilly WG, Fang WH, Longley MJ, Li GM, Modrich P (1993) An alkylation-tolerant, mutator human cell line is deficient in strand-specific mismatch repair. Proc Natl Acad Sci USA 90:6424–6428PubMedGoogle Scholar
  70. Katcher HL, Wallace SS (1983) Characterization of the Escherichia coli X-ray endonuclease, endonuclease III. Biochemistry 22:4071–4081PubMedGoogle Scholar
  71. Kido M, Yoneda Y, Nakanishi M, Uchida T, Okada Y (1992) Escherichia coli RecA protein modified with a nuclear location signal binds to chromosomes in living mammalian cells. Exp Cell Res 198:107–114PubMedGoogle Scholar
  72. Kleibl K (2002) Molecular mechanisms of adaptive response to alkylating agents in Escherichia coli and some remarks on O6 -methylguanine DNA-methyltransferase in other organisms. Mutat Res 512:67–84PubMedGoogle Scholar
  73. Kow YW, Wallace SS (1987) Mechanism of action of Escherichia coli endonuclease III. Biochemistry 26:8200–8206PubMedGoogle Scholar
  74. Kowalczykowski SC, Dixon DA, Eggleston AK, Lauder SD, Rehrauer WM (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev 58:401–465PubMedGoogle Scholar
  75. Krejči L, Damborsky J, Thomsen B, Duno M, Bendixen C (2001) Molecular dissection of interactions between Rad51 and members of the recombination-repair group. Mol Cell Biol 21:966–976CrossRefPubMedGoogle Scholar
  76. Langeveld SA, Yasui A, Eker APM (1985) Expression of an Escherichia coli phr gene in the yeast Saccharomyces cerevisiae. Mol Gen Genet 199: 396–400PubMedGoogle Scholar
  77. Lindahl T, Sedgwick B, Sekiguchi M, Nakabeppu Y (1988) Regulation and expression of the adaptive response to alkylating agents. Annu Rev Biochem 57:133–157CrossRefPubMedGoogle Scholar
  78. Little JW, Edmiston SH, Pacelli LZ, Mount DW (1980) Cleavage of the Escherichia coli LexA protein by the RecA protease. Proc Natl Acad Sci USA 77:3225–3229PubMedGoogle Scholar
  79. Maga JA, McEntee K (1985) Response of S. cerevisiae to N-methyl-N′-nitro-N-nitrosoguanidine: mutagenesis, survival and DDR gene expression. Mol Gen Genet 200:313–321PubMedGoogle Scholar
  80. Mahajan KN, Mitchell BS (2003) Role of human Pso4 in mammalian DNA repair and association with terminal deoxynucleotidyl transferase. Proc Natl Acad Sci USA 100:10746–10751CrossRefPubMedGoogle Scholar
  81. Melamede RJ, Hatahet Z, Kow YW, Ide H, Wallace SS (1994) Isolation and characterization of endonuclease VIII from Escherichia coli. Biochemistry 33:1255–1264PubMedGoogle Scholar
  82. Memisoglu A, Samson L (1996) DNA repair functions in heterologous cells. Crit Rev Biochem Mol Biol 31:405–447PubMedGoogle Scholar
  83. Memisoglu A, Samson L (2000) Base excision repair in yeast and mammals. Mutat Res 451:39–51PubMedGoogle Scholar
  84. Morais MA, Brozmanová J, Benfato MS, Duraj J, Vlčková V, Henriques JA (1994) The E. coli recA gene can restore the defect in mutagenesis of the pso4-1 mutant of S. cerevisiae. Mutat Res 314:209–220PubMedGoogle Scholar
  85. Morais MA, Vicente EJ, Brozmanová J, Schenberg AC, Henriques JA (1996) Further characterization of the yeast pso4-1 mutant: interaction with rad51 and rad52 mutants after photoinduced psoralen lesions. Curr Genet 29:211–218CrossRefPubMedGoogle Scholar
  86. Morais MA, Vlčková V, Fridrichová I, Slaninová M, Brozmanová J (1998) Effect of bacterial recA expression on DNA repair in the rad51 and rad52 mutants of Saccharomyces cerevisiae. Genet Mol Biol 21:3–9Google Scholar
  87. Ogawa T, Wabiko H, Tsurimoto T, Horii T, Masukata H, Ogawa H (1979) Characteristics of purified RecA protein and the regulation of its synthesis in vivo. Cold Spring Harb Symp Quant Biol 43:909–915PubMedGoogle Scholar
  88. Polakowska R, Perozzi G, Prakash L (1986) Alkylation mutagenesis in Saccharomyces cerevisiae: lack of evidence for an adaptive response. Curr Genet 10:647–655PubMedGoogle Scholar
  89. Potter PM, Wilkinson MC, Fitton J, Carr FJ, Brennand J, Cooper DP, Margison GP (1987) Characterisation and nucleotide sequence of ogt, the O6 -alkylguanine-DNA-alkyltransferase gene of E. coli. Nucleic Acids Res 15:9177–9193PubMedGoogle Scholar
  90. Radman M (1976) An endonuclease from Escherichia coli that introduces single polynucleotide chain scissions in ultraviolet-irradiated DNA. J Biol Chem 251:1438–1445PubMedGoogle Scholar
  91. Reiss B, Klemm M, Kosak H, Schell J (1996) RecA protein stimulates homologous recombination in plants. Proc Natl Acad Sci USA 93:3094–3098CrossRefPubMedGoogle Scholar
  92. Reiss B, Kosak H, Klemm M, Schell J (1997) Targeting of a functional Escherichia coli RecA protein to the nucleus of plant cells. Mol Gen Genet 253:695–702CrossRefPubMedGoogle Scholar
  93. Reiss B, Schubert I, Kopchen K, Wendeler E, Schell J, Puchta H (2000) RecA stimulates sister chromatid exchange and the fidelity of double-strand break repair, but not gene targeting, in plants transformed by Agrobacterium. Proc Natl Acad Sci USA 97:3358–3363CrossRefPubMedGoogle Scholar
  94. Resnick MA, Cox BS (2000) Yeast as an honorary mammal. Mutat Res 451:1–11PubMedGoogle Scholar
  95. Revers LF, Cardone JM, Bonatto D, Saffi J, Grey M, Feldmann H, Brendel M, Henriques JA (2002) Thermoconditional modulation of the pleiotropic sensitivity phenotype by the Saccharomyces cerevisiae PRP19 mutant allele pso4-1. Nucleic Acids Res 30:4993–5003CrossRefPubMedGoogle Scholar
  96. Roberts JW, Roberts CW, Craig NL, Phizicky EM (1979) Activity of the Escherichia coli recA-gene product. Cold Spring Harb Symp Quant Biol 43:917–920PubMedGoogle Scholar
  97. Roca AI, Cox MM (1997) RecA protein: structure, function, and role in recombinational DNA repair. Prog Nucleic Acid Res Mol Biol 56:129–223PubMedGoogle Scholar
  98. Roche H, Gietz RD, Kunz BA (1993) Specificities of the Saccharomyces cerevisiae rad6, rad18, and rad52 mutators exhibit different degrees of dependance on the REV3 gene product, a putative nonessential DNA polymerase. Genetics 140:443–456Google Scholar
  99. Saffhill R, Margison GP, O’Connor PJ (1985) Mechanisms of carcinogenesis induced by alkylating agents. Biochim Biophys Acta 823:111–145CrossRefPubMedGoogle Scholar
  100. Saito Y, Uraki F, Nakajima S, Asaeda A, Ono K, Kubo K, Yamamoto K (1997) Characterization of endonuclease III (nth) and endonuclease VIII (nei) mutants of Escherichia coli K-12. J Bacteriol 179:3783–3785PubMedGoogle Scholar
  101. Samson L, Cairns J (1977) A new pathway for DNA repair in Escherichia coli. Nature 267:281–283PubMedGoogle Scholar
  102. Samson LD (1992) The repair of DNA alkylation damage by methyltransferases and glycosylases. Essays Biochem 27:69–78PubMedGoogle Scholar
  103. Samson L, Derfler B, Waldstein EA (1986) Suppression of human DNA alkylation DNA repair defects by Escherichia coli DNA-repair genes. Proc Natl Acad Sci USA 83: 5607–5610PubMedGoogle Scholar
  104. Sassanfar M, Samson L (1990) Identification and preliminary characterization of an O6 -methylguanine DNA repair methyltransferase in the yeast Saccharomyces cerevisiae. J Biol Chem 265:20–25PubMedGoogle Scholar
  105. Sassanfar M, Dosanjh MK, Essigmann JM, Samson L (1991) Relative efficiencies of the bacterial, yeast, and human DNA methyltransferases for the repair of O6-methylguanine and O4-methylthymine. Suggestive evidence for O4-methylthymine repair by eukaryotic methyltransferases. J Biol Chem 266:2767–2771PubMedGoogle Scholar
  106. Sedgwick B, Robins P, Totty N, Lindahl T (1988) Functional domains and methyl acceptor sites of the Escherichia coli Ada protein. J Biol Chem 263:4430–4433PubMedGoogle Scholar
  107. Shcherbakova OG, Lanzov VA, Ogawa H, Filatov MV (2000) Overexpression of bacterial RecA protein stimulates homologous recombination in somatic mammalian cells. Mutat Res 459:65–71PubMedGoogle Scholar
  108. Shinagawa H, Iwasaki H, Kato T, Nakata A (1988) RecA protein-dependent cleavage of UmuD protein and SOS mutagenesis. Proc Natl Acad Sci USA 85:1806–1810PubMedGoogle Scholar
  109. Shinohara A, Ogawa A, Ogawa T (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69:457–470CrossRefPubMedGoogle Scholar
  110. Shinohara A, Ogawa H, Matsuda Y, Ushio N, Ikeo K, Ogawa T (1993) Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA. Nat Genet 4:239–243CrossRefPubMedGoogle Scholar
  111. Singer B (1975) The chemical effects of nucleic acid alkylation and their relation to mutagenesis and carcinogenesis. Prog Nucleic Acid Res Mol Biol 15:219–284PubMedGoogle Scholar
  112. Slaninová M, Vlčková V, Brozmanová J, Morais MA, Henriques JA (1996) Biological consequences of E. coli RecA protein expression in the repair defective pso4-1 and rad51::URA3 mutants of S. cerevisiae after treatment with N-methyl-N′-nitro-N-nitrosoguanidine. Neoplasma 43:315–319PubMedGoogle Scholar
  113. Sung P (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast Rad51 protein. Science 265:1241–1243PubMedGoogle Scholar
  114. Sung P, Robberson DL (1995) DNA strand exchange mediated by a Rad51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell 82:453–461CrossRefPubMedGoogle Scholar
  115. Sutton MD, Narumi I, Walker GC (2002) Posttranslational modification of the umuD-encoded subunit of Escherichia coli DNA polymerase V regulates its interactions with the beta processivity clamp. Proc Natl Acad Sci USA 99:5307–5312CrossRefPubMedGoogle Scholar
  116. Swanson RL, Morey NJ, Doetsch PW, Jinks-Robertson S (1999) Overlapping specificities of base excision repair, nucleotide excision repair, recombination, and translesion synthesis pathways for DNA base damage in Saccharomyces cerevisiae. Mol Cell Biol 19:2929–2935PubMedGoogle Scholar
  117. Symington LS (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol Mol Biol Rev 66:630–670Google Scholar
  118. Škorvaga M, Černaková L, Chovanec M, Vlasáková D, Kleibl K, Hendry JH, Margison GP, Brozmanová J (2003) Effect of expression of the Escherichia coli nth gene in Saccharomyces cerevisiae on the toxicity of ionizing radiation and hydrogen peroxide. Int J Radiat Biol 79:747–755CrossRefPubMedGoogle Scholar
  119. Thayer MM, Ahern H, Xing D, Cunningham RP, Tainer JA (1995) Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J 14:4108–4120PubMedGoogle Scholar
  120. Trewick SC, Henshaw TF, Hausinger RP, Lindahl T, Sedgwick B (2002) Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 419:174–178CrossRefPubMedGoogle Scholar
  121. Valerie K, Fronko G, Henderson EE, Riel JK (1986) Expresion of the denV gene of coliphage T4 in UV sensitive rad mutants of Saccharomyces cerevisiae. Mol Cell Biol 6:3559–3562PubMedGoogle Scholar
  122. Valerie K, Green AP, Riel JK, Henderson EE (1987) Transient and stable complementation of ultraviolet repair in XP cells by the denV gene of bacteriophage T4. Cancer Res 47:2967–2971PubMedGoogle Scholar
  123. van den Bosch M, Lohman PH, Pastink A (2002) DNA double-strand break repair by homologous recombination. Biol Chem 383:873–892PubMedGoogle Scholar
  124. Vlčková V, Černáková L, Farkašová E, Brozmanová J (1994) The Escherichia coli recA gene increases UV-induced mitotic gene conversion in Saccharomyces cerevisiae. Curr Genet 25:472–474PubMedGoogle Scholar
  125. Vlčková V, Slaninová M, Morais MA, Henriques JA, Fridrichová I, Brozmanová J (1997) Searching for a functional analogy between yeast Pso4 and bacterial RecA proteins in induced mitotic recombination. Neoplasma 44:374–379PubMedGoogle Scholar
  126. Walker GC (1984) Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Rev 48:60–93PubMedGoogle Scholar
  127. Wallace SS (1998) Enzymatic processing of radiation-induced free radical damage in DNA. Radiat Res 150:S60-S79PubMedGoogle Scholar
  128. Wallace SS, Bandaru V, Kathe SD, Bond JP (2003) The enigma of endonuclease VIII. DNA Repair 2:441–453CrossRefPubMedGoogle Scholar
  129. Ward JF (1981) Some biochemical consequences of the spatial distribution of ionizing radiation-produced free radicals. Radiat Res 86:185–195PubMedGoogle Scholar
  130. Ward JF (1985) Biochemistry of DNA lesions. Radiat Res [Suppl] 8:S103–S111Google Scholar
  131. Xiao W, Derfler B, Chen J, Samson L (1991) Primary sequence and biological functions of a Saccharomyces cerevisiae O6-methylguanine/O4-methylthymine DNA repair methyltransferase gene. EMBO J 10:2179–2186PubMedGoogle Scholar
  132. Xiao W, Samson L (1992) The Saccharomyces cerevisiae MGT1 DNA repair methyltransferase gene: its promoter and entire coding sequence, regulation and in vivo biological functions. Nucleic Acids Res 20:3599–3606PubMedGoogle Scholar
  133. You HJ, Swanson RL, Doetsch PW (1998) Saccharomyces cerevisiae possesses two functional homologues of Escherichia coli endonuclease III. Biochemistry 37:6033–6040CrossRefPubMedGoogle Scholar
  134. You HJ, Swanson RL, Harrington C, Corbett AH, Jinks-Robertson S, Senturker S, Wallace SS, Boiteux S, Dizdaroglu M, Doetsch PW (1999) Saccharomyces cerevisiae Ntg1p and Ntg2p: broad specificity N-glycosylases for the repair of oxidative DNA damage in the nucleus and mitochondria. Biochemistry 38:11298–11306CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Jela Brozmanová
    • 1
    Email author
  • Viera Vlčková
    • 2
  • Miroslav Chovanec
    • 1
  1. 1.Laboratory of Molecular GeneticsCancer Research InstituteBratislavaSlovak Republic
  2. 2.Faculty of Natural Sciences, Department of GeneticsComenius UniversityBratislavaSlovak Republic

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