1932

Abstract

The primary mechanisms by which bacteria lose viability when deprived of thymine have been elusive for over half a century. Early research focused on stalled replication forks and the deleterious effects of uracil incorporation into DNA from thymidine-deficient nucleotide pools. The initiation of the replication cycle and origin-proximal DNA degradation during thymine starvation have now been quantified via whole-genome microarrays and other approaches. These advances have fostered innovative models and informative experiments in bacteria since this topic was last reviewed. Given that thymineless death is similar in mammalian cells and that certain antibacterial and chemotherapeutic drugs elicit thymine deficiency, a mechanistic understanding of this phenomenon might have valuable biomedical applications.

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2015-10-15
2024-06-25
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Literature Cited

  1. Adelberg EA, Coughlin CA. 1.  1956. Bacterial mutation induced by thymine starvation. Nature 178:531–32 [Google Scholar]
  2. Ahmad SI, Kirk SH, Eisenstark A. 2.  1998. Thymine metabolism and thymineless death in prokaryotes and eukaryotes. Annu. Rev. Microbiol. 52:591–625 [Google Scholar]
  3. Amyes SG. 3.  1982. Bactericidal activity of trimethoprim alone and in combination with sulfamethoxazole on susceptible and resistant Escherichia coli K-12. Antimicrob. Agents Chemother. 21:288–93 [Google Scholar]
  4. Amyes SG, Smith JT. 4.  1974. Trimethoprim action and its analogy with thymine starvation. Antimicrob. Agents Chemother. 5:169–78 [Google Scholar]
  5. Amyes SG, Smith JT. 5.  1975. Thymineless mutants and their resistance to trimethoprim. J. Antimicrob. Chemother. 1:85–89 [Google Scholar]
  6. An Q, Robins P, Lindahl T, Barnes DE. 6.  2007. 5-Fluorouracil incorporated into DNA is excised by the Smug1 DNA glycosylase to reduce drug cytotoxicity. Cancer Res. 67:940–45 [Google Scholar]
  7. Assaraf YG. 7.  2007. Molecular basis of antifolate resistance. Cancer Metastasis Rev. 26:153–81 [Google Scholar]
  8. Baker TA, Kornberg A. 8.  1988. Transcriptional activation of initiation of replication from the E. coli chromosomal origin: an RNA-DNA hybrid near oriC. Cell 55:113–23 [Google Scholar]
  9. Barner HD, Cohen SS. 9.  1954. The induction of thymine synthesis by T2 infection of a thymine requiring mutant of Escherichia coli. J. Bacteriol. 68:80–88 [Google Scholar]
  10. Barner HD, Cohen SS. 10.  1958. Protein synthesis and RNA turnover in a pyrimidine-deficient bacterium. Biochim. Biophys. Acta 30:12–20 [Google Scholar]
  11. Bates DB, Boye E, Asai T, Kogoma T. 11.  1997. The absence of effect of gid or mioC transcription on the initiation of chromosomal replication in Escherichia coli. PNAS 94:12497–502 [Google Scholar]
  12. Bazill GW. 12.  1967. Lethal unbalanced growth in bacteria. Nature 216:346–49 [Google Scholar]
  13. Beck CF, Eisenhardt AR, Neuhard J. 13.  1975. Deoxycytidine triphosphate deaminase of Salmonella typhimurium. Purification and characterization. J. Biol. Chem. 250:609–16 [Google Scholar]
  14. Belotserkovskii BP, Neil AJ, Saleh SS, Shin JH, Mirkin SM, Hanawalt PC. 14.  2013. Transcription blockage by homopurine DNA sequences: Role of sequence composition and single-strand breaks. Nucleic Acids Res. 41:1817–28 [Google Scholar]
  15. Bertino JB, Stacey KA. 15.  1966. A suggested mechanism for the selective procedure for isolating thymine-requiring mutants of Escherichia coli. Biochem. J. 101:32C–33C [Google Scholar]
  16. Besier S, Zander J, Kahl BC, Kraiczy P, Brade V, Wichelhaus TA. 16.  2008. The thymidine-dependent small-colony-variant phenotype is associated with hypermutability and antibiotic resistance in clinical Staphylococcus aureus isolates. Antimicrob. Agents Chemother. 52:2183–89 [Google Scholar]
  17. Bouvier F, Sicard N. 17.  1975. Interference of dna ts mutations of Escherichia coli with thymineless death. J. Bacteriol. 124:1198–204 [Google Scholar]
  18. Bremer H, Churchward G. 18.  1977. An examination of the Cooper-Helmstetter theory of DNA replication in bacteria and its underlying assumptions. J. Theor. Biol. 69:645–54 [Google Scholar]
  19. Burchall JJ, Hitchings GH. 19.  1965. Inhibitor binding analysis of dihydrofolate reductases from various species. Mol. Pharmacol. 1:126–36 [Google Scholar]
  20. Bushby SR, Hitchings GH. 20.  1968. Trimethoprim, a sulphonamide potentiator. Br. J. Pharmacol. Chemother. 33:72–90 [Google Scholar]
  21. Canman CE, Lawrence TS, Shewach DS, Tang HY, Maybaum J. 21.  1993. Resistance to fluorodeoxyuridine-induced DNA damage and cytotoxicity correlates with an elevation of deoxyuridine triphosphatase activity and failure to accumulate deoxyuridine triphosphate. Cancer Res. 53:5219–24 [Google Scholar]
  22. Carl PL. 22.  1970. Escherichia coli mutants with temperature-sensitive synthesis of DNA. Mol. Gen. Genet. 109:107–22 [Google Scholar]
  23. Carreras CW, Santi DV. 23.  1995. The catalytic mechanism and structure of thymidylate synthase. Annu. Rev. Biochem. 64:721–62 [Google Scholar]
  24. Casaregola S, D'Ari R, Huisman O. 24.  1982. Quantitative evaluation of recA gene expression in Escherichia coli. Mol. Gen. Genet. 185:430–39 [Google Scholar]
  25. Chatterjee I, Kriegeskorte A, Fischer A, Deiwick S, Theimann N. 25.  et al. 2008. In vivo mutations of thymidylate synthase (encoded by thyA) are responsible for thymidine dependency in clinical small-colony variants of Staphylococcus aureus. J. Bacteriol. 190:834–42 [Google Scholar]
  26. Claeys KC, Smith JR, Casapao AM, Mynatt RP, Avery L. 26.  et al. 2015. Impact of the combination of daptomycin and trimethoprim-sulfamethoxazole on clinical outcomes in methicillin-resistant Staphylococcus aureus infections. Antimicrob. Agents Chemother. 59:1969–76 [Google Scholar]
  27. Cohen SS, Barner HD. 27.  1954. Studies on unbalanced growth in Escherichia coli. PNAS 40:885–93 [Google Scholar]
  28. Courcelle J, Donaldson JR, Chow KH, Courcelle CT. 28.  2003. DNA damage-induced replication fork regression and processing in Escherichia coli. Science 299:1064–67 [Google Scholar]
  29. Courcelle J, Hanawalt PC. 29.  1999. RecQ and RecJ process blocked replication forks prior to the resumption of replication in UV-irradiated Escherichia coli. Mol. Gen. Genet. 262:543–51 [Google Scholar]
  30. Courcelle J, Hanawalt PC. 30.  2003. RecA-dependent recovery of arrested DNA replication forks. Annu. Rev. Genet. 37:611–46 [Google Scholar]
  31. Courcelle J, Khodursky A, Peter B, Brown PO, Hanawalt PC. 31.  2001. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158:41–64 [Google Scholar]
  32. Craig NL, Roberts JW. 32.  1980. E. coli recA protein-directed cleavage of phage λ repressor requires polynucleotide. Nature 283:26–30 [Google Scholar]
  33. Dale BA, Greenberg GR. 33.  1972. Effect of the folic acid analogue, trimethoprim, on growth, macromolecular synthesis, and incorporation of exogenous thymine in Escherichia coli. J. Bacteriol. 110:905–16 [Google Scholar]
  34. Donachie WD, Hobbs DG. 34.  1967. Recovery from “thymineless death” in Escherichia coli 15T. Biochem. Biophys. Res. Commun. 29:172–77 [Google Scholar]
  35. Duncan BK, Diamond GR, Bessman MJ. 35.  1972. Regulation of enzymatic activity through subunit interaction: a possible example. J. Biol. Chem. 247:8136–38 [Google Scholar]
  36. Dynes JL, Firtel RA. 36.  1989. Molecular complementation of a genetic marker in Dictyostelium using a genomic DNA library. PNAS 86:7966–70 [Google Scholar]
  37. Fonville NC, Bates D, Hastings PJ, Hanawalt PC, Rosenberg SM. 37.  2010. Role of RecA and the SOS response in thymineless death in Escherichia coli. PLOS Genet. 6:e1000865 [Google Scholar]
  38. Friedman KL, Brewer BJ. 38.  1995. Analysis of replication intermediates by two-dimensional agarose gel electrophoresis. Methods Enzymol. 262:613–27 [Google Scholar]
  39. Fuller RS, Kaguni JM, Kornberg A. 39.  1981. Enzymatic replication of the origin of the Escherichia coli chromosome. PNAS 78:7370–74 [Google Scholar]
  40. Gallant J, Suskind SR. 40.  1961. Relationship between thymineless death and ultraviolet inactivation in Escherichia coli. J. Bacteriol. 82:187–94 [Google Scholar]
  41. Giese KC, Michalowski CB, Little JW. 41.  2008. RecA-dependent cleavage of LexA dimers. J. Mol. Biol. 377:148–61 [Google Scholar]
  42. Godoy VG, Jarosz DF, Walker FL, Simmons LA, Walker GC. 42.  2006. Y-family DNA polymerases respond to DNA damage-independent inhibition of replication fork progression. EMBO J. 25:868–79 [Google Scholar]
  43. Goulian M, Bleile BM, Dickey LM, Grafstrom RH, Ingraham HA. 43.  et al. 1986. Mechanism of thymineless death. Adv. Exp. Med. Biol. 195:Part B89–95 [Google Scholar]
  44. Guarino E, Salguero I, Jiménez-Sánchez A, Guzmán EC. 44.  2007. Double-strand break generation under deoxyribonucleotide starvation in Escherichia coli. J. Bacteriol. 189:5782–86 [Google Scholar]
  45. Hanawalt P. 45.  1958. Macromolecular synthesis in E. coli under conditions of unbalanced growth. Ph.D. Thesis, Yale Univ., New Haven, CT [Google Scholar]
  46. Hanawalt P. 46.  1959. Use of phosphorus-32 in microassay for nucleic acid synthesis in Escherichia coli. Science 130:386–87 [Google Scholar]
  47. Hanawalt PC. 47.  1963. Involvement of synthesis of RNA in thymineless death. Nature 198:286 [Google Scholar]
  48. Hanawalt PC. 48.  2015. A balanced perspective on unbalanced growth and thymineless death. Front. Microbiol. 6504 [Google Scholar]
  49. Hanawalt PC, Maaløe O, Cummings DJ, Schaechter M. 49.  1961. The normal DNA replication cycle. II. J. Mol. Biol. 3:156–65 [Google Scholar]
  50. Harvey RJ, Dev IK. 50.  1975. Regulation in the folate pathway of Escherichia coli. Adv. Enzyme Regul. 13:99–124 [Google Scholar]
  51. Hitchings GH. 51.  1973. Mechanism of action of trimethoprim-sulfamethoxazole—I. J. Infect. Dis. 128:Suppl.433–36 [Google Scholar]
  52. Itsko M, Schaaper RM. 52.  2011. The dgt gene of Escherichia coli facilitates thymine utilization in thymine-requiring strains. Mol. Microbiol. 81:1221–32 [Google Scholar]
  53. Itsko M, Schaaper RM. 53.  2014. dGTP starvation in Escherichia coli provides new insights into the thymineless-death phenomenon. PLOS Genet. 10:e1004310 [Google Scholar]
  54. Jarroll EL, Manning P, Berrada A, Hare D, Lindmark DG. 54.  1989. Biochemistry and metabolism of Giardia. J. Protozool. 36:190–97 [Google Scholar]
  55. Jiménez-Sánchez A, Guzmán EC. 55.  1988. Direct procedure for the determination of the number of replication forks and the reinitiation fraction in bacteria. Comput. Appl. Biosci. 4:431–33 [Google Scholar]
  56. Kasho K, Katayama T. 56.  2013. DnaA binding locus datA promotes DnaA-ATP hydrolysis to enable cell cycle-coordinated replication initiation. PNAS 110:936–41 [Google Scholar]
  57. Khodursky AB, Bernstein JA, Peter BJ, Rhodius V, Wendisch VF, Zimmer DP. 57.  2003. Escherichia coli spotted double-strand DNA microarrays: RNA extraction, labeling, hybridization, quality control, and data management. Methods Mol. Biol. 224:61–78 [Google Scholar]
  58. Khodursky AB, Peter BJ, Schmid MB, DeRisi J, Botstein D. 58.  et al. 2000. Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. PNAS 97:9419–24 [Google Scholar]
  59. King CH, Shlaes DM, Dul MJ. 59.  1983. Infection caused by thymidine-requiring, trimethoprim-resistant bacteria. J. Clin. Microbiol. 18:79–83 [Google Scholar]
  60. Kitagawa R, Mitsuki H, Okazaki T, Ogawa T. 60.  1996. A novel DnaA protein-binding site at 94.7 min on the Escherichia coli chromosome. Mol. Microbiol. 19:1137–47 [Google Scholar]
  61. Kornberg A, Baker T. 61.  2005. DNA Replication Sausalito, CA: Univ. Sci. Books [Google Scholar]
  62. Kornberg SR, Lehman IR, Bessman MJ, Simms ES, Kornberg A. 62.  1958. Enzymatic cleavage of deoxyguanosine triphosphate to deoxyguanosine and tripolyphosphate. J. Biol. Chem. 233:159–62 [Google Scholar]
  63. Kriegeskorte A, Block D, Drescher M, Windmuller N, Mellmann A. 63.  et al. 2014. Inactivation of thyA in Staphylococcus aureus attenuates virulence and has a strong impact on metabolism and virulence gene expression. mBio 5:e01447–14 [Google Scholar]
  64. Krokan HE, Saetrom P, Aas PA, Pettersen HS, Kavli B, Slupphaug G. 64.  2014. Error-free versus mutagenic processing of genomic uracil—relevance to cancer. DNA Repair 19:38–47 [Google Scholar]
  65. Kunz BA, Glickman BW. 65.  1985. Mechanism of mutation by thymine starvation in Escherichia coli: clues from mutagenic specificity. J. Bacteriol. 162:859–64 [Google Scholar]
  66. Kunz C, Focke F, Saito Y, Schuermann D, Lettieri T. 66.  et al. 2009. Base excision by thymine DNA glycosylase mediates DNA-directed cytotoxicity of 5-fluorouracil. PLOS Biol. 7:e91 [Google Scholar]
  67. Kuong KJ, Kuzminov A. 67.  2010. Stalled replication fork repair and misrepair during thymineless death in Escherichia coli. Genes Cells 15:619–34 [Google Scholar]
  68. Kuong KJ, Kuzminov A. 68.  2012. Disintegration of nascent replication bubbles during thymine starvation triggers RecA- and RecBCD-dependent replication origin destruction. J. Biol. Chem. 287:23958–70 [Google Scholar]
  69. Kwon YK, Higgins MB, Rabinowitz JD. 69.  2010. Antifolate-induced depletion of intracellular glycine and purines inhibits thymineless death in. E. coli. ACS Chem. Biol. 5:787–95 [Google Scholar]
  70. Lark KG. 70.  1972. Evidence for the direct involvement of RNA in the initiation of DNA replication in Escherichia coli 15T. J. Mol. Biol. 64:47–60 [Google Scholar]
  71. Leonard AC, Grimwade JE. 71.  2011. Regulation of DnaA assembly and activity: taking directions from the genome. Annu. Rev. Microbiol. 65:19–35 [Google Scholar]
  72. Lewis K. 72.  2010. Persister cells. Annu. Rev. Microbiol. 64:357–72 [Google Scholar]
  73. Liao ZY, Sordet O, Zhang HL, Kohlhagen G, Antony S. 73.  et al. 2005. A novel polypyrimidine antitumor agent FdUMP[10] induces thymineless death with topoisomerase I-DNA complexes. Cancer Res. 65:4844–51 [Google Scholar]
  74. Little JG, Hanawalt PC. 74.  1973. Thymineless death and ultraviolet sensitivity in Micrococcus radiodurans. J. Bacteriol. 113:233–40 [Google Scholar]
  75. Maaløe O, Hanawalt PC. 75.  1961. Thymine deficiency and the normal DNA replication cycle. I.. J. Mol. Biol. 3:144–55 [Google Scholar]
  76. Makino F, Munakata N. 76.  1978. Deoxyuridine residues in DNA of thymine-requiring Bacillus subtilis strains with defective N-glycosidase activity for uracil-containing DNA. J. Bacteriol. 134:24–29 [Google Scholar]
  77. Martín CM, Guzmán EC. 77.  2011. DNA replication initiation as a key element in thymineless death. DNA Repair 10:94–101 [Google Scholar]
  78. Martín CM, Viguera E, Guzmán EC. 78.  2014. Rifampicin suppresses thymineless death by blocking the transcription-dependent step of chromosome initiation. DNA Repair 18:10–17 [Google Scholar]
  79. Masters PA, O'Bryan TA, Zurlo J, Miller DQ, Joshi N. 79.  2003. Trimethoprim-sulfamethoxazole revisited. Arch. Intern. Med. 163:402–10 [Google Scholar]
  80. Messer W. 80.  1972. Initiation of deoxyribonucleic acid replication in Escherichia coli B-r: chronology of events and transcriptional control of initiation. J. Bacteriol. 112:7–12 [Google Scholar]
  81. Miovic M, Pizer LI. 81.  1971. Effect of trimethoprim on macromolecular synthesis in Escherichia coli. J. Bacteriol. 106:856–62 [Google Scholar]
  82. Molina F, Jimenez-Sanchez A, Zyskind JW, Guzmán EC. 82.  1999. Chromosomal insertions localized around oriC affect the cell cycle in Escherichia coli. Biochimie 81:811–18 [Google Scholar]
  83. Mollgaard H, Neuhard J. 83.  1978. Deoxycytidylate deaminase from Bacillus subtilis: purification, characterization, and physiological function. J. Biol. Chem. 253:3536–42 [Google Scholar]
  84. Morganroth PA, Hanawalt PC. 84.  2006. Role of DNA replication and repair in thymineless death in Escherichia coli. J. Bacteriol. 188:5286–88 [Google Scholar]
  85. Morigen, Molina F, Skarstad K. 85.  2005. Deletion of the datA site does not affect once-per-cell-cycle timing but induces rifampin-resistant replication. J. Bacteriol. 187:3913–20 [Google Scholar]
  86. Myllykallio H, Lipowski G, Leduc D, Filee J, Forterre P, Liebl U. 86.  2002. An alternative flavin-dependent mechanism for thymidylate synthesis. Science 297:105–7 [Google Scholar]
  87. Nakayama H. 87.  2005. Escherichia coli RecQ helicase: a player in thymineless death. Mutat. Res. 577:228–36 [Google Scholar]
  88. Nakayama H, Couch JL. 88.  1973. Thymineless death in Escherichia coli in various assay systems: viability determined in liquid medium. J. Bacteriol. 114:228–32 [Google Scholar]
  89. Nakayama H, Hanawalt P. 89.  1975. Sedimentation analysis of deoxyribonucleic acid from thymine-starved Escherichia coli. J. Bacteriol. 121:537–47 [Google Scholar]
  90. Nakayama H, Nakayama K, Nakayama R, Irino N, Nakayama Y, Hanawalt PC. 90.  1984. Isolation and genetic characterization of a thymineless death-resistant mutant of Escherichia coli K12: identification of a new mutation (recQ1) that blocks the RecF recombination pathway. Mol. Gen. Genet. 195:474–80 [Google Scholar]
  91. Nakayama H, Nakayama K, Nakayama R, Nakayama Y. 91.  1982. Recombination-deficient mutations and thymineless death in Escherichia coli K12: reciprocal effects of recBC and recF and indifference of recA mutations. Can. J. Microbiol. 28:425–30 [Google Scholar]
  92. Nakayama K, Kusano K, Irino N, Nakayama H. 92.  1994. Thymine starvation-induced structural changes in Escherichia coli DNA. Detection by pulsed field gel electrophoresis and evidence for involvement of homologous recombination. J. Mol. Biol. 243:611–20 [Google Scholar]
  93. Neil AJ, Belotserkovskii BP, Hanawalt PC. 93.  2012. Transcription blockage by bulky end termini at single-strand breaks in the DNA template: differential effects of 5′ and 3′ adducts. Biochemistry 51:8964–70 [Google Scholar]
  94. Pauling C, Hanawalt P. 94.  1965. Nonconservative DNA replication in bacteria after thymine starvation. PNAS 54:1728–35 [Google Scholar]
  95. Pohlhaus JR, Long DT, O'Reilly E, Kreuzer KN. 95.  2008. The epsilon subunit of DNA polymerase III is involved in the nalidixic acid-induced SOS response in Escherichia coli. J. Bacteriol. 190:5239–47 [Google Scholar]
  96. Pritchard RH, Lark KG. 96.  1964. Induction of replication by thymine starvation at the chromosome origin in Escherichia coli. J. Mol. Biol. 9:288–307 [Google Scholar]
  97. Pritchard RH, Zaritsky A. 97.  1970. Effect of thymine concentration on the replication velocity of DNA in a thymineless mutant of Escherichia coli. Nature 226:126–31 [Google Scholar]
  98. Proudfoot M, Kuznetsova E, Brown G, Rao NN, Kitagawa M. 98.  et al. 2004. General enzymatic screens identify three new nucleotidases in Escherichia coli: biochemical characterization of SurE, YfbR, and YjjG. J. Biol. Chem. 279:54687–94 [Google Scholar]
  99. Quirk S, Seto D, Bhatnagar SK, Gauss P, Gold L, Bessman MJ. 99.  1989. Location and molecular cloning of the structural gene for the deoxyguanosine triphosphate triphosphohydrolase of Escherichia coli. Mol. Microbiol. 3:1391–95 [Google Scholar]
  100. Ramareddy G, Reiter H. 100.  1970. Sequential loss of loci in thymine-starved Bacillus subtilis 168 cells: evidence for a circular chromosome. J. Mol. Biol. 50:525–32 [Google Scholar]
  101. Razzell WE, Casshyap P. 101.  1964. Substrate specificity and induction of thymidine phosphorylase in Escherichia coli. J. Biol. Chem. 239:1789–93 [Google Scholar]
  102. Regamey A, Harry EJ, Wake RG. 102.  2000. Mid-cell Z ring assembly in the absence of entry into the elongation phase of the round of replication in bacteria: co-ordinating chromosome replication with cell division. Mol. Microbiol. 38:423–34 [Google Scholar]
  103. Reiter H, Ramareddy G. 103.  1970. Loss of DNA behind the growing point of thymine-starved Bacillus subtilis 168. J. Mol. Biol. 50:533–48 [Google Scholar]
  104. Sangurdekar DP, Hamann BL, Smirnov D, Srienc F, Hanawalt PC, Khodursky AB. 104.  2010. Thymineless death is associated with loss of essential genetic information from the replication origin. Mol. Microbiol. 75:1455–67 [Google Scholar]
  105. Sangurdekar DP, Zhang Z, Khodursky AB. 105.  2011. The association of DNA damage response and nucleotide level modulation with the antibacterial mechanism of the anti-folate drug trimethoprim. BMC Genomics 12:583 [Google Scholar]
  106. Sassanfar M, Roberts JW. 106.  1990. Nature of the SOS-inducing signal in Escherichia coli: the involvement of DNA replication. J. Mol. Biol. 212:79–96 [Google Scholar]
  107. Sat B, Reches M, Engelberg-Kulka H. 107.  2003. The Escherichia coli mazEF suicide module mediates thymineless death. J. Bacteriol. 185:1803–7 [Google Scholar]
  108. Sawai H, Nagashima J, Kuwahara M, Kitagata R, Tamura T, Matsui I. 108.  2007. Differences in substrate specificity of C(5)-substituted or C(5)-unsubstituted pyrimidine nucleotides by DNA polymerases from thermophilic bacteria, archaea, and phages. Chem. Biodivers. 4:1979–95 [Google Scholar]
  109. Schena M, Shalon D, Davis RW, Brown PO. 109.  1995. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270:467–70 [Google Scholar]
  110. Seiple L, Jaruga P, Dizdaroglu M, Stivers JT. 110.  2006. Linking uracil base excision repair and 5-fluorouracil toxicity in yeast. Nucleic Acids Res. 34:140–51 [Google Scholar]
  111. Sergott RC, Debeer LJ, Bessman MJ. 111.  1971. On the regulation of a bacterial deoxycytidylate deaminase. J. Biol. Chem. 246:7755–58 [Google Scholar]
  112. Seto D, Bhatnagar SK, Bessman MJ. 112.  1988. The purification and properties of deoxyguanosine triphosphate triphosphohydrolase from Escherichia coli. J. Biol. Chem. 263:1494–99 [Google Scholar]
  113. Simmons LA, Goranov AI, Kobayashi H, Davies BW, Yuan DS. 113.  et al. 2009. Comparison of responses to double-strand breaks between Escherichia coli and Bacillus subtilis reveals different requirements for SOS induction. J. Bacteriol. 191:1152–61 [Google Scholar]
  114. Smith DW, Hanawalt PC. 114.  1968. Macromolecular synthesis and thymineless death in Mycoplasma laidlawii B. J. Bacteriol. 96:2066–76 [Google Scholar]
  115. Smith RJ, Midgley JE. 115.  1973. The effect of trimethoprim on macromolecular synthesis in Escherichia coli. Biochem. J. 136:225–34 [Google Scholar]
  116. Sueoka N, Yoshikawa H. 116.  1965. The chromosome of Bacillus subtilis. I. Theory of marker frequency analysis. Genetics 52:747–57 [Google Scholar]
  117. Su'etsugu M, Emoto A, Fujimitsu K, Keyamura K, Katayama T. 117.  2003. Transcriptional control for initiation of chromosomal replication in Escherichia coli: Fluctuation of the level of origin transcription ensures timely initiation. Genes Cells 8:731–45 [Google Scholar]
  118. Uerkvitz W, Karlstrom O, Munch-Petersen A. 118.  1973. A deoxyuridine monophosphate phosphatase detected in mutants of Escherichia coli lacking alkaline phosphatase and 5′-nucleotidase. Mol. Gen. Genet. 121:337–46 [Google Scholar]
  119. Waldman BC, Wang Y, Kilaru K, Yang Z, Bhasin A. 119.  et al. 2008. Induction of intrachromosomal homologous recombination in human cells by raltitrexed, an inhibitor of thymidylate synthase. DNA Repair 7:1624–35 [Google Scholar]
  120. Wang TC, Smith KC. 120.  1983. Mechanisms for recF-dependent and recB-dependent pathways of postreplication repair in UV-irradiated Escherichia coli uvrB. J. Bacteriol. 156:1093–98 [Google Scholar]
  121. Weiss B. 121.  2007. The deoxycytidine pathway for thymidylate synthesis in Escherichia coli. J. Bacteriol. 189:7922–26 [Google Scholar]
  122. Weiss B. 122.  2007. YjjG, a dUMP phosphatase, is critical for thymine utilization by Escherichia coli K-12. J. Bacteriol. 189:2186–89 [Google Scholar]
  123. Williams JS, Kunkel TA. 123.  2014. Ribonucleotides in DNA: origins, repair and consequences. DNA Repair 19:27–37 [Google Scholar]
  124. Wyatt MD, Wilson DM III. 124.  2009. Participation of DNA repair in the response to 5-fluorouracil. Cell Mol. Life Sci. 66:788–99 [Google Scholar]
  125. Zaritsky A, Pritchard RH. 125.  1971. Replication time of the chromosome in thymineless mutants of Escherichia coli. J. Mol. Biol. 60:65–74 [Google Scholar]
  126. Zaritsky A, Woldringh CL, Einav M, Alexeeva S. 126.  2006. Use of thymine limitation and thymine starvation to study bacterial physiology and cytology. J. Bacteriol. 188:1667–79 [Google Scholar]
  127. Zhou W, Doetsch PW. 127.  1993. Effects of abasic sites and DNA single-strand breaks on prokaryotic RNA polymerases. PNAS 90:6601–5 [Google Scholar]
  128. Zhou W, Doetsch PW. 128.  1994. Transcription bypass or blockage at single-strand breaks on the DNA template strand: Effect of different 3′ and 5′ flanking groups on the T7 RNA polymerase elongation complex. Biochemistry 33:14926–34 [Google Scholar]
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