Pathways of resistance to thymineless death in Escherichia coli and the function of UvrD

Genetics

Volumn 189, Issue 1, 2011, Pages 23-36

  Fonville, Natalie C ^a   Vaksman, Zalman ^a,b   Denapoli, Jessica ^a   Hastings, P J ^a   Rosenberg, Susan M ^a,c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CROSSOVER JUNCTION ENDODEOXYRIBONUCLEASE; DOUBLE STRANDED DNA; EXODEOXYRIBONUCLEASE V; HELICASE; RECA PROTEIN; RECJ PROTEIN; RECQ HELICASE; THYMINE; UNCLASSIFIED DRUG; UVRD HELICASE;

ARTICLE; CELL DEATH; CELL GROWTH; CELL PROTECTION; DNA REPAIR; DNA REPLICATION; DNA STRUCTURE; ENZYME DEGRADATION; ESCHERICHIA COLI; EXCISION REPAIR; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; RECA GENE; SIGNAL TRANSDUCTION; THYMINELESS DEATH;

DNA HELICASES; DNA REPAIR; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EXODEOXYRIBONUCLEASES; GENE EXPRESSION REGULATION, BACTERIAL; METABOLIC NETWORKS AND PATHWAYS; RECOMBINASES; RECOMBINATION, GENETIC; SOS RESPONSE (GENETICS); THYMINE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 80052665932     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.130161     Document Type: Article

References (63)

1. Ahmad, S. I., S. H. Kirk, and A. Eisenstark, 1998 Thymine metabolism and thymineless death in prokaryotes and eukaryotes. Annu. Rev. Microbiol. 52: 591-625.
2. Anderson, J. A., and S. D. Barbour, 1973 Effect of thymine starvation on deoxyribonucleic acid repair systems of Escherichia coli K-12. J. Bacteriol. 113: 114-121.
3. Arnold, D. A., and S. C. Kowalczykowski, 2000 Facilitated loading of RecA protein is essential to recombination by RecBCD enzyme. J. Biol. Chem. 275: 12261-12265.
4. Baba, T., T. Ara, M. Hasegawa, Y. Takai, Y. Okumura et al., 2006 Construction of Escherichia coli K-12 in-frame, singlegene knockout mutants: the Keio collection. Mol. Syst. Biol. 2: 2006.0008.
5. Bachmann, B. J., 1972 Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol. Rev. 36: 525-557.
6. Barner, H. D., and S. S. Cohen, 1954 The induction of thymine synthesis by T2 infection of a thymine requiring mutant of Escherichia coli. J. Bacteriol. 68: 80-88.
7. Bentchikou, E., P. Servant, G. Coste, and S. Sommer, 2010 A major role of the RecFOR pathway in DNA double-strand-break repair through ESDSA in Deinococcus radiodurans. PLoS Genet. 6: e1000774.
8. Blattner, F. R., G. Plunkett 3rd, C. A. Bloch, N. T. Perna, V. Burland et al., 1997 The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1474.
9. Cirz, R. T., J. K. Chin, D. R. Andes, V. de Crecy-Lagard, W. A. Craig et al., 2005 Inhibition of mutation and combating the evolution of antibiotic resistance. PLoS Biol. 3: e176.
10. Clark, A. J., and S. J. Sandler, 1994 Homologous genetic recombination: the pieces begin to fall into place. Crit. Rev. Microbiol. 20: 125-142.
11. Courcelle, J., C. Carswell-Crumpton, and P. C. Hanawalt, 1997 RecF and recR are required for the resumption of replication at DNA replication forks in Escherichia coli. Proc. Natl. Acad. Sci. USA 94: 3714-3719.
12. Cummings, D. J., and A. R. Kusy, 1970 Thymineless death in Escherichia coli: deoxyribonucleic acid replication and the immune state. J. Bacteriol. 102: 106-117.
13. Datsenko, K. A., and B. L. Wanner, 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97: 6640-6645.
14. Dri, A. M., J. Rouviere-Yaniv, and P. L. Moreau, 1991 Inhibition of cell division in hupA hupB mutant bacteria lacking HU protein. J. Bacteriol. 173: 2852-2863.
15. Dutreix, M., P. L. Moreau, A. Bailone, F. Galibert, J. R. Battista et al., 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.
16. Ennis, D. G., B. Fisher, S. Edmiston, and D. W. Mount, 1985 Dual role for Escherichia coli RecA protein in SOS mutagenesis. Proc. Natl. Acad. Sci. USA 82: 3325-3329.
17. Fekairi, S., S. Scaglione, C. Chahwan, E. R. Taylor, A. Tissier et al., 2009 Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138: 78-89.
18. Flores, M. J., N. Sanchez, and B. Michel, 2005 A fork-clearing role for UvrD. Mol. Microbiol. 57: 1664-1675.
19. Fonville, N. C., D. Bates, P. J. Hastings, P. C. Hanawalt, and S. M. Rosenberg, 2010a Role of RecA and the SOS Response in Thymineless Death in Escherichia coli. PLoS Genet. 6: e1000865.
20. Fonville, N. C., M. D. Blankschien, D. B. Magner, and S. M. Rosenberg, 2010b RecQ-dependent death-by-recombination in cells lacking RecG and UvrD. DNA Repair 9: 403-413.
21. Freifelder, D., 1969 Single-strand breaks in bacterial DNA associated with thymine starvation. J. Mol. Biol. 45: 1-7.
22. Friedberg, E., G. Walker, W. Siede, R. Wood, R. Schultz et al., 2005 DNA Repair and Mutagenesis, Ed. 2. ASM Press, Washington, DC.
23. Holthausen, J. T., C. Wyman, and R. Kanaar, 2010 Regulation of DNA strand exchange in homologous recombination. DNA Repair 9: 1264-1272.
24. Howard-Flanders, P., R. P. Boyce, and L. Theriot, 1966 Three loci in Escherichia coli K-12 that control the excision of pyrimidine dimers and certain other mutagen products from DNA. Genetics 53: 1119-1136.
25. Inouye, M., 1971 Pleiotropic effect of the recA gene of Escherichia coli: uncoupling of cell division from deoxyribonucleic acid replication. J. Bacteriol. 106: 539-542.
26. Ip, S. C., U. Rass, M. G. Blanco, H. R. Flynn, J. M. Skehel et al., 2008 Identification of Holliday junction resolvases from humans and yeast. Nature 456: 357-361.
27. Ivancic-Bace, I., E. Salaj-Smic, and K. Brcic-Kostic, 2005 Effects of recJ, recQ, and recFOR mutations on recombination in nucleasedeficient recB recD double mutants of Escherichia coli. J. Bacteriol. 187: 1350-1356.
28. Jensen, R. B., A. Carreira, and S. C. Kowalczykowski, 2010 Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 467: 678-683.
29. Koroleva, O., N. Makharashvili, C. T. Courcelle, J. Courcelle, and S. Korolev, 2007 Structural conservation of RecF and Rad50: implications for DNA recognition and RecF function. EMBO J. 26: 867-877.
30. Kuong, K. J., and A. Kuzminov, 2010 Stalled replication fork repair and misrepair during thymineless death in Escherichia coli. Genes Cells 15: 619-634.
31. Lestini, R., and B. Michel, 2008 UvrD and UvrD252 counteract RecQ, RecJ, and RecFOR in a rep mutant of Escherichia coli. J. Bacteriol. 190: 5995-6001.
32. Li, G. M., 2008 Mechanisms and functions of DNA mismatch repair. Cell Res. 18: 85-98.
33. Liu, J., T. Doty, B. Gibson, and W. D. Heyer, 2010 Human BRCA2 protein promotes RAD51 filament formation on RPA-covered single-stranded DNA. Nat. Struct. Mol. Biol. 17: 1260-1262.
34. Lopez, C. R., S. Yang, R. W. Deibler, S. A. Ray, J. M. Pennington et al., 2005 A role for topoisomerase III in a recombination pathway alternative to RuvABC. Mol. Microbiol. 58: 80-101.
35. Madiraju, M. V., P. E. Lavery, S. C. Kowalczykowski, and A. J. Clark, 1992 Enzymatic properties of the RecA803 protein, a partial suppressor of recF mutations. Biochemistry 31: 10529-10535.
36. Magner, D. B., M. D. Blankschien, J. A. Lee, J. M. Pennington, J. R. Lupski et al., 2007 RecQ promotes toxic recombination in cells lacking recombination intermediate-removal proteins. Mol. Cell 26: 273-286.
37. McGuire, J. J., 2003 Anticancer antifolates: current status and future directions. Curr. Pharm. Des. 9: 2593-2613.
38. McPartland, A., L. Green, and H. Echols, 1980 Control of recA gene RNA in E. coli: regulatory and signal genes. Cell 20: 731-737.
39. Miller, J., 1972 Generalized Transduction: Use of P1 in Strain Construction. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
40. Monnat, R. J., Jr., 2010 Human RECQ helicases: roles in DNA metabolism, mutagenesis and cancer biology. Semin. Cancer Biol. 20: 329-339.
41. Morganroth, P. A., and P. C. Hanawalt, 2006 Role of DNA replication and repair in thymineless death in Escherichia coli. J. Bacteriol. 188: 5286-5288.
42. Moynahan, M. E., and M. Jasin, 2010 Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 11: 196-207.
43. Nakayama, H., and P. Hanawalt, 1975 Sedimentation analysis of deoxyribonucleic acid from thymine-starved Escherichia coli. J. Bacteriol. 121: 537-547.
44. Nakayama, H., K. Nakayama, R. Nakayama, and Y. Nakayama 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: 425-430.
45. Nakayama, H., K. Nakayama, R. Nakayama, N. Irino, Y. Nakayama et al., 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: 474-480.
46. Nakayama, K., S. Shiota, and H. Nakayama, 1988 Thymineless death in Escherichia coli mutants deficient in the RecF recombination pathway. Can. J. Microbiol. 34: 905-907.
47. Nakayama, K., K. Kusano, N. Irino, and H. Nakayama, 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: 611-620.
48. Pennington, J. M., and S. M. Rosenberg, 2007 Spontaneous DNA breakage in single living Escherichia coli cells. Nat. Genet. 39: 797-802.
49. Rudolph, C. J., A. L. Upton, and R. G. Lloyd, 2008 Maintaining replication fork integrity in UV-irradiated Escherichia coli cells. DNA Repair 7: 1589-1602.
50. Sai Sree, L., M. Reddy, and J. Gowrishankar, 2000 Lon incompatibility associated with mutations causing SOS induction: null uvrD alleles induce an SOS response in Escherichia coli. J. Bacteriol. 182: 3151-3157.
51. Sancar, A., 1996 DNA excision repair. Annu. Rev. Biochem. 65: 43-81.
52. Sangurdekar, D. P., B. L. Hamann, D. Smirnov, F. Srienc, P. C. Hanawalt et al., 2010 Thymineless death is associated with loss of essential genetic information from the replication origin. Mol. Microbiol.
53. Seigneur, M., V. Bidnenko, S. D. Ehrlich, and B. Michel, 1998 RuvAB acts at arrested replication forks. Cell 95: 419-430.
54. Siegal, E., 1973 Ultraviolet-sensitive mutator strain of Escherichia coli K-12. J. Bacteriol. 113: 145-160.
55. Slack, A., P. C. Thornton, D. B. Magner, S. M. Rosenberg, and P. J. Hastings, 2006 On the mechanism of gene amplification induced under stress in Escherichia coli. PLoS Genet. 2: e48.
56. Somyajit, K., S. Subramanya, and G. Nagaraju, 2010 RAD51C: a novel cancer susceptibility gene is linked to Fanconi anemia and breast cancer. Carcinogenesis 31: 2031-2038.
57. Takahashi, N. K., K. Yamamoto, Y. Kitamura, S. Q. Luo, H. Yoshikura et al., 1992 Nonconservative recombination in Escherichia coli. Proc. Natl. Acad. Sci. USA 89: 5912-5916.
58. Takemura, Y., and A. L. Jackman, 1997 Folate-based thymidylate synthase inhibitors in cancer chemotherapy. Anticancer Drugs 8: 3-16.
59. Thacker, J., 2005 The RAD51 gene family, genetic instability and cancer. Cancer Lett. 219: 125-135.
60. Veaute, X., S. Delmas, M. Selva, J. Jeusset, E. Le Cam et al., 2005 UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli. EMBO J. 24: 180-189.
61. Vlasic, I., I. Ivancic-Bace, M. Imesek, B. Mihaljevic, and K. Brcic-Kostic, 2008 RecJ nuclease is required for SOS induction after introduction of a double-strand break in a RecA loading deficient recB mutant of Escherichia coli. Biochimie 90: 1347-1355.
62. Volkert, M. R., and M. A. Hartke, 1987 Effects of the Escherichia coli recF suppressor mutation, recA801, on recF-dependent DNArepair associated phenomena. Mutat. Res. 184: 181-186.
63. Yamao, F., Y. Nagai, S. Kaneda, S. Yoshida, and T. Seno, 1993 Conditional resistance to thymineless death predominantly selects DNA synthesis-deficient mutants of mammalian cells. Mutat. Res. 289: 83-89.