Promoting and avoiding recombination: Contrasting activities of the Escherichia coli RuvABC Holliday junction resolvase and RecG DNA translocase

Genetics

Volumn 185, Issue 1, 2010, Pages 23-37

  Zhang, Jing ^a   Mahdi, Akeel A ^a   Briggs, Geoffrey S ^a   Lloyd, Robert G ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CROSSOVER JUNCTION ENDODEOXYRIBONUCLEASE; MEMBRANE PROTEIN; NUCLEASE; ORIC PROTEIN; PRIA PROTEIN; RECG DNA TRANSLOCASE; RECG HELICASE; RUVABC HOLLIDAY JUNCTION RESOLVASE; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; DEOXYRIBONUCLEASE; ESCHERICHIA COLI PROTEIN; HELICASE; HOLLIDAY JUNCTION DNA HELICASE, E COLI; RECG PROTEIN, E COLI; RUVB PROTEIN, BACTERIA; RUVC PROTEIN, E COLI;

ARTICLE; CATALYSIS; CONTROLLED STUDY; DAM GENE; ESCHERICHIA COLI; GENE; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENE MAPPING; GENE MUTATION; GENE REPLICATION; GENETIC RECOMBINATION; LETHALITY; NONHUMAN; POLA GENE; PRIORITY JOURNAL; SSB GENE; UVRD GENE; AMINO ACID SUBSTITUTION; BACTERIAL CHROMOSOME; BIOLOGICAL MODEL; CYTOLOGY; DNA REPAIR; DNA REPLICATION; ENZYMOLOGY; GENE REPRESSION; GENETICS; METABOLISM; MICROBIAL VIABILITY;

ESCHERICHIA COLI;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; DNA HELICASES; DNA REPAIR; DNA REPLICATION; DNA, BACTERIAL; ENDODEOXYRIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HOLLIDAY JUNCTION RESOLVASES; MICROBIAL VIABILITY; MODELS, BIOLOGICAL; RECOMBINATION, GENETIC; SUPPRESSION, GENETIC;

EID: 77956628003     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.114413     Document Type: Article

References (83)

1. AL-DEIB, A. A., A. A. MAHDI and R. G. LLOYD, 1996 Modulation of recombination and DNA repair by the RecG and PriA helicases of Escherichia coli K-12. J. Bacteriol. 178: 6782-6789.
2. ARTHUR, H. M., and R. G. LLOYD, 1980 Hyper-recombination in uvrD mutants of Escherichia coli K-12. Mol. Gen. Genet. 180: 185-191.
3. ASAI, T., and T. KOGOMA, 1994a D-loops and R-loops: alternative mechanisms for the initiation of chromosome replication in Escherichia coli. J. Bacteriol. 176: 1807-1812. (Pubitemid 24103526)
4. ASAI, T., and T. KOGOMA, 1994b Roles of ruvA, ruvC and recG gene functions in normal and DNA damage-inducible replication of the Escherichia coli chromosome. Genetics 137: 895-902.
5. BERNHARDT, T. G., and P. A. DE BOER, 2004 Screening for synthetic lethal mutants in Escherichia coli and identification of EnvC (YibP) as a periplasmic septal ring factor with murein hydrolase activity. Mol. Microbiol. 52: 1255-1269.
6. BOLT, E. L., and R. G. LLOYD, 2002 Substrate specificity of RusA resolvase reveals the DNA structures targeted by RuvAB and RecG in vivo. Mol. Cell 10: 187-198.
7. BUSS, J. A., Y. KIMURA and P. R. BIANCO, 2008 RecG interacts directly with SSB: implications for stalled replication fork regression. Nucleic Acids Res. 36: 7029-7042.
8. CADMAN, C. J., and P. MCGLYNN, 2004 PriA helicase and SSB interact physically and functionally. Nucleic Acids Res. 32: 6378-6387.
9. COX, M. M., 2007a Motoring along with the bacterial RecA protein. Nat. Rev. Mol. Cell. Biol. 8: 127-138.
10. COX, M. M., 2007b Regulation of bacterial RecA protein function. Crit. Rev. Biochem. Mol. Biol. 42: 41-63.
11. CURTH, U., J. GENSCHEL, C. URBANKE and J. GREIPEL, 1996 In vitro and in vivo function of the C-terminus of Escherichia coli single-stranded DNA binding protein. Nucleic Acids Res. 24: 2706-2711.
12. 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.
13. DILLINGHAM, M. S., and S. C. KOWALCZYKOWSKI, 2008 RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol. Mol. Biol. Rev. 72: 642-671.
14. DONALDSON, J. R., C. T. COURCELLE and J. COURCELLE, 2004 RuvAB and RecG are not essential for the recovery of DNA synthesis following UV-induced DNA damage in Escherichia coli. Genetics 166: 1631-1640.
15. FLORES, M. J., N. SANCHEZ and B. MICHEL, 2005 A fork-clearing role for UvrD. Mol. Microbiol. 57: 1664-1675.
16. FUKUOH, A., H. IWASAKI, K. ISHIOKA and H. SHINAGAWA, 1997 ATP-dependent resolution of R-loops at the ColE1 replication origin by Escherichia coli RecG protein, a Holliday junction-specific helicase. EMBO J. 16: 203-209.
17. GREGG, A. V., P. MCGLYNN, R. P. JAKTAJI and R. G. LLOYD, 2002 Direct rescue of stalled DNA replication forks via the combined action of PriA and RecG helicase activities. Mol. Cell 9: 241-251.
18. GROVE, J. I., L. HARRIS, C. BUCKMAN and R. G. LLOYD, 2008 DNA double strand break repair and crossing over mediated by RuvABC resolvase and RecG translocase. DNA Repair 7: 1517-1530.
19. HIASA, H., and K. J. MARIANS, 1994 Tus prevents overreplication of oriC plasmid DNA. J. Biol. Chem. 269: 26959-26968.
20. HONG, X., G. W. CADELL and T. KOGOMA, 1995 Escherichia coli RecG and RecA proteins in R-loop formation. EMBO J. 14: 2385-2392.
21. ISHIOKA, K., H. IWASAKI and H. SHINAGAWA, 1997 Roles of the recG gene product of Escherichia coli in recombination repair: effects of the delta recG mutation on cell division and chromosome partition. Genes Genet. Syst. 72: 91-99.
22. ISHIOKA, K., A. FUKUOH, H. IWASAKI, A. NAKATA and H. SHINAGAWA, 1998 Abortive recombination in Escherichia coli ruv mutants blocks chromosome partitioning. Genes Cells 3: 209-220.
23. JAKTAJI, R. P., and R. G. LLOYD, 2003 PriA supports two distinct pathways for replication restart in UV-irradiated Escherichia coli cells. Mol. Microbiol. 47: 1091-1100.
24. KOGOMA, T., 1997 Stable DNA replication: Interplay between DNA replication, homologous recombination, and transcription. Microbiol. Mol. Biol. Rev. 61: 212-238.
25. KOWALCZYKOWSKI, S. C., 2000 Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci. 25: 156-165.
26. KRABBE, M., J. ZABIELSKI, R. BERNANDER and K. NORDSTROM, 1997 Inactivation of the replication-termination system affects the replication mode and causes unstable maintenance of plasmid R1. Mol. Microbiol. 24: 723-735.
27. KUZMINOV, A., 1995 Collapse and repair of replication forks in Escherichia coli. Mol. Microbiol. 16: 373-384.
28. LECOINTE, F., C. SERENA, M. VELTEN, A. COSTES, S. MCGOVERN et al., 2007 Anticipating chromosomal replication fork arrest: SSB targets repair DNA helicases to active forks. EMBO J. 26: 4239-4251.
29. LESTINI, R., and B. MICHEL, 2007 UvrD controls the access of recombination proteins to blocked replication forks. EMBO J. 26: 3804-3814. (Pubitemid 47295871)
30. LIU, J., and K. J. MARIANS, 1999 PriA-directed assembly of a primosome on D loop DNA. J. Biol. Chem. 274: 25033-25041.
31. LIU, J., L. XU, S. J. SANDLER and K. J. MARIANS, 1999 Replication fork assembly at recombination intermediates is required for bacterial growth. Proc. Natl. Acad. Sci. USA 96: 3552-3555.
32. LLOYD, R. G., 1991 Conjugational recombination in resolvase-deficient ruvC mutants of Escherichia coli K-12 depends on recG. J. Bacteriol. 173: 5414-5418.
33. LLOYD, R. G., and G. J. SHARPLES, 1993 Dissociation of synthetic Holliday junctions by E. coli RecG protein. EMBO J. 12: 17-22.
34. - phenotype. J. Bacteriol. 120: 407-415.
35. LOVETT, S. T., P. T. DRAPKIN, V. A. SUTERA, JR. and T. J. GLUCKMAN-PESKIND, 1993 A sister-strand exchange mechanism for recA-independent deletion of repeated DNA sequences in Escherichia coli. Genetics 135: 631-642.
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. MAHDI, A. A., G. J. SHARPLES, T. N. MANDAL and R. G. LLOYD, 1996 Holliday junction resolvases encoded by homologous rusA genes in Escherichia coli K-12 and phage 82. J. Mol. Biol. 257: 561-573.
38. MAHDI, A. A., G. S. BRIGGS, G. J. SHARPLES, Q. WEN and R. G. LLOYD, 2003 A model for dsDNA translocation revealed by a structural motif common to RecG and Mfd proteins. EMBO J. 22: 724-734.
39. MAHDI, A. A., C. BUCKMAN, L. HARRIS and R. G. LLOYD, 2006 Rep and PriA helicase activities prevent RecA from provoking unnecessary recombination during replication fork repair. Genes Dev. 20: 2135-2147.
40. MANDAL, T. N., A. A. MAHDI, G. J. SHARPLES and R. G. LLOYD, 1993 Resolution of Holliday intermediates in recombination and DNA repair: indirect suppression of ruvA, ruvB and ruvC mutations. J. Bacteriol. 175: 4325-4334.
41. MARINUS, M. G., 2000 Recombination is essential for viability of an Escherichia coli dam (DNA adenine methyltransferase) mutant. J. Bacteriol. 182: 463-468.
42. MARKOVITZ, A., 2005 A new in vivo termination function for DNA polymerase I of Escherichia coli K12. Mol. Microbiol. 55: 1867-1882.
43. MASAI, H., T. ASAI, Y. KUBOTA, K. ARAI and T. KOGOMA, 1994 Escherichia coli PriA protein is essential for inducible and constitutive stable DNA replication. EMBO J. 13: 5338-5345. (Pubitemid 24351812)
44. MATSON, S. W., and K. A. KAISER-ROGERS, 1990 DNA helicases. Annu. Rev. Biochem. 59: 289-329.
45. MATSUMOTO, T., Y. MORIMOTO, N. SHIBATA, T. KINEBUCHI, N. SHIMAMOTO et al., 2000 Roles of functional loops and the C-terminal segment of a single-stranded DNA binding protein elucidated by X-Ray structure analysis. J. Biochem. 127: 329-335.
46. MCCOOL, J. D., and S. J. SANDLER, 2001 Effects of mutations involving cell division, recombination, and chromosome dimer resolution on a priA2:kan mutant. Proc. Natl. Acad. Sci. USA 98: 8203-8210.
47. MCGLYNN, P., A. A. AL-DEIB, J. LIU, K. J. MARIANS and R. G. LLOYD, 1997 The DNA replication protein PriA and the recombination protein RecG bind D-loops. J. Mol. Biol. 270: 212-221.
48. MCGLYNN, P., and R. G. LLOYD, 2000 Modulation of RNA polymerase by (p)ppGpp reveals a RecG-dependent mechanism for replication fork progression. Cell 101: 35-45.
49. MCGLYNN, P., and R. G. LLOYD, 2001 Rescue of stalled replication forks by RecG: simultaneous translocation on the leading and lagging strand templates supports an active DNA unwinding model of fork reversal and Holliday junction formation. Proc. Nat. Acad. Sci. USA 98: 8227-8234.
50. MCGLYNN, P., and R. G. LLOYD, 2002a Genome stability and the processing of damaged replication forks by RecG. Trends Genet. 18: 413-419.
51. MCGLYNN, P., and R. G. LLOYD, 2002b Recombinational repair and restart of damaged replication forks. Nat. Rev. Mol. Cell. Biol. 3: 859-870.
52. MEDDOWS, T. R., A. P. SAVORY and R. G. LLOYD, 2004 RecG helicase promotes DNA double-strand break repair. Mol. Microbiol. 52: 119-132.
53. MENDONCA, V. M., and S. W. MATSON, 1995 Genetic analysis of ΔhelD and ΔuvrD mutations in combination with other genes in the RecF recombination pathway in Escherichia coli: suppression of a ruvB mutation by a uvrD deletion. Genetics 141: 443-452.
54. MICHEL, B., H. BOUBAKRI, Z. BAHAROGLU, M. LEMASSON and R. LESTINI, 2007 Recombination proteins and rescue of arrested replication forks. DNA Repair (Amst.) 6: 967-980. (Pubitemid 46880477)
55. MODRICH, P., 1991 Mechanisms and biological effects of mismatch repair. Annu. Rev. Genet. 25: 229-253.
56. MOOLENAAR, G. F., C. MOORMAN and N. GOOSEN, 2000 Role of the Escherichia coli nucleotide excision repair proteins in DNA replication. J. Bacteriol. 182: 5706-5714.
57. MOORE, T., P. MCGLYNN, H. P. NGO, G. J. SHARPLES and R. G. LLOYD, 2003 The RdgC protein of Escherichia coli binds DNA and counters a toxic effect of RecFOR in strains lacking the replication restart protein PriA. EMBO J. 22: 735-745.
58. MORIMATSU, K., and S. C. KOWALCZYKOWSKI, 2003 RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol. Cell 11: 1337-1347.
59. NURSE, P., J. LIU and K. J. MARIANS, 1999 Two modes of PriA binding to DNA. J. Biol. Chem. 274: 25026-25032.
60. RAGHUNATHAN, S., A. G. KOZLOV, T. M. LOHMAN and G. WAKSMAN, 2000 Structure of the DNA binding domain of E. coli SSB bound to ssDNA. Nat. Struct. Biol. 7: 648-652.
61. REYES-LAMOTHE, R., X. WANG and D. SHERRATT, 2008 Escherichia coli and its chromosome. Trends Microbiol. 16: 238-245.
62. RUDOLPH, C. J., P. DHILLON, T. MOORE and R. G. LLOYD, 2007 Avoiding and resolving conflicts between DNA replication and transcription. DNA Repair 6: 981-993.
63. RUDOLPH, C. J., A. L. UPTON and R. G. LLOYD, 2008 Maintaining replication fork integrity in UV-irradiated Escherichia coli cells. DNA Repair (Amst.) 7: 1589-1602.
64. RUDOLPH, C. J., A. L. UPTON, L. HARRIS and R. G. LLOYD, 2009a Pathological replication in cells lacking RecG DNA translocase. Mol. Microbiol. 73: 352-366.
65. RUDOLPH, C. J., A. L. UPTON and R. G. LLOYD, 2009b Replication fork collisions cause pathological chromosomal amplification in cells lacking RecG DNA translocase. Mol. Microbiol. 74: 940-955.
66. RYDER, L., M. C. WHITBY and R. G. LLOYD, 1994 Mutation of recF, recJ, recO, recQ, or recR improves Hfr recombination in resolvase-deficient ruv recG strains of Escherichia coli. J. Bacteriol. 176: 1570-1577.
67. SAVVIDES, S. N., S. RAGHUNATHAN, K. FUTTERER, A. G. KOZLOV, T. M. LOHMAN et al., 2004 The C-terminal domain of full-length E. coli SSB is disordered even when bound to DNA. Protein Sci. 13: 1942-1947.
68. SHARPLES, G. J., S. C. CHAN, A. A. MAHDI, M. C. WHITBY and R. G. LLOYD, 1994 Processing of intermediates in recombination and DNA repair: identification of a new endonuclease that specifically cleaves Holliday junctions. EMBO J. 13: 6133-6142.
69. SHEREDA, R. D., D. A. BERNSTEIN and J. L. KECK, 2007 A central role for SSB in Escherichia coli RecQ DNA helicase function. J. Biol. Chem. 282: 19247-19258.
70. SHEREDA, R. D., A. G. KOZLOV, T. M. LOHMAN, M. M. COX and J. L. KECK, 2008 SSB as an organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol. 43: 289-318.
71. SINGLETON, M. R., S. SCAIFE and D. B. WIGLEY, 2001 Structural analysis of DNA replication fork reversal by RecG. Cell 107: 79-89.
72. SINGLETON, M. R., M. S. DILLINGHAM, M. GAUDIER, S. C. KOWALCZYKOWSKI and D. B. WIGLEY, 2004 Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks. Nature 432: 187-193.
73. SMITH, G. R., 1991 Conjugational recombination in E. coli: myths and mechanisms. Cell 64: 19-27.
74. TANAKA, T., C. TANIYAMA, K. ARAI and H. MASAI, 2003 ATPase/helicase motif mutants of Escherichia coli PriA protein essential for recombination-dependent DNA replication. Genes Cells 8: 251-261. (Pubitemid 36511706)
75. TRAUTINGER, B. W., R. P. JAKTAJI, E. RUSAKOVA and R. G. LLOYD, 2005 RNA polymerase modulators and DNA repair activities resolve conflicts between DNA replication and transcription. Mol. Cell 19: 247-258.
76. UMEZU, K., N. CHI and R. D. KOLODNER, 1993 Biochemical interaction of the Escherichia coli RecF, RecO, and RecR proteins with RecA protein and single-stranded DNA binding protein. Proc. Natl. Acad. Sci. USA 90: 3875-3879.
77. VAN GOOL, A. J., R. SHAH, C. MEZARD and S. C. WEST, 1998 Functional interactions between the Holliday junction resolvase and the branch migration motor of Escherichia coli. EMBO J. 17: 1838-1845.
78. 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.
79. VINCENT, S. D., A. A. MAHDI and R. G. LLOYD, 1996 The RecG branch migration protein of Escherichia coli dissociates R-loops. J. Mol. Biol. 264: 713-721.
80. WARDROPE, L., E. OKELY and D. LEACH, 2009 Resolution of joint molecules by RuvABC and RecG following cleavage of the Escherichia coli chromosome by EcoKI. PLoS One 4: e6542.
81. WHITBY, M. C., and R. G. LLOYD, 1995 Branch migration of three-strand recombination intermediates by RecG, a possible pathway for securing exchanges initiated by 3′-tailed duplex DNA. EMBO J. 14: 3302-3310.
82. WHITBY, M. C., L. RYDER and R. G. LLOYD, 1993 Reverse branch migration of Holliday junctions by RecG protein: a new mechanism for resolution of intermediates in recombination and DNA repair. Cell 75: 341-350.
83. ZAVITZ, K. H., and K. J. MARIANS, 1992 ATPase-deficient mutants of the Escherichia coli DNA replication protein PriA are capable of catalyzing the assembly of active primosomes. J. Biol. Chem. 267: 6933-6940.