Differential requirements of two recA mutants for constitutive SOS expression in Escherichia coli K-12

PLoS ONE

Volumn 3, Issue 12, 2008, Pages

  Long, Jarukit Edward ^a   Renzette, Nicholas ^a   Centore, Richard C ^a   Sandler, Steven J ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; ESCHERICHIA COLI PROTEIN; EXODEOXYRIBONUCLEASE V; MUTANT PROTEIN; PROTEIN DINL; PROTEIN RECX; PROTEIN XTHA; RECA PROTEIN; RECF PROTEIN; SOS PROTEIN; UNCLASSIFIED DRUG; DINI PROTEIN, E COLI; RECX PROTEIN, E COLI;

ARTICLE; BACTERIAL GENETICS; BACTERIUM CULTURE; BACTERIUM MUTANT; CELL GROWTH; CELL POPULATION; CONTROLLED STUDY; CULTURE MEDIUM; ESCHERICHIA COLI K 12; FLUORESCENCE; GENETIC ANALYSIS; GROWTH CURVE; MOLECULAR MECHANICS; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REPORTER GENE; BACTERIAL GENE; BIOLOGICAL MODEL; CLASSIFICATION; DNA REPAIR; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY;

ESCHERICHIA COLI K12;

ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MODELS, BIOLOGICAL; MUTATION; REC A RECOMBINASES; SOS RESPONSE (GENETICS);

EID: 58149345832     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004100     Document Type: Article

References (76)

1. Ogawa T, Yu X, Shinohara A, Egelman EH (1993) Similarity of the Yeast RAD51 filament to the bacterial RecA filament. Science 259: 1896-1899.
2. Courcelle J, Donaldson JR, Chow KH, Courcelle CT (2003) DNA damage-induced replication fork regression and processing in Escherichia coli. Science 299: 1064-1067.
3. Hishida T, Han YW, Shibata T, Kubota Y, Ishino Y, et al. (2004) Role of the Escherichia coli RecQ DNA helicase in SOS signaling and genome stabilization at stalled replication forks. Genes and Development 18: 1886-1897.
4. Liberi G, Maffioletti G, Lucca C, Chiolo I, Baryshnikova A, et al. (2005) Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes & Development 19: 339-350.
5. Veaute X, Delmas S, Selva M, Jeusset J, Le Cam E, et al. (2005) UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli. EMBO Journal 24: 180-189.
6. Lee BI, Kim KH, Park SJ, Eom SH, Song HK, et al. (2004) Ring-shaped architecture of RecR: implications for its role in homologous recombinational DNA repair. EMBO Journal 23: 2029-2038.
7. Sung P (1997) Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombination. Genes and Development 11: 1111-1121.
8. Sung P (1997) Function of the yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. Journal of Biological Chemistry 272: 28194-28197.
9. Fu Y, Pastushok L, Xiao W (2008) DNA damage-induced gene expression in Saccharomyces cerevisiae. FEMS Microbiology Reviews. pp 1-19.
10. Scully R, Xie A, Nagaraju G (2004) Molecular functions of BRCA1 in the DNA damage response. Cancer biology & therapy 3: 521-527.
11. Jasin M (2002) Homologous repair of DNA damage and tumorigenesis: the BRCA connection. Oncogene 21: 8981-8993.
12. Venkitaraman AR (2001) Functions of BRCA1 and BRCA2 in the biological response to DNA damage. Journal of Cell Science 114: 3591-3598.
13. Little JW, Mount DW (1982) The SOS regulatory system of Escherichia coli. Cell 29: 11-22.
14. Courcelle J, Khodursky A, Peter B, Brown PO, Hanawalt PC (2001) Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158: 41-64.
15. Beaber JW, Hochhut B, Waldor MK (2004) SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427: 72-74.
16. Kelley WL (2006) Lex marks the spot: the virulent side of SOS and a closer look at the LexA regulon. Molecular Microbiology 62: 1228-1238.
17. Blazquez J, Gomez-Gomez JM, Oliver A, Juan C, Kapur V, et al. (2006) PBP3 inhibition elicits adaptive responses in Pseudomonas aeruginosa. Molecular microbiology 62: 84-99.
18. Lopez E, Elez M, Matic I, Blazquez J (2007) Antibiotic-mediated recombination: ciprofloxacin stimulates SOS-independent recombination of divergent sequences in Escherichia coli. Molecular microbiology 64: 83-93.
19. Miller C, Thomsen LE, Gaggero C, Mosseri R, Ingmer H, et al. (2004) SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305: 1629-1631.
20. Cox MM, Goodman MF, Kreuzer KN, Sherratt DJ, Sandler SJ, et al. (2000) The importance of repairing stalled replication forks. Nature 404: 37-41.
21. Lusetti SL, Cox MM (2002) The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annual Reviews of Biochemistry 71: 71-100.
22. McCool JD, Long E, Petrosino JF, Sandler HA, Rosenberg SM, et al. (2004) Measurement of SOS expression in individual Escherichia coli K-12 cells using fluorescence microscopy. Molecular Microbiology 53: 1343-1357.
23. Pennington JM, Rosenberg SM (2007) Spontaneous DNA breakage in single living Escherichia coli cells. Nature Genetics 39: 797-802.
24. Renzette N, Gumlaw N, Nordman JT, Krieger M, Yeh SP, et al. (2005) Localization of RecA in Escherichia coli K-12 using RecA-GFP. Molecular Microbiology 57: 1074-1085.
25. Steiner WW, Kuempel PL (1998) Sister chromatid exchange frequencies in Escherichia coli analyzed by recombination at the dif resolvase site. Journal of Bacteriology 180: 6269-6275.
26. Gruenig MC, Renzette N, long E, Chitteni-Pattu S, Inman RB, et al. (2008) RecA-Mediated SOS induction requires an extended filament conformation but no ATP hydrolysis. Molecular Microbiology 69: 1165-1179.
27. McGrew DA, Knight KL (2003) Molecular design and functional organization of the RecA protein. Critical Reviews in Biochemistry and Molecular Biology 38: 385-432.
28. Kirby EP, Jacob F, Goldthwait DA (1967) Prophage induction and filament formation in a mutant strain of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 58: 1903-1910.
29. Bi E, Lutkenhaus J (1990) Analysis of ftsZ mutations that confer resistance to the cell division inhibitor SulA (SfiA). Journal of Bacteriology 172: 5602-5609.
30. Knight KL, Aoki KH, Ujita EL, McEntee K (1984) Identification of the amino acid substitutions in two mutant forms of the recA protein from Escherichia coli: recA441 and recA629. The Journal of Biological Chemistry 259: 11279-11283.
31. Witkin EM, McCall JO, Volkert MR, Wermundsen IE (1982) Constitutive expression of SOS functions and modulation of mutagenesis resulting from resolution of genetic instability at or near the recA locus of Escherichia coli. Molecular and General Genetics 185: 43-50.
32. Tessman ES, Peterson P (1985) Plaque color method for rapid isolation of novel recA mutants of Escherichia coli K-12: new classes of protease-constitutive recA mutants. Journal of Bacteriology 163: 677-687.
33. Chen Z, Yang H, Pavletich NP (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453: 489-484.
34. Eggler AL, Lusetti SL, Cox MM (2003) The C terminus of the Escherichia coli RecA protein modulates the DNA binding competition with single-stranded DNA-binding protein. Journal of Biological Chemistry 278: 16389-16396.
35. Lavery PE, Kowalczykowski SC (1990) Properties of recA441 protein-catalyzed DNA strand exchange can be attributed to an enhanced ability to compete with SSB protein. Journal of Biological Chemistry 265: 4004-4010.
36. De Zutter JK, Forget AL, Logan KM, Knight KL (2001) Phe217 regulates the transfer of allosteric information across the subunit interface of the RecA protein filament. Structure (Camb) 9: 47-55.
37. Uhlin BE, Clark AJ (1981) Overproduction of the Escherichia coli recA protein without stimulation of its proteolytic activity. Journal of Bacteriology 148: 386-390.
38. Cox MM (2001) Recombinational DNA repair of damaged replication forks in Escherichia coli: questions. Annual Reviews of Genetics 35: 53-82.
39. Kowalczykowski SC (2000) Initiation of genetic recombination and recombination-dependent replication. Trends in Biochemical Sciences 25: 156-165.
40. Bork JM, Cox MM, Inman RB (2001) The RecOR proteins modulate RecA protein function at 5′ ends of single- stranded DNA. EMBO Journal 20: 7313-7322.
41. Hobbs MD, Sakai A, Cox MM (2007) SSB protein limits RecOR binding onto single-stranded DNA. The Journal of Biological Chemistry 282: 11058-11067.
42. Webb BL, Cox MM, Inman RB (1997) Recombinational DNA repair: the RecF and RecR proteins limit the extension of RecA filaments beyond single-strand DNA gaps. Cell 91: 347-356.
43. Cox MM (2007) Regulation of bacterial RecA protein function. Critical Reviews in Biochemistry and Molecular Biology 42: 41-63.
44. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, et al. (2006) DNA Repair and Mutagenesis. Washington, D.C.: ASM Press.
45. Yasuda T, Morimatsu K, Horii T, Nagata T, Ohmori H (1998) Inhibition of Escherichia coli RecA coprotease activities by DinI. EMBO Journal 17: 3207-3216.
46. Lusetti SL, Voloshin ON, Inman RB, Camerini-Otero RD, Cox MM (2004) The DinI protein stabilizes RecA protein filaments. Journal of Biological Chemistry 279: 30037-30046.
47. Renzette N, Gumlaw N, Sandler SJ (2007) DinI and RecX modulate RecA-DNA structures in Escherichia coli K-12. Molecular Microbiology 63: 103-115.
48. Yasuda T, Morimatsu K, Kato R, Usukura J, Takahashi M, et al. (2001) Physical interactions between DinI and RecA nucleoprotein filament for the regulation of SOS mutagenesis. EMBO Journal 20: 1192-1202.
49. Ramirez BE, Voloshin ON, Camerini-Otero RD, Bax A (2000) Solution structure of DinI provides insight into its mode of RecA inactivation. Protein Science 9: 2161-2169.
50. Yoshimasu M, Aihara H, Ito Y, Rajesh S, Ishibe S, et al. (2003) An NMR study on the interaction of Escherichia coli DinI with RecA-ssDNA complexes. Nucleic Acids Research 31: 1735-1743.
51. Bork JM, Cox MM, Inman RB (2001) RecA protein filaments disassemble in the 5′ to 3′ direction on single- stranded DNA. Journal of Biological Chemistry 276: 45740-45743.
52. Drees JC, Lusetti SL, Chitteni-Pattu S, Inman RB, Cox MM (2004) A RecA filament capping mechanism for RecX protein. Molecular Cell 15: 789-798.
53. Ragone S, Maman JD, Furnham N, Pellegrini L (2008) Structural basis for inhibition of homologous recombination by the RecX protein. The EMBO Journal 27: 2259-2269.
54. Lusetti SL, Hobbs MD, Stohl EA, Chitteni-Pattu S, Inman RB, et al. (2006) The RecF protein antagonizes RecX function via direct interaction. Molecular Cell 21: 41-50.
55. Pages V, Koffel-Schwartz N, Fuchs RP (2003) recX, a new SOS gene that is cotranscribed with the recA gene in Escherichia coli. DNA Repair (Amst) 2: 273-284.
56. Centore RC, Sandler SJ (2007) UvrD limits the number and intensities of RecA-green fluorescent protein structures in Escherichia coli K-12. Journal of Bacteriology 189: 2915-2920.
57. Flores MJ, Sanchez N, Michel B (2005) A fork-clearing role for UvrD. Molecular Microbiology 57: 1664-1675.
58. Lestini R, Michel B (2008) UvrD and UvrD252 counteract RecQ, RecJ, and RecFOR in a rep mutant of Escherichia coli. Journal of Bacteriology 190: 5995-6001.
59. Centore RC, Lestini R, Sandler SJ (2008) XthA (Exonuclease III) regulates loading of RecA onto DNA substrates in log phase Escherichia coli cells. Molecular Microbiology 67: 88-101.
60. Hegde S, Sandler SJ, Clark AJ, Madiraju MV (1995) recO and recR mutations delay induction of the SOS response in Escherichia coli . Molecular and General Genetics 246: 254-258.
61. Drees JC, Lusetti SL, Cox MM (2004) Inhibition of RecA protein by the Escherichia coli RecX protein: modulation by the RecA C terminus and filament functional state. Journal of Biological Chemistry 279: 52991-52997.
62. Ivancic-Bace I, Peharec P, Moslavac S, Skrobot N, Salaj-Smic E, et al. (2003) RecFOR function is required for DNA repair and recombination in a RecA loading-deficient recB mutant of Escherichia coli. Genetics 163: 485-494.
63. O'Reilly EK, Kreuzer KN (2004) Isolation of SOS constitutive mutants of Escherichia coli. Journal of Bacteriology 186: 7149-7160.
64. Uzest M, Ehrlich SD, Michel B (1995) Lethality of rep recB and rep recC double mutants of Escherichia coli. Molecular Microbiology 17: 1177-1188.
65. Seigneur M, Bidnenko V, Ehrlich SD, Michel B (1998) RuvAB acts at arrested replication forks. Cell 95: 419-430.
66. Mirshad JK, Kowalczykowski SC (2003) Biochemical characterization of a mutant RecA protein altered in DNA-binding loop 1. Biochemistry 42: 5945-5954.
67. Willetts NS, Clark AJ, Low B (1969) Genetic location of certain mutations conferring recombination deficiency in Escherichia coli. Journal of Bacteriology 97: 244-249.
68. Clark AJ, Margulies AD (1965) Isolation and characterization of recombination deficient mutants of Escherichia coli K-12. Proceedings of the National Academy of Sciences, USA 53: 451-459.
69. Sandler SJ, Samra HS, Clark AJ (1996) Differential suppression of priA2::kan phenotypes in Escherichia coli K-12 by mutations in priA, lexA, and dnaC. Genetics 143: 5-13.
70. Levin PA (2002) Light Microscopy Techniques for Bacterial Cell Biology. In: Sansonetti P, Zychlinsky A, eds. Methods in Microbiology: Molecular Cellular Microbiology. London: Academic Press Ltd. pp 115-132.
71. Sandler SJ (1994) Studies on the mechanism of reduction of UV-inducible sulAp expression by recF overexpression in Escherichia coli K-12. Molecular and General Genetics 245: 741-749.
72. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Molecular Systems Biology 2: 2006 0008.
73. Konrad EB (1977) Method for the isolation of Escherichia coli mutants with enhanced recombination between chromosomal duplications. Journal of Bacteriology 130: 167-172.
74. Zieg J, Kushner SR (1977) Analysis of genetic recombination between two partially deleted lactose operons of Escherichia coli K-12. Journal of Bacteriology 131: 123-132.
75. Huang LC, Wood EA, Cox MM (1997) Convenient and reversible site-specific targeting of exogenous DNA into a bacterial chromosome by use of the FLP recombinase: the FLIRT system. Journal of Bacteriology 179: 6076-6083.
76. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proceedings of the National Academy of Science USA 97: 6640-6645.