Physical analyses of E. coli Heteroduplex recombination products in Vivo: On the prevalence of 5∥ime and 3∥ime patches

PLoS ONE

Volumn 2, Issue 11, 2007, Pages

  Gumbiner Russo, Laura M ^a   Rosenberg, Susan M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; EXODEOXYRIBONUCLEASE V; HETERODUPLEX; PROTEIN ORF; RAP PROTEIN; PRIMER DNA;

ARTICLE; BACTERIAL STRAIN; BACTERIOPHAGE LAMBDA; CONTROLLED STUDY; DNA ISOLATION; DNA REPAIR; DNA REPLICATION; DNA SEQUENCE; DNA STRAND; DOUBLE STRANDED DNA BREAK; ESCHERICHIA COLI; GENE FUNCTION; HETERODUPLEX ANALYSIS; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; IN VIVO STUDY; NONHUMAN; SEQUENCE ANALYSIS; SOUTHERN BLOTTING; GENETIC RECOMBINATION; GENETICS; NUCLEOTIDE SEQUENCE;

ENTEROBACTERIA PHAGE LAMBDA; ESCHERICHIA COLI;

BASE SEQUENCE; DNA PRIMERS; ESCHERICHIA COLI; NUCLEIC ACID HETERODUPLEXES; RECOMBINATION, GENETIC;

EID: 44249089250     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001242     Document Type: Article

References (113)

1. Kowalczykowski SC, Dixon DA, Eggleston AK, Lauder SD, Rehrauer WM (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev 58: 401-465.
2. Myers RS, Stahl FW (1994) X and RecBCD enzyme of Escherichia coli. Annu Rev Genet 28: 49-70.
3. Palas KM, Kushner SR (1990) Biochemical and physical characterization of exonuclease V from Escherichia coli. Comparison of the catalytic activities of the RecBC and RecBCD enzymes. J Biol Chem 265: 3447-3454.
4. Taylor AF, Smith GR (1985) Substrate specificity of the DNA unwinding activity of the RecBC enzyme of Escherichia coli. J Mol Biol 185: 431-443.
5. Ganesan S, Smith GR (1993) Strand-specific binding to duplex DNA ends by the subunits of the Escherichia coli RecBCD enzyme. J Mol Biol 229: 67-78.
6. Smith GR, Amundsen SK, Chaudhury AM, Cheng KC, Ponticelli AS, et al. (1984) Roles of RecBC enzyme and Chi sites in homologous recombination. Cold Spring Harbor Symp Quant Biol 49: 485-495.
7. Smith GR, Schultz DW, Taylor AF, Triman K (1981) Chi sites, RecBC enzyme, and generalized recombination. Stadler Genet Symp 13: 25-37.
8. Kowalczykowski SC (2000) Initiation of genetic recombination and recombination-dependent replication. Trends Biochem Sci 25: 156-165.
9. Rosenberg.SM (1987) Chi stimulated patches are heteroduplex, with recombinant information on the phage λ r chain. Cell. 48: 855-865.
10. Rosenberg SM (1988) Chairt-bias of Escherichia coli Rec-mediated λ patch recombinants is independent of the orientation of λ cos. Genetics 120: 7-21.
11. Hagemann AT, Rosenberg SM (1991) Chain bias in Chi-stimulated heteroduplex patches in the λ ren gene is determined by the orientation of λ cos. Genetics 129: 611-621.
12. Razavy H, Szigety SK, Rosenberg SM (1996) Evidence for both 3′ and 5′ single-strand DNA ends in intermediates in Chi-stimulated recombination in vivo. Genetics 142: 333-339.
13. Miesel L, Roth JR (1996) Evidence that SbcB and RecF pathway functions contribute to RecBCD-dependent transductional recombination. J Bacteriol 178: 3146-3155.
14. Dutreix M, Rao BJ, Radding CM (1991) The effects on strand exchange of 5′ versus 3′ ends of single-stranded DNA in RecA Nucleoprotein filaments. J Mol Biol 219: 645-654.
15. McIlwraith MJ, West SC (2001) The efficiency of strand invasion by Escherichia coli RecA is dependent upon the length and polarity of ssDNA taus. J Mol Biol 305: 23-31.
16. Register JC 3rd, Griffith J (1985) The direction of RecA protein assembly onto single strand DNA is the same as the direction of strand assimilation during strand exchange. J Biol Chem 260: 12308-12312.
17. Konforti BB, Davis RW (1990) The preference for a 3′ homologous end is intrinsic to RecA-promoted strand exchange. J Biol Chem 265: 6916-6920.
18. Konforti BB, Davis RW (1987) 3′ homologous free ends are required for stable joint molecule formation by the RecA and single-stranded binding proteins of Escherichia coli Proc Natl Acad Sci U S A 84: 690-694.
19. Shan Q, Bork JM, Webb BL, Inman RB, Cox MM (1997) RecA protein filaments: end-dependent disassociation from asDNA and stabilization by RecO and RecR proteins. J Mol Biol 265: 519-540.
20. 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.
21. Rosenberg SM, Hastings PJ (1991) The split-end model for homologous recombination at double-strand breaks and at Chi. Biochimie 73: 385-397.
22. -), and RecF pathways. Genetics 128: 7-22.
23. Holbeck SL, Smith GR (1992) Chi enhances heteroduplex DNA levels during recombination. Genetics 132: 879-891.
24. White RL, Fox MS (1974) On the molecular basis of high negative interference. Proc, Natl Acad Sci U S A 71: 1544-1548.
25. Nag DK, Peres TD (1990) Genetic evidence for preferential strand transfer during meiotic recombination in yeast. Genetics 125: 753-761.
26. Sawitzke JA, Stahl FW (1992) Phage λ has an analog of the Escherichia coli recO, recR and recF genes. Genetics 130: 7-16.
27. Sharples GJ, Curtis FA, McGlynn P, Bolt EL (2004) Holliday junction binding and resolution by the Rap structure-specific endonuclease of phage lambda. J Mol Biol 340: 739-751.
28. Nagamine CM, Chan Y, Lau YF (1989) A PCR artifact: generation of heteroduplexes. Am J Hum Genet 45: 337-339.
29. Silberstein Z, Shalit M, Cohen A (1993) Heteroduplex strand-specificity in restriction-stimulated recombination by the RecE pathway of Escherichia coli. Genetics 133: 439-448.
30. Murphy KC (1991) Lambda Gam protein inhibits the helicase and Chi-sumutated recombination activities of Escherichia coli RecbCD enzyme. J Bacteriol 173: 5808-5821.
31. Wold MS, Mallory JB, Roberts JD, LeBowitz JH, McMacken R (1982) Initiation of bacteriophage lambda DNA replication in vitro with purified lambda replication proteins, Proc Natl Acad Sci U S A 79: 6176-6180.
32. Cohen A, Clark AJ (1986) Synthesis of linear plasmid multimers in Escherichia coli K-12. J Bacteriol 167: 327-335.
33. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
34. Martinez-Morales F, Borges AC, Martinez A, Shanmugram KT, Ingram LO (1999) Chromosomal integration of heterologous DNA in Escherichia coli with precise removal of markers and replicons used during construction. J Bacteriol 181: 7143-7148.
35. Arber W, Enquist L, Hohn B, Murray NE, Murray K (1983), Experimental Methods for use with Lambda. In: Hendrix RW, Roberts JW, Stahl FW, Weisberg RW, eds. Lambda II Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. pp 433-466.
36. Miller JH (1992) A Short Course in Bacterial Genetics. Cold Spring Harbor, N. Y.: Cold Spring Harbor Laboratory Press.
37. Rosenberg SM, Stahl MM, Kobayashi I, Stahl FW (1985) Improved in vitro packaging of coliphage lambda DNA: a one-strain system free from endogenous phage. Gene 38: 165-175.
38. Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, N. Y.: Cold Spring Harbor Laboratory Press.
39. Jordan H (1997) Gel Loading Buffer Affects Electrophoresis Results. Focus 19: 60-61.
40. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci U S A 81: 1991-1995.
41. Mason JC, Steinberg R, Lidington EA, Kinderlerer AR, Ohba M, et al. (2004) Decay-accelerating factor induction on vascular endothelium by vascular endothelial growth factor (VEGF) is mediated via a VEGF receptor-2 (VEGF-R2)- and protein kinase C-alpha/epsilon (PKCadpha/ epsilon)-dependent cytoprotective signaling pathway and is inhibited by cyclosporin A. J Biol Chem 279: 41611-41618.
42. Shiao T, Fond A, Deng B, Wehling-Henricks M, Adams ME, et al. (2004) Defects in neuromuscular junction structure in dystrophic muscle are corrected by expression of a NOS transgene in dystrophin-deficient muscles, but not in muscles lacking alpha- and beta 1 -syntrophins. Hum Mol Genet 13: 1873-1884.
43. Diamonti AJ, Guy PM, Ivanof C, Wong K, Sweeney C, et al. (2002) An RBCC protein implicated in maintenance of steady-state neuregulin receptor levels. Proc Natl Acad Sci U S A 99: 2866-2871.
44. Pearson RK, Fox MS (1988) Effects of DNA heterologies on bacteriophage lambda recombination. Genetics 118: 13-19.
45. Parker BO, Marinus MG (1992) Repair of DNA heteraduplexes containing small heterolognus sequences in Escherichia coli Proc Natld Acad Sci U S A 89: 1730-1734.
46. Carraway M, Marinus MG (1993) Repair of heteroduplex DNA molecules with multibase loops in Escherichia coli. J Bacteriol 176: 3972-3980.
47. Wang J, Chen R, Julin DA (2000) A single nuclease active site of the Escherichia coli RecBCD enzyme catalyzes single-stranded DNA degradation in both directions. J Biol Chem 275: 507-513.
48. Lusetti SL, Cox MM (2002) The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu Rev Biochem 71: 71-100.
49. Taylor AF (1988) RecBCD enzyme of Escherichia coli. In: Kucherlapati R, Smith GR, eds. Genetic Recombination. Washington D. C.: Am. Soc. Microbiol. pp 231-263.
50. Maxwell KL, Reed P, Zhang RG, Beasley S, Walmsley AR, et al (2005) Functional similarities between phage lambda Orf and Escherichia coli RecFOR in initiation of genetic exchange. Proc Natl Acad Sci U S A 102: 11260-11265.
51. Sawitzke JA, Stahl FW (1994) The phage lambda orf gene encodes a trans-acting factor that suppresses Escherichia coli recO, recR, and recF mutations for recombination of lambda but not of E. coli. J Bacteriol 176: 6730-6737.
52. Sawitzke JA, Stahl FW (1997) Roles for lambda Orf and Escherichia coli RecO, RecR and RecF in lambda recombination. Genetics 147: 357-369.
53. Morimatsu K, Kowalczykowski SC (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.
54. Poteete AR, Fenton AC, Wang HR (2002) Recombination-promoting activity of the bacteriophage lambda Rap protein in Escherichia coli K-12. J Bacteriol 184: 4626-4629.
55. Sharples GJ, Corbett LM, Graham IR (1998) λ Rap protein is a structure-specific endonuclease involved in phage recombination. Proc Natl Acad Sci U S A 95: 13507-13512.
56. Hollifield WC, Kaplan EN, Huang H (1987) Efficient RecABC-dependent, homologous recombination between coliphage lambda and plasmids requires a phage ninR region gene. Mol Gen Genet 210: 248-255.
57. Bolt EL, Lloyd RG (2002) Substrate specificity of RusA resolvase reveals the DNA structures targeted by RuvAB and RecG in vivo. Mol Cell 10: 187-198.
58. Saintigny Y, Makienko K, Swanson C, Emond MJ, Monnat RJ Jr (2002) Homologous recombination resolution defect in Werner syndrome. Mol Cell Biol 22: 6971-6978.
59. Doe CL, Whitby MC (2004) The involvement of Srs2 in post-replication repair and homologous recombination in fission yeast. Nucleic Acids Res 32: 1480-1491.
60. Stahl FW, Shurvinton CE, Thomason LC, Hill S, Stahl MN (1995) On the clustered exchanges of the RecBCD pathway operating on phage λ. Genetics 139: 1107-1121.
61. Dixon DA, Kowalczykowski SC (1993) The recombination hotspot, Chi, is a regulatory sequence that acts by attenuating the nuclease activity of the Escherichia coli recBCD enzyme. Cell 73: 87-96.
62. Anderson DG, Kowalczykowski SC (1997) The recombination hot spot chi is a regulatory element that switches the polarity of DNA degradation by the RecBCD enzyme. Genes Dev 11: 571-581.
63. Anderson DG, Churchill JJ, Kowalczykowski SC (1997) Chi-activated RecBCD enzyme possesses 5′->3′ nucleolytic activity, but RecBC enzyme does not: evidence suggesting that the alteration induced by Chi is not simply ejection of the RecD subunit. Genes Cells 2: 117-128.
64. Dabert PS, Ehrlich SD, Gruss A (1992) Chi sequence protects against RecBCD degradation of DNA in vivo. Proc Natl Acad Sci U S A 89: 12073-12077.
65. Myers RM, Kuzminov A, Stahl FW (1995) The recombination hot spot χ activates RecBCD recombination by converting Escherichia coli to a recD mutant phenocopy. Proc Natl Acad Sci USA 92: 6244-6248.
66. Korangy F, Julin DA (1993) Kinetics and processivity of ATP hydrolysis and DNA unwinding by the RecBC enzyme from Escherichia coli. Biochemistry 32: 4873-4880.
67. Korangy F, Julin DA (1994) Efficiency of ATP hydrolysis and DNA unwinding by the RecBC enzyme from Escherichia coli. Biochemistry 33: 9552-9560.
68. Rinken R, Thoms B, Wackernagel W (1992) Evidence that recBC-dependent degradation of duplex DNA in Escherichia coli recD mutants involves DNA unwinding. J Bacteriol 174: 5424-5429.
69. Singleton MR, Dillingham MS, Gaudier M, Kowalczykowski SC, Wigley DB (2004) Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks. Nature 432: 187-193.
70. Lloyd RG, Sharples GJ (1993) Processing of recombination intermediates by the RecG and RuvAB proteins of Escherichia coli. Nucleic Acids Res 21: 1719-1725.
71. McGlynn P, Lloyd RG (1999) RecG helicase activity at three- and four-strand DNA structures. Nucleic Acids Res 27: 3049-3056.
72. West SC (1997) Processing of recombination intermediates by the RuvABC proteins. Annu Rev Genet 31: 213-244.
73. Whitby MC, Ryder L, Lloyd RG (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.
74. Harris RS, Ross KJ, Rosenberg SM (1996) Opposing roles of the Holliday junction processing systems of Escherichia coli in recombination-dependent adaptive mutation. Genetics 142: 681-691.
75. Thaler DS, Stahl NW, Stahl FW (1987) Tests of the double-strand-break repair model for red-mediated recombination of phage lambda and plasmid lambda dv. Genetics 116: 501-511.
76. Lopez CR, Yang S, Deibler RW, Ray SA, Pennington JM, et al. (2005) A role for topoisomerase III in a recombination pathway alternative to RuvABC. Mol Microbiol 58: 80-101.
77. Motamedi M, Szigety SK, Rosenberg SM (1999) Double-strand break-repair in E. coli: direct physical evidence for a replicational mechanism in vivo. Genes & Dev 13: 2889-2903.
78. Magner DB (2006) On Replicative and Break-Join Resolution, and RecQ-Promoted Accumulation of Recombination Intermediates in vivo. PhD Thesis.
79. Friedman-Ohana R, Cohen A (1998) Heteroduplex joint formation in Escherichia coli recombination is initiated by pairing of a 3′-ending strand. Proc Natl Acad Sci U S A 95: 6909-6914.
80. Lichten M, Goyon C, Schultes NP, Treco D, Szostak JW, et al. (1990) Detection of heteroduplex DNA molecules among the products of Saccharomyces cerevisiae meiosis. Proc Natl Acad Sci USA 87: 7653-7657.
81. Dower NA, Stahl FW (1981) χ activity during transduction-associated recombination. Proc Natl Acad Sci U S A 78: 7033-7037.
82. Kuzminov A (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev 63: 751-813.
83. Lloyd RG, Low KB (1996) Homologous recombination. In: Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, et al. eds. Escherichia coli and Salmonella: cellular and molecular biology. 2nd ed. Washington, D. C.: ASM Press. pp 2236-2255.
84. Smith GR, Stahl FW (1985) Homologous recombination promoted by Chi sites and RecBC enzyme of Escherichia coli. Bioessays 2: 244-249.
85. Thaler DS, Sampson E, Siddiqi I, Rosenberg SM, Thomason LC, et al. (1989) Recombination of bacteriophage λ in recD mutants of Escherichia roli. Genome 31: 53-67.
86. Koppen A, Krobitsch S, Thoms B, Wackernagel W (1995) Interaction with the recombination hot spot chi in vivo converts the RecBCD enzyme of Escherichia coli into a chi-independent recombinase by inactivation of the RecD subunit. Proc Natl Acad Sci U S A 92: 6249-6253.
87. Biek DP, Cohen SN (1986) Identification and characterization of recD, a gene affecting plasmid maintenance and recombination in Escherichia coli. J Bacteriol 167: 594-603.
88. Lloyd RG (1991) Conjugational recombination in resolvase-deficient nwC mutants of Escherichia coli depends on recG. J Bacteriol 173: 5114-5118.
89. Paques F, Haber JE (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63: 349-404.
90. Gloor GB, Nassif NA, Johnson-Schlitz DM, Preston CR, Engels WR (1991) Targeted gene replacement in Drosophila via P element-induced gap repair, Science 253: 1110-1117.
91. Nassif N, Penney J, Pal S, Engels WR, Gloor GB (1994) Efficient copying of nonhomologous sequences from ectopic sites via P element-induced gap repair. Mol Cell Biol 14: 1613-1625.
92. Allers T, Lichten M (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47-57.
93. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW (1983) The double-strand break repair model for recombination. Cell 33: 25-33.
94. Stitt BL, Mosig G (1989) Impaired expression of certain prereplicative bacteriophage T4 genes explains impaired T4 DNA synthesis in Escherichia coli rho (nusD) mutants. J Bacteriol 171: 3872-3880.
95. Zahradka K, Slade D, Bailone A, Sommer S, Averbeck D, et al (2006) Reassembly of shattered chromosomes in Deinoccus radiodurans. Nature 443: 569-573.
96. Leung W-Y, Malkova A, Haber JE (1997) Gene targeting by linear duplex DNA frequently occurs by assimilation of a single strand that is subject to preferential-mismatch correction. Proc Natl Acad Sci U S A 94: 6851-6856.
97. Ellis HM, Yu D, DiTizio T, Court DL (2001) High efficiency mutagenesis, repair, and engineering of chromosomal DNA using single-stranded oligonucleotides. Proc Natl Acad Sci U S A 98: 6742-6746.
98. Court DL, Sawitzke JA, Thomason LC (2002) Genetic engineering using homologous recombination. Annu Rev Genet 36: 361-388.
99. Storici F, Durham CL, Gordenin DA, Resnick MA (2003) Chromosomal site-specific double-strand breaks are efficiently targeted for repair by oligonucleotides in yeast. Proc Natl Acad Sci U S A 100: 14994-14999.
100. Storici F, Snipe JR, Chan GK, Gordenin DA, Resnick MA (2006) Conservative repair of a chromosomal double-strand break by single-strand DNA through two steps of annealing. Mol Cell Biol 26: 7645-7657.
101. Feiss M, Becker A (1983) DNA packaging and cutting. In: Hendrix RW, Roberts JW, Stahl FW, Weisberg RW, eds. Lambda II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. pp. 305-350.
102. Thaler DS, Stahl FW (1988) DNA double-chain breaks ia recombination of phage λ and yeast. Annu Rev Genet 22: 169-197.
103. Bachmann BJ (1996) Derivatives and genotypes of some mutant derivatives of Escherichia coli K-12. In: Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, et al. eds. Escherichia coli and Salmonella: Cellular and Molecular Biology. 2nd ed. Washington, D. C.: American Society for Microbiology. pp 2460-2488.
104. Woodcock DM, Crowther PJ, Doherty J, Jefferson S, DeCruz E, et al. (1989) Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res 17: 3469-3478.
105. 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. Mol Syst Biol 2: 2006 0008.
106. Gumbiner-Russo LM, Lombardo MJ, Ponder RG, Rosenberg SM (2001) The TGV transgenic vectors for single-copy gene expression from the Escherichia coli chromosome. Gene 273: 97-104.
107. Harris RS, Longerich S, Rosenberg SM (1994) Recombination in adaptive mutation. Science 264: 258-260.
108. Signer ER, Weil J (1968) Recombination in bacteriophage lambda. I. Mutants deficient in general recombination. J Mol Biol 34: 261-271.
109. Zissler J, Signer E, Schaefer F (1971) The role of recombination in the growth of bacteriophage lambda. I. The gamma gene. In: Hershey AD, ed. The Bacteriophage Lambda. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory. pp 455-468.
110. Campbell A (1971) Genetic structure. In: Hershey AD, ed. The Bacteriophage Lambda. Cold Spring Harbor, N.Y. Cold Spring Harbor Laboratory. pp 13-14.
111. Murray NE, Murray K (1974) Manipulation restriction targets in phage lambda to form receptor chromosomes for DNA fragments. Nature 251: 476-481.
112. Stahl FW, Crasemann JM, Stahl MM (1975) Rec-mediated recombinational hotspot activity in bacteriophage lambda III. Chi mutations are site mutations stimulating Rec-mediated recombination. J Mol Biol 94: 203-212.
113. Goldberg AR, Howe M (1969) New mutations in the S cistron of bacteriophage lambda affecting host cell lysis. Virology 38: 209-202.