Viewing single λ site-specific recombination events from start to finish

EMBO Journal

Volumn 25, Issue 19, 2006, Pages 4586-4595

  Mumm, Jeffrey P ^a,b   Landy, Arthur ^a   Gelles, Jeff ^b  

^a BROWN UNIVERSITY   (United States)

^b BRANDEIS UNIVERSITY   (United States)

Author keywords

Bacteriophage ; DNA recombination; Holliday junction; Synapsis; Tyrosine recombinase

Indexed keywords

DNA; DNA BINDING PROTEIN; INTEGRASE;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIOPHAGE LAMBDA; CHROMOSOME PAIRING; DNA CLEAVAGE; DNA RECOMBINATION; DNA STRAND; DNA STRUCTURE; ESCHERICHIA COLI; EXCISION REPAIR; HOLLIDAY JUNCTION; MICROSCOPY; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN DNA BINDING;

ATTACHMENT SITES, MICROBIOLOGICAL; BACTERIOPHAGE LAMBDA; DNA, BACTERIAL; DNA, VIRAL; ESCHERICHIA COLI; INTEGRASES; KINETICS; MUTATION; RECOMBINATION, GENETIC;

ENTEROBACTERIA PHAGE LAMBDA; ESCHERICHIA COLI; SYNAPSIS;

EID: 33749359386     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601325     Document Type: Article

References (71)

1. Abremski K, Gottesman S (1982) Purification of the bacteriophage λ xis gene product required for λ excisive recombination. J Biol Chem 257: 9658-9662
2. Amin AA, Sadowski PD (1989) Synthesis of an enzymatically active FLP recombinase in vitro: search for a DNA-binding domain. Mol Cell Biol 9: 1987-1995
3. Azaro MA, Landy A (2002) λ Int and the λ Int family. In Mobile DNA II, Craig NL, Craigie R, Gellert M, Lambowitz A (eds) pp 118-148. Washington, DC: ASM Press
4. Ball CA, Johnson RC (1991) Multiple effects of Fis on integration and the control of lysogeny in phage λ. J Bacteriol 173: 4032-4038
5. Ball CA, Osuna R, Ferguson KC, Johnson RC (1992) Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J Bacteriol 174: 8043-8056
6. Bankhead TM, Etzel BJ, Wolven F, Bordenave S, Boldt JL, Larsen TA, Segall AM (2003) Mutations at residues 282, 286, and 293 of phage λ integrase exert pathway-specific effects on synapsis and catalysis in recombination. J Bacteriol 185: 2653-2666
7. Bauer CE, Hesse SD, Gumport RI, Gardner JF (1986) Mutational analysis of integrase arm-type binding sites of bacteriophage lambda. J Mol Biol 192: 513-527
8. Berliner E, Mahtani HK, Karki S, Chu LF, Cronan Jr JE, Gelles J (1994) Microtubule movement by a biotinated kinesin bound to a streptavidin-coated surface. J Biol Chem 269: 8610-8615
9. Biswas T, Aihara H, Radman-Livaja M, Filman D, Landy A, Ellenberger T (2005) A structural basis for allosteric control of DNA recombination by λ integrase. Nature 435: 1059-1066
10. Burgin Jr AB, Huizenga BN, Nash HA (1995) A novel suicide substrate for DNA topoisomerases and site-specific recombinases. Nucleic Acids Res 23: 2973-2979
11. Bushman W, Thompson JF, Vargas L, Landy A (1985) Control of directionality in lambda site-specific recombination. Science 230: 906-911
12. Campbell AM (1962) Episomes. In Advances in Genetics, Caspari EW, Thoday JM (eds) pp 101-145. New York, NY: Academic Press
13. Cassell G, Klemm M, Pinilla C, Segall A (2000) Dissection of bacteriophage λ site-specific recombination using synthetic peptide combinatorial libraries. J Mol Biol 299: 1193-1202
14. Chen Y, Rice PA (2003) New insight into site-specific recombination from Flp recombinase-DNA structures. Annu Rev Biophys Biomol Struct 32: 135-139
15. Colquhoun D, Sigworth FJ (1995) Fitting and statistical analysis of single-channel records. In Single-channel Recording, Sakmann B, Neher E (eds) pp 483-585. New York: Plenum Press
16. Cox M (1989) DNA inversion in the 2μ plasmid of Saccharomyces cerevisiae. In Mobile DNA, Berg DE, Howe MM (eds) pp 661-670. Washington, DC: American Society for Microbiology
17. Craig NL, Nash HA (1983) The mechanism of phage lambda site-specific recombination: collison versus sliding in att site juxtaposition. In Mechanism of DNA Replication and Recombination, Cozzarelli NR (ed) pp 617-636. New York: Alan R Liss Inc.
18. Ditto MD, Roberts D, Weisberg RA (1994) Growth phase variation of integration host factor level in Escherichia coli. J Bacteriol 176: 3738-3748
19. Esposito D, Scocca JJ (1997) The integrase family of tyrosine recombinases: evolution of a conserved active site domain. Nucleic Acids Res 25: 3605-3614
20. Finzi L, Gelles J (1995) Measurement of lactose repressor-mediated loop formation and breakdown in single DNA molecules. Science 267: 378-380
21. Futcher AB (1986) Copy number amplification of the 2 micron circle plasmid of Saccharomyces cerevisiae. J Theor Biol 119: 197-204
22. Gallacher Jr NC, Wise GL (1981) A theoretical analysis of the properties of median filters. IEEE Transactions on Acoustics, Speech and Signal Processing ASSP-29: 1136-1141
23. Gardner JF, Nash HA (1986) Role of Escherichia coli IHF protein in lambda site-specific recombination. A mutational analysis of binding sites. J Mol Biol 191: 181-189
24. Gopaul DN, Guo F, Van Duyne GD (1998) Structure of the Holliday junction intermediate in Cre-loxP site-specific recombination. EMBO J 17: 4175-4187
25. Grainge I, Jayaram M (1999) The integrase family of recombinase: organization and function of the active site. Mol Microbiol 33: 449-456
26. Guo F, Gopaul DN, Van Duyne GD (1997) Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature 389: 40-46
27. Guo F, Gopaul DN, Van Duyne GD (1999) Asymmetric DNA-bending in the Cre-loxP site-specific recombination synapse. Proc Natl Acad Sci USA 96: 7143-7148
28. Ha T, Rasnik I, Babcock HP, Gauss GH, Lohman TM, Chu S (2002) Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature 419: 638-641
29. Hickman AB, Waninger S, Scocca JJ, Dyda F (1997) Molecular organization in site-specific recombination: The catalytic domain of bacteriophage HP1 integrase at 2.7 Å resolution. Cell 89: 227-237
30. Jayaram M, Crain KL, Parsons RL, Harshey RM (1988) Holliday junctions in FLP recombination: resolution by step-arrest mutants of FLP protein. Proc Natl Acad Sci USA 85: 7902-7906
31. Jayaram M, Grainge I, Tribble G (2002) Site-specific recombination by the Flp protein of Saccharomyces cerevisiae. In Mobile DNA II, Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) pp 192-218. Washington, DC: ASM Press
32. Kim S-H, Landy A (1992) Lambda Int protein bridges between higher order complexes at two distant chromosomal loci attL and attR. Science 256: 198-203
33. Kim S, Moitoso de Vargas L, Nunes-Düby SE, Landy A (1990) Mapping of a higher order protein-DNA complex: two kinds of long-range interactions in λ attL. Cell 63: 773-781
34. Kitts PA, Nash HA (1987) Homology-dependent interactions in phage λ site-specific recombination. Nature 329: 346-348
35. Kitts PA, Nash HA (1988) An intermediate in the phage λ site-specific recombination reaction is revealed by phosphorothioate substitution in DNA. Nucleic Acids Res 16: 6839-6856
36. Lewis JA, Hatfull GF (2001) Control of directionality in integrase-mediated recombination: examination of recombination directionality factors (RDFs) including Xis and Cox proteins. Nucleic Acids Res 29: 2205-2216
37. Lewis JA, Hatfull GF (2003) Control of directionality in L5 integrase-mediated site-specific recombination. J Mol Biol 326: 805-821
38. MacWilliams M, Gumport RI, Gardner JF (1997) Mutational analysis of protein binding sites involved in formation of the bacteriophage λ attL complex. J Bacteriol 179: 1059-1067
39. Moitoso de Vargas L, Kim S, Landy A (1989) DNA looping generated by the DNA-bending protein IHF and the two domains of lambda integrase. Science 244: 1457-1461
40. Nash HA (1996) Site-specific recombination: integration, excision, resolution, and inversion of defined DNA segments. In Escherichia coli and Salmonella, Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) pp 2363-2376. Washington: ASM Press
41. Nash HA, Pollock TJ (1983) Site-specific recombination of bacteriophage lambda: the change in topological linking number associated with exchange of DNA strands. J Mol Biol 170: 19-38
42. Nash HA, Robertson CA (1989) Heteroduplex substrates for bacteriophage lambda site-specific recombination: cleavage and strand transfer products. EMBO J 8: 3523-3533
43. Nash HA, Robertson CA, Flamm E, Weisberg RA, Miller HI (1987) Overproduction of Escherichia coli integration host factor, a protein with nonidentical subunits. J Bacteriol 169: 4124-4127
44. Numrych TE, Gumport RI, Gardner JF (1990) A comparison of the effects of single-base and triple-base changes in the integrase arm-type binding sites on the site-specific recombination of bacteriophage lambda. Nucleic Acids Res 18: 3953-3959
45. Nunes-Düby S, Tirumalai RS, Kwon HJ, Ellenberger T, Landy A (1998) Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res 26: 391-406
46. Nunes-Düby SE, Matsumoto L, Landy A (1987) Site-specific recombination intermediates trapped with suicide substrates. Cell 50: 779-788
47. Nunes-Düby SE, Matsumoto L, Landy A (1989) Half-att site substrates reveal the homology independence and minimal protein requirements for productive synapsis in λ excisive recombination. Cell 59: 197-206
48. Nunes-Düby SE, Radman-Livaja M, Kuimelis RG, Pearline RV, McLaughlin LW, Landy A (2002) λ integrase complementation at the level of DNA binding and complex formation. J Bacteriol 184: 1385-1394
49. Pan G, Sadowski PD (1992) Ligation activity of FLP recombinase. The strand ligation activity of a site-specific recombinase using an activated DNA substrate. J Biol Chem 267: 12397-12399
50. Pargellis CA, Nunes-Düby SE, Moitoso de Vargas L, Landy A (1988) Suicide recombination substrates yield covalent λ integrase-NA complexes and lead to identification of the active site tyrosine. J Biol Chem 263: 7678-7685
51. Parsons RL, Prasad PV, Harshey RM, Jayaram M (1988) Step-arrest mutants of FLP recombinase: implications for the catalytic mechanism of DNA recombination. Mol Cell Biol 8: 3303-3310
52. Perkins TT, Li H-W, Dalal RV, Gelles J, Block SM (2004) Forward and reverse motion of single RecBCD molecules on DNA. Biophys J 86: 1640-1648
53. Pollock TJ, Nash HA (1983) Knotting of DNA caused by a genetic rearrangement: evidence for a nucleosome-like structure in site-specific recombination for bacteriophage lambda. J Mol Biol 170: 1-18
54. Radman-Livaja M, Biswas T, Mierke D, Landy A (2005) Architecture of recombination intermediates visualized by In-gel FRET of λ integrase-Holliday junction-arm-DNA complexes. Proc Natl Acad Sci USA 102: 3913-3920
55. Rice PA, Yang S-W, Mizuuchi K, Nash HA (1996) Crystal structure of an IHF-DNA complex: a protein-induced DNA u-turn. Cell 87: 1295-1306
56. Rudy C, Taylor KL, Hinerfeld D, Scott JR, Churchward G (1997a) Excision of a conjugative transposon in vitro by the Int and Xis proteins of Tn916. Nucleic Acids Res 25: 4061-4066
57. Rudy CK, Scott JR, Churchward G (1997b) DNA binding by the Xis protein of the conjugative transposon Tn916. J Bacteriol 179: 2567-2572
58. Sadowski PD (1993) Site-specific genetic recombination: hops, flips and flops. FASEB J 7: 760-767
59. Sarkar D, Radman-Livaja M, Landy A (2001) The small DNA binding domain of λ Int is a context-sensitive modulator of recombinase functions. EMBO J 20: 1203-1212
60. Segall AM, Nash HA (1996) Architectural flexibility in lambda site-specific recombination: three alternate conformations channel the attL site into three distinct pathways. Genes Cells 1: 453-463
61. Serre MC, Jayaram M (1992) Half-site strand transfer by step-arrest mutants of yeast site-specific recombinase Flp. J Mol Biol 225: 643-649
62. Thompson JF, Moitoso de Vargas L, Koch C, Kahmann R, Landy A (1987a) Cellular factors couple recombination with growth phase: characterization of a new component in the λ site-specific recombination pathway. Cell 50: 901-908
63. Thompson JF, Moitoso de Vargas L, Skinner SE, Landy A (1987b) Protein-protein interactions in a higher-order structure direct lambda site-specific recombination. J Mol Biol 195: 481-493
64. Thompson JF, Waechter-Brulla D, Gumport RI, Gardner JF, Moitoso de Vargas L, Landy A (1986) Mutations in an integration host factor-binding site: effect on lambda site-specific recombination and regulatory implications. J Bacteriol 168: 1343-1351
65. Tolic-Norrelykke SF, Engh AM, Landick R, Gelles J (2004) Diversity in the rates of transcript elongation by single RNA polymerase molecules. J Biol Chem 279: 3292-3299
66. Van Duyne GD (2001) A structural view of cre-loxp site-specific recombination. Annu Rev Biophys Biomol Struct 30: 87-104
67. Van Duyne GD (2002) A structural view of tyrosine recombinase site-specific recombination. In Mobile DNA II, In Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) pp 93-117. Washington, DC: ASM Press
68. Voziyanov Y, Pathania S, Jayaram M (1999) A general model for site-specific recombination by the integrase family recombinases. Nucleic Acids Res 27: 930-941
69. Warren D, Sam M, Manley K, Sarkar D, Lee SY, Abbani M, Clubb RT, Landy A (2003) Identification of the λ integrase surface that interacts with the Xis accessory protein reveals a residue that is also critical for homomeric dimer formation. Proc Natl Acad Sci USA 100: 8176-8181
70. Wierzbicki A, Kendall M, Abremski K, Hoess R (1987) A mutational analysis of the bacteriophage P1 recombinase Cre. J Mol Biol 195: 785-794
71. Yin H, Landick R, Gelles J (1994) Tethered particle motion method for studying transcript elongation by a single RNA polymerase molecule. Biophys J 67: 2468-2478