Protein binding sites involved in the assembly of the KplE1 prophage intasome

Virology

Volumn 404, Issue 1, 2010, Pages 41-50

  Panis, Gaël ^a,b   Duverger, Yohann ^a   Champ, Stéphanie ^a   Ansaldi, Mireille ^a,b  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Bacteriophage; Intasome; Integrase; Prophage; Prophage excision; Recombination directionality factor; Site specific recombination

Indexed keywords

INTEGRASE; INTEGRATION HOST FACTOR; OLIGOMER;

ARTICLE; BACTERIOPHAGE; BINDING SITE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE TARGETING; GENETIC RECOMBINATION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROPHAGE; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN STABILITY; SITE DIRECTED MUTAGENESIS;

ESCHERICHIA COLI;

EID: 77953705852     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.04.027     Document Type: Article

References (50)

1. Abbani M.A., Papagiannis C.V., Sam M.D., Cascio D., Johnson R.C., Clubb R.T. Structure of the cooperative Xis-DNA complex reveals a micronucleoprotein filament that regulates phage lambda intasome assembly. Proc. Natl. Acad. Sci. U. S. A 2007, 104:2109-2114.
2. Abremski K., Gottesman S. Site-specific recombination Xis-independent excisive recombination of bacteriophage lambda. J. Mol. Biol. 1981, 153:67-78.
3. Abremski K., Gottesman S. Purification of the bacteriophage lambda xis gene product required for lambda excisive recombination. J. Biol. Chem. 1982, 257:9658-9662.
4. Ahlgren-Berg A., Cardoso-Palacios C., Eriksson J.M., Mandali S., Sehlen W., Sylwan L., Haggard-Ljungquist E. A comparative analysis of the bifunctional Cox proteins of two heteroimmune P2-like phages with different host integration sites. Virology 2009, 385:303-312.
5. Ansaldi M., Théraulaz L., Méjean V. TorI, a response regulator inhibitor of phage origin in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A 2004, 101:9423-9428.
6. Argos P., Landy A., Abremski K., Egan J.B., Haggard-Ljungquist E., Hoess R.H., Kahn M.L., Kalionis B., Narayana S.V., Pierson L.S. The integrase family of site-specific recombinases: regional similarities and global diversity. EMBO J. 1986, 5:433-440.
7. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K.A., Tomita M., Wanner B.L., Mori H. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2006, 2:2006.
8. Ball C.A., Johnson R.C. Efficient excision of phage lambda from the Escherichia coli chromosome requires the Fis protein. J. Bacteriol. 1991, 173:4027-4031.
9. Biswas T., Aihara H., Radman-Livaja M., Filman D., Landy A., Ellenberger T. A structural basis for allosteric control of DNA recombination by lambda integrase. Nature 2005, 435:1059-1066.
10. Cali S., Spoldi E., Piazzolla D., Dodd I.B., Forti F., Deho G., Ghisotti D. Bacteriophage P4 Vis protein is needed for prophage excision. Virology 2004, 322:82-92.
11. Casadaban M.J. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J. Mol. Biol. 1976, 104:541-555.
12. Casjens S. Prophages and bacterial genomics: what have we learned so far?. Mol. Microbiol. 2003, 49:277-300.
13. Casjens S., Winn-Stapley D.A., Gilcrease E.B., Morona R., Kuhlewein C., Chua J.E., Manning P.A., Inwood W., Clark A.J. The chromosome of Shigella flexneri bacteriophage Sf6: complete nucleotide sequence, genetic mosaicism, and DNA packaging. J. Mol. Biol. 2004, 339:379-394.
14. Cho E.H., Nam C.E., Alcaraz R., Gardner J.F. Site-specific recombination of bacteriophage P22 does not require integration host factor. J. Bacteriol. 1999, 181:4245-4249.
15. Clark A.J., Inwood W., Cloutier T., Dhillon T.S. Nucleotide sequence of coliphage HK620 and the evolution of lambdoid phages. J. Mol. Biol. 2001, 311:657-679.
16. Datsenko K.A., Wanner B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A 2000, 97:6640-6645.
17. ElAntak L., Ansaldi M., Guerlesquin F., Méjean V., Morelli X. Structural and genetic analyses reveal a key role in prophage excision for the TorI response regulator inhibitor. J. Biol. Chem. 2005, 280:36802-36808.
18. Fadeev E.A., Sam M.D., Clubb R.T. NMR structure of the amino-terminal domain of the lambda integrase protein in complex with DNA: immobilization of a flexible tail facilitates beta-sheet recognition of the major groove. J. Mol. Biol. 2009, 388:682-690.
19. Frumerie C., Sylwan L., Ahlgren-Berg A., Haggard-Ljungquist E. Cooperative interactions between bacteriophage P2 integrase and its accessory factors IHF and Cox. Virology 2005, 332:284-294.
20. Gardner J.F., Nash H.A. Role of Escherichia coli IHF protein in lambda site-specific recombination. A mutational analysis of binding sites. J. Mol. Biol. 1986, 191:181-189.
21. Goodman S.D., Kay O. Replacement of integration host factor protein-induced DNA bending by flexible regions of DNA. J. Biol. Chem. 1999, 274:37004-37011.
22. Goodman S.D., Nicholson S.C., Nash H.A. Deformation of DNA during site-specific recombination of bacteriophage lambda: replacement of IHF protein by HU protein or sequence-directed bends. Proc. Natl. Acad. Sci. U. S. A 1992, 89:11910-11914.
23. Gottesman S., Abremski K. The role of HimA and Xis in lambda site-specific recombination. J. Mol. Biol. 1980, 138:503-512.
24. Hazelbaker D., Azaro M.A., Landy A. A biotin interference assay highlights two different asymmetric interaction profiles for lambda integrase arm-type binding sites in integrative versus excisive recombination. J. Biol. Chem. 2008, 283:12402-12414.
25. Huang W., Yuan C., Ansaldi M., Morelli X., Meehan E.J., Chen L.Q., Huang M. Expression, purification, crystallization and molecular replacement studies of TorI, an inhibition protein of Tor system. Chin. J. Struct. Chem. 2007, 26:594-598.
26. Jessop L., Bankhead T., Wong D., Segall A.M. The amino terminus of bacteriophage lambda integrase is involved in protein-protein interactions during recombination. J. Bacteriol. 2000, 182:1024-1034.
27. Kamadurai H.B., Foster M.P. DNA recognition via mutual-induced fit by the core-binding domain of bacteriophage lambda integrase. Biochemistry 2007, 46:13939-13947.
28. King M.R., Vimr R.P., Steenbergen S.M., Spanjaard L., Plunkett G., Blattner F.R., Vimr E.R. Escherichia coli K1-specific bacteriophage CUS-3 distribution and function in phase-variable capsular polysialic acid O acetylation. J. Bacteriol. 2007, 189:6447-6456.
29. Kovach M.J., Tirumalai R., Landy A. Site-specific photo-cross-linking between lambda integrase and its DNA recombination target. J. Biol. Chem. 2002, 277:14530-14538.
30. Lee S.Y., Radman-Livaja M., Warren D., Aihara H., Ellenberger T., Landy A. Non-equivalent interactions between amino-terminal domains of neighboring lambda integrase protomers direct Holliday junction resolution. J. Mol. Biol. 2005, 345:475-485.
31. Lewis J.A., Hatfull G.F. Control of directionality in integrase-mediated recombination: examination of recombination directionality factors (RDFs) including Xis and Cox proteins. Nucleic Acids Res. 2001, 29:2205-2216.
32. Miller H.I., Friedman D.I. An E. coli gene product required for lambda site-specific recombination. Cell 1980, 20:711-719.
33. Miller H.I., Mozola M.A., Friedman D.I. int-h: an int mutation of phage lambda that enhances site-specific recombination. Cell 1980, 20:721-729.
34. Murtin C., Engelhorn M., Geiselmann J., Boccard F. A quantitative UV laser footprinting analysis of the interaction of IHF with specific binding sites: re-evaluation of the effective concentration of IHF in the cell. J. Mol. Biol. 1998, 284:949-961.
35. Nash H.A., Robertson C.A. Purification and properties of the Escherichia coli protein factor required for lambda integrative recombination. J. Biol. Chem. 1981, 256:9246-9253.
36. Numrych T.E., Gumport R.I., Gardner J.F. A genetic analysis of Xis and FIS interactions with their binding sites in bacteriophage lambda. J. Bacteriol. 1991, 173:5954-5963.
37. Numrych T.E., Gumport R.I., Gardner J.F. Characterization of the bacteriophage lambda excisionase (Xis) protein: the C-terminus is required for Xis-integrase cooperativity but not for DNA binding. EMBO J. 1992, 11:3797-3806.
38. Nunes-Duby S.E., Kwon H.J., Tirumalai R.S., Ellenberger T., Landy A. Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res. 1998, 26:391-406.
39. Panis G., Méjean V., Ansaldi M. Control and regulation of KplE1 prophage site-specific recombination: a new recombination module analyzed. J. Biol. Chem. 2007, 282:21798-21809.
40. Papagiannis C.V., Sam M.D., Abbani M.A., Yoo D., Cascio D., Clubb R.T., Johnson R.C. Fis targets assembly of the Xis nucleoprotein filament to promote excisive recombination by phage lambda. J. Mol. Biol. 2007, 367:328-343.
41. Radman-Livaja M., Biswas T., Ellenberger T., Landy A., Aihara H. DNA arms do the legwork to ensure the directionality of lambda site-specific recombination. Curr. Opin. Struct. Biol. 2006, 16:42-50.
42. Rice P.A., Yang S., Mizuuchi K., Nash H.A. Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell 1996, 87:1295-1306.
43. Rudd K.E. Novel intergenic repeats of Escherichia coli K-12. Res. Microbiol. 1999, 150:653-664.
44. Sam M.D., Papagiannis C.V., Connolly K.M., Corselli L., Iwahara J., Lee J., Phillips M., Wojciak J.M., Johnson R.C., Clubb R.T. Regulation of directionality in bacteriophage lambda site-specific recombination: structure of the Xis protein. J. Mol. Biol. 2002, 324:791-805.
45. Shiga Y., Sekine Y., Kano Y., Ohtsubo E. Involvement of H-NS in transpositional recombination mediated by IS1. J. Bacteriol. 2001, 183:2476-2484.
46. Smith M.C., Thorpe H.M. Diversity in the serine recombinases. Mol. Microbiol. 2002, 44:299-307.
47. Thompson J.F., Waechter-Brulla D., Gumport R.I., Gardner J.F., Moitoso de Vargas L., Landy A. Mutations in an integration host factor-binding site: effect on lambda site-specific recombination and regulatory implications. J. Bacteriol. 1986, 168:1343-1351.
48. Tirumalai R.S., Healey E., Landy A. The catalytic domain of lambda site-specific recombinase. Proc. Natl. Acad. Sci. U. S. A 1997, 94:6104-6109.
49. Tirumalai R.S., Kwon H.J., Cardente E.H., Ellenberger T., Landy A. Recognition of core-type DNA sites by lambda integrase. J. Mol. Biol. 1998, 279:513-527.
50. Yu A., Haggard-Ljungquist E. The Cox protein is a modulator of directionality in bacteriophage P2 site-specific recombination. J. Bacteriol. 1993, 175:7848-7855.