Are two better than one? Analysis of an FtsK/Xer recombination system that uses a single recombinase

Nucleic Acids Research

Volumn 38, Issue 19, 2010, Pages 6477-6489

  Nolivos, Sophie ^a,b   Pages, Carine ^a,b   Rousseau, Philippe ^a,b   Le Bourgeois, Pascal ^a,b   Cornet, François ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; PROTEIN DIF; PROTEIN FTSK; PROTEIN FTSK GAMMA; PROTEIN XER; PROTEIN XERCD; PROTEIN XERS; RECOMBINASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL METABOLISM; CELL DIVISION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; ESCHERICHIA COLI; GENETIC RECOMBINATION; IN VITRO STUDY; LACTOCOCCUS LACTIS; MICROBIAL MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEOBACTERIA;

AMINO ACID SEQUENCE; BINDING SITES; CHROMOSOMES, BACTERIAL; DIMERIZATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LACTOCOCCUS LACTIS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; RECOMBINASES; RECOMBINATION, GENETIC;

ESCHERICHIA COLI; LACTOCOCCUS LACTIS; PROTEOBACTERIA;

EID: 78049353926     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq507     Document Type: Article

References (51)

1. Lesterlin, C., Barre, F. and Cornet, F. (2004) Genetic recombination and the cell cycle: what we have learned from chromosome dimers. Mol. Microbiol., 54, 1151-1160.
2. Sherratt, D. (2003) Bacterial chromosome dynamics. Science, 301, 780-785.
3. Bigot, S., Sivanathan, V., Possoz, C., Barre, F. and Cornet, F. (2007) FtsK, a literate chromosome segregation machine. Mol. Microbiol., 64, 1434-1441.
4. Sherratt, D., Søballe, B., Barre, F., Filipe, S., Lau, I., Massey, T. and Yates, J. (2004) Recombination and chromosome segregation. Philos. Trans Roy. Soc. Lond. B Biol. Sci., 359, 61-69.
5. Grindley, N., Whiteson, K. and Rice, P. (2006) Mechanisms of site-specific recombination. Annu. Rev. Biochem., 75, 567-605.
6. Bregu, M., Sherratt, D. and Colloms, S. (2002) Accessory factors determine the order of strand exchange in Xer recombination at psi. EMBO J., 21, 3888-3897.
7. Aussel, L., Barre, F., Aroyo, M., Stasiak, A., Stasiak, A. and Sherratt, D. (2002) FtsK Is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell, 108, 195-205.
8. Colloms, S., McCulloch, R., Grant, K., Neilson, L. and Sherratt, D. (1996) Xer-mediated site-specific recombination in vitro. EMBO J., 15, 1172-1181.
9. Val, M., Bouvier, M., Campos, J., Sherratt, D., Cornet, F., Mazel, D. and Barre, F. (2005) The single-stranded genome of phage CTX is the form used for integration into the genome of Vibrio cholerae. Mol. Cell, 19, 559-566.
10. Barre, F., Aroyo, M., Colloms, S., Helfrich, A., Cornet, F. and Sherratt, D. (2000) FtsK functions in the processing of a Holliday junction intermediate during bacterial chromosome segregation. Genes Dev., 14, 2976-2988.
11. Massey, T., Mercogliano, C., Yates, J., Sherratt, D. and Löwe, J. (2006) Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol. Cell, 23, 457-469.
12. Bigot, S., Saleh, O., Lesterlin, C., Pages, C., El Karoui, M., Dennis, C., Grigoriev, M., Allemand, J., Barre, F. and Cornet, F. (2005) KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J., 24, 3770-3780.
13. Levy, O., Ptacin, J., Pease, P., Gore, J., Eisen, M., Bustamante, C. and Cozzarelli, N. (2005) Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc. Natl Acad. Sci. USA, 102, 17618-17623.
14. Bigot, S., Saleh, O., Cornet, F., Allemand, J. and Barre, F. (2006) Oriented loading of FtsK on KOPS. Nat. Struct. Mol. Biol., 13, 1026-1028.
15. Ptacin, J., Nöllmann, M., Bustamante, C. and Cozzarelli, N. (2006) Identification of the FtsK sequence-recognition domain. Nat. Struct. Mol. Biol., 13, 1023-1025.
16. Sivanathan, V., Allen, M., de Bekker, C., Baker, R., Arciszewska, L., Freund, S., Bycroft, M., Löwe, J. and Sherratt, D. (2006) The FtsK gamma domain directs oriented DNA translocation by interacting with KOPS. Nat. Struct. Mol. Biol., 13, 965-972.
17. Löwe, J., Ellonen, A., Allen, M., Atkinson, C., Sherratt, D. and Grainge, I. (2008) Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol. Cell, 31, 498-509.
18. Graham, J., Sivanathan, V., Sherratt, D. and Arciszewska, L. (2010) FtsK translocation on DNA stops at XerCD-dif. Nucleic Acids Res., 38, 72-81.
19. Bonné, L., Bigot, S., Chevalier, F., Allemand, J. and Barre, F. (2009) Asymmetric DNA requirements in Xer recombination activation by FtsK. Nucleic Acids Res., 37, 2371-2380.
20. Yates, J., Zhekov, I., Baker, R., Eklund, B., Sherratt, D. and Arciszewska, L. (2006) Dissection of a functional interaction between the DNA translocase, FtsK, and the XerD recombinase. Mol. Microbiol., 59, 1754-1766.
21. Possoz, C., Ribard, C., Gagnat, J., Pernodet, J. and Guérineau, M. (2001) The integrative element pSAM2 from Streptomyces: kinetics and mode of conjugal transfer. Mol. Microbiol., 42, 159-166.
22. Wu, L. and Errington, J. (1994) Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. Science, 264, 572-575.
23. Val, M., Kennedy, S., El Karoui, M., Bonné, L., Chevalier, F. and Barre, F. (2008) FtsK-dependent dimer resolution on multiple chromosomes in the pathogen Vibrio cholerae. PLoS Genet., 4, e1000201.
24. Biller, S. and Burkholder, W. (2009) The Bacillus subtilis SftA (YtpS) and SpoIIIE DNA translocases play distinct roles in growing cells to ensure faithful chromosome partitioning. Mol. Microbiol., 74, 790-809.
25. Kaimer, C., González-Pastor, J. and Graumann, P. (2009) SpoIIIE and a novel type of DNA translocase, SftA, couple chromosome segregation with cell division in Bacillus subtilis. Mol. Microbiol., 74, 810-825.
26. Hallet, B. and Sherratt, D. (1997) Transposition and site-specific recombination: adapting DNA cut-and-paste mechanisms to a variety of genetic rearrangements. FEMS Microbiol. Rev., 21, 157-178.
27. Recchia, G. and Sherratt, D. (1999) Conservation of xer site-specific recombination genes in bacteria. Mol. Microbiol., 34, 1146-1148.
28. Le Bourgeois, P., Bugarel, M., Campo, N., Daveran-Mingot, M., Labonté, J., Lanfranchi, D., Lautier, T., Pagés, C. and Ritzenthaler, P. (2007) The unconventional Xer recombination machinery of Streptococci/Lactococci. PLoS Genet., 3, e117.
29. Carnoy, C. and Roten, C. (2009) The dif/Xer recombination systems in proteobacteria. PLoS ONE, 4, e6531.
30. Cornet, F., Mortier, I., Patte, J. and Louarn, J. (1994) Plasmid pSC101 harbors a recombination site, psi, which is able to resolve plasmid multimers and to substitute for the analogous chromosomal Escherichia coli site dif. J. Bacteriol., 176, 3188-3195.
31. Cornet, F., Louarn, J., Patte, J. and Louarn, J. (1996) Restriction of the activity of the recombination site dif to a small zone of the Escherichia coli chromosome. Genes Dev., 10, 1152-1161.
32. Sivanathan, V., Emerson, J., Pages, C., Cornet, F., Sherratt, D. and Arciszewska, L. (2009) KOPS-guided DNA translocation by FtsK safeguards Escherichia coli chromosome segregation. Mol. Microbiol., 71, 1031-1042.
33. Maguin, E., Prévost, H., Ehrlich, S. and Gruss, A. (1996) Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J. Bacteriol., 178, 931-935.
34. Pérals, K., Cornet, F., Merlet, Y., Delon, I. and Louarn, J. (2000) Functional polarization of the Escherichia coli chromosome terminus: the dif site acts in chromosome dimer resolution only when located between long stretches of opposite polarity. Mol. Microbiol., 36, 33-43.
35. Arciszewska, L. and Sherratt, D. (1995) Xer site-specific recombination in vitro. EMBO J., 14, 2112-2120.
36. de Massy, B., Dorgai, L. and Weisberg, R. (1989) Mutations of the phage lambda attachment site alter the directionality of resolution of Holliday structures. EMBO J., 8, 1591-1599.
37. Lee, J. and Jayaram, M. (1995) Junction mobility and resolution of Holliday structures by Flp site-specific recombinase. Testing partner compatibility during recombination. J. Biol. Chem., 270, 19086-19092.
38. Capiaux, H., Lesterlin, C., Pérals, K., Louarn, J. and Cornet, F. (2002) A dual role for the FtsK protein in Escherichia coli chromosome segregation. EMBO Rep., 3, 532-536.
39. Bigot, S., Corre, J., Louarn, J., Cornet, F. and Barre, F. (2004) FtsK activities in Xer recombination, DNA mobilization and cell division involve overlapping and separate domains of the protein. Mol. Microbiol., 54, 876-886.
40. Dubarry, N. and Barre, F. (2010) Fully efficient chromosome dimer resolution in Escherichia coli cells lacking the integral membrane domain of FtsK. EMBO J., 29, 597-605.
41. Pérals, K., Capiaux, H., Vincourt, J., Louarn, J., Sherratt, D. and Cornet, F. (2001) Interplay between recombination, cell division and chromosome structure during chromosome dimer resolution in Escherichia coli. Mol. Microbiol., 39, 904-913.
42. Yates, J., Aroyo, M., Sherratt, D. and Barre, F. (2003) Species specificity in the activation of Xer recombination at dif by FtsK. Mol. Microbiol., 49, 241-249.
43. Blakely, G., May, G., McCulloch, R., Arciszewska, L., Burke, M., Lovett, S. and Sherratt, D. (1993) Two related recombinases are required for site-specific recombination at dif and cer in E. coli K12. Cell, 75, 351-361.
44. Arciszewska, L., Grainge, I. and Sherratt, D. (1995) Effects of Holliday junction position on Xer-mediated recombination in vitro. EMBO J., 14, 2651-2660.
45. Sciochetti, S., Piggot, P. and Blakely, G. (2001) Identification and characterization of the dif Site from Bacillus subtilis. J. Bacteriol., 183, 1058-1068.
46. Steiner, W. and Kuempel, P. (1998) Cell division is required for resolution of dimer chromosomes at the dif locus of Escherichia coli. Mol. Microbiol., 27, 257-268.
47. Kennedy, S., Chevalier, F. and Barre, F. (2008) Delayed activation of Xer recombination at dif by FtsK during septum assembly in Escherichia coli. Mol. Microbiol., 68, 1018-1028.
48. Leslie, N. and Sherratt, D. (1995) Site-specific recombination in the replication terminus region of Escherichia coli: functional replacement of dif. EMBO J., 14, 1561-1570.
49. Lin, N., Chang, R., Lee, S. and Tseng, Y. (2001) Plasmids carrying cloned fragments of RF DNA from the filamentous phage (phi)Lf can be integrated into the host chromosome via site-specific integration and homologous recombination. Mol. Genet. Genomics, 266, 425-435.
50. Gonzalez, M., Lichtensteiger, C., Caughlan, R. and Vimr, E. (2002) Conserved filamentous prophage in Escherichia coli O18:K1:H7 and Yersinia pestis biovar orientalis. J. Bacteriol., 184, 6050-6055.
51. Hamilton, H., Domínguez, N., Schwartz, K., Hackett, K. and Dillard, J. (2005) Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol. Microbiol., 55, 1704-1721.