TPM analyses reveal that FtsK contributes both to the assembly and the activation of the XerCD-dif recombination synapse

Nucleic Acids Research

Volumn 42, Issue 3, 2014, Pages 1721-1732

  Diagne, Cheikh Tidiane ^a,b,c   Salhi, Maya ^c   Crozat, Estelle ^c   Salomé, Laurence ^a,b   Cornet, Francois ^c   Rousseau, Philippe ^c   Tardin, Catherine ^a,b  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c UMR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FTSK PROTEIN; PROTEIN XERC; PROTEIN XERCD DIF; PROTEIN XERD; RECOMBINASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INACTIVATION; ESCHERICHIA COLI; GENETIC RECOMBINATION; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; SYNAPSE; SYNAPTOGENESIS; TETHERED PARTICLE MOTION;

ESCHERICHIA COLI PROTEINS; INTEGRASES; KINETICS; MEMBRANE PROTEINS; MOTION; PROTEIN STRUCTURE, TERTIARY; RECOMBINATION, GENETIC;

EID: 84896697880     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1024     Document Type: Article

References (44)

1. Steiner, W.W. and Kuempel, P.L. (1998) Sister chromatid exchange frequencies in Escherichia coli analyzed by recombination at the dif resolvase site. J. Bacteriol., 180, 6269-6275.
2. Lesterlin, C., Barre, F.X. and Cornet, F. (2004) Genetic recombination and the cell cycle: what we have learned from chromosome dimers. Mol. Microbiol., 54, 1151-1160.
3. Carnoy, C. and Roten, C.-A. (2009) The dif/Xer recombination systems in proteobacteria. PLoS ONE, 4, e6531.
4. Kono, N., Arakawa, K. and Tomita, M. (2011) Comprehensive prediction of chromosome dimer resolution sites in bacterial genomes. BMC Genomics, 12, 19.
5. Grindley, N.D., Whiteson, K.L. and Rice, P.A. (2006) Mechanisms of site-specific recombination. Annu. Rev. Biochem., 75, 567-605.
6. Blakely, G.W. and Sherratt, D.J. (1994) Interactions of the sitespecific recombinases XerC and XerD with the recombination site dif. Nucleic Acids Res., 22, 5613-5620.
7. Blakely, G.W., Davidson, A.O. and Sherratt, D.J. (1997) Binding and cleavage of nicked substrates by site-specific recombinases XerC and XerD. J. Mol. Biol., 265, 30-39.
8. Hallet, B., Arciszewska, L.K. and Sherratt, D.J. (1999) Reciprocal control of catalysis by the tyrosine recombinases XerC and XerD: an enzymatic switch in site-specific recombination. Mol. Cell, 4, 949-959.
9. Aussel, L., Barre, F.X., Aroyo, M., Stasiak, A., Stasiak, A.Z. 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.
10. Barre, F.X., Aroyo, M., Colloms, S.D., Helfrich, A., Cornet, F. and Sherratt, D.J. (2000) FtsK functions in the processing of a Holliday junction intermediate during bacterial chromosome segregation. Genes Dev., 14, 2976-2988.
11. Grainge, I. (2010) FtsK-A bacterial cell division checkpoint? Mol. Microbiol., 78, 1055-1057.
12. Stouf, M., Meile, J.-C. and Cornet, F. (2013) FtsK actively segregates sister chromosomes in Escherichia coli. Proc. Natl Acad. Sci. USA, 110, 11157-11162.
13. Dubarry, N., Possoz, C. and Barre, F.-X. (2010) Multiple regions along the Escherichia coli FtsK protein are implicated in cell division. Mol. Microbiol., 78, 1088-1100.
14. Dubarry, N. and Barre, F.-X. (2010) Fully efficient chromosome dimer resolution in Escherichia coli cells lacking the integral membrane domain of FtsK. EMBO J., 29, 597-605.
15. Massey, T.H., Mercogliano, C.P., Yates, J., Sherratt, D.J. and Lowe, J. (2006) Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol. Cell, 23, 457-469.
16. Crozat, E. and Grainge, I. (2010) FtsK DNA translocase: the fast motor that knows where its going. ChemBioChem, 11, 2232-2243.
17. Erzberger, J.P. and Berger, J.M. (2006) Evolutionary relationships and structural mechanisms of AAA+proteins. Ann. Rev. Biophys. Biomol. Struct., 35, 93-114.
18. Bigot, S., Sivanathan, V., Possoz, C., Barre, F.X. and Cornet, F. (2007) FtsK, a literate chromosome segregation machine. Mol. Microbiol., 64, 1434-1441.
19. Bigot, S., Saleh, O., Cornet, F., Allemand, J.F. and Barre, F.X. (2006) Oriented loading of FtsK on KOPS. Nat. Struct. Mol. Biol., 13, 1026-1028.
20. Sivanathan, V., Allen, M.D., de Bekker, C., Baker, R., Arciszewska, L.K., Freund, S.M., Bycroft, M., Löwe, J. and Sherratt, D.J. (2006) The FtsK gamma domain directs oriented DNA translocation by interacting with KOPS. Nat. Struct. Mol. Biol., 13, 965-972.
21. Löwe, J., Ellonen, A., Allen, M.D., Atkinson, C., Sherratt, D.J. and Grainge, I. (2008) Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol. Cell, 31, 498-509.
22. Graham, J.E., Sherratt, D.J. and Szczelkun, M.D. (2010) Sequencespecific assembly of FtsK hexamers establishes directional translocation on DNA. Proc. Natl Acad. Sci. USA, 107, 20263-20268.
23. Lee, J.Y., Finkelstein, I.J., Crozat, E., Sherratt, D.J. and Greene, E.C. (2012) Single-molecule imaging of DNA curtains reveals mechanisms of KOPS sequence targeting by the DNA translocase FtsK. Proc. Natl Acad. Sci. USA, 109, 6531-6536.
24. Yates, J., Zhekov, I., Baker, R., Eklund, B., Sherratt, D.J. and Arciszewska, L.K. (2006) Dissection of a functional interaction between the DNA translocase, FtsK, and the XerD recombinase. Mol. Microbiol., 59, 1754-1766.
25. Bonné , L., Bigot, S., Chevalier, F., Allemand, J.-F. and Barre, F.-X. (2009) Asymmetric DNA requirements in Xer recombination activation by FtsK. Nucleic Acids Res., 37, 2371-2380.
26. Graham, J.E., Sivanathan, V., Sherratt, D.J. and Arciszewska, L.K. (2010) FtsK translocation on DNA stops at XerCD-dif. Nucleic Acids Res., 38, 72-81.
27. Grainge, I., Lesterlin, C. and Sherratt, D.J. (2011) Activation of XerCD-dif recombination by the FtsK DNA translocase. Nucleic Acids Res., 39, 5140-5148.
28. Segall, A.M. and Nash, H.A. (1993) Synaptic intermediates in bacteriophage lambda site-specific recombination: integrase can align pairs of attachment sites. EMBO J., 12, 4567-4576.
29. Ghosh, K., Lau, C.K., Gupta, K. and Van Duyne, G.D. (2005) Preferential synapsis of loxP sites drives ordered strand exchange in Cre-loxP site-specific recombination. Nat. Chem. Biol., 1, 275-282.
30. Lee, L., Chu, L.C. and Sadowski, P.D. (2003) Cre induces an asymmetric DNA bend in its target loxP site. J. Biol. Chem., 278, 23118-23129.
31. Ghosh, K., Guo, F. and Van Duyne, G.D. (2007) Synapsis of loxP sites by Cre recombinase. J. Biol. Chem., 282, 24004-24016.
32. Cassell, G., Moision, R., Rabani, E. and Segall, A. (1999) The geometry of a synaptic intermediate in a pathway of bacteriophage lambda site-specific recombination. Nucleic Acids Res., 27, 1145-1151.
33. Vetcher, A.A., Lushnikov, A.Y., Navarra-Madsen, J., Scharein, R.G., Lyubchenko, Y.L., Darcy, I.K. and Levene, S.D. (2006) DNA topology and geometry in Flp and Cre recombination. J. Mol. Biol., 357, 1089-1104.
34. Mumm, J.P., Landy, A. and Gelles, J. (2006) Viewing single lambda site-specific recombination events from start to finish. EMBO J., 25, 4586-4595.
35. Fan, H.-F. (2012) Real-time single-molecule tethered particle motion experiments reveal the kinetics and mechanisms of Cre-mediated site-specific recombination. Nucleic Acids Res., 40, 6208-6222.
36. Pinkney, J.N.M., Zawadzki, P., Mazuryk, J., Arciszewska, L.K., Sherratt, D.J. and Kapanidis, A.N. (2012) Capturing reaction paths and intermediates in Cre-loxP recombination using single-molecule fluorescence. Proc. Natl Acad. Sci. USA, 109, 20871-20876.
37. Fan, H.-F., Ma, C.-H. and Jayaram, M. (2013) Real-time single-molecule tethered particle motion analysis reveals mechanistic similarities and contrasts of Flp site-specific recombinase with Cre and- Int. Nucleic Acids Res., 41, 7031-7047.
38. Ausubel, F.M., Brent, B., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K. (1987) Current Protocols in Molecular Biology. John Wiley & Sons, Inc, Hoboken, NJ, E tats-Unis.
39. Plénat, T., Tardin, C., Rousseau, P. and Salomé, L. (2012) High-throughput single-molecule analysis of DNA-protein interactions by tethered particle motion. Nucleic Acids Res., 40, e89.
40. Laurens, N., Bellamy, S.R.W., Harms, A.F., Kovacheva, Y.S., Halford, S.E. and Wuite, G.J.L. (2009) Dissecting protein-induced DNA looping dynamics in real time. Nucleic Acids Res., 37, 5454-5464.
41. Manghi, M., Tardin, C., Baglio, J., Rousseau, P., Salomé, L. and Destainville, N. (2010) Probing DNA conformational changes with high temporal resolution by tethered particle motion. Phys. Biol., 7, 046003.
42. Pouget, N., Turlan, C., Destainville, N., Salomé, L. and Chandler, M. (2006) IS911 transpososome assembly as analysed by tethered particle motion. Nucleic Acids Res., 34, 4313-4323.
43. Bates, D., Epstein, J., Boye, E., Fahrner, K., Berg, H. and Kleckner, N. (2005) The Escherichia coli baby cell column: a novel cell synchronization method provides new insight into the bacterial cell cycle. Mol. Microbiol., 57, 380-391.
44. Gopaul, D.N., Guo, F. and Van Duyne, G.D. (1998) Structure of the Holliday junction intermediate in Cre-loxP site-specific recombination. EMBO J., 17, 4175-4187.