KOPS-guided DNA translocation by FtsK safeguards Escherichia coli chromosome segregation

Molecular Microbiology

Volumn 71, Issue 4, 2009, Pages 1031-1042

  Sivanathan, Viknesh ^a,b   Emerson, Jenny E ^b   Pages, Carine ^c   Cornet, François ^c   Sherratt, David J ^b   Arciszewska, Lidia K ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UPS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; DIMER; FTSK PROTEIN; MONOMER; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; BACTERIAL GROWTH; CELL DIVISION; CELL POPULATION; CELL VIABILITY; CHROMOSOME SEGREGATION; ESCHERICHIA COLI; GENE SEQUENCE; GENE TRANSLOCATION; NONHUMAN; PRIORITY JOURNAL;

CELL DIVISION; CHROMOSOME SEGREGATION; CHROMOSOMES, BACTERIAL; DIMERIZATION; DNA REPLICATION; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS;

ESCHERICHIA COLI;

EID: 60349124253     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06586.x     Document Type: Article

References (47)

1. Aussel, L., Barre, F.-X., Aroyo, M., Stasiak, A., Stasiak, A.Z. 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.
2. Barre, F.-X., Aroyo, M., Colloms, S.D., Helfrich, A., Cornet, F. Sherratt, D.J. (2000) FtsK functions in the processing of a Holliday Junction intermediate during bacterial chromosome segregation. Genes Dev 14 : 2976 2988.
3. Becker, E. Pogliano, K. (2007) Cell-specific SpoIIIE assembly and DNA translocation polarity are dictated by chromosome orientation. Mol Microbiol 66 : 1066 1079.
4. Bigot, S., Corre, J., Louarn, J.M., Cornet, F. Barre, F.-X. (2004) FtsK activities in Xer recombination, DNA mobilization and cell division involve overlapping and separate domains of the protein. Mol Microbiol 54 : 876 886.
5. Bigot, S., Saleh, O.A., Lesterlin, C., Pages, C., El Karoui, M., Dennis, C., et al. (2005) KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J 24 : 3770 3780.
6. Bigot, S., Saleh, O.A., Cornet, F., Allemand, J.F. Barre, F.-X. (2006) Oriented loading of FtsK on KOPS. Nat Struct Mol Biol 13 : 1026 1028.
7. Bigot, S., Sivanathan, V., Possoz, C., Barre, F.-X. Cornet, F. (2007) FtsK, a literate chromosome segregation machine. Mol Microbiol 64 : 1434 1441.
8. Blakely, G., Colloms, S., May, G., Burke, M. Sherratt, D. (1991) Escherichia coli XerC recombinase is required for chromosomal segregation at cell division. New Biol 3 : 789 798.
9. Blakely, G., May, G., McCulloch, R., Arciszewska, L.A., Burke, M., Lovett, S.T. Sherratt, D.J. (1993) Two related recombinases are required for site-specific recombination at dif and cer in E. coli K12. Cell 75 : 351 361.
10. Britton, R. Grossman, A. (1999) Synthetic lethal phenotypes caused by mutations affecting chromosome partitioning in Bacillus subtilis. J Bacteriol 181 : 5860 5864.
11. Britton, R., Lin, D. Grossman, A. (1998) Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev 12 : 1254 1259.
12. Capiaux, H., Lesterlin, C., Perals, K., Louarn, J.M. Cornet, F. (2002) A dual role for the FtsK protein in Escherichia coli chromosome segregation. EMBO Rep 6 : 532 536.
13. Cornet, F., Mortier, I., Patte, J. 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.
14. Corre, J. Louarn, J.M. (2005) Extent of the activity domain and possible roles of FtsK in the Escherichia coli chromosome terminus. Mol Microbiol 6 : 1539 1548.
15. Danilova, O., Reyes-Lamothe, R., Pinskaya, M., Sherratt, D. Possoz, C. (2007) MukB colocalizes with the oriC region and is required for organization of the two Escherichia coli chromosome arms into separate cell halves. Mol Microbiol 65 : 1485 1492.
16. Diez, A.A., Farewell, A., Nannmark, U. Nyström, T. (1997) A mutation in the ftsK gene of Escherichia coli affects cell-cell separation, stationary phase survival, stress adaptation, and expression of the gene encoding the stress protein UspA. J Bacteriol 179 : 5878 5883.
17. Draper, G.G., McClennan, N., Begg, K., Masters, M. Donachie, W.D. (1998) Only the N-terminal domain of FtsK functions in cell division. J Bacteriol 180 : 4621 4627.
18. Ferreira, H., Sherratt, D.J. Arciszewska, L.K. (2001) Switching catalytic activity in the XerCD site-specific recombination machine. J Mol Biol 312 : 45 57.
19. Goehring, N. Beckwith, J. (2005) Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15 : 514 526.
20. Grainge, I., Bregu, M., Vazquez, M., Sivanathan, V., Ip, S.C.Y. Sherratt, D. (2007) Unlinking chromosome catenanes in vivo by site-specific recombination. EMBO J 26 : 4228 4238.
21. Hendricks, E., Szerlong, H., Hill, T. Kuempel, P. (2000) Cell division, guillotining of dimer chromosomes and SOS induction in resolution mutants (dif, xerC and xerD) of Escherichia coli. Mol Microbiol 36 : 973 981.
22. Hendrickson, H. Lawrence, J.G. (2006) Selection of chromosome architecture in bacteria. J Mol Evol 62 : 615 629.
23. Ip, S.C.Y., Bregu, M., Barre, F.-X. Sherratt, D.J. (2003) Decatenation of DNA circles by FtsK-dependent Xer site-specific recombination. EMBO J 22 : 6399 6407.
24. Kennedy, S., Chevalier, F. Barre, F.-X. (2008) Delayed activation of Xer recombination at dif by FtsK during septum assembly in Escherichia coli. Mol Microbiol 68 : 1018 1028.
25. Kouzminova, E.A., Rotman, E., Macomber, L., Zhang, J. Kuzminov, A. (2004) RecA-dependent mutants in Escherichia coli reveal strategies to avoid chromosomal fragmentation. Proc Natl Acad Sci USA 101 : 16262 16267.
26. Kuempel, P.L., Henson, J.M., Dircks, L., Tecklenburg, M. Lim, D.F. (1991) dif, a recA-independent recombination site in the terminus region of the chromosome of Escherichia coli. New Biol 3 : 799 811.
27. Lemon, K.P., Kurtser, I., Wu, J. Grossman, A.D. (2001) Effects of replication termination mutants on chromosome partitioning in Bacillus subtilis. Proc Natl Acad Sci USA 98 : 212 217.
28. Leslie, N. Sherratt, D. (1995) Site-specific recombination in the replication terminus region of Escherichia coli: functional replacement of dif. EMBO J 4 : 1561 1570.
29. Levy, O., Ptacin, J.L., Pease, P.J., Gore, J., Eissen, M.B., Bustamante, C. Cozzarelli, N.R. (2005) Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc Natl Acad Sci USA 102 : 17618 17623.
30. Löwe, J., Ellonen, A., Allen, D., Atkinson, C., Sherratt, D. Grainge, I. (2008) Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol Cell 31 : 498 509.
31. Markovitz, A. (2005) A new in vivo termination function for DNA polymerase I of Escherichia coli K12. Mol Microbiol 55 : 1867 1882.
32. Massey, T.H., Mercogliano, C.P., Yates, J., Sherratt, D.J. Lowe, J. (2006) Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol Cell 23 : 457 469.
33. Morris, P., Binkley, J., Henson, J. Kuempel, P. (1985) Cloning and location of the dgsA gene E. coli. J Bacteriol 163 : 785 786.
34. Neylon, C., Kralicek, A., Hill, T. Dixon, N. (2005) Replication termination in Escherichia coli: structure and antihelicase activity of the Tus-Ter complex. Microbiol Mol Biol Rev 69 : 501 526.
35. Niki, H., Jaffé, A., Imamura, R., Ogura, T. Hiraga, S. (1991) The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J 10 : 183 193.
36. Perals, K., Cornet, F., Merlet, Y., Delon, I. Louarn, J.M. (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.
37. Prikryl, J., Hendricks, E. Kuempel, P. (2001) DNA degradation in the terminus region of resolvase mutants of Escherichia coli, and suppression of this degradation and the Dif phenotype by recD. Biochimie 83 : 171 176.
38. Ptacin, J., Nollmann, M., Becker, E., Cozzarelli, N., Pogliano, K. Bustamante, C. (2008) Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis. Nat Struct Mol Biol 15 : 485 493.
39. Recchia, G.D., Aroyo, M., Wolf, D., Blakely, G. Sherratt, D.J. (1999) FtsK-dependent and -independent pathways of Xer site-specific recombination. EMBO J 18 : 5724 5734.
40. Sherratt, D.J., Lau, I.F. Barre, F.-X. (2001) Chromosome segregation. Curr Opin Microbiol 4 : 653 659.
41. Sivanathan, V., Allen, M.D., de Bekker, C., Baker, R., Arciszewska, L., Freund, S.M., et al. (2006) The FtsKγ domain directs oriented DNA translocation by interacting with KOPS. Nat Struct Mol Biol 13 : 965 972.
42. Steiner, W.W. Kuempel, P.L. (1998) Sister-chromatid exchange frequencies in Escherichia coli analysed by recombination at the dif resolvase site. J Bacteriol 180 : 6269 6275.
43. Steiner, W., Liu, G., Donachie, W. Kuempel, P. (1999) The cytoplasmic domain of FtsK protein is required for resolution of chromosome dimers. Mol Microbiol 31 : 579 583.
44. Wu, L. Errington, J. (1994) Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. Science 264 : 572 575.
45. Yamanaka, K., Ogura, T., Niki, H. Hiraga, S. (1996) Identification of two new genes, mukE and mukF, involved in chromosome partitioning in Escherichia coli. Mol Gen Genet 250 : 241 251.
46. Yates, J., Zhekov, I., Baker, R., Eklund, B., Sherratt, D.J. Arciszewska, L.K. (2006) Dissection of a functional interaction between the DNA translocase, FtsK, and the XerD recombinase. Mol Microbiol 59 : 1754 1766.
47. Yu, X., Weihe, E. Margolin, W. (1998) Role of the C terminus of FtsK in Escherichia coli chromosome segregation. J Bacteriol 180 : 6424 6428.