The N-terminal membrane-spanning domain of the Escherichia coli DNA translocase FtsK hexamerizes at midcell

mBio

Volumn 4, Issue 6, 2013, Pages

  Bisicchia, Paola ^a   Steel, Bradley ^b   Mariam Debela, Mekdes H ^c   Löwe, Jan ^c   Sherratt, David ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DICARBOXYLATE TRANSPORTER; MEMBRANE PROTEIN; PROTEIN FTSK; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; FTSK PROTEIN, E COLI;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CHROMOSOME REPLICATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; ESCHERICHIA COLI; IN VITRO STUDY; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PURIFICATION; HUMAN; METABOLISM; PROTEIN MULTIMERIZATION;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HUMANS; MEMBRANE PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION;

EID: 84891587996     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00800-13     Document Type: Article

References (48)

1. Hirota Y, Ryter A, Jacob F. 1968. Thermosensitive mutants of E. coli affected in the processes of DNA synthesis and cellular division. Cold Spring Harb. Symp. Quant. Biol. 33:677-693.
2. Van De Putte P, Van D, Roersch A. 1964. The selection of mutants of Escherichia coli with impaired cell division at elevated temperature. Mutat. Res. 106:121-128.
3. Egan AJ, Vollmer W. 2013. The physiology of bacterial cell division. Ann. N. Y. Acad. Sci. 1277:8-28.
4. Goehring NW, Beckwith J. 2005. Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr. Biol. 15:R514-R526.
5. Lutkenhaus J, Pichoff S, Du S. 2012. Bacterial cytokinesis: from Z ring to divisome. Cytoskeleton 69:778-790.
6. Adams DW, Errington J. 2009. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat. Rev. Microbiol. 7:642-653.
7. Erickson HP, Anderson DE, Osawa M. 2010. FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol. Mol. Biol. Rev. 74:504-528.
8. Löwe J, Ellonen A, Allen MD, Atkinson C, Sherratt DJ, Grainge I. 2008. Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol. Cell 31:498-509.
9. Liu G, Draper GC, Donachie WD. 1998. FtsK is a bifunctional protein involved in cell division and chromosome localization in Escherichia coli. Mol. Microbiol. 29:893-903.
10. Bigot S, Corre J, Louarn JM, Cornet F, Barre FX. 2004. FtsK activities in Xer recombination, DNA mobilization and cell division involve overlapping and separate domains of the protein. Mol. Microbiol. 54:876-886.
11. Pérals K, Capiaux H, Vincourt JB, Louarn JM, Sherratt DJ, Cornet F. 2001. Interplay between recombination, cell division and chromosome structure during chromosome dimer resolution in Escherichia coli. Mol. Microbiol. 39:904-913.
12. Bigot S, Sivanathan V, Possoz C, Barre FX, Cornet F. 2007. FtsK, a literate chromosome segregation machine. Mol. Microbiol. 64: 1434-1441.
13. Draper GC, McLennan N, Begg K, Masters M, Donachie WD. 1998. Only the N-terminal domain of FtsK functions in cell division. J. Bacteriol. 180:4621-4627.
14. Yu XC, Tran AH, Sun Q, Margolin W. 1998. Localization of cell division protein FtsK to the Escherichia coli septum and identification of a potential N-terminal targeting domain. J. Bacteriol. 180:1296-1304.
15. Di Lallo G, Fagioli M, Barionovi D, Ghelardini P, Paolozzi L. 2003. Use of a two-hybrid assay to study the assembly of a complex multicomponent protein machinery: bacterial septosome differentiation. Microbiology 149:3353-3359.
16. Geissler B, Margolin W. 2005. Evidence for functional overlap among multiple bacterial cell division proteins: compensating for the loss of FtsK. Mol. Microbiol. 58:596-612.
17. Dubarry N, Possoz C, Barre FX. 2010. Multiple regions along the Escherichia coli FtsK protein are implicated in cell division. Mol. Microbiol. 78:1088-1100.
18. Aussel L, Barre FX, Aroyo M, Stasiak A, Stasiak AZ, 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.
19. Capiaux H, Lesterlin C, Pérals K, Louarn JM, Cornet F. 2002. A dual role for the FtsK protein in Escherichia coli chromosome segregation. EMBO Rep. 3:532-536.
20. Espeli O, Levine C, Hassing H, Marians KJ. 2003. Temporal regulation of topoisomerase IV activity in E. coli. Mol. Cell 11:189-201.
21. Espeli O, Lee C, Marians KJ. 2003. A physical and functional interaction between Escherichia coli FtsK and topoisomerase IV. J. Biol. Chem. 278: 44639-44644.
22. Lesterlin C, Barre FX, Cornet F. 2004. Genetic recombination and the cell cycle: what we have learned from chromosome dimers. Mol. Microbiol. 54:1151-1160.
23. Steiner WW, Kuempel PL. 1998. Cell division is required for resolution of dimer chromosomes at the dif locus of Escherichia coli. Mol. Microbiol. 27:257-268.
24. Steiner W, Liu G, Donachie WD, Kuempel P. 1999. The cytoplasmic domain of FtsK protein is required for resolution of chromosome dimers. Mol. Microbiol. 31:579-583.
25. Yates J, Aroyo M, Sherratt DJ, Barre FX. 2003. Species specificity in the activation of Xer recombination at dif by FtsK. Mol. Microbiol. 49: 241-249.
26. Stouf M, Meile JC, Cornet F. 18 June 2013. FtsK actively segregates sister chromosomes in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. doi:10.1073/pnas.1304080110.
27. Wu LJ, Errington J. 1994. Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. Science 264:572-575.
28. Bath J, Wu LJ, Errington J, Wang JC. 2000. Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science 290:995-997.
29. Ptacin JL, Nollmann M, Becker EC, Cozzarelli NR, Pogliano K, Bustamante C. 2008. Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis. Nat. Struct. Mol. Biol. 15:485-493.
30. Errington J, Bath J, Wu LJ. 2001. DNA transport in bacteria. Nat. Rev. Mol. Cell Biol. 2:538-545.
31. Massey TH, Mercogliano CP, Yates J, Sherratt DJ, Löwe J. 2006. Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol. Cell 23:457-469.
32. Sherratt DJ, Arciszewska LK, Crozat E, Graham JE, Grainge I. 2010. The Escherichia coli DNA translocase FtsK. Biochem. Soc. Trans. 38:-395-398.
33. Wang X, Possoz C, Sherratt DJ. 2005. Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli. Genes Dev. 19: 2367-2377.
34. Kennedy SP, Chevalier F, Barre FX. 2008. Delayed activation of Xer recombination at dif by FtsK during septum assembly in Escherichia coli. Mol. Microbiol. 68:1018-1028.
35. Grenga L, Luzi G, Paolozzi L, Ghelardini P. 2008. The Escherichia coli FtsK functional domains involved in its interaction with its divisome protein partners. FEMS Microbiol. Lett. 287:163-167.
36. Reyes-Lamothe R, Sherratt DJ, Leake MC. 2010. Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science 328:498-501.
37. Crozat E, Grainge I. 2010. FtsK DNA translocase: the fast motor that knows where it's going. Chembiochem 11:2232-2243.
38. Recchia GD, Aroyo M, Wolf D, Blakely G, Sherratt DJ. 1999. FtsK dependent and independent pathways of Xer site-specific recombination. EMBO J. 18:5724-5734.
39. Fukuoka H, Sowa Y, Kojima S, Ishijima A, Homma M. 2007. Visualization of functional rotor proteins of the bacterial flagellar motor in the cell membrane. J. Mol. Biol. 367:692-701.
40. Saxton MJ, Jacobson K. 1997. Single-particle tracking: applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26:373-399.
41. Hale CA, Shiomi D, Liu B, Bernhardt TG, Margolin W, Niki H, de Boer PA. 2011. Identification of Escherichia coli ZapC (YcbW) as a component of the division apparatus that binds and bundles FtsZ polymers. J. Bacteriol. 193:1393-1404.
42. Gerding MA, Ogata Y, Pecora ND, Niki H, de Boer PA. 2007. The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Mol. Microbiol. 63:1008-1025.
43. Carson MJ, Barondess J, Beckwith J. 1991. The FtsQ protein of Escherichia coli: membrane topology, abundance, and cell division phenotypes due to overproduction and insertion mutations. J. Bacteriol. 173: 2187-2195.
44. van den Ent F, Vinkenvleugel TM, Ind A, West P, Veprintsev D, Nanninga N, den Blaauwen T, Löwe J. 2008. Structural and mutational analysis of the cell division protein FtsQ. Mol. Microbiol. 68:110-123.
45. Karimova G, Dautin N, Ladant D. 2005. Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J. Bacteriol. 187:2233-2243.
46. D'Ulisse V, Fagioli M, Ghelardini P, Paolozzi L. 2007. Three functional subdomains of the Escherichia coli FtsQ protein are involved in its interaction with the other division proteins. Microbiology 153:124-138.
47. Zhang XY, Goemaere EL, Seddiki N, Célia H, Gavioli M, Cascales E, Lloubes R. 2011. Mapping the interactions between Escherichia coli TolQ transmembrane segments. J. Biol. Chem. 286:11756-11764.
48. Burton BM, Marquis KA, Sullivan NL, Rapoport TA, Rudner DZ. 2007. The ATPase SpoIIIE transports DNA across fused septal membranes during sporulation in Bacillus subtilis. Cell 131:1301-1312