Premature targeting of a cell division protein to midcell allows dissection of divisome assembly in Escherichia coli

Genes and Development

Volumn 19, Issue 1, 2005, Pages 127-137

  Goehring, Nathan W ^a   Gueiros Filho, Frederico ^b,c   Beckwith, Jon ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Cell division; Divisome; FtsQ; Septal targeting; ZapA

Indexed keywords

BACTERIAL PROTEIN; CELL CYCLE PROTEIN; CYTOSKELETON PROTEIN; ESCHERICHIA COLI PROTEIN; MEMBRANE PROTEIN; PENICILLIN BINDING PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; CELL COMPARTMENTALIZATION; CELL DIVISION; CONTROLLED STUDY; CYTOPLASM; DIMERIZATION; ESCHERICHIA COLI; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TWO HYBRID SYSTEM;

CELL CYCLE PROTEINS; CELL DIVISION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 11844267151     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1253805     Document Type: Article

References (39)

1. Anderson, D.E., Gueiros-Filho, F.J., and Erickson, H.P. 2004. Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J. Bacteriol. 186: 5775-5781.
2. Bi, E.F. and Lutkenhaus, J. 1991. FtsZ ring structure associated with division in Escherichia coli. Nature 354: 161-164.
3. Bork, P., Sander, C., and Valencia, A. 1992. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc. Natl. Acad. Sci. 89: 7290-7294.
4. Boyd, D., Weiss, D.S., Chen, J.C., and Beckwith, J. 2000. Towards single-copy gene expression systems making gene cloning physiologically relevant: λ InCh, a simple Escherichia coli plasmid-chromosome shuttle system. J. Bacteriol. 182: 842-847.
5. Buddelmeijer, N. and Beckwith, J. 2002. Assembly of cell division proteins at the E. coli cell center. Curr. Opin. Microbiol. 5: 553-557.
6. _. 2004. A complex of the Escherichia coli cell division proteins FtsL, FtsB and FtsQ forms independently of its localization to the septal region. Mol. Microbiol. 52: 1315-1327.
7. Buddelmeijer, N., Judson, N., Boyd, D., Mekalanos, J.J., and Beckwith, J. 2002. YgbQ, a cell division protein in Escherichia coli and Vibrio cholerae, localizes in codependent fashion with FtsL to the division site. Proc. Natl. Acad. Sci. 99: 6316-6321.
8. Carson, M.J., Barondess, J., and 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.
9. Chen, J.C. and Beckwith, J. 2001. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol. Microbiol. 42: 395-413.
10. Chen, J.C., Weiss, D.S., Ghigo, J.M., and Beckwith, J. 1999. Septal localization of FtsQ, an essential cell division protein in Escherichia coli. J. Bacteriol. 181: 521-530.
11. Dai, K., Xu, Y., and Lutkenhaus, J. 1993. Cloning and characterization of ftsN, an essential cell division gene in Escherichia coli isolated as a multicopy suppressor of ftsA12(Ts). J. Bacteriol. 175: 3790-3797.
12. _. 1996. Topological characterization of the essential Escherichia coli cell division protein FtsN. J. Bacteriol. 178: 1328-1334.
13. Di Lallo, G., Fagioli, M., Barionovi, D., Ghelardini, P., and 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.
14. Draper, G.C., McLennan, N., Begg, K., Masters, M., and Donachie, W.D. 1998. Only the N-terminal domain of FtsK functions in cell division. J. Bacteriol. 180: 4621-4627.
15. Errington, J., Daniel, R.A., and Scheffers, D.J. 2003. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67: 52-65.
16. Ghigo, J.M., Weiss, D.S., Chen, J.C., Yarrow, J.C., and Beckwith, J. 1999. Localization of FtsL to the Escherichia coli septal ring. Mol. Microbiol. 31: 725-737.
17. Gueiros-Filho, F.J. and Losick, R. 2002. A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes & Dev. 16: 2544-2556.
18. Guzman, L.M., Barondess, J.J., and Beckwith, J. 1992. FtsL, an essential cytoplasmic membrane protein involved in cell division in Escherichia coli. J. Bacteriol. 174: 7716-7728.
19. Guzman, L.M., Weiss, D.S., and Beckwith, J. 1997. Domain-swapping analysis of FtsI, FtsL, and FtsQ, bitopic membrane proteins essential for cell division in Escherichia coli. J. Bacteriol. 179: 5094-5103.
20. Hale, C.A. and de Boer, P.A. 1997. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell 88: 175-185.
21. _. 2002. ZipA is required for recruitment of FtsK, FtsQ, FtsL, and FtsN to the septal ring in Escherichia coli. J. Bacteriol. 184: 2552-2556.
22. Johnson, J.E., Lackner, L.L., Hale, C.A., and de Boer, P.A. 2004. ZipA is required for targeting of DMinC/DicB, but not DMinC/MinD, complexes to septal ring assemblies in Escherichia coli. J. Bacteriol. 186: 2418-2429.
23. Low, H.H., Moncrieffe, M.C., and Lowe, J. 2004. The crystal structure of ZapA and its modulation of FtsZ polymerisation. J. Mol. Biol. 341: 839-852.
24. Lowe, J. and Amos, L.A. 1998. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391: 203-206.
25. Ma, X. and Margolin, W. 1999. Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J. Bacteriol. 181: 7531-7544.
26. Margolin, W. 2000. Themes and variations in prokaryotic cell division. FEMS Microbiol. Rev. 24: 531-548.
27. Miller, J.H. 1992. A short course in bacterial genetics: A laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
28. Morlot, C., Noirclerc-Savoye, M., Zapun, A., Dideberg, O., and Vernet, T. 2004. The D,D-carboxypeptidase PBP3 organizes the division process of Streptococcus pneumoniae. Mol. Microbiol. 51: 1641-1648.
29. Mosyak, L., Zhang, Y., Glasfeld, E., Haney, S., Stahl, M., Seehra, J., and Somers, W.S. 2000. The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J. 19: 3179-3191.
30. Moy, F.J., Glasfeld, E., Mosyak, L., and Powers, R. 2000. Solution structure of ZipA, a crucial component of Escherichia coli cell division. Biochemistry 39: 9146-9156.
31. Mukherjee, A., Dai, K., and Lutkenhaus, J. 1993. Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc. Natl. Acad. Sci. 90: 1053-1057.
32. Pichoff, S. and Lutkenhaus, J. 2002. Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 21: 685-693.
33. Romberg, L. and Levin, P.A. 2003. Assembly dynamics of the bacterial cell division protein FTSZ: Poised at the edge of stability. Annu. Rev. Microbiol. 57: 125-154.
34. van den Ent, F. and Lowe, J. 2000. Crystal structure of the cell division protein FtsA from Thermotoga maritima. EMBO J. 19: 5300-5307.
35. van Helvoort, J.M. and Woldringh, C.L. 1994. Nucleoid partitioning in Escherichia coli during steady-state growth and upon recovery from chloramphenicol treatment. Mol. Microbiol. 13: 577-583.
36. Wang, X., Huang, J., Mukherjee, A., Cao, C., and Lutkenhaus, J. 1997. Analysis of the interaction of FtsZ with itself, GTP, and FtsA. J. Bacteriol. 179: 5551-5559.
37. Weiss, D.S., Chen, J.C., Ghigo, J.M., Boyd, D., and Beckwith, J. 1999. Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL. J. Bacteriol. 181: 508-520.
38. Wissel, M.C. and Weiss, D.S. 2004. Genetic analysis of the cell division protein FtsI (PBP3): Amino acid substitutions that impair septal localization of FtsI and recruitment of FtsN. J. Bacteriol. 186: 490-502.
39. Yan, K., Pearce, K.H., and Payne, D.J. 2000. A conserved residue at the extreme C terminus of FtsZ is critical for the FtsA-FtsZ interaction in Staphylococcus aureus. Biochem. Biophys. Res. Commun. 270: 387-392.