Functional analysis of the cell division protein FtsW of Escherichia coli

Journal of Bacteriology

Volumn 186, Issue 24, 2004, Pages 8370-8379

  Pastoret, Soumya ^a   Fraipont, Claudine ^a   Den Blaauwen, Tanneke ^b   Wolf, Benoît ^a   Aarsman, Mirjam E G ^b   Piette, André ^a   Thomas, Annick ^a   Brasseur, Robert ^a   Nguyen Distèche, Martine ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MEMBRANE PROTEIN; PENICILLIN BINDING PROTEIN; PEPTIDOGLYCAN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CATALYSIS; CELL DIVISION; CROSS LINKING; FLUORESCENCE MICROSCOPY; GENETIC COMPLEMENTATION; MORPHOGENESIS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FAMILY; PROTEIN FOLDING; SITE DIRECTED MUTAGENESIS; SPOROGENESIS;

BACTERIAL PROTEINS; CELL DIVISION; ESCHERICHIA COLI; GENETIC COMPLEMENTATION TEST; GREEN FLUORESCENT PROTEINS; IMAGE PROCESSING, COMPUTER-ASSISTED; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MUTAGENESIS, SITE-DIRECTED; PEPTIDOGLYCAN; RECOMBINANT FUSION PROTEINS;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 10044283085     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.24.8370-8379.2004     Document Type: Article

References (56)

1. Addinall, S. G., and J. Lutkenhaus. 1996. FtsA is localized to the septum in an FtsZ-dependent manner. J. Bacteriol. 178:7167-7172.
2. Begg, K. J., A. Takasuga, D. H. Edwards, S. J. Dewar, B. G. Spratt, H. Adachi, T. Ohta, H. Matsuzawa, and W. D. Donachie. 1990. The balance between different peptidoglycan precursors determines whether Escherichia coli cells will elongate or divide. J. Bacteriol. 172:6697-6703.
3. Boyle, D. S., M. M. Khattar, S. G. Addinall, J. Lutkenhaus, and W. D. Donachie. 1997. ftsW is an essential cell-division gene in Escherichia coli. Mol. Microbiol. 24:1263-1273.
4. Buddelmeijer, N., and J. Beckwith. 2002. Assembly of cell division proteins at the E. coli cell center. Curr. Opin. Microbiol. 5:553-557.
5. Buddelmeijer, N., and J. Beckwith. 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.
6. Buddelmeijer, N., N. Judson, D. Boyd, J. J. Mekalanos, and J. Beckwith. 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. USA 99:6316-6321.
7. Chen, J. C., and J. Beckwith. 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.
8. Daniel, R. A., S. Drake, C. E. Buchanan, R. Scholle, and J. Errington. 1994. The Bacillus subtilis spoVD gene encodes a mother-cell-specific penicillin-binding protein required for spore morphogenesis. J. Mol. Biol. 235:209-220.
9. De Loof, H., M. Rosseneu, R. Brasseur, and J. M. Ruysschaert. 1986. Use of hydrophobicity profiles to predict receptor binding domains on apolipoprotein E and the low density lipoprotein apolipoprotein B-E receptor. Proc. Natl. Acad. Sci. USA 83:2295-2299.
10. den Blaauwen, T., A. Lindqvist, J. Löwe, and N. Nanninga. 2001. Distribution of the Escherichia coli structural maintenance of chromosomes (SMC)-like protein MukB in the cell. Mol. Microbiol. 42:1179-1188.
11. den Blaauwen, T, M. E. G. Aarsman, N. O. E. Vischer, and N. Nanninga. 2003. Penicillin-binding protein PBP2 of Escherichia coli localizes preferentially in the lateral wall and at mid-cell in comparison with the old cell pole. Mol. Microbiol. 47:539-547.
12. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
13. Di Lallo, G., M. Fagioli, P. Gheraldini, and L. Paolozzi. 2003. Use of a two-hybrid system to study the assembly of a complex multicomponent protein machinery: bacterial septosome differentiation. Microbiology 149:3353-3359.
14. Eisenberg, D., R. M. Weiss, and T. C. Terwilliger. 1982. The helical hydrophobic moment: a measure of the amphiphilicity of a helix. Nature 299:371-374.
15. Eisenberg, D., E. Schwarz, M. Komaromy, and R. Wall. 1984. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J. Mol. Biol. 179:125-142.
16. Errington, J., R. A. Daniel, and D.-J. Scheffers. 2003. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67:52-65.
17. Figge, R. M., A. V. Divakaruni, and W. J. Gober. 2004. MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol. Microbiol. 51:1321-1332.
18. Gallet, X., B. Charloteaux, A. Thomas, and R. Brasseur. 2000. A fast method to predict protein interaction sites from sequences. J. Mol. Biol. 302:917-926.
19. Gérard, P., T. Vernet, and A. Zapun. 2002. Membrane topology of the Streptococcus pneumoniae FtsW division protein. J. Bacteriol. 184:1925-1931.
20. Heidrich, C., M. F. Templin, A. Ursinus, M. Merdanosic, J. Berger, H. Schwarz, M. A. de Pedro, and J. V. Holtje. 2001. Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol. Microbiol. 41:167-178.
21. Henriques, A. O., H. de Lencastre, and P. J. Piggot. 1992. A Bacillus subtilis morphogene cluster that includes spoVE is homologous to the mra region of Escherichia coli. Biochimie 74:735-748.
22. Henriques, A. O., P. Glaser, P. J. Piggot, and C. P. Moran, Jr. 1998. Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol. Microbiol. 28:235-247.
23. Ikeda, M., T. Sato, M. Wachi, H. K. Jung, F. Ishino, Y. Kobayashi, and M. Matsuhashi. 1989. Structural similarity among Escherichia coli FtsW and RodA proteins and Bacillus subtilis SpoVE protein, which function in cell division, cell elongation, and spore formation, respectively. J. Bacteriol. 171:6375-6378.
24. Ishino, F., H. K. Jung, M. Ikeda, M. Doi, M. Wachi, and M. Matsuhashi. 1989. New mutations fts-36, lts-33, and ftsW clustered in the mra region of the Escherichia coli chromosome induce thermosensitive cell growth and division. J. Bacteriol. 171:5523-5530.
25. Jones, L. J., R. Carballido-Lopez, and J. Errington. 2001. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913-922.
26. Joris, B., G. Dive, A. Henriques, P. J. Piggot, and J. M. Ghuysen. 1990. The life-cycle proteins RodA of Escherichia coli and SpoVE of Bacillus subtilis have very similar primary structures. Mol. Microbiol. 4:513-517.
27. Kamman, M., J. Laufs, J. Schell, and B. Gronenborn. 1989. Rapid insertion mutagenesis of DNA by polymerase chain reaction (PCR). Nucleic Acids Res. 17:5404.
28. Khattar, M. M., S. G. Addinall, K. H. Stedul, D. S. Boyle, J. Lutkenhaus, and W. D. Donachie. 1997. Two polypeptide products of the Escherichia coli cell division gene ftsW and a possible role for FtsW in FtsZ function. J. Bacteriol. 179:784-793.
29. Khattar, M. M., K. J. Begg, and W. D. Donachie. 1994. Identification of FtsW and characterization of a new ftsW division mutant of Escherichia coli. J. Bacteriol. 176:7140-7147.
30. Kini, R. M., and J. H. Evans. 1995. A hypothetical structural role for proline residues in the flanking segments of protein-protein interaction sites. Biochem. Biophys. Res. Commun. 212:115-1124.
31. Koppelman, C. M., M. E. G. Aarsman, J. Postmus, E. Pas, A. O. Muysers, D. J. Scheffers, N. Nanninga, and T. den Blaauwen. 2004. R174 of Escherichia coli FtsZ is involved in membrane interaction and protofilament bundling, and is essential for cell division. Mol. Microbiol. 51:645-657.
32. Kruse, T., J. Moller-Jensen, A. Lobner-Olesen, and K. Gerdes. 2003. Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J. 22:5283-5292.
33. Lara, B., and J. A. Ayala. 2002. Topological characterization of the essential Escherichia coli cell division protein FtsW. FEMS Microbiol. Lett. 216:23-32.
34. Löwe, J., and L. A. Amos. 1998. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391:203-206.
35. Lutkenhaus, J., and S. G. Addinall. 1997. Bacterial cell division and the Z ring. Annu. Rev. Biochem. 66:93-116.
36. Margolin, W. 2000. Themes and variations in prokaryotic cell division. FEMS Microbiol. Rev. 24:531-548.
37. Marrec-Fairley, M., A. Piette, X. Gallet, R. Brasseur, H. Hara, C. Fraipont, J. M. Ghuysen, and M. Nguyen-Distèche. 2000. Differential functionalities of amphiphilic peptide segments of the cell-septation penicillin-binding protein 3 of Escherichia coli. Mol. Microbiol. 37:1019-1031.
38. Matsuhashi, M., M. Wachl, and F. Ishino. 1990. Machinery for cell growth and division: penicillin-binding proteins and other proteins. Res. Microbiol. 141:89-103.
39. Matsuhashi, M. 1994. Utilization of lipid-linked precursors and the formation of peptidoglycan in the process of cell growth and division: membrane enzymes involved in the final steps of peptidoglycan synthesis and the mechanism of their regulation. New Compr. Biochem. 27:55-71.
40. Mercer, K. L., and D. S. Weiss. 2002. The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site. J. Bacteriol. 184:904-912.
41. Nakano, Y., Y. Yoshida, Y. Yamashita, and T. Koga. 1995. Construction of a series of pACYC-derived plasmid vectors. Gene 162:157-158.
42. Nanninga, N. 1998. Morphogenesis of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:110-129.
43. Pichoff, S., and J. Lutkenhaus. 2002. Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 21:685-693.
44. Piette, A., C. Fraipont, T. den Blaauwen, M. E. G. Aarsman, S. Pastoret, and M. Nguyen-Distèche. 2004. Structural determinants required to target penicillin-binding protein 3 to the septum of Escherichia coli. J. Bacteriol. 186:6110-6117.
45. Russ, W. P., and D. M. Engelman. 2000. The GxxxG motif: a framework for transmembrane helix-helix association. J. Mol. Biol. 296:911-919.
46. Senes, A., M. Gerstein, and D. M. Engelman. 2000. Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions. J. Mol. Biol. 296:921-936.
47. Senes, A., I. Ubarretxena-Belandia, and D. M. Engelman. 2001. The Cα-H...O hydrogen bond: a determinant of stability and specificity in transmembrane helix interactions. Proc. Natl. Acad. Sci. USA 98:9056-9061.
48. Shih, Y. L., T. Le, and L. Rothfield. 2003. Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles. Proc. Natl. Acad. Sci. USA 100:7865-7870.
49. Spratt, B. G. 1975. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc. Natl. Acad. Sci. USA 72:2999-3003.
50. Stoker, N. G., J. K. Broome-Smith, A. Edelman, and B. G. Spratt. 1983. Organization and subcloning of the dacA-rodA-pbpA cluster of cell shape genes in Escherichia coli. J. Bacteriol. 155:847-853.
51. Taschner, P. E., P. G. Huls, E. Pas, and C. L. Woldringh. 1988. Division behavior and shape changes in isogenic ftsZ, ftsQ, ftsA, pbpB, and ftsE cell division mutants of Escherichia coli during temperature shift experiments. J. Bacteriol. 170:1533-1540.
52. Van den Ent, F., and J. Löwe. 2000. Crystal structure of the cell division protein FtsA from Thermotoga maritima. EMBO J. 19:5300-5307.
53. Wachi, M., M. Doi, Y. Okada, and M. Matsuhashi. 1989. New mre genes mreC and mreD, responsible for formation of the rod shape of Escherichia coli cells. J. Bacteriol. 171:6511-6516.
54. Wachi, M., and M. Matsuhashi. 1989. Negative control of cell division by mreB, a gene that functions in determining the rod shape of Escherichia coli cells. J. Bacteriol. 171:3123-3127.
55. Weiss, D. S., J. C. Chen, J.-M. Ghigo, D. Boyd, and J. Beckwith. 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.
56. Wissel, M. C., and D. S. Weiss. 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.