Bacterial cell division: Assembly, maintenance and disassembly of the Z ring

Nature Reviews Microbiology

Volumn 7, Issue 9, 2009, Pages 642-653

  Adams, David W ^a   Errington, Jeff ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ENDOPEPTIDASE CLPX; FTSZ PROTEIN; PROTEIN EZRA; PROTEIN FTSA; PROTEIN MCIZ; PROTEIN SEPF; PROTEIN SULA; PROTEIN UGTP; PROTEIN ZAPA; PROTEIN ZAPB; PROTEIN ZIPA; TUBULIN; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GLUCOSE;

BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL REPRODUCTION; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE REGULATION; CELL DIVISION; CELL KINETICS; CRYSTAL STRUCTURE; ESCHERICHIA COLI; MICROBIAL ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; STREPTOCOCCUS PNEUMONIAE; SYNECHOCOCCUS ELONGATUS;

BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL PROTEINS; CELL DIVISION; CYTOSKELETAL PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION;

BACTERIA (MICROORGANISMS);

EID: 69249126551     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2198     Document Type: Review

References (155)

1. Errington, J., Daniel, R. A. & Scheffers, D. J. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67, 52-65 (2003).
2. Goehring, N. W. & Beckwith, J. Diverse paths to midcell: Assembly of the bacterial cell division machinery. Curr. Biol. 15, R514-R526 (2005).
3. Harry, E., Monahan, L. & Thompson, L. Bacterial cell division: The mechanism and its precison. Int. Rev. Cytol. 253, 27-94 (2006).
4. Bi, E. F. & Lutkenhaus, J. FtsZ ring structure associated with division in Escherichia coli. Nature 354, 161-164 (1991).
5. Addinall, S. G. & Lutkenhaus, J. FtsZ-spirals and -arcs determine the shape of the invaginating septa in some mutants of Escherichia coli. Mol. Microbiol. 22, 231-237 (1996).
6. Margolin, W. FtsZ and the division of prokaryotic cells and organelles. Nature Rev. Mol. Cell Biol. 6, 862-871 (2005).
7. Haydon, D. J. et al. An inhibitor of FtsZ with potent and selective anti-staphylococcal activity. Science 321, 1673-1675 (2008).
8. Kelly, A. J., Sackett, M. J., Din, N., Quardokus, E. & Brun, Y. V. Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. Genes Dev. 12, 880-893 (1998).
9. Quardokus, E., Din, N. & Brun, Y. V. Cell cycle regulation and cell type-specific localization of the FtsZ division initiation protein in Caulobacter. Proc. Natl Acad. Sci. USA 93, 6314-6319 (1996).
10. Rueda, S., Vicente, M. & Mingorance, J. Concentration and assembly of the division ring proteins FtsZ, FtsA, and ZipA during the Escherichia coli cell cycle. J. Bacteriol. 185, 3344-3351 (2003).
11. Weart, R. B. & Levin, P. A. Growth rate-dependent regulation of medial FtsZ ring formation. J. Bacteriol. 185, 2826-2834 (2003).
12. Romberg, L. & Levin, P. A. Assembly dynamics of the bacterial cell division protein FtsZ: Poised at the edge of stability. Annu. Rev. Microbiol. 57, 125-154 (2003).
13. Löwe, J. & Amos, L. A. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391, 203-206 (1998).
14. Nogales, E., Wolf, S. G. & Downing, K. H. Structure of the αβ tubulin dimer by electron crystallography. Nature 391, 199-203 (1998).
15. Erickson, H. P. FtsZ, a prokaryotic homolog of tubulin? Cell 80 367-370 (1995).
16. Mukherjee, A. & Lutkenhaus, J. Guanine nucleotide-dependent assembly of FtsZ into filaments. J. Bacteriol. 176, 2754-2758 (1994).
17. Erickson, H. P., Taylor, D. W., Taylor, K. A. & Bramhill, D. Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc. Natl Acad. Sci. USA 93, 519-523 (1996).
18. 2+-induced FtsZ sheets. EMBO J. 18, 2364-2371 (1999).
19. Oliva, M. A., Cordell, S. C. & Löwe, J. Structural insights into FtsZ protofilament formation. Nature Struct. Mol. Biol. 11, 1243-1250 (2004).
20. de Boer, P., Crossley, R. & Rothfield, L. The essential bacterial cell-division protein FtsZ is a GTPase. Nature 359, 254-256 (1992).
21. RayChaudhuri, D. & Park, J. T. Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature 359, 251-254 (1992).
22. Mukherjee, A., Dai, K. & Lutkenhaus, J. Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc. Natl Acad. Sci. USA 90, 1053-1057 (1993).
23. Scheffers, D. J., de Wit, J. G., den Blaauwen, T. & Driessen, A. J. Substitution of a conserved aspartate allows cation-induced polymerization of FtsZ. FEBS Lett. 494, 34-37 (2001).
24. Scheffers, D. J., de Wit, J. G., den Blaauwen, T. & Driessen, A. J. GTP hydrolysis of cell division protein FtsZ: Evidence that the active site is formed by the association of monomers. Biochemistry 41, 521-529 (2002).
25. Romberg, L., Simon, M. & Erickson, H. P. Polymerization of Ftsz, a bacterial homolog of tubulin: Is assembly cooperative? J. Biol. Chem. 276, 11743-11753 (2001).
26. Caplan, M. R. & Erickson, H. P. Apparent cooperative assembly of the bacterial cell division protein FtsZ demonstrated by isothermal titration calorimetry. J. Biol. Chem. 278, 13784-13788 (2003).
27. Chen, Y., Bjornson, K., Redick, S. D. & Erickson, H. P. A rapid fluorescence assay for FtsZ assembly indicates cooperative assembly with a dimer nucleus. Biophys. J. 88, 505-514 (2005).
28. Wang, X. & Lutkenhaus, J. The FtsZ protein of Bacillus subtilis is localized at the division site and has GTPase activity that is dependent upon FtsZ concentration. Mol. Microbiol. 9, 435-442 (1993).
29. Romberg, L. & Mitchison, T. J. Rate-limiting guanosine 5′-triphosphate hydrolysis during nucleotide turnover by FtsZ, a prokaryotic tubulin homologue involved in bacterial cell division. Biochemistry 43 282-288 (2004).
30. Mukherjee, A. & Lutkenhaus, J. Dynamic assembly of FtsZ regulated by GTP hydrolysis. EMBO J. 17, 462-469 (1998).
31. Bramhill, D. & Thompson, C. M. GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc. Natl Acad. Sci. USA 91, 5813-5817 (1994).
32. Popp, D., Iwasa, M., Narita, A., Erickson, H. P. & Maéda, Y. FtsZ condensates: An in vitro electron microscopy study. Biopolymers 91, 340-350 (2009).
33. Li, Z., Trimble, M. J., Brun, Y. V. & Jensen, G. J. The structure of FtsZ filaments in vivo suggests a forcegenerating role in cell division. EMBO J. 26, 4694-4708 (2007).
34. Chen, Y. & Erickson, H. P. Rapid in vitro assembly dynamics and subunit turnover of FtsZ demonstrated by fluorescence resonance energy transfer. J. Biol. Chem. 280, 22549-22554 (2005).
35. Dajkovic, A., Mukherjee, A. & Lutkenhaus, J. Investigation of regulation of FtsZ assembly by SulA and development of a model for FtsZ polymerization. J. Bacteriol. 190, 2513-2526 (2008).
36. Huecas, S. et al. Energetics and geometry of FtsZ polymers: nucleated self-assembly of single protofilaments. Biophys. J. 94, 1796-1806 (2008).
37. Miraldi, E. R., Thomas, P. J. & Romberg, L. Allosteric models for cooperative polymerization of linear polymers. Biophys. J. 95 2470-2486 (2008).
38. Lu, C., Stricker, J. & Erickson, H. P. FtsZ from Escherichia coli, Azotobacter vinelandii, and Thermotoga maritima - quantitation, GTP hydrolysis, and assembly. Cell. Motil. Cytoskeleton 40, 71-86 (1998).
39. Mingorance, J., Rueda, S., Gómez-Puertas, P., Valencia, A. & Vicente, M. Escherichia coli FtsZ polymers contain mostly GTP and have a high nucleotide turnover. Mol. Microbiol. 41, 83-91 (2001).
40. Stricker, J., Maddox, P., Salmon, E. D. & Erickson, H. P. Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc. Natl Acad. Sci. USA 99, 3171-3175 (2002).
41. Anderson, D. E., Gueiros-Filho, F. J. & Erickson, H. P. Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J. Bacteriol. 186, 5775-5781 (2004).
42. Levin, P. A., Schwartz, R. L. & Grossman, A. D. Polymer stability plays an important role in the positional regulation of FtsZ. J. Bacteriol. 183, 5449-5452 (2001).
43. Lu, C., Reedy, M. & Erickson, H. P. Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J. Bacteriol. 182, 164-170 (2000).
44. Oliva, M. A., Trambaiolo, D. & Löwe, J. Structural insights into the conformational variability of FtsZ. J. Mol. Biol. 373, 1229-1242 (2007).
45. Mukherjee, A., Saez, C. & Lutkenhaus, J. Assembly of an FtsZ mutant deficient in GTPase activity has implications for FtsZ assembly and the role of the Z ring in cell division. J. Bacteriol. 183, 7190-7197 (2001).
46. Erickson, H. P. Modeling the physics of FtsZ assembly and force generation. Proc. Natl Acad. Sci. USA 106, 9238-9243 (2009).
47. Osawa, M., Anderson, D. E. & Erickson, H. P. Reconstitution of contractile FtsZ rings in liposomes. Science 320, 792-794 (2008).
48. Lan, G., Daniels, B. R., Dobrowsky, T. M., Wirtz, D. & Sun, S. X. Condensation of FtsZ filaments can drive bacterial cell division. Proc. Natl Acad. Sci. USA 106, 121-126 (2009).
49. Nogales, E., Downing, K. H., Amos, L. A. & Löwe, J. Tubulin and FtsZ form a distinct family of GTPases. Nature Struct. Biol. 5, 451-458 (1998).
50. Ma, X. & Margolin, W. Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J. Bacteriol. 181, 7531-7544 (1999).
51. Erickson, H. P. The FtsZ protofilament and attachment of ZipA - structural constraints on the FtsZ power stroke. Curr. Opin. Cell Biol. 13, 55-60 (2001).
52. Vaughan, S., Wickstead, B., Gull, K. & Addinall, S. G. Molecular evolution of FtsZ protein sequences encoded within the genomes of Archaea, Bacteria, and Eukaryota. J. Mol. Evol. 58, 19-29 (2004).
53. Erickson, H. P. FtsZ, a tubulin homologue in prokaryote cell division. Trends Cell Biol. 7, 362-367 (1997).
54. Pichoff, S. & Lutkenhaus, J. Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 21 685-693 (2002).
55. Hale, C. A. & de Boer, P. A. J. 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 (1997).
56. Hale, C. A. & de Boer, P. A. J. Recruitment of ZipA to the septal ring of Escherichia coli is dependent on FtsZ and independent of FtsA. J. Bacteriol. 181, 167-176 (1999).
57. Mosyak, L. et al. The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J. 19, 3179-3191 (2000).
58. Moy, F. J., Glasfeld, E., Mosyak, L. & Powers, R. Solution structure of ZipA, a crucial component of Escherichia coli cell division. Biochemistry 39, 9146-9156 (2000).
59. Hale, C. A., Rhee, A. C. & de Boer, P. A. J. ZipA-induced bundling of FtsZ polymers mediated by an interaction between C-terminal domains. J. Bacteriol. 182, 5153-5166 (2000).
60. Levin, P. A., Kurtser, I. G. & Grossman, A. D. Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. Proc. Natl Acad. Sci. USA 96, 9642-9647 (1999).
61. Liu, Z., Mukherjee, A. & Lutkenhaus, J. Recruitment of ZipA to the division site by interaction with FtsZ. Mol. Microbiol. 31, 1853-1861 (1999).
62. Hale, C. A. & de Boer, P. A. J. ZipA is required for recruitment of FtsK, FtsQ, FtsL, and FtsN to the septal ring in Escherichia coli. J. Bacteriol. 184, 2552-2556 (2002).
63. Haney, S. A. et al. Genetic analysis of the Escherichia coli FtsZ.ZipA interaction in the yeast two-hybrid system. Characterization of FtsZ residues essential for the interactions with ZipA and with FtsA. J. Biol. Chem. 276, 11980-11987 (2001).
64. RayChaudhuri, D. ZipA is a MAP-Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division. EMBO J. 18, 2372-2383 (1999).
65. Ohashi, T., Hale, C. A., de Boer, P. A. & Erickson, H. P. Structural evidence that the P/Q domain of ZipA is an unstructured, flexible tether between the membrane and the C-terminal FtsZ-binding domain. J. Bacteriol. 184, 4313-4315 (2002).
66. Geissler, B., Elraheb, D. & Margolin, W. A gain-of-function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli. Proc. Natl Acad. Sci. USA 100 4197-4202 (2003).
67. Pichoff, S. & Lutkenhaus, J. Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol. Microbiol. 55, 1722-1734 (2005).
68. van den Ent, F. & Löwe, J. Crystal structure of the cell division protein FtsA from Thermotoga maritima. EMBO J. 19, 5300-5307 (2000).
69. Sánchez, M., Valencia, A., Ferrándiz, M. J., Sander, C. & Vicente, M. Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family. EMBO J. 13, 4919-4925 (1994).
70. Feucht, A., Lucet, I., Yudkin, M. D. & Errington, J. Cytological and biochemical characterization of the FtsA cell division protein of Bacillus subtilis. Mol. Microbiol. 40, 115-125 (2001).
71. Lara, B. et al. Cell division in cocci: Localization and properties of the Streptococcus pneumoniae FtsA protein. Mol. Microbiol. 55, 699-711 (2005).
72. Pichoff, S. & Lutkenhaus, J. Identification of a region of FtsA required for interaction with FtsZ. Mol. Microbiol. 64, 1129-1138 (2007).
73. Rico, A. I., García-Ovalle, M., Mingorance, J. & Vicente, M. Role of two essential domains of Escherichia coli FtsA in localization and progression of the division ring. Mol. Microbiol. 53, 1359-1371 (2004).
74. Shiomi, D. & Margolin, W. Dimerization or oligomerization of the actin-like FtsA protein enhances the integrity of the cytokinetic Z ring. Mol. Microbiol. 66, 1396-1415 (2007).
75. Yan, K., Pearce, K. H. & Payne, D. J. 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 (2000).
76. Yim, L. et al. Role of the carboxy terminus of Escherichia coli FtsA in self-interaction and cell division. J. Bacteriol. 182, 6366-6373 (2000).
77. Carettoni, D. et al. Phage-display and correlated mutations identify an essential region of subdomain 1C involved in homodimerization of Escherichia coli FtsA. Proteins 50 192-206 (2003).
78. Dai, K. & Lutkenhaus, J. The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J. Bacteriol. 174, 6145-6151 (1992).
79. Shiomi, D. & Margolin, W. Compensation for the loss of the conserved membrane targeting sequence of FtsA provides new insights into its function. Mol. Microbiol. 67, 558-569 (2008).
80. Corbin, B. D., Geissler, B., Sadasivam, M. & Margolin, W. Z-ring-independent interaction between a subdomain of FtsA and late septation proteins as revealed by a polar recruitment assay. J. Bacteriol. 186, 7736-7744 (2004).
81. Bernard, C. S., Sadasivam, M., Shiomi, D. & Margolin, W. An altered FtsA can compensate for the loss of essential cell division protein FtsN in Escherichia coli. Mol. Microbiol. 64, 1289-1305 (2007).
82. Geissler, B., Shiomi, D. & Margolin, W. The ftsA* gain-of-function allele of Escherichia coli and its effects on the stability and dynamics of the Z ring. Microbiology 153, 814-825 (2007).
83. Beall, B. & Lutkenhaus, J. Impaired cell division and sporulation of a Bacillus subtilis strain with the ftsA gene deleted. J. Bacteriol. 174, 2398-2403 (1992).
84. Jensen, S. O., Thompson, L. S. & Harry, E. J. Cell division in Bacillus subtilis: FtsZ and FtsA association is Z-ring independent, and FtsA is required for efficient midcell Z-ring assembly. J. Bacteriol. 187, 6536-6544 (2005).
85. Ishikawa, S., Kawai, Y., Hiramatsu, K., Kuwano, M. & Ogasawara, N. A new FtsZ-interacting protein, YlmF, complements the activity of FtsA during progression of cell division in Bacillus subtilis. Mol. Microbiol. 60, 1364-1380 (2006).
86. Gueiros-Filho, F. J. & Losick, R. A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev. 16, 2544-2556 (2002).
87. DMinC/MinD, complexes to septal ring assemblies in Escherichia coli. J. Bacteriol. 186 2418-2429 (2004).
88. Hamoen, L. W., Meile, J. C., de Jong, W., Noirot, P. & Errington, J. SepF, a novel FtsZ-interacting protein required for a late step in cell division. Mol. Microbiol. 59, 989-999 (2006).
89. Low, H. H., Moncrieffe, M. C. & Löwe, J. The crystal structure of ZapA and its modulation of FtsZ polymerisation. J. Mol. Biol. 341, 839-852 (2004).
90. Small, E. et al. FtsZ polymer-bundling by the Escherichia coli ZapA orthologue, YgfE, involves a conformational change in bound GTP. J. Mol. Biol. 369, 210-221 (2007).
91. Marrington, R., Small, E., Rodger, A., Dafforn, T. R. & Addinall, S. G. FtsZ fiber bundling is triggered by a conformational change in bound GTP. J. Biol. Chem. 279, 48821-48829 (2004).
92. Dajkovic, A., Lan, G., Sun, S. X., Wirtz, D. & Lutkenhaus, J. MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ. Curr. Biol. 18, 235-244 (2008).
93. Scheffers, D. J. The effect of MinC on FtsZ polymerization is pH dependent and can be counteracted by ZapA. FEBS Lett. 582, 2601-2608 (2008).
94. Ebersbach, G., Galli, E., Møller-Jensen, J., Löwe, J. & Gerdes, K. Novel coiled-coil cell division factor ZapB stimulates Z ring assembly and cell division. Mol. Microbiol. 68, 720-735 (2008).
95. Haeusser, D. P., Schwartz, R. L., Smith, A. M., Oates, M. E. & Levin, P. A. EzrA prevents aberrant cell division by modulating assembly of the cytoskeletal protein FtsZ. Mol. Microbiol. 52, 801-814 (2004).
96. Chung, K. M., Hsu, H. H., Govindan, S. & Chang, B. Y. Transcription regulation of ezrA and its effect on cell division of Bacillus subtilis. J. Bacteriol. 186, 5926-5932 (2004).
97. Haeusser, D. P., Garza, A. C., Buscher, A. Z. & Levin, P. A. The division inhibitor EzrA contains a seven-residue patch required for maintaining the dynamic nature of the medial FtsZ ring. J. Bacteriol. 189, 9001-9010 (2007).
98. Kawai, Y. & Ogasawara, N. Bacillus subtilis EzrA and FtsL synergistically regulate FtsZ ring dynamics during cell division. Microbiology 152, 1129-1141 (2006).
99. Chung, K. M., Hsu, H. H., Yeh, H. Y. & Chang, B. Y. Mechanism of regulation of prokaryotic tubulin-like GTPase FtsZ by membrane protein EzrA. J. Biol. Chem. 282, 14891-14897 (2007).
100. Singh, J. K., Makde, R. D., Kumar, V. & Panda, D. A membrane protein, EzrA, regulates assembly dynamics of FtsZ by interacting with the C-terminal tail of FtsZ. Biochemistry 46, 11013-11022 (2007).
101. Claessen, D. et al. Control of the cell elongation-division cycle by shuttling of PBP1 protein in Bacillus subtilis. Mol. Microbiol. 68, 1029-1046 (2008).
102. Tavares, J. R., de Souza, R. F., Meira, G. L. & Gueiros-Filho, F. J. Cytological characterization of YpsB, a novel component of the Bacillus subtilis divisome. J. Bacteriol. 190, 7096-7107 (2008).
103. Fadda, D. et al. Characterization of divIVA and other genes located in the chromosomal region downstream of the dcw cluster in Streptococcus pneumoniae. J. Bacteriol. 185, 6209-6214 (2003).
104. Miyagishima, S. Y., Wolk, C. P. & Osteryoung, K. W. Identification of cyanobacterial cell division genes by comparative and mutational analyses. Mol. Microbiol. 56, 126-143 (2005).
105. Weart, R. B., Nakano, S., Lane, B. E., Zuber, P. & Levin, P. A. The ClpX chaperone modulates assembly of the tubulin-like protein FtsZ. Mol. Microbiol. 57, 238-249 (2005).
106. Haeusser, D. P., Lee, A. H., Weart, R. B. & Levin, P. A. ClpX inhibits FtsZ assembly in a manner that does not require its ATP hydrolysis-dependent chaperone activity. J. Bacteriol. 191, 1986-1991 (2009).
107. Weart, R. B. et al. A metabolic sensor governing cell size in bacteria. Cell 130, 335-347 (2007).
108. Huisman, O. & D'Ari, R. An inducible DNA replication-cell division coupling mechanism in E. coli. Nature 290, 797-799 (1981).
109. Huisman, O., D'Ari, R. & Gottesman, S. Cell-division control in Escherichia coli: Specific induction of the SOS function SfiA protein is sufficient to block septation. Proc. Natl Acad. Sci. USA 81 4490-4494 (1984).
110. Justice, S. S., García-Lara, J. & Rothfield, L. I. Cell division inhibitors SulA and MinC/MinD block septum formation at different steps in the assembly of the Escherichia coli division machinery. Mol. Microbiol. 37, 410-423 (2000).
111. Bi, E. & Lutkenhaus, J. Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J. Bacteriol. 175, 1118-1125 (1993).
112. Mukherjee, A., Cao, C. & Lutkenhaus, J. Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. Proc. Natl Acad. Sci. USA 95, 2885-2890 (1998).
113. Cordell, S. C., Robinson, E. J. & Löwe, J. Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc. Natl Acad. Sci. USA 100, 7889-7894 (2003).
114. A of Escherichia coli directly interacts with FtsZ through GTP hydrolysis. Biochem. Biophys. Res. Commun. 209, 198-204 (1995).
115. Trusca, D., Scott, S., Thompson, C. & Bramhill, D. Bacterial SOS checkpoint protein SulA inhibits polymerization of purified FtsZ cell division protein. J. Bacteriol. 180, 3946-3953 (1998).
116. Huang, J., Cao, C. & Lutkenhaus, J. Interaction between FtsZ and inhibitors of cell division. J. Bacteriol. 178, 5080-5085 (1996).
117. Dai, K., Mukherjee, A., Xu, Y. & Lutkenhaus, J. Mutations in ftsZ that confer resistance to SulA affect the interaction of FtsZ with GTP. J. Bacteriol. 176, 130-136 (1994).
118. Kawai, Y., Moriya, S. & Ogasawara, N. Identification of a protein, YneA, responsible for cell division suppression during the SOS response in Bacillus subtilis. Mol. Microbiol. 47, 1113-1122 (2003).
119. Ogino, H., Teramoto, H., Inui, M. & Yukawa, H. DivS, a novel SOS-inducible cell-division suppressor in Corynebacterium glutamicum. Mol. Microbiol. 67, 597-608 (2008).
120. Handler, A. A., Lim, J. E. & Losick, R. Peptide inhibitor of cytokinesis during sporulation in Bacillus subtilis. Mol. Microbiol. 68, 588-599 (2008).
121. Stokes, N. R. et al. Novel inhibitors of bacterial cytokinesis identified by a cell-based antibiotic screening assay. J. Biol. Chem. 280, 39709-39715 (2005).
122. Amos, L. A. The tektin family of microtubule-stabilizing proteins. Genome Biol. 9, 229 (2008).
123. Loose, M., Fischer-Friedrich, E., Ries, J., Kruse, K. & Schwille, P. Spatial regulators for bacterial cell division self-organize into surface waves in vitro. Science 320, 789-792 (2008).
124. Glöckner, F. O. et al. Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc. Natl Acad. Sci. USA 100, 8298-8303 (2003).
125. Jaffe, J. D. et al. The complete genome and proteome of Mycoplasma mobile. Genome Res. 14, 1447-1461 (2004).
126. Erickson, H. P. Dynamin and FtsZ. Missing links in mitochondrial and bacterial division. J. Cell Biol. 148, 1103-1105 (2000).
127. Brown, W. J. & Rockey, D. D. Identification of an antigen localized to an apparent septum within dividing chlamydiae. Infect. Immun. 68, 708-715 (2000).
128. Lindås, A. C., Karlsson, E. A., Lindgren, M. T., Ettema, T. J. & Bernander, R. A unique cell division machinery in the Archaea. Proc. Natl Acad. Sci. USA 105, 18942-18946 (2008).
129. Samson, R. Y., Obita, T., Freund, S. M., Williams, R. L. & Bell, S. D. A role for the ESCRT system in cell division in archaea. Science 322, 1710-1713 (2008).
130. Leaver, M., Domínguez-Cuevas, P., Coxhead, J. M., Daniel, R. A. & Errington, J. Life without a wall or division machine in Bacillus subtilis. Nature 457, 849-853 (2009).
131. McCormick, J. R., Su, E. P., Driks, A. & Losick, R. Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol. Microbiol. 14, 243-254 (1994).
132. Rothfield, L., Taghbalout, A. & Shih, Y. L. Spatial control of bacterial division-site placement. Nature Rev. Microbiol. 3, 959-968 (2005).
133. Lutkenhaus, J. Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu. Rev. Biochem. 76, 539-562 (2007).
134. Wu, L. J. & Errington, J. Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117, 915-925 (2004).
135. Bernhardt, T. G. & de Boer, P. A. SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol. Cell 18, 555-564 (2005).
136. Hu, Z., Mukherjee, A., Pichoff, S. & Lutkenhaus, J. The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc. Natl Acad. Sci. USA 96, 14819-14824 (1999).
137. Hu, Z. & Lutkenhaus, J. Analysis of MinC reveals two independent domains involved in interaction with MinD and FtsZ. J. Bacteriol. 182 3965-3971 (2000).
138. C/MinD. Mol. Microbiol. 72, 410-424 (2009).
139. Raskin, D. M. & de Boer, P. A. The MinE ring: An FtsZ-independent cell structure required for selection of the correct division site in E. coli. Cell 91, 685-694 (1997).
140. Hu, Z. & Lutkenhaus, J. Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol. Microbiol. 34, 82-90 (1999).
141. Raskin, D. M. & de Boer, P. A. MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J. Bacteriol. 181, 6419-6424 (1999).
142. Edwards, D. H. & Errington, J. The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol. Microbiol. 24, 905-915 (1997).
143. Marston, A. L., Thomaides, H. B., Edwards, D. H., Sharpe, M. E. & Errington, J. Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Dev. 12, 3419-3430 (1998).
144. Marston, A. L. & Errington, J. Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC. Mol. Microbiol. 33, 84-96 (1999).
145. Patrick, J. E. & Kearns, D. B. MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis. Mol. Microbiol. 70, 1166-1179 (2008).
146. Bramkamp, M. et al. A novel component of the division-site selection system of Bacillus subtilis and a new mode of action for the division inhibitor MinCD. Mol. Microbiol. 70, 1556-1569 (2008).
147. Gregory, J. A., Becker, E. C. & Pogliano, K. Bacillus subtilis MinC destabilizes FtsZ-rings at new cell poles and contributes to the timing of cell division. Genes Dev. 22, 3475-3488 (2008).
148. Ben-Yehuda, S. & Losick, R. Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109, 257-266 (2002).
149. Thanedar, S. & Margolin, W. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14, 1167-1173 (2004).
150. Michie, K. A., Monahan, L. G., Beech, P. L. & Harry, E. J. Trapping of a spiral-like intermediate of the bacterial cytokinetic protein FtsZ. J. Bacteriol. 188, 1680-1690 (2006).
151. Peters, P. C., Migocki, M. D., Thoni, C. & Harry, E. J. A new assembly pathway for the cytokinetic Z ring from a dynamic helical structure in vegetatively growing cells of Bacillus subtilis. Mol. Microbiol. 64, 487-499 (2007).
152. Gamba, P., Veening, J. W., Saunders, N. J., Hamoen, L. W. & Daniel, R. A. Two-step assembly dynamics of the Bacillus subtilis divisome. J. Bacteriol. 191, 4186-4194 (2009).
153. Vicente, M., Rico, A. I., Martínez-Arteaga, R. & Mingorance, J. Septum enlightenment: Assembly of bacterial division proteins. J. Bacteriol. 188, 19-27 (2006).
154. Goehring, N. W., Gonzalez, M. D. & Beckwith, J. Premature targeting of cell division proteins to midcell reveals hierarchies of protein interactions involved in divisome assembly. Mol. Microbiol. 61 33-45 (2006).
155. Aarsman, M. E. et al. Maturation of the Escherichia coli divisome occurs in two steps. Mol. Microbiol. 55, 1631-1645 (2005).