Bacterial cell division: assembly, maintenance and disassembly of the Z ring (original) (raw)

• Errington, J., Daniel, R. A. & Scheffers, D. J. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67, 52–65 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Goehring, N. W. & Beckwith, J. Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr. Biol. 15, R514–R526 (2005).
  Article CAS PubMed Google Scholar
• Harry, E., Monahan, L. & Thompson, L. Bacterial cell division: the mechanism and its precison. Int. Rev. Cytol. 253, 27–94 (2006).
  Article CAS PubMed Google Scholar
• Bi, E. F. & Lutkenhaus, J. FtsZ ring structure associated with division in Escherichia coli. Nature 354, 161–164 (1991).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Margolin, W. FtsZ and the division of prokaryotic cells and organelles. Nature Rev. Mol. Cell Biol. 6, 862–871 (2005).
  Article CAS Google Scholar
• Haydon, D. J. et al. An inhibitor of FtsZ with potent and selective anti-staphylococcal activity. Science 321, 1673–1675 (2008). This paper describes the validation of FtsZ as a clinically relevant target for new antibiotics.
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Weart, R. B. & Levin, P. A. Growth rate-dependent regulation of medial FtsZ ring formation. J. Bacteriol. 185, 2826–2834 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Löwe, J. & Amos, L. A. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391, 203–206 (1998).
  Article PubMed Google Scholar
• Nogales, E., Wolf, S. G. & Downing, K. H. Structure of the αβ tubulin dimer by electron crystallography. Nature 391, 199–203 (1998).
  Article CAS PubMed Google Scholar
• Erickson, H. P. FtsZ, a prokaryotic homolog of tubulin? Cell 80, 367–370 (1995).
  Article CAS PubMed Google Scholar
• Mukherjee, A. & Lutkenhaus, J. Guanine nucleotide-dependent assembly of FtsZ into filaments. J. Bacteriol. 176, 2754–2758 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Löwe, J. & Amos, L. A. Tubulin-like protofilaments in Ca2+-induced FtsZ sheets. EMBO J. 18, 2364–2371 (1999).
  Article PubMed PubMed Central Google Scholar
• Oliva, M. A., Cordell, S. C. & Löwe, J. Structural insights into FtsZ protofilament formation. Nature Struct. Mol. Biol. 11, 1243–1250 (2004). The work described in references 18 and 19 provides evidence that the protofilaments of FtsZ and tubulin make similar longitudinal contacts.
  Article CAS Google Scholar
• de Boer, P., Crossley, R. & Rothfield, L. The essential bacterial cell-division protein FtsZ is a GTPase. Nature 359, 254–256 (1992).
  Article CAS PubMed Google Scholar
• RayChaudhuri, D. & Park, J. T. Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature 359, 251–254 (1992).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Mukherjee, A. & Lutkenhaus, J. Dynamic assembly of FtsZ regulated by GTP hydrolysis. EMBO J. 17, 462–469 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Popp, D., Iwasa, M., Narita, A., Erickson, H. P. & Maéda, Y. FtsZ condensates: an in vitro electron microscopy study. Biopolymers 91, 340–350 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Li, Z., Trimble, M. J., Brun, Y. V. & Jensen, G. J. The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J. 26, 4694–4708 (2007). This study generated the first high-resolution images of FtsZ polymers in the Z ring in vivo , which revealed that the structure might not be a ring after all. The force-generating potential of the observed polymers is also discussed in this article.
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Huecas, S. et al. Energetics and geometry of FtsZ polymers: nucleated self-assembly of single protofilaments. Biophys. J. 94, 1796–1806 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Miraldi, E. R., Thomas, P. J. & Romberg, L. Allosteric models for cooperative polymerization of linear polymers. Biophys. J. 95, 2470–2486 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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). References 34, 40 and 41 show that FtsZ polymers are highly dynamic and discuss the physiological implications of this behaviour.
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Lu, C., Reedy, M. & Erickson, H. P. Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J. Bacteriol. 182, 164–170 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Oliva, M. A., Trambaiolo, D. & Löwe, J. Structural insights into the conformational variability of FtsZ. J. Mol. Biol. 373, 1229–1242 (2007).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Erickson, H. P. Modeling the physics of FtsZ assembly and force generation. Proc. Natl Acad. Sci. USA 106, 9238–9243 (2009). This manuscript provides a comprehensive summary of the recent attempts to model the assembly of FtsZ and a discussion of the potential mechanisms by which a single-stranded polymer can behave cooperatively.
  Article CAS PubMed PubMed Central Google Scholar
• Osawa, M., Anderson, D. E. & Erickson, H. P. Reconstitution of contractile FtsZ rings in liposomes. Science 320, 792–794 (2008). This groundbreaking study shows that a membrane-tethered FtsZ is itself sufficient to assemble Z rings and that these rings can constrict within tubular liposomes. This article also proposes a powerful new in vitro model for cell division.
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Erickson, H. P. FtsZ, a tubulin homologue in prokaryote cell division. Trends Cell Biol. 7, 362–367 (1997).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Liu, Z., Mukherjee, A. & Lutkenhaus, J. Recruitment of ZipA to the division site by interaction with FtsZ. Mol. Microbiol. 31, 1853–1861 (1999).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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). This article describes the discovery of an amphipathic helix in FtsA, which explains the ability of FtsA to act as a membrane tether for the Z ring.
  Article CAS PubMed Google Scholar
• van den Ent, F. & Löwe, J. Crystal structure of the cell division protein FtsA from Thermotoga maritima. EMBO J. 19, 5300–5307 (2000). The work in this paper shows that FtsA is structurally related to actin.
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Lara, B. et al. Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Mol. Microbiol. 55, 699–711 (2005).
  Article CAS PubMed Google Scholar
• Pichoff, S. & Lutkenhaus, J. Identification of a region of FtsA required for interaction with FtsZ. Mol. Microbiol. 64, 1129–1138 (2007).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Johnson, J. E., Lackner, L. L., Hale, C. A. & de Boer, P. A. 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 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• 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). References 85 and 88 describe SepF, the only non-essential accessory protein identified to date that, when absent, greatly affects septum morphology.
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Kawai, Y. & Ogasawara, N. Bacillus subtilis EzrA and FtsL synergistically regulate FtsZ ring dynamics during cell division. Microbiology 152, 1129–1141 (2006).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Weart, R. B. et al. A metabolic sensor governing cell size in bacteria. Cell 130, 335–347 (2007). This study identifies a glucose-sensitive regulator of Z ring assembly that can delay cell division during rapid growth.
  Article CAS PubMed PubMed Central Google Scholar
• Huisman, O. & D'Ari, R. An inducible DNA replication-cell division coupling mechanism in E. coli. Nature 290, 797–799 (1981).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Bi, E. & Lutkenhaus, J. Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J. Bacteriol. 175, 1118–1125 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Higashitani, A., Higashitani, N. & Horiuchi, K. A cell division inhibitor SulA of Escherichia coli directly interacts with FtsZ through GTP hydrolysis. Biochem. Biophys. Res. Commun. 209, 198–204 (1995).
  Article CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• Huang, J., Cao, C. & Lutkenhaus, J. Interaction between FtsZ and inhibitors of cell division. J. Bacteriol. 178, 5080–5085 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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). References 118 and 119 describe the identification of two unrelated proteins that halt cell division following DNA damage.
  Article CAS PubMed Google Scholar
• Handler, A. A., Lim, J. E. & Losick, R. Peptide inhibitor of cytokinesis during sporulation in Bacillus subtilis. Mol. Microbiol. 68, 588–599 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Amos, L. A. The tektin family of microtubule-stabilizing proteins. Genome Biol. 9, 229 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article PubMed PubMed Central Google Scholar
• Jaffe, J. D. et al. The complete genome and proteome of Mycoplasma mobile. Genome Res. 14, 1447–1461 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Erickson, H. P. Dynamin and FtsZ. Missing links in mitochondrial and bacterial division. J. Cell Biol. 148, 1103–1105 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Brown, W. J. & Rockey, D. D. Identification of an antigen localized to an apparent septum within dividing chlamydiae. Infect. Immun. 68, 708–715 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article PubMed PubMed Central Google Scholar
• 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). References 128 and 129 report the discovery of a new division machinery in the Crenarchaeota, explaining how they divide without FtsZ.
  Article CAS PubMed PubMed Central Google Scholar
• 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). This paper provides evidence that B. subtilis retains the ability to divide independently of FtsZ when forced to grow without its protective cell wall.
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Rothfield, L., Taghbalout, A. & Shih, Y. L. Spatial control of bacterial division-site placement. Nature Rev. Microbiol. 3, 959–968 (2005).
  Article CAS Google Scholar
• Lutkenhaus, J. Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu. Rev. Biochem. 76, 539–562 (2007). References 132 and 133 are two recent, comprehensive reviews of division-site selection in bacteria.
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Hu, Z. & Lutkenhaus, J. Analysis of MinC reveals two independent domains involved in interaction with MinD and FtsZ. J. Bacteriol. 182, 3965–3971 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Shen, B. & Lutkenhaus, J. The conserved C-terminal tail of FtsZ is required for the septal localization and division inhibitory activity of MinCC/MinD. Mol. Microbiol. 72, 410–424 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Patrick, J. E. & Kearns, D. B. MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis. Mol. Microbiol. 70, 1166–1179 (2008).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Thanedar, S. & Margolin, W. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14, 1167–1173 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Vicente, M., Rico, A. I., Martínez-Arteaga, R. & Mingorance, J. Septum enlightenment: assembly of bacterial division proteins. J. Bacteriol. 188, 19–27 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Aarsman, M. E. et al. Maturation of the Escherichia coli divisome occurs in two steps. Mol. Microbiol. 55, 1631–1645 (2005).
  Article CAS PubMed Google Scholar