1887

Abstract

Formation of the FtsZ ring (Z ring) in is the first step in the assembly of the divisome, a protein machine required for cell division. Although the biochemical functions of most divisome proteins are unknown, several, including ZipA, FtsA and FtsK, have overlapping roles in ensuring that the Z ring assembles at the cytoplasmic membrane, and that it is active. As shown previously, a single amino acid change in FtsA, R286W, also called FtsA*, bypasses the requirement for either ZipA or FtsK in cell division. In this study, the properties of FtsA* were investigated further, with the eventual goal of understanding the molecular mechanism behind the bypass. Compared to wild-type FtsA, the presence of FtsA* resulted in a modest but significant decrease in the mean length of cells in the population, accelerated the reassembly of Z rings, and suppressed the cell-division block caused by excessively high levels of FtsZ. These effects were not mediated by Z-ring remodelling, because FtsA* did not alter the kinetics of FtsZ turnover within the Z ring, as measured by fluorescence recovery after photobleaching. FtsA* was also unable to permit normal cell division at below normal levels of FtsZ, or after thermoinactivation of (ts). However, turnover of FtsA* in the ring was somewhat faster than that of wild-type FtsA, and overexpressed FtsA* did not inhibit cell division as efficiently as wild-type FtsA. Finally, FtsA* interacted more strongly with FtsZ compared with FtsA in a yeast two-hybrid system. These results suggest that FtsA* interacts with FtsZ in a markedly different way compared with FtsA.

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2007-03-01
2021-10-19
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References

  1. Addinall S. G., Bi E., Lutkenhaus J. 1996; FtsZ ring formation in fts mutants. J Bacteriol 178:3877–3884
    [Google Scholar]
  2. Anderson D. E., Gueiros-Filho F. J., 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 [CrossRef]
    [Google Scholar]
  3. Begg K., Nikolaichik Y., Crossland N., Donachie W. D. 1998; Roles of FtsA and FtsZ in activation of division sites. J Bacteriol 180:881–884
    [Google Scholar]
  4. Bi E., Lutkenhaus J. 1991; FtsZ ring structure associated with division in E. coli . Nature 354:161–164 [CrossRef]
    [Google Scholar]
  5. Corbin B. D., Geissler B., Sadasivam M., Margolin W. 2004; A 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 [CrossRef]
    [Google Scholar]
  6. Errington J. 1996; Determination of cell fate in Bacillus subtilis . Trends Genet 12:31–34 [CrossRef]
    [Google Scholar]
  7. 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 [CrossRef]
    [Google Scholar]
  8. Geissler B., Elraheb D., Margolin W. 2003; A gain of function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli . Proc Natl Acad Sci U S A 100:4197–4202 [CrossRef]
    [Google Scholar]
  9. Ghosh A. S., Young K. D. 2005; Helical disposition of proteins and lipopolysaccharide in the outer membrane of Escherichia coli . J Bacteriol 187:1913–1922 [CrossRef]
    [Google Scholar]
  10. Goehring N. W., Beckwith J. 2005; Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15:R514–R526 [CrossRef]
    [Google Scholar]
  11. Gueiros-Filho F. J., Losick R. 2002; A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev 16:2544–2556 [CrossRef]
    [Google Scholar]
  12. Guzman L. M., Belin D., Carson M. J., Beckwith J. 1995; Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121–4130
    [Google Scholar]
  13. Hale C. A., 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 [CrossRef]
    [Google Scholar]
  14. Hale C. A., de Boer P. A. 1999; Recruitment of ZipA to the septal ring of Escherichia coli is dependent on FtsZ and independent of FtsA. J Bacteriol 181:167–176
    [Google Scholar]
  15. Harry E. J. 2001; Bacterial cell division: regulating Z-ring formation. Mol Microbiol 40:795–803 [CrossRef]
    [Google Scholar]
  16. Hu Z., Mukherjee A., Pichoff S., Lutkenhaus J. 1999; The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc Natl Acad Sci U S A 96:14819–14824 [CrossRef]
    [Google Scholar]
  17. Jensen S. O., Thompson L. S., Harry E. J. 2005; 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 [CrossRef]
    [Google Scholar]
  18. Liu Z., Mukherjee A., Lutkenhaus J. 1999; Recruitment of ZipA to the division site by interaction with FtsZ. Mol Microbiol 31:1853–1861 [CrossRef]
    [Google Scholar]
  19. Lowe J., Amos L. A. 1998; Crystal structure of the bacterial cell-division protein FtsZ. Nature 391:203–206 [CrossRef]
    [Google Scholar]
  20. Ma X., Ehrhardt D. W., Margolin W. 1996; Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc Natl Acad Sci U S A 93:12998–13003 [CrossRef]
    [Google Scholar]
  21. McCool J. D., Long E., Petrosino J. F., Sandler H. A., Rosenberg S. M., Sandler S. J. 2004; Measurement of SOS expression in individual Escherichia coli K-12 cells using fluorescence microscopy. Mol Microbiol 53:1343–1357 [CrossRef]
    [Google Scholar]
  22. Pichoff S., Lutkenhaus J. 2001; Escherichia coli division inhibitor MinCD blocks septation by preventing Z-ring formation. J Bacteriol 183:6630–6635 [CrossRef]
    [Google Scholar]
  23. Pichoff S., Lutkenhaus J. 2002; Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli . EMBO J 21:685–693 [CrossRef]
    [Google Scholar]
  24. Raychaudhuri D. 1999; 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 [CrossRef]
    [Google Scholar]
  25. Rico A. I., Garcia-Ovalle M., Mingorance J., Vicente M. 2004; Role of two essential domains of Escherichia coli FtsA in localization and progression of the division ring. Mol Microbiol 53:1359–1371 [CrossRef]
    [Google Scholar]
  26. Romberg L., 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 [CrossRef]
    [Google Scholar]
  27. Rothfield L., Taghbalout A., Shih Y. L. 2005; Spatial control of bacterial division-site placement. Nat Rev Microbiol 3:959–968 [CrossRef]
    [Google Scholar]
  28. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  29. Stenoien D. L., Patel K., Mancini M. G., Dutertre M., Smith C. L., O'Malley B. W., Mancini M. A. 2001; FRAP reveals that mobility of oestrogen receptor-alpha is ligand- and proteasome-dependent. Nat Cell Biol 3:15–23 [CrossRef]
    [Google Scholar]
  30. Stricker J., Maddox P., Salmon E. D., Erickson H. P. 2002; Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc Natl Acad Sci U S A 99:3171–3175 [CrossRef]
    [Google Scholar]
  31. van Den Ent F., Lowe J. 2000; Crystal structure of the cell division protein FtsA from Thermotoga maritima . EMBO J 19:5300–5307 [CrossRef]
    [Google Scholar]
  32. Vicente M., Rico A. I., Martinez-Arteaga R., Mingorance J. 2006; Septum enlightenment: assembly of bacterial division proteins. J Bacteriol 188:19–27 [CrossRef]
    [Google Scholar]
  33. Ward J. E., Lutkenhaus J. 1985; Overproduction of FtsZ induces minicells in E. coli . Cell 42:941–949 [CrossRef]
    [Google Scholar]
  34. Weiss D. S. 2004; Bacterial cell division and the septal ring. Mol Microbiol 54:588–597 [CrossRef]
    [Google Scholar]
  35. Weiss D. S., Chen J. C., Ghigo J. M., Boyd D., 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
    [Google Scholar]
  36. Yu X.-C., Margolin W. 1999; FtsZ ring clusters in min and partition mutants: role of both the Min system and the nucleoid in regulating FtsZ ring localization. Mol Microbiol 32:315–326 [CrossRef]
    [Google Scholar]
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