Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1999 May 4;18(9):2364–2371. doi: 10.1093/emboj/18.9.2364

Tubulin-like protofilaments in Ca2+-induced FtsZ sheets.

J Löwe 1, L A Amos 1
PMCID: PMC1171319  PMID: 10228151

Abstract

The 40 kDa protein FtsZ is a major septum-forming component of bacterial cell division. Early during cytokinesis at midcell, FtsZ forms a cytokinetic ring that constricts as septation progresses. FtsZ has a high propensity to polymerize in vitro into various structures, including sheets and filaments, in a GTP-dependent manner. Together with limited sequence homology, the occurrence of the tubulin signature motif in FtsZ and a similar three-dimensional structure, this leads to the conclusion that FtsZ is the bacterial tubulin homologue. We have polymerized FtsZ1 from Methanococcus jannaschii in the presence of millimolar concentrations of Ca2+ ions to produce two-dimensional crystals of plane group P2221. Most of the protein precipitates and forms filaments approximately 23.0 nm in diameter. A three-dimensional reconstruction of tilted micrographs of FtsZ sheets in negative stain between 0 and 60 degrees shows protofilaments of FtsZ running along the sheet axis. Pairs of parallel FtsZ protofilaments associate in an antiparallel fashion to form a two-dimensional sheet. The antiparallel arrangement is believed to generate flat sheets instead of the curved filaments seen in other FtsZ polymers. Together with the subunit spacing along the protofilament axis, a fitting of the FtsZ crystal structure into the reconstruction suggests a protofilamant structure very similar to that of tubulin protofilaments.

Full Text

The Full Text of this article is available as a PDF (648.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Addinall S. G., Lutkenhaus J. FtsZ-spirals and -arcs determine the shape of the invaginating septa in some mutants of Escherichia coli. Mol Microbiol. 1996 Oct;22(2):231–237. doi: 10.1046/j.1365-2958.1996.00100.x. [DOI] [PubMed] [Google Scholar]
  2. Amos L. A., Henderson R., Unwin P. N. Three-dimensional structure determination by electron microscopy of two-dimensional crystals. Prog Biophys Mol Biol. 1982;39(3):183–231. doi: 10.1016/0079-6107(83)90017-2. [DOI] [PubMed] [Google Scholar]
  3. Baker T. S., Amos L. A. Structure of the tubulin dimer in zinc-induced sheets. J Mol Biol. 1978 Jul 25;123(1):89–106. doi: 10.1016/0022-2836(78)90378-9. [DOI] [PubMed] [Google Scholar]
  4. Barton G. J. ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng. 1993 Jan;6(1):37–40. doi: 10.1093/protein/6.1.37. [DOI] [PubMed] [Google Scholar]
  5. Bi E. F., Lutkenhaus J. FtsZ ring structure associated with division in Escherichia coli. Nature. 1991 Nov 14;354(6349):161–164. doi: 10.1038/354161a0. [DOI] [PubMed] [Google Scholar]
  6. Bramhill D. Bacterial cell division. Annu Rev Cell Dev Biol. 1997;13:395–424. doi: 10.1146/annurev.cellbio.13.1.395. [DOI] [PubMed] [Google Scholar]
  7. Bramhill D., Thompson C. M. GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5813–5817. doi: 10.1073/pnas.91.13.5813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chang C. F., Shuman H., Somlyo A. P. Electron probe analysis, X-ray mapping, and electron energy-loss spectroscopy of calcium, magnesium, and monovalent ions in log-phase and in dividing Escherichia coli B cells. J Bacteriol. 1986 Sep;167(3):935–939. doi: 10.1128/jb.167.3.935-939.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Crowther R. A., Henderson R., Smith J. M. MRC image processing programs. J Struct Biol. 1996 Jan-Feb;116(1):9–16. doi: 10.1006/jsbi.1996.0003. [DOI] [PubMed] [Google Scholar]
  10. 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. 1994 Jan;176(1):130–136. doi: 10.1128/jb.176.1.130-136.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Erickson H. P. Atomic structures of tubulin and FtsZ. Trends Cell Biol. 1998 Apr;8(4):133–137. doi: 10.1016/s0962-8924(98)01237-9. [DOI] [PubMed] [Google Scholar]
  12. Erickson H. P. FtsZ, a prokaryotic homolog of tubulin? Cell. 1995 Feb 10;80(3):367–370. doi: 10.1016/0092-8674(95)90486-7. [DOI] [PubMed] [Google Scholar]
  13. Erickson H. P. FtsZ, a tubulin homologue in prokaryote cell division. Trends Cell Biol. 1997 Sep;7(9):362–367. doi: 10.1016/S0962-8924(97)01108-2. [DOI] [PubMed] [Google Scholar]
  14. 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 U S A. 1996 Jan 9;93(1):519–523. doi: 10.1073/pnas.93.1.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Faguy D. M., Doolittle W. F. Cytoskeletal proteins: the evolution of cell division. Curr Biol. 1998 May 7;8(10):R338–R341. doi: 10.1016/s0960-9822(98)70216-7. [DOI] [PubMed] [Google Scholar]
  16. Hirota Y., Ryter A., Jacob F. Thermosensitive mutants of E. coli affected in the processes of DNA synthesis and cellular division. Cold Spring Harb Symp Quant Biol. 1968;33:677–693. doi: 10.1101/sqb.1968.033.01.077. [DOI] [PubMed] [Google Scholar]
  17. Lutkenhaus J., Addinall S. G. Bacterial cell division and the Z ring. Annu Rev Biochem. 1997;66:93–116. doi: 10.1146/annurev.biochem.66.1.93. [DOI] [PubMed] [Google Scholar]
  18. Löwe J., Amos L. A. Crystal structure of the bacterial cell-division protein FtsZ. Nature. 1998 Jan 8;391(6663):203–206. doi: 10.1038/34472. [DOI] [PubMed] [Google Scholar]
  19. Mukherjee A., Lutkenhaus J. Dynamic assembly of FtsZ regulated by GTP hydrolysis. EMBO J. 1998 Jan 15;17(2):462–469. doi: 10.1093/emboj/17.2.462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mukherjee A., Lutkenhaus J. Guanine nucleotide-dependent assembly of FtsZ into filaments. J Bacteriol. 1994 May;176(9):2754–2758. doi: 10.1128/jb.176.9.2754-2758.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nogales E., Whittaker M., Milligan R. A., Downing K. H. High-resolution model of the microtubule. Cell. 1999 Jan 8;96(1):79–88. doi: 10.1016/s0092-8674(00)80961-7. [DOI] [PubMed] [Google Scholar]
  22. Nogales E., Wolf S. G., Downing K. H. Structure of the alpha beta tubulin dimer by electron crystallography. Nature. 1998 Jan 8;391(6663):199–203. doi: 10.1038/34465. [DOI] [PubMed] [Google Scholar]
  23. Norris V. A calcium flux at the termination of replication triggers cell division in Escherichia coli. Hypothesis. Cell Calcium. 1989 Nov-Dec;10(8):511–517. doi: 10.1016/0143-4160(89)90012-2. [DOI] [PubMed] [Google Scholar]
  24. Osteryoung K. W., Vierling E. Conserved cell and organelle division. Nature. 1995 Aug 10;376(6540):473–474. doi: 10.1038/376473b0. [DOI] [PubMed] [Google Scholar]
  25. Rothfield L. I., Justice S. S. Bacterial cell division: the cycle of the ring. Cell. 1997 Mar 7;88(5):581–584. doi: 10.1016/s0092-8674(00)81899-1. [DOI] [PubMed] [Google Scholar]
  26. Yu X. C., Margolin W. Ca2+-mediated GTP-dependent dynamic assembly of bacterial cell division protein FtsZ into asters and polymer networks in vitro. EMBO J. 1997 Sep 1;16(17):5455–5463. doi: 10.1093/emboj/16.17.5455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. de Pereda J. M., Leynadier D., Evangelio J. A., Chacón P., Andreu J. M. Tubulin secondary structure analysis, limited proteolysis sites, and homology to FtsZ. Biochemistry. 1996 Nov 12;35(45):14203–14215. doi: 10.1021/bi961357b. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES