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. 1999 May 4;18(9):2372–2383. doi: 10.1093/emboj/18.9.2372

ZipA is a MAP-Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division.

D RayChaudhuri 1
PMCID: PMC1171320  PMID: 10228152

Abstract

The first visible event in prokaryotic cell division is the assembly of the soluble, tubulin-like FtsZ GTPase into a membrane-associated cytokinetic ring that defines the division plane in bacterial and archaeal cells. In the temperature-sensitive ftsZ84 mutant of Escherichia coli, this ring assembly is impaired at the restrictive temperature causing lethal cell filamentation. Here I present genetic and morphological evidence that a 2-fold higher dosage of the division gene zipA suppresses thermosensitivity of the ftsZ84 mutant by stabilizing the labile FtsZ84 ring structure in vivo. I demonstrate that purified ZipA promotes and stabilizes protofilament assembly of both FtsZ and FtsZ84 in vitro and cosediments with the protofilaments. Furthermore, ZipA organizes FtsZ protofilaments into arrays of long bundles or sheets that probably represent the physiological organization of the FtsZ ring in bacterial cells. The N-terminal cytoplasmic domain of membrane-anchored ZipA contains sequence elements that resemble the microtubule-binding signature motifs in eukaryotic Tau, MAP2 and MAP4 proteins. It is postulated that the MAP-Tau-homologous motifs in ZipA mediate its binding to FtsZ, and that FtsZ-ZipA interaction represents an ancient prototype of the protein-protein interaction that enables MAPs to suppress microtubule catastrophe and/or to promote rescue.

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Selected References

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  1. Addinall S. G., Cao C., Lutkenhaus J. FtsN, a late recruit to the septum in Escherichia coli. Mol Microbiol. 1997 Jul;25(2):303–309. doi: 10.1046/j.1365-2958.1997.4641833.x. [DOI] [PubMed] [Google Scholar]
  2. Addinall S. G., Cao C., Lutkenhaus J. Temperature shift experiments with an ftsZ84(Ts) strain reveal rapid dynamics of FtsZ localization and indicate that the Z ring is required throughout septation and cannot reoccupy division sites once constriction has initiated. J Bacteriol. 1997 Jul;179(13):4277–4284. doi: 10.1128/jb.179.13.4277-4284.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berlyn M. K. Linkage map of Escherichia coli K-12, edition 10: the traditional map. Microbiol Mol Biol Rev. 1998 Sep;62(3):814–984. doi: 10.1128/mmbr.62.3.814-984.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Blattner F. R., Plunkett G., 3rd, Bloch C. A., Perna N. T., Burland V., Riley M., Collado-Vides J., Glasner J. D., Rode C. K., Mayhew G. F. The complete genome sequence of Escherichia coli K-12. Science. 1997 Sep 5;277(5331):1453–1462. doi: 10.1126/science.277.5331.1453. [DOI] [PubMed] [Google Scholar]
  6. Boyle D. S., Khattar M. M., Addinall S. G., Lutkenhaus J., Donachie W. D. ftsW is an essential cell-division gene in Escherichia coli. Mol Microbiol. 1997 Jun;24(6):1263–1273. doi: 10.1046/j.1365-2958.1997.4091773.x. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Buddelmeijer N., Aarsman M. E., Kolk A. H., Vicente M., Nanninga N. Localization of cell division protein FtsQ by immunofluorescence microscopy in dividing and nondividing cells of Escherichia coli. J Bacteriol. 1998 Dec;180(23):6107–6116. doi: 10.1128/jb.180.23.6107-6116.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dai K., Lutkenhaus J. The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J Bacteriol. 1992 Oct;174(19):6145–6151. doi: 10.1128/jb.174.19.6145-6151.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Degnen G. E., Cox E. C. Conditional mutator gene in Escherichia coli: isolation, mapping, and effector studies. J Bacteriol. 1974 Feb;117(2):477–487. doi: 10.1128/jb.117.2.477-487.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Desai A., Mitchison T. J. Microtubule polymerization dynamics. Annu Rev Cell Dev Biol. 1997;13:83–117. doi: 10.1146/annurev.cellbio.13.1.83. [DOI] [PubMed] [Google Scholar]
  12. Dewar S. J., Begg K. J., Donachie W. D. Inhibition of cell division initiation by an imbalance in the ratio of FtsA to FtsZ. J Bacteriol. 1992 Oct;174(19):6314–6316. doi: 10.1128/jb.174.19.6314-6316.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Draper G. C., McLennan N., Begg K., Masters M., Donachie W. D. Only the N-terminal domain of FtsK functions in cell division. J Bacteriol. 1998 Sep;180(17):4621–4627. doi: 10.1128/jb.180.17.4621-4627.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Drechsel D. N., Hyman A. A., Cobb M. H., Kirschner M. W. Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell. 1992 Oct;3(10):1141–1154. doi: 10.1091/mbc.3.10.1141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Drewes G., Ebneth A., Mandelkow E. M. MAPs, MARKs and microtubule dynamics. Trends Biochem Sci. 1998 Aug;23(8):307–311. doi: 10.1016/s0968-0004(98)01245-6. [DOI] [PubMed] [Google Scholar]
  16. 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]
  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 U S A. 1996 Jan 9;93(1):519–523. doi: 10.1073/pnas.93.1.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Goedert M., Baur C. P., Ahringer J., Jakes R., Hasegawa M., Spillantini M. G., Smith M. J., Hill F. PTL-1, a microtubule-associated protein with tau-like repeats from the nematode Caenorhabditis elegans. J Cell Sci. 1996 Nov;109(Pt 11):2661–2672. doi: 10.1242/jcs.109.11.2661. [DOI] [PubMed] [Google Scholar]
  19. Goode B. L., Denis P. E., Panda D., Radeke M. J., Miller H. P., Wilson L., Feinstein S. C. Functional interactions between the proline-rich and repeat regions of tau enhance microtubule binding and assembly. Mol Biol Cell. 1997 Feb;8(2):353–365. doi: 10.1091/mbc.8.2.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gustke N., Trinczek B., Biernat J., Mandelkow E. M., Mandelkow E. Domains of tau protein and interactions with microtubules. Biochemistry. 1994 Aug 16;33(32):9511–9522. doi: 10.1021/bi00198a017. [DOI] [PubMed] [Google Scholar]
  21. Hale C. A., de Boer P. A. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell. 1997 Jan 24;88(2):175–185. doi: 10.1016/s0092-8674(00)81838-3. [DOI] [PubMed] [Google Scholar]
  22. Hale C. A., de Boer P. A. Recruitment of ZipA to the septal ring of Escherichia coli is dependent on FtsZ and independent of FtsA. J Bacteriol. 1999 Jan;181(1):167–176. doi: 10.1128/jb.181.1.167-176.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hiraga S., Ichinose C., Niki H., Yamazoe M. Cell cycle-dependent duplication and bidirectional migration of SeqA-associated DNA-protein complexes in E. coli. Mol Cell. 1998 Feb;1(3):381–387. doi: 10.1016/s1097-2765(00)80038-6. [DOI] [PubMed] [Google Scholar]
  24. Holland I. B. Genetic analysis of the E. coli division clock. Cell. 1987 Feb 13;48(3):361–362. doi: 10.1016/0092-8674(87)90183-8. [DOI] [PubMed] [Google Scholar]
  25. Höltje J. V. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev. 1998 Mar;62(1):181–203. doi: 10.1128/mmbr.62.1.181-203.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Irminger-Finger I., Hurt E., Roebuck A., Collart M. A., Edelstein S. J. MHP1, an essential gene in Saccharomyces cerevisiae required for microtubule function. J Cell Biol. 1996 Dec;135(5):1323–1339. doi: 10.1083/jcb.135.5.1323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Khattar M. M., Addinall S. G., Stedul K. H., Boyle D. S., Lutkenhaus J., Donachie W. D. Two polypeptide products of the Escherichia coli cell division gene ftsW and a possible role for FtsW in FtsZ function. J Bacteriol. 1997 Feb;179(3):784–793. doi: 10.1128/jb.179.3.784-793.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kirschner M., Mitchison T. Beyond self-assembly: from microtubules to morphogenesis. Cell. 1986 May 9;45(3):329–342. doi: 10.1016/0092-8674(86)90318-1. [DOI] [PubMed] [Google Scholar]
  29. Kneller D. G., Cohen F. E., Langridge R. Improvements in protein secondary structure prediction by an enhanced neural network. J Mol Biol. 1990 Jul 5;214(1):171–182. doi: 10.1016/0022-2836(90)90154-E. [DOI] [PubMed] [Google Scholar]
  30. Koop A. H., Hartley M. E., Bourgeois S. A low-copy-number vector utilizing beta-galactosidase for the analysis of gene control elements. Gene. 1987;52(2-3):245–256. doi: 10.1016/0378-1119(87)90051-5. [DOI] [PubMed] [Google Scholar]
  31. Lee G., Cowan N., Kirschner M. The primary structure and heterogeneity of tau protein from mouse brain. Science. 1988 Jan 15;239(4837):285–288. doi: 10.1126/science.3122323. [DOI] [PubMed] [Google Scholar]
  32. Levin P. A., Losick R. Transcription factor Spo0A switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis. Genes Dev. 1996 Feb 15;10(4):478–488. doi: 10.1101/gad.10.4.478. [DOI] [PubMed] [Google Scholar]
  33. Lewis S. A., Wang D. H., Cowan N. J. Microtubule-associated protein MAP2 shares a microtubule binding motif with tau protein. Science. 1988 Nov 11;242(4880):936–939. doi: 10.1126/science.3142041. [DOI] [PubMed] [Google Scholar]
  34. Lu C., Stricker J., Erickson H. P. FtsZ from Escherichia coli, Azotobacter vinelandii, and Thermotoga maritima--quantitation, GTP hydrolysis, and assembly. Cell Motil Cytoskeleton. 1998;40(1):71–86. doi: 10.1002/(SICI)1097-0169(1998)40:1<71::AID-CM7>3.0.CO;2-I. [DOI] [PubMed] [Google Scholar]
  35. Lutkenhaus J. F., Wolf-Watz H., Donachie W. D. Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ). J Bacteriol. 1980 May;142(2):615–620. doi: 10.1128/jb.142.2.615-620.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. Maurer R., Osmond B. C., Shekhtman E., Wong A., Botstein D. Functional interchangeability of DNA replication genes in Salmonella typhimurium and Escherichia coli demonstrated by a general complementation procedure. Genetics. 1984 Sep;108(1):1–23. doi: 10.1093/genetics/108.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. McDermott J. B., Aamodt S., Aamodt E. ptl-1, a Caenorhabditis elegans gene whose products are homologous to the tau microtubule-associated proteins. Biochemistry. 1996 Jul 23;35(29):9415–9423. doi: 10.1021/bi952646n. [DOI] [PubMed] [Google Scholar]
  40. Mukherjee A., Dai K., Lutkenhaus J. Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):1053–1057. doi: 10.1073/pnas.90.3.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. 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]
  43. Noda A., Courtright J. B., Denor P. F., Webb G., Kohara Y., Ishihama A. Rapid identification of specific genes in E. coli by hybridization to membranes containing the ordered set of phage clones. Biotechniques. 1991 Apr;10(4):474, 476-7. [PubMed] [Google Scholar]
  44. Nogales E., Downing K. H., Amos L. A., Löwe J. Tubulin and FtsZ form a distinct family of GTPases. Nat Struct Biol. 1998 Jun;5(6):451–458. doi: 10.1038/nsb0698-451. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. 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]
  47. Phoenix P., Drapeau G. R. Cell division control in Escherichia coli K-12: some properties of the ftsZ84 mutation and suppression of this mutation by the product of a newly identified gene. J Bacteriol. 1988 Sep;170(9):4338–4342. doi: 10.1128/jb.170.9.4338-4342.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Pogliano J., Pogliano K., Weiss D. S., Losick R., Beckwith J. Inactivation of FtsI inhibits constriction of the FtsZ cytokinetic ring and delays the assembly of FtsZ rings at potential division sites. Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):559–564. doi: 10.1073/pnas.94.2.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Powell B. S., Court D. L. Control of ftsZ expression, cell division, and glutamine metabolism in Luria-Bertani medium by the alarmone ppGpp in Escherichia coli. J Bacteriol. 1998 Mar;180(5):1053–1062. doi: 10.1128/jb.180.5.1053-1062.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. RayChaudhuri D., Park J. T. A point mutation converts Escherichia coli FtsZ septation GTPase to an ATPase. J Biol Chem. 1994 Sep 16;269(37):22941–22944. [PubMed] [Google Scholar]
  51. RayChaudhuri D., Park J. T. Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature. 1992 Sep 17;359(6392):251–254. doi: 10.1038/359251a0. [DOI] [PubMed] [Google Scholar]
  52. 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]
  53. Stephens R. S., Kalman S., Lammel C., Fan J., Marathe R., Aravind L., Mitchell W., Olinger L., Tatusov R. L., Zhao Q. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science. 1998 Oct 23;282(5389):754–759. doi: 10.1126/science.282.5389.754. [DOI] [PubMed] [Google Scholar]
  54. Strepp R., Scholz S., Kruse S., Speth V., Reski R. Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4368–4373. doi: 10.1073/pnas.95.8.4368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. doi: 10.1016/0076-6879(90)85008-c. [DOI] [PubMed] [Google Scholar]
  56. Trinczek B., Biernat J., Baumann K., Mandelkow E. M., Mandelkow E. Domains of tau protein, differential phosphorylation, and dynamic instability of microtubules. Mol Biol Cell. 1995 Dec;6(12):1887–1902. doi: 10.1091/mbc.6.12.1887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Wang H. C., Gayda R. C. High-level expression of the FtsA protein inhibits cell septation in Escherichia coli K-12. J Bacteriol. 1990 Aug;172(8):4736–4740. doi: 10.1128/jb.172.8.4736-4740.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Wang L., Khattar M. K., Donachie W. D., Lutkenhaus J. FtsI and FtsW are localized to the septum in Escherichia coli. J Bacteriol. 1998 Jun;180(11):2810–2816. doi: 10.1128/jb.180.11.2810-2816.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Wang L., Lutkenhaus J. FtsK is an essential cell division protein that is localized to the septum and induced as part of the SOS response. Mol Microbiol. 1998 Aug;29(3):731–740. doi: 10.1046/j.1365-2958.1998.00958.x. [DOI] [PubMed] [Google Scholar]
  60. Ward J. E., Jr, Lutkenhaus J. Overproduction of FtsZ induces minicell formation in E. coli. Cell. 1985 Oct;42(3):941–949. doi: 10.1016/0092-8674(85)90290-9. [DOI] [PubMed] [Google Scholar]
  61. Weiss D. S., Pogliano K., Carson M., Guzman L. M., Fraipont C., Nguyen-Distèche M., Losick R., Beckwith J. Localization of the Escherichia coli cell division protein Ftsl (PBP3) to the division site and cell pole. Mol Microbiol. 1997 Aug;25(4):671–681. doi: 10.1046/j.1365-2958.1997.5041869.x. [DOI] [PubMed] [Google Scholar]
  62. Williamson M. P. The structure and function of proline-rich regions in proteins. Biochem J. 1994 Jan 15;297(Pt 2):249–260. doi: 10.1042/bj2970249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. 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]
  64. Yu X. C., Tran A. H., Sun Q., Margolin W. Localization of cell division protein FtsK to the Escherichia coli septum and identification of a potential N-terminal targeting domain. J Bacteriol. 1998 Mar;180(5):1296–1304. doi: 10.1128/jb.180.5.1296-1304.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. de Boer P., Crossley R., Rothfield L. The essential bacterial cell-division protein FtsZ is a GTPase. Nature. 1992 Sep 17;359(6392):254–256. doi: 10.1038/359254a0. [DOI] [PubMed] [Google Scholar]

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