Trapping of a spiral-like intermediate of the bacterial cytokinetic protein FtsZ

Journal of Bacteriology

Volumn 188, Issue 5, 2006, Pages 1680-1690

  Michie, Katherine A ^a,d   Monahan, Leigh G ^a,b   Beech, Peter L ^c   Harry, Elizabeth J ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c DEAKIN UNIVERSITY   (Australia)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FTSZ PROTEIN; MUTANT PROTEIN; TUBULIN;

BACILLUS SUBTILIS; BACTERIAL GENE; CELL DIVISION; CHROMOSOME REPLICATION; CONFERENCE PAPER; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOKINESIS; CYTOSKELETON; FTSZ GENE; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; TEMPERATURE DEPENDENCE; TEMPERATURE SENSITIVE MUTANT;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL DIVISION; CHROMOSOMES, BACTERIAL; CYTOSKELETAL PROTEINS; CYTOSKELETON; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POINT MUTATION; SEQUENCE ALIGNMENT; TEMPERATURE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

EID: 33644778043     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.188.5.1680-1690.2006     Document Type: Conference Paper

References (61)

1. Addinall, S. G., and J. Lutkenhaus. 1996. FtsZ-spirals and -arcs determine the shape of the invaginating septa in some mutants of Escherichia coli. Mol. Microbiol. 22:231-237.
2. Addinall, S. G., E. Small, D. Whitaker, S. Sturrock, W. D. Donachie, and M. M. Khattar. 2005. New temperature-sensitive alleles of ftsZ in Escherichia coli. J. Bacteriol. 187:358-365.
3. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
4. Anderson, D. E., F. J. Gueiros-Filho, and H. P. Erickson. 2004. Assembly dynamics of RsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J. Bacteriol. 186:5775-5781.
5. Andreu, J. M., M. A. Oliva, and O. Monasterio. 2002. Reversible unfolding of FtsZ cell division proteins from archaea and bacteria: Comparison with eukaryotic tubulin folding and assembly. J. Biol. Chem. 277:43262-43270.
6. Beall, B., M. Lowe, and J. Lutkenhaus. 1988. Cloning and characterization of Bacillus subtilis homologs of Escherichia coli cell division genes ftsZ and ftsA. J. Bacteriol. 170:4855-4864.
7. Ben-Yehuda, S., and R. Losick. 2002. Asymmetric cell division in Bacillus subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109:257-266.
8. Bernhardt, T. G., and P. A. J. de Boer. 2005. SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in Escherichia coli. Mol. Cell 18:555-564.
9. Bi, E., and J. Lutkenhaus. 1990. FtsZ regulates frequency of cell division in Escherichia coli. J. Bacteriol. 172:2765-2768.
10. Bi, E., and J. Lutkenhaus. 1993. Cell division inhibitors, SulA and MinCD, prevent formation of the FtsZ ring. J. Bacteriol. 175:1118-1125.
11. Bramhill, D., and C. M. Thompson. 1994. GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc. Natl. Acad. Sci. USA 91:5813-5817.
12. Callister, H., and R. G. Wake. 1981. Characterization and mapping of temperature-sensitive division initiation mutations of Bacillus subtilis. J. Bacteriol. 145:1042-1051.
13. Callister, H., T. McGinness, and R. G. Wake. 1983. Timing and other features of the action of the ts1 division initiation gene product of Bacillus subtilis. J. Bacteriol. 154:537-546.
14. Chenna, R., H. Sugawara, T. Koike, R. Lopez, T. J. Gibson, D. G. Higgins, and J. D. Thompson. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31:3497-3500.
15. Daniel, R. A., E. J. Harry, V. L. Katis, R. G. Wake, and J. Errington. 1998. Characterization of the essential cell division gene ftsL (yllD) of Bacillus subtilis and its role in the assembly of the division apparatus. Mol. Microbiol. 29:593-604.
16. DeLano, W. L. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, Calif.
17. Erickson, H. P., D. W. Taylor, K. A. Taylor, and D. Bramhill. 1996. Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc. Natl. Acad. Sci. USA 93:519-523.
18. Errington, J. 1984. Efficient Bacillus subtilis cloning system using bacteriophage vector phi 105J9. J. Gen. Microbiol. 130:2615-2628.
19. Feucht, A., and P. J. Lewis. 2001. Improved plasmid vectors for the production of multiple fluorescent protein fusions in Bacillus subtilis. Gene 264:289-297.
20. Feucht, A., I. Lucet, M. D. Yudkin, and J. Errington. 2001. Cytological and biochemical characterization of the FtsA cell division protein of Bacillus subtilis. Mol. Microbiol. 40:115-125.
21. Feucht, A., and J. Errington. 2005. ftsZ mutations affecting cell division frequency, placement and morphology in Bacillus subtilis. Microbiology 151:2053-2064.
22. Grantcharova, N., U. Lustig, and K. Flärdh. 2005. Dynamics of FtsZ assembly during sporulation in Streptomyces coelicolor A3(2). J. Bacteriol. 187:3227-3237.
23. Gueiros-Filho, F. J., and R. Losick. 2002. A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev. 16:2544-2556.
24. Guex, N., and M. C. Peitsch. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714-2723.
25. Hale, C. A., and P. A. de Boer. 1997. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in Escherichia coli. Cell 88:175-185.
26. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
27. Harry, E. J., and R. G. Wake. 1989. Cloning and expression of a Bacillus subtilis division initiation gene for which a homolog has not been identified in another organism. J. Bacteriol. 171:6835-6839.
28. Harry, E. J., J. Rodwell, and R. G. Wake. 1999. Co-ordinating DNA replication with cell division in bacteria: a link between the early stages of a round of replication and mid-cell Z ring assembly. Mol. Microbiol. 33:33-40.
29. Hauser, P. M., and J. Errington. 1995. Characterization of cell cycle events during the onset of sporulation in Bacillus subtilis. J. Bacteriol. 177:3923-3931.
30. Hu, Z. M., A. Pichoff, and J. Lutkenhaus. 1999. 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.
31. Levin, P. A., I. G. Kurtser, and A. D. Grossman. 1999. Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 96:9642-9647.
32. Levin, P. A., R. L. Schwartz, and A. D. Grossman. 2001. Polymer stability plays an important role in the positional regulation of FtsZ. J. Bacteriol. 183:5449-5452.
33. Liang, M. P., D. R. Banatao, T. E. Klein, D. L. Brutlag, and R. B. Altman. 2003. WebFEATURE: an interactive web tool for identifying and visualizing functional sites on macromolecular structures. Nucleic Acids Res. 31:3324-3327.
34. Löwe, J., and L. A. Amos. 1998. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391:203-206.
35. 2+-induced FtsZ sheets. EMBO J. 18:2364-2371.
36. Löwe, J., and L. A. Amos. 2000. Helical tubes of FtsZ from Methanococcus jannaschii. J. Biol. Chem. 381:993-999.
37. Löwe, J., F. van den Ent, and L. A. Amos. 2004. Molecules of the bacterial cytoskeleton. Annu. Rev. Biophys. Biomol. Struct. 33:177-198.
38. Ma, X., D. W. Ehrhardt, and W. Margolin. 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. USA 93:12998-13003.
39. Migocki, M. D., M. K. Freeman, R. G. Wake, and E. J. Harry. 2002. The Min system is not required for precise placement of the midcell Z ring in Bacillus subtilis. EMBO Rep. 3:1163-1167.
40. Mileykovskaya, E., Q. Sun, W. Margolin, and W. Dowhan. 1998. Localization and function of early cell division proteins in filamentous Escherichia coli cells lacking phosphatidylethanolamine. J. Bacteriol. 180:4252-4257.
41. Nogales, E., K. H. Downing, L. A. Amos, and J. Löwe. 1998. Tubulin and FtsZ form a distinct family of GTPases. Nat. Struct. Biol. 5:451-458.
42. Nukushina, J. I., and Y. Ikeda. 1969. Genetic analysis of the developmental processes during germination and outgrowth of Bacillus subtilis spores with temperature-sensitive mutants. Genetics 63:63-74.
43. Oliva, M. A., S. C. Cordell, and J. Löwe. 2004. Structural insights into FtsZ protofilament formation. Nat. Struct. Mol. Biol. 11:1243-1250.
44. Pichoff, S., and J. Lutkenhaus. 2002. Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 21:685-693.
45. Pichoff, S., and J. Lutkenhaus. 2005. Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol. Microbiol. 55:1722-1734.
46. Regamey, A., E. J. Harry, and R. G. Wake. 2000. Mid-cell Z ring assembly in the absence of entry into the elongation phase of the round of replication in bacteria: coordinating chromosome replication with cell division. Mol. Microbiol. 38:423-434.
47. Romberg, L., M. Simon, and H. P. Erickson. 2001. Polymerization of FtsZ, a bacterial homolog of tubulin. Is assembly cooperative? J. Biol. Chem. 276:11743-11753.
48. Romberg, L., and P. A. Levin. 2003. Assembly dynamics of the bacterial cell division protein FtsZ: poised at the edge of stability. Annu. Rev. Microbiol. 57:125-154.
49. Santra, M. K., and D. Panda. 2003. Detection of an intermediate during unfolding of bacterial cell division protein FtsZ. J. Biol. Chem. 278:21336-21343.
50. Schwede, T., J. Kopp, N. Guex, and M. Peitsch. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385.
51. Spizizen, J. 1958. Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc. Natl. Acad. Sci. USA 44:407-408.
52. Sreerama, N., and R. W. Woody. 2000. Estimation of protein secondary structure from CD spectra: comparison of CONTIN, SELCON and CDSSTR methods with an expanded reference set. Anal. Biochem. 282:252-260.
53. Sreerama, N., S. Y. Venyaminov, and R. W. Woody. 2001. Analysis of protein circular dichroism spectra based on the tertiary structure classification. Anal. Biochem. 299:271-274.
54. Stricker, J., P. Maddox, E. D. Salmon, and H. P. Erickson. 2002. Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc. Natl. Acad. Sci. USA 99:3171-3175.
55. Stricker, J., and H. P. Erickson. 2003. In vivo characterization of Escherichia coli ftsZ mutants: effects on Z-ring structure and function. J. Bacteriol. 185:4796-4805.
56. Thanedar, S., and W. Margolin. 2004. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14:1167-1173.
57. Wang, X., and J. Lutkenhaus. 1993. 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.
58. Wang, Y., B. Jones, and Y. Brun. 2001. A set of ftsZ mutants blocked at different stages of cell division in Caulobacter. Mol. Microbiol. 40:347-360.
59. Woldringh, C. L., E. Mulder, P. G. Huls, and N. O. E. Vischer. 1991. Toporegulation of bacterial division according to the nucleoid occlusion model. Res. Microbiol. 142:309-320.
60. Wu, L. J., and J. Errington. 2004. Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117:915-925.
61. 2+-mediated GTP-dependent dynamic assembly of bacterial cell division protein FtsZ into asters and polymer networks in vitro. EMBO J. 16:5455-5463.