The GTPase activity of Escherichia coli FtsZ determines the magnitude of the FtsZ polymer bundling by ZapA in vitro

Biochemistry

Volumn 48, Issue 46, 2009, Pages 11056-11066

  Mohammadi, Tamimount ^a,d   Ploeger, Ginette E J ^a   Verheul, Jolanda ^a   Comvalius, Anouskha D ^a   Martos, Ariadna ^b   Alfonso, Carlos ^b   Van Marle, Jan ^c   Rivas, German ^b   Den Blaauwen, Tanneke ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DIVISIONS; CONCENTRATION OF; COOPERATIVITY; GTP HYDROLYSIS; GTPASE ACTIVITY; HELICAL FILAMENT; HIS-TAG; IN-VITRO; IN-VIVO; NON-DIVIDING CELLS; PHYSIOLOGICAL PH; PROTOFILAMENTS; RATE LIMITING FACTORS;

CELL PROLIFERATION; ESCHERICHIA COLI; HYDROLYSIS; PELLETIZING; PH EFFECTS; PROTEINS; STABILIZATION;

POLYMERS;

BACTERIAL PROTEIN; FTSZ PROTEIN; GUANOSINE TRIPHOSPHATASE; PROTEIN ZAPA; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVITY; ESCHERICHIA COLI; IN VITRO STUDY; LIGHT SCATTERING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION;

BACTERIAL PROTEINS; BIOPOLYMERS; CARRIER PROTEINS; CELL SIZE; CYTOSKELETAL PROTEINS; CYTOSKELETON; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GTP PHOSPHOHYDROLASES; GUANOSINE TRIPHOSPHATE; HISTIDINE; HYDROGEN-ION CONCENTRATION; LIGHT; MAGNESIUM CHLORIDE; OLIGOPEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; RECOMBINANT FUSION PROTEINS; SCATTERING, RADIATION; ULTRACENTRIFUGATION;

ESCHERICHIA COLI;

EID: 72749125802     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901461p     Document Type: Article

References (55)

1. den Blaauwen, T., de Pedro, M. A., Nguyen-Disteche, M., and Ayala, J. A. (2008) Morphogenesis of rod-shaped sacculi. FEMS Microbiol. Rev. 32, 321-344.
2. Harry, E., Monahan, L., and Thompson, L. (2006) Bacterial cell division: the mechanism and its precison. Int. Rev. Cytol. 253, 27-94.
3. Anderson, D. E., Gueiros-Filho, F. J., and Erickson, H. P. (2004) Assembly dynamics ofFtsZrings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J. Bacteriol. 186, 5775-5781.
4. Pla, J., Sanchez, M., Palacios, P., Vicente, M., and Aldea, M. (1991) Preferential cytoplasmic location of FtsZ, a protein essential for Escherichia coli septation. Mol. Microbiol. 5, 1681-1686.
5. Rueda, S., Vicente, M., and Mingorance, J. (2003) Concentration and assembly of the division ring proteins FtsZ, FtsA, and ZipA during the Escherichia coli cell cycle. J. Bacteriol. 185, 3344-3351.
6. Feucht, A., and Errington, J. (2005) ftsZ mutations affecting cell division frequency, placement and morphology in Bacillus subtilis. Microbiology 151, 2053-2064. (Pubitemid 40909047)
7. Mukherjee, A., and Lutkenhaus, J. (1999) Analysis of FtsZ assembly by light scattering and determination of the role of divalent metal cations. J. Bacteriol. 181, 823-832. (Pubitemid 29061564)
8. Raskin, D. M., and de Boer, P. A. (1999) Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 96, 4971-4976.
9. Bernhardt, T. G., and de Boer, P. A. (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol. Cell 18, 555-564.
10. Mukherjee, A., Dai, K., and Lutkenhaus, J. (1993) Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc. Natl. Acad. Sci. U.S.A. 90, 1053-1057.
11. Michie, K. A., and Lowe, J. (2006) Dynamic filaments of the bacterial cytoskeleton. Annu. Re. Biochem. 75, 467-492.
12. Scheffers, D. J., de Wit, J. G., den Blaauwen, T., and Driessen, A. J. (2002) GTP hydrolysis of cell division protein FtsZ: evidence that the active site is formed by the association of monomers. Biochemistry 41, 521-529.
13. Scheffers, D. J., and Driessen, A. J. (2002) Immediate GTP hydrolysis upon FtsZ polymerization. Mol. Microbiol. 43, 1517-1521.
14. Romberg, L., and Mitchison, T. J. (2004) Rate-limiting guanosine 5′-triphosphate hydrolysis during nucleotide turnover by FtsZ, a prokaryotic tubulin homologue involved in bacterial cell division. Biochemistry 43, 282-288. (Pubitemid 38055966)
15. Romberg, L., and 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.
16. 2+-induced FtsZ sheets. EMBO J. 18, 2364-2371.
17. 2+-mediated GTP-dependent dynamic assembly of bacterial cell division protein FtsZ into asters and polymer networks in vitro. EMBO J. 16, 5455-5463.
18. Rivas, G., Lopez, A., Mingorance, J., Ferrandiz, M. J., Zorrilla, S., Minton, A. P., Vicente, M., and Andreu, J. M. (2000) Magnesiuminduced linear self-association of the FtsZ bacterial cell division protein monomer. The primary steps for FtsZ assembly. J. Biol. Chem. 275, 11740-11749.
19. Tadros, M., Gonzalez, J. M., Rivas, G., Vicente, M., and Mingorance, J. (2006) Activation of the Escherichia coli cell division protein FtsZ by a low-affinity interaction with monovalent cations. FEBS Lett. 580, 4941-4946. (Pubitemid 44286847)
20. Popp, D., Iwasa, M., Narita, A., Erickson, H. P., and Maeda, Y. (2009) FtsZ condensates: an in vitro electron microscopy study. Biopolymers 91, 340-350.
21. Huecas, S., Llorca, O., Boskovic, J., Martin-Benito, J., Valpuesta, J. M., and Andreu, J. M. (2008) Energetics and geometry of FtsZ polymers: nucleated self-assembly of single protofilaments. Biophys. J. 94, 1796-1806.
22. Gonzalez, J. M., Velez, M., Jimenez, M., Alfonso, C., Schuck, P., Mingorance, J., Vicente, M., Minton, A. P., and Rivas, G. (2005) Cooperative behavior of Escherichia coli cell-division protein FtsZ assembly involves the preferential cyclization of long single-stranded fibrils. Proc. Natl. Acad. Sci. U.S.A. 102, 1895-1900.
23. Mukherjee, A., and Lutkenhaus, J. (1998) Dynamic assembly of FtsZ regulated by GTP hydrolysis. EMBO J. 17, 462-469. (Pubitemid 28045487)
24. White, E. L., Ross, L. J., Reynolds, R. C., Seitz, L. E., Moore, G. D., and Borhani, D. W. (2000) Slow polymerization of Mycobacterium tuberculosis FtsZ. J. Bacteriol. 182, 4028-4034.
25. Small, E., Marrington, R., Rodger, A., Scott, D. J., Sloan, K., Roper, D., Dafforn, T. R., and Addinall, S. G. (2007) FtsZ polymer-bundling by the Escherichia coli ZapA orthologue, YgfE, involves a conformational change in bound GTP. J. Mol. Biol. 369, 210-221.
26. Mendieta, J., Rico, A. I., Lopez-Vinas, E., Vicente, M., Mingorance, J., and Gomez-Puertas, P. (2009) Structural and functional model for ionic (K(+)/Na(+)) and pH dependence of GTPase activity and polymerization of FtsZ, the prokaryotic ortholog of tubulin. J. Mol. Biol. 390, 17-25.
27. Low, H. H., Moncrieffe, M. C., and Lowe, J. (2004) The crystal structure of ZapA and its modulation of FtsZ polymerisation. J. Mol. Biol. 341, 839-852.
28. Gueiros-Filho, F. J., and Losick, R. (2002) A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev. 16, 2544-2556.
29. Peters, J. E., Thate, T. E., and Craig, N. L. (2003) Definition of the Escherichia coli MC4100 genome by use of aDNA array. J. Bacteriol. 185, 2017-2021.
30. Taschner, P. E., Huls, P. G., Pas, E., and Woldringh, C. L. (1988) Division behavior and shape changes in isogenic ftsZ, ftsQ, ftsA, pbpB, and ftsE cell division mutants of Escherichia coli during temperature shift experiments. J. Bacteriol. 170, 1533-1540.
31. Baneyx, F., and Georgiou, G. (1990) In vivo degradation of secreted fusion proteins by the Escherichia coli outer membrane protease OmpT. J. Bacteriol. 172, 491-494.
32. Koppelman, C. M., Aarsman, M. E., Postmus, J., Pas, E., Muijsers, A. O., Scheffers, D. J., Nanninga, N., and den Blaauwen, T. (2004) R174 of Escherichia coli FtsZ is involved in membrane interaction and protofilament bundling, and is essential for cell division. Mol. Microbiol. 51, 645-657.
33. van der Does, C., Manting, E. H., Kaufmann, A., Lutz, M., and Driessen, A. J. (1998) Interaction between SecA and SecYEG in micellar solution and formation of the membrane-inserted state. Biochemistry 37, 201-210. (Pubitemid 28049122)
34. Fishov, I., Zaritsky, A., and Grover, N. B. (1995) On microbial states of growth. Mol. Microbiol. 15, 789-794.
35. Voskuil, J. L., Westerbeek, C. A., Wu, C., Kolk, A. H., and Nanninga, N. (1994) Epitope mapping of Escherichia coli cell division protein FtsZ with monoclonal antibodies. J. Bacteriol. 176, 1886-1893. (Pubitemid 24103536)
36. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78, 1606-1619.
37. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992) Computer-aided interpretation of analytical sedimentation data for proteins, in Analytical Ultracentrifugation in Biochemistry and Polymer Science (Harding, S. E., Rowe, A. J., Horton, J. C., Eds.) The Royal Society of Chemistry, Cambridge, pp 90-125.
38. Attri, A. K., and Minton, A. P. (2005) New methods for measuring macromolecular interactions in solution via static light scattering: basic methodology and application to nonassociating and self-associating proteins. Anal. Biochem. 337, 103-110.
39. Läppchen, T., Hartog, A. F., Pinas, V. A., Koomen, G. J., and den Blaauwen, T. (2005) GTP analogue inhibits polymerization and GTPase activity of the bacterial protein FtsZ without affecting its eukaryotic homologue tubulin. Biochemistry 44, 7879-7884. (Pubitemid 40740771)
40. Real, G., Autret, S., Harry, E. J., Errington, J., and Henriques, A. O. (2005) Cell division protein DivIB influences the Spo0J/Soj system of chromosome segregation in Bacillus subtilis. Mol. Microbiol. 55, 349-367.
41. Padan, E., Zilberstein, D., and Schuldiner, S. (1981) pH homeostasis in bacteria. Biochim. Biophys. Acta 650, 151-166.
42. Zilberstein, D., Agmon, V., Schuldiner, S., and Padan, E. (1984) Escherichia coli intracellular pH, membrane potential, and cell growth. J. Bacteriol. 158, 246-252. (Pubitemid 14125217)
43. Johnson, J. E., Lackner, L. L., Hale, C. A., and de Boer, P. A. (2004) 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.
44. Aarsman, M. E., Piette, A., Fraipont, C., Vinkenvleugel, T. M., Nguyen-Disteche, M., and den Blaauwen, T. (2005) Maturation of the Escherichia coli divisome occurs in two steps. Mol. Microbiol. 55, 1631-1645.
45. Dajkovic, A., Lan, G., Sun, S. X., Wirtz, D., and Lutkenhaus, J. (2008) MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ. Curr. Biol. 18, 235-244.
46. Scheffers, D. J. (2008) The effect of MinC on FtsZ polymerization is pH dependent and can be counteracted by ZapA. FEBS Lett. 582, 2601-2608.
47. Scheffers, D., and Driessen, A. J. (2001) The polymerization mechanism of the bacterial cell division protein FtsZ. FEBS Lett. 506, 6-10. (Pubitemid 32925222)
48. Romberg, L., Simon, M., and Erickson, H. P. (2001) Polymerization of Ftsz, a bacterial homolog of tubulin, is assembly cooperative? J. Biol. Chem. 276, 11743-11753.
49. Peters, P. C., Migocki, M. D., Thoni, C., and Harry, E. J. (2007) 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.
50. Thanedar, S., and Margolin, W. (2004) FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14, 1167-1173.
51. Erickson, H. P. (1997) FtsZ, a tubulin homologue in prokaryote cell division. Trends Cell Biol. 7, 362-367. (Pubitemid 27384782)
52. den Blaauwen, T., Buddelmeijer, N., Aarsman, M. E. G., Hameete, C. M., and Nanninga, N. (1999) Timing of FtsZ assembly in Escherichia coli. J. Bacteriol. 181, 5167-5175. (Pubitemid 29416333)
53. Chen, Y., and Erickson, H. P. (2009) FtsZfilament dynamics at steady state: subunit exchange with and without nucleotide hydrolysis. Biochemistry 48, 6664-6673.
54. Li, Z., Trimble, M. J., Brun, Y. V., and Jensen, G. J. (2007) The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J. 26, 4694-4708. (Pubitemid 350126800)
55. Lan, G., Dajkovic, A., Wirtz, D., and Sun, S. X. (2008) Polymerization and bundling kinetics of FtsZ filaments. Biophys. J. 95, 4045-4056.