Structural Insights into the Conformational Variability of FtsZ

Journal of Molecular Biology

Volumn 373, Issue 5, 2007, Pages 1229-1242

  Oliva, María A ^a   Trambaiolo, Daniel ^a   Löwe, Jan ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

bacterial cell division; crystal structure; divisome; FtsZ; tubulin

Indexed keywords

CYTOSKELETON PROTEIN; FTSZ PROTEIN; TUBULIN;

AQUIFEX AEOLICUS; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; CELL DIVISION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DEPOLYMERIZATION; METHANOCOCCUS JANNASCHII; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN POLYMERIZATION; PROTEIN PURIFICATION; PSEUDOMONAS AERUGINOSA; SPECIES DIFFERENCE;

AQUIFEX AEOLICUS; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); EUKARYOTA; METHANOCALDOCOCCUS JANNASCHII; PROKARYOTA; PSEUDOMONAS AERUGINOSA;

EID: 35148840132     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.08.056     Document Type: Article

References (49)

1. Bi E.F., and Lutkenhaus J. FtsZ ring structure associated with division in Escherichia coli. Nature 354 (1991) 161-164
2. Stricker J., Maddox P., Salmon E.D., and Erickson H.P. Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc. Natl Acad. Sci. USA 99 (2002) 3171-3175
3. Mukherjee A., Dai K., and Lutkenhaus J. Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc. Natl Acad. Sci. USA 90 (1993) 1053-1057
4. Bramhill D., and Thompson C.M. GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc. Natl Acad. Sci. USA 91 (1994) 5813-5817
5. Romberg L., and Levin P.A. Assembly dynamics of the bacterial cell division protein FTSZ: poised at the edge of stability. Annu. Rev. Microbiol. 57 (2003) 125-154
6. Errington J., Daniel R.A., and Scheffers D.J. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67 (2003) 52-65
7. Weiss D.S. Bacterial cell division and the septal ring. Mol. Microbiol. 54 (2004) 588-597
8. Michie K.A., and Löwe J. Dynamic filaments of the bacterial cytoskeleton. Annu. Rev. Biochem. 75 (2006) 467-492
9. Graumann P.L. Cytoskeletal elements in bacteria. Annu. Rev. Microbiol. (2006) 10.1146/annurev.micro.61.080706.093236
10. Varma A., and Young K.D. FtsZ collaborates with penicillin binding proteins to generate bacterial cell shape in Escherichia coli. J. Bacteriol. 186 (2004) 6768-6774
11. Aaron M., Charbon G., Lam H., Schwarz H., Vollmer W., and Jacobs-Wagner C. The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus. Mol. Microbiol. 64 (2007) 938-952
12. Varma A., de Pedro M., and Young K.D. FtsZ directs a second mode of peptidoglycan synthesis in Escherichia coli. J. Bacteriol. 15 (2007) 5692-5704
13. Löwe J., and Amos L.A. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391 (1998) 203-206
14. Nogales E., Wolf S.G., and Downing K.H. Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391 (1998) 199-203
15. Nogales E., Downing K.H., Amos L.A., and Löwe J. Tubulin and FtsZ form a distinct family of GTPases. Nature, Struct. Biol. 5 (1998) 451-458
16. Desai A., and Mitchison T.J. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13 (1997) 83-117
17. Molodtsov M.I., Grishchuk E.L., Efremov A.K., McIntosh J.R., and Ataullakhanov F.I. Force production by depolymerizing microtubules: a theoretical study. Proc. Natl Acad. Sci. USA 102 (2005) 4353-4358
18. Westermann S., Wang H.W., Avila-Sakar A., Drubin D.G., Nogales E., and Barnes G. The Dam1 kinetochore ring complex moves processively on depolymerizing microtubule ends. Nature 440 (2006) 565-569
19. Gonzalez J.M., Jimenez M., Velez M., Mingorance J., Andreu J.M., Vicente M., and Rivas G. Essential cell division protein FtsZ assembles into one monomer-thick ribbons under conditions resembling the crowded intracellular environment. J. Biol. Chem. 278 (2003) 37664-37671
20. Oliva M.A., Huecas S., Palacios J.M., Martin-Benito J., Valpuesta J.M., and Andreu J.M. Assembly of archaeal cell division protein FtsZ and a GTPase-inactive mutant into double-stranded filaments. J. Biol. Chem. 278 (2003) 33562-33570
21. Lu C., Reedy M., and Erickson H.P. Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J. Bacteriol. 182 (2000) 164-170
22. Huecas S., and Andreu J.M. Polymerization of nucleotide-free, GDP- and GTP-bound cell division protein FtsZ: GDP makes the difference. FEBS Letters 569 (2004) 43-48
23. Mingorance J., Rueda S., Gomez-Puertas P., Valencia A., and Vicente M. Escherichia coli FtsZ polymers contain mostly GTP and have a high nucleotide turnover. Mol. Microbiol. 41 (2001) 83-91
24. Chen Y., and Erickson H.P. Rapid in vitro assembly dynamics and subunit turnover of FtsZ demonstrated by fluorescence resonance energy transfer. J. Biol. Chem. 280 (2005) 22549-22554
25. Li H., DeRosier D.J., Nicholson W.V., Nogales E., and Downing K.H. Microtubule structure at 8 Å resolution. Structure 10 (2002) 1317-1328
26. Ravelli R.B., Gigant B., Curmi P.A., Jourdain I., Lachkar S., Sobel A., and Knossow M. Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain. Nature 428 (2004) 198-202
27. Wang H.W., and Nogales E. Nucleotide-dependent bending flexibility of tubulin regulates microtubule assembly. Nature 435 (2005) 911-915
28. Aldaz H., Rice L.M., Stearns T., and Agard D.A. Insights into microtubule nucleation from the crystal structure of human gamma-tubulin. Nature 435 (2005) 523-527
29. Schlieper D., Oliva M.A., Andreu J.M., and Löwe J. Structure of bacterial tubulin BtubA/B: evidence for horizontal gene transfer. Proc. Natl Acad. Sci. USA 102 (2005) 9170-9175
30. Schlichting I., Almo S.C., Rapp G., Wilson K., Petratos K., Lentfer A., et al. Time-resolved X-ray crystallographic study of the conformational change in Ha-Ras p21 protein on GTP hydrolysis. Nature 345 (1990) 309-315
31. Wittinghofer A., and Pai E.F. The structure of Ras protein: a model for a universal molecular switch. Trends Biochem. Sci. 16 (1991) 382-387
32. Kjeldgaard M., Nissen P., Thirup S., and Nyborg J. The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation. Structure 1 (1993) 35-50
33. Roll-Mecak A., Cao C., Dever T.E., and Burley S.K. X-ray structures of the universal translation initiation factor IF2/eIF5B: conformational changes on GDP and GTP binding. Cell 103 (2000) 781-792
34. Nogales E., and Wang H.W. Structural mechanisms underlying nucleotide-dependent self-assembly of tubulin and its relatives. Curr. Opin. Struct. Biol. 16 (2006) 221-229
35. Nogales E., and Wang H.W. Structural intermediates in microtubule assembly and disassembly: how and why?. Curr. Opin. Cell Biol. 18 (2006) 179-184
36. Oliva M.A., Cordell S.C., and Löwe J. Structural insights into FtsZ protofilament formation. Nature Struct. Mol. Biol. 11 (2004) 1243-12450
37. Buey R.M., Diaz J.F., and Andreu J.M. The nucleotide switch of tubulin and microtubule assembly: a polymerization-driven structural change. Biochemistry 45 (2006) 5933-5938
38. Urgaonkar S., La Pierre H.S., Meir I., Lund H., RayChaudhuri D., and Shaw J.T. Synthesis of antimicrobial natural products targeting FtsZ: (+/-)-dichamanetin and (+/-)-2′ ″-hydroxy-5′ ′-benzylisouvarinol-B. Org. Letters 7 (2005) 5609-5612
39. Erickson H.P., Taylor D.W., Taylor K.A., and Bramhill D. Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc. Natl Acad. Sci. USA 93 (1996) 519-523
40. Wang H.W., Long S., Finley K.R., and Nogales E. Assembly of GMPCPP-bound tubulin into helical ribbons and tubes and effect of colchicine. Cell Cycle 4 (2005) 1157-1160
41. Cordell S.C., Robinson E.J., and Lowe J. Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc. Natl Acad. Sci. USA 100 (2003) 7889-7894
42. Mukherjee A., Cao C.N., and Lutkenhaus J. Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. Proc. Natl Acad. Sci. USA 95 (1998) 2885-2890
43. Nicholson W.V., Lee M., Downing K.H., and Nogales E. Cryo-electron microscopy of GDP-tubulin rings. Cell Biochem. Biophys. 31 (1999) 175-183
44. Rivas G., Lopez A., Mingorance J., Ferrandiz M.J., Zorrilla S., Minton A.P., et al. Magnesium-induced linear self-association of the FtsZ bacterial cell division protein monomer. The primary steps for FtsZ assembly. J. Biol. Chem. 275 (2000) 11740-11749
45. Stock D., Perisic O., and Löwe J. Robotic nanolitre protein crystallisation at the MRC Laboratory of Molecular Biology. Prog. Biophys. Mol. Biol. 88 (2005) 311-327
46. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
47. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
48. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
49. Krissinel E., and Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallog. sect. D 60 (2004) 2256-2268