Nucleotide-dependent conformations of FtsZ dimers and force generation observed through molecular dynamics simulations

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 24, 2012, Pages 9432-9437

  Hsin, Jen ^a   Gopinathan, Ajay ^b   Huang, Kerwyn C ^a  

^a Stanford University   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bacterial cell division; Bacterial cytoskeleton; GTP hydrolysis

Indexed keywords

CYTOSKELETON PROTEIN; DIMER; FTSZ PROTEIN; GUANOSINE DIPHOSPHATE; LIPOSOME; MONOMER; NUCLEOTIDE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR;

ARTICLE; CELL DIVISION; CELL WALL; MOLECULAR DYNAMICS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE;

BACTERIAL PROTEINS; CYTOSKELETAL PROTEINS; DIMERIZATION; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION;

EID: 84862189021     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1120761109     Document Type: Article

References (50)

1. Bi E, Lutkenhaus J (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354:161-164. (Pubitemid 21896803)
2. Li Z, Trimble MJ, Brun YV, Jensen GJ (2007) The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J 26:4694-4708. (Pubitemid 350126800)
3. Fu G, et al. (2010) In vivo structure of the E. coli FtsZ-ring revealed by photoactivated localization microscopy (PALM). PLoS ONE 5:e12680.
4. Dai K, Lutkenhaus J (1991) ftsZ is an essential cell division gene in Escherichia coli. J Bacteriol 173:3500-3506.
5. Adams DW, Errington J (2009) Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7:642-653.
6. Goley ED, et al. (2011) Assembly of the Caulobacter cell division machine. Mol Microbiol 80:1680-1698.
7. Osawa M, Anderson DE, Erickson HP (2008) Reconstitution of contractile FtsZ rings in liposomes. Science 320:792-794. (Pubitemid 351929627)
8. Osawa M, Anderson DE, Erickson HP (2009) Curved FtsZ protofilaments generate bending forces on liposome membranes. EMBO J 28:3476-3484.
9. Erickson HP, Anderson DE, Osawa M (2010) FtsZ in bacterial cytokinesis: Cytoskeleton and force generator all in one. Microbiol Mol Biol R 74:504-528.
10. Osawa M, Erickson HP (2011) Inside-out Z-rings - constriction with and without GTP hydrolysis. Mol Microbiol 81:571-579.
11. Erickson HP (2009) Modeling the physics of FtsZ assembly and force generation. Proc Natl Acad Sci USA 106:9238-9243.
12. Erickson HP, Taylor DW, Taylor KA, Bramhill D (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. (Pubitemid 26038188)
13. Erickson HP (1997) FtsZ, a tubulin homologue in prokaryote cell division. Trends Cell Biol 7:362-367.
14. Lu C, Reedy M, Erickson HP (2000) Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J Bacteriol 182:164-170. (Pubitemid 30004571)
15. Huecas S, Andreu JM (2004) Polymerization of nucleotide-free, GDP- and GTP-bound cell division protein FtsZ: GDP makes the difference. FEBS Lett 569:43-48. (Pubitemid 38844590)
16. Allard JF, Cytrynbaum EN (2009) Force generation by a dynamic Z-ring in Escherichia coli cell division. Proc Natl Acad Sci USA 106:145-150.
17. Lan G, Wolgemuth CW, Sun SX (2007) Z-ring force and cell shape during division in rod-like bacteria. Proc Natl Acad Sci USA 104:16110-16115. (Pubitemid 350099370)
18. Oliva MA, Trambaiolo D, Löwe J (2007) Structural insights into the conformational variability of FtsZ. J Mol Biol 373:1229-1242. (Pubitemid 47539485)
19. Chu JW, Voth GA (2005) Allostery of actin filaments: molecular dynamics simulations and coarse-grained analysis. Proc Natl Acad Sci USA 102:13111-13116.
20. Wells DB, Aksimentiev A (2010) Mechanical properties of a complete microtubule revealed through molecular dynamics simulation. Biophys J 99:629-637.
21. Skjaerven L, et al. (2011) Conformational sampling and nucleotide-dependent transitions of the GroEL subunit probed by unbiased molecular dynamics simulations. PLoS Comput Biol 7:e1002004.
22. Lukman S, Grant BJ, Gorfe AA, Grant GH, McCammon JA (2010) The distinct conformational dynamics of K-Ras and H-Ras A59G. PLoS Comput Biol 6:e1000922.
23. Oliva MA, Cordell SC, Löwe J (2004) Structural insights into FtsZ protofilament formation. Nat Struct Mol Biol 11:1243-1250.
24. Mukherjee A, Dai K, Lutkenhaus J (1993) Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc Natl Acad Sci USA 90:1053-1057. (Pubitemid 23053949)
25. Mukherjee A, 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)
26. Scheffers DJ, Driessen AJ (2001) The polymerization mechanism of the bacterial cell division protein FtsZ. FEBS Lett 506:6-10.
27. Romberg L, Simon M, Erickson HP (2001) Polymerization of FtsZ, a bacterial homolog of tubulin. J Biol Chem 276:11743-11753.
28. Huecas S, et al. (2007) The interactions of cell division protein FtsZ with guanine nucleotides. J Biol Chem 282:37515-37528.
29. Martin-Galiano AJ, Buey RM, Cabezas M, Andreu JM (2010) Mapping flexibility and the assembly switch of cell division protein FtsZ by computational and mutational approaches. J Biol Chem 285:22554-22565.
30. Chen Y, Bjornson K, Redick SD, Erickson HP (2005) A rapid fluorescence assay for FtsZ assembly indicates cooperative assembly with a dimer nucleus. Biophys J 88:505-514. (Pubitemid 40070696)
31. Gonzàlez JM, et al. (2005) Cooperative behavior of Escherichia coli cell-division protein FtsZ assembly involves the preferential cyclization of long single-stranded fibrils. Proc Natl Acad Sci USA 102:1895-1900. (Pubitemid 40261983)
32. Mingorance J, et al. (2005) Visualization of single Escherichia coli FtsZ filament dynamics with atomic force microscopy. J Biol Chem 280:20909-20914. (Pubitemid 40776797)
33. Huecas S, et al. (2008) Energetics and geometry of FtsZ polymers: Nucleated self-assembly of single protofilaments. Biophys J 94:1796-1806.
34. Mukherjee A, Saez C, Lutkenhaus J (2001) Assembly of an FtsZ mutant deficient in GTPase activity has implications for FtsZ assembly and the role of the Z ring in cell division. J Bacteriol 183:7190-7197. (Pubitemid 33121853)
35. Sun Q, Margolin W (1998) FtsZ dynamics during the division cycle of live Escherichia coli cells. J Bacteriol 180:2050-2056. (Pubitemid 28212689)
36. Margolin W (2002) Bacterial sporulation: FtsZ rings do the twist. Curr Biol 12: R391-R392.
37. Ben-Yehuda S, Losick R (2002) Asymmetric cell division inB.subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109:257-266. (Pubitemid 34518263)
38. Thanedar S, Margolin W (2004) FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr Biol 14:1167-1173. (Pubitemid 38893979)
39. Helfrich W (1973) Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch 28:693-703.
40. Rawicz W, Olbrich KC, McIntosh T, Needham D, Evans E (2000) Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J 79:328-339. (Pubitemid 30436749)
41. Lu C, Stricker J, Erickson HP (2001) Site-specific mutations of FtsZ - effects on GTPase and in vitro assembly. BMC Microbiol 1:7.
42. Stricker J, Erickson HP (2003) In vivo characterization of Escherichia coli ftsZ mutants: Effects on Z-ring structure and function. J Bacteriol 185:4796-4805. (Pubitemid 36962287)
43. Redick SD, Stricker J, Briscoe G, Erickson HP (2005) Mutants of FtsZ targeting the protofilament interface: effects on cell division and GTPase activity. J Bacteriol 187:2727-2736. (Pubitemid 40490377)
44. Phillips JC, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781-1802. (Pubitemid 43078511)
45. MacKerell AD, Jr, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102:3586-3616.
46. Foloppe N, MacKerrell AD, Jr (2000) All-atom empirical force field for nucleic acids: I. Parameter optimization based on small molecule and condensed phase macromolecular target data. J Comput Chem 21:86-104.
47. MacKerell AD, Jr, Feig M, Brooks CL, III (2004) Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 25:1400-1415.
48. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79:926-935.
49. Humphrey W, Dalke A, Schulten K (1996) VMD - Visual Molecular Dynamics. J Mol Graphics 14:33-38.
50. Roberts E, Eargle J, Wright D, Luthey-Schulten Z (2006) MultiSeq: unifying sequence and structure data for evolutionary analysis. BMC Bioinformatics 7:382.