Insights into nucleotide recognition by cell division protein FtsZ from a mant-GTP competition assay and molecular dynamics

Biochemistry

Volumn 49, Issue 49, 2010, Pages 10458-10472

  Schaffner Barbero, Claudia ^a   Gil Redondo, Rubén ^b   Ruiz Avila, Laura B ^a   Huecas, Sonia ^a   Läppchen, Tilman ^c   Den Blaauwen, Tanneke ^c   Diaz, J Fernando ^a   Morreale, Antonio ^b   Andreu, Jose M ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITIES; BINDING FREE ENERGY; CELL DIVISIONS; DOMINANT CONTRIBUTIONS; FLUORESCENCE ANISOTROPY; FREE ENERGY CHANGE; GTP ANALOGUE; GUANOSINES; MIMETICS; NUCLEOTIDE BINDING; RATIONAL DESIGN; RELATIVE CONTRIBUTION; TUBULIN ASSEMBLY; VIRTUAL SCREENING;

CELL PROLIFERATION; COMPETITION; COMPLEXATION; DIGITAL LIBRARIES; FREE ENERGY; MOLECULAR DYNAMICS; MONOMERS; NUCLEOTIDES;

BINDING ENERGY;

FTSZ PROTEIN; GUANINE; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; NUCLEOTIDE; RIBOSE;

ANISOTROPY; ARTICLE; BINDING AFFINITY; CELL DIVISION; CRYSTAL STRUCTURE; LIGAND BINDING; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN POLYMERIZATION;

ANTHRANILIC ACIDS; BACTERIAL PROTEINS; BINDING SITES; BINDING, COMPETITIVE; CELL DIVISION; CRYSTALLOGRAPHY, X-RAY; CYTOSKELETAL PROTEINS; GUANOSINE TRIPHOSPHATE; METHANOCOCCUS; MOLECULAR DYNAMICS SIMULATION; PSEUDOMONAS AERUGINOSA; REPRODUCIBILITY OF RESULTS;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 78650089200     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101577p     Document Type: Article

References (61)

1. Bi, E. and Lutkenhaus, J. (1991) FtsZ ring structure associated with division in Escherichia coli Nature 354, 161-164
2. Ma, X. L., Ehrhardt, D. W., and Margolin, W. (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. U.S.A. 93, 12998-13003
3. Hale, C. A. and deBoer, P. A. J. (1997) Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli Cell 88, 175-185
4. Pichoff, S. and Lutkenhaus, J. (2005) Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA Mol. Microbiol. 55, 1722-1734
5. Osawa, M., Anderson, D. E., and Erickson, H. P. (2008) Reconstitution of contractile FtsZ rings in liposomes Science 320, 792-794
6. Löwe, J. and Amos, L. A. (1998) Crystal structure of the bacterial cell-division protein FtsZ Nature 391, 203-206 (Pubitemid 28092483)
7. Nogales, E., Wolf, S. G., and Downing, K. H. (1998) Structure of the alpha beta tubulin dimer by electron crystallography Nature 393, 191-191
8. Erickson, H. P. (2007) Evolution of the cytoskeleton BioEssays 29, 668-677
9. Nogales, E., Downing, K. H., Amos, L. A., and Löwe, J. (1998) Tubulin and FtsZ form a distinct family of GTPases Nat. Struct. Biol. 5, 451-458
10. Oliva, M. A., Cordell, S. C., and Löwe, J. (2004) Structural insights into FtsZ protofilament formation Nat. Struct. Mol. Biol. 11, 1243-1250
11. Scheffers, D. J., de Wit, J. G., den Blaauwen, T., and Driessen, A. J. M. (2002) GTP hydrolysis of cell division protein FtsZ: Evidence that the active site is formed by the association of monomers Biochemistry 41, 521-529
12. Huecas, S., Schaffner-Barbero, C., Garcia, W., Yebenes, H., Palacios, J. M., Diaz, J. F., Menendez, M., and Andreu, J. M. (2007) The interactions of cell division protein FtsZ with guanine nucleotides J. Biol. Chem. 282, 37515-37528
13. Chen, Y. D. and Erickson, H. P. (2009) FtsZ filament dynamics at steady state: Subunit exchange with and without nucleotide hydrolysis Biochemistry 48, 6664-6673
14. 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
15. Dajkovic, A., Mukherjee, A., and Lutkenhaus, J. (2008) Investigation of regulation of FtsZ assembly by SulA and development of a model for FtsZ polymerization J. Bacteriol. 190, 2513-2526
16. Miraldi, E. R., Thomas, P. J., and Romberg, L. (2008) Allosteric models for cooperative polymerization of linear polymers Biophys. J. 95, 2470-2486
17. Martin-Galiano, A. J., Buey, R. M., Cabezas, M., and Andreu, J. M. (2010) Mapping flexibility and the assembly switch of cell division protein FtsZ by computational and mutational approaches J. Biol. Chem. 285, 22554-22565
18. Vollmer, W. (2006) The prokaryotic cytoskeleton: A putative target for inhibitors and antibiotics? Appl. Microbiol. Biotechnol. 73, 37-47
19. Lock, R. L. and Harry, E. J. (2008) Cell-division inhibitors: New insights for future antibiotics Nat. Rev. Drug Discov. 7, 324-338
20. Margalit, D. N., Romberg, L., Mets, R. B., Hebert, A. M., Mitchison, T. J., Kirschner, M. W., and RayChaudhuri, D. (2004) Targeting cell division: Small-molecule inhibitors of FtsZ GTPase perturb cytokinetic ring assembly and induce bacterial lethality Proc. Natl. Acad. Sci. U.S.A. 101, 13969-13969
21. Beuria, T. K., Santra, M. K., and Panda, D. (2005) Sanguinarine blocks cytokinesis in bacteria by inhibiting FtsZ assembly and bundling Biochemistry 44, 16584-16593
22. Domadia, P., Swarup, S., Bhunia, A., Sivaraman, J., and Dasgupta, D. (2007) Inhibition of bacterial cell division protein FtsZ by cinnamaldehyde Biochem. Pharmacol. 74, 831-840
23. Jaiswal, R., Beuria, T. K., Mohan, R., Mahajan, S. K., and Panda, D. (2007) Totarol inhibits bacterial cytokinesis by perturbing the assembly dynamics of FtsZ Biochemistry 46, 4211-4220
24. Haydon, D. J., Stokes, N. R., Ure, R., Galbraith, G., Bennett, J. M., Brown, D. R., Baker, P. J., Barynin, V. V., Rice, D. W., Sedelnikova, S. E., Heal, J. R., Sheridan, J. M., Aiwale, S. T., Chauhan, P. K., Srivastava, A., Taneja, A., Collins, I., Errington, J., and Czaplewski, L. G. (2008) An inhibitor of FtsZ with potent and selective anti-staphylococcal activity Science 321, 1673-1675
25. Andreu, J. M., Schaffner-Barbero, C., Huecas, S., Alonso, D., Lopez-Rodriguez, M. L., Ruiz-Avila, L. B., Nunez-Ramirez, R., Llorca, O., and Martin-Galiano, A. J. (2010) The antibacterial cell division inhibitor PC190723 is a FtsZ polymer stabilizing agent which induces filament assembly and condensation J. Biol. Chem. 285, 14239-14246
26. Läppchen, T., Pinas, V. A., Hartog, A. F., Koomen, G. J., Schaffner-Barbero, C., Andreu, J. M., Trambaiolo, D., Löwe, J., Juhem, A., Popov, A. V., and den Blaauwen, T. (2008) Probing FtsZ and tubulin with C8-substituted GTP analogs reveals differences in their nucleotide binding sites Chem. Biol. 15, 189-199
27. 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
28. Vollmer, W. (2008) Targeting the bacterial Z-ring Chem. Biol. 15, 93-94
29. Gordon, J. C., Myers, J. B., Folta, T., Shoja, V., Heath, L. S., and Onufriev, A. (2005) H++: A server for estimating pKas and adding missing hydrogens to macromolecules Nucleic Acids Res. 33, W368-W371
30. Honig, B. and Nicholls, A. (1995) Classical electrostatics in biology and chemistry Science 268, 1144-1149
31. Wang, J. M., Cieplak, P., and Kollman, P. A. (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 21, 1049-1074
32. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926-935
33. Case, D. A., Darden, T. A., Cheatham, T. E., Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Crowley, M., Walker, R. C., Zhang, W., Merz, K. M., Wang, B., Hayik, S., Roitberg, A., Seabra, G., Kolossváry, I., Wong, K. F., Paesani, F., Vanicek, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Yang, L., Tan, C., Mongan, J., Hornak, V., Cui, G., Mathews, D. H., Seetin, M. G., Sagui, C., Babin, V., and Kollman, P. A. (2008) AMBER 10, University of California, San Francisco.
34. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual molecular dynamics J. Mol. Graphics 14 (33-38) 27-38
35. Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S. H., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., Donini, O., Cieplak, P., Srinivasan, J., Case, D. A., and Cheatham, T. E. (2000) Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models Acc. Chem. Res. 33, 889-897
36. Karplus, M. and Kushick, J. (1981) Method for estimating the configurational entropy of macromolecules Macromolecules 14, 325-332
37. Schlitter, J. (1993) Estimation of absolute and relative entropies of macromolecules using the covariance matrix Chem. Phys. Lett. 215, 617-621
38. Gil-Redondo, R., Estrada, J., Morreale, A., Herranz, F., Sancho, J., and Ortiz, A. R. (2009) VSDMIP: Virtual screening data management on an integrated platform J. Comput.-Aided Mol. Des. 23, 171-184
39. Ruiz, F. M., Gil-Redondo, R., Morreale, A., Ortiz, A. R., Fabrega, C., and Bravo, J. (2008) Structure-based discovery of novel non-nucleosidic DNA alkyltransferase inhibitors: Virtual screening and in vitro and in vivo activities J. Chem. Inf. Model. 48, 844-854
40. Kuntz, I. D., Blaney, J. M., Oatley, S. J., Langridge, R., and Ferrin, T. E. (1982) A geometric approach to macromolecule-ligand interactions J. Mol. Biol. 161, 269-288
41. Perez, C. and Ortiz, A. R. (2001) Evaluation of docking functions for protein-ligand docking J. Med. Chem. 44, 3768-3785
42. Lipinski, C. A., Lombardo, F., Dominy, B. W., and Feeney, P. J. (1997) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings Adv. Drug Delivery Rev. 23, 3-25
43. Irwin, J. J. and Shoichet, B. K. (2005) ZINC-A free database of commercially available compounds for virtual screening J. Chem. Inf. Model. 45, 177-182
44. Wang, K., Murcia, M., Constans, P., Perez, C., and Ortiz, A. R. (2004) Gaussian mapping of chemical fragments in ligand binding sites J. Comput.-Aided Mol. Des. 18, 101-118
45. Huecas, S. and Andreu, J. M. (2004) Polymerization of nucleotide-free, GDP- and GTP-bound cell division protein FtsZ: GDP makes the difference FEBS Lett. 569, 43-48
46. Diaz, J. F. and Buey, R. M. (2007) Characterizing ligand-microtubule binding by competition methods Methods Mol. Med. 137, 245-260
47. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, 2 nd ed., Kluwer Academic/Plenum Publishers, New York.
48. Andreu, J. M. and Barasoain, I. (2001) The interaction of baccatin III with the taxol binding site of microtubules determined by a homogeneous assay with fluorescent taxoid Biochemistry 40, 11975-11984
49. Huecas, S. and Andreu, J. M. (2003) Energetics of the cooperative assembly of cell division protein FtsZ and the nucleotide hydrolysis switch J. Biol. Chem. 278, 46146-46154
50. Andreu, J. M. and Timasheff, S. N. (1982) Interaction of tubulin with single ring analogs of colchicine Biochemistry 21, 534-543
51. Fersht, A. R. (1987) The hydrogen-bond in molecular recognition Trends Biochem. Sci. 12, 301-304
52. Buey, R. M., Diaz, J. F., Andreu, J. M., O'Brate, A., Giannakakou, P., Nicolaou, K. C., Sasmal, P. K., Ritzen, A., and Namoto, K. (2004) Interaction of epothilone analogs with the paclitaxel binding site: Relationship between binding affinity, microtubule stabilization, and cytotoxicity Chem. Biol. 11, 225-236
53. Devoe, H. and Wasik, S. P. (1984) Aqueous solubilities and enthalpies of solution of adenine and guanine J. Solution Chem. 13, 51-60
54. Oliva, M. A., Trambaiolo, D., and Löwe, J. (2007) Structural insights into the conformational variability of FtsZ J. Mol. Biol. 373, 1229-1242
55. Jorgensen, W. L. and Duffy, E. M. (2002) Prediction of drug solubility from structure Adv. Drug Delivery Revs. 54, 355-366
56. Stokes, N. R., Sievers, J., Barker, S., Bennett, J. M., Brown, D. R., Collins, I., Errington, V. M., Foulger, D., Hall, M., Halsey, R., Johnson, H., Rose, V., Thomaides, H. B., Haydon, D. J., Czaplewski, L. G., and Errington, J. (2005) Novel inhibitors of bacterial cytokinesis identified by a cell-based antibiotic screening assay J. Biol. Chem. 280, 39709-39715
57. Plaza, A., Keffer, J. L., Bifulco, G., Lloyd, J. R., and Bewley, C. A. (2010) Chrysophaentins A-H, antibacterial bisdiarylbutene macrocycles that inhibit the bacterial cell division protein FtsZ J. Am. Chem. Soc. 132, 9069-9077
58. Hritz, J., Läppchen, T., and Oostenbrink, C. (2010) Calculations of binding affinity between C8-substituted GTP analogs and the bacterial cell-division protein FtsZ, Eur. Biophys. J. 39, 1573 - 1580.
59. 2+ dependence of guanine-nucleotide binding to tubulin J. Biol. Chem. 262, 17278-17284
60. Kong, C. G., Ito, K., Walsh, M. A., Wada, M., Liu, Y. Y., Kumar, S., Barford, D., Nakamura, Y., and Song, H. W. (2004) Crystal structure and functional analysis of the eukaryotic class II release factor eRF3 from S. pombe Mol. Cell 14, 233-245
61. Sprang, S. R. (1997) G protein mechanisms: Insights from structural analysis Annu. Rev. Biochem. 66, 639-678