Molecular modelling of FtsZ proteins based on their homology in Escherichia coli and Mycobacterium tuberculosis as the key stage of rational design of new antituberculous compounds

Authors

  • Oleh Demchuk
  • Pavel Karpov
  • Peter Raspor
  • Yaroslav Blume

DOI:

https://doi.org/10.14720/abs.54.2.15476

Keywords:

FtsZ, Escherichia coli, Mycobacterium tuberculosis, 3D-structure modelling and verification, in silico

Abstract

The analysis of the quality of X-ray structures from Mycobacterium tuberculosis FtsZ proteins, which are deposited in the ProteinDataBank, gave a possibility to select a 2Q1Y (Chain A) structure as a template for future in silico research. Also several spatial models of FtsZ protein from Escherichia coli were reconstructed with on-line servers »Swiss-Model Workspace« and I-Tasser, than the most appropriate structure was selected. Basing on complex bioinformatic study, the model, which was rebuilt by SwissModel server from 2Q1Y (chain A) template, was supposed as the most significant.

References

Arnold, K., Bordoli, L., Kopp, J., Schwede, T., 2006. The »SWISS-MODEL Workspace«: A web-based environment for protein structure homology modelling. Bioinformatics, 22, 195–201. DOI: https://doi.org/10.1093/bioinformatics/bti770

Benkert, P., Biasini, M., Schwede, T., 2011. Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics, 27, (3), 343–350. DOI: https://doi.org/10.1093/bioinformatics/btq662

Benkert, P., Schwede, T., Tosatto, S.C.E., 2009. QMEANclust: Estimation of protein model quality bycombining a composite scoring function with structural density information. BMC Struct. Biol., 9 (35), doi:10.1186/1472-6807-9-35. DOI: https://doi.org/10.1186/1472-6807-9-35

Berman, H.M., Henrick, K., Nakamura, H., 2003. Announcing the worldwide Protein Data Bank. Nat. Struct. Biol., 10 (12), p. 980. DOI: https://doi.org/10.1038/nsb1203-980

Chen, V.B., Arendall, W.B. III, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S., Richardson, D.C., 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D: Biol. Crystallogr., D66 (1), 12–21. DOI: https://doi.org/10.1107/S0907444909042073

Cole, S.T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C.M., Harris, D.E., Gordon, S.V., Eiglmeier, K., Gas, S., Barry, C.E. III, Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R.M., Devlin, K., Barrell, B.G., 1998. Deciphering the biology of M. tuberculosis from the complete genome sequence, Nature, 393, 537–544. DOI: https://doi.org/10.1038/31159

Cordell, S.C., Robinson, E.J.H., Löwe, J., 2003. Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc. Natl. Acad. Sci. USA, 100 (13), 7889–7894. DOI: https://doi.org/10.1073/pnas.1330742100

Demchuk, O.N., Blume, Ya.B., 2005. Phylogenetic tree of bacterial and eucaryotic FtsZ-proteins created according to the homology of their primary sequences, Cytol. Genetics, 39 (4), 3–12.

Erickson, H.P., 1998. Atomic structures of tubulin and FtsZ, Trends Cell Biol., 8, 133–137. DOI: https://doi.org/10.1016/S0962-8924(98)01237-9

Fleischmann, R.D., Alland, D., Eisen, J.A., Carpenter, L., White, O., Peterson, J.D., DeBoy, R.T., Dodson, R.J., Gwinn, M.L., Haft, D.H., Hickey, E.K., Kolonay, J.F., Nelson, W.C., Umayam, L.A., Ermolaeva, M.D., Salzberg, S.L., Delcher, A., Utterback, T.R., Fraser, C.M., 2002. Whole-genome

comparison of M. tuberculosis clinical and laboratory strains. J. Bacteriol., 184, 5479–5490.

Gu, J., Bourne, P.E., 2009. Structural Bioinformatics, 2nd ed. John Wiley and Sons, New Jersey, 1035 pр. Guex, N., Peitsch, M.C., 1997. SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modelling. Electrophoresis, 18 (15), 2714–2723. DOI: https://doi.org/10.1002/elps.1150181505

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., Czaplewski, L.G., 2008. An inhibitor of FtsZ

with potent and selective anti-staphylococcal activity. Science, 321, 1673–1675. DOI: https://doi.org/10.1126/science.1159961

Höltje, H.-D., Sippl, W., Rognan, D., Folkers, G., 2008. Molecular modeling. Basic Principles and Applications, 3rd Ed.. Wiley-VCH, p. 320,

Huang, Q., Kirikae, F., Kirikae, T., Pepe, A., Slayden, R.A., Tonge, P.J., Ojima, I., 2006. Targeting FtsZ for anti-tuberculosis drug discovery: non-cytotoxic taxanes as novel anti-tuberculosis agents. J. Med. Chem., 49 (2), 463–466. DOI: https://doi.org/10.1021/jm050920y

Jaiswal, R., Beuria, T.K., Mohan, R., Mahajan, S.K., Panda, D., 2007. Totarol inhibits bacterial cytokinesis by perturbing the assembly dynamics of FtsZ. Biochem., 46 (14), 4211–4220. DOI: https://doi.org/10.1021/bi602573e

Kumar, K., Awasthi, D., Berger, W.T., Tonge, P.J., Slayden, R.A., Ojima, I., 2010. Discovery of anti-TB agents that target the cell-division protein FtsZ. Future Med Chem., 2 (8), 1305–1323. DOI: https://doi.org/10.4155/fmc.10.220

Kumar, K., Awasthi, D., Lee, S-Y., Zanardi, I., Ruzsicska, B., Knudson, S., Tonge, P.J., Slayden, R.A., Ojima, I., 2011.Novel trisubstituted benzimidazoles, targeting Mtb FtsZ, as a new class of antitubercular agents. J. Med. Chem., 54, 374–381. DOI: https://doi.org/10.1021/jm1012006

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., den Blaauwen, T., 2008. Probing FtsZ and tubulin with C8-substituted GTP analogs reveals differences in their nucleotide binding sites. Chem. DOI: https://doi.org/10.1016/j.chembiol.2007.12.013

Biol., 15, 189–199.

Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G., 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948. DOI: https://doi.org/10.1093/bioinformatics/btm404

Leung, A.K., Lucile White, E., Ross, L.J., Reynolds, R.C., DeVito, J.A., Borhani, D.W., 2004. Structure of M. tuberculosis FtsZ reveals unexpected, G protein-like conformational switches. J. Mol. Biol., 342 (3), 953–970. DOI: https://doi.org/10.1016/j.jmb.2004.07.061

Li, Y., Zhang, Y., 2009. REMO: A new protocol to refine full atomic protein models from C-alpha traces by optimizing hydrogen-bonding networks. Proteins, 76, 665–676. DOI: https://doi.org/10.1002/prot.22380

Löwe, J., Amos, L.A., 1998. Crystal structure of the bacterial cell-division protein FtsZ. Nature, 391, 203–206. DOI: https://doi.org/10.1038/34472

Margalit, D.N., Romberg, L., Mets, R.B., Hebert, A.M., Mitchison, T.J., Kirschner, M.W., Chaudhuri, D.R., 2004. Targeting cell division: small-molecule inhibitors of FtsZ GTPase perturb cytokinetic ring assembly and induce bacterial lethality. PNAS., 101, 11821–11826. DOI: https://doi.org/10.1073/pnas.0404439101

Mosyak, L., Zhang, Y., Glasfeld, E., Haney, S., Stahl, M., Seehra, J., Somers, W.S., 2000. The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J., 19 (13), 3179–3191. DOI: https://doi.org/10.1093/emboj/19.13.3179

Nyporko, A.Yu., Blume, Ya.B., 2001. Comparative analysis of the tubulin secondary structure. Biopolym. Сell, 17, (1), 61–69, in Russian. DOI: https://doi.org/10.7124/bc.00059E

Ohashi, Y., Chijiiwa, Y., Suzuki, K., Takahashi, K., Nanamiya, H., Sato, T., Hosoya, Y., Ochi, K., Kawamura, F., 1999. The lethal effect of a benzamide derivative, 3-methoxybenzamide, can be suppressed by mutations within a cell division gene, ftsZ, in Bacillus subtilis. J. Bacteriol., 181 (4), 1348–1351. DOI: https://doi.org/10.1128/JB.181.4.1348-1351.1999

Oliva, M.A., Cordell, S.C., Löwe, J., 2004. Structural insights into FtsZ protofilament formation, Nat. Struct. Mol. Biol., 11 (12), 1243–1250. DOI: https://doi.org/10.1038/nsmb855

Oliva, M.A., Trambaiolo, D., Löwe, J., 2007. Structural insights into the conformational variability of FtsZ. J. Mol. Biol., 373 (5), 1229–1242. DOI: https://doi.org/10.1016/j.jmb.2007.08.056

Perna, N.T., Plunkett 3rd, G., Burland, V., Mau, B., Glasner, J.D., Rose, D.J., Mayhew, G.F., Evans, P.S., Gregor, J., Kirkpatrick, H.A., Pósfai, G., Hackett, J., Klink, S., Boutin, A., Shao, Y., Miller, L., Grotbeck, E.J., Davis, N.W., Lim, A., Dimalanta, E.T., Potamousis, K.D., Apodaca, J., Anantharaman, T.S., Lin, J., Yen, G., Schwartz, D.C., Welch, R.A., Blattner, F.R., 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7, Nature, 409 (6819), 529–533. DOI: https://doi.org/10.1038/35054089

Raymond, A., Lovell, S., Lorimer, D., Walchli, J., Mixon, M., Wallace, E., Thompkins, K., Archer, K., Burgin, A., Stewart, L., 2009. Combined protein construct and synthetic gene engineering for heterologous protein expression and crystallization using Gene Composer, BMC Biotechnol., 9

(37), doi: 10.1186/1472-6750-9-37. DOI: https://doi.org/10.1186/1472-6750-9-37

Raviglione, M.C., 2000. Issues facing TB control (7). Multiple drug-resistant tuberculosis, Scott. Med. J., 45, (5), 52–55. DOI: https://doi.org/10.1177/00369330000450S124

Respicio, L., Nair, P.A., Huang, Q., Anil, B., Tracz, S., Truglio, J.J., Kisker, C., Raleigh, D.P., Ojima, I., Knudson, D.L., Identification of FtsZ polymerization regulatory elements using a M. tuberculosis FtsZ temperature sensitive mutant. To be published, DOI:10.2210/pdb2q1y/pdb DOI: https://doi.org/10.2210/pdb2q1y/pdb

Roy, A., Kucukural, A., Zhang, Y. 2010. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc., 5 (4), 725–738. DOI: https://doi.org/10.1038/nprot.2010.5

Roy, A., Zhang, Y., 2011 COFACTOR: protein-ligand binding site predictions by global structure similarity match and local geometry refinement, – in print. The UniProt Consortium, 2008. The Universal Protein Resource (UniProt). Nucl Acids Res., 36, 190–195. DOI: https://doi.org/10.1093/nar/gkm895

Vaughan, S., Wickstead, B., Gull, K., Addinall, S.G., 2004. Molecular evolution of FtsZ protein sequences encoded within the genomes of archaea, bacteria, and eukaryote. J. Mol. Evol., 58 (1), 19–39. DOI: https://doi.org/10.1007/s00239-003-2523-5

White, E.L., Ross, L.J., Reynolds, R.C., Seitz, L.E., Moore, G.D., Borhani, D.W., 2000. Slow polymerization of M. tuberculosis FtsZ. J. Bacteriol., 182 (14), 4028–4034. DOI: https://doi.org/10.1128/JB.182.14.4028-4034.2000

White, E.L., Suling, W.J., Ross, L.J., Seitz, L.E., Reynolds, R.C., 2002. 2-alkoxycarbonylaminopyridines: inhibitors of M. tuberculosis FtsZ. J. Antimicrob Chemother., 50 (1), 111–114. DOI: https://doi.org/10.1093/jac/dkf075

Wu, S., Zhang, Y., 2007. LOMETS: a local meta-threading-server for protein structure prediction. Nucleic Acids Res., 35, 3375–3382. DOI: https://doi.org/10.1093/nar/gkm251

Yu, X.-C., Margolin, W., 1998. Inhibition of assembly of bacterial cell division protein FtsZ by the hydrophobic dye 5,5*-Bis-(8-anilino-1-aphthalenesulfonate). J. Biol. Chem., 273 (17), 10216–10222. DOI: https://doi.org/10.1074/jbc.273.17.10216

Zhang, J., Zhang, Y., 2011. High-resolution protein structure refinement using fragment guided molecular dynamics simulations. Structure, in press. Zhang, Y., Kihara, D., Skolnick, J., 2002. Local energy landscape flattening: parallel hyperbolic Monte Carlo sampling of protein folding. Proteins, 48, 192–201. DOI: https://doi.org/10.1002/prot.10141

Zhang, Y., Skolnick, J., 2004. Scoring function for automated assessment of protein structure template quality. Proteins, 57 (4), 702–710. DOI: https://doi.org/10.1002/prot.20264

Zhou, H., Zhou, Y., 2002. Distance-scaled, finite ideal-gas reference state improves structurederived potentials of mean force for structure selection and stability prediction. Protein Sci., 11, 2714–2726. DOI: https://doi.org/10.1110/ps.0217002

Downloads

Published

01.12.2011

Issue

Section

Original Research Paper

How to Cite

Demchuk, O., Karpov, P., Raspor, P., & Blume, Y. (2011). Molecular modelling of FtsZ proteins based on their homology in Escherichia coli and Mycobacterium tuberculosis as the key stage of rational design of new antituberculous compounds. Acta Biologica Slovenica, 54(2), 15-30. https://doi.org/10.14720/abs.54.2.15476

Similar Articles

1-10 of 41

You may also start an advanced similarity search for this article.

Most read articles by the same author(s)