Identification of a new class of FtsZ inhibitors by structure-based design and in vitro screening

Journal of Chemical Information and Modeling

Volumn 53, Issue 8, 2013, Pages 2131-2140

  Chan, Fung Yi ^a,b   Sun, Ning ^a   Neves, Marco A C ^b   Lam, Polo Chun Hung ^c   Chung, Wai Hong ^a   Wong, Lai King ^a   Chow, Ho Yin ^a   Ma, Dik Lung ^a   Chan, Pak Ho ^a   Leung, Yun Chung ^a   Chan, Tak Hang ^a   Abagyan, Ruben ^b,c   Wong, Kwok Yin ^a  

^a HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MOLSOFT LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; ESCHERICHIA COLI;

ANTI-BACTERIAL ACTIVITY; BACTERIAL CELL DIVISION; BIOLOGICAL EVALUATION; GRAM-NEGATIVE BACTERIA; NATURAL PRODUCT LIBRARIES; STRUCTURE ACTIVITY RELATIONSHIPS; STRUCTURE-BASED DESIGNS; TEMPERATURE SENSITIVE;

DIGITAL LIBRARIES;

ANTIINFECTIVE AGENT; ENZYME INHIBITOR; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; PYRIMIDINE; PYRIMIDINE DERIVATIVE; QUINUCLIDINE DERIVATIVE; TUBULIN;

ANIMAL; ANTAGONISTS AND INHIBITORS; BINDING SITE; BOVINAE; CHEMISTRY; DRUG DESIGN; DRUG EFFECTS; DRUG SCREENING; ENZYMOLOGY; ESCHERICHIA COLI; HUMAN; METABOLISM; MOLECULAR DOCKING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; SEQUENCE HOMOLOGY; STAPHYLOCOCCUS AUREUS; STRUCTURE ACTIVITY RELATION; ARTICLE; CATTLE; DRUG ANTAGONISM; DRUG EFFECT;

ANIMALS; ANTI-BACTERIAL AGENTS; BINDING SITES; CATTLE; DRUG DESIGN; DRUG EVALUATION, PRECLINICAL; ENZYME INHIBITORS; ESCHERICHIA COLI; GTP PHOSPHOHYDROLASES; GUANOSINE TRIPHOSPHATE; HUMANS; MOLECULAR DOCKING SIMULATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PYRIMIDINES; QUINUCLIDINES; SEQUENCE HOMOLOGY, AMINO ACID; STAPHYLOCOCCUS AUREUS; STRUCTURE-ACTIVITY RELATIONSHIP; TUBULIN;

EID: 84883241483     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci400203f     Document Type: Article

References (53)

1. Levy, S. B.; Marshall, B. Antibacterial resistance worldwide: causes, challenges and responses Nat. Med. 2004, 10, S122-S129
2. Rasko, D. A.; Sperandio, V. Anti-virulence strategies to combat bacteria-mediated disease Nat. Rev. Drug Discovery 2010, 9, 117-128
3. Klevens, R. M.; Morrison, M. A.; Nadle, J.; Petit, S.; Gershman, K.; Ray, S.; Harrison, L. H.; Lynfield, R.; Dumyati, G.; Townes, J. M.; Craig, A. S.; Zell, E. R.; Fosheim, G. E.; McDougal, L. K.; Carey, R. B.; Fridkin, S. K. Invasive methicillin-resistant Staphylococcus aureus infections in the United States J. Am. Med. Assoc. 2007, 298, 1763-1771
4. Acar, J. F. Consequences of bacterial resistance to antibiotics in medical practice Clin. Infect. Dis. 1997, 24, S17-S18
5. Erickson, H. P. FtsZ, a prokaryotic homolog of tubulin Cell 1995, 80, 367-370
6. Addinall, S. G.; Holland, B. The tubulin ancester, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis J. Mol. Biol. 2002, 318, 219-236
7. Erickson, H. P. FtsZ, a tubulin homologue in prokaryote cell division Trends Cell Biol. 1997, 7, 362-367
8. Margolin, W. Themes and variations in prokaryotic cell division FEMS Microbiol. Rev. 2000, 24, 531-548
9. Bi, E.; Lutkenhaus, J. FtsZ ring structure associated with division in Escherichia coli Nature 1991, 354, 161-164
10. Oliva, M. A.; Cordell, S. C.; Lowe, J. Structural insights into FtsZ protofilament formation Nat. Struct. Mol. Biol. 2004, 11, 1243-1250
11. Adams, D. W.; Errington, J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring Nat. Rev. Microbiol. 2009, 7, 642-653
12. Margolin, W. FtsZ and the division of prokaryotic cells and organelles Nat. Rev. Mol. Cell Biol. 2005, 6, 862-871
13. Payne, D. J.; Gwynn, M. N.; Holmes, D. J.; Pompliano, D. L. Drugs for bad bugs: confronting the challenges of antibacterial discovery Nat. Rev. Drug Discovery 2007, 6, 29-40
14. Lock, R. L.; Harry, E. J. Cell-division inhibitors: new insights for future antibiotics Nat. Rev. Drug Discovery 2008, 7, 324-338
15. Li, Z. R.; Garner, A. L.; Gloeckner, C.; Janda, K. D.; Carlow, C. K. Targeting the Wolbachia cell division protein FtsZ as a new approach for antifilarial therapy PLoS Neglected Trop. Dis. 2011, 5, e1411
16. Margalit, D. N.; Romberg, L.; Mets, R. B.; Hebert, A. M.; Mitchison, T. J.; Kirschner, M. W.; RayChaudhuri, D. Targeting cell division: small-molecule inhibitors of FtsZ GTPase perturb cytokinetic ring assembly and induce bacterial lethality Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 11821-11826
17. Urgaonkar, S.; La Pierre, H. S.; Meir, I.; Lund, H.; RayChaudhuri, D.; Shaw, J. T. Synthesis of antimicrobial natural products targeting FtsZ: (±)-dichamanetin and (±)-2-hydroxy-5″- benzylisouvarinol-B Org. Lett. 2005, 7, 5609-5612
18. Beuria, T. K.; Santra, M. K.; Panda, D. Sanguinarine blocks cytokinesis in bacteria by inhibiting FtsZ assembly and bundling Biochemistry 2005, 44, 16584-16593
19. 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.; Errington, J. Novel inhibitors of bacterial cytokinesis identified by a cell-based antibiotic screening assay J. Biol. Chem. 2005, 280, 39709-39715
20. Domadia, P.; Swarup, S.; Bhunia, A.; Sivaraman, J.; Dasgupta, D. Inhibition of bacterial cell division protein FtsZ by cinnamaldehyde Biochem. Pharmacol. 2007, 74, 831-840
21. Jaiswal, R.; Beuria, T. K.; Mohan, R.; Mahajan, S. K.; Panda, D. Totarol inhibits bacterial cytokinesis by perturbing the assembly dynamics of FtsZ Biochemistry 2007, 46, 4211-4220
22. Plaza, A.; Keffer, J. L.; Bifulco, G.; Lloyd, J. R.; Bewley, C. A. Chrysophaentins A-H, antibacterial bisdiarylbutene macrocycles that inhibit the bacterial cell division protein FtsZ J. Am. Chem. Soc. 2010, 132, 9069-9077
23. 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. An inhibitor of FtsZ with potent and selective anti-staphylococcal activity Science 2008, 321, 1673-1675
24. Tan, C. M.; Therien, A. G.; Lu, J.; Lee, S. H.; Caron, A.; Gill, C. J.; Lebeau-Jacob, C.; Benton-Perdomo, L.; Monteiro, J. M.; Pereira, P. M.; Elsen, N. L.; Wu, J.; Deschamps, K.; Petcu, M.; Wong, S.; Daigneault, E.; Kramer, S.; Liang, L.; Maxwell, E.; Claveau, D.; Vaillancourt, J.; Skorey, K.; Tam, J.; Wang, H.; Meredith, T. C.; Sillaots, S.; Wang-Jarantow, L.; Ramtohul, Y.; Langlois, E.; Landry, F.; Reid, J. C.; Parthasarathy, G.; Sharma, S.; Baryshnikova, A.; Lumb, K. J.; Pinho, M. G.; Soisson, S. M.; Roemer, T. Restoring methicillin-resistant Staphylococcus aureus susceptibility to β-lactam antibiotics Sci. Transl. Med. 2012, 4, 126ra35
25. Jorgensen, W. L. The many roles of computation in drug discovery Science 2004, 303, 1813-1818
26. Bajorath, F. Integration of virtual and high-throughput screening Nat. Rev. Drug Discovery 2002, 1, 882-894
27. Simmons, K. J.; Chopra, I.; Fishwick, C. W. G. Structure-based discovery of antibacterial drugs Nat. Rev. Microbiol. 2010, 8, 501-510
28. Rollinger, J. M.; Stuppner, H.; Langer, T. Virtual screening for the discovery of bioactive natural products. In Natural Compounds as Drugs, Vol 1; Petersen, F.; Amstutz, R., Eds.; 2008; Vol. 65, pp 211-249.
29. Newman, D. J.; Cragg, G. M. Natural products as sources of new drugs over the last 25 years J. Nat. Prod. 2007, 70, 461-477
30. Harvey, A. L. Natural products in drug discovery Drug Discovery Today 2008, 13, 894-901
31. Oliva, M. A.; Trambaiolo, D.; Loewe, J. Structural insights into the conformational variability of FtsZ J. Mol. Biol. 2007, 373, 1229-1242
32. Neves, M. A. C.; Totrov, M.; Abagyan, R. Docking and scoring with ICM: the benchmarking results and strategies for improvement J. Comput.-Aided Mol. Des. 2012, 26, 675-686
33. Halgren, T. A. Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94 J. Comput. Chem. 1996, 17, 490-519
34. An, J. H.; Totrov, M.; Abagyan, R. Pocketome via comprehensive identification and classification of ligand binding envelopes Mol. Cell. Proteomics 2005, 4, 752-761
35. Bottegoni, G.; Kufareva, I.; Totrov, M.; Abagyan, R. A new method for ligand docking to flexible receptors by dual alanine scanning and refinement (SCARE) J. Comput.-Aided Mol. Des. 2008, 22, 311-325
36. Abagyan, R. A.; Batalov, S. Do aligned sequences share the same fold? J. Mol. Biol. 1997, 273, 355-368
37. Domadia, P. N.; Bhunia, A.; Sivaraman, J.; Swarup, S.; Dasgupta, D. Berberine targets assembly of Escherichia coli cell division protein FtsZ Biochemistry 2008, 47, 3225-3234
38. Yongye, A. B.; Waddell, J.; Medina-Franco, J. L. Molecular scaffold analysis of natural products databases in the public domain Chem. Biol. Drug Des. 2012, 80, 717-724
39. Ganesan, A. The impact of natural products upon modern drug discovery Curr. Opin. Chem. Biol. 2008, 12, 306-317
40. Abagyan, R.; Totrov, M. Biased probability Monte Carlo conformational searches and electrostatic calculations for peptides and proteins J. Mol. Biol. 1994, 235, 983-1002
41. Schapira, M.; Abagyan, R.; Totrov, M. Nuclear hormone receptor targeted virtual screening J. Med. Chem. 2003, 46, 3045-3059
42. Rueda, M.; Totrov, M.; Abagyan, R. ALiBERO: evolving a team of complementary pocket conformations rather than a single leader J. Chem. Inf. Model. 2012, 52, 2705-2714
43. Bohm, H. J.; Banner, D.; Bendels, S.; Kansy, M.; Kuhn, B.; Muller, K.; Obst-Sander, U.; Stahl, M. Fluorine in medicinal chemistry ChemBioChem 2004, 5, 637-643
44. Smith, E. C.; Kaatz, G. W.; Seo, S. M.; Wareham, N.; Williamson, E. M.; Gibbons, S. The phenolic diterpene totarol inhibits multidrug efflux pump activity in Staphylococcus aureus Antimicrob. Agents Chemother. 2007, 51, 4480-4483
45. Haraguchi, H.; Oike, S.; Muroi, H.; Kubo, I. Mode of antibacterial action of totarol, a diterpene from Podocarpus nagi Planta Med. 1996, 62, 122-125
46. Foss, M. H.; Eun, Y. J.; Grove, C. I.; Pauw, D. A.; Sorto, N. A.; Rensvold, J. W.; Pagliarini, D. J.; Shaw, J. T.; Weibel, D. B. Inhibitors of bacterial tubulin target bacterial membranes MedChemComm 2013, 4, 112-119
47. Stahl, M. Modifications of the scoring function in FlexX for virtual screening applications Perspect. Drug Discovery Des. 2000, 20, 83-98
48. Lin, C. M.; Hamel, E. Effects of inhibitors of tubulin polymerization on GTP hydrolysis J. Biol. Chem. 1981, 256, 9242-9245
49. Mayer, M.; Meyer, B. Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor J. Am. Chem. Soc. 2001, 123, 6108-6117
50. Scheffers, D. J.; den Blaauwen, T.; Driessen, A. J. Non-hydrolysable GTP-gamma-S stabilizes the FtsZ polymer in a GDP-bound state Mol. Microbiol. 2000, 35, 1211-1219
51. Urbina, J. A.; Concepcion, J. L.; Caldera, A.; Payares, G.; Sanoja, C.; Otomo, T.; Hiyoshi, H. In vitro and in vivo activities of E5700 and ER-119884, two novel orally active squalene synthase inhibitors, against Trypanosoma cruzi Antimicrob. Agents Chemother. 2004, 48, 2379-2387
52. 7 nicotinic acetylcholine receptor agonist in humans Drug Metab. Dispos. 2007, 35, 1188-1195
53. Bucher, C.; Sparr, C.; Schweizer, W. B.; Gilmour, R. Fluorinated quinine alkaloids: synthesis, X-ray structure analysis and antimalarial parasite chemotherapy Chem.-Eur. J. 2009, 15, 7637-7647