Structure-based design, synthesis, and biological evaluation of inhibitors of Mycobacterium tuberculosis type II dehydroquinase

Journal of Medicinal Chemistry

Volumn 48, Issue 15, 2005, Pages 4871-4881

  Sánchez Sixto, Cristina ^a   Prazeres, Verónica F V ^a   Castedo, Luis ^a   Lamb, Heather ^b   Hawkins, Alastair R ^b   González Bello, Concepción ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1,3,4 TRIHYDROXYCYCLOHEX 5 EN 1 CARBOXYLIC ACID DERIVATIVE; 3 NITROPHENYL CARBOXYLIC ACID DERIVATIVE; 5 FLUORO 1,3,4 TRIHYDROXYCYCLOHEX 5 EN 1 CARBOXYLIC ACID; ARGININE; BACTERIAL ENZYME; CARBOXYLIC ACID DERIVATIVE; ENZYME INHIBITOR; POLYCYCLIC AROMATIC HYDROCARBON DERIVATIVE; SHIKIMIC ACID; TYPE II DEHYDROQUINASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; COMPETITIVE INHIBITION; COMPUTER PROGRAM; DRUG BINDING; DRUG DESIGN; DRUG SYNTHESIS; ELECTRICITY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; MOLECULAR DOCKING; MYCOBACTERIUM TUBERCULOSIS; STRUCTURE BASED DESIGN; SUZUKI REACTION;

CYCLOHEXANOLS; HYDRO-LYASES; MODELS, MOLECULAR; MYCOBACTERIUM TUBERCULOSIS; PROTEIN BINDING; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 22744449929     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm0501836     Document Type: Article

References (57)

1. Kochi, A. Global challenge of tuberculosis. Lancet 1994, 44, 608.
2. Dye, C.; Scheele, S.; Dolin, P.; Pathania, V.; Raviglione, M. C. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. J. Am. Med. Assoc. 1999, 282, 677.
3. Bloom, B. R.; Small, P. M. The evolving relation between humans and Mycobacterium tuberculosis. N. Engl. J. Med. 1998, 338, 677.
4. (a) Kaufman, S.; Van Embden, J. Tuberculosis: a neglected disease strikes back. Trend. Microbiol. 1993, 1, 2.
5. (b) Bloom, B. R.; Murray, C. J. Tuberculosis: commentary on a reemergent killer. Science 1992, 257, 1055.
6. Fischl, M. A.; Daikos, G. L.; Uttamchandani, R. B.; Poblete, R. B.; Moreno, J. N.; Reyes, R. R.; Boota, A. M.; Thompson, L. M.; Cleary, T. J.; Oldham, S. A. Clinical presentation and outcome of patients with HIV infection and tuberculosis caused by multiple-drug-resistant bacilli. Ann. Intern. Med. 1992, 117, 184.
7. Abell, C. Enzymology and Molecular Biology of the Shikimate Pathway. In Comprehensive Natural Products Chemistry; Sankawa, U., Ed.; Elsevier Science Ltd.: Oxford, 1999; p 573.
8. (a) Roberts, F.; Roberts, C. W.; Johnson, J. J.; Kyle, D. E.; Krell, T.; Coggins, J. R.; Coombs, G. H.; Milhous, W. K.; Tzipori, S.; Ferguson, D. J.; Chakrabarti, D.; McLeod, R. Evidence for the shikimate pathway in apicomplexan parasites. Nature 1998, 393, 801.
9. (b) Campbell, S. A.; Richards, T. A.; Mui, E. J.; Samuel, B. U.; Coggins, J. R.; McLeod, R.; Roberts, C. W. A complete shikimate pathway in Toxoplasma gondii: an ancient eukaryotic innovation. Int. J. Parasitol. 2004, 34, 5.
10. (a) Steinrücken, H. C.; Amhrein, N. The herbicide glyphosate is a potent inhibitor of 5-enolpyruvylshikimic acid 3-phosphate synthase. Biochem. Biophys. Res. Commun. 1980, 94, 1207.
11. (b) Sikorski, J. A.; Gruys, K. J. Understanding glyphosate's molecular mode of action with EPSP synthase: evidence favoring an allosteric inhibitor model. Acc. Chem. Res. 1997, 30, 2.
12. (c) Steinrücken, H. C.; Amhrein, N. 5-Enolpyruvylshikimate-3- phosphate synthase of Klebsiella pneumoniae 2. Inhibition by glyphosate [N-(phosphonomethyl)glycine]. Eur. J. Biochem. 1984, 143, 351.
13. Davies, G. M.; Barrett-Bee, K. J.; Jude, D. A.; Lehan, M.; Nichols, W. W.; Finder, P. E.; Thain, J. L.; Watkins, W. J.; Wilson, R. G. (6S)-6-Fluoroshikimic acid, an antibacterial agent acting on the aromatic biosynthesis pathway. Antimicrob. Agents Chemother. 1994, 38, 403.
14. (a) Giles, N. H.; Case, M. E.; Baum, J. A.; Geever, R. F.; Huiet, L.; Patel, V. B.; Tyler, B. M. Gene organisation and regulation in the QA (quinic acid) cluster of Neurospora crassa. Microbiol. Rev. 1985, 49, 338.
15. (b) Hawkins, A. R.; Lamb, H. K.; Moore, J. D.; Charles, I. G.; Roberts, C. F. The pre-chorismate (shikimate) and quinate pathways in filamentous fungi: theorical and practical aspects. J. Gen. Microbiol. 1993, 139, 1891.
16. Chauduri, C.; Ducan, K.; Graham, L. D.; Coggins, J. R. Identification of the active-site lysine residues of two biosynthetic 3-dehydroquinases. Biochem. J. 1990, 275, 1.
17. (a) White, P. J.; Young, J.; Hunter, I. S.; Nimmo, H. G.; Coggins, J. R. The purification and characterization of 3-dehydroquinase from Streptomyces coelicolor. Biochem. J. 1990, 265, 735.
18. (b) Moore, J. D.; Lamb, H. K.; Garbe, T.; Servos, S.; Dougan, G.; Charles, I. G.; Hawkins, A. R. Inducible overproduction of the Aspergillus nidulans pentafunctional AROM protein and the type I and II 3-dehydroquinases from Salmonella typhi and Mycobacterium tuberculosis. Biochem. J. 1992, 287, 173.
19. (c) Garbe, T.; Servos, S.; Hawkins, A.; Dimitriadis, G.; Young, D.; Dougan, G.; Charles, I. The Mycobacterium tuberculosis shikimate pathway genes: evolutionary relationship between biosynthetic and catabolic 3-dehydroquinases. Mol. Gen. Genet. 1991, 228, 385.
20. (d) Haslam, E.; Turner, M. J.; Sargent, D.; Thompson, R. S. Shikimate pathway. I. Preparation of stereospecifically labelled 2-deuterio derivatives of 3-dehydroquinic acid. J. Chem. Soc., C 1971, 1489.
21. (e) Shneier, A.; Harris, J.; Kleanthous, C.; Coggins, J. R.; Hawkins, A. R.; Abell, C. Evidence for opposite stereochemical courses for the reactions catalyzed by type I and type II dehydroquinases. Bioorg. Med. Chem. Lett. 1993, 3, 1399.
22. (f) Krell, T.; Pitt, A. R.; Coggins, J. R. The use of electrospray mass spectrometry to identify an essential arginine residue in type II dehydroquinases. FEBS Lett. 1995, 360, 93.
23. (a) Shneier, A.; Kleanthous, C.; Deka, R.; Coggins, J. R.; Abell, C. Observation of an imine intermediate on dehydroquinase by electrospray mass spectrometry. J. Am. Chem. Soc. 1991, 113, 9416.
24. (b) Leech, A. P.; James, R.; Coggins, J. R.; Kleanthous, C. Mutagenesis of active site residues in type I dehydroquinase from Escherichia coli. Stalled catalysis in a histidine to alanine mutant. J. Biol. Chem. 1995, 270, 25827.
25. Hanson, K. R.; Rose, I. A. The absolute stereochemical course of citric acid biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 1963, 50, 981.
26. Smith, B. W.; Turner, M. J.; Haslam, E. Stereochemical course of the 3-dehydroquinate dehydratase reaction and a novel preparation of shikimic acid labelled with isotopic hydrogen at C-2. J. Chem. Soc., Chem. Commun. 1970, 842.
27. (e) Harris, J.; Kleanthous, C.; Coggins, J. R.; Hawkins, A. R.; Abell, C. Different mechanistic and stereochemical courses for the reactions catalysed by type I and type II dehydroquinases. J. Chem. Soc., Chem. Commun. 1993, 13, 1080.
28. (f) Butler, J. R.; Alworth, W. L.; Nugent, M. Mechanism of dehydroquinase catalysed dehydratation. I. Formation of a schiff base intermediate. J. Am. Chem. Soc. 1974, 96, 1617.
29. (g) Chaudhuri, S.; Duncan, K.; Graham, L. D.; Coggins, J. R. Identification of the active-site lysine residues of two biosynthetic 3-dehydroquinases. Biochemistry 1991, 275, 1.
30. (h) Gourley, D. G.; Shrive, A. K.; Polikarpov, I.; Krell, T.; Coggins, J. R.; Hawkins, A. R.; Issacs, N. W.; Sawyer, L. The two types of 3-dehydroquinase have distint structures but catalyze the same overall reaction. Nat. Struct. Biol. 1999, 6, 521.
31. Deka, R. K.; Kleanthous, C.; Coggins, J. R. Identification of the essential histidine residue at the active site of Escherichia coli dehydroquinase. J. Biol. Chem. 1998, 273, 22237.
32. 13C NMR. J. Biol. Chem. 1998, 273, 9602.
33. (k) Boys, C. W. G.; Bury, S. M.; Sawyer, L.; Moore, J. D.; Charles, I. G.; Hawkins, A. R.; Deka, R.; Kleanthous, C.; Coggins, J. R. Crystallization of a type I 3-dehydroquinase from Salmonella typhi. J. Mol. Biol. 1992, 227, 352.
34. (a) Harris, J.; González-Bello, C.; Kleanthous, C.; Coggins, J. R.; Hawkins, A. R.; Abell, C. Evidence from kinetic isotope studies for and enolate intermediate in the mechanism of type II dehydroquinases. Biochem. J. 1996, 319, 333.
35. (b) Roszak, A. W.; Robinson, D. A.; Krell, T.; Hunter, I. S.; Frederickson, M.; Abell, C.; Coggins, J. R.; Lapthorn, A. J. The structure and mechanism of the type II dehydroquinase from Streptomyces coelicolor. Structure 2002, 10, 493.
36. (a) Krell, T.; Pitt, A. R.; Coggins, J. R. The use of electrospray mass spectrometry to identify an essential arginine residue in type II dehydroquinases. FEBS Lett. 1995, 360, 93.
37. (b) Krell, T.; Horsburgh, M. J.; Cooper, A.; Kelly, S. M.; Coggins, J. R. Localization of the active site of type II dehydroquinase. Identification of a common arginine-containing motif in the two classes of dehydroquinases. J. Biol. Chem. 1996, 277, 24492.
38. González-Bello, C.; Harris, J. M.; Manthey, M. K.; Coggins, J. R.; Abell, C. Irreversible inhibition of type I dehydroquinase by substrates for type II dehydroquinases. Bioorg. Med. Chem. Lett. 2000, 10, 407.
39. (a) Frederickson, M.; Parker, E. J.; Hawkins, A. R.; Coggins, J. R.; Abell, C. Selective inhibition of type II dehydroquinases. J. Org. Chem. 1999, 64, 2612.
40. (b) Toscano, M. D.; Frederickson, M.; Evans, D. P.; Coggins, J. R.; Abell, C.; González-Bello, C. Design, synthesis and evaluation of bifunctional inhibitors of type II dehydroquinase. Org. Biomol. Chem. 2003, 1, 2075.
41. (c) Frederickson, M.; Roszak, A. W.; Coggins, J. R.; Lapthorn, A. J.; Abell, C. (1R,4S,5R)-3-Fluoro-1,4,5-trihydroxy-2-cyclohexene-1-carboxylic acid: the fluoro analogue of the enolate intermediate in the reaction catalyzed by type II dehydroquinases. Org. Biomol. Chem. 2004, 2, 1592.
42. González-Bello, C.; Lence, E.; Toscano, M. D.; Castedo, L.; Coggins, J. R.; Abell, C. Parallel solid-phase synthesis and evaluation of inhibitors of Streptomyces coelicolor type II dehydroquinase. J. Med. Chem. 2003, 46, 5735.
43. (a) Frederickson, M.; Coggins, J. R.; Abell, C. Vinyl fluoride as an isoelectronic replacement for an enolate anion: inhibition of type II dehydroquinases. Chem. Commun. 2002, 1886.
44. (b) Le Sann, C.; Abell, C. Abell, A. D. A simple method for the preparation of 3-hydroxyiminodehydroquinate, a potent inhibitor of type II dehydroquinase. J. Chem. Soc., Perkin Trans, 1 2002, 2065.
45. Gourley, D. G.; Shrive, A. K.; Polikarpov, I.; Krell, T.; Coggins, J. R.; Hawkins, A. R.; Issacs, N. W.; Sawyer, L. The two types of 3-dehydroquinase have distinct structures but catalyze the same overall reaction. Nat. Struct. Biol. 1999, 6, 521.
46. X-ray crystal structure (PDB: 1HOR) of type II dehydroquinase from Mycobacterium tuberculosis complexed with 2,3-anydroquinic acid 3a (2.1 Å resolution) by Roszak, A. W.; Robinson, D. A.; Frederickson, M.; Abell, C.; Coggins, J. R.; Lapthorn, A. J.
47. X-ray crystal structure (PDB: 1HOS) of type II dehydroquinase from Mycobacterium tuberculosis complexed with 3-hydroxyimino-quinic acid 3c (1.7 Å resolution) by Roszak, A. W.; Frederickson, M.; Abell, C.; Coggins, J. R.; Lapthorn, A. J.
48. Barco, A.; Benetti, S.; De Risi, C.; Marchetti, P.; Pollini, G. P.; Zanirato, V. D-(-)-Quinic acid: a chiron store for natural product synthesis. Tetrahedron: Asymmetry 1997, 8, 3515.
49. Hanessian, S.; Pan, J.; Carnell, A.; Bouchard, H.; Lesage, L. Total synthesis of (-)-reserpine using the chiron approach. J. Org. Chem. 1997, 62, 465.
50. Trost, B. M.; Schroeder, G. M. Cyclic 1,2-diketones as building blocks for asymmetric synthesis of cycloalkenones. J. Am. Chem. Soc. 2000, 122, 3785.
51. (a) Jones, G.; Willett, P.; Glen, R. C. Molecular recognition of receptor sites using a genetic alorithm with a description of desolvation. J. Mol. Biol. 1995, 245, 43.
52. (b) Jones, G.; Willett, P.; Glen, R. C.; Leach, A. R.; Taylor, R. Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 1997, 267, 727.
53. Krell, T.; Horsburgh, M. J.; Cooper, A.; Kelly, S. M.; Coggins, J. R. Localization of the active site of type II dehydroquinases. Identification of a common arginine-containing motif in the two classes of dehydroquinases. J. Biol. Chem. 1996, 271, 24492.
54. (a) Evans, L. D. B.; Roszak, A. W.; Noble, L. J.; Robinson, D. A.; Chalk, P. A.; Matthews, J. L.; Coggins, J. R.; Price, N. C.; Lapthorn, A. J. Specificity of substrate recognition by type II dehydroquinases as revealed by binding of polyanions. FEBS Lett. 2002, 530, 24.
55. (b) The atomic coordinates were obtained from the Protein Data Bank with the accession code 1HO5.
56. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Zakrzewski, V. G.; Montgomery, J. A., Jr.; Stratmann, R. E.; Burant, J. C.; Pprich, S.; Millam, J. M.; Daniels, A. D.; Kudin, K. N.; Strain, M. C.; Farkas, O.; Tomasi, J.; Barone, V.; Cossi, M.; Cammi, R.; Mennucci, B.; Pomelli, C.; Adamo, C.; Clifford, S.; Ochterski, J.; Petersson, G. A.; Ayala, P. Y.; Cui, Q.; Morokuma, K.; Malick, D. K.; Rabuck, A. D.; Raghavachari, K.; Foresman, J. B.; Cioslowski, J.; Ortiz, J. V.; Baboul, A. G.; Stefanov, B. B.; Liu, G.; Liashenko, A.; Piskorz, P.; Komaromi, I.; Gomperts, R.; Martin, R. L.; Fox, D. J.; Keith, T.; Al-Laham, M. A.; Peng, C. Y.; Nanayakkara, A.; González, C.; Challacombe, M.; Gill, P. M. W.; Johnson, B. G.; Chen, W.; Wong, M. W.; Andres, J. L.; Head-Gordon, M.; Replogle, E. S.; Pople, J. A. Gaussian 98W, revision A.9; Gaussian, Inc.: Pittsburgh, PA, 1998.
57. Gourley, D. G.; Coggins, J. R.; Isaacs, N. W.; Moore, J. D.; Charles, I. G.; Hawkins, A. R. Crystallization of a type II dehydroquinase from Mycobacterium tuberculosis. J. Mol. Biol. 1994, 241, 488.