Progress in type II dehydroquinase inhibitors: From concept to practice

Medicinal Research Reviews

Volumn 27, Issue 2, 2007, Pages 177-208

  González Bello, Concepción ^a   Castedo, Luis ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

Antibiotics; Antiparasitic; Dehydroquinase; Herbicides; Inhibitors; Shikimic acid pathway

Indexed keywords

2 BROMO 3 DEHYDROQUINIC ACID; 2 BROMO 3 DEHYDROSHIKIMIC ACID; 2 FLUORO 3 DEHYDROQUINIC ACID; 2 FLUORO 3 DEHYDROSHIKIMIC ACID; 2,3 DEHYDROQUINIC ACID; 3 DEHYDROQUINATE DEHYDRATASE; 3 DEHYDROQUINIC ACID; 3 DEOXYQUINIC ACID; ALKENE DERIVATIVE; BACTERIAL ENZYME; BROMOBENZOIC ACID DERIVATIVE; ENZYME INHIBITOR; LACTONE DERIVATIVE; NITROGEN DERIVATIVE; OXIME DERIVATIVE; SHIKIMIC ACID; TRIFLUOROMETHANESULFONIC ACID; TYPE 2 DEHYDROQUINASE INHIBITOR; UNCLASSIFIED DRUG;

CRYSTAL STRUCTURE; DRUG EFFICACY; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME INHIBITION; ENZYME SUBSTRATE COMPLEX; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYDROGEN BOND; MALARIA; NONHUMAN; PNEUMONIA; REVIEW; STEREOCHEMISTRY; STRUCTURE ANALYSIS; SUZUKI REACTION; TOXOPLASMOSIS; TUBERCULOSIS; X RAY CRYSTALLOGRAPHY;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BIOCHEMISTRY; DRUG DESIGN; ENZYME INHIBITORS; HUMANS; HYDRO-LYASES; MODELS, MOLECULAR; MOLECULAR MIMICRY;

EID: 33847125327     PISSN: 01986325     EISSN: None     Source Type: Journal    
DOI: 10.1002/med.20076     Document Type: Review

References (83)

1. The biochemistry of plant phenolics. In: Van Sumere CF, Lea PJ, editors. Annual Proceedings of the Phytochemical Society, Vol. 25. Oxford: Clarendon Press; 1985.
2. Abell C. Enzymology and molecular biology of the shikimate pathway. In: Sankawa U, editor. Comprehensive natural products chemistry. Oxford: Pergamon, Elsevier Science Ltd.; 1998. p 573-607.
3. Haslam E. The shikimate pathway. New York: Wiley; 1974.
4. Bentley R. The shikimate pathway-A metabolic tree with branches. Crit Rev Biochem Mol Biol 1990;25:307-383.
5. Herrmann K, Weaver L. The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 1999;50:473-755.
6. Gibson F, Pittard AJ. Pathways of biosynthesis of aromatic amino acids and vitamins and their control in microorganisms. Bacteriol Rev 1968;32:465-492.
7. Pittard AJ. Biosynthesis of the aromatic amino acids. In: Niedhardt FC, editor. Escherichia coli and Salmonella typhimurium: Cellular and molecular biology. Washington DC: American Society for Microbiology; 1991. Vol 1: p 368-394.
8. Braus GH. Aromatic amino acid biosynthesis in the yeast Saccaromyces cerevisiae: A model system for the regulation of a eukaryotic biosynthesis pathway. Microbiol Rev 1991;55:349-370.
9. Roberts F, Roberts CW, Johnson JJ, Kyle DE, Krell T, Coggins JR, Coombs GH, Milhous WK, Tzipori S, Ferguson DJP, Chakrabarti D, McLeod R. Evidence for the shikimate pathway in apicomplexan parasites. Nature 1998;393:801-805.
10. Keeling PJ, Palmer JD, Donald RG, Roos DS, Waller RF, McFadden GI. Shikimate pathway in apicomplexan parasites. Nature 1999;397:219-220.
11. Campbell SA, Richards TA, Mui EJ, Samuel BU, Coggins JR, McLeod R, Roberts CW. A complete shikimate pathway in Toxoplasma gondii: An ancient eukaryotic innovation. Int J Parasit 2004;34:5-13.
12. Roberts CW, Roberts F, Lyons RE, Kirisits MJ, Mui EJ, Finnerty J, Johnson JJ, Ferguson DJ, Coggins JR, Krell T, Coombs GH, Milhous WK, Kyle DE, Tzipori S, Barnwell J, Dame JB, Carlton J, McLeod R. The shikimate pathway and its branches in apicomplexan parasites. J Infect Dis 2002;185:S25-S36.
13. McConkey GA, Pinney JW, Westhead DR, Plueckhahn K, Fitzpatrick TB, Macheroux P, Kappes B. Annotating the Plasmodium genome and the enigma of the shikimate pathway. Trends in Parasitology 2004;20:60-65.
14. Davies GM, Barrett-Bee KJ, Jude DA, Lehan M, Nichols WW, Pinder PE, Thain JL, Watkins WJ, Wilson RG. (6S)-6-Fluoroshikimic acid, an antibacterial agent acting on the aromatic biosynthesis pathway. Antimicrob Agents Chemother 1994;38:403-406.
15. Mousdale DM, Coggins JR. Amino acid synthesis. In: Kirkwood RC, editor. Target sites for herbicide action. New York: Plenum Press; 1991. p 29-56.
16. Steinrücken HC, Amhrein N. The herbicide glyphosate is a potent inhibitor of 5-enolpyruvylshikimic acid 3-phosphate synthase. Biochem Biophys Res Commun 1980;94:1207-1212.
17. Franz JE, Mao MK, Sikorski JA. Glyphosate: A unique global herbicide. Washington, DC: American Chemical Society Monograph 189; American Chemical Society; 1997.
18. Sikorski JA, Gruys KJ. Understanding Glyphosate's molecular mode of action with EPSP synthase: Evidence favoring an allosteric inhibitor model. Acc Chem Res 1997;30:2-8.
19. Grossbard E, Atkinson D. The herbicide glyphosate. Boston, MA: Butterworths; 1985. pp 3-17.
20. Steinrücken HC, Amhrein N. 5-Enolpyruvylshikimate-3-phosphate synthase of Klebsiella pneumoniae 2. Inhibition by glyphosate [N-(phosphonomethyl)glycine]. Eur J Biochem 1984;143:351-357.
21. Bulloch EMM, Jones MA, Parker EJ, Osborne AP, Stephens E, Davies GM, Coggins JR, Abell C. Identification of 4-amino-4-deoxychorismate synthase as the molecular target for the antimicrobial action of (6S)-6-fluoroshikimate. J Am Chem Soc 2004;126:9912-9913.
22. Coggins JR, Duncan K, Anton IA, Boocock MR, Chaudhuri S, Lambert JM, Lewendon A, Millar G, Mousdale DM, Smith DD. The anatomy of a multifunctional enzyme. Biochem Soc Trans 1987;15:754-759.
23. Butler JR, Alworth WL, Nugent MJ. Mechanism of dehydroquinase catalysed dehydration 1. Formation of a shiff base intermediate. J Am Chem Soc 1974;96:1617-1618.
24. Duncan K, Edwards RM, Coggins JR. The pentafunctional arom emzyme of Saccharomyces cerevisiae is a mosaic of monofunctional domains. Biochem J 1987;246:375-386.
25. Giles NH, Case ME, Baum JA, Geever RF, Huiet L, Patel VB, Tyler BM. Gene organisation and regulation in the QA (quinic acid) cluster of Neurospora crassa. Microbiol Rev 1985;49:338-358.
26. Hawkins AR, Lamb HK, Moore JD, Charles IG, Roberts CF. The pre-chorismate (shikimate) and quinate pathways in filamentous fungi: Theorical and practical aspects. J Gen Microbiol 1993;139:1891-1899.
27. Kleanthous CK, Deka R, Davis K, Kelly SM, Cooper A, Harding SE, Price NC, Hawkins AR, Coggins JR. A comparison of the enzymological and biophysical properties of two distinct classes of dehydroquinase enzymes. Biochem J 1992;282:687-695.
28. Moore JD, Hawkins AR, Charles IG, Deka R, Coggins JR, Cooper A, Kelly SM, Price NC. Characterization of the type I dehydroquinase from Salmonella typhi. Biochem J 1993;295:277-285.
29. Servos S, Chatfield S, Hone D, Levine M, Dimitriadis G, Pickard D, Dougan G, Fairweather N, Charles IG. Molecular cloning and characterization of the aroD gene encoding 3-dehydroquinase from Salmonella typhi. J Gen Microbiol 1991;137:147-152.
30. Moore JD, Lamb HK, Garbe T, Servos S, Dougan G, Charles IG, Hawkins AR. 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;287:173-181.
31. Duncan K, Chaudhuri S, Campbell MS, Coggins JR. The overexpression and complete amino acid sequence of Escherichia coli 3-dehydroquinase. Biochem J 1986;238:475-483.
32. Hanson KR, Rose IA. The absolute stereochemical course of citric acid biosynthesis. Proc Natl Acad Sci USA 1963;50:981-988.
33. Smith BW, Turner MJ, Haslam E. Stereochemical course of the 3-dehydroquinate dehydratase reaction and a novel preparation of shikimic acid labelled with isotopic hydrogen at C2. J Chem Soc Chem Commun 1970;842-843.
34. Haslam E, Turner MJ, Sargent D, Thompson RS. Shikimate pathway. I. Preparation of stereospecifically labelled 2-deuterio derivatives of 3-dehydroquinic acid. J Chem Soc (C) 1971;1489-1495.
35. Chaudhuri A, Duncan K, Graham LD, Coggins JR. Identification of the active-site lysine residues of two biosynthetic 3-dehydroquinases. Biochem J 1991;275:1-6.
36. Shneier A, Kleanthous C, Deka R, Coggins JR, Abell C. Observation of an imine intermediate on dehydroquinase by electrospray mass spectrometry. J Am Chem Soc 1991;113:9416-9418.
37. Mitsuhashi S, Davis BD. Aromatic biosynthesis XII. Conversion of 5-dehydroquinic acid to 5-dehydroshikimic acid by 5-dehydroquinase. Biochim Biophys Acta 1954;15:54-61.
38. Boys CWG, Bury SM, Sawyer L, Moore JD, Charles IG, Hawkins AR, Deka R, Kleanthous C, Coggins JR. Crystallization of a type I 3-dehydroquinase from Salmonella typhi. J Mol Biol 1992;227:352-355.
39. Gourley DG, Shrive AK, Polikarpov I, Krell T, Coggins JR, Hawkins AR, Isaacs NW, Sawyer L. The two types of 3-dehydroquinase have distinct structures but catalyse the same overall reaction. Nat Struct Biol 1999;6:521-525.
40. Deka RK, Kleanthous C, Coggins JR. Identification of the essential histidine residue at the active site of Escherichia coli dehydroquinase. J Biol Chem 1992;267:22237-22242.
41. Leech AP, James R, Coggins JR, 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;270:25827-25836.
42. 13C NMR. J Biol Chem 1998;273:9602-9607.
43. Kleanthous C, Coggins JR. Reversible alkylation of an active site methionine residue in dehydroquinase. J Biol Chem 1990;265:10935-10939.
44. Price NC, Boam DJ, Kelly SM, Duncan D, Krell T, Gourley DG, Coggins JR, Virden R, Hawkins AR. The folding and assembly of the dodecameric type II dehydroquinases. Biochem J 1999;338:195-202.
45. Garbe T, Servos S, Hawkins AR, 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;228:385-392.
46. White PJ, Young J, Hunter IS, Nimmo HG, Coggins JR. The purification and characterization of 3-dehydroquinase from Streptomyces coelicolor. Biochem J 1990;265:735-738.
47. White PJ, Nairn J, Price NC, Nimmo HG, Coggins JR, Hunter IS. Phosphoglycerate mutase from Streptomyces coelicolor A3(2): Purification and characterization of the enzyme and cloning and sequence analysis of the gene. J Bacteriol 1992;174:434-440.
48. Krell T, Horsburgh MJ, Cooper A, Kelly SM, Coggins JR. 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;271:24492-24497.
49. Bottomley JR, Clayton CL, Chalk PA, Kleanthous C. Cloning, sequencing, expression, purification and preliminary characterization of a type II dehydroquinase from Helicobacter pylori. Biochem J 1996;319:559-565.
50. Lee BII, Kwak JE, Suh SW. Crystal structure of the type II 3-dehydroquinase from Helicobacter pylori. Proteins 2003;51:616-617.
51. Da Silva AJF, Whittington H, Clements J, Roberts C, Hawkins AR. Sequence analysis and transformation by the catabolic 3-dehydroquinate (QUTE) gene from Aspergillus nidulans. Biochem J 1986;240:481-488.
52. Hawkins AR, Giles NH, Kinghorn JR. Genetical and biochemical aspects of quinate breakdown in the filamentous fungus Aspergillus nidulans. Biochem Genet 1982;20:271-286.
53. Beri RK, Grant S, Roberts CF, Smith M, Hawkins AR. Selective overexpression of the QUTE gene encoding catabolic 3-dehydroquinase in multicopy transformants of Aspergillus nidulans. Biochem J 1990;265:337-342.
54. Hautala JA, Jacobson JW, Case ME, Giles NH. Purification and characterization of catabolic dehydroquinase, an enzyme in the inducible quinic acid catabolic pathway of Neurospora crassa. J Biol Chem 1975;250:6008-6014.
55. Hawkins AR, Reinert WR, Giles NH. Characterization of Neurospora crassa catabolic dehydroquinase purified from N. crassa and Escherichia coli. Biochem J 1982;203:769-773.
56. Euverink GJW, Hessels GI, Vrijbloed JW, Coggins JR, Dijkhuizen L. Purification and characterization of a dual function 3-dehydroquinate dehydratase from Amycolatopsis methanolica. J Gen Microbiol 1992;138:2449-2457.
57. Harris J, Kleanthous C, Coggins JR, Hawkins JR, Abell C. Different mechanistic and stereochemical courses for the reactions catalysed by type I and type II dehydroquinases. J Chem Soc Chem Commun 1993:1080-1081.
58. Shneier A, Harris J, Kleanthous C, Coggins JR, Hawkins AR, Abell C. Evidence for opposite stereochemical courses for the reaction catalysed by type I and type II dehydroquinases. Bioorg Med Chem Lett 1993;3:1399-1402.
59. Krell T, Pitt AR, Coggins JR. The use of electrospray mass spectrometry to identify an essential arginine residue in type II dehydroquinases. FEBS Lett 1995;360:93-96.
60. Harris J, González-Bello C, Kleanthous C, Coggins JR, Hawkins AR, Abell C. Evidence from kinetic isotope studies for and enolate intermediate in the mechanism of type II dehydroquinases. Biochem J 1996;319:333-336.
61. Roszak AW, Robinson DA, Krell T, Hunter IS, Frederickson M, Abell C, Coggins JR, Lapthorn AJ. The structure and mechanism of the type II dehydroquinase from Streptomyces coelicolor. Structure 2002;10:493-503.
62. González-Bello C, Manthey MK, Harris JM, Hawkins AR, Coggins JR, Abell C. Synthesis of 2-bromo- and 2-fluoro-3-dehydroshikimic acids and 2-bromo- and 2-fluoroshikimic acids using synthetic and enzymatic approaches. J Org Chem 1998;63:1591-1597.
63. Manthey MK, González-Bello C, Abell C. Synthesis of (2R)-2-bromodehydroquinic acid and (2R)-2-fluorodehydroquinic acid. J Chem Soc Perkin Trans 1 1997;625-628.
64. González Bello C, Harris JM, Manthey MK, Coggins JR, Abell C. Irreversible inhibition of type I dehydroquinase by substrates for type II dehydroquinase. Bioorg Med Chem Lett 2000;10:407-409.
65. Frederickson M, Parker EJ, Hawkins AR, Cogins JR, Abell C. Selective inhibition of type II dehydroquinase. J Org Chem 1999;64:2612-2613.
66. Frederickson M, Coggins JR, Abell C. Vinyl fluoride as an isoelectronic replacement for an enolate anion: Inhibition of type II dehydroquinases. Chem Commun 2002;1886-1887.
67. Le Sann C, Abell C, Abell AD. A simple method for the preparation of 3-hydroxyiminodehydroquinate, a potent inhibitor of type II dehydroquinase. J Chem Soc Perkin Trans 1 2002;2065-2068.
68. Frederickson M, Roszak AW, Coggins JR, Lapthorn AJ, 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;2:1592-1596.
69. Barlett PA, Maitra U, Chouinard PM. Synthesis of "Iso-EPSP" and evaluation of its interaction with chorismate synthase. J Am Chem Soc 1986;108:8068-8071.
70. Tian F, Montchamp J-L, Frost JW. Inhibitor ionization as a determinant of binding to 3-dehydroquinate synthase. J Org Chem 1996;61:7373-7381.
71. Protein Data Bank: Robinson DA, Roszak AW, Frederickson M, Abell C, Coggins JR, Lapthorn AJ. Structural basis for selectivity of oxime based inhibitors towards type II dehydroquinase from Mycobacterium tuberculosis.
72. Toscano MD, Frederickson M, Evans DP, Coggins JR, Abell C, González-Bello C. Design, synthesis and evaluation of bifunctional inhibitors of type II dehydroquinase. Org Biomol Chem 2003;1:2075-2083.
73. Hanessian S, Wang J, Montgomery D, Stoll V, StewartKD, Kati W, Maring C, Kempf D, Hutchins C, Laver WG. Design, synthesis, and neuraminidase inhibitory activity of GS-4071 analogues that utilize a novel hydrophobic paradigm. Bioorg Med Chem Lett 2002;12:3425-3429.
74. The assay conditions were Tris.HCl 50 mM, pH = 7.0 and 25°C.
75. Evans LDB, Roszak AW, Noble LJ, Robinson DA, Chalk PA, Mattews JL, Coggins JR, Price NC, Lapthorn AJ. Specificity of substrate recognition by type II dehydroquinases as revealed by binding of polyanions. FEBS Lett 2002;530:24-30.
76. González-Bello C, Lence E, Toscano MD, Castedo L, Coggins JR, Abell C. Parallel solid-phase synthesis and evaluation of inhibitors of Streptomyces coelicolor type II dehydroquinase. J Med Chem 2003;46:5735-5744.
77. González-Bello C, Carballido M, Castedo L. Synthesis of polyhydroxycyclohexanes and relatives from (-)-quinic acid. J Org Chem 2003;68:2248-2255.
78. Carballido M, Castedo L, González C. Synthesis of carba-sugars from (-)-quinic acid. Tetrahedron Lett 2001;42:3973-3976.
79. Sánchez-Sixto C, Prazeres VFV, Castedo L, Lamb H, Hawkins AR, González-Bello C. Structure-based design, synthesis and biological evaluation of inhibitors of Mycobacterium tuberculosis type II dehydroquinase. J Med Chem 2005;48:4871-4881.
80. Hanessian S, Pan J, Carnell A, Bouchard H, Lesage L. Total synthesis of (-)-reserpine using the Chiron approach. J Org Chem 1997;62:465-473.
81. M value of 40 μM was obtained at the assay conditions (Tris.HOAc 50 mM, pH = 8.2, 25°C).
82. Chana SS, Cockerill GS, Madge D. Preparation of bissulfonamides as inhibitors of dehydroquinate synthetases and type II dehydroquinases. 2002; Int. Pat. WO02083629.
83. Arrou Therapeutics Ltd. Bissulfonamides as inhibitors of the dehydroquinate synthetase enzyme AroB and of the type II dehydroquinase Aro Q. Expert Opin Ther Patents 2001;11:1797-1799.