DXP reductoisomerase: Reaction of the substrate in pieces reveals a catalytic role for the nonreacting phosphodianion group

Biochemistry

Volumn 52, Issue 13, 2013, Pages 2302-2308

  Kholodar, Svetlana A ^a   Murkin, Andrew S ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; CATALYTIC ROLE; CONFORMATIONAL CHANGE; DIANIONS; LOOP CLOSURE; REDUCTOISOMERASE; TRANSITION STATE STABILIZATION;

CATALYSIS;

SUBSTRATES;

1 DEOXY DEXTRO XYLULOSE 5 PHOSPHATE; 1 DEOXY DEXTRO XYLULOSE 5 PHOSPHATE REDUCTOISOMERASE; OXIDOREDUCTASE; PHOSPHATE; PHOSPHITE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; ESCHERICHIA COLI; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MOLECULAR STABILITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; THERMOANAEROBACTERIUM; THERMOANAEROBIUM BROCKII;

ALDOSE-KETOSE ISOMERASES; CATALYTIC DOMAIN; KINETICS; MODELS, MOLECULAR; MYCOBACTERIUM TUBERCULOSIS; PENTOSEPHOSPHATES; PHOSPHATES; PHOSPHITES; SUBSTRATE SPECIFICITY;

EID: 84875780747     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400092n     Document Type: Article

References (38)

1. Grawert, T., Groll, M., Rohdich, F., Bacher, A., and Eisenreich, W. (2011) Biochemistry of the non-mevalonate isoprenoid pathway Cell. Mol. Life Sci. 68, 3797-3814
2. Miziorko, H. M. (2011) Enzymes of the mevalonate pathway of isoprenoid biosynthesis Arch. Biochem. Biophys. 505, 131-143
3. Manning, K. A., Sathyamoorthy, B., Eletsky, A., Szyperski, T., and Murkin, A. S. (2012) Highly precise measurement of kinetic isotope effects using 1H-detected 2D [13C,1H]-HSQC NMR spectroscopy J. Am. Chem. Soc. 134, 20589-20592
4. Munos, J. W., Pu, X., Mansoorabadi, S. O., Kim, H. J., and Liu, H. W. (2009) A secondary kinetic isotope effect study of the 1-deoxy-D-xylulose-5- phosphate reductoisomerase-catalyzed reaction: evidence for a retroaldol-aldol rearrangement J. Am. Chem. Soc. 131, 2048-2049
5. Proteau, P. J. (2004) 1-Deoxy-D-xylulose 5-phosphate reductoisomerase: an overview Bioorg. Chem. 32, 483-493
6. Kuzuyama, T., Takahashi, S., Takagi, M., and Seto, H. (2000) Characterization of 1-deoxy-D-xylulose 5-phosphate reductoisomerase, an enzyme involved in isopentenyl diphosphate biosynthesis, and identification of its catalytic amino acid residues J. Biol. Chem. 275, 19928-19932
7. Takahashi, S., Kuzuyama, T., Watanabe, H., and Seto, H. (1998) A 1-deoxy-D-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2-C-methyl-D-erythritol 4-phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis Proc. Natl. Acad. Sci. U. S. A. 95, 9879-9884
8. Perruchon, J., Ortmann, R., Altenkamper, M., Silber, K., Wiesner, J., Jomaa, H., Klebe, G., and Schlitzer, M. (2008) Studies addressing the importance of charge in the binding of fosmidomycin-like molecules to deoxyxylulosephosphate reductoisomerase ChemMedChem 3, 1232-1241
9. Phaosiri, C. and Proteau, P. J. (2004) Substrate analogs for the investigation of deoxyxylulose 5-phosphate reductoisomerase inhibition: synthesis and evaluation Bioorg. Med. Chem. Lett. 14, 5309-5312
10. Goryanova, B., Spong, K., Amyes, T. L., and Richard, J. P. (2013) Catalysis by orotidine 5′-monophosphate decarboxylase: Effect of 5-fluoro and 4′-substituents on the decarboxylation of two-part substrates Biochemistry 52, 537-546
11. Argyrou, A. and Blanchard, J. S. (2004) Kinetic and chemical mechanism of Mycobacterium tuberculosis 1-deoxy-D-xylulose-5-phosphate isomeroreductase Biochemistry 43, 4375-4384
12. Liu, J. and Murkin, A. S. (2012) Pre-steady-state kinetic analysis of 1-deoxy-D-xylulose-5-phosphate reductoisomerase from Mycobacterium tuberculosis reveals partially rate-limiting product release by parallel pathways Biochemistry 51, 5307-5319
13. Schurmann, M., Schurmann, M., and Sprenger, G. A. (2002) Fructose 6-phosphate aldolase and 1-deoxy-D-xylulose 5-phosphate synthase from Escherichia coli as tools in enzymatic synthesis of 1-deoxysugars J. Mol. Catal. B: Enzym. 19, 247-252
14. Amyes, T. L. and Richard, J. P. (2007) Enzymatic catalysis of proton transfer at carbon: activation of triosephosphate isomerase by phosphite dianion Biochemistry 46, 5841-5854
15. Bongini, A., Cardillo, G., Orena, M., Porzi, G., and Sandri, S. (1982) Regiocontrolled and stereocontrolled synthesis of epoxy alcohols and triols from allylic and homoallylic alcohols via iodo carbonates J. Org. Chem. 47, 4626-4633
16. Forbes, D. C., Ene, D. G., and Doyle, M. P. (1998) Stereoselective synthesis of substituted 5-hydroxy-1,3-dioxanes Synthesis 879-882
17. Smith, M. E. B., Hibbert, E. G., Jones, A. B., Dalby, P. A., and Hailes, H. C. (2008) Enhancing and reversing the stereoselectivity of Escherichia coli transketolase via single-point mutations Adv. Synth. Catal. 350, 2631-2638
18. Procopio, A., Dalpozzo, R., De Nino, A., Maiuolo, L., Russo, B., and Sindona, G. (2004) Erbium(III) triflate as an extremely active acylation catalyst Adv. Synth. Catal. 346, 1465-1470
19. Kis, K., Volk, R., and Bacher, A. (1995) Biosynthesis of riboflavin. Studies on the reaction mechanism of 6,7-dimethyl-8-ribityllumazine synthase Biochemistry 34, 2883-2892
20. Segel, I. H. (1975) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady State Enzyme Systems, Wiley, New York.
21. Richard, J. P. (2012) A paradigm for enzyme-catalyzed proton transfer at carbon: triosephosphate isomerase Biochemistry 51, 2652-2661
22. Amyes, T. L., O'Donoghue, A. C., and Richard, J. P. (2001) Contribution of phosphate intrinsic binding energy to the enzymatic rate acceleration for triosephosphate isomerase J. Am. Chem. Soc. 123, 11325-11326
23. Amyes, T. L., Richard, J. P., and Tait, J. J. (2005) Activation of orotidine 5′-monophosphate decarboxylase by phosphite dianion: the whole substrate is the sum of two parts J. Am. Chem. Soc. 127, 15708-15709
24. Tsang, W. Y., Amyes, T. L., and Richard, J. P. (2008) A substrate in pieces: allosteric activation of glycerol 3-phosphate dehydrogenase (NAD+) by phosphite dianion Biochemistry 47, 4575-4582
25. Jencks, W. P. (1981) On the attribution and additivity of binding energies Proc. Natl. Acad. Sci. U. S. A. 78, 4046-4050
26. Amyes, T. L. and Richard, J. P. (2013) Specificity in transition state binding: The Pauling model revisited Biochemistry 10.1021/bi301491r
27. Noble, M. E., Zeelen, J. P., and Wierenga, R. K. (1993) Structures of the "open" and "closed" state of trypanosomal triosephosphate isomerase, as observed in a new crystal form: implications for the reaction mechanism Proteins 16, 311-326
28. Callahan, B. P. and Miller, B. G. (2007) OMP decarboxylase - An enigma persists Bioorg. Chem. 35, 465-469
29. Ou, X., Ji, C., Han, X., Zhao, X., Li, X., Mao, Y., Wong, L. L., Bartlam, M., and Rao, Z. (2006) Crystal structures of human glycerol 3-phosphate dehydrogenase 1 (GPD1) J. Mol. Biol. 357, 858-869
30. Henriksson, L. M., Bjorkelid, C., Mowbray, S. L., and Unge, T. (2006) The 1.9 A resolution structure of Mycobacterium tuberculosis 1-deoxy-D-xylulose 5-phosphate reductoisomerase, a potential drug target Acta Crystallogr., Sect. D: Biol. Crystallogr. 62, 807-813
31. Henriksson, L. M., Unge, T., Carlsson, J., Aqvist, J., Mowbray, S. L., and Jones, T. A. (2007) Structures of Mycobacterium tuberculosis 1-deoxy-D-xylulose-5-phosphate reductoisomerase provide new insights into catalysis J. Biol. Chem. 282, 19905-19916
32. Andaloussi, M., Henriksson, L. M., Wieckowska, A., Lindh, M., Bjorkelid, C., Larsson, A. M., Suresh, S., Iyer, H., Srinivasa, B. R., and Bergfors, T. 2011, Design, synthesis, and X-ray crystallographic studies of alpha-aryl substituted fosmidomycin analogues as inhibitors of Mycobacterium tuberculosis 1-deoxy-D-xylulose 5-phosphate reductoisomerase J. Med. Chem. 54, 4964-4976
33. Bjorkelid, C., Bergfors, T., Unge, T., Mowbray, S. L., and Jones, T. A. (2012) Structural studies on Mycobacterium tuberculosis DXR in complex with the antibiotic FR-900098 Acta Crystallogr., Sect. D: Biol. Crystallogr. 68, 134-143
34. Umeda, T., Tanaka, N., Kusakabe, Y., Nakanishi, M., Kitade, Y., and Nakamura, K. T. (2011) Molecular basis of fosmidomycin's action on the human malaria parasite Plasmodium falciparum Sci. Rep. 1, 9
35. Mac Sweeney, A., Lange, R., Fernandes, R. P., Schulz, H., Dale, G. E., Douangamath, A., Proteau, P. J., and Oefner, C. (2005) The crystal structure of E. coli 1-deoxy-D-xylulose-5-phosphate reductoisomerase in a ternary complex with the antimalarial compound fosmidomycin and NADPH reveals a tight-binding closed enzyme conformation J. Mol. Biol. 345, 115-127
36. Zingle, C., Kuntz, L., Tritsch, D., Grosdemange-Billiard, C., and Rohmer, M. (2010) Isoprenoid biosynthesis via the methylerythritol phosphate pathway: structural variations around phosphonate anchor and spacer of fosmidomycin, a potent inhibitor of deoxyxylulose phosphate reductoisomerase J. Org. Chem. 75, 3203-3207
37. Nguyen-Trung, A. T., Tritsch, D., Grosdemange-Billiard, C., and Rohmer, M. (2013) Synthesis of tetrazole analogues of phosphonohydroxamic acids: An attempt to improve the inhibitory activity against the DXR Bioorg. Med. Chem. Lett. 23, 1643-1647
38. Deng, L., Endo, K., Kato, M., Cheng, G., Yajima, S., and Song, Y. (2011) Structures of 1-deoxy-D-xylulose-5-phosphate reductoisomerase/lipophilic phosphonate complexes ACS Med. Chem. Lett. 2, 165-170