Structural Views along the Mycobacterium tuberculosis MenD Reaction Pathway Illuminate Key Aspects of Thiamin Diphosphate-Dependent Enzyme Mechanisms

Structure

Volumn 24, Issue 7, 2016, Pages 1167-1177

  Jirgis, Ehab N M ^a   Bashiri, Ghader ^a   Bulloch, Esther M M ^a   Johnston, Jodie M ^a   Baker, Edward N ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

crystal structures; menaquinone biosynthesis; MenD; reaction intermediates; thiamin diphosphate

Indexed keywords

2 OXOGLUTARIC ACID; 2 SUCCINYL 5 ENOLPYRUVYL 6 HYDROXY 3 CYCLOHEXADIENE 1 CARBOXYLATE SYNTHASE; BACTERIAL ENZYME; MENAQUINONE; SYNTHETASE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; PROTEIN BINDING; PYRUVATE OXIDASE; THIAMINE;

ARTICLE; BACILLUS SUBTILIS; CRYSTAL STRUCTURE; CRYSTALLIZATION; ELECTRON TRANSPORT; ENVIRONMENTAL TEMPERATURE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME STRUCTURE; ESCHERICHIA COLI; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; MOLECULAR RECOGNITION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; REACTION ANALYSIS; RESPIRATORY CHAIN; SIZE EXCLUSION CHROMATOGRAPHY; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; METABOLISM; MOLECULAR DYNAMICS; PROTEIN MULTIMERIZATION;

BACTERIAL PROTEINS; CATALYTIC DOMAIN; MOLECULAR DYNAMICS SIMULATION; MYCOBACTERIUM TUBERCULOSIS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PYRUVATE OXIDASE; THIAMINE;

EID: 84978942683     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2016.04.018     Document Type: Article

References (41)

1. Balakrishnan, A., Paramasivam, S., Chakraborty, S., Polenova, T., Jordan, F., Solid-state nuclear magnetic resonance studies delineate the role of the protein in activation of both aromatic rings of thiamin. J. Am. Chem. Soc. 134 (2012), 665–672.
2. Bald, D., Koul, A., Respiratory ATP synthesis: the new generation of mycobacterial drug targets?. FEMS Microbiol. Lett. 308 (2010), 1–7.
3. Bhasin, M., Billinsky, J.L., Palmer, D.R.J., Steady-state kinetics and molecular evolution of Escherichia coli MenD [(1R,6R)-2-succinyl-6-hydroxy-2,4-cyclohexadiene-1-carboxylate synthase], an anomalous thiamin diphosphate-dependent decarboxylase-carboligase. Biochemistry 42 (2003), 13496–13504.
4. Bashiri, G., Baker, E.N., Production of recombinant proteins in Mycobacterium smegmatis for structural and functional studies. Protein Sci. 24 (2015), 1–10.
5. 420 production in Mycobacterium smegmatis. PLoS One, 5, 2010, e15803.
6. Bax, A.D., A spatially selective composite 90° radiofrequency pulse. J. Mag. Res. 65 (1985), 142–145.
7. Berthold, C.L., Toyota, C.G., Moussatche, P., Wood, M.D., Leeper, F., Richards, N.G., Lindqvist, Y., Crystallographic snapshots of oxalyl-CoA decarboxylase give insights into catalysis by nonoxidative ThDP-dependent decarboxylases. Structure 15 (2007), 853–861.
8. Dawson, A., Fyfe, P.K., Hunter, W.N., Specificity and reactivity in menaquinone biosynthesis: the structure of Escherichia coli MenD (2-succinyl-5-enolpyruvyl-6-hydroxy-3-cyclohexadiene-1-carboxylate synthase). J. Mol. Biol. 384 (2008), 1353–1368.
9. Dawson, A., Chen, M., Fyfe, P.K., Guo, Z., Hunter, W.N., Structure and reactivity of Bacillus subtilis MenD catalyzing the first committed step in menaquinone biosynthesis. J. Mol. Biol. 401 (2010), 253–264.
10. Debnath, J., Siricilla, S., Wan, B., Crick, D.C., Lenaerts, A.J., Franzblau, S.G., Kurosu, M., Discovery of selective menaquinone biosynthesis inhibitors against Mycobacterium tuberculosis. J. Med. Chem. 55 (2012), 3739–3755.
11. Dhiman, R.K., Mahapatra, S., Slayden, R.A., Boyne, M.E., Lenaerts, A., Hinshaw, J.C., Angala, S.K., Chatterjee, D., Biswas, K., Narayanasamy, P., et al. Menaquinone synthesis is critical for maintaining mycobacterial viability during exponential growth and recovery from non-replicating persistence. Mol. Microbiol. 72 (2009), 85–97.
12. Duggleby, R.G., Domain relationships in thiamine diphosphate-dependent enzymes. Acc. Chem. Res. 39 (2006), 550–557.
13. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 486–501.
14. Evans, P.R., Murshudov, G.N., How good are my data and what is the resolution?. Acta Crystallogr. D Biol. Crystallogr. 69 (2013), 1204–1214.
15. Fang, M., Macova, A., Hanson, K.L., Kos, J., Palmer, D.R., Using substrate analogues to probe the kinetic mechanism and active site of Escherichia coli MenD. Biochemistry 50 (2011), 8712–8721.
16. Frank, R.A., Titman, C.M., Pratap, J.V., Luisi, B.F., Perham, R.N., A molecular switch and proton wire synchronize the active sites in thiamine enzymes. Science 306 (2004), 872–876.
17. Frank, R.A., Leeper, F.J., Luisi, B.F., Structure, mechanism and catalytic duality of thiamine-dependent enzymes. Cell. Mol. Life Sci. 64 (2007), 892–905.
18. Jiang, M., Cao, Y., Guo, Z.F., Chen, M., Chen, X., Guo, Z., Menaquinone biosynthesis in Escherichia coli: identification of 2-succinyl-5-enolpyruvyl-6-hydroxy-3-cyclohexene-1-carboxylate as a novel intermediate and re-evaluation of MenD activity. Biochemistry 46 (2007), 10979–10989.
19. Jiang, M., Chen, M., Cao, Y., Yang, Y., Sze, K.H., Chen, X., Guo, Z., Determination of the stereochemistry of 2-succinyl-5-enolpyruvyl-6-hydroxy-3- cyclohexene-1-carboxylate, a key intermediate in menaquinone biosynthesis. Org. Lett. 9 (2007), 4765–4767.
20. Jordan, F., Current mechanistic understanding of thiamin diphosphate-dependent enzymatic reactions. Nat. Prod. Rep. 20 (2003), 184–201.
21. Jordan, F., Nemeria, N.S., Progress in the experimental observation of thiamin diphosphate-bound intermediates on enzymes and mechanistic information derived from these observations. Bioorg. Chem. 57 (2014), 251–262.
22. Jordan, F., Nemeria, N.S., Sergienko, E., Multiple modes of active center communication in thiamin diphosphate-dependent enzymes. Acc. Chem. Res. 38 (2005), 755–763.
23. Kabsch, W., XDS. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 125–132.
24. Kurosu, M., Narayanasamy, P., Biswas, K., Dhiman, R., Crick, D.C., Discovery of 1,4-dihydroxy-2-naphthoate [corrected] prenyltransferase inhibitors: new drug leads for multidrug-resistant gram-positive pathogens. J. Med. Chem. 50 (2007), 3973–3975.
25. Kaplun, A., Binshtein, E., Vyazmensky, M., Steinmetz, A., Barak, Z., Chipman, D.M., Tittman, K., Shaanan, B., Glyoxylate carboligase lacks the canonical active site glutamate of thiamine-dependent enzymes. Nat. Chem. Biol. 2 (2008), 113–118.
26. Ludtke, S., Neumann, P., Erixon, K.M., Leeper, F., Kluger, R., Ficner, R., Tittmann, K., Sub-angstrom-resolution crystallography reveals physical distortions that enhance reactivity of a covalent enzymatic intermediate. Nat. Chem. 5 (2013), 762–767.
27. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., Read, R.J., Phaser crystallographic software. J. Appl. Crystallogr. 40 (2007), 658–674.
28. Moreland, N., Ashton, R., Baker, H.M., Ivanovic, I., Patterson, S., Arcus, V.L., Baker, E.N., Lott, J.S., A flexible and economical medium-throughput strategy for protein production and crystallization. Acta Crystallogr. D Biol. Crystallogr. 61 (2005), 1378–1385.
29. Murshudov, G.N., Skubak, P., Lebedev, A.A., Pannu, N.S., Steiner, R.A., Nicholls, R.A., Winn, M.D., Long, F., Vagin, A.A., REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67 (2011), 355–367.
30. Nemeria, N., Korotchkina, L., McLeish, M.J., Kenyon, G.L., Patel, M.S., Jordan, F., Elucidation of the chemistry of enzyme-bound thiamin diphosphate prior to substrate binding: defining internal equilibria among tautomeric and ionization states. Biochemistry 46 (2007), 10739–10744.
31. Nemeria, N.S., Arjunan, P., Chandrasekhar, K., Mossad, M., Tittmann, K., Furey, W., Jordan, F., Communication between thiamin cofactors in the Escherichia coli pyruvate dehydrogenase complex E1 component active centers: evidence for a “direct pathway” between the 4′-aminopyrimidine N1′ atoms. J. Biol. Chem. 285 (2010), 11197–11209.
32. Nemeria, N., Binshtein, E., Patel, H., Balakrishnan, A., Vered, I., Shaanan, B., Barak, Z., Chipman, D., Jordan, F., Glyoxylate carboligase: a unique thiamin diphosphate-dependent enzyme that can cycle between the 4′-aminopyrimidinium and 1′,4′-iminopyrimidine tautomeric forms in the absence of the conserved glutamate. Biochemistry 51 (2012), 7940–7952.
33. Priyadarshi, A., Saleem, Y., Nam, K.H., Kim, K.S., Park, S.Y., Kim, E.E., Hwang, K.Y., Structural insights of the MenD from Escherichia coli reveal ThDP affinity. Biochem. Biophys. Res. Commun. 380 (2009), 797–801.
34. Rao, S.P., Alonso, S., Rand, L., Dick, T., Pethe, K., The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, non-replicating Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 105 (2008), 11945–11950.
35. Schroder-Tittmann, K., Meyer, D., Arens, J., Wechsler, C., Tietzel, M., Golbik, R., Tittmann, K., Alternating sites reactivity is a common feature of thiamin diphosphate-dependent enzymes as evidenced by isothermal titration calorimetry studies of substrate binding. Biochemistry 52 (2013), 2505–2507.
36. Sergienko, E.A., Wang, J., Polovnikova, L., Hasson, M.S., McLeish, M.J., Kenyon, G.L., Jordan, F., Spectroscopic detection of transient thiamin diphosphate-bound intermediates on benzoylformate decarboxylase. Biochemistry 39 (2000), 13862–13869.
37. Studier, F.W., Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41 (2005), 207–234.
38. Vyazmensky, M., Steinmetz, A., Meyer, D., Golbik, R., Barak, Z., Tittmann, K., Chipman, D.M., Significant catalytic roles for Glu47 and Gln110 in all four of the C-C bond-making and -breaking steps of the reactions of acetohydroxyacid synthase II. Biochemistry 50 (2011), 3250–3260.
39. Weinstein, E.A., Yano, T., Li, L.S., Avarbock, D., Avarbock, A., Helm, D., McColm, A.A., Duncan, K., Lonsdale, J.T., Rubin, H., Inhibitors of Type II NADH:menaquinone oxidoreductase represent a class of antitubercular drugs. Proc. Natl. Acad. Sci. USA 102 (2005), 4548–4553.
40. Zhang, S., Zhou, L., Nemeria, N., Yan, Y., Zhang, Z., Zou, Y., Jordan, F., Evidence for dramatic acceleration of a C-H bond ionization rate in thiamin diphosphate enzymes by the protein environment. Biochemistry 44 (2005), 2237–2243.
41. Zwart, P.H., Afonine, P.V., Grosse-Kunstleve, R.W., Hung, L.W., Ioerger, T.R., McCoy, A.J., McKee, E., Moriarty, N.W., Read, R.J., Sacchettini, J.C., et al. Automated structure solution with the PHENIX suite. Methods Mol. Biol. 426 (2008), 419–435.