Structural insights into the prereaction state of pyruvate decarboxylase from zymomonas mobilise

Biochemistry

Volumn 49, Issue 8, 2010, Pages 1727-1736

  Pei, Xue Yuan ^a   Erixon, Karl M ^a   Luisi, Ben F ^a   Leeper, Finian J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE POCKET; CATALYTIC MECHANISMS; COFACTORS; INHIBITORY EFFECT; PRE-REACTIONS; PYRUVATE DECARBOXYLASE; PYRUVATES; SECOND CRYSTAL; STRUCTURAL INSIGHTS; THIAMINE DIPHOSPHATES; WATER MOLECULE;

ALDEHYDES; BINDING ENERGY; ETHANOL; QUANTUM CHEMISTRY;

CRYSTAL STRUCTURE;

ACETALDEHYDE; COCARBOXYLASE; HALIDE; PYRUVATE DECARBOXYLASE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTALLOGRAPHY; ENZYME MECHANISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; ZYMOMONAS MOBILIS;

BACTERIAL PROTEINS; BINDING SITES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; FLUORIDES; PROTEIN STRUCTURE, SECONDARY; PYRUVATE DECARBOXYLASE; PYRUVIC ACID; ZYMOMONAS;

BACTERIA (MICROORGANISMS); ZYMOMONAS;

EID: 77749255567     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi901864j     Document Type: Article

References (48)

1. Jordan, F. (2003) Current mechanistic understanding of thiamin diphosphate-dependent enzymatic reactions, Nat. Prod. Rep. 20, 184-201.
2. Schellenberger, A. (1998) Sixty years of thiamin diphosphate biochemistry. Biochim. Biophys. Acta 1385, 177-186.
3. Kern, D., Kern, G., Neef, H., Tittmann, K., Killenberg-Jabs, M., Wikner, C., Schneider, G., and Hübner, G. (1997) How Thiamin Diphosphate Is Activated in Enzymes. Science 275, 67-70. (Pubitemid 27020308)
4. Nemeria, N., Korotchkina, L., McLeish, M. J., Kenyon, G. L., Patel, M. S., and Jordan, F. (2007) Elucidation of the Chemistry of EnzymeBound Thiamin Diphosphate Prior to Substrate Binding: Defining Internal Equilibria among Tautomeric and Ionization States. Biochemistry 46, 10739-10744. (Pubitemid 47417266)
5. Nemeria, N., Chakraborty, S., Balakrishnan, A., and Jordan, F. (2009) Reaction mechanisms of thiamin diphosphate enzymes: Defining states of ionization and tautomerization of the cofactor at individual steps. FEBS J. 276, 2432-3446.
6. Lindqvist, Y., Schneider, G., Ermler, U., and Sundström, M. (1992) Three-dimensional structure of transketolase, a thiamine diphosphate dependent enzyme, at 2.5 Å resolution. EMBO J. 2373-2379.
7. Nikkola, M., Lindqvist, Y., and Schneider, G. (1994) Refined Structure of Transketolase from Saccharomyces cerevisiae at 2.0 Å Resolution. J. Biol. 238, 387-1104 (Pubitemid 124001727)
8. Dyda, F., Furey, W., Swaminathan, S., Sax, M., Farrenkopf, B., and Jordan, F. (1993) Catalytic centers in the thiamin diphosphate dependent enzyme pyruvate decarboxylase at 2.4 Å resolution. Biochemistry 32, 6165. (Pubitemid 23196871)
9. Arjunan, P., Umland, T., Dyda, F., Swaminathan, S., Furey, W., Sax, M., Farrenkopf, B., Gao, Y., Zhang, D., and Jordan, F. (1996) Crystal Structure of the Thiamin Diphosphate-dependent Enzyme Pyruvate Decarboxylase from the Yeast Saccharomyces cerevisiae at 2.3 Å Resolution. J. Mol. Biol. 256, 590-600. (Pubitemid 126352693)
10. Dobritzsch, D., König, S., Schneider, G., and Lu, G. (1998) High Resolution Crystal Structure of Pyruvate Decarboxylase from Zymomonas mobilis: Implications for Substrate Activation in Pyruvate Decarboxylases. J. Biol. Chem. 273, 20196-20204. (Pubitemid 28377580)
11. Lu, G., Dobritzsch, D., Baumann, S., Schneider, G., and König, S. (2000) The structural basis of substrate activation in yeast pyruvate decarboxylase: A crystallographic and kinetic study. Eur. J. Biochem. 267, 861-868. (Pubitemid 30082400)
12. Kutter, S., Weiss, M. S., Wille, G., Golbik, R., Spinka, M., and Konig, S. (2009) Covalently Bound Substrate at the Regulatory Site of Yeast Pyruvate Decarboxylases Triggers Allosteric Enzyme Activation. J. Biol. Chem. 284, 12136-12144.
13. óvarsson, A., Seger, K., Turley, S., Sokatch, J. R., and Hol, W. G. J. (1999) Crystal structure of 2-oxoisovalerate and dehydrogenase and the architecture of 2-oxo acid dehydrogenase multienzyme complexes. Nat. Struct. Biol. 6, 785-792.
14. Ciszak, E. M., Korotchkina, L. G., Dominak, P. M., Sidhu, S., and Patel, M. S. (2003) Structural Basis for Flip-Flop Action of Thiamin Pyrophosphate-dependent Enzymes Revealed by Human Pyruvate Dehydrogenase. J. Biol. Chem. 278, 21240-21246. (Pubitemid 36806439)
15. Muller, Y. A., and Schultz, G. E. (1993) Structure of the thiamine- and flavin-dependent enzyme pyruvate oxidase. Science 259, 965-967. (Pubitemid 23080664)
16. Muller, Y. A., Schumacher, G., Rudolph, R., and Schulz, G. E. (1994) The Refined Structures of a Stabilized Mutant and of Wild-type Pyruvate Oxidase from Lactobacillus plantarum. J. Mol. Biol. 237, 315-335.
17. Muller, Y. A., Lindqvist, Y., Furey, W., Schultz, G. E., Jordan, F., and Schneider, G. (1993) A thiamin diphosphate binding fold revealed by comparison of the crystal structures of transketolase, pyruvate oxidase and pyruvate decarboxylase. Structure 1, 95-103. (Pubitemid 223009038)
18. Versees, W., Spaepen, S., Wood, M. D. H., Leeper, F. J., Vanderleyden, J., and Steyaert, J. (2007) Molecular Mechanism of Allosteric Substrate Activation, in a Thiamine Diphosphate-dependent Decarboxylase. J. Biol. Chem. 282, 35269-35278. (Pubitemid 350232435)
19. Sun, S., Duggleby, R. G., and Schowen, R. L (1995) Linkage of Catalysis and Regulation in Enzyme Action. Carbon Isotope Effects, Solvent Isotope Effects, and Proton Inventories for the Unregulated Pyruvate Decarboxylase of Zymomonas mobilis. J. Am. Chem. Soc. 117, 7317-7322.
20. Erixon, K. M., Dabalos, C. L., and Leeper, F. J. (2007) Inhibition of pyruvate decarboxylase from Z. mobilis by novel analogues of thiamine pyrophosphate: Investigating pyrophosphate mimics. Chem. Commun., 960.
21. Erixon, K. M., Dabalos, C. L., and Leeper, F. J. (2008) Synthesis and biological evaluation, of pyrophosphate mimics of thiamine pyrophosphate based on a triazole scaffold, Org. Biomol. Chem. 6, 3561-3572.
22. Mann, S., Perez Melero, C., Hawksley, D., and Leeper, F. J. (2004) Inhibition of thiamin diphosphate dependent enzymes by 3-deazathiamin diphosphate, Biomol. Chem 2, 1732-1741.
23. Jordan, F., Li, H., and Brown, A. (1999) Remarkable Stabilization of Zwitterionic Intermediates May Account for a Billion-fold Rate Acceleration by Thiamin Diphosphate-Dependent Decarboxylases. Biochemistry 38, 6369-6373. (Pubitemid 29242028)
24. Schenk, G., Leeper, F. J., England, R., Nixon, P. F., and Duggleby, R. G. (1997) The Role of His 113 and Hisl 14 in Pyruvate Decarboxylase from Zymomonas mobilis. Eur. J. Biochem. 248, 63-71.
25. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., and Pannu, N. S.; et al. (1998) Crystallography & NMR system.: A new software suite for macromolecular structure determination. Acta Crystallogr. D54, 905-921. (Pubitemid 28443603)
26. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53, 240-255.
27. Emsley, P., and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics, Acta Crystallogr. D60, 2126-2132. (Pubitemid 41742764)
28. Schuettelkopf, A. W., and van Aalten, D. M. F. (2004) PRODRG: A tool for high-throughput crystallography of protein-ligand complexes, Acta Crystallogr. D60, 1355-1363.
29. Bürgi, H. B., Dunitz, J. D., Lehn, J. M., and Wipff, G. (1974) Stereochemistry of Reaction Paths at Carbonyl Centres. Tetrahedron 30, 1563-1572.
30. Diefenbach, R. J., and Duggleby, R. G. (1991) Pyruvate decarboxylase from. Zymomonas mobilis. Structure and re-activation of apoenzyme by the cofactors thiamin diphosphate and magnesium ion. Biochem. J. 276, 439.
31. Sundström, M., Lindqvist, Y., and Schneider, G. (1992) Threedimensional structure of apotransketolase. Flexible loops at the active site enable cofactor binding. FEBS Lett. 313, 229-231.
32. Chandrasekhar, K., Arjunan, P., Sax, M., Nemeria, N., Jordan, F., and Furey, W. (2006) Active-site changes in the pyruvate dehydrogenase multienzyme complex E1 apoenzyme component from Escherichia coli observed at 2.32 Å resolution. Acta Crystallogr. D62, 13821386.
33. Li, J., Wynn, R. M., Machius, M., Chuang, J. L., Karthikeyan, S., Tomchick, D. R, and Chuang, D. T. (2004) Cross-talk between Thiamin Diphosphate Binding and Phosphorylation Loop Conformation in Human Branched-chain a-Keto Acid Decarboxylase/Dehydrogenase. J. Biol. Chem. 279, 32968-32978. (Pubitemid 39014757)
34. Nakai, T., Nakagawa, N., Maoka, N., Masui, R., Kuramitsu, S., and Kamiya, N. (2004) Ligand-induced Conformational Changes and a Reaction Intermediate in Branched-chain 2-Oxo Acid Dehydrogenase (E1) from Thermus thermophilus HB8, as Revealed by X-ray Crystallography. J. Mol. Biol. 337, 1011-1033. (Pubitemid 38368941)
35. Frank, R. A. W., Price, A. J., Northrop, F. D., Perham, R. N., and Luisi, B. F. (2007) Crystal Structure of the El Component of the Escherichia coli 2-Oxoglutarate Dehydrogenase Multienzyme Complex. J. Mol- Biol. 368, 639-651. (Pubitemid 46527607)
36. Asztalos, P., Parthier, C., Golbik, R., Kleinschmidt, M., Hübner, G., Weiss, M. S., Friedemann, R., Wille, G., and Tittmann, K. (2007) Strain and Near Attack Conformera in Enzymic Thiamin Catalysis: X-ray Crystallographic Snapshots of Bacterial Transketolase in Covalent Complex with Donor Ketoses Xylulose 5-phosphate and Fructose 6-phosphate, and in Noncovalent Complex with Acceptor Aldose Ribose 5-phosphate. Biochemistry 46, 1203712052. (Pubitemid 350022361)
37. Arjunan, P., Sax, M., Brunskill, A., Chandrasekhar, K., Nemeria, N., Zhang, S., Jordan, F., and Furey, W. (2006) A thiamin-bound, pre-decarboxylation reaction intermediate analogue in the pyruvate dehydrogenase El subunit induces large scale disorder-toorder transformations in the enzyme and reveals novel structural features in the covalently bound adduct. J. Biol. Chem. 281, 1529615303.
38. Lie, M. A., Celik, L., Jorgensen, K. A., and Schiott, B. (2005) Cofactor activation and substrate binding in pyruvate decarboxylase. Insights into the reaction mechanism from molecular dynamics simulations. Biochemistry 44, 14792-14806. (Pubitemid 41612259)
39. Huang, C. Y., Chang, A. K., Nixon, P. F., and Duggleby, R. G. (2001) Site-directed mutagenesis of the ionizable groups in the active site of Zymomonas mobilis pyruvate decarboxylase: Effect on activity and pH dependence. EM. J. Biochem. 268, 3558-3565.
40. Liu, M., Sergienko, E. A., Guo, F., Wang, J., Tittmann, K., Hübner, G., Furey, W., and Jordan, F. (2001) Catalytic Acid-Base Groups in Yeast Pyruvate Decarboxylase. 1. Site-Directed Mutagenesis and Steady-State Kinetic Studies on the Enzyme with the D28A, H114F, H115F, and E477Q Substitutions. Biochemistry 40, 73557368.
41. Sergienko, E. A., and Jordan, F. (2001) Catalytic Acid-Base Groups in Yeast Pyruvate Decarboxylase. 2. Insights into the Specific Roles of D28 and E477 from, the Rates and Stereospecificity of Formation of Carboligase Side Products. Biochemistry 40, 7369-7381.
42. Lobell, M., and Crout, D. H. G. (1996) Pyruvate Decarboxylase: A Molecular Modeling Study of Pyruvate Decarboxylation and Acyloin Formation. J. Am. Chem. Soc. 118, 1867-1873. (Pubitemid 26100199)
43. Wille, G., Meyer, D., Steinmetz, A., Hinze, E., Golbik, R., and Tittmann, K. (2006) The catalytic cycle of a thiamin diphosphate enzyme examined by cryocrystallography. Nat. Chem. Biol. 2, 324-328. (Pubitemid 43787214)
44. Chang, A. K., Nixon, P. F., and Duggleby, R. G. (1999) Aspartate-27 and glutamate-473 are involved in catalysis by Zymomonas mobilis pyruvate decarboxylase. Biochem. J. 339, 255-260.
45. Tittmann, K., Golbik, R., Uhlemann, K., Khailova, L., Schneider, G., Patel, M., Jordan, F., Chipman, D. M., Duggleby, R. G., and Hübner, G. (2003) NMR Analysis of Covalent Intermediates in Thiamin Diphosphate Enzymes. Biochemistry 42, 7885-7891. (Pubitemid 36807705)
46. Berthold, C. L., Toyota, C. G., Moussatche, P., Wood, M. D., Leeper, F., Richards, N. G. J., and Lindqvist, Y. (2007) Crystallographic Snapshots of Oxalyl-CoA Decarboxylase Give Insights into Catalysis by Nonoxidative ThDP-Dependent Decarboxylases. Structure 15, 853-861. (Pubitemid 47042431)
47. Hasson, M. S., Muscate, A., McLeish, M. J., Polovnikova, L. S., Gerlt, J. A., Kenyon, G. L., Petsko, G. A., and Ringe, D. (1998) The crystal structure of benzoylformate decarboxylase at 1.6 A resolution: Diversity of catalytic residues in thiamin diphosphate-dependent enzymes. Biochemistry 37, 9918-9930. (Pubitemid 28366346)
48. Frank, R. A. W., Titman, C. M., Pratap, J. V., Luisi, B. F., and Perham, R.N. (2004) A molecular switch and proton wire synchronize the active sites in thiamine enzymes. Science 306, 872-876.