Enzymatic catalysis of proton transfer at carbon: Activation of triosephosphate isomerase by phosphite dianion

Biochemistry

Volumn 46, Issue 19, 2007, Pages 5841-5854

  Amyes, Tina L ^a   Richard, John P ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CARBON; CATALYSIS; CONFORMATIONS; ENZYME KINETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

ACTIVE SITE; OXYDIANION; PHOSPHODIANION; TRANSITION STATE;

PROTON TRANSFER;

GLYCERALDEHYDE 3 PHOSPHATE; TRIOSEPHOSPHATE ISOMERASE;

ACCELERATION; ANIMAL TISSUE; ARTICLE; CATALYSIS; ENZYME ACTIVE SITE; ENZYME BINDING; ISOMERIZATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTON TRANSPORT;

ACETALDEHYDE; ANIMALS; ANIONS; DEUTERIUM OXIDE; ENZYME ACTIVATION; GLYCERALDEHYDE 3-PHOSPHATE; KINETICS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHITES; RABBITS; THERMODYNAMICS; TRIOSE-PHOSPHATE ISOMERASE;

EID: 34248548552     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700409b     Document Type: Article

References (93)

1. Gerlt, J. A. (2007) Enzymatic Catalysis of Proton Transfer at Carbon Atoms, in Hydrogen-Transfer Reactions, Volume 3, Biological Aspects I-II (Hynes, J. T., Klinman, J. P., Limbach, H.-H., and Schowen, R. L., Eds.) pp 1107-1137, Wiley-VCH, Weinheim, Germany.
2. Gerlt, J. A., Babbitt, P. C., and Rayment, I. (2005) Divergent evolution in the enolase superfamify: The interplay of mechanism and specificity, Arch. Biochem. Biophys. 433, 59-70.
3. Pollack, R. M. (2004) Enzymatic mechanisms for catalysis of enolization: Ketosteroid isomerase, Bioorg. Chem. 32, 341-353.
4. Kenyon, G. L., Gerlt, J. A., Petsko, G. A., and Kozarich, J. W. (1995) Mandelate Racemase: Structure-Function Studies of a Pseudosymmetric Enzyme, Acc. Chem. Res. 28, 178-186.
5. Amyes, T. L., and Richard, J. P. (2007) Proton Transfer to and from Carbon in Model Systems, in Hydrogen-Transfer Reactions, Volume 3, Biological Aspects 1-11 (Hynes, J. T., Klinman, J. P., Limbach, H.-H., and Schowen, R. L., Eds.) pp 949-973, Wiley-VCH, Weinheim, Germany.
6. Richard, J. P., and Amyes, T. L. (2001) Proton Transfer at Carbon, Curr. Opin. Chem. Biol. 5, 626-633.
7. Gerlt, J. A., and Gassman, P. G. (1993) Understanding the rates of certain enzyme-catalyzed reactions: Proton abstraction from carbon acids, acyl transfer reactions, and displacement reactions of phosphodiesters, Biochemistry 32, 11943-11952.
8. Rieder, S. V., and Rose, I. A. (1959) Mechanism of the triose phosphate isomerase reaction, J. Biol. Chem. 234, 1007-1010.
9. Knowles, J. R. (1991) Enzyme catalysis: Not different, just better, Nature 350, 121-124.
10. Knowles, J. R. (1991) To build an enzyme, Philos. Trans. R. Soc. London, Ser. B 332, 115-121.
11. Knowles, J. R., and Albery, W. J. (1977) Perfection in enzyme catalysis: The energetics of triosephosphate isomerase, Acc. Chem. Res. 10, 105-111.
12. Miller, J. C., and Waley, S. G. (1971) Active center of rabbit muscle triose phosphate isomerase. Site that is labeled by glycidol phosphate, Biochem. J. 123, 163-170.
13. Hartman, F. C. (1971) Haloacetol phosphates. Characterization of the active site of rabbit muscle triose phosphate isomerase, Biochemistry 10, 146-154.
14. De la Mare, S., Coulson, A. F. W., Knowles, J. R., Priddle, J. D., and Offord, R. E. (1972) Active-site labeling of triose phosphate isomerase. Reaction of bromohydroxyacetone phosphate with a unique glutamic acid residue and the migration of the label to tyrosine, Biochem. J. 129, 321-331.
15. Lodi, P. J., and Knowles, J. R. (1991) Neutral imidazole is the electrophile in the reaction catalyzed by triosephosphate isomerase: Structural origins and catalytic implications, Biochemistry 30, 6948-6956.
16. 31P nuclear magnetic resonance, Biochem. J. 179, 607-621.
17. Webb, M. R., Standring, D. N., and Knowles, J. R. (1977) Phosphorus-31 nuclear magnetic resonance of dihydroxyacetone phosphate in the presence of triosephosphate isomerase. The question of nonproductive binding of the substrate hydrate, Biochemistry 16, 2738-2741.
18. Komives, E. A., Chang, L. C., Lolis, E., Tilton, R. F., Petsko, G. A., and Knowles, J. R. (1991) Electrophilic catalysis in triosephosphate isomerase: The role of histidine-95, Biochemistry 30, 3011-3019.
19. Putman, S. J., Coulson, A. F. W., Farley, I. R. T., Riddleston, B., and Knowles, J. R. (1972) Specificity and kinetics of triose phosphate isomerase from chicken muscle, Biochem. J. 129, 301-310.
20. Plaut, B., and Knowles, J. R. (1972) pH-Dependence of the triose phosphate isomerase reaction, Biochem. J. 129, 311-320.
21. Belasco, J. G., Herlihy, J. M., and Knowles, J. R. (1978) Critical ionization states in the reaction catalyzed by triosephosphate isomerase, Biochemistry 17, 2971-2978.
22. a of the active-site carboxyl group, Biochemistry 14, 5274-5279.
23. a 6.0 in triosephosphate isomerase, Biochem. Biophys. Res. Commun. 77, 746-752.
24. 2O, Biochemistry 44, 2622-2631.
25. 2O, Biochemistry 44, 2610-2621.
26. Harris, T. K., Cole, R. N., Comer, F. I., and Mildvan, A. S. (1998) Proton Transfer in the Mechanism of Triosephosphate Isomerase, Biochemistry 37, 16828-16838.
27. Rose, I. A., Fung, W. J., and Warms, J. V. B. (1990) Proton diffusion in the active site of triosephosphate isomerase, Biochemistry 29, 4312-4317.
28. 8-barrel enzymes, Curr. Opin. Chem. Biol. 7, 252-264.
29. Nagano, N., Orengo, C. A., and Thornton, J. M. (2002) One fold with many functions: The evolutionary relationships between TIM barrel families based on their sequences, structures and functions, J. Mol. Biol. 321, 741-765.
30. Wierenga, R. K. (2001) The TIM-barrel fold: A versatile framework for efficient enzymes, FEBS Lett. 492, 193-198.
31. Lodi, P. J., Chang, L. C., Knowles, J. R., and Komives, E. A. (1994) Triosephosphate Isomerase Requires a Positively Charged Active Site: The Role of Lysine-12, Biochemistry 33, 2809-2814.
32. Nickbarg, E. B., Davenport, R. C., Petsko, G. A., and Knowles, J. R. (1988) Triosephosphate isomerase: Removal of a putatively electrophilic histidine residue results in a subtle change in catalytic mechanism, Biochemistry 27, 5948-5960.
33. Straus, D., Raines, R., Kawashima, E., Knowles, J. R., and Gilbert, W. (1985) Active site of triosephosphate isomerase: In vitro mutagenesis and characterization of an altered enzyme, Proc. Natl. Acad. Sci. U.S.A. 82, 2272-2276.
34. Alber, T., Banner, D. W., Bloomer, A. C., Petsko, G. A., Phillips, D., Rivers, P. S., and Wilson, I. A. (1981) On the three-dimensional structure and catalytic mechanism of triose phosphate isomerase, Philos. Trans. R. Soc. London, Ser. B 293, 159-171.
35. Lolis, E., Alber, T., Davenport, R. C., Rose, D., Hartman, F. C., and Petsko, G. A. (1990) Structure of yeast triosephosphate isomerase at 1.9-Å resolution, Biochemistry 29, 6609-6618.
36. Lolis, E., and Petsko, G. A. (1990) Crystallographic analysis of the complex between triosephosphate isomerase and 2-phosphoglycolate at 2.5-Å resolution: Implications for catalysis, Biochemistry 29, 6619-6625.
37. Davenport, R. C., Bash, P. A., Seaton, B. A., Karplus, M., Petsko, G. A., and Ringe, D. (1991) Structure of the triosephosphate isomerase- phosphoglycolohydroxamate complex: An analog of the intermediate on the reaction pathway, Biochemistry 30, 5821-5826.
38. Noble, M. E. M., Wierenga, R. K., Lambeir, A. M., Opperdoes, F. R., Thunnissen, A. M. W. H., Kalk, K. H., Groendijk, H., and Hol, W. G. J. (1991) The adaptability of the active site of trypanosomal triosephosphate isomerase as observed in the crystal structures of three different complexes, Proteins: Struct., Funct., Genet. 10, 50-69.
39. Wierenga, R. K., Noble, M. E. M., Vriend, G., Nauche, S., and Hol, W. G. J. (1991) Refined 1.83 Å structure of trypanosomal triosephosphate isomerase crystallized in the presence of 2.4 M ammonium sulfate. A comparison with the structure of the trypanosomal triosephosphate isomerase-glycerol-3- phosphate complex, J. Mol. Biol. 220, 995-1015.
40. Wierenga, R. K., Borchert, T. V., and Noble, M. E. M. (1992) Crystallographic binding studies with triosephosphate isomerases: Conformational changes induced by substrate and substrate analogs, FEBS Lett. 307, 34-39.
41. Wierenga, R. K., Noble, M. E. M., and Davenport, R. C. (1992) Comparison of the refined crystal structures of liganded and unliganded chicken, yeast and trypanosomal triosephosphate isomerase, J. Mol. Biol. 224, 1115-1126.
42. Zhang, Z., Sugio, S., Komives, E. A., Liu, K. D., Knowles, J. R., Petsko, G. A., and Ringe, D. (1994) Crystal Structure of Recombinant Chicken Triosephosphate Isomerase-Phosphoglycolohydroxamate Complex at 1.8-Å Resolution, Biochemistry 33, 2830-2837.
43. Jogl, G., Rozovsky, S., McDermott, A. E., and Tong, L. (2003) Optimal alignment for enzymatic proton transfer: Structure of the Michaelis complex of triosephosphate isomerase at 1.2 Å resolution, Proc. Natl. Acad. Sci. U.S.A. 100, 50-55.
44. Kursula, I., and Wierenga, R. K. (2003) Crystal structure of triosephosphate isomerase complexed with 2-phosphoglycolate at 0.83-Å resolution, J. Biol. Chem. 278, 9544-9551.
45. Noble, M. E. M., 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: Struct., Funct., Genet. 16, 311-326.
46. Pompliano, D. L., Peyman, A., and Knowles, J. R. (1990) Stabilization of a reaction intermediate as a catalytic device: Definition of the functional role of the flexible loop in triosephosphate isomerase, Biochemistry 29, 3186-3194.
47. Sampson, N. S., and Knowles, J. R. (1992) Segmental movement: Definition of the structural requirements for loop closure in catalysis by triosephosphate isomerase, Biochemistry 31, 8482-8487.
48. Sampson, N. S., and Knowles, J. R. (1992) Segmental motion in catalysis: Investigation of a hydrogen bond critical for loop closure in the reaction of triosephosphate isomerase, Biochemistry 31, 8488-8494.
49. Sun, J., and Sampson, N. S. (1999) Understanding Protein Lids: Kinetic Analysis of Active Hinge Mutants in Triosephosphate Isomerase, Biochemistry 38, 11474-11481.
50. Xiang, J., Sun, J., and Sampson, N. S. (2001) The Importance of Hinge Sequence for Loop Function and Catalytic Activity in the Reaction Catalyzed by Triosephosphate Isomerase, J. Mol. Biol. 307, 1103-1112.
51. Xiang, J., Jung, J.-y., and Sampson, N. S. (2004) Entropy effects on protein hinges: The reaction catalyzed by triosephosphate isomerase, Biochemistry 43, 11436-11445.
52. Massi, F., Wang, C., and Palmer, A. G., III (2006) Solution NMR and computer simulation studies of active site loop motion in triosephosphate isomerase, Biochemistry 45, 10787-10794.
53. Kurkcuoglu, O., Jemigan, R. L., and Doruker, P. (2006) Loop motions of triosephosphate isomerase observed with elastic networks, Biochemistry 45, 1173-1182.
54. Guallar, V., Jacobson, M., McDermott, A., and Friesner, R. A. (2004) Computational Modeling of the Catalytic Reaction in Triosephosphate Isomerase, J. Mol. Biol. 337, 227-239.
55. Derreumaux, P., and Schlick, T. (1998) The loop opening/closing motion of the enzyme triosephosphate isomerase, Biophys. J. 74, 72-81.
56. Joseph, D., Petsko, G. A., and Karplus, M. (1990) Anatomy of a conformational change: Hinged "lid" motion of the triosephosphate isomerase loop, Science 249, 1425-1428.
57. Rozovsky, S., Jogl, G., Tong, L., and McDermott, A. E. (2001) Solution-state NMR investigations of triosephosphate isomerase active site loop motion: Ligand release in relation to active site loop dynamics, J. Mol. Biol. 310, 271-280.
58. Rozovsky, S., and McDermott, A. E. (2001) The time scale of the catalytic loop motion in triosephosphate isomerase, J. Mol. Biol. 310, 259-270.
59. Desamero, R., Rozovsky, S., Zhadin, N., McDermott, A., and Callender, R. (2003) Active Site Loop Motion in Triosephosphate Isomerase: T-Jump Relaxation Spectroscopy of Thermal Activation, Biochemistry 42, 2941-2951.
60. Norledge, B. V., Lambeir, A. M., Abagyan, R. A., Rottmann, A., Fernandez, A. M., Filimonov, V. V., Peter, M. G., and Wierenga, R. K. (2001) Modeling, mutagenesis, and structural studies on the fully conserved phosphate-binding loop (loop 8) of triose-phosphate isomerase: Toward a new substrate specificity, Proteins: Struct., Funct., Genet. 42, 383-389.
61. Richard, J. P. (1984) Acid-base catalysis of the elimination and isomerization reactions of triose phosphates, J. Am. Chem. Soc. 106, 4926-4936.
62. 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.
63. Collins, G. C. S., and George, W. O. (1971) Nuclear Magnetic Resonance Spectra of Glycolaldehyde, J. Chem. Soc. B, 1352-1355.
64. Glushonok, G. K., Petryaev, E. P., Turetskaya, E. A., and Shadyro, O. I. (1986) Equilibrium between the Molecular Forms of Glycolaldehyde and DL-Glyceraldehyde in Aqueous Solutions, Russ. J. Phys. Chem. 60, 1788-1794.
65. Glasoe, P. K., and Long, F. A. (1960) Use of glass electrodes to measure acidities in deuterium oxide, J. Phys. Chem. 64, 188-190.
66. Krietsch, W. K. G., Pentchev, P. G., Klingenbuerg, H., Hofstaetter, T., and Buecher, T. (1970) Isolation and crystallization of yeast and rabbit liver triose phosphate isomerase and a comparative characterization with the rabbit muscle enzyme, Eur. J. Biochem. 14, 289-300.
67. Raiford, D. S., Fisk, C. L., and Becker, E. D. (1979) Calibration of methanol and ethylene glycol nuclear magnetic resonance thermometers, Anal. Chem. 51, 2050-2051.
68. Nagorski, R. W., and Richard, J. P. (2001) Mechanistic Imperatives for Aldose-Ketose Isomerization in Water: Specific, General Base-and Metal Ion-Catalyzed Isomerization of Glyceraldehyde with Proton and Hydride Transfer, J. Am. Chem. Soc. 123, 794-802.
69. Nagorski, R. W., and Richard, J. P. (1996) Mechanistic Imperatives for Enzymatic Catalysis of Aldose-Ketose Isomerization: Isomerization of Glyceraldehyde in Weakly Alkaline Solution Occurs with Intramolecular Transfer of a Hydride Ion, J. Am. Chem. Soc. 118, 7432-7433.
70. 2+ and Acetic Acid as Catalysts of Enolization: Imperatives for Enzymatic Catalysis of Proton Transfer at Carbon, J. Am. Chem. Soc. 126, 5164-5173.
71. Johnson, L. N., and Wolfenden, R. (1970) Changes in absorption spectrum and crystal structure of triose phosphate isomerase brought about by 2-phosphoglycollate, a potential transition state analog, J. Mol. Biol. 47, 93-100.
72. Davis, L. (1973) Structure of dihydroxyacetone in solution, Bioorg. Chem. 2, 197-201.
73. 13C NMR and UV Study of the State of Hydroxyacetone in Aqueous Solutions, Russ. J. Gen. Chem. 73, 1027-1031.
74. Glomb, M. A., and Monnier, V. M. (1995) Mechanism of protein modification by glyoxal and glycolaldehyde, reactive intermediates of the Maillard reaction, J. Biol. Chem. 270, 10017-10026.
75. Thornalley, P. J., Langborg, A., and Minhas, H. S. (1999) Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose, Biochem. J. 344, 109-116.
76. Jencks, W. P. (1981) On the attribution and additivity of binding energies, Proc. Natl. Acad. Sci. U.S.A. 78, 4046-4050.
77. Jencks, W. P. (1987) Economics of enzyme catalysis, Cold Spring Harbor Symp. Quant. Biol. 52, 65-73.
78. Kursula, I., Partanen, S., Lambeir, A.-M., Antonov, D. M., Augustyns, K., and Wierenga, R. K. (2001) Structural determinants for ligand binding and catalysis of triosephosphate isomerase, Eur. J. Biochem. 268, 5189-5196.
79. Verlinde, C. L. M. J., Noble, M. E. M., Kalk, K. H., Groendijk, H., Wierenga, R. K., and Hoi, W. G. J. (1991) Anion binding at the active site of trypanosomal triosephosphate isomerase. Monohydrogen phosphate does not mimic sulfate, Eur. J. Biochem. 198, 53-57.
80. Campbell, I. D., Jones, R. B., Kiener, P. A., Richards, E., Waley, S. C., and Wolfenden, R. (1978) The form of 2-phosphoglycollic acid bound by triosephosphate isomerase, Biochem. Biophys. Res. Commun. 83, 347-352.
81. Richard, J. P. (1998) The Enhancement of Enzymic Rate Accelerations by Brønsted Acid-Base Catalysis, Biochemistry 37, 4305-4309.
82. Richard, J. P., and Amyes, T. L. (2004) On the importance of being zwitterionic: Enzymic catalysis of decarboxylation and deprotonation of cationic carbon, Bioorg. Chem. 32, 354-366.
83. Jencks, W. P. (1975) Binding Energy, Specificity and Enzymic Catalysis: The Circe Effect, Adv. Enzymol. Relat. Areas Mol. Biol. 43, 219-410.
84. 3 transfer process in the phosphoglucomutase reaction, Biochemistry 15, 3993-4006.
85. Ray, W. J., Jr., Long, J. W., and Owens, J. D. (1976) An analysis of the substrate-induced rate effect in the phosphoglucomutase system, Biochemistry 15, 4006-4017.
86. Page, M. I., and Jencks, W. P. (1971) Entropic contributions to rate accelerations in enzymic and intramolecular reactions and the chelate effect, Proc. Natl. Acad. Sci. U.S.A. 68, 1678-1683.
87. 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.
88. L-gulonate 6-Phosphate Decarboxylase, Biochemistry 41, 3861-3869.
89. Gerlt, J. A., and Babbitt, P. C. (2001) Divergent evolution of enzymatic function: Mechanistically diverse superfamilies and functionally distinct suprafamilies, Annu. Rev. Biochem. 70, 209-246.
90. Begley, T. P., Appleby, T. C., and Ealick, S. E. (2000) The structural basis for the remarkable catalytic proficiency of orotidine 5'-monophosphate decarboxylase, Curr. Opin. Struct. Biol. 10, 711-718.
91. Miller, B. G., Hassell, A. M., Wolfenden, R., Milbum, M. V., and Short, S. A. (2000) Anatomy of a proficient enzyme: The structure of orotidine 5′-monophosphate decarboxylase in the presence and absence of a potential transition state analog, Proc. Natl. Acad. Sci. U.S.A. 97, 2011-2016.
92. Radzicka, A., and Wolfenden, R. (1995) A proficient enzyme, Science 267, 90-93.
93. Jones, J. M., and Bender, M. L. (1960) Secondary deuterium isotope effects in the addition equilibria of ketones, J. Am. Chem. Soc. 82, 6322-6326