Modification of residue 42 of the active site loop with a lysine-mimetic side chain rescues isochorismate-pyruvate lyase activity in Pseudomonas aeruginosa PchB

Biochemistry

Volumn 51, Issue 38, 2012, Pages 7525-7532

  Olucha, José ^a   Meneely, Kathleen M ^a   Lamb, Audrey L ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; CATALYTIC POWER; CHEMICAL RESCUE; EFFICIENT PRODUCTION; ELECTROSTATIC EFFECT; ETHYLAMINE; FREE ENERGY OF ACTIVATIONS; ISOSTERIC; LOOP CLOSURE; LYASE ACTIVITY; LYSINE RESIDUES; POSITIVE CHARGES; POSITIVELY CHARGED; PROPYLAMINES; PSEUDOMONAS AERUGINOSA; SIDE-CHAINS; STERIC EFFECT; TRANSITION STATE STABILIZATION; TRANSITION-STATE;

BACTERIA; CONFORMATIONS; FREE ENERGY; HYDROGEN BONDS; STABILIZATION;

AMINO ACIDS;

ALIPHATIC AMINE; BACTERIAL ENZYME; ETHYLAMINE; LYASE; LYSINE; MUTANT PROTEIN; PCHB PROTEIN; PROPYLAMINE; PROTEIN VARIANT; SALICYLIC ACID; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; CIRCULAR DICHROISM; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME KINETICS; HYDROGEN BOND; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PSEUDOMONAS AERUGINOSA; WILD TYPE;

BASE SEQUENCE; CARBON-OXYGEN LYASES; CATALYSIS; CATALYTIC DOMAIN; CIRCULAR DICHROISM; DNA PRIMERS; KINETICS; LYSINE; MODELS, MOLECULAR; MOLECULAR MIMICRY; PSEUDOMONAS AERUGINOSA; THERMODYNAMICS;

PSEUDOMONAS AERUGINOSA;

EID: 84866645497     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300472n     Document Type: Article

References (52)

1. Peracchi, A. (2008) How (and why?) to revivie a dead enzyme: The power of chemical rescue Curr. Chem. Biol. 2, 32-49
2. Toney, M. D. and Kirsch, J. F. (1989) Direct Bronsted analysis of the restoration of activity to a mutant enzyme by exogenous amines Science 243, 1485-1488
3. Toney, M. D. and Kirsch, J. F. (1992) Bronsted analysis of aspartate aminotransferase via exogenous catalysis of reactions of an inactive mutant Protein Sci. 1, 107-119
4. Arnett, S. O., Gerratana, B., and Townsend, C. A. (2007) Rate-limiting steps and role of active site Lys443 in the mechanism of carbapenam synthetase Biochemistry 46, 9337-9345
5. Harpel, M. R. and Hartman, F. C. (1994) Chemical rescue by exogenous amines of a site-directed mutant of ribulose 1,5-bisphosphate carboxylase/oxygenase that lacks a key lysyl residue Biochemistry 33, 5553-5561
6. Jiang, W., Locke, G., Harpel, M. R., Copeland, R. A., and Marcinkeviciene, J. (2000) Role of Lys100 in human dihydroorotate dehydrogenase: Mutagenesis studies and chemical rescue by external amines Biochemistry 39, 7990-7997
7. Zheng, R. and Blanchard, J. S. (2000) Identification of active site residues in E. coli ketopantoate reductase by mutagenesis and chemical rescue Biochemistry 39, 16244-16251
8. Boehlein, S. K., Walworth, E. S., Richards, N. G., and Schuster, S. M. (1997) Mutagenesis and chemical rescue indicate residues involved in beta-aspartyl-AMP formation by Escherichia coli asparagine synthetase B J. Biol. Chem. 272, 12384-12392
9. Muratore, K. E., Seeliger, M. A., Wang, Z., Fomina, D., Neiswinger, J., Havranek, J. J., Baker, D., Kuriyan, J., and Cole, P. A. (2009) Comparative analysis of mutant tyrosine kinase chemical rescue Biochemistry 48, 3378-3386
10. Phillips, M. A., Hedstrom, L., and Rutter, W. J. (1992) Guanidine derivatives restore activity to carboxypeptidase lacking arginine-127 Protein Sci. 1, 517-521
11. Qiao, Y., Molina, H., Pandey, A., Zhang, J., and Cole, P. A. (2006) Chemical rescue of a mutant enzyme in living cells Science 311, 1293-1297
12. Rynkiewicz, M. J. and Seaton, B. A. (1996) Chemical rescue by guanidine derivatives of an arginine-substituted site-directed mutant of Escherichia coli ornithine transcarbamylase Biochemistry 35, 16174-16179
13. Williams, D. M., Wang, D., and Cole, P. A. (2000) Chemical rescue of a mutant protein-tyrosine kinase J. Biol. Chem. 275, 38127-38130
14. Barrick, D. (1994) Replacement of the proximal ligand of sperm whale myoglobin with free imidazole in the mutant His-93→Gly Biochemistry 33, 6546-6554
15. Maupin, C. M., Castillo, N., Taraphder, S., Tu, C., McKenna, R., Silverman, D. N., and Voth, G. A. (2011) Chemical rescue of enzymes: Proton transfer in mutants of human carbonic anhydrase II J. Am. Chem. Soc. 133, 6223-6234
16. Newmyer, S. L. and de Montellano, P. R. (1996) Rescue of the catalytic activity of an H42A mutant of horseradish peroxidase by exogenous imidazoles J. Biol. Chem. 271, 14891-14896
17. Tu, C. K., Silverman, D. N., Forsman, C., Jonsson, B. H., and Lindskog, S. (1989) Role of histidine 64 in the catalytic mechanism of human carbonic anhydrase II studied with a site-specific mutant Biochemistry 28, 7913-7918
18. Perona, J. J., Hedstrom, L., Wagner, R. L., Rutter, W. J., Craik, C. S., and Fletterick, R. J. (1994) Exogenous acetate reconstitutes the enzymatic activity of trypsin Asp189Ser Biochemistry 33, 3252-3259
19. Pond, A. E., Roach, M. P., Thomas, M. R., Boxer, S. G., and Dawson, J. H. (2000) The H93G myoglobin cavity mutant as a versatile template for modeling heme proteins: Ferrous, ferric, and ferryl mixed-ligand complexes with imidazole in the cavity Inorg. Chem. 39, 6061-6066
20. Highbarger, L. A., Gerlt, J. A., and Kenyon, G. L. (1996) Mechanism of the reaction catalyzed by acetoacetate decarboxylase. Importance of lysine 116 in determining the pKa of active-site lysine 115 Biochemistry 35, 41-46
21. Hopkins, C. E., O'Connor, P. B., Allen, K. N., Costello, C. E., and Tolan, D. R. (2002) Chemical-modification rescue assessed by mass spectrometry demonstrates that gamma-thia-lysine yields the same activity as lysine in aldolase Protein Sci. 11, 1591-1599
22. Dhalla, A. M., Li, B., Alibhai, M. F., Yost, K. J., Hemmingsen, J. M., Atkins, W. M., Schineller, J., and Villafranca, J. J. (1994) Regeneration of catalytic activity of glutamine synthetase mutants by chemical activation: Exploration of the role of arginines 339 and 359 in activity Protein Sci. 3, 476-481
23. Colleluori, D. M., Reczkowski, R. S., Emig, F. A., Cama, E., Cox, J. D., Scolnick, L. R., Compher, K., Jude, K., Han, S., Viola, R. E., Christianson, D. W., and Ash, D. E. (2005) Probing the role of the hyper-reactive histidine residue of arginase Arch. Biochem. Biophys. 444, 15-26
24. Kim, D. W., Yoshimura, T., Esaki, N., Satoh, E., and Soda, K. (1994) Studies of the active-site lysyl residue of thermostable aspartate aminotransferase: Combination of site-directed mutagenesis and chemical modification J. Biochem. 115, 93-97
25. Planas, A. and Kirsch, J. F. (1991) Reengineering the catalytic lysine of aspartate aminotransferase by chemical elaboration of a genetically introduced cysteine Biochemistry 30, 8268-8276
26. Zaitseva, J., Lu, J., Olechoski, K. L., and Lamb, A. L. (2006) Two crystal structures of the isochorismate pyruvate lyase from Pseudomonas aeruginosa J. Biol. Chem. 281, 33441-33449
27. Gaille, C., Kast, P., and Haas, D. (2002) Salicylate biosynthesis in Pseudomonas aeruginosa. Purification and characterization of PchB, a novel bifunctional enzyme displaying isochorismate pyruvate-lyase and chorismate mutase activities J. Biol. Chem. 277, 21768-21775
28. Luo, Q., Olucha, J., and Lamb, A. L. (2009) Structure-function analyses of isochorismate-pyruvate lyase from Pseudomonas aeruginosa suggest differing catalytic mechanisms for the two pericyclic reactions of this bifunctional enzyme Biochemistry 48, 5239-5245
29. Gustin, D. J., Mattei, P., Kast, P., Wiest, O., Lee, L., Cleland, W. W., and Hilvert, D. (1999) Heavy atom isotope effects reveal a highly polarized transition state for chorismate mutase J. Am. Chem. Soc. 121, 1756-1757
30. DeClue, M. S., Baldridge, K. K., Kunzler, D. E., Kast, P., and Hilvert, D. (2005) Isochorismate pyruvate lyase: A pericyclic reaction mechanism? J. Am. Chem. Soc. 127, 15002-15003
31. Marti, S., Andres, J., Moliner, V., Silla, E., Tunon, I., and Bertran, J. (2009) Mechanism and plasticity of isochorismate pyruvate lyase: A computational study J. Am. Chem. Soc. 131, 16156-16161
32. Olucha, J., Ouellette, A. N., Luo, Q., and Lamb, A. L. (2011) pH dependence of catalysis by Pseudomonas aeruginosa isochorismate-pyruvate lyase: Implications for transition state stabilization and the role of lysine 42 Biochemistry 50, 7198-7207
33. Luo, Q., Meneely, K. M., and Lamb, A. L. (2011) Entropic and enthalpic components of catalysis in the mutase and lyase activities of Pseudomonas aeruginosa PchB J. Am. Chem. Soc. 133, 7229-7233
34. Chook, Y. M., Gray, J. V., Ke, H., and Lipscomb, W. N. (1994) The monofunctional chorismate mutase from Bacillus subtilis. Structure determination of chorismate mutase and its complexes with a transition state analog and prephenate, and implications for the mechanism of the enzymatic reaction J. Mol. Biol. 240, 476-500
35. Chook, Y. M., Ke, H., and Lipscomb, W. N. (1993) Crystal structures of the monofunctional chorismate mutase from Bacillus subtilis and its complex with a transition state analog Proc. Natl. Acad. Sci. U.S.A. 90, 8600-8603
36. Kast, P., Asif-Ullah, M., Jiang, N., and Hilvert, D. (1996) Exploring the active site of chorismate mutase by combinatorial mutagenesis and selection: The importance of electrostatic catalysis Proc. Natl. Acad. Sci. U.S.A. 93, 5043-5048
37. Kast, P., Grisostomi, C., Chen, I. A., Li, S., Krengel, U., Xue, Y., and Hilvert, D. (2000) A strategically positioned cation is crucial for efficient catalysis by chorismate mutase J. Biol. Chem. 275, 36832-36838
38. Lee, A. Y., Karplus, P. A., Ganem, B., and Clardy, J. (1995) Atomic structure of the buried catalytic pocket of Escherichia coli chorismate mutase J. Am. Chem. Soc. 117, 3627-3628
39. Lee, A. Y., Stewart, J. D., Clardy, J., and Ganem, B. (1995) New insight into the catalytic mechanism of chorismate mutases from structural studies Chem. Biol. 2, 195-203
40. Liu, D. R., Cload, S. T., Pastor, R. M., and Schultz, P. G. (1996) Analysis of active site residues in Escherichia coli chorismate mutase by site-directed mutagenesis J. Am. Chem. Soc. 118, 1789-1790
41. Zhang, S., Kongsaeree, P., Clardy, J., Wilson, D. B., and Ganem, B. (1996) Site-directed mutagenesis of monofunctional chorismate mutase engineered from the E. coli P-protein Bioorg. Med. Chem. 4, 1015-1020
42. Hur, S. and Bruice, T. C. (2002) The mechanism of catalysis of the chorismate to prephenate reaction by the Escherichia coli mutase enzyme Proc. Natl. Acad. Sci. U.S.A. 99, 1176-1181
43. Hur, S. and Bruice, T. C. (2003) The near attack conformation approach to the study of the chorismate to prephenate reaction Proc. Natl. Acad. Sci. U.S.A. 100, 12015-12020
44. Hur, S. and Bruice, T. C. (2003) Just a near attack conformer for catalysis (chorismate to prephenate rearrangements in water, antibody, enzymes, and their mutants) J. Am. Chem. Soc. 125, 10540-10542
45. Hur, S. and Bruice, T. C. (2003) Comparison of formation of reactive conformers (NACs) for the Claisen rearrangement of chorismate to prephenate in water and in the E. coli mutase: The efficiency of the enzyme catalysis J. Am. Chem. Soc. 125, 5964-5972
46. Zhang, X., Zhang, X., and Bruice, T. C. (2005) A definitive mechanism for chorismate mutase Biochemistry 44, 10443-10448
47. Sedlak, J. and Lindsay, R. H. (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent Anal. Biochem. 25, 192-205
48. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., WIlkinds, M. R., Appel, R. D., and Bairoch, A. (2005) Protein identification and analysis tools on the ExPASy server, in The Proteomics Protocols Handook (Walker, J. M., Ed.), pp 571-607, Humana Press, Totowa, NJ.
49. Taylor, R. A. (1982) An Introduction to Error Analysis, University Science Books, Mill Valley, CA.
50. Go, M. K., Amyes, T. L., and Richard, J. P. (2010) Rescue of K12G triosephosphate isomerase by ammonium cations: the reaction of an enzyme in pieces J. Am. Chem. Soc. 132, 13525-13532
51. Barnett, S. A., Amyes, T. L., Wood, B. M., Gerlt, J. A., and Richard, J. P. (2010) Activation of R235A mutant orotidine 5′-monophosphate decarboxylase by the guanidinium cation: effective molarity of the cationic side chain of Arg-235 Biochemistry 49, 824-826
52. DeLano, W. (2002) The PyMOL Molecular Graphics System, www.pymol.org, DeLano Scientific, San Carlos, CA.