Stability for function trade-offs in the enolase superfamily "catalytic module"

Biochemistry

Volumn 46, Issue 23, 2007, Pages 6688-6695

  Nagatani, Ray A ^a   Gonzalez, Ana ^c   Shoichet, Brian K ^a   Brinen, Linda S ^a,b   Babbitt, Patricia C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT ENZYMES; PARTIAL REACTION; TRANSITION STATES;

ENZYMES; ESCHERICHIA COLI; FUNCTIONAL GROUPS; PROTEINS; STABILITY;

CATALYSIS;

2 SUCCINYLBENZOATE SYNTHASE; BENZOIC ACID DERIVATIVE; ENOLASE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; ENZYME ACTIVE SITE; ESCHERICHIA COLI; MOLECULAR DYNAMICS; MUTANT; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REACTION ANALYSIS; WILD TYPE;

AMINO ACID SUBSTITUTION; BINDING SITES; CALORIMETRY; CATALYSIS; ENZYME STABILITY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHOSPHOPYRUVATE HYDRATASE; PROTEIN CONFORMATION; PROTEIN DENATURATION; RECOMBINANT PROTEINS;

ESCHERICHIA COLI;

EID: 34250181697     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700507d     Document Type: Article

References (47)

1. Beadle, B. M., and Shoichet, B. K. (2002) Structural bases of stability-function tradeoffs in enzymes. J. Mol. Biol. 321, 285-296.
2. Benkovic, S. J., and Hammes-Schiffer, S. (2003) A perspective on enzyme catalysis. Science 301, 1196-1202.
3. Shoichet, B. K., Baase, W. A., Kuroki, R., and Matthews, B. W. (1995) A relationship between protein stability and protein function, Proc. Natl. Acad. Sci. U.S.A. 92, 452-456.
4. Wang, X., Minasov, G., and Shoichet, B. K. (2002) Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs. J. Mol. Biol. 320, 85-95.
5. Meiering, E. M., Serrano, L., and Fersht, A. R. (1992) Effect of active site residues in barnase on activity and stability, J. Mol. Biol. 225, 585-589.
6. Schreiber, G., Buckle, A. M., and Fersht, A. R. (1994) Stability and function: Two constraints in the evolution of barstar and other proteins. Structure 2, 945-951.
7. Bershtein, S., Segal, M., Bekerman, R., Tokuriki, N., and Tawfik, D. S. (2006) Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein. Nature 444, 929-932.
8. Besenmatter, W., Kast, P., and Hilvert, D. (2004) New enzymes from combinatorial library modules, Methods Enzymol. 388, 91-102.
9. Bloom, J. D., Labthavikul, S. T., Otey, C. R., and Arnold, F. H. (2006) Protein stability promotes evolvability, Proc. Natl. Acad. Sci. U.S.A. 103, 5869-5874.
10. Dodson, G., and Wlodawer, A. (1998) Catalytic triads and their relatives. Trends Biochem. Sci. 23, 347-352.
11. 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.
12. Elcock, A. H. (2001) Prediction of functionally important residues based solely on the computed energetics of protein structure. J. Mol. Biol. 312, 885-896.
13. Livesay, D. R., Jambeck, P., Rojnuckarin, A., and Subramaniam, S. (2003) Conservation of electrostatic properties within enzyme families and superfamilies. Biochemistry 42, 3464-3473.
14. Livesay, D. R., and La, D. (2005) The evolutionary origins and catalytic importance of conserved electrostatic networks within TIM-barrel proteins. Protein Sci. 14, 1158-1170.
15. Gerlt, J. A., Babbitt, P. C. and Rayment, I. (2005) Divergent evolution in the enolase superfamily: The interplay of mechanism and specificity. Arch. Biochem. Biophys. 433, 59-70.
16. Babbitt, P. C. Mrachko, G. T., Hasson, M. S., Huisman, G. W., Kolter, R., Ringe, D., Petsko, G. A., Kenyon, G. L., and Gerlt, J. A. (1995) A functionally diverse enzyme superfamily that abstracts the α protons of carboxylic acids, Science 267, 1159-1161.
17. Babbitt, P. C. Hasson, M. S., Wedekind, J. E., Palmer, D. R., Barrett, W. C., Reed, G. H., Rayment, I., Ringe, D., Kenyon, G. L., and Gerlt, J. A. (1996) The enolase superfamily: A general strategy for enzyme-catalyzed abstraction of the α-protons of carboxylic acids, Biochemistry 35, 16489-16501.
18. Esaki, N., and Walsh, C. T. (1986) Biosynthetic alanine racemase of Salmonella typhimurium: Purification and characterization of the enzyme encoded by the air gene. Biochemistry 25, 3261-3267.
19. Glavas, S., and Tanner, M. E. (1999) Catalytic acid/base residues of glutamate racemase. Biochemistry 38, 4106-4113.
20. Herron, S. R., Benen, J. A., Scavetta, R. D., Visser, J., and Jurnak, F. (2000) Structure and function of pectic enzymes: Virulence factors of plant pathogens. Proc. Natl. Acad. Sci. U.S.A. 97, 8762-8769.
21. Scavetta, R. D., Herron, S. R., Hotchkiss, A. T., Kita, N., Keen, N. T., Benen, J. A., Kester, H. C., Visser, J., and Jurnak, F. (1999) Structure of a plant cell wall fragment complexed to pectate lyase C, Plant Cell 11, 1081-1092.
22. Sharma, V., Meganathan, R., and Hudspeth, M. E. (1993) Menaquinone (vitamin K2) biosynthesis: Cloning, nucleotide sequence, and expression of the menC gene from Escherichia coli, J. Bacteriol. 175, 4917-4921.
23. Klenchin, V. A., Taylor Ringia, E. A., Gerlt, J. A., and Rayment, I. (2003) Evolution of enzymatic activity in the enolase superfamily: Structural and mutagenic studies of the mechanism of the reaction catalyzed by o-succinylbenzoate synthase from Escherichia coli, Biochemistry 42, 14427-14433.
24. Rieger, C. E., and Turnbull, J. L. (1996) Small scale biosynthesis and purification of gram quantities of chorismic acid, Prep. Biochem. Biotechnol. 26, 67-76.
25. Palmer, D. R., Garrett, J. B., Sharma, V., Meganathan, R., Babbitt, P. C., and Gerlt, J. A. (1999) Unexpected divergence of enzyme function and sequence: "N-Acylamino acid racemase" is o-succinylbenzoate synthase, Biochemistry 38, 4252-4258.
26. Popp, J. L., Berliner, C., and Bentley, R. (1989) Vitamin K (menaquinone) biosynthesis in bacteria: High-performance liquid chromatographic assay of the overall synthesis of o-succinylbenzoic acid and of 2-succinyl-6-hydroxy-2,4- cyclohexadiene-1-carboxylic acid synthase. Anal. Biochem. 178, 306-310.
27. Kirchhoff, W. (1993) National Institute of Standards and Technology Technical Note 1401, U.S. Department of Commerce Technology Administration, Washington, DC.
28. Becktel, W. J., and Schellman, J. A. (1987) Protein stability curves, Biopolymers 26, 1859-1877.
29. Leslie, A. G. W. (1992) Recent changes to the MOSFLM package for processing film and image plate data, Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography 26.
30. Collaborative Computational Project Number 4 (1994) The CCP4 Suite: Programs for Protein Crystallography, Acta Crystallogr. D50, 760-763.
31. Vagin, A., and Teplyakov, A. (1997) MOLREP: An automated program for molecular replacement, J. Appl. Crystallogr. 30, 1022-1025.
32. 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.
33. Perrakis, A., Morris, R., and Lamzin, V. S. (1999) Automated protein model building combined with iterative structure refinement, Nat. Struct. Biol. 6, 458-463.
34. Emsley, P., and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D60, 2126-2132.
35. Winn, M. D., Isupov, M. N., and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D57, 122-133.
36. Kanzaki, H., McPhie, P., and Miles, E. W. (1991) Effect of single amino acid substitutions at positions 49 and 60 on the thermal unfolding of the tryptophan synthase α subunit from Salmonella typhimurium. Arch. Biochem. Biophys. 284, 174-180.
37. Dill, K. A., Alonso, D. O., and Hutchinson, K. (1989) Thermal stabilities of globular proteins. Biochemistry 28, 5439-5449.
38. Pantoliano, M. W., Whitlow, M., Wood, J. F., Dodd, S. W., Hardman, K. D., Rollence, M. L., and Bryan, P. N. (1989) Large increases in general stability for subtilisin BPN′ through incremental changes in the free energy of unfolding, Biochemistry 28, 7205-7213.
39. Matsumura, M., Signor, G., and Matthews, B. W. (1989) Substantial increase of protein stability by multiple disulphide bonds, Nature 342, 291-293.
40. Pegg, S. C., Brown, S. D., Ojha, S., Seffernick, J., Meng, E. C., Morris, J. H., Chang, P. J., Huang, C. C. Ferrin, T. E., and Babbitt, P. C. (2006) Leveraging enzyme structure-function relationships for functional inference and experimental design: The structure-function linkage database. Biochemistry 45, 2545-2555.
41. Zhang, X. J., Baase, W. A., Shoichet, B. K., Wilson, K. P., and Matthews, B. W. (1995) Enhancement of protein stability by the combination of point mutations in T4 lysozyme is additive. Protein Eng. 8, 1017-1022.
42. Offredi, F., Dubail, F., Kischel, P., Sarinski, K., Stern, A. S., Van de Weerdt, C. Hoch, J. C., Prosperi, C., Francois, J. M., Mayo, S. L., and Martial, J. A. (2003) De novo backbone and sequence design of an idealized α/β-barrel protein: Evidence of stable tertiary structure, J. Mol. Biol. 325, 163-174.
43. Taylor Ringia, E. A., Garrett, J. B., Thoden, J. B., Holden, H. M., Rayment, I., and Gerlt, J. A. (2004) Evolution of enzymatic activity in the enolase superfamily: Functional studies of the promiscuous o-succinylbenzoate synthase from Amycolatopsis. Biochemistry 43, 224-229.
44. Landro, J. A., Kallarakal, A. T., Ransom, S. C., Gerlt, J. A., Kozarich, J. W., Neidhart, D. J., and Kenyon, G. L. (1991) Mechanism of the reaction catalyzed by mandelate racemase. 3. Asymmetry in reactions catalyzed by the H297N mutant, Biochemistry 30, 9274-9281.
45. Stites, W. E., Gittis, A. G., Lattman, E. E., and Shortle, D. (1991) In a staphylococcal nuclease mutant the side-chain of a lysine replacing valine 66 is fully buried in the hydrophobic core. J. Mol. Biol. 221, 7-14.
46. Besenmatter, W., Kast, P., and Hilvert, D. (2007) Relative tolerance of mesostable and thermostable protein homologs to extensive mutation, Proteins 66, 500-506.
47. Petterson, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C. and Ferrin, T. E. (2004) UCSF Chimera: A Visualization System for Exploratory Research and Analysis, J. Comput. Chem. 25, 1605-1612.