Kinetic isotope effects support the twisted amide mechanism of Pin1 peptidyl-prolyl isomerase

Biochemistry

Volumn 52, Issue 44, 2013, Pages 7707-7713

  Mercedes Camacho, Ana Y ^a   Mullins, Ashley B ^a   Mason, Matthew D ^a   Xu, Guoyan G ^a   Mahoney, Brendan J ^b   Wang, Xingsheng ^b   Peng, Jeffrey W ^b   Etzkorn, Felicia A ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC EFFICIENCIES; EXCHANGE SPECTROSCOPIES; EXCHANGEABLE PROTONS; KINETIC ISOTOPE EFFECTS; NUCLEOPHILIC ADDITIONS; PEPTIDYL-PROLYL ISOMERASE; RATE DETERMINING STEP; RATE-LIMITING STEPS;

ADDITION REACTIONS; AMIDES; AMINO ACIDS; CARRIER MOBILITY; CATALYSIS; ISOMERIZATION; ISOMERS; ISOTOPES; SUBSTRATES;

KINETICS;

AMIDE; CYCLOPHILIN; DEUTERIUM; ISOTOPE; NITROGEN; PEPTIDYLPROLYL ISOMERASE PIN1; SERINE;

ARTICLE; CIS TRANS ISOMERISM; CRYSTAL STRUCTURE; ENZYME CONFORMATION; ENZYME KINETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HYDROGEN BOND; ISOMERIZATION; LIMIT OF DETECTION; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOPHILICITY; PRIORITY JOURNAL; QUANTUM MECHANICS; REACTION ANALYSIS; STEREOSPECIFICITY;

AMIDES; CYTOPLASMIC DYNEINS; DEUTERIUM; ISOMERISM; ISOTOPE LABELING; KINETICS; PEPTIDES; SUBSTRATE SPECIFICITY;

EID: 84887684420     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400700b     Document Type: Article

References (43)

1. Lu, K. P., Hanes, S. D., and Hunter, T. (1996) A human peptidyl-prolyl isomerase essential for regulation of mitosis Nature 380, 544-547
2. Yaffe, M. B., Schutkowski, M., Shen, M., Zhou, X. Z., Stukenberg, P. T., Rahfeld, J. U., Xu, J., Kuang, J., Kirschner, M. W., Fischer, G., Cantley, L. C., and Lu, K. P. (1997) Sequence-specific and phosphorylation-dependent proline isomerization: A potential mitotic regulatory mechanism Science 278, 1957-1960
3. Fischer, G., Bang, H., and Mech, C. (1984) [Determination of enzymatic catalysis for the cis-trans-isomerization of peptide binding in proline-containing peptides] Biomed. Biochim. Acta 43, 1101-1111
4. Fischer, G. (1994) Peptidyl-Prolyl cis/trans Isomerases and Their Effectors Angew. Chem., Int. Ed. 33, 1415-1436
5. Ranganathan, R., Lu, K. P., Hunter, T., and Noel, J. P. (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent Cell 89, 875-886
6. Schroeder, O. E., Carper, E., Wind, J. J., Poutsma, J. L., Etzkorn, F. A., and Poutsma, J. C. (2006) Theoretical and Experimental Investigation of the Energetics of Cis-Trans Proline Isomerization in Peptide Models J. Phys. Chem. A 110, 6522-6530
7. Zhang, Y., Daum, S., Wildemann, D., Zhou, X. Z., Verdecia, M. A., Bowman, M. E., Lucke, C., Hunter, T., Lu, K. P., Fischer, G., and Noel, J. P. (2007) Structural basis for high-affinity peptide inhibition of human Pin1 ACS Chem. Biol. 2, 320-328
8. Liu, J., Albers, M. W., Chen, C.-M., Schreiber, S. L., and Walsh, C. T. (1990) Cloning, expression, and purification of human cyclophilin in Escherichia coli and assessment of the catalytic role of cysteines by site-directed mutagenesis Proc. Natl. Acad. Sci. U.S.A. 87, 2304-2308
9. Zydowsky, L. D., Etzkorn, F. A., Chang, H. Y., Ferguson, S. B., Stolz, L. A., Ho, S. I., and Walsh, C. T. (1992) Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition Protein Sci. 1, 1092-1099
10. Harrison, R. K. and Stein, R. L. (1990) Mechanistic Studies of Peptidyl Prolyl Cis-Trans Isomerase: Evidence for Catalysis by Distortion Biochemistry 29, 1684-1689
11. Harrison, R. K., Caldwell, C. G., Rosegay, A., Melillo, D., and Stein, R. L. (1990) Confirmation of the secondary deuterium isotope effect for the peptidyl prolyl cis-trans isomerase activity of cyclophilin by a competitive, double-label technique J. Am. Chem. Soc. 112, 7063-7064
12. Park, S. T., Aldape, R. A., Futer, O., DeCenzo, M. T., and Livingston, D. J. (1992) PPIase Catalysis by Human FK506-binding Protein Proceeds Through a Conformational Twist Mechanism J. Biol. Chem. 267, 3316-3324
13. Rosen, M. K., Standaert, R. F., Galat, A., Nakatsuka, M., and Schreiber, S. L. (1990) Inhibition of FKBP Rotamase Activity by Immunosuppressant FK506: Twisted Amide Surrogate Science 248, 863-866
14. Fischer, S., Michnick, S., and Karplus, M. (1993) A Mechanism for Rotamase Catalysis by the FK506 Binding Protein (FKBP) Biochemistry 32, 13830-13837
15. Wiederrecht, G. and Etzkorn, F. (1994) The immunophilins Perspect. Drug Discovery Des. 57-84
16. Cox, C. and Lectka, T. (1998) Intramolecular Catalysis of Amide Isomerization: Kinetic Consequences of the 5-NH-Na Hydrogen Bond in Prolyl Peptides J. Am. Chem. Soc. 120, 10660-10668
17. Choudhary, A. and Raines, R. T. (2011) An evaluation of peptide-bond isosteres ChemBioChem 12, 1801-1807
18. Kallen, J. and Walkinshaw, M. D. (1992) The X-ray structure of a tetrapeptide bound to the active site of human cyclophilin A FEBS Lett. 300, 286-290
19. Howard, B., Vajdos, F., Li, S., Sundquist, W., and Hill, C. (2003) Structural insights into the catalytic mechanism of cyclophilin A Nat. Struct. Biol. 10, 475-481
20. Hur, S. and Bruice, T. C. (2002) The mechanism of cis-trans isomerization of prolyl peptides by cyclophilin J. Am. Chem. Soc. 124, 7303-7313
21. Behrsin, C. D., Bailey, M. L., Bateman, K. S., Hamilton, K. S., Wahl, L. M., Brandl, C. J., Shilton, B. H., and Litchfield, D. W. (2007) Functionally important residues in the peptidyl-prolyl isomerase Pin1 revealed by unigenic evolution J. Mol. Biol. 365, 1143-1162
22. Xu, G. G. and Etzkorn, F. A. (2010) Convergent synthesis of α-ketoamide inhibitors of Pin1 Org. Lett. 12, 696-699
23. Xu, G. G., Slebodnick, C., and Etzkorn, F. A. (2012) Cyclohexyl ketone inhibitors of Pin1 dock in a trans-diaxial cyclohexane conformation PLoS One 7, e44226
24. Xu, G. G., Zhang, Y., Mercedes-Camacho, A. Y., and Etzkorn, F. A. (2011) A reduced-amide inhibitor of Pin1 binds in a conformation resembling a twisted-amide transition state Biochemistry 50, 9545-9550
25. Vöhringer-Martinez, E., Duarte, F., and Toro-Labbe, A. (2012) How does Pin1 catalyze the cis-trans prolyl peptide bond isomerization? A QM/MM and mean reaction force study J. Phys. Chem. B 116, 12972-12979
26. Bernhardt, A., Drewello, M., and Schutkowski, M. (1997) The solid-phase synthesis of side-chain-phosphorylated peptide-4-nitroanilides J. Pept. Res. 50, 143-152
27. Lu, P. J., Wulf, G., Zhou, X. Z., Davies, P., and Lu, K. P. (1999) The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein Nature 399, 784-788
28. Wang, X. J., Xu, B., Mullins, A. B., Neiler, F. K., and Etzkorn, F. A. (2004) Conformationally locked isostere of phosphoSer- cis -Pro inhibits Pin1 23-fold better than phosphoSer- trans -Pro isostere J. Am. Chem. Soc. 126, 15533-15542
29. Kofron, J. L., Kuzmic, P., Kishore, V., Colon-Bonilla, E., and Rich, D. H. (1991) Determination of kinetic constants for peptidyl prolyl cis-trans isomerase by an improved spectroscopy assay Biochemistry 30, 6127-6134
30. Jeener, J., Meier, B. H., Bachmann, P., and Ernst, R. R. (1979) Investigation of exchange processes by two-dimensional NMR spectroscopy J. Chem. Phys. 71, 4546-4553
31. 13C-NMR Biophys. Chem. 32, 89-95
32. Greenwood, A. I., Rogals, M. J., De, S., Lu, K. P., Kovrigin, E. L., and Nicholson, L. K. (2011) Complete determination of the Pin1 catalytic domain thermodynamic cycle by NMR lineshape analysis J. Biomol. NMR 51, 21-34
33. Cleland, W. W. (1979) Statistical Analysis of Enzyme Kinetic Data Methods Enzymol. 63, 103-138
34. Maitra, U. and Chandrasekhar, J. (1997) Use of Isotopes for Studying Reaction Mechanisms. 3. Secondary Kinetic Isotope Effect Resonance 2, 18-25
35. do Amaral, L., Bull, H. G., and Cordes, E. H. (1972) Secondary Deuterium Isotope Effects for Carbonyl Addition Reactions J. Am. Chem. Soc. 94, 7579-7580
36. Perrin, C. L., Thoburn, J. D., and Kresge, A. J. (1992) Secondary kinetic isotope effects in carbon-nitrogen rotation of amides J. Am. Chem. Soc. 114, 8800-8807
37. Garoutte, M. P., Bibbs, J. A., and Schowen, R. L. (2006) Solvent Isotope Effects and the Question of Quantum Tunneling in Hydrolytic Enzyme Action J. Nucl. Sci. Technol. 43, 455-460
38. Olson, L. P., Li, Y., Houk, K. N., Kresge, A. J., and Schaad, L. J. (1995) Theoretical Analysis of Secondary Kinetic Isotope Effects in C-N Rotation of Amides J. Am. Chem. Soc. 117, 2992-2997
39. Zhang, M., Wang, X. J., Chen, X., Bowman, M. E., Luo, Y., Noel, J. P., Ellington, A. D., Etzkorn, F. A., and Zhang, Y. (2012) Structural and Kinetic Analysis of Prolyl-isomerization/Phosphorylation Cross-Talk in the CTD Code ACS Chem. Biol. 7, 1462-1470
40. Bender, M. L., Kezdy, F. J., and Zerner, B. (1963) Intramolecular Catalysis in the Hydrolysis of p-Nitrophenyl Salicylates J. Am. Chem. Soc. 85, 3017-3024
41. Gandour, R. D., Pivert, M. A., Kelley, E. L., Minor, B. D., Spencer, R., Ingraham, R. H., and Spindler, S. J. (1979) Solvent isotope effects in intramolecular catalysis: Acyl transfer reactions of 4-nitrophenyl 5-nitrosalicylate in aqueous tris buffer Bioorg. Chem. 8, 45-58
42. Pesando, J. M. (1975) Proton magnetic resonance studies of carbonic anhydrase. II. Group controlling catalytic activity Biochemistry 14, 681-688
43. Hoffmann, R., Minkin, V. I., and Carpenter, B. K. (1997) Ockham's Razor and Chemistry HYLE 3, 3-28