Probing the origins of catalytic discrimination between phosphate and sulfate monoester hydrolysis: Comparative analysis of alkaline phosphatase and protein tyrosine phosphatases

Biochemistry

Volumn 53, Issue 43, 2014, Pages 6811-6819

  Andrews, Logan D ^a   Zalatan, Jesse G ^a   Herschlag, Daniel ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CATALYSIS; ELECTROSTATICS; HYDROGEN BONDS; HYDROLYSIS; IONIC STRENGTH; METAL IONS; METALS; POLYPEPTIDES; PROTEINS; SUBSTRATES; SULFUR COMPOUNDS;

ALKALINE PHOSPHATASE; COMPARATIVE ANALYSIS; HYDROGEN BOND DONORS; HYDROLYSIS REACTION; IONIC STRENGTH DEPENDENCE; PHOSPHATE MONOESTER; PROTEIN-TYROSINE PHOSPHATASE; SUBSTRATE SPECIFICITY;

PHOSPHATASES;

ALKALINE PHOSPHATASE; GLUTATHIONE TRANSFERASE P1; ORGANOPHOSPHATE; PROTEIN TYROSINE PHOSPHATASE; SULFATE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PURIFICATION; ENZYME SPECIFICITY; ESCHERICHIA COLI; HYDROGEN BOND; HYDROLYSIS; IONIC STRENGTH; NONHUMAN; PREDICTION; PROTEIN EXPRESSION; CHEMISTRY; COMPARATIVE STUDY; HUMAN; STATIC ELECTRICITY;

ALKALINE PHOSPHATASE; HUMANS; HYDROLYSIS; ORGANOPHOSPHATES; PROTEIN TYROSINE PHOSPHATASES; STATIC ELECTRICITY; SUBSTRATE SPECIFICITY; SULFURIC ACID ESTERS;

EID: 84908499924     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500765p     Document Type: Article

References (57)

1. Jensen, R. A. (1976) Enzyme recruitment in evolution of new function Annu. Rev. Microbiol. 30, 409-425
2. OBrien, P. J. (2006) Catalytic promiscuity and the divergent evolution of DNA repair enzymes Chem. Rev. 106, 720-752
3. Aharoni, A., Gaidukov, L., Khersonsky, O., Gould, S. M., Roodveldt, C., and Tawfik, D. S. (2004) The "evolvability of promiscuous protein functions Nat. Genet. 37, 73-76
4. Khersonsky, O. and Tawfik, D. S. (2010) Enzyme promiscuity: A mechanistic and evolutionary perspective Annu. Rev. Biochem. 79, 471-505
5. OBrien, P. J. and Herschlag, D. (2002) Alkaline phosphatase revisited: Hydrolysis of alkyl phosphates Biochemistry 41, 3207-3225
6. Zalatan, J., Fenn, T., Brunger, A., and Herschlag, D. (2006) Structural and functional comparisons of nucleotide pyrophosphatase/phosphodiesterase and alkaline phosphatase: Implications for mechanism and evolution Biochemistry 45, 9788-9803
7. Lassila, J. and Herschlag, D. (2008) Promiscuous sulfatase activity and thio-effects in a phosphodiesterase of the alkaline phosphatase superfamily Biochemistry 47, 12853-12859
8. Berlutti, F., Passariello, C., Selan, L., Thaller, M. C., and Rossolini, G. M. (2001) The Chryseobacterium meningosepticum PafA enzyme: Prototype of a new enzyme family of prokaryotic phosphate-irrepressible alkaline phosphatases? Microbiology 147, 2831-2839
9. Kim, A., Benning, M. M., OkLee, S., Quinn, J., Martin, B. M., Holden, H. M., and Dunaway-Mariano, D. (2011) Divergence of chemical function in the alkaline phosphatase superfamily: Structure and mechanism of the P-C Bond cleaving enzyme phosphonoacetate hydrolase Biochemistry 50, 3481-3494
10. Van Loo, B., Jonas, S., Babtie, A. C., Benjdia, A., Berteau, O., Hyvonen, M., and Hollfelder, F. (2010) An efficient, multiply promiscuous hydrolase in the alkaline phosphatase superfamily Proc. Natl. Acad. Sci. U.S.A. 107, 2740-2745
11. 13 for phosphate monoester hydrolysis J. Am. Chem. Soc. 130, 16547-16555
12. OBrien, P. J. and Herschlag, D. (1998) Sulfatase activity of E. coli alkaline phosphatase demonstrates a functional link to arylsulfatases, and evolutionarily related enzyme family J. Am. Chem. Soc. 120, 12369-12370
13. Nikolic-Hughes, I., OBrien, P., and Herschlag, D. (2005) Alkaline phosphatase catalysis is ultrasensitive to charge sequestered between the active site zinc ions J. Am. Chem. Soc. 127, 9314-9315
14. Zhang, Z. Y., Zhou, G., Denu, J. M., Wu, L., Tang, X., Mondesert, O., Russell, P., Butch, E., and Guan, K. L. (1995) Purification and characterization of the low molecular weight protein tyrosine phosphatase, Stp1, from the fission yeast Schizosaccharomyces pomb e Biochemistry 34, 10560-10568
15. Zhang, Y. L. and Zhang, Z. Y. (1998) Low-affinity binding determined by titration calorimetry using a high-affinity coupling ligand: A thermodynamic study of ligand binding to protein tyrosine phosphatase 1B Anal. Biochem. 261, 139-148
16. Zhang, Z. Y., Clemens, J. C., Schubert, H. L., Stuckey, J. A., Fischer, M. W., Hume, D. M., Saper, M. A., and Dixon, J. E. (1992) Expression, purification, and physicochemical characterization of a recombinant Yersinia protein tyrosine phosphatase J. Biol. Chem. 267, 23759-23766
17. Zalatan, J., Fenn, T., and Herschlag, D. (2008) Comparative enzymology in the alkaline phosphatase superfamily to determine the catalytic role of an active-site metal ion J. Mol. Biol. 384, 1174-1189
18. OBrien, P. J., Lassila, J. K., Fenn, T. D., Zalatan, J. G., and Herschlag, D. (2008) Arginine coordination in enzymatic phosphoryl transfer: Evaluation of the effect of Arg166 mutations in Escherichia coli alkaline phosphatase Biochemistry 47, 7663-7672
19. Zalatan, J. and Herschlag, D. (2006) Alkaline phosphatase mono-and diesterase reactions: Comparative transition state analysis J. Am. Chem. Soc. 128, 1293-1303
20. Wu, L. and Zhang, Z. Y. (1996) Probing the function of Asp128 in the lower molecular weight protein-tyrosine phosphatase-catalyzed reaction. A pre-steady-state and steady-state kinetic investigation Biochemistry 35, 5426-5434
21. OBrien, P. J. and Herschlag, D. (2001) Functional interrelationships in the alkaline phosphatase superfamily: phosphodiesterase activity of Escherichia coli alkaline phosphatase Biochemistry 40, 5691-5699
22. Zhang, Z. Y. (1998) Protein-Tyrosine phosphatases: Biological function, structural characteristics, and mechanism of catalysis Crit. Rev. Biochem. Mol. Biol. 33, 1-52
23. Zhang, Z. Y. and Dixon, J. E. (1994) Protein tyrosine phosphatases: Mechanism of catalysis and substrate specificity Adv. Enzymol. Relat. Areas Mol. Biol. 68, 1-36
24. Barford, D., Das, A. K., and Egloff, M. P. (1998) The structure and mechanism of protein phosphatases: Insights into catalysis and regulation Annu. Rev. Biophys. Biomol. Struct. 27, 133-164
25. Zhang, Z. Y., Wang, Y. A., and Dixon, J. E. (1994) Dissecting the catalytic mechanism of protein-tyrosine phosphatases Proc. Natl. Acad. Sci. U.S.A. 91, 1624-1627
26. Fischer, E. H., Charbonneau, H., and Tonks, N. K. (1991) Protein tyrosine phosphatases-a diverse family of intracellular and transmembrane enzymes Science 253, 401-406
27. a of the leaving group Biochemistry 32, 8737-8741
28. Hengge, A. C., Edens, W. A., and Elsing, H. (1994) Transition-state structures for phosphoryl-transfer reactions of p-nitrophenyl phosphate J. Am. Chem. Soc. 116, 5045-5049
29. Simopoulos, T. T. and Jencks, W. P. (1994) Alkaline phosphatase is an almost perfect enzyme Biochemistry 33, 10375-10380
30. OBrien, P. J. and Herschlag, D. (2002) Alkaline phosphatase revisited: Hydrolysis of alkyl phosphates Biochemistry 41, 3207-3225
31. Kirby, A. and Jencks, W. (1965) The reactivity of nucleophilic reagents toward the p-nitrophenyl phosphate dianion J. Am. Chem. Soc. 87, 3209-3216
32. Kirby, A. and Varvoglis, A. (1967) The reactivity of phosphate esters. Monoester hydrolysis J. Am. Chem. Soc. 89, 415-423
33. Thatcher, G. R. J. and Kluger, R. (1989) Mechanism and catalysis of nucleophilic substitution in phosphate esters Adv. Phys. Org. Chem. 25, 99-265
34. Hengge, A. (2005) Mechanistic studies on enzyme-catalyzed phosphoryl transfer Adv. Phys. Org. Chem. 40, 49-108
35. Benkovic, S. J. and Benkovic, P. A. (1966) Studies on sulfate esters. I. Nucleophilic reactions of amines with p-nitrophenyl sulfate J. Am. Chem. Soc. 88, 5504-5511
36. Fendler, E. J. and Fendler, J. H. (1968) Hydrolysis of nitrophenyl and dinitrophenyl sulfate esters J. Org. Chem. 33, 3852-3859
37. Hopkins, A., Day, R. A., and Williams, A. (1983) Sulfate group transfer between nitrogen and oxygen: Evidence consistent with an open "exploded transition state J. Am. Chem. Soc. 105, 6062-6070
38. 3-) transfer between pyridine nucleophiles J. Am. Chem. Soc. 107, 4327-4331
39. Lassila, J. K., Zalatan, J. G., and Herschlag, D. (2011) Biological phosphoryl transfer reactions: Understanding mechanism and catalysis Annu. Rev. Biochem. 80, 669-702
40. Catrina, I., OBrien, P. J., Purcell, J., Nikolic-Hughes, I., Zalatan, J. G., Hengge, A. C., and Herschlag, D. (2007) Probing the origin of the compromised catalysis of E. coli alkaline phosphatase in its promiscuous sulfatase reaction J. Am. Chem. Soc. 129, 5760-5765
41. Zalatan, J. G., Catrina, I., Mitchell, R., Grzyska, P. K., OBrien, P. J., Herschlag, D., and Hengge, A. C. (2007) Kinetic isotope effects for alkaline phosphatase reactions: Implications for the role of active-site metal ions in catalysis J. Am. Chem. Soc. 129, 9789-9798
42. Nikolic-Hughes, I., Rees, D. C., and Herschlag, D. (2004) Do electrostatic interactions with positively charged active site groups tighten the transition state for enzymatic phosphoryl transfer? J. Am. Chem. Soc. 126, 11814-11819
43. Hengge, A. C., Edens, W. A., and Elsing, H. (1994) Transition-state structures for phosphoryl-transfer reactions of p-nitrophenyl phosphate J. Am. Chem. Soc. 116, 5045-5049
44. Hoff, R. H., Larsen, P., and Hengge, A. C. (2001) Isotope effects and medium effects on sulfuryl transfer reactions J. Am. Chem. Soc. 123, 9338-9344
45. Sigala, P., Kraut, D., Caaveiro, J., Pybus, B., Ruben, E., Ringe, D., Petsko, G., and Herschlag, D. (2008) Testing geometrical discrimination within an enzyme active site: Constrained hydrogen bonding in the ketosteroid isomerase oxyanion hole J. Am. Chem. Soc. 130, 13696-13708
46. Fuhrmann, C. N., Kelch, B. A., Ota, N., and Agard, D. A. (2004) The 0.83 A resolution crystal structure of alpha-lytic protease reveals the detailed structure of the active site and identifies a source of conformational strain J. Mol. Biol. 338, 999-1013
47. Elias, M., Wellner, A., Goldin-Azulay, K., Chabrire, E., Vorholt, J., Erb, T., and Tawfik, D. S. (2012) The molecular basis of phosphate discrimination in arsentate-rich environments Nature 491, 134-137
48. Abell, K. and Kirby, A. (1986) Acceleration of P-O cleavage reactions of phosphate monoester dianions in dipolar aprotic solvents Tetrahedron Lett. 27, 1085-1088
49. Montserat, J., Chen, L., Lawrence, D. S., and Zhang, Z. Y. (1996) Potent low molecular weight substrates for protein-tyrosine phosphatase J. Biol. Chem. 271, 7868-7872
50. 2O: A problem in pseudo-symmetry Acta Crystallogr. B27, 1315-1319
51. Jarvis, J. A. J. (1953) Crystal structure of potassium ethyl sulphate Acta Crystallogr. 6, 327-330
52. Truter, M. R. (1958) A detailed refinement of the crystal structure of potassium ethyl sulphate Acta Crystallogr. 11, 680-685
53. Sali, A. and Blundell, T. L. (1993) Comparative protein modeling by satisfaction of spatial restraints J. Mol. Biol. 234, 779-815
54. DeLano, W. (2007) MacPyMOL: A PyMOL-based molecular graphics application for MacOS X, DeLano Scientific LLC, Palo Alto, CA.
55. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
56. Zhang, M., Zhou, M., Van Etten, R. L., and Stauffacher, C. V. (1997) Crystal structure of bovine low molecular weight phosphotyrosyl phosphatase complexed with the transition state analog vanadate Biochemistry 36, 15-23
57. Bobyr, E., Lassila, J., Wiersma-Koch, H., Fenn, T., Lee, J., Nikolic-Hughes, I., Hodgson, K., Rees, D., Hedman, B., and Herschlag, D. (2012) High-resolution analysis of Zn2+ coordination in the alkaline phosphatase superfamily by EXAFS and x-ray crystallography J. Mol. Biol. 415, 102-117