Reduction and oxidation of the active site iron in tyrosine hydroxylase: Kinetics and specificity

Biochemistry

Volumn 45, Issue 7, 2006, Pages 2372-2379

  Frantom, Patrick A ^a   Seravalli, Javier ^b   Ragsdale, Stephen W ^b   Fitzpatrick, Paul F ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSTS; FREEZING; HYDROXYLATION; IRON; OXIDATION; PARAMAGNETIC RESONANCE; QUENCHING; RATE CONSTANTS; REACTION KINETICS;

ANAEROBIC STOPPED-FLOW SPECTROSCOPY; DIHYDROXYPHENYLALANINE; PHOSPHORYLATED; TYROSINE HYDROXYLASE (TYRH);

ENZYMES;

1,4 BENZOQUINONE; ALANINE; ASCORBIC ACID; DOPA; FERRIC ION; FERROUS ION; GLUTAMIC ACID; GLUTATHIONE; IRON; METHYLTETRAHYDROBIOPTERIN; OXYGEN; PTERIN; RADICAL; REDUCING AGENT; SERINE; TETRAHYDROBIOPTERIN; TYROSINE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; CHEMICAL REACTION KINETICS; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME SPECIFICITY; FREEZING; HYDROXYLATION; MICHAELIS MENTEN KINETICS; MOLECULAR MIMICRY; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; SPECTROSCOPY; ULTRAVIOLET RADIATION;

ANAEROBIOSIS; ANIMALS; ASCORBIC ACID; BINDING SITES; BIOPTERIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTRON SPIN RESONANCE SPECTROSCOPY; IRON; KINETICS; OXIDATION-REDUCTION; PTERINS; RATS; SPECTROPHOTOMETRY, ULTRAVIOLET; TYROSINE 3-MONOOXYGENASE;

EID: 33144475971     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052283j     Document Type: Article

References (39)

1. Fitzpatrick, P. F. (2000) The aromatic amino acid hydroxylases, in Advances in Enzymology and Related Areas of Molecular Biology (Purich, D. L., Ed.) pp 235-294, John Wiley & Sons, New York.
2. Ramsey, A. J., Hillas, P. J., and Fitzpatrick, P. F. (1996) Characterization of the active site iron in tyrosine hydroxylase: Redox states of the iron, J. Biol. Chem. 271, 24395-24400.
3. Sura, G., Daubner, S. C., and Fitzpatrick, P. F. (2004) Effects of phosphorylation by protein kinase A on binding of catecholamines to the human tyrosine hydroxylase isoforms, J. Neurochem. 90, 970-978.
4. Fitzpatrick, P. F. (1989) The metal requirement of rat tyrosine hydroxylase, Biochem. Biophys. Res. Commun. 161, 211-215.
5. Fitzpatrick, P. F. (2003) Mechanism of aromatic amino acid hydroxylation, Biochemistry 42, 14083-14091.
6. Ramsey, A. J., and Fitzpatrick, P. F. (2000) Effects of phosphorylation on binding of catecholamines to tyrosine hydroxylase: specificity and thermodynamics, Biochemistry 39, 773-778.
7. Andersson, K. K., Cox, D. D., Que, L., Jr., Flatmark, T., and Haavik, J. (1988) Resonance Raman studies on the blue-green-colored bovine adrenal tyrosine 3-monooxygenase (tyrosine hydroxylase). Evidence that the feedback inhibitors adrenaline and noradrenaline are coordinated to iron, J. Biol. Chem. 263, 18621-18626.
8. Daubner, S. C., Lauriano, C., Haycock, J. W., and Fitzpatrick, P. F. (1992) Site-directed mutagenesis of serine 40 of rat tyrosine hydroxylase. Effects of dopamine and cAMP-dependent phosphorylation on enzyme activity, J. Biol. Chem. 267, 12639-12646.
9. Ramsey, A. J., and Fitzpatrick, P. F. (1998) Effects of phosphorylation of serine 40 of tyrosine hydroxylase on binding of catecholamines: Evidence for a novel regulatory mechanism, Biochemistry 37, 8980-8986.
10. Wallick, D. E., Bloom, L. M., Gaffney, B. J., and Benkovic, S. J. (1984) Reductive activation of phenylalanine hydroxylase and its effect on the redox state of the non-heme iron, Biochemistry 23, 1295-1302.
11. Marota, J. J. A., and Shiman, R. (1984) Stoichiometric reduction of phenylalanine hydroxylase by its cofactor: A requirement for enzymatic activity, Biochemistry 23, 1303-1311.
12. Shiman, R., Gray, D. W., and Hill, M. A. (1994) Regulation of rat liver phenylalanine hydroxylase. I. Kinetic properties of the enzyme's iron and enzyme reduction site, J. Biol. Chem. 269, 24637-24646.
13. Daubner, S. C., and Fitzpatrick, P. F. (1999) Site-directed mutants of charged residues in the active site of tyrosine hydroxylase, Biochemistry 38, 4448-4454.
14. McCulloch, R. I., Daubner, S. C., and Fitzpatrick, P. F. (2001) Effects of substitution at serine 40 of tyrosine hydroxylase on catecholamine binding, Biochemistry 40, 7273-7278.
15. Fitzpatrick, P., Ralph, E. C., Ellis, H. R., Willmon, O. J., and Daubner, S. C. (2003) Characterization of metal ligand mutants of tyrosine hydroxylase: Insights into the plasticity of a 2-histidine-1-carboxylate triad, Biochemistry 42, 2081-2088.
16. Ballou, D. P. (1978) Freeze-quench and chemical-quench techniques, Methods Enzymol. 54, 85-93.
17. Barshop, B. A., Wrenn, R. F., and Frieden, C. (1983) Analysis of numerical methods for computer simulation of kinetic processes: Development of KINSIM-a flexible, portable system, Anal. Biochem. 130, 134-145.
18. Kuzmic, P. (1996) Program DYNAFIT for the analysis of enzyme kinetic data: Application to HIV proteinase, Anal. Biochem. 237, 260-273.
19. Wei, C., Wang, Z., Arvai, A. S., Hemann, C., Hille, R., Getzoff, E. D., and Stuehr, D. J. (2003) Structure of tetrahydrobiopterin tunes its electron transfer to the heme-dioxy intermediate in nitric oxide synthase, Biochemistry 42, 1969-1977.
20. Pfleiderer, W. (1985) Chemistry of naturally occurring pterins, in Folates and Pterins (Blakley, R. L., and Benkovic, S. J., Eds.) Vol. II, pp 43-114, John Wiley & Sons, New York.
21. Shiman, R. (1985) Phenylalanine hydroxylase and dihydropterin reductase, in Folates and Pterins (Blakley, R. L., and Benkovic, S. J., Eds.) Vol. II, pp 179-249, John Wiley & Sons, New York.
22. Andersen, O. A., Stokka, A. J., Flatmark, T., and Hough, E. (2003) 2.0 Å resolution crystal structures of the ternary complexes of human phenylalanine hydroxylase catalytic domain with tetrahydrobiopterin and 3-(2-thienyl)-L-alanine or L-norleucine: Substrate specificity and molecular motions related to substrate binding, J. Mol. Biol. 333, 747-757.
23. Moran, G. R., Daubner, S. C., and Fitzpatrick, P. F. (1998) Expression and characterization of the catalytic core of tryptophan hydroxylase, J. Biol. Chem. 273, 12259-12266.
24. Haavik, J., Andersson, K. K., Petersson, L., and Flatmark, T. (1988) Soluble tyrosine hydroxylase (tyrosine 3-monooxygenase) from bovine adrenal medulla: Large-scale purification and physicochemical properties, Biochim. Biophys. Acta 953, 142-156.
25. Gottschall, D. W., Dietrich, R. F., and Benkovic, S. J. (1982) Phenylalanine hydroxylase. Correlation of the iron content with activity and the preparation and reconstitution of the apoenzyme, J. Biol. Chem. 257, 845-849.
26. Fisher, D. B., Kirkwood, R., and Kaufman, S. (1972) Rat liver phenylalanine hydroxylase, an iron enzyme, J. Biol. Chem. 247, 5161-5167.
27. Hill, M. A., Marota, J. J. A., and Shiman, R. (1988) Reaction of rat liver phenylalanine hydroxylase with fatty acid hydroperoxides. Characterization and mechanism, J. Biol. Chem. 263, 5646-5655.
28. Hagedoorn, P.-L., Schmidt, P. P., Andersson, K. K., Hagen, W. R., Flatmark, T., and Martinez, A. (2001) The effect of the substrate, dihydrobiopterin and dopamine on the EPR spectroscopic properties and the midpoint potential of the catalytic iron in recombinant human phenylalanine hydroxylase, J. Biol. Chem. 276, 22850-22856.
29. Goodwill, K. E., Sabatier, C., and Stevens, R. C. (1998) Crystal structure of tyrosine hydroxylase with bound cofactor analogue and iron at 2.3 Å resolution: self-hydroxylation of phe300 and the pterin-binding site, Biochemistry 37, 13437-13445.
30. Andersen, O. A., Flatmark, T., and Hough, E. (2001) High resolution crystal structures of the catalytic domain of human phenylalanine hydroxylase in its catalytically active Fe(II) form and binary complex with tetrahydrobiopterin, J. Mol. Biol. 314, 279-291.
31. Patel, K. B., Stratford, M. R. L., Wardman, P., and Everett, S. A. (2002) Oxidation of tetrahydrobiopterin by biological radicals and scavenging of the trihydrobiopterin radical by ascorbate, Free Radical Biol. Med. 32, 203-211.
32. Levine, R. A., Miller, L. P., and Lovenberg, W. (1981) Tetrahydrobiopterin in striatum: localization in dopamine nerve terminals and role in catecholamine synthesis, Science 214, 919-921.
33. 31P NMR and EPR oximetry study, Am. J. Physiol. 279, 9-16.
34. Fitzpatrick, P. F., Chlumsky, L. J., Daubner, S. C., and O'Malley, K. L. (1990) Expression of rat tyrosine hydroxylase in insect tissue culture cells and purification and characterization of the cloned enzyme, J. Biol Chem. 265, 2042-2047.
35. Buu, N. T., Duhaime, J., and Kuchel, O. (1985) Effects of L-DOPA on the concentrations of free and sulfoconjugated catecholamines in plasma, cerebrospinal fluid, urine, and central and peripheral nervous system tissues of the rat, J. Neurochem. 44, 787-792.
36. Gorren, A. C. F., Kungl, A. J., Schmidt, K., Werner, E. R., and Mayer, B. (2001) Electrochemistry of pterin cofactors and inhibitors of nitric oxide synthase, Nitric Oxide 5, 176-186.
37. Buettner, G. R., and Oberley, L. W. (1978) Considerations in the spin trapping of superoxide and hydroxyl radical in aqueous systems using 5,5-dimethyl-1-pyrroline-1-oxide, Biochem. Biophys. Res. Commun. 83, 69-74.
38. Ilan, Y. A., Czapski, G., and Meisel, D. (1976) The one-electron transfer redox potentials of free radicals. I. The oxygen/superoxide system, Biochim. Biophys. Acta 430, 209-224.
39. Koppenol, W. H. (1993) A thermodynamic appraisal of the radical sink hypothesis, Free Radical Biol. Med. 14, 91-94.