Tyrosine hydroxylase is inactivated by catechol-quinones and converted to a redox-cycling quinoprotein: Possible relevance to Parkinson's disease

Journal of Neurochemistry

Volumn 73, Issue 3, 1999, Pages 1309-1317

  Kuhn, Donald M ^a,c   Arthur Jr , Robert E ^a   Thomas, David M ^b   Elferink, Lisa A ^b  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c Cellular and Clinical Neurobiology Program   (United States)

Author keywords

DOPA; Dopamine; Quinones; Quinoproteins; Redox cycling; Tyrosine hydroxylase

Indexed keywords

ANTIOXIDANT; COPPER; DOPA; DOPAMINE; IRON; N ACETYLDOPAMINE; PROTEIN; QUINONE DERIVATIVE; REDUCING AGENT; THIOL GROUP; TYROSINE 3 MONOOXYGENASE;

ARTICLE; ENZYME ACTIVATION; ENZYME MODIFICATION; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL;

ANIMALS; CATECHOLS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DIHYDROXYPHENYLALANINE; DOPAMINE; ELECTROCHEMISTRY; ENZYME INHIBITORS; HYDROLYSIS; OXIDATION-REDUCTION; PARKINSON DISEASE; QUINONES; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TYROSINE 3-MONOOXYGENASE;

EID: 0032842040     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0731309.x     Document Type: Article

References (57)

1. Almas B., Le Bourdelles B., Flatmark T., Mallet J., and Haavik J. (1992) Regulation of recombinant human tyrosine hydroxylase isozymes by catecholamine binding and phosphorylation: structure/activity studies and mechanistic implications. Eur. J. Biochem. 209, 249-255.
2. Andersson K. K., Vassort C., Brennan B. A., Que L., Haavik J., Flatmark T., and Thibault J. (1992) Purification and characterization of the blue-green rat phaeochromocytoma (PC12) tyrosine hydroxylase with a dopamine-Fe(III) complex: reversal of the endogenous feedback inhibition by phosphorylation of serine 40. Biochem. J. 284, 687-695.
3. Bernheimer H., Birkmayer W., Hornykiewicz O., Jellinger K., and Seitelberger F. (1973) Brain dopamine and the syndromes of Parkinson and Huntington: clinical, morphological, and neurochemical correlations. J. Neurol. Sci. 20, 415-455.
4. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
5. Cohen G., Farooqui R., and Kesler N. (1997) Parkinson disease: a new link between monoamine oxidase and mitochondrial electron flow. Proc. Natl. Acad. Sci. USA 94, 4890-4894.
6. Dean R. T., Gebicki J., Geiseg S., Grant A. J., and Simpson J. A. (1992) Hypothesis: a damaging role in aging for reactive protein oxidation products? Mutat. Res. 275, 387-393.
7. Dean R. T., Fu S., Stocker R., and Davies M. J. (1997) Biochemistry and pathology of radical-mediated protein oxidation. Biochem. J. 324, 1-18.
8. D'Sa C. M., Arthur R. E. Jr., and Kuhn D. M. (1996) Expression and deletion mutagenesis of tryptophan hydroxylase fusion proteins: delineation of the enzyme catalytic core. J. Neurochem. 67, 917-926.
9. Ellman G. L. (1959) Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70-77.
10. Fahn S. and Cohen G. (1992) The oxidant stress hypothesis in Parkinson's disease: evidence supporting it. Ann. Neurol. 32, 804-812.
11. Gibb J. W., Johnson M., Elayan I., Lim H. K., Matsuda L., and Hanson G. R. (1997) Neurotoxicity of amphetamines and their metabolites. NIDA Res. Monogr. 173, 128-145.
12. Götz M. E., Kunig G., Riederer P., and Youdim M. B. H. (1994) Oxidative stress: free radical production in neural degeneration. Pharmacol. Ther. 14, 633-643.
13. Graham D. G. (1978) Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol. Pharmacol. 14, 633-643.
14. Graham D. G., Tiffany S. M., Bell W. R. Jr., and Gutknecht W. F. (1978) Autooxidation versus covalent binding of quinones as the mechanism of toxicity of dopamine, 6-hydroxydopamine, and related compounds toward C1300 neuroblastoma cells in vitro. Mol. Pharmacol. 146, 644-653.
15. Grennet H. E., Ledley F. D., Reed L. L., and Woo S. L. (1987) Functional domains and evolution of aromatic amino acid hydroxylases. Proc. Natl. Acad. Sci. USA 84, 5530-5534.
16. Grima B., Lamouroux A., Blanot F., Biguet N. F., and Mallet J. (1985) Complete coding sequence of rat tyrosine hydroxylase mRNA. Proc. Natl. Acad. Sci. USA 82, 617-621.
17. Haavik J. (1997) L-DOPA is a substrate for tyrosine hydroxylase. J. Neurochem. 69, 1720-1728.
18. Haavik J., Martinez A., and Flatmark T. (1990) pH-dependent release of catecholamines from tyrosine hydroxylase and the effect of phosphorylation of Ser-40. FEBS Lett. 262, 363-365.
19. Haavik J., Le Bourdelles B., Martinez A., Flatmark T., and Mallet J. (1991) Recombinant human tyrosine hydroxylase isoforms: reconstitution with iron and inhibitory effect of other metal ions. Eur. J. Biochem. 199, 371-378.
20. Haavik J., Almås B., and Flatmark T. (1997) Generation of reactive oxygen species by tyrosine hydroxylase: a possible contribution to the degeneration of dopaminergic neurons? J. Neurochem. 68, 328-332.
21. Halliwell B. (1992) Reactive oxygen species and central nervous system. J. Neurochem. 59, 1609-1623.
22. 3H]dopamine: impact of ascorbic acid and glutathione. J. Neurochem. 63, 1126-1132.
23. Hastings T. G., Lewis D. A., and Zigmond M. J. (1996a) Reactive dopamine metabolites and neurotoxicity. Adv. Exp. Med. Biol. 387, 97-106.
24. Hastings T. G., Lewis D. A., and Zigmond M. J. (1996b) The role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc. Natl. Acad. Sci. USA 93, 1956-1961.
25. Jenner P. and Olanow C. W. (1998) Understanding cell death in Parkinson's disease. Ann. Neurol. 44 (Suppl. 1), S72-S84.
26. Jenner P., Dexter D. T., Sian J., Schapira A. H. V., and Marsden C. D. (1992) Oxidative stress as a cause of nigral cell death in Parkinson's disease and incidental Lewy body disease. The Royal Kings and Queens Parkinson's Disease Research Group. Ann. Neurol. 32 (Suppl.), S82-S87.
27. Kato T., Ito S., and Fujita K. (1986) Tyrosinase-catalyzed binding of 3,4-dihydroxyphenylalanine with proteins through the sulfhydryl group. Biochim. Biophys. Acta 881, 415-421.
28. Kuhn D. M. and Arthur R. E. Jr. (1998) Dopamine inactivates tryptophan hydroxylase and forms a redox-cycling quinoprotein: possible endogenous toxin to serotonin neurons. J. Neurosci. 15, 7111-7117.
29. Kuhn D. M. and Billingsley M. L. (1987) Tyrosine hydroxylase: purification from PC12 cells, characterization, and production of antibodies. Neurochem. Int. 11, 463-475.
30. Kuhn D. M., Ruskin B., and Lovenberg W. (1980) Tryptophan hydroxylase: the role of oxygen, iron, and sulfhydryl groups as determinants of stability and catalytic activity. J. Biol. Chem. 255, 4137-4143.
31. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
32. LaVoie M. J. and Hastings T. G. (1999) Dopamine quinone formation and protein modification associated with the striatal neurotoxicity of methamphetamine: evidence against a role for extracellular dopamine. J. Neurosci. 19, 1484-1491.
33. Lerner P., Nose P., Ames M. M., and Lovenberg W. (1978) Modification of the tyrosine hydroxylase assay: increases in enzyme activity in the presence of ascorbic acid. Neurochem. Res. 3, 641-651.
34. Maker H. S., Weiss C., Silides D. J., and Cohen D. (1981) Coupling of dopamine oxidation (monoamine oxidase activity) to glutathione oxidation via the generation of hydrogen peroxide in rat brain homogenates. J. Neurochem. 36, 589-593.
35. Martinez A., Haavik J., Flatmark T., Arrondo J. L. R., and Muga A. (1996) Conformational properties and stability of tyrosine hydroxylase studied by infrared spectroscopy: effect of iron/catecholamine binding and phosphorylation. J. Biol. Chem. 271, 19737-19742.
36. Miller D. M., Buettner G. R., and Aust S. D. (1990) Transition metals as catalysts of "autooxidation" reactions. Free Radic. Biol. Med. 8, 95-108.
37. Nappi A. J., Vass E., Prota G., and Memoli S. (1995) The effects of hydroxyl radical attack on dopa, dopamine, 6-hydroxydopa, and 6-hydroxydopamine. Pigment Cell Res. 8, 283-293.
38. Paz M. A., Fluckiger R., Boak A., Kagan H. M., and Gallop P. M. (1991) Specific detection of quinoproteins by redox-cycling staining. J. Biol. Chem. 266, 689-692.
39. Rabinovic A. D. and Hastings T. G. (1998) Role of endogenous glutathione in the oxidation of dopamine. J. Neurochem. 71, 2071-2078.
40. 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.
41. Ribeiro P., Wang Y., Citron B. A., and Kaufman S. (1992) Regulation of recombinant rat tyrosine hydroxylase by dopamine. Proc. Natl. Acad. Sci. USA 89, 9593-9597.
42. Riddles P. W., Blakeley R. L., and Zerner B. (1983) Reassessment of Ellman's reagent. Methods Enzymol. 91, 49-60.
43. Riederer P., Sofic E., Rausch W.-D., Schmidt B., Reynolds G. P., Jellinger K., and Youdim M. B. H. (1989) Transition metals, ferritin, glutathione, and ascorbic acid in parkinsonian brains. J. Neurochem. 52, 515-520.
44. Rosengren E., Linder-Eliasson E., and Carlsson A. (1985) Detection of 5-S-cysteinyldopamine in human brain. J. Neural Transm. 63, 247-253.
45. Rowe D. B., Le W., Smith R. G., and Appel S. H. (1998) Antibodies from patients with Parkinson's disease react with protein modified by dopamine oxidation. J. Neurosci. Res. 53, 551-558.
46. Simonian N. A. and Coyle J. T. (1996) Oxidative stress in neuro-degenerative diseases. Annu. Rev. Pharmacol. Toxicol. 36, 83-106.
47. Simpson J. A., Narita S., Geiseg S., Gebicki S., and Dean R. T. (1992) Long-lived reactive species on free-radical-damaged proteins. Biochem. J. 282, 621-624.
48. Simpson J. A., Geiseg S. P., and Dean R. T. (1993) Free radical and enzymatic mechanisms for the generation of protein bound reducing moieties. Biochim. Biophys. Acta 1156, 190-196.
49. Smythies J. and Galzigna L. (1998) The oxidative metabolism of catecholamines in the brain: a review. Biochim. Biophys. Acta 1380, 159-162.
50. Spencer J. P. E., Jenner P., Daniel S. E., Lees A. J., Marsden D. C., and Halliwell B. (1998) Conjugates of catecholamines with cysteine and GSH in Parkinson's disease: possible mechanisms of formation involving reactive oxygen species. J. Neurochem. 71, 2112-2122.
51. Stone D. M., Hanson G. R., and Gibb J. W. (1989a) In vitro reactivation of rat cortical tryptophan hydroxylase following in vivo inactivation by methylenedioxymethamphetamine. J. Neurochem. 53, 572-581.
52. Stone D. M., Johnson M., Hanson G. R., and Gibb J. W. (1989b) Acute inactivation of tryptophan hydroxylase by amphetamine analogs involves the oxidation of sulfhydryl sites. Eur. J. Pharmacol. 172, 93-97.
53. Van Gelder B. F. and Slater E. C. (1962) The extinction coefficient of cytochrome c. Biochim. Biophys. Acta 58, 593-595.
54. Van Iwaarden P. R., Driessen A. J. M., and Konings W. N. (1992) What we can learn from the effects of thiol reagents on transport proteins. Biochim. Biophys. Acta 1113, 161-170.
55. Wood J. M. and Schallreuter K. U. (1991) Studies on the reactions between human tyrosinase, superoxide anion, hydrogen peroxide and thiols. Biochim. Biophys. Acta 1074, 378-385.
56. Xu Y., Stokes A. H., Roskoski R. Jr., and Vrana K. E. (1998) Dopamine, in the presence of tyrosinase, covalently modifies and inactivates tyrosine hydroxylase. J. Neurosci. Res. 54, 691-697.
57. Zeevalk G. D., Bernard L. P., and Nicklas W. J. (1998) Role of oxidative stress and the glutathione system in loss of dopamine neurons due to impairment of energy metabolism. J. Neurochem. 70, 1421-1430.