Inhibition of the Fe(III)-catalyzed dopamine oxidation by ATP and its relevance to oxidative stress in Parkinson's disease

ACS Chemical Neuroscience

Volumn 4, Issue 9, 2013, Pages 1305-1313

  Jiang, Dianlu ^a   Shi, Shuyun ^a   Zhang, Lin ^a   Liu, Lin ^a   Ding, Bingrong ^a   Zhao, Bingqing ^a   Yagnik, Gargey ^a   Zhou, Feimeng ^a  

^a CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

ATP; catalytic oxidation; dopamine; inhibition; iron; Parkinson's disease

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; ADENOSINE TRIPHOSPHATE; DOPAMINE; FERRITIN; IRON; OXYGEN;

ARTICLE; BRAIN; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IRON STORAGE; OXIDATION; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; SUBSTANTIA NIGRA; SYNAPSE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CATALYSIS; CELLS, CULTURED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DOPAMINE; ELECTROCHEMISTRY; FERRIC COMPOUNDS; FERRITINS; MACROMOLECULAR SUBSTANCES; MASS SPECTROMETRY; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXIDOPAMINE; PARKINSON DISEASE; RATS; SUBSTANTIA NIGRA;

EID: 84884381007     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn400105d     Document Type: Article

References (52)

1. Moore, D. J., West, A. B., Dawson, V. L., and Dawson, T. M. (2005) Molecular pathophysiology of Parkinson′s disease Annu. Rev. Neurosci. 28, 57-87
2. Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R., and Goedert, M. (1997) a-Synuclein in Lewy bodies Nature 388, 839-840
3. Malkus, K. A., Tsika, E., and Ischiropoulos, H. (2009) Oxidative modifications, mitochondrial dysfunction, and impaired protein degradation in Parkinson′s disease: how neurons are lost in the Bermuda triangle Mol. Neurodegener. 4, 24-40
4. Luo, Y., Umegaki, H., Wang, X., Abe, R., and Roth, G. S. (1998) Dopamine induces apoptosis through an oxidation-involved SAPK/JNK activation pathway J. Biol. Chem. 273, 3756-3764
5. Irwin, I. and Langston, J. W. (1995) Endogenous toxins as potential etiologic agents in Parkinson′s disease, pp 153-201, Marcel Dekker, New York.
6. Graham, D. G. (1978) Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones Mol. Pharmacol. 14, 633-643
7. Napolitano, A., Pezzella, A., and Prota, G. (1999) New reaction pathways of dopamine under oxidative stress conditions: nonenzymatic iron-assisted conversion to norepinephrine and the neurotoxins 6-hydroxydopamine and 6,7-dihydroxytetrahydroisoquinoline Chem. Res. Toxicol. 12, 1090-1097
8. Pezzella, A., d'Ischia, M., Napolitano, A., Misuraca, G., and Prota, G. (1997) Iron-mediated generation of the neurotoxin 6-hydroxydopamine quinone by reaction of fatty acid hydroperoxides with dopamine: a possible contributory mechanism for neuronal degeneration in Parkinson′s disease J. Med. Chem. 40, 2211-2216
9. 2+, and relevance to Parkinson disease J. Biol. Chem. 280, 15587-15594
10. Sulzer, D. and Zecca, L. (2000) Intraneuronal dopamine-quinone synthesis: a review Neurotoxic. Res. 1, 181-195
11. Kuhar, M. J., Minnema, K., and Muly, E. C. (2006) Catecholamines. In Basic Neurochemistry: Molecular, Cellular, and Medical Aspects (Siegel, G. J., Albers, R. W., Brady, S. T., and Price, D. L., Eds.), Elsevier Academic Press, New York.
12. Clark, D. L., Boutros, N. N., and Mendez, M. F. (2005) The brain and behavior: An introduction to behavioval neuroanatomy, p 255, Cambridge University Press, New York.
13. Elsworth, J. D. and Roth, R. H. (1997) Dopamine synthesis, uptake, metabolism, and receptors: relevance to gene therapy of Parkinson′s disease Exp. Neurol. 144, 4-9
14. Erickson, J. D., Eiden, L. E., and Hoffman, B. J. (1992) Distinct pharmacological properties and distribution in neurons and endocrine cells of two isoforms of the human vesicular monoamine transporter Proc. Natl. Acad. Sci. U.S.A. 89, 10993-10997
15. McKie, A. T., Barrow, D., Latunde-Dada, G. O., Rolfs, A., Sager, G., Mudaly, E., Mudaly, M., Richardson, C., Barlow, D., Bomford, A., Peters, T. J., Raja, K. B., Shirali, S., Hediger, M. A., Farzaneh, F., and Simpson, R. J. (2001) An iron-regulated ferric reductase associated with the absorption of dietary iron Science 291, 1755-1759
16. Ward, R. J. and Crichton, R. R. (2006) Iron and Its Role in Neurodegenerative Diseases. In Neurodegenertive Diseases and Metal Ions (Sigel, A., Sigel, H., and Sigel, R. K. O., Eds.), Vol. 1, John Wiley & Sons Ltd, West Sussex.
17. Götz, M. E., Double, K., Gerlach, M., Youdim, M. B., and Riederer, P. (2004) The relevance of iron in the pathogenesis of Parkinson′s disease Ann. N.Y. Acad. Sci. 1012, 193-208
18. Golts, N., Snyder, H., Frasier, M., Theisler, C., Choi, P., and Wolozin, B. (2002) Magnesium inhibits spontaneous and iron-induced aggregation of α-synuclein J. Biol. Chem. 277, 16116-16123
19. Paris, I., Martinez-Alvarado, P., Crdenas, S., Perez-Pastene, C., Graumann, R., Fuentes, P., Olea-Azar, C., Caviedes, P., and Segura-Aguilar, J. (2005) Dopamine-dependent iron toxicity in cells derived from rat hypothalamus Chem. Res. Toxicol. 18, 415-419
20. Velez-Pardo, C., Jimenez Del Rio, M., Verschueren, H., Ebinger, G., and Vauquelin, G. (1997) Dopamine and iron induce apoptosis in PC12 cells Pharmacol. Toxicol. 80, 76-84
21. Hermida-Ameijeiras, A., Méndez-Alvarez, E., Sánchez- Iglesias, S., Sanmartín-Suárez, C., and Soto-Otero, R. (2004) Autoxidation and MAO-mediated metabolism of dopamine as a potential cause of oxidative stress: role of ferrous and ferric ions Neurochem. Int. 45, 103-116
22. Linert, W., Herlinger, E., Jameson, R. F., Kienzl, E., Jellinger, K., and Youdim, M. B. H. (1996) Dopamine, 6-hydroxydopamine, iron, and dioxygen-their mutual interactions and possible implication in the development of Parkinson′ s disease Biochim. Biophys. Acta 1316, 160-168
23. Linert, W. and Jameson, G. N. L. (2000) Redox reactions of neurotransmitters possibly involved in the progression of Parkinson′s Disease J. Inorg. Biochem. 79, 319-326
24. Ortega, R., Cloetens, P., Devès, G., Carmona, A., and Bohic, S. (2007) Iron storage within dopamine neurovesicles revealed by chemical nano-imaging PLoS One 2, e925
25. Sidhu, A., Wersinger, C., and Vernier, P. (2004) Does a-synuclein modulate dopaminergic synaptic content and tone at the synapse? FASEB J. 18, 637-647
26. Linert, W., Jameson, G. N. L., Jameson, R. F., and Jellinger, K. A. (2006) The Chemical Interplay between Catecholamines and Metal Ions in Neurological Diseases. In Metal Ions In Life Sciences (Sigel, A., Sigel, H., and Sigel, R. K. O., Eds.), Vol. 1, pp 281-315, John Wiley & Sons Ltd, West Sussex.
27. Kakhlon, O. and Cabantchik, Z. I. (2002) The labile iron pool: characterization, measurement, and participation in cellular processes Free Radical Biol. Med. 33, 1037-1046
28. Beis, I. and Newsholme, E. A. (1975) The contents of adenine nucleotides, phosphagens and some glycolytic intermediates in resting muscles from vertebrates and invertebrates Biochem. J. 152, 23-32
29. Ebadi, M. and Pfeiffer, R. F. (2005) Parkinson′s Disease, CRC Press, Boca Raton, FL.
30. Burnstock, G. (2007) Physiology and pathophysiology of purinergic neurotransmission Physiol. Rev. 87, 659-797
31. 2- redox couple Inorg. Chem. 31, 870-877
32. Arreguin, S., Nelson, P., Padway, S., Shirazi, M., and Pierpont, C. (2009) Dopamine complexes of iron in the etiology and pathogenesis of Parkinson′s disease J. Inorg. Biochem. 103, 87-93
33. Charkoudian, L. K. and Franz, K. J. (2006) Fe(III)-coordination properties of neuromelanin components: 5,6-dihydroxyindole and 5,6-dihydroxyindole-2-carboxylic Acid Inorg. Chem. 45, 3657-3664
34. 4+ chelates of ampicillin, dopamine and α-methyl L-dopa in aqueous medium Anal. Lett. 17, 205-216
35. Costas, M., Mehn, M. P., Jensen, M. P., and Que, L., Jr. (2004) Dioxygen activation at mononuclear nonheme iron active sites: enzymes, models, and intermediates Chem. Rev. 104, 939-986
36. Hawley, M. D., Tatawawadi, S. V., Piekarski, S., and Adarns, R. N. (1967) Electrochemical studies of the oxidation pathways of catecholamines J. Am. Chem. Soc. 89, 447-450
37. Young, T. E. and Babbitt, B. W. (1983) Electrochemical study of the oxidation of a-methyldopamine, a-methylnoradrenaline, and dopamine J. Org. Chem. 48, 562-566
38. Chen, S.-M. and Peng, K.-T. (2003) The electrochemical properties of dopamine, epinephrine, norepinephrine, and their electrocatalytic reactions on cobalt(II) hexacyanoferrate films J. Electroanal. Chem. 547, 179-189
39. Bard, A. J. and Faulkner, L. R. (2001) Electrochemical Methods. Fundamentals and Applications, John Wiley and Sons, New York.
40. Shen, X.-M. and Dryhurst, G. (1998) Iron- and manganese-catalyzed autoxidation of dopamine in the presence of L-Cysteine: possible insights into iron- and manganese-mediated dopaminergic neurotoxicity Chem. Res. Toxicol. 11, 824-837
41. Napolitano, A., Pezzella, A., and Prota, G. (1999) 6,7-Dihydroxy-l,2,3,4- tetrahydroisoquinoline formation by iron mediated dopamine oxidation: a novel route to endogenous neurotoxins under oxidative stress conditions Tetrahedron lett. 40, 2833-2836
42. Abu-Omar, M. M., Loaiza, A., and Hontzeas, N. (2005) Reaction mechanisms of mononuclear non-heme iron oxygenases Chem. Rev. 105, 2227-2252
43. Cox, D. D. and Que, L., Jr. (1988) Functional models for catechol 1,2-dioxygenase: the role of the iron(III) center J. Am. Chem. Soc. 110, 8085-8092
44. Snyder, A. M. and Connor, J. R. (2009) Iron, the substantia nigra and related neurological disorders Biochim. Biophys. Acta 1790, 606-614
45. Hill, J. M. (1988) The distribution of iron in the brain. In Brain Iron: Neurochemistry and Behavioural Aspects (Youdim, M. B. H., Ed.), pp 1-24, Taylor and Francis, London.
46. Erikson, K. M., Pinero, D. J., Connor, J. R., and Beard, J. L. (1997) Regional brain iron, ferritin and transferrin concentrations during iron deficiency and iron repletion in developing rats J. Nutr. 127, 2030-2038
47. Singleton, A. B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R., Lincoln, S., Crawley, A., Hanson, M., Maraganore, D., Adler, C., Cookson, M. R., Muenter, M., Baptista, M., Miller, D., Blancato, J., Hardy, J., and Gwinn-Hardy, K. (2003) α-Synuclein Locus Triplication Causes Parkinson′s Disease Science 302, 841
48. Spillantini, M. G., Crowther, R. A., Jakes, R., Hasegawa, M., and Goedert, M. (1998) α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson′s disease and dementia with Lewy bodies Proc. Natl. Acad. Sci. U.S.A. 95, 6469-6473
49. Nakamura, K., Bindokas, V. P., Marks, J. D., Wright, D. A., Frim, D. M., Miller, R. J., and Kang, U. J. (2000) The selective toxicity of 1-methyl-4-phenylpyridinium to dopaminergic neurons: the role of mitochondrial complex I and reactive oxygen species revisited Mol. Pharmacol. 58, 271-278
50. Mizuno, Y., Suzuki, K., and Sone, N. (1990) Inhibition of ATP synthesis by 1-methyl-4-phenylpyridinium ion (MPP+) in mouse brain in vitro and in vivo Adv. Neurol. 53, 197-200
51. Dooley, C. T., Li, L., Misler, J. A., and Thompson, J. H. (2012) Toxicity of 6-hydroxydopamine: live cell imaging of cytoplasmic redox flux Cell Biol. Toxicol. 28, 89-101
52. Hanrott, K., Gudmunsen, L., O'Neill, M. J., and Wonnacott, S. (2006) 6-Hydroxydopamine-induced apoptosis is mediated via extracellular auto-oxidation and caspase 3-dependent activation of protein kinase Cδ J. Biol. Chem. 281, 5373-5382