Products of oxidative stress inhibit aldehyde oxidation and reduction pathways in dopamine catabolism yielding elevated levels of a reactive intermediate

Chemical Research in Toxicology

Volumn 22, Issue 5, 2009, Pages 835-841

  Jinsmaa, Yunden ^a   Florang, Virginia R ^a   Rees, Jennifer N ^a   Anderson, David G ^a   Strack, Stefan ^b   Doorn, Jonathan A ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3,4 DIHYDROXYPHENYLACETALDEHYDE; 4 HYDROXYNONENAL; ACETALDEHYDE; ALDEHYDE; AMINE OXIDASE (FLAVIN CONTAINING); DOPAMINE; MALONALDEHYDE; NERVE GROWTH FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BIOTRANSFORMATION; CATABOLISM; CELL DIFFERENTIATION; CELL VIABILITY; CHEMICAL REACTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; OXIDATIVE STRESS;

3,4-DIHYDROXYPHENYLACETIC ACID; ALDEHYDE REDUCTASE; ALDEHYDES; ANIMALS; DOPAMINE; LIPID PEROXIDATION; MALONDIALDEHYDE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PC12 CELLS; PHENYLETHYL ALCOHOL; RATS;

EID: 67649949078     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx800405v     Document Type: Article

References (44)

1. Jenner, P. (2003) Oxidative stress in Parkinson's disease. Ann. Neurol. 53 (Suppl. 3), S26-36; discussion S36-28.
2. Landrigan, P. J., Sonawane, B., Butler, R. N., Trasande, L., Callan, R., and Droller, D. (2005) Early environmental origins of neurodegenerative disease in later life. Environ. Health Perspect. 113, 1230-1233.
3. Drechsel, D. A., and Patel, M. (2008) Role of reactive oxygen species in the neurotoxicity of environmental agents implicated in Parkinson's disease. Free Radical Biol. Med. 44, 1873-1886.
4. Yoritaka, A., Hattori, N., Uchida, K., Tanaka, M., Stadtman, E. R., and Mizuno, Y. (1996) Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease. Proc. Natl. Acad. Sci. U.S.A. 93, 2696-2701.
5. Dexter, D. T., Carter, C. J., Wells, F. R., Javoy-Agid, F., Agid, Y., Lees, A., Jenner, P., and Marsden, C. D. (1989) Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease. J. Neurochem. 52, 381-389.
6. Esterbauer, H., Schaur, R. J., and Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biol. Med. 11, 81-128.
7. Mitchell, D. Y., and Petersen, D. R. (1991) Inhibition of rat hepatic mitochondrial aldehyde dehydrogenase-mediated acetaldehyde oxidation by trans-4-hydroxy-2-nonenal. Hepatology 13, 728-734.
8. Hjelle, J. J., Grubbs, J. H., and Petersen, D. R. (1982) Inhibition of mitochondrial aldehyde dehydrogenase by malondialdehyde. Toxicol. Lett. 14, 35-43.
9. Florang, V. R., Rees, J. N., Brogden, N. K., Anderson, D. G., Hurley, T. D., and Doorn, J. A. (2007) Inhibition of the oxidative metabolism of 3,4-dihydroxyphenylacetaldehyde, a reactive intermediate of dopamine metabolism, by 4-hydroxy-2-nonenal. Neurotoxicology 28, 76-82.
10. Marchitti, S. A., Deitrich, R. A., and Vasiliou, V. (2007) Neurotoxicity and metabolism of the catecholamine-derived 3,4-dihydroxyphenylacetaldehyde and 3,4-dihydroxyphenylglycolaldehyde: The role of aldehyde dehydrogenase. Pharmacol. Rev. 59, 125-150.
11. 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.
12. Turner, A. J., Illingworth, J. A., and Tipton, K. F. (1974) Simulation of biogenic amine metabolism in the brain. Biochem. J. 144, 353-360.
13. Rees, J. N., Florang, V. R., Anderson, D. G., and Doorn, J. A. (2007) Lipid peroxidation products inhibit dopamine catabolism yielding aberrant levels of a reactive intermediate. Chem. Res. Toxicol. 20, 1536-1542.
14. Burke, W. J., Li, S. W., Chung, H. D., Ruggiero, D. A., Kristal, B. S., Johnson, E. M., Lampe, P., Kumar, V. B., Franko, M., Williams, E. A., and Zahm, D. S. (2004) Neurotoxicity of MAO metabolites of catecholamine neurotransmitters: role in neurodegenerative diseases. Neurotoxicology 25, 101-115.
15. Burke, W. J., Li, S. W., Williams, E. A., Nonneman, R., and Zahm, D. S. (2003) 3,4-Dihydroxyphenylacetaldehyde is the toxic dopamine metabolite in vivo: Implications for Parkinson's disease pathogenesis. Brain Res. 989, 205-213.
16. Helander, A., and Tottmar, O. (1989) Reactions of biogenic aldehydes with hemoglobin. Alcohol 6, 71-75.
17. Nilsson, G. E., and Tottmar, O. (1987) Biogenic aldehydes in brain: on their preparation and reactions with rat brain tissue. J. Neurochem. 48, 1566-1572.
18. Pittman, R. N., Wang, S., DiBenedetto, A. J., and Mills, J. C. (1993) A system for characterizing cellular and molecular events in programmed neuronal cell death. J. Neurosci. 13, 3669-3680.
19. Shafer, T. J., and Atchison, W. D. (1991) Transmitter, ion channel and receptor properties of pheochromocytoma (PC12) cells: A model for neurotoxicological studies. Neurotoxicology 12, 473-492.
20. Kitazawa, M., Anantharam, V., and Kanthasamy, A. G. (2001) Dieldrin-induced oxidative stress and neurochemical changes contribute to apoptopic cell death in dopaminergic cells. Free Radical Biol. Med. 31, 1473-1485.
21. Naoi, M., Takahashi, T., and Nagatsu, T. (1988) Effect of 1-methyl-4-phenylpyridinium ion (MPP+) on catecholamine levels and activity of related enzymes in clonal rat pheochromocytoma PC12h cells. Life Sci 43, 1485-1491.
22. Gardner, H. W., Bartelt, R. J., and Weisleder, D. (1992) A facile synthesis of 4-hydroxy-2(E)-nonenal. Lipids 27, 686-689.
23. Ungar, F., Tabakoff, B., and Alivisatos, S. G. (1973) Inhibition of binding of aldehydes of biogenic amines in tissues. Biochem. Pharmacol. 22, 1905-1913.
24. Burke, W. J. (2003) 3,4-Dihydroxyphenylacetaldehyde: A potential target for neuroprotective therapy in Parkinson's disease. Curr. Drug Targets CNS Neurol. Disord. 2, 143-148.
25. Kristal, B. S., Conway, A. D., Brown, A. M., Jain, J. C., Ulluci, P. A., Li, S. W., and Burke, W. J. (2001) Selective dopaminergic vulnerability: 3,4-Dihydroxyphenylacetaldehyde targets mitochondria. Free Radical Biol. Med. 30, 924-931.
26. Lamensdorf, I., Eisenhofer, G., Harvey-White, J., Nechustan, A., Kirk, K., and Kopin, I. J. (2000) 3,4-Dihydroxyphenylacetaldehyde potentiates the toxic effects of metabolic stress in PC12 cells. Brain Res. 868, 191-201.
27. Mattammal, M. B., Haring, J. H., Chung, H. D., Raghu, G., and Strong, R. (1995) An endogenous dopaminergic neurotoxin: Implication for Parkinson's disease. Neurodegeneration 4, 271-281.
28. Lamensdorf, I., Eisenhofer, G., Harvey-White, J., Hayakawa, Y., Kirk, K., and Kopin, I. J. (2000) Metabolic stress in PC12 cells induces the formation of the endogenous dopaminergic neurotoxin, 3,4-dihydroxyphenylacetaldehyde. J. Neurosci. Res. 60, 552-558.
29. Jia, Z., Zhu, H., Misra, H. P., and Li, Y. (2008) Potent induction of total cellular GSH and NQO1 as well as mitochondrial GSH by 3H-1,2-dithiole-3- thione in SH-SY5Y neuroblastoma cells and primary human neurons: Protection against neurocytotoxicity elicited by dopamine, 6-hydroxydopamine, 4-hydroxy-2-nonenal, or hydrogen peroxide. Brain Res. 1197, 159-169.
30. Dixit, B. L., Balendiran, G. K., Watowich, S. J., Srivastava, S., Ramana, K. V., Petrash, J. M., Bhatnagar, A., and Srivastava, S. K. (2000) Kinetic and structural characterization of the glutathione-binding site of aldose reductase. J. Biol. Chem. 275, 21587-21595.
31. O'Connor, T., Ireland, L. S., Harrison, D. J., and Hayes, J. D. (1999) Major differences exist in the function and tissue-specific expression of human aflatoxin B1 aldehyde reductase and the principal human aldo-keto reductase AKR1 family members. Biochem. J. 343 (Part 2), 487-504.
32. Burczynski, M. E., Sridhar, G. R., Palackal, N. T., and Penning, T. M. (2001) The reactive oxygen species - and Michael acceptor-inducible human aldo-keto reductase AKR1C1 reduces the alpha,beta-unsaturated aldehyde 4-hydroxy-2-nonenal to 1,4-dihydroxy-2-nonene. J. Biol. Chem. 276, 2890-2897.
33. Koh, Y. H., Park, Y. S., Takahashi, M., Suzuki, K., and Taniguchi, N. (2000) Aldehyde reductase gene expression by lipid peroxidation end products, MDA and HNE. Free Radical Res. 33, 739-746.
34. Yamaoka, T., Matsuura, Y., Yamashita, K., Tanimoto, T., and Nishimura, C. (1992) Site-directed mutagenesis of His-42, His-188 and Lys-263 of human aldose reductase. Biochem. Biophys. Res. Commun. 183, 327-333.
35. Tarle, I., Borhani, D. W., Wilson, D. K., Quiocho, F. A., and Petrash, J. M. (1993) Probing the active site of human aldose reductase. Sitedirected mutagenesis of Asp-43, Tyr-48, Lys-77, and His-110. J. Biol. Chem. 268, 25687-25693.
36. McGeer, P. L., and McGeer, E. G. (2008) Glial reactions in Parkinson's disease. Mov. Disord. 23, 474-483.
37. Burke, W. J., Kumar, V. B., Pandey, N., Panneton, W. M., Gan, Q., Franko, M. W., O'Dell, M., Li, S. W., Pan, Y., Chung, H. D., and Galvin, J. E. (2008) Aggregation of alpha-synuclein by DOPAL, the monoamine oxidase metabolite of dopamine. Acta Neuropathol. 115, 193-203.
38. Graham, D. G. (1978) Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol. Pharmacol. 14, 633-643.
39. Graham, D. G., Tiffany, S. M., Bell, W. R., Jr., and and Gutknecht, W. F. (1978) Autoxidation 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. 14, 644-653.
40. LaVoie, M. J., Ostaszewski, B. L., Weihofen, A., Schlossmacher, M. G., and Selkoe, D. J. (2005) Dopamine covalently modifies and functionally inactivates parkin. Nat. Med. 11, 1214-1221.
41. Hastings, T. G., and Zigmond, M. J. (1994) Identification of catecholprotein conjugates in neostriatal slices incubated with [3H]dopamine: Impact of ascorbic acid and glutathione. J. Neurochem. 63, 1126-1132.
42. Tse, D. C., McCreery, R. L., and Adams, R. N. (1976) Potential oxidative pathways of brain catecholamines. J. Med. Chem. 19, 37-40.
43. Bisaglia, M., Mammi, S., and Bubacco, L. (2007) Kinetic and structural analysis of the early oxidation products of dopamine: Analysis of the interactions with alpha-synuclein. J. Biol. Chem. 282, 15597-15605.
44. Hastings, T. G. (1995) Enzymatic oxidation of dopamine: the role of prostaglandin H synthase. J. Neurochem. 64, 919-924.