The neurotoxicity of DOPAL: Behavioral and stereological evidence for its role in Parkinson disease pathogenesis

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Panneton, W Michael ^a   Kumar, V B ^a   Gan, Qi ^a   Burke, William J ^a   Galvin, James E ^b  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3,4 DIHYDROXYPHENYLACETALDEHYDE; DOPAMINE DERIVATIVE; PHOSPHATE BUFFERED SALINE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; 3,4 DIHYDROXYPHENYLACETIC ACID; 3,4-DIHYDROXYPHENYLACETALDEHYDE; DOPAMINE; DRUG DERIVATIVE; GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CELL SURVIVAL; CIRCLING BEHAVIOR; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LOCOMOTION; MALE; NERVE CELL; NERVE ENDING; NEUROTOXICITY; NONHUMAN; OPTICAL DENSITY; PARKINSON DISEASE; PATHOGENESIS; QUANTITATIVE ANALYSIS; RAT; STEREOLOGY; STEREOTACTIC PROCEDURE; SUBSTANTIA NIGRA; SUBSTANTIA NIGRA PARS COMPACTA; SUBSTANTIA NIGRA PARS RETICULATA; ANIMAL; DRUG EFFECT; METABOLISM; METHODOLOGY; MICROGLIA; PHENOTYPE; SPRAGUE DAWLEY RAT;

ANIMALIA; RATTUS;

3,4-DIHYDROXYPHENYLACETIC ACID; ANIMALS; BEHAVIOR, ANIMAL; DOPAMINE; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; NEURONS; PARKINSON DISEASE; PHENOTYPE; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE;

EID: 78650789638     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015251     Document Type: Article

References (73)

1. Eriksen JL, Dawson TM, Dickson DW, Petrucelli L (2003) Caught in the act: asynuclein is the culprit in Parkinson's disease. Neuron 40: 453-456.
2. Terzioglu M, Galter D (2008) Parkinson's disease: genetic versus toxin-induced rodent models. FEBS J 275: 1384-1391.
3. Fleming SM, Fernagut PO, Chesselet MF (2005) Genetic mouse models of parkinsonism: strengths and limitations. NeuroRx 2: 495-503.
4. McCormack AL, Atienza JG, Langston JW, Di Monte DA (2006) Decreased susceptibility to oxidative stress underlies the resistance of specific dopaminergic cell populations to paraquat-induced degeneration. Neuroscience 141: 929-937.
5. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, et al. (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci. pp 1301-1306.
6. Langston JW, Ballard P, Tetrud JW, Irwin I (1983) Chronic parkinsonism in humans due to a product meperidine-analog synthesis. Science 219: 979-980.
7. Whitton PS (2007) Inflammation as a causative factor in the aetiology of Parkinson's disease. Br J Pharmacol 150: 963-976.
8. Tansey MG, McCoy MK, Frank-Cannon TC (2007) Neuroinflammatory mechanisms in Parkinson's disease: Potential environmental triggers, pathways, and targets for early therapeutic intervention. Exp Neur 208: 1-25.
9. Hald A, Van Beek J, Lotharius J (2007) Inflammation in Parkinson's Disease. In: Harris RE, ed. Springer. pp 249-279.
10. Reichmann H, Janetzky B (2000) Mitochondrial dysfunction-a pathogenetic factor in Parkinson's disease. J Neurol 247: 1163-1168.
11. Abou-Sleiman PM, Muqit MM, Wood NW (2006) Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat Rev Neurosci 7: 207-219.
12. Caudle WM, Richardson JR, Wang MZ, Taylor TN, Guillot TS, et al. (2007) Reduced vesicular storage of dopamine causes progressive nigrostriatal neurodegeneration. J Neurosci 27: 8138-8148.
13. Taylor TN, Caudle WM, Shepherd KR, Noorian A, Jackson CR, et al. (2009) Nonmotor symptoms of Parkinson's disease revealed in an animal model with reduced monoamine storage capacity. J Neurosci 29: 8103-8113.
14. Plaitakis A, Shashidharan P (2000) Glutamate transport and metabolism in dopaminergic neurons of substantia nigra: implications for the pathogenesis of Parkinson's disease. J Neurol 247: 1125-1135.
15. Blandini F, Porter RH, Greenamyre JT (1996) Glutamate and Parkinson's disease. Mol Neurobiol 12: 73-94.
16. Blashko H (1952) Amine oxidase and amine metabolism. Pharmacol Rev 4: 415-453.
17. Fahn S (1997) L-DOPA induced neurotoxicity. CNS Drugs 8: 376-393.
18. Burke WJ, Chung HD, Li SW (1999) Quantitation of 3,4-dihydroxyphenylacetylaldehyde and 3,4-dihydroxyphenylglycoaldehyde, the monoamine oxidase metabolites of dopamine and neuroadrenaline in human tissues by microcolumn high-performance liquid chromatography. Anal Biochem 273: 111-116.
19. Kristal BS, Conway AD, Brown AM, Jain JC, Ulluci PA, Li SW, et al. (2001) Selective dopaminergic vulnerability: 3,4-dihydroxyphenylacetaldehyde targets mitochondria. Free Radical Biol Med 30: 924-931.
20. Burke WJ, Li SW, Williams EA, Nonneman R, Zahm DS (2003) 3,4-Dihydroxyphenylacetaldehyde is the toxic dopamine metabolite in vivo: implication for Parkinson's disease pathogenesis. Brain Res 989: 205-213.
21. Burke WJ, Kumar VB, Panneton WM, Gan Q, Pandey, et al. (2008) Aggregation of-synuclein aggregation by DOPAL, the monoamine oxidase metabolite of dopamine. Acta Neurpoathol 115: 193-203.
22. Lamensdorf I, Eisenhofer G, Harvey-White J, Hayakawa Y, Kirk K, et al. (2000) Metabolic stress in PC12 cells induces the formation of the endogenous dopaminergic neurotoxin, 3,4-dihydroxyphenylacetaldehyde. J Neurosci Res 60: 552-558.
23. Lamensdorf I, Eisenhofer G, Harvey-White J, Nechustan A, Kirk K, et al. (2000) 3,4-Dihydroxyphenylacetaldehyde potentiates the toxic effects of metabolic stress in PC12 cells. Brain Res 868: 191-201.
24. Volles MJ, Lee SJ, Rochet JC, Shtilerman MD, Ding TT, et al. (2001) Vesicle permeabilization by protofibrillar alpha-synuclein: implications for the pathogenesis and treatment of Parkinson's disease. Biochemistry 40: 7812-7819.
25. Li SW, Lin TS, Minteer S, Burke WJ (2001) 3,4-Dihydroxyphenylacetaldehyde and hydrogen peroxide generate a hydroxyl radical: possible role in Parkinson's disease pathogenesis. Mol Brain Res 93: 1-7.
26. Chen JJ, Anh-Vuong L (2006) Rasageline: a second generation monamine oxidase type B inhibitor for treatment of Parkinson's disease. Am J Health-Syst Pharm 63: 915-928.
27. Rees JN, Florang VR, Eckert LL, Doorn JA (2009) Protein reactivity of 3,4-dihdroxyphenylacetaldehyde, a toxic dopamine metabolite, is dependent on both the aldehyde and the catechol. Chem Res Toxicol 22: 1256-1263.
28. Xu J, Kao SY, Lee FJ, Song W, Jin LW, et al. (2002) Dopamine-dependent neurotoxicity of alpha-synuclein: a mechanism for selective neurodegeneration in Parkinson disease. Nat Med 8: 600-606.
29. Lee FJ, Liu F, Pristupa ZB, Niznik HB (2001) Direct binding and functional coupling of alpha-synuclein to the dopamine transporters accelerate dopamineinduced apoptosis. FASEB J 15: 916-926.
30. Mattammal MB, Chung HD, Strong R (1993) Confirmation of a dopamine metabolite in parkinsonian brain tissue by gas chromoatogtaphy-mass spectrometry. J Chromatog 614: 205-212.
31. Werner CJ, Heyny-von Haussen R, Mall G, Wolf S (2008) Proteome analysis of human substantia nigra in Parkinson's disease. Proteome Sci 6: 8.
32. Goldstein D, Sullivan P, Holmes C, Kopin I, Basile M (2009) Decreased putamen aldehyde dehydrogenase in Parkinson disease. World Congress on PD & Related Disorders: P1.240 (unpublished).
33. Galter D, Buervenich S, Carmine A, Anvert M, Olson L (2003) ALDH1A1 mRNA: presence in human dopamine neurons and decreased in substantia nigra in Parkinson's disease and in ventral tegmental area in schizophrenia. Neurobiol Dis 14: 637-647.
34. Mandel S, Grunblatt E, Riederer P, Amarglio N, Jacob-Hirsch JJ, et al. (2005) Gene expression profiling of sporadic Parkinson's disease substantia nigra pars compacta reveals impairment of ubiqutin-protesome subunits, SKP1A, aldehyde dehydrogenase, and Chaperone HSC-70. Ann NY Acad Sci 1053: 356-375.
35. Burke WJ, Joh TH (1988) Dopamine represses the synthesis of tyrosine hydroxylase in cultured adrenal medulla. Biochem Pharmacol 37: 1391-1397.
36. Schmitz C, Hof PR (2005) Design-based stereology in neuroscience. Neuroscience 130: 813-831.
37. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119: 7-35.
38. Galvin JE (2006) Interaction of a-synuclein and dopamine metabolites in the pathogenesis of Parkinsn's disease: a case for selective vulnerability of the substantia nigra. Acta Neuropath 112: 115-126.
39. Nair-Roberts RG, Chatelain-Badie SD, Benson E, White-Cooper H, Bolam JP, et al. (2008) Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience 152: 1024-1031.
40. Oorschot DE (1996) Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: a stereological study using the cavalieri and optical dissector methods. J Comp Neurol 366: 580-599.
41. Sakai K, Gash DM (1994) Effect of bilateral 6-OHDA lesions of the substantia nigra on locomotor activity in the rat. Brain Res 633: 144-150.
42. Emborg E (2004) Evaluation of animal models of Parkinson's disease for neuroprotective strategies. J Neurosci Methods 131: 121-143.
43. Schwarting RKW, Huston JP (1996) The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments. Prog Neurobiol 50: 275-331.
44. Blandini F, Armentero MT, Martignoni E (2008) The 6-hydroxydopamine model: news from the past. Parkinsonism Relat Disord 14: S124-129.
45. Konitsiotis S, Tsironis C (2006) Levodopa-induced dyskinesia and rotational behavior in hemiparkinsonian rats: independent features or components of the same phenomenon? Behav Brain Res 170: 337-341.
46. Mokrý J (1995) Experimental models and behavioural tests used in the study of Parkinson's disease. Physiol Res 44: 143-150.
47. Ungerstedt U, Arbuthnott GW (1970) Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res 24: 485-493.
48. Gonzalez D, Miyamoto O, Touge T, Sumitani K, Kuriyama S, et al. (2006) Unilateral ibotenic acid lesions of the prefrontal cortex reduce rotational behavior in 6-hydroxydopamine-lesioned rats. Acta Med Okayama 60: 319-324.
49. Henderson JM, Schleimer SB, Allbutt H, Dabholkar V, Abela, et al. (2005) Behavioural effects of parafascicular thalamic lesions in an animal model of parkinsonism. Behav Brain Res 162: 222-232.
50. Blandini F (2001) The role of the subthalamic nucleus in the pathophysiology of Parkinson's disease. Funct Neurol 16: 99-106.
51. Blandini F, Greenamyre JT, Fancellu R, Nappi G (2001) Blockade of subthalamic glutamatergic activity corrects changes in neuronal metabolism and motor behavior in rats with nigrostriatal lesions. Neurol Sci 22: 49-50.
52. Henderson JM, Stanic D, Tomas D, Patch J, Horne MK, et al. (2005) Postural changes after lesions of the substantia nigra pars reticulata in hemiparkinsonian monkeys. Behav Brain Res 160: 267-276.
53. McPherson RJ, Marshall JF (2000) Substantia nigra glutamate antagonists produce contralateral turning and basal ganglia Fos expression: interactions with D1 and D2 dopamine receptor agonists. Synapse 36: 194-204.
54. Henderson JM, Watson S, Halliday GM, Heinemann T, Gerlach M (2003) Relationship between various behavioural abnormalities and nigrostriatal dopamine depletion in the unilateral 6-OHDA-lesioned rat. Behav Brain Res 139: 105-113.
55. Baquet ZC, Williams D, Brody J, Smeyne RJ (2009) A comparison of modelbased (2D) and design-based (3D) stereological methods for estimating cell number in the stubstantia nigra pars compacta (SNpc) of the C57BL/6J mouse. Neuroscience 161: 1082-1090.
56. Pioli EY, Meissner W, Sohr R, Gross CE, Bezard E, et al. (2008) Differential behavioral effects of partial bilateral lesions of ventral tegmental area or substantia nigra pars compacta in rats. Neuroscience 153: 1213-1224.
57. Pioli EY, Dovero S, Bioulac BH, Gross CE, Bezard E (2004) Asymmetrically lesioned mesencephalon in healthy rodents: call for caution. Brain Res 1022: 251-253.
58. Yuan H, Sarre S, Ebinger G, Michotte Y (2005) Histological, behavioural and neurochemical evaluation of medial forebrain bundle and striatal 6-OHDA lesions as rat models of Parkinson's disease. J Neurosci Methods 144: 35-45.
59. Björklund A, Lindvall A (1984) Dopamine containing systems in the CNS. In: Björklund A and Hö kfelt T. Handbook of Chemical Neuroanatomy: Classical Transmitters in the CNS. Vol. 2. New York, NY: Elsevier Science Publishers. pp 55-122.
60. Leshan RL, Opland DM, Louis GW, Leinninger GM, Patterson CM, et al. (2010) Ventral tegmental area leptin receptor neurons specifically project to and regulate cocaine-and amphetamine-related transcript neurons of the extended central amygdala. J Neuroscience 30: 5713-5723.
61. Cahill AL, Ehret CF (1981) Circadian variations in the activity of tyrosine hydroxylase, tyrosine aminotransferase, and tryptophan hydroxylase: Relationship to catecholamine metabolism. J Neurochem 37: 1109-1115.
62. Weber M, Lauterberg T, Tobler I, Burgrunder J-M (2004) Circadian patterns of neurotransmitter related gene expression in motor regions of the rat brain. Neurosci Let 358: 17-20.
63. Thiel CM, Schwarting RK (2001) Dopaminergic lateralisation in the forebrain: relations to behavioural asymmetries and anxiety in male Wistar rats. Neuropsychobiol 43: 192-199.
64. Rodrigues RWP, Gomide VC, Chadi G (2001) Astroglial and microglial reactions after partial nigrostriatal degeneration induced by the striatal injection of different doses of 6-hydoxydopamine. Int J Neuroscience 109: 91-126.
65. Burke WJ, Li SW, Chung HD, Ruggiero DA, Kristal BS, Johnson EM, et al. (2004) Neurotoxicity of MAO metabolites of catecholamine neurotransmitters: role in neurodegenerative diseases. Neurotoxicol 25: 101-115.
66. Burke WJ, Schmitt CA, Miller C, Li SW (1997) Norepinephrine transmitter metabolite induces apoptosis in differentiated rat pheochromocytoma cells. Brain Res 760: 290-293.
67. Burke WJ, Kristal BS, Yu BP, Schmitt CA, Li SWW, et al. (1998) Norepinephrine transmitter metabolite activates mitochondrial permeability transition: a mechanism for DOPEGAL-induced apoptosis. Brain Res 787: 332-338.
68. Konitsiotis S, Kafetzopoulos E, Anastasopoulos D, Blanchet PJ (1998) Opposite rotation induced by dopamine agonists in rats with unilateral lesions of the globus pallidus or substantia nigra. Behav Brain Res 92: 77-83.
69. Thomas J, Wang J, Takubo H, Sheng J, de Jesus S, et al. (1994) A 6-hydroxydopamine-induced selective parkinsonian rat model: further biochemical and behavioral characterization. Exp Neurol 126: 159-167.
70. Willis GL, Sandyk R (1993) Amphetamine-induced rotational behavior in rats: relationship to hypothalamic and striatal degeneration. Int J Neurosci 71: 135-146.
71. Glick SD, Shapiro RM, Drew KL, Hinds PA, Carlson JN (1986) Differences in spontaneous and amphetamine-induced rotational behavior, and in sensitization to amphetamine, among Sprague-Dawley derived rats from different sources. Physiol Behav 38: 67-70.
72. Carman LS, Gage FH, Shults CW (1991) Partial lesion of the substantia nigra: relation between extent of lesion and rotational behavior. Brain Res 553: 275-283.
73. Li SW, Spaziano VT, Burke WJ (1998) Synthesis of a biochemically important aldehyde, 3,4-dihydroxyphenylacetaldhyde. Bioorg Chem 26: 45-50.