In vitro dopaminergic neurotoxicity of pesticides: a link with neurodegeneration?

Veterinary Quarterly

Volumn 34, Issue 3, 2014, Pages 120-131

  Heusinkveld, Harm J ^a,b,c   van den Berg, Martin ^a   Westerink, Remco H S ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b IUF LEIBNIZ RESEARCH INSTITUTE FOR ENVIRONMENTAL MEDICINE   (Germany)

^c NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

Author keywords

in vitro neurotoxicity; intracellular calcium; neurodegeneration; Parkinson's disease; pesticides

Indexed keywords

BRAIN METASTASIS; CANCER CHEMOTHERAPY; CANCER SURGERY; CANCER THERAPY; MOLECULARLY TARGETED THERAPY; NON SMALL CELL LUNG CANCER; REVIEW; ANIMAL; CHEMICALLY INDUCED; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; HOMEOSTASIS; HUMAN; IN VITRO STUDY; METABOLISM; NEUROTOXICITY SYNDROMES; OXIDATIVE STRESS; PARKINSON DISEASE; RISK ASSESSMENT;

PARKINSONIA;

CALCIUM; PESTICIDE;

ANIMALS; CALCIUM; DOPAMINERGIC NEURONS; HOMEOSTASIS; HUMANS; IN VITRO TECHNIQUES; NEURODEGENERATIVE DISEASES; NEUROTOXICITY SYNDROMES; OXIDATIVE STRESS; PARKINSON DISEASE; PESTICIDES; RISK ASSESSMENT;

EID: 84919777642     PISSN: 01652176     EISSN: 18755941     Source Type: Journal    
DOI: 10.1080/01652176.2014.980934     Document Type: Review

References (114)

1. Ascherio A, Honglei C, Weisskopf MG, O’Reilly E, McCullough ML, Calle EE, Schwarzschild MA, Thun MJ. 2006. Pesticide exposure and risk for Parkinson's disease. Ann Neurol. 60:197–203.
2. Barbeau A. 1984. Manganese and extrapyrimidal disorders (a critical review and tribute to Dr. George C. Cotzias). Neurotoxicology. 5:13–35.
3. Barclay JW, Morgan A, Burgoyne RD. 2005. Calcium-dependent regulation of exocytosis. Cell Calcium. 38:343–353.
4. Barlow BK, Cory-Slechta DA, Richfield EK, Thiruchelvam M. 2007. The gestational environment and Parkinson's disease: evidence for neurodevelopmental origins of a neurodegenerative disorder. Reprod Toxicol. 23:457–470.
5. Bartels AL, Leenders KL. 2009. Parkinson's disease: the syndrome, the pathogenesis and pathophysiology. Cortex. 45:915–921.
6. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre TJ. 2000. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci. 3:1301–1306.
7. Bezard E, Przedborski S. 2011. A tale on animal models of Parkinson's disease. Move Disord. 26:993–1002.
8. Bezprozvanny I. 2009. Calcium signaling and neurodegenerative diseases. Trends Mol Med. 15:89–100.
9. Blandini F, Nappi G, Tassorelli C, Martignoni E. 2000. Functional changes of the basal ganglia circuitry in Parkinson's disease. Prog Neurobiol. 62:63–88.
10. Botella B, Crespo J, Rivas A, Cerrillo I, Olea-Serrano MF, Olea N. 2004. Exposure of women to organochlorine pesticides in Southern Spain. Environ Res. 96:34–40.
11. Braak H, Tredici KD, Rnb U, de Vos RAI, Jansen Steur ENH, Braak E. 2003. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging. 24:197–211.
12. Brooks DJ. 2012. Parkinson's disease: diagnosis. Parkinsonism Relat Disord. 18(Supplement 1):S31–S33.
13. Brown TP, Rumsby PC, Capleton AC, Rushton L, Levy LS. 2006. Pesticides and Parkinson's disease – is there a link? Environ Health Perspect. 114:156–164.
14. Butler Walker J, Seddon L, McMullen E, Houseman J, Tofflemire K, Corriveau A, Weber J-P, Mills C, Smith S, Van Oostdam J. 2003. Organochlorine levels in maternal and umbilical cord blood plasma in Arctic Canada. Sci Total Environ. 302:27–52.
15. Bywood PT, Johnson SM. 2003. Mitochondrial complex inhibitors preferentially damage substantia nigra dopamine neurons in rat brain slices. Exp Neurol. 179:47–59.
16. Carreño J, Rivas A, Granada A, Jose Lopez-Espinosa M, Mariscal M, Olea N, Olea-Serrano F. 2007. Exposure of young men to organochlorine pesticides in Southern Spain. Environ Res. 103:55–61.
17. Chan CS, Guzman JN, Ilijic E, Mercer JN, Rick C, Tkatch T, Meredith GE, Surmeier DJ. 2007. Rejuvenation’ protects neurons in mouse models of Parkinson's disease. Nature. 447:1081–1086.
18. Chinta SJ, Andersen JK. 2008. Redox imbalance in Parkinson's disease. Biochim Biophys Acta. 1780:1362–1367.
19. Chinta SJ, Rane A, Poksay KS, Bredesen DE, Andersen JK, Rao RV. 2008. Coupling endoplasmic reticulum stress to cell death program in dopaminergic cells: effect of paraquat. Neuromolecular Med. 10:333–342.
20. Cicchetti F, Drouin-Ouellet J, Gross RE. 2009. Environmental toxins and Parkinson's disease: what have we learned from pesticide-induced animal models? Trends Pharmacol Sci. 30:475–483.
21. Corrigan FM, French M, Murray L. 1996. Organochlorine compounds in human brain. Human Exp Toxicol. 15:262–264.
22. Corrigan FM, Wienburg CL, Shore RF, Daniel SE, Mann D. 2000. Organochlorine insecticides in substantia nigra in Parkinson's disease. J Toxicol Environ Health A. 59:229–234.
23. Crowell SR, Henderson WM, Kenneke JF, Fisher JW. 2011. Development and application of a physiologically based pharmacokinetic model for triadimefon and its metabolite triadimenol in rats and humans. Toxicol Lett. 205:154–162.
24. Cruz S, Lino C, Silveira MI. 2003. Evaluation of organochlorine pesticide residues in human serum from an urban and two rural populations in Portugal. Sci Total Environ. 317:23–35.
25. de Groot MW, Westerink RH, Dingemans MM. 2013. Don't judge a neuron only by its cover: neuronal function in in vitro developmental neurotoxicity testing. Toxicol Sci. 132:1–7.
26. de Lau LM, Breteler MM. 2006. Epidemiology of Parkinson's disease. Lancet Neurol. 5:525–535.
27. Dexter DT, Jenner P. 2013. Parkinson disease: from pathology to molecular disease mechanisms. Free Radical Biol Med. 62:132–144.
28. Dirtu AC, Cernat R, Dragan D, Mocanu R, van Grieken R, Neels H, Covaci A. 2006. Organohalogenated pollutants in human serum from Iassy, Romania and their relation with age and gender. Environ Int. 32:797–803.
29. Dunning CJR, Reyes JF, Steiner JA, Brundin P. 2012. Can Parkinson's disease pathology be propagated from one neuron to another? Prog Neurobiol. 97:205–219.
30. Elbaz A, Clavel J, Rathouz PJ, Moisan F, Galanaud J-P, Delemotte B, Alpérovitch A, Tzourio C. 2009. Professional exposure to pesticides and Parkinson disease. Ann Neurol. 66:494–504.
31. Elbaz A, Tranchant C. 2007. Epidemiologic studies of environmental exposures in Parkinson's disease. J Neurol Sci. 262:37–44.
32. Elder A, Gelein R, Silva V, Feikert T, Opanashuk L, Carter J, Potter R, Maynard A, Ito Y, Finkelstein J, Oberdörster G. 2006. Translocation of inhaled ultrafine manganese oxide particles to the central nervous system. Environ Health Perspect. 114:1172–1178.
33. Estevez AO, Mueller CL, Morgan KL, Szewczyk NJ, Teece L, Miranda-Vizuete A, Estevez M. 2012. Selenium induces cholinergic motor neuron degeneration in Caenorhabditis elegans. Neurotoxicology. 33:1021–1032.
34. Fleming L, Mann JB, Bean J, Briggle T, Sanchez-Ramos JR. 1994. Parkinson's disease and brain levels of organochlorine pesticides. Ann Neurol. 36:100–103.
35. Freire C, Koifman S. 2012. Pesticide exposure and Parkinson's disease: epidemiological evidence of association. Neurotoxicology. 33:947–971.
36. Gagne JJ, Power MC. 2010. Anti-inflammatory drugs and risk of Parkinson disease: a meta-analysis. Neurology. 74:995–1002.
37. Garcia AG, Garcia-De-Diego AM, Gandia L, Borges R, Garcia-Sancho J. 2006. calcium signaling and exocytosis in adrenal chromaffin cells. Physiol Rev. 86:1093–1131.
38. Gibson JE, Rao KS. 1973. Disposition of 2-sec-butyl-4,6-dinitrophenol (dinoseb) in pregnant mice. Fd Cosmet Toxical. 11:45–52.
39. Goodwin J, Nath S, Engelborghs Y, Pountney DL. 2013. Raised calcium and oxidative stress cooperatively promote alpha-synuclein aggregate formation. Neurochem Int. 62:703–711.
40. Guzman JN, Sánchez-Padilla J, Chan CS, Surmeier DJ. 2009. Robust pacemaking in substantia nigra dopaminergic neurons. J Neurosci. 29:11011–11019.
41. Harvey DG, Bidstrup PL, Bonnell JAL. 1951. Poisoning by Dinitro-ortho-cresol: some observations on the effects of Dinitro-ortho-cresol administered by mouth to human volunteers. Br Med J. 2:13–16.
42. Hatcher JM, Delea KC, Richardson JR, Pennell KD, Miller GW. 2008. Disruption of dopamine transport by DDT and its metabolites. Neurotoxicology. 29:682–690.
43. Hernández-Romero MC, Delgado-Cortés MJ, Sarmiento M, de Pablos RM, Espinosa-Oliva AM, Argüelles S, Bández MJ, Villarán RF, Mauriño R, Santiago M, 2012. Peripheral inflammation increases the deleterious effect of CNS inflammation on the nigrostriatal dopaminergic system. Neurotoxicology. 33:347–360.
44. Heusinkveld HJ, Molendijk J, van den Berg M, Westerink RHS. 2013. Azole fungicides disturb intracellular Ca2+ in an additive manner in dopaminergic PC12 cells. Toxicol Sci. 134:374–381.
45. Heusinkveld HJ, Thomas GO, Lamot I, van den Berg M, Kroese ABA, Westerink RHS. 2010. Dual actions of lindane (γ-hexachlorocyclohexane) on calcium homeostasis and exocytosis in rat PC12 cells. Toxicol Appl Pharmacol. 248:12–19.
46. Heusinkveld HJ, Westerink RHS. 2011. Caveats and limitations of plate reader-based high-throughput kinetic measurements of intracellular calcium levels. Toxicol Appl Pharmacol. 255:1–8.
47. Heusinkveld HJ, Westerink RHS. 2012. The organochlorine insecticides lindane, dieldrin and their binary mixture disturb calcium homeostasis in dopaminergic PC12 cells. Environ Sci Technol. 46:1842–1848.
48. Heuts FJM. 1993. Biological Monitoring of DNOC in applicators after use as Haulmkiller in seed potatoes. Rotterdam (unpublished report prepared for Elf Atochem Agri bv).
49. Hughes AJ, Daniel SE, Kilford L, Lees AJ. 1992. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry. 55:181–184.
50. Imtiaz M. 2012. Calcium oscillations and pacemaking. In: Islam MS, editor. Calcium signaling, Vol. 740. Netherlands: Springer; p. 511–520.
51. Jimenez-Torres M, Campoy-Folgoso C, Canabate-Reche F, Rivas-Velasco A, Cerrillo-Garcia I, Mariscal-Arcas M, Olea-Serrano F. 2006. Organochlorine pesticides in serum and adipose tissue of pregnant women in Southern Spain giving birth by cesarean section. Sci Total Environ. 372:32–38.
52. Koppen G, Covaci A, Van Cleuvenbergen R, Schepens P, Winneke G, Nelen V, van Larebeke N, Vlietinck R, Schoeters G. 2002. Persistent organochlorine pollutants in human serum of 50–65 years old women in the Flanders Environmental and Health Study (FLEHS). Part 1: concentrations and regional differences. Chemosphere. 48:811–825.
53. Kortenkamp A. 2008. Low dose mixture effects of endocrine disrupters: implications for risk assessment and epidemiology. Int J Androl. 31:233–240.
54. Langston JW. 1996. The etiology of Parkinson's disease with emphasis on the MPTP story. Neurology. 47:S153–160.
55. Langston JW, Ballard P, Tetrud JW, Irwin I. 1983. Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science. 219:979–980.
56. Lees AJ, Hardy J, Revesz T. 2009. Parkinson's disease. The Lancet. 373:2055–2066.
57. Lopez-Espinosa MJ, Lopez-Navarrete E, Rivas A, Fernandez MF, Nogueras M, Campoy C, Olea-Serrano F, Lardelli P, Olea N. 2008. Organochlorine pesticide exposure in children living in southern Spain. Environ Res. 106:1–6.
58. Lucchini RG, Dorman DC, Elder A, Veronesi B. 2012. Neurological impacts from inhalation of pollutants and the nose– brain connection. Neurotoxicology. 33:838–841.
59. Mattson MP. 2012. Parkinson's disease: don't mess with calcium. J Clin Invest. 122:1195–1198.
60. McGeer PL, McGeer EG. 2004. Inflammation and neurodegeneration in Parkinson's disease. Parkinsonism Relat Disord. 10:S3–S7.
61. Meijer M, Dingemans MM, van den Berg M, Westerink RH. 2014a. Inhibition of voltage-gated calcium channels as common mode of action for (mixtures of) distinct classes of insecticides. Toxicol Sci. 141:103–111.
62. Meijer M, Hendriks HS, Heusinkveld HJ, Langeveld WT, Westerink RH. 2014b. Comparison of plate reader-based methods with fluorescence microscopy for measurements of intracellular calcium levels for the assessment of in vitro neurotoxicity. Neurotoxicology. 45C:31–37.
63. Mosharov EV, Larsen KE, Kanter E, Phillips KA, Wilson K, Schmitz Y, Krantz DE, Kobayashi K, Edwards RH, Sulzer D. 2009. interplay between cytosolic dopamine, calcium, and α-synuclein causes selective death of substantia nigra neurons. Neuron. 62:218–229.
64. Mostafalou S, Abdollahi M. 2013. Pesticides and human chronic diseases: evidences, mechanisms, and perspectives. Toxicol Appl Pharmacol. 268:157–177.
65. Mustafa MD, Pathak R, Tripathi A, Ahmed R, Guleria K, Banerjee B. 2010. Maternal and cord blood levels of Aldrin and Dieldrin in Delhi population. Environ Monit Assess. 171:633–638.
66. Nath S, Goodwin J, Engelborghs Y, Pountney DL. 2011. Raised calcium promotes α-synuclein aggregate formation. Mol Cellular Neurosci. 46:516–526.
67. Neve KA, Seamans JK, Trantham-Davidson H. 2004. Dopamine receptor signalling. J Receptors Signal Transduction. 24:165–205.
68. Nolan K, Kamrath J, Levitt J. 2012. Lindane toxicity: a comprehensive review of the medical literature. Pediatr Dermatol. 29:141–146.
69. Nougadère A, Sirot V, Kadar A, Fastier A, Truchot E, Vergnet C, Hommet F, Baylé J, Gros P, Leblanc J-C. 2012. Total diet study on pesticide residues in France: levels in food as consumed and chronic dietary risk to consumers. Environ Int. 45:135–150.
70. Oates L, Cohen M. 2011. Assessing diet as a modifiable risk factor for pesticide exposure. Int J Environ Res Public Health. 8:1792–1804.
71. Oberdorster G, Sharp Z, Atudorei V, Elder A, Gelein R, Kreyling W, Cox C. 2004. Translocation of inhaled ultrafine particles to the brain. Inhal Toxicol. 16:437–445.
72. Obermeier B, Daneman R, Ransohoff RM. 2013. Development, maintenance and disruption of the blood-brain barrier. Nat Med. 19:1584–1596.
73. Obeso JA, Rodríguez-Oroz MC, Benitez-Temino B, Blesa FJ, Guridi J, Marin C, Rodriguez M. 2008. Functional organization of the basal ganglia: therapeutic implications for Parkinson's disease. Move Disord. 23:S548–559.
74. Parkinson J. 2002. An essay on the shaking palsy. Neuropsychiatry Classics. 14:223–236.
75. Pezzoli G, Cereda E. 2013. Exposure to pesticides or solvents and risk of Parkinson disease. Neurology. 80:2035–2041.
76. Prachar V, Veningerová M, Uhnák J. 1993. Levels of polychlorinated biphenyls and some other organochlorine compounds in breast milk samples in Bratislava. Sci Total Environ. 134:237–242.
77. Pravettoni E, Bacci A, Coco S, Forbicini P, Matteoli M, Verderio C. 2000. Different localizations and functions of L-type and N-type calcium channels during development of hippocampal neurons. Dev Biol. 227:581–594.
78. Purisai MG, McCormack AL, Cumine S, Li J, Isla MZ, Di Monte DA. 2007. Microglial activation as a priming event leading to paraquat-induced dopaminergic cell degeneration. Neurobiol Dis. 25:392–400.
79. Putzier I, Kullmann PHM, Horn JP, Levitan ES. 2009. Cav1.3 channel voltage dependence, Not Ca2+ selectivity, drives pacemaker activity and amplifies bursts in nigral dopamine neurons. J Neurosci. 29:15414–15419.
80. Radad K, Rausch WD, Gille G. 2006. Rotenone induces cell death in primary dopaminergic culture by increasing ROS production and inhibiting mitochondrial respiration. Neurochem Int. 49:379–386.
81. Rajput AH, Birdi S. 1997. Epidemiology of Parkinson's disease. Parkinsonism Relat Disord. 3:175–186.
82. Ramwell CT, Johnson PD, Boxall ABA, Rimmer DA. 2005. Pesticide residues on the external surfaces of field crop sprayers: occupational exposure. Ann Occup Hyg. 49:345–350.
83. Raymond-Delpech V, Matsuda K, Sattelle BM, Rauh JJ, Sattelle DB. 2005. Ion channels: molecular targets of neuroactive insecticides. Invertebrate Neurosci. 5:119–133.
84. Rice ME, Patel JC, Cragg SJ. 2011. Dopamine release in the basal ganglia. Neuroscience. 198:112–137.
85. Richardson JR, Caudle WM, Wang M, Dean ED, Pennell KD, Miller GW. 2006. Developmental exposure to the pesticide dieldrin alters the dopamine system and increases neurotoxicity in an animal model of Parkinson's disease. Faseb J. 20:1695–1697.
86. Rivas A, Cerrillo I, Granada A, Mariscal-Arcas M, Olea-Serrano F. 2007. Pesticide exposure of two age groups of women and its relationship with their diet. Sci Total Environ. 382:14–21.
87. Rodríguez J, Verkhratsky A. 2010. Neuroglial roots of neurodegenerative diseases? Mol Neurobiol. 43:87–96.
88. Schapira AH, Jenner P. 2011. Etiology and pathogenesis of Parkinson's disease. Move Disord. 26:1049–1055.
89. Schapira AHV. 2009. Neurobiology and treatment of Parkinson's disease. Trends Pharmacol Sci. 30:41–47.
90. Sherer TB, Betarbet R, Kim J-H, Greenamyre JT. 2003a. Selective microglial activation in the rat rotenone model of Parkinson's disease. Neurosci Lett. 341:87–90.
91. Sherer TB, Kim J-H, Betarbet R, Greenamyre JT. 2003b. Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and α-synuclein aggregation. Exp Neurol. 179:9–16.
92. Shimizu K, Ohtaki K, Matsubara K, Aoyama K, Uezono T, Saito O, Suno M, Ogawa K, Hayase N, Kimura K, Shiono H. 2001. Carrier-mediated processes in blood–brain barrier penetration and neural uptake of paraquat. Brain Res. 906:135–142.
93. Stevens DA. 2012. Advances in systemic antifungal therapy. Clin Dermatol. 30:657–661.
94. Subramanian A, Ohtake M, Kunisue T, Tanabe S. 2007. High levels of organochlorines in mothers’ milk from Chennai (Madras) city, India. Chemosphere. 68:928–939.
95. Surmeier DJ, Guzman JN, Sanchez-Padilla J, Schumacker PT. 2011. The role of calcium and mitochondrial oxidant stress in the loss of substantia nigra pars compacta dopaminergic neurons in Parkinson's disease. Neuroscience. 198:221–231.
96. Tansey MG, Goldberg MS. 2010. Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention. Neurobiol Dis. 37:510–518.
97. Taylor JM, Main BS, Crack PJ. 2013. Neuroinflammation and oxidative stress: co-conspirators in the pathology of Parkinson's disease. Neurochem Int. 62:803–819.
98. Thomas GO, Wilkinson M, Hodson S, Jones KC. 2006. Organohalogen chemicals in human blood from the United Kingdom. Environ Pollut. 141:30–41.
99. Trejo-Acevedo A, Diaz-Barriga F, Carrizales L, Dominguez G, Costilla R, Ize-Lema I, Yarto-Ramirez M, Gavilan-Garcia A, Jesus Mejia-Saavedra J, Perez-Maldonado IN. 2009. Exposure assessment of persistent organic pollutants and metals in Mexican children. Chemosphere. 74:974–980.
100. Turski L, Bressler K, Rettig KJ, Loschmann PA, Wachtel H. 1991. Protection of substantia nigra from MPP +neurotoxicity by N-methyl-D-aspartate antagonists. Nature. 349:414–418.
101. Vale C, Fonfra E, Bujons J, Messeguer A, Rodriguez-Farr E, Sunol C. 2003. The organochlorine pesticides gamma-hexachlorocyclohexane (lindane), alpha -endosulfan and dieldrin differentially interact with GABAA and glycine-gated chloride channels in primary cultures of cerebellar granule cells. Neuroscience. 117:397–403.
102. van der Mark M, Brouwer M, Kromhout H, Nijssen P, Huss A, Vermeulen R. 2011. Is pesticide use related to parkinson disease? some clues to heterogeneity in study results. Environ Health Perspect. 120:340–347.
103. van Noort H, Mandema E, Juul Christensen EK, Huizinga T. 1960. 4,6-Dinitro-o-cresol poisoning caused by sprays. Nederlands Tijdschrift voor Geneeskunde. 104:676–684.
104. Venda LL, Cragg SJ, Buchman VL, Wade-Martins R. 2010. α-Synuclein and dopamine at the crossroads of Parkinson's disease. Trends Neurosci. 33:559–568.
105. Walsh GM, Fink GB. 1972. Comparative toxicity and distribution of endrin and dieldrin after intravenous administration in mice. Toxicol Appl Pharmacol. 23:408–416.
106. Weisskopf MG, Knekt P, O’Reilly EJ, Lyytinen J, Reunanen A, Laden F, Altshul L, Ascherio A. 2010. Persistent organochlorine pesticides in serum and risk of Parkinson disease. Neurology. 74:1055–1061.
107. Westerink RH. 2013. Do we really want to REACH out to in vitro? Neurotoxicology. 39:169–172.
108. Westerink RH, Hondebrink L. 2010. Are high-throughput measurements of intracellular calcium using plate-readers sufficiently accurate and reliable? Toxicol Appl Pharmacol. 249:247–248; author reply 249-250.
109. Westerink RHS. 2006. Targeting Exocytosis: ins and outs of the modulation of quantal dopamine release. CNS Neurol Disord - Drug Targets. 5:57–77.
110. Whitacre DM, Ware GW, Whitacre DM, Ware GW. 2004. The pesticide book. 6th ed. Willoughby (OH): Meister-Pro Information Resources (Meister Media Worldwide).
111. Wilkaniec A, Strosznajder JB, Adamczyk A. 2013. Toxicity of extracellular secreted alpha-synuclein: Its role in nitrosative stress and neurodegeneration. Neurochem Int. 62:776–783.
112. Wu J, Chan P, Schroeder KM, Ellsworth K, Partridge LDL. 2002. 1-Methyl-4-phenylpridinium (MPP+)-induced functional run-down of GABAA receptor-mediated currents in acutely dissociated dopaminergic neurons. J Neurochem. 83:87–99.
113. Xu X, Dailey AB, Talbott EO, Ilacqua VA, Kearney G, Asal NR. 2010. Associations of serum concentrations of organochlorine pesticides with breast cancer and prostate cancer in U.S. adults. Environ Health Perspect. 118:60–66.
114. Yasuda T, Nakata Y, Mochizuki H. 2013. α-Synuclein and neuronal cell death. Mol Neurobiol. 47:466–483.