Of Pesticides and Men: a California Story of Genes and Environment in Parkinson’s Disease

Current environmental health reports

Volumn 3, Issue 1, 2016, Pages 40-52

  Ritz, Beate R ^a,b,c   Paul, Kimberly C ^a   Bronstein, Jeff M ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Gene environment interactions; Parkinson s disease; Pesticides

Indexed keywords

ABCB1 PROTEIN, HUMAN; ALDEHYDE DEHYDROGENASE ISOENZYME 2; ALDH2 PROTEIN, HUMAN; ARYLDIALKYLPHOSPHATASE; DOPAMINE TRANSPORTER; HLA DR ANTIGEN; MULTIDRUG RESISTANCE PROTEIN; NEURONAL NITRIC OXIDE SYNTHASE; NOS1 PROTEIN, HUMAN; PESTICIDE; PON1 PROTEIN, HUMAN; S PHASE KINASE ASSOCIATED PROTEIN; SKP1 PROTEIN, HUMAN; SLC6A3 PROTEIN, HUMAN;

ADVERSE EFFECTS; AGED; CALIFORNIA; CASE CONTROL STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; INCIDENCE; MALE; MIDDLE AGED; PARKINSON DISEASE;

AGED; ALDEHYDE DEHYDROGENASE, MITOCHONDRIAL; ARYLDIALKYLPHOSPHATASE; CALIFORNIA; CASE-CONTROL STUDIES; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; ENVIRONMENTAL EXPOSURE; FEMALE; GENE-ENVIRONMENT INTERACTION; HLA-DR ANTIGENS; HUMANS; INCIDENCE; MALE; MIDDLE AGED; NITRIC OXIDE SYNTHASE TYPE I; P-GLYCOPROTEINS; PARKINSON DISEASE; PESTICIDES; S-PHASE KINASE-ASSOCIATED PROTEINS;

EID: 84984663523     PISSN: None     EISSN: 21965412     Source Type: Journal    
DOI: 10.1007/s40572-016-0083-2     Document Type: Article

References (102)

1. Caudle WM, Guillot TS, Lazo CR, et al. Industrial toxicants and Parkinson’s disease. Neurotoxicology. 2012;33:178–88.
2. Lill CM, Roehr JT, McQueen MB, et al. Comprehensive research synopsis and systematic meta-analyses in Parkinson’s disease genetics: the PDGene database. PLoS Genet. 2012;8:e1002548. This study provides an exhaustive summary of the status of PD genetics on more than seven million polymorphisms originating from GWAS or smaller-scale PD association studies.
3. Goldman SM. Environmental toxins and Parkinson’s disease. Annu Rev Pharmacol Toxicol. 2014;54:141–64.
4. Nalls MA, Pankratz N, Lill CM, et al. Large-scale meta-analysis of genome-wide association data identifies six new risk loci for Parkinson’s disease. Nat Genet. 2014;46:989–93.
5. Langston JW, Ballard P, Tetrud JW, et al. Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science. 1983;219:979–80. This study was the first to describe a specific toxicant as acting selectively on dopamine neurons.
6. Barbeau A, Dallaire L, Buu NT, et al. Comparative behavioral, biochemical and pigmentary effects of MPTP, MPP+ and paraquat in Rana pipiens. Life Sci. 1985;37:1529–38.
7. Brown TP, Rumsby PC, Capleton AC, et al. Pesticides and Parkinson’s disease—is there a link? Environ Health Perspect. 2006;114:156–64.
8. Trinh J, Farrer M. Advances in the genetics of Parkinson disease. Nat Rev Neurol. 2013;9:445–54.
9. Pihlstrøm L, Toft M. Parkinson’s disease: what remains of the ‘missing heritability’? Mov Disord. 2011;26:1971–3.
10. Quadri M, Yang X, Cossu G, et al. An exome study of Parkinson’s disease in Sardinia, a Mediterranean genetic isolate. Neurogenetics. 2015;16:55–64.
11. Goldberg DW, Wilson JP, Knoblock CA, et al. An effective and efficient approach for manually improving geocoded data. Int J Health Geogr. 2008;7:60.
12. Rull RP, Ritz B. Historical pesticide exposure in California using pesticide use reports and land-use surveys: an assessment of misclassification error and bias. Environ Health Perspect. 2003;111:1582–9.
13. Ritz B, Costello S. Geographic model and biomarker-derived measures of pesticide exposure and Parkinson’s disease. Ann N Y Acad Sci. 2006;1076:378–87.
14. Narayan S, Liew Z, Paul K, et al. Household organophosphorus pesticide use and Parkinson’s disease. Int J Epidemiol. 2013;42:1476–85.
15. Liew Z, Wang A, Bronstein J, et al. Job exposure matrix (JEM)-derived estimates of lifetime occupational pesticide exposure and the risk of Parkinson’s disease. Arch Environ Occup Health. 2014;69:241–51.
16. Przedborski S, Ischiropoulos H. Reactive oxygen and nitrogen species: weapons of neuronal destruction in models of Parkinson’s disease. Antioxid Redox Signal. 2005;7:685–93.
17. Martinez TN, Greenamyre JT. Toxin models of mitochondrial dysfunction in Parkinson’s disease. Antioxid Redox Signal. 2012;16:920–34.
18. Cannon JR, Greenamyre JT. Neurotoxic in vivo models of Parkinson’s disease recent advances. Prog Brain Res. 2010;184:17–33.
19. Wang X-F, Li S, Chou AP, et al. Inhibitory effects of pesticides on proteasome activity: implication in Parkinson’s disease. Neurobiol Dis. 2006;23:198–205.
20. Zhou Y, Shie F-S, Piccardo P, et al. Proteasomal inhibition induced by manganese ethylene-bis-dithiocarbamate: relevance to Parkinson’s disease. Neuroscience. 2004;128:281–91.
21. Fitzmaurice AG, Rhodes SL, Cockburn M, et al. Aldehyde dehydrogenase variation enhances effect of pesticides associated with Parkinson disease. Neurology. 2014;82:419–26.
22. Roede JR, Jones DP. Thiol-reactivity of the fungicide maneb. Redox Biol. 2014;2:651–5.
23. Johnson ME, Bobrovskaya L. An update on the rotenone models of Parkinson’s disease: their ability to reproduce the features of clinical disease and model gene-environment interactions. Neurotoxicology. 2015;46:101–16.
24. Pan-Montojo F, Schwarz M, Winkler C, et al. Environmental toxins trigger PD-like progression via increased alpha-synuclein release from enteric neurons in mice. Sci Rep. 2012;2:898.
25. Van der Mark M, Brouwer M, Kromhout H, et al. Is pesticide use related to Parkinson disease? Some clues to heterogeneity in study results. Environ Health Perspect. 2012;120:340–7. This is a comprehensive systematic review of PD and exposure to pesticides that investigates methodological differences between studies and heterogeneity in results.
26. Barr DB, Olsson AO, Wong L-Y, et al. Urinary concentrations of metabolites of pyrethroid insecticides in the general U.S. population: National Health and Nutrition Examination Survey 1999–2002. Environ Health Perspect. 2010;118:742–8.
27. Glotfelty DE, Seiber JN, Liljedahl LA. Pesticides in fog. Nature. 1987;325:602–5.
28. USGS. Pesticides in the atmosphere—distribution, trends and governing factors. Sacromento: U.S. Geological Survey; 1995. p. 94–506.
29. Tiefenbacher J. Mapping the pesticide driftscape: theoretical patterns of the drift hazard. Geogr Environ Model. 1998;2:83–102.
30. Camann DE, Geno PW, Harding HJ, et al. A pilot study of pesticides in indoor air in relation to agricultural applications. In: Indoor air’93: proceedings of 6th International Conference on Indoor Air Quality and Climate. Helsinki: Finnish Society of Indoor Air Quality and Climate; 1993. p. 207–12.
31. CPDR. Summary of pesticide use report data. Sacramento: California Department of Pesticide Regulation; 2000.
32. Teschke K, Chow Y, Bartlett K, et al. Spatial and temporal distribution of airborne Bacillus thuringiensis var. kurstaki during an aerial spray program for gypsy moth eradication. Environ Health Perspect. 2001;109:47–54.
33. Baker LW, Fitzell DL, Seiber JN, et al. Ambient air concentrations of pesticides in California. Environ Sci Technol. 1996;30:1365–8.
34. Majewski MS, Foreman WT, Goolsby DA, et al. Airborne pesticide residues along the Mississippi River. Environ Sci Technol. 1998;32:3689–98.
35. Harnly M, McLaughlin R, Bradman A, et al. Correlating agricultural use of organophosphates with outdoor air concentrations: a particular concern for children. Environ Health Perspect. 2005;113:1184–9.
36. Wofford P, Segawa R, Schreider J, et al. Community air monitoring for pesticides. Part 3: using health-based screening levels to evaluate results collected for a year. Environ Monit Assess. 2014;186:1355–70.
37. Ward MH, Colt JS, Metayer C, et al. Residential exposure to polychlorinated biphenyls and organochlorine pesticides and risk of childhood leukemia. Environ Health Perspect. 2009;117:1007–13.
38. Jones BC, Huang X, Mailman RB, et al. The perplexing paradox of paraquat: the case for host-based susceptibility and postulated neurodegenerative effects. J Biochem Mol Toxicol. 2014;28:191–7.
39. Costello S, Cockburn M, Bronstein J, et al. Parkinson’s disease and residential exposure to maneb and paraquat from agricultural applications in the central valley of California. Am J Epidemiol. 2009;169:919–26.
40. Kelada SNP, Checkoway H, Kardia SLR, et al. 5′ and 3′ region variability in the dopamine transporter gene (SLC6A3), pesticide exposure and Parkinson’s disease risk: a hypothesis-generating study. Hum Mol Genet. 2006;15:3055–62. doi:10.1093/hmg/ddl247.
41. Kelada SN, Costa-Mallen P, Checkoway H, et al. Dopamine transporter (SLC6A3) 5′ region haplotypes significantly affect transcriptional activity in vitro but are not associated with Parkinson’s disease. Pharmacogenet Genomics. 2005;15:659–68.
42. Drgon T, Lin Z, Wang G-J, et al. Common human 5′ dopamine transporter (SLC6A3) haplotypes yield varying expression levels in vivo. Cell Mol Neurobiol. 2006;26:875–89.
43. Ritz BR, Manthripragada AD, Costello S, et al. Dopamine transporter genetic variants and pesticides in Parkinson’s disease. Environ Health Perspect. 2009;117:964–9.
44. Droździk M, Białecka M, Myśliwiec K, et al. Polymorphism in the P-glycoprotein drug transporter MDR1 gene: a possible link between environmental and genetic factors in Parkinson’s disease. Pharmacogenetics. 2003;13:259–63.
45. Zschiedrich K, König IR, Brüggemann N, et al. MDR1 variants and risk of Parkinson disease. Association with pesticide exposure? J Neurol. 2009;256:115–20.
46. Dutheil F, Beaune P, Tzourio C, et al. Interaction between ABCB1 and professional exposure to organochlorine insecticides in Parkinson disease. Arch Neurol. 2010;67:739–45.
47. Narayan S, Sinsheimer JS, Paul KC, et al. Genetic variability in ABCB1, occupational pesticide exposure, and Parkinson’s disease. Environ Res. 2015. Accepted A.
48. Lee P-C, Rhodes SL, Sinsheimer JS, et al. Functional paraoxonase 1 variants modify the risk of Parkinson’s disease due to organophosphate exposure. Environ Int. 2013;56:42–7.
49. Hancock DB, Martin ER, Vance JM, et al. Nitric oxide synthase genes and their interactions with environmental factors in Parkinson’s disease. Neurogenetics. 2008;9:249–62.
50. Paul KC, Sinsheimer JS, Rhodes SL, et al. Organophosphate pesticide exposures, nitric oxide synthase gene variants, and gene-pesticide interactions in a case-control study of Parkinson’s Disease, California (USA). Environ Health Perspect. 2015. doi:10.1289/ehp.1408976. Published Online First.
51. Rhodes SL, Fitzmaurice AG, Cockburn M, et al. Pesticides that inhibit the ubiquitin-proteasome system: effect measure modification by genetic variation in SKP1 in Parkinson׳s disease. Environ Res. 2013;126:1–8.
52. Kannarkat GT, Cook DA, Lee J-K, et al. Common genetic variant association with altered HLA expression, synergy with pyrethroid exposure, and risk for Parkinson’s disease: an observational and case–control study. NPJ Park Dis. 2015;1:15002.
53. Shimizu K, Matsubara K, Ohtaki K, et al. Paraquat leads to dopaminergic neural vulnerability in organotypic midbrain culture. Neurosci Res. 2003;46:523–32.
54. Richardson JR, Quan Y, Sherer TB, et al. Paraquat neurotoxicity is distinct from that of MPTP and rotenone. Toxicol Sci. 2005;88:193–201.
55. Rappold PM, Cui M, Chesser AS, et al. Paraquat neurotoxicity is mediated by the dopamine transporter and organic cation transporter-3. Proc Natl Acad Sci U S A. 2011;108:20766–71.
56. Van de Giessen EM, de Win MML, Tanck MWT, et al. Striatal dopamine transporter availability associated with polymorphisms in the dopamine transporter gene SLC6A3. J Nucl Med. 2009;50:45–52.
57. Schinkel AH, Smit JJ, van Tellingen O, et al. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell. 1994;77:491–502.
58. Bain LJ, McLachlan JB, LeBlanc GA. Structure-activity relationships for xenobiotic transport substrates and inhibitory ligands of P-glycoprotein. Environ Health Perspect. 1997;105:812–8.
59. Lecoeur S, Videmann B, Mazallon M. Effect of organophosphate pesticide diazinon on expression and activity of intestinal P-glycoprotein. Toxicol Lett. 2006;161:200–9.
60. Sreeramulu K, Liu R, Sharom FJ. Interaction of insecticides with mammalian P-glycoprotein and their effect on its transport function. Biochim Biophys Acta. 2007;1768:1750–7.
61. Kimchi-Sarfaty C, Oh JM, Kim I-W, et al. A ‘silent’ polymorphism in the MDR1 gene changes substrate specificity. Science. 2007;315:525–8.
62. Cascorbi I, Gerloff T, Johne A, et al. Frequency of single nucleotide polymorphisms in the P-glycoprotein drug transporter MDR1 gene in white subjects. Clin Pharmacol Ther. 2001;69:169–74.
63. Hitzl M, Schaeffeler E, Hocher B, et al. Variable expression of P-glycoprotein in the human placenta and its association with mutations of the multidrug resistance 1 gene (MDR1, ABCB1). Pharmacogenetics. 2004;14:309–18.
64. Wang A, Cockburn M, Ly TT, et al. The association between ambient exposure to organophosphates and Parkinson’s disease risk. Occup Environ Med. 2014;71:275–81. doi:10.1136/oemed-2013-101394.
65. Davies HG, Richter RJ, Keifer M, et al. The effect of the human serum paraoxonase polymorphism is reversed with diazoxon, soman and sarin. Nat Genet. 1996;14:334–6.
66. Richter RJ, Jarvik GP, Furlong CE. Paraoxonase 1 (PON1) status and substrate hydrolysis. Toxicol Appl Pharmacol. 2009;235:1–9.
67. Costa LG, Cole TB, Furlong CE. Polymorphisms of paraoxonase (PON1) and their significance in clinical toxicology of organophosphates. J Toxicol Clin Toxicol. 2003;41:37–45.
68. O’Leary KA, Edwards RJ, Town MM, et al. Genetic and other sources of variation in the activity of serum paraoxonase/diazoxonase in humans: consequences for risk from exposure to diazinon. Pharmacogenet Genomics. 2005;15:51–60.
69. Liu Y-L, Yang J, Zheng J, et al. Paraoxonase 1 polymorphisms L55M and Q192R were not risk factors for Parkinson’s disease: a HuGE review and meta-analysis. Gene. 2012;501:188–92.
70. Taylor MC, Le Couteur DG, Mellick GD, et al. Paraoxonase polymorphisms, pesticide exposure and Parkinson’s disease in a Caucasian population. J Neural Transm. 2000;107:979–83.
71. Dick FD, De Palma G, Ahmadi A, et al. Gene-environment interactions in Parkinsonism and Parkinson’s disease: the Geoparkinson study. Occup Environ Med. 2007;64:673–80.
72. Kavya R, Saluja R, Singh S, et al. Nitric oxide synthase regulation and diversity: implications in Parkinson’s disease. Nitric Oxide. 2006;15:280–94.
73. Dauer W, Przedborski S. Parkinson’s disease: mechanisms and models. Neuron. 2003;39:889–909.
74. Lukaszewicz-Hussain A. Role of oxidative stress in organophosphate insecticide toxicity—short review. Pestic Biochem Physiol. 2010;98:145–50.
75. Licinio J, Prolo P, McCann SM, et al. Brain iNOS: current understanding and clinical implications. Mol Med Today. 1999;5:225–32.
76. Hague S, Peuralinna T, Eerola J, et al. Confirmation of the protective effect of iNOS in an independent cohort of Parkinson disease. Neurology. 2004;62:635–6.
77. Huerta C, Sánchez-Ferrero E, Coto E, et al. No association between Parkinson’s disease and three polymorphisms in the eNOS, nNOS, and iNOS genes. Neurosci Lett. 2007;413:202–5.
78. Levecque C, Elbaz A, Clavel J, et al. Association between Parkinson’s disease and polymorphisms in the nNOS and iNOS genes in a community-based case-control study. Hum Mol Genet. 2003;12:79–86.
79. Schulte C, Sharma M, Mueller JC, et al. Comprehensive association analysis of the NOS2A gene with Parkinson disease. Neurology. 2006;67:2080–2.
80. Przedborski S, Jackson-Lewis V, Yokoyama R, et al. Role of neuronal nitric oxide in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced dopaminergic neurotoxicity. Proc Natl Acad Sci U S A. 1996;93:4565–71.
81. Liberatore GT, Jackson-Lewis V, Vukosavic S, et al. Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat Med. 1999;5:1403–9.
82. Hunot S, Boissière F, Faucheux B, et al. Nitric oxide synthase and neuronal vulnerability in Parkinson’s disease. Neuroscience. 1996;72:355–63.
83. Tsang AHK, Lee Y-I, Ko HS, et al. S-nitrosylation of XIAP compromises neuronal survival in Parkinson’s disease. Proc Natl Acad Sci U S A. 2009;106:4900–5.
84. Michel TM, Käsbauer L, Gsell W, et al. Aldehyde dehydrogenase 2 in sporadic Parkinson’s disease. Parkinsonism Relat Disord. 2014;20:S68–72.
85. Goldstein DS, Sullivan P, Cooney A, et al. Rotenone decreases intracellular aldehyde dehydrogenase activity: implications for the pathogenesis of Parkinson’s disease. J Neurochem. 2015;133:14–25.
86. Chiu C-C, Yeh T-H, Lai S-C, et al. Neuroprotective effects of aldehyde dehydrogenase 2 activation in rotenone-induced cellular and animal models of parkinsonism. Exp Neurol. 2015;263:244–53.
87. Fitzmaurice AG, Rhodes SL, Lulla A, et al. Aldehyde dehydrogenase inhibition as a pathogenic mechanism in Parkinson disease. Proc Natl Acad Sci U S A. 2013;110:636–41. doi:10.1073/pnas.1220399110.
88. Yoshii SR, Kishi C, Ishihara N, et al. Parkin mediates proteasome-dependent protein degradation and rupture of the outer mitochondrial membrane. J Biol Chem. 2011;286:19630–40.
89. Ebrahimi-Fakhari D, Wahlster L, McLean PJ. Protein degradation pathways in Parkinson’s disease: curse or blessing. Acta Neuropathol. 2012;124:153–72.
90. Licker V, Kövari E, Hochstrasser DF, et al. Proteomics in human Parkinson’s disease research. J Proteome. 2009;73:10–29.
91. Wakabayashi K, Tanji K, Odagiri S, et al. The Lewy body in Parkinson’s disease and related neurodegenerative disorders. Mol Neurobiol. 2013;47:495–508.
92. Chen Q, Thorpe J, Keller JN. Alpha-synuclein alters proteasome function, protein synthesis, and stationary phase viability. J Biol Chem. 2005;280:30009–17.
93. Betarbet R, Sherer TB, Greenamyre JT. Ubiquitin-proteasome system and Parkinson’s diseases. Exp Neurol. 2005;191 Suppl 1:S17–27.
94. Chou AP, Li S, Fitzmaurice AG, et al. Mechanisms of rotenone-induced proteasome inhibition. Neurotoxicology. 2010;31:367–72.
95. Chou AP, Maidment N, Klintenberg R, et al. Ziram causes dopaminergic cell damage by inhibiting E1 ligase of the proteasome. J Biol Chem. 2008;283:34696–703.
96. Wills J, Credle J, Oaks AW, et al. Paraquat, but not maneb, induces synucleinopathy and tauopathy in striata of mice through inhibition of proteasomal and autophagic pathways. PLoS ONE. 2012;7:e30745.
97. Bai C, Sen P, Hofmann K, et al. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell. 1996;86:263–74.
98. Grünblatt E, Mandel S, Jacob-Hirsch J, et al. Gene expression profiling of parkinsonian substantia nigra pars compacta; alterations in ubiquitin-proteasome, heat shock protein, iron and oxidative stress regulated proteins, cell adhesion/cellular matrix and vesicle trafficking genes. J Neural Transm. 2004;111:1543–73.
99. Fishman-Jacob T, Reznichenko L, Youdim MBH, et al. A sporadic Parkinson disease model via silencing of the ubiquitin-proteasome/E3 ligase component SKP1A. J Biol Chem. 2009;284:32835–45.
100. Esa AH, Warr GA, Newcombe DS. Immunotoxicity of organophosphorus compounds. Modulation of cell-mediated immune responses by inhibition of monocyte accessory functions. Clin Immunol Immunopathol. 1988;49:41–52.
101. Freire C, Koifman S. Pesticide exposure and Parkinson’s disease: epidemiological evidence of association. Neurotoxicology. 2012;33:947–71.
102. Dardiotis E, Xiromerisiou G, Hadjichristodoulou C, et al. The interplay between environmental and genetic factors in Parkinson’s disease susceptibility: the evidence for pesticides. Toxicology. 2013;307:17–23. doi:10.1016/j.tox.2012.12.016.