Developmental heptachlor exposure increases susceptibility of dopamine neurons to N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)in a gender-specific manner

NeuroToxicology

Volumn 29, Issue 5, 2008, Pages 855-863

  Richardson, Jason R ^a,b   Caudle, W Michael ^a,b   Wang, Min Zheng ^a,b   Dean, E Danielle ^a,b   Pennell, Kurt D ^a,c   Miller, Gary W ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c Georgia Institute of Technology   (United States)

Author keywords

Dopamine transporter; Fetal basis of adult disease; Heptachlor; Parkinson's disease; Pesticide; Vesicular monoamine transporter 2

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ALPHA SYNUCLEIN; DOPAMINE TRANSPORTER; GLIAL FIBRILLARY ACIDIC PROTEIN; HEPTACHLOR; VESICULAR MONOAMINE TRANSPORTER 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; FEMALE; GESTATION PERIOD; LACTATION; MALE; MOUSE; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SEX DIFFERENCE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPTACHLOR; HOMEODOMAIN PROTEINS; MALE; MICE; MICE, INBRED C57BL; MPTP POISONING; NEURONS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEX FACTORS; TRANSCRIPTION FACTORS; VESICULAR MONOAMINE TRANSPORT PROTEINS;

ANIMALIA; MUS;

EID: 52149102505     PISSN: 0161813X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuro.2008.05.007     Document Type: Article

References (54)

1. Ascherio A., Chen H., Weisskopf M.G., et al. Pesticide exposure and risk for Parkinson's disease. Ann Neurol 60 2 (2006) 197-203
2. Baker D.B., Loo S., and Barker J. Evaluation of human exposure to the heptachlor epoxide contamination of milk in Hawaii. Hawaii Med J 50 3 (1991) 108-112 118
3. Baldereschi M., Di Carlo A., Vanni P., et al. Lifestyle-related risk factors for Parkinson's disease: a population-based study. Acta Neurol Scand 108 4 (2003) 239-244
4. Barker D.J., Osmond C., and Law C.M. The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis. J Epidemiol Community Health 43 3 (1989) 237-240
5. Barlow B.K., Richfield E.K., Cory-Slechta D.A., and Thiruchelvam M. A fetal risk factor for Parkinson's disease. Dev Neurosci 26 1 (2004) 11-23
6. Barlow B.K., Cory-Slechta D.A., Richfield E.K., and Thiruchelvam M. The gestational environment and Parkinson's disease: evidence for neurodevelopmental origins of a neurodegenerative disorder. Reprod Toxicol 23 3 (2007) 457-470
7. Brosenitsch T.A., and Katz D.M. Physiological patterns of electrical stimulation can induce neuronal gene expression by activating N-type calcium channels. J Neurosci 21 8 (2001) 2571-2579
8. Calne D.B., and Langston J.W. Aetiology of Parkinson's disease. Lancet 2 8365-8366 (1983) 1457-1459
9. Carvey P.M., Chang Q., Lipton J.W., and Ling Z. Prenatal exposure to the bacteriotoxin lipopolysaccharide leads to long-term losses of dopamine neurons in offspring: a potential, new model of Parkinson's disease. Front Biosci 8 (2003) 826-837
10. Caudle W.M., Richardson J.R., Wang M., and Miller G.W. Perinatal heptachlor exposure increases expression of presynaptic dopaminergic markers in mouse striatum. Neurotoxicology 26 4 (2005) 721-728
11. Caudle W.M., Richardson J.R., Wang M.Z., et al. Reduced vesicular storage of dopamine causes progressive nigrostriatal neurodegeneration. J Neurosci 27 30 (2007) 8138-8148
12. Chen H., O'Reilly E., McCullough M.L., et al. Consumption of dairy products and risk of Parkinson's disease. Am J Epidemiol 165 9 (2007) 998-1006
13. Corrigan F.M., Murray L., Wyatt C.L., and Shore R.F. Diorthosubstituted polychlorinated biphenyls in caudate nucleus in Parkinson's disease. Exp Neurol 150 2 (1998) 339-342
14. Corrigan F.M., Wienburg C.L., Shore R.F., Daniel S.E., and Mann D. Organochlorine insecticides in substantia nigra in Parkinson's disease. J Toxicol Environ Health A 59 4 (2000) 229-234
15. Cory-Slechta D.A., Thiruchelvam M., Barlow B.K., and Richfield E.K. Developmental pesticide models of the Parkinson disease phenotype. Environ Health Perspect 113 9 (2005) 1263-1270
16. den Tonkelaar E.M., and van Esch G.J. No-effect levels of organochlorine pesticides based on induction of microsomal liver enzymes in short-term toxicity experiments. Toxicology 2 4 (1974) 371-380
17. Di Paola R., and Uitti R.J. Early detection of Parkinson's disease. Implications for treatment. Drugs Aging 9 3 (1996) 159-168
18. Donovan D.M., Miner L.L., Perry M.P., et al. Cocaine reward and MPTP toxicity: alteration by regional variant dopamine transporter overexpression. Brain Res Mol Brain Res 73 1-2 (1999) 37-49
19. Fearnley J.M., Lees A.J., and Ageing. Parkinson's disease: substantia nigra regional selectivity. Brain 114 (1991) 2283-2301 (Pt 5)
20. Fleming L., Mann J.B., Bean J., Briggle T., and Sanchez-Ramos J.R. Parkinson's disease and brain levels of organochlorine pesticides. Ann Neurol 36 1 (1994) 100-103
21. Gainetdinov R.R., Fumagalli F., Jones S.R., and Caron M.G. Dopamine transporter is required for in vivo MPTP neurotoxicity: evidence from mice lacking the transporter. J Neurochem 69 3 (1997) 1322-1325
22. Gainetdinov R.R., Fumagalli F., Wang Y.M., et al. Increased MPTP neurotoxicity in vesicular monoamine transporter 2 heterozygote knockout mice. J Neurochem 70 5 (1998) 1973-1978
23. Hatcher J.M., Richardson J.R., Guillot T.S., et al. Dieldrin exposure induces oxidative damage in the mouse nigrostriatal dopamine system. Exp Neurol 204 2 (2007) 619-630
24. Heindel J.J. Role of exposure to environmental chemicals in the developmental basis of disease and dysfunction. Reprod Toxicol 23 3 (2007) 257-259
25. Hermanson E., Joseph B., Castro D., et al. Nurr1 regulates dopamine synthesis and storage in MN9D dopamine cells. Exp Cell Res 288 2 (2003) 324-334
26. Jia Z., and Misra H.P. Developmental exposure to pesticides zineb and/or endosulfan renders the nigrostriatal dopamine system more susceptible to these environmental chemicals later in life. Neurotoxicology 28 4 (2007) 727-735
27. Kirby M.L., Barlow R.L., and Bloomquist J.R. Neurotoxicity of the organochlorine insecticide heptachlor to murine striatal dopaminergic pathways. Toxicol Sci 61 1 (2001) 100-106
28. Le Couteur D.G., McLean A.J., Taylor M.C., Woodham B.L., and Board P.G. Pesticides and Parkinson's disease. Biomed Pharmacother 53 3 (1999) 122-130
29. Le Marchand L., Kolonel L.N., Siegel B.Z., and Dendle III W.H. Trends in birth defects for a Hawaiian population exposed to heptachlor and for the United States. Arch Environ Health 41 3 (1986) 145-148
30. Ling Z., Gayle D.A., Ma S.Y., et al. In utero bacterial endotoxin exposure causes loss of tyrosine hydroxylase neurons in the postnatal rat midbrain. Mov Disord 17 1 (2002) 116-124
31. Liu J., Morrow A.L., Devaud L.L., Grayson D.R., and Lauder J.M. Regulation of GABA(A) receptor subunit mRNA expression by the pesticide dieldrin in embryonic brainstem cultures: a quantitative, competitive reverse transcription-polymerase chain reaction study. J Neurosci Res 49 5 (1997) 645-653
32. Lloyd S.A., Faherty C.J., and Smeyne R.J. Adult and in utero exposure to cocaine alters sensitivity to the Parkinsonian toxin 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine. Neuroscience 137 3 (2006) 905-913
33. Martinat C., Bacci J.J., Leete T., et al. Cooperative transcription activation by Nurr1 and Pitx3 induces embryonic stem cell maturation to the midbrain dopamine neuron phenotype. Proc Natl Acad Sci U S A 103 8 (2006) 2874-2879
34. Miller G.W., Staley J.K., Heilman C.J., et al. Immunochemical analysis of dopamine transporter protein in Parkinson's disease. Ann Neurol 41 4 (1997) 530-539
35. Miller G.W., Gainetdinov R.R., Levey A.I., and Caron M.G. Dopamine transporters and neuronal injury. Trends Pharmacol Sci 20 10 (1999) 424-429
36. Miller G.W., Kirby M.L., Levey A.I., and Bloomquist J.R. Heptachlor alters expression and function of dopamine transporters. Neurotoxicology 20 4 (1999) 631-637
37. Moser V.C., Shafer T.J., Ward T.R., Meacham C.A., Harris M.W., and Chapin R.E. Neurotoxicological outcomes of perinatal heptachlor exposure in the rat. Toxicol Sci 60 2 (2001) 315-326
38. Narahashi T. Nerve membrane Na+ channels as targets of insecticides. Trends Pharmacol Sci 13 6 (1992) 236-241
39. Park M., Ross G.W., Petrovitch H., et al. Consumption of milk and calcium in midlife and the future risk of Parkinson disease. Neurology 64 6 (2005) 1047-1051
40. Perez-Otano I., Luquin M.R., Oset C., et al. Neurotoxicity induced by prenatal exposure to MPTP on the monoaminergic and peptidergic systems of the marmoset brain. Exp Neurol 131 1 (1995) 108-113
41. Priyadarshi A., Khuder S.A., Schaub E.A., and Shrivastava S. A meta-analysis of Parkinson's disease and exposure to pesticides. Neurotoxicology 21 4 (2000) 435-440
42. Purkerson-Parker S., McDaniel K.L., and Moser V.C. Dopamine transporter binding in the rat striatum is increased by gestational, perinatal, and adolescent exposure to heptachlor. Toxicol Sci 64 2 (2001) 216-223
43. Reuhl K.R. Delayed expression of neurotoxicity: the problem of silent damage. Neurotoxicology 12 3 (1991) 341-346
44. Richardson J.R., and Miller G.W. Acute exposure to aroclor 1016 or 1260 differentially affects dopamine transporter and vesicular monoamine transporter 2 levels. Toxicol Lett 148 1-2 (2004) 29-40
45. Richardson J.R., Caudle W.M., Wang M., Dean E.D., Pennell K.D., and Miller G.W. Developmental exposure to the pesticide dieldrin alters the dopamine system and increases neurotoxicity in an animal model of Parkinson's disease. Faseb J 20 10 (2006) 1695-1697
46. Schmitt C.J. Organochlorine chemical residues in fish from the Mississippi River basin, 1995. Arch Environ Contam Toxicol 43 1 (2002) 81-97
47. Semchuk K.M., Love E.J., and Lee R.G. Parkinson's disease and exposure to agricultural work and pesticide chemicals. Neurology 42 7 (1992) 1328-1335
48. Smialowicz R.J., Williams W.C., Copeland C.B., et al. The effects of perinatal/juvenile heptachlor exposure on adult immune and reproductive system function in rats. Toxicol Sci 61 1 (2001) 164-175
49. Smidt M.P., Smits S.M., and Burbach J.P. Homeobox gene Pitx3 and its role in the development of dopamine neurons of the substantia nigra. Cell Tissue Res 318 1 (2004) 35-43
50. Smith R.J. Hawaiian milk contamination creates alarm: a sour response by state regulators. Science 217 4555 (1982) 137-140
51. Tanner C.M., and Goldman S.M. Epidemiology of Parkinson's disease. Neurol Clin 14 2 (1996) 317-335
52. Thiruchelvam M., Richfield E.K., Goodman B.M., Baggs R.B., and Cory-Slechta D.A. Developmental exposure to the pesticides paraquat and maneb and the Parkinson's disease phenotype. Neurotoxicology 23 4-5 (2002) 621-633
53. Tillerson J.L., Caudle W.M., Reveron M.E., and Miller G.W. Detection of behavioral impairments correlated to neurochemical deficits in mice treated with moderate doses of 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine. Exp Neurol 178 1 (2002) 80-90
54. Van Den Eeden S.K., Tanner C.M., and Bernstein A.L. et al. Incidence of Parkinson's disease: variation by age, gender, and race/ethnicity. Am J Epidemiol 157 11 (2003) 1015-1022