Exposure to atrazine during gestation and lactation periods: Toxicity effects on dopaminergic neurons in offspring by downregulation of Nurr1 and VMAT2

International Journal of Molecular Sciences

Volumn 15, Issue 2, 2014, Pages 2811-2825

  Sun, Yan ^a   Li, Yan Shu ^a   Yang, Jun Wei ^a   Yu, Jia ^a   Wu, Yan Ping ^a   Li, Bai Xiang ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Atrazine; Dopaminergic neuron; Orphan nuclear hormone; Vesicular monoaminetransporter 2

Indexed keywords

ATRAZINE; DOPAMINE; DOPAMINE TRANSPORTER; NUCLEAR RECEPTOR RELATED FACTOR 1; TYROSINE 3 MONOOXYGENASE; VESICULAR MONOAMINE TRANSPORTER 2; HERBICIDE; MESSENGER RNA; NR4A2 PROTEIN, RAT; SLC18A2 PROTEIN, RAT; VESICULAR MONOAMINE TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FEMALE; FOOD INTAKE; GENDER; GESTATION PERIOD; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LACTATION; MALE; NONHUMAN; PROGENY; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; WESTERN BLOTTING; ADVERSE EFFECTS; ANIMAL; CORPUS STRIATUM; DOWN REGULATION; DRUG EFFECTS; ENVIRONMENTAL EXPOSURE; GENETICS; METABOLISM; PREGNANCY; SPRAGUE DAWLEY RAT;

ANIMALS; ATRAZINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CORPUS STRIATUM; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOPAMINERGIC NEURONS; DOWN-REGULATION; FEMALE; HERBICIDES; LACTATION; MALE; MATERNAL EXPOSURE; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 2; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TYROSINE 3-MONOOXYGENASE; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 84894079357     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15022811     Document Type: Article

References (48)

1. Tanner, C.M.; Chen, B.; Wang, W.; Peng, M.; Liu, Z.; Liang, X.; Kao, L.C.; Gilley, D.W.; Goetz, C.G.; Schoenberg, B.S. Environmental factors and Parkinson's disease: A case-control study in China. Neurology 1989, 39, 660-664.
2. Cory-Slechta, D.A.; Thiruchelvam, M.; Barlow, B.K.; Richfield, E.K. Developmental pesticide models of the Parkinson disease phenotype. Environ. Health Perspect. 2005, 113, 1263-1270.
3. Brown, T.P.; Rumsby, P.C.; Capleton, A.C.; Rushton, L.; Levy, L.S. Pesticides and Parkinson's disease-is there a Link? Environ. Health Perspect. 2006, 114, 156-164.
4. McCormack, A.L.; Thiruchelvam, M.; Manning-Bog, A.B.; Thiffault, C.; Langston, J.W.; Cory-Slechta, D.A.; di Monte, D.A. Environmental risk factors and Parkinson's disease: Selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat. Neurobiol. Dis. 2002, 10, 119-127.
5. Drechsel, D.A.; Patel, M. Role of reactive oxygen species in the neurotoxicity of environmental agents implicated in Parkinson's disease. Free Radic. Biol. Med. 2008, 44, 1873-1886.
6. Gao, H.M.; Hong, J.S.; Zhang, W.; Liu, B. Synergistic dopaminergic neurotoxicity of the pesticide rotenone and inflammogen lipopolysaccharide: Relevance to the etiology of Parkinson's disease. J. Neurosci. 2003, 23, 1228-1236.
7. Hines, C.J.; Deddens, J.A.; Lu, C.; Fenske, R.; Striley, C.A. Mixed-effect models for evaluating multiple measures of atrazine exposure among custom applicators. J. Occup. Environ Hyg. 2006, 3, 274-283.
8. Cooper, R.L.; Stoker, T.E.; Tyrey, L.; Goldman, J.M.; McElroy, W.K. Atrazine disrupts the hypothalamic control of pituitary-ovarian function. Toxicol. Sci. 2000, 53, 297-307.
9. Narotsky, M.G.; Best, D.S.; Guidici, D.L.; Cooper, R.L. Strain comparisons of atrazine-induced pregnancy loss in the rat. Reprod. Toxicol. 2001, 15, 61-69.
10. Stoker, T.E.; Guidici, D.L.; Laws, S.C.; Cooper, R.L. The effects of atrazine metabolites on puberty and thyroid function in the male Wistar rat. Toxicol. Sci. 2002, 67, 198-206.
11. Rodriguez, V.M.; Thiruchelvam, M.; Cory-Slechta, D.A. Sustained exposure to the widely used herbicide atrazine: Altered function and loss of neurons in brain monoamine systems. Environ. Health Perspect. 2005, 113, 708-715.
12. Coban, A.; Filipov, N.M. Dopaminergic toxicity associated with oral exposure to the herbicide atrazine in juvenile male C57BL/6 mice. J. Neurochem. 2007, 100, 1177-1187.
13. Rosenberg, B.G.; Chen, H.; Folmer, J.; Liu, J.; Papadopoulos, V.; Zirkin, B.R. Gestational exposure to atrazine: Effects on the postnatal development of male offspring. J. Androl. 2008, 29, 304-311.
14. Richardson, J.R.; Caudle, W.M.; Wang, M.Z.; Dean, E.D.; Pennell, K.D.; Miller, G.W. 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 2008, 29, 855-863.
15. Tanner, C.M.; Ottman, R.; Goldman, S.M.; Ellenberg, J.; Chan, P.; Mayeux, R.; Langston, J.W. Parkinson disease in twins: An etiologic study. JAMA 1999, 281, 341-346.
16. Federoff, H.J. Nur(R1) turing a notion on the etiopathogenesis of Parkinson's disease. Neurotox. Res. 2009, 16, 261-270.
17. Katunar, M.R.; Saez, T.; Brusco, A.; Antonelli, M.C. Immunocytochemical expression of dopamine-related transcription factors Pitx3 and Nurr1 in prenatally stressed adult rats. J. Neurosci. Res. 2009, 87, 1014-1022.
18. Decressac, M.; Kadkhodaei, B.; Mattsson, B.; Laguna, A.; Perlmann, T.; Björklund, A. Alpha-synuclein-induced down-regulation of nurr1 disrupts GDNF signaling in nigral dopamine neurons. Sci. Transl. Med. 2012, 4, 163ra156.
19. Short, P.; Colborn, T. Pesticide use in the U.S. and policy implications: A focus on herbicides. Toxicol. Ind. Health 1999, 15, 240-275.
20. Gilliom, R.J.; Barbash, J.E.; Crawford, C.G.; Hamilton, P.A.; Martin, J.D.; Nakagaki, N.; Nowell, L.H.; Scott, J.C. Pesticides in the Nation's Streams and Groundwater, 1992-2001; U.S. Geological Survey: Reston, VA, USA, 2006; pp. 2006-3028.
21. Benotti, M.J.; Trenholm, R.A.; Vanderford, B.J.; Holady, J.C.; Stanford, B.D.; Snyder, S.A. Pharmaceuticals and endocrine disrupting compounds in U.S. drinking water. Environ. Sci. Technol. 2009, 43, 597-603.
22. Bossi, R.; Vejrup, K.V.; Mogensen, B.B.; Asman, W.A. Analysis of polar pesticides in rainwater in Denmark by liquid chromatography-tandem mass spectrometry. J. Chromatogr. A 2002, 957, 27-36.
23. Brun, G.L.; MacDonald, R.M.; Verge, J.; Aubé, J. Long-term atmospheric deposition of current-use and banned pesticides in Atlantic Canada; 1980-2000. Chemosphere 2008, 71, 314-327.
24. Jablonowski, N.D.; Schaffer, A.; Burauel, P. Still present after all these years: Persistence plus potential toxicity raise questions about the use of atrazine. Environ. Sci. Pollut. Res. Int. 2011, 18, 328-331.
25. Ross, M.K.; Jones, T.L.; Filipov, N.M. Disposition of the herbicide 2-chloro-4-(ethylamino)-6-(isopropylamino)-s-triazine (Atrazine) and its major metabolites in mice: A liquid chromatography/mass spectrometry analysis of urine, plasma, and tissue levels. Drug Metab. Dispos. 2009, 37, 776-786.
26. US Environmental Protection Agency (EPA). Atrazine, Simazine, and Cyanazine: Notice of Initiation of Special Review; EPA: Washington, DC, USA, 1994.
27. Gammon, D.W.; Aldous, C.N.; Carr, W.C., Jr.; Sanborn, J.R.; Pfeifer, K.F. A risk assessment of atrazine use in California: Human health and ecological aspects. Pest Manag. Sci. 2005, 61, 331-355.
28. Curwin, B.D.; Hein, M.J.; Sanderson, W.T.; Striley, C.; Heederik, D.; Kromhout, H.; Reynolds, S.J.; Alavanja, M.C. Urinary pesticide concentrations among children, mothers and fathers living in farm and non-farm households in iowa. Ann. Occup. Hyg. 2007, 51, 53-65.
29. Rayner, J.L.; Enoch, R.R.; Wolf, D.C.; Fenton, S.E. Atrazine-induced reproductive tract alterations after transplacental and/or lactational exposure in male Long-Evans rats. Toxicol. Appl. Pharmacol. 2007, 218, 238-248.
30. US Environmental Protection Agency (EPA). Interim Registration Eligibility Decision for Atrazine; EPA: Washington, DC, USA, 2003.
31. Bayer, S.A.; Wills, K.V.; Triarhou, L.C.; Verina, T.; Thomas, J.D.; Ghetti, B. Selective vulnerability of late-generated dopaminergic neurons of the substantia nigra in weaver mutant mice. Proc. Natl. Acad. Sci. USA 1995, 92, 9137-9140.
32. Van den Munckhof, P.; Luk, K.C.; Ste-Marie, L.; Montgomery, J.; Blanchet, P.J.; Sadikot, A.F.; Drouin, J. Pitx3 is required for motor activity and for survival of a subset of midbrain dopaminergic neurons. Development 2003, 130, 2535-2542.
33. Rayner, J.L.; Wood, C.; Fenton, S.E. Exposure parameters necessary for delayed puberty and mammary gland development in Long-Evans rats exposed in utero to atrazine. Toxicol. Appl. Pharmacol. 2004, 195, 23-34.
34. Stoker, T.E.; Robinette, C.L.; Cooper, R.L. Maternal exposure to atrazine during lactation suppresses suckling-induced prolactin release and results in prostatitis in the adult offspring. Toxicol. Sci. 1999, 52, 68-79.
35. Cooper, R.L.; Laws, S.C.; Das, P.C.; Narotsky, M.G.; Goldman, J.M.; Lee Tyrey, E.; Stoker, T.E. Atrazine and reproductive function: Mode and mechanism of action studies. Birth Defects Res. B Dev. Reprod. Toxicol. 2007, 80, 98-112.
36. Heindel, J.J. Role of exposure to environmental chemicals in the developmental basis of disease and dysfunction. Reprod. Toxicol. 2007, 23, 257-259.
37. Barker, D.J.; Osmond, C.; Law, C.M. The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis. J. Epidemiol. Community Health 1989, 43, 237-240.
38. Das, P.C.; McElroy, W.K.; Cooper, R.L. Differential modulation of catecholamines by chlorotriazine herbicides in pheochromocytoma (PC12) cells in vitro. Toxicol. Sci. 2000, 56, 324-331.
39. Das, P.C.; McElroy, W.K.; Cooper, R.L. Potential mechanisms responsible for chlorotriazine-induced alterations in catecholamines in pheochromocytoma (PC12) cells. Life Sci. 2003, 73, 3123-3138.
40. Filipov, N.M.; Stewart, M.A.; Carr, R.L.; Sistrunk, S.C. Dopaminergic toxicity of the herbicide atrazine in rat striatal slices. Toxicology 2007, 232, 68-78.
41. Cooper, J.R.; Bloom, F.E.; Roth, R.H. The Biochemical Basis of Neuropharmacology; Oxford University Press: New York, NY, USA, 2003.
42. Caudle, W.M.; Richardson, J.R.; Wang, M.; Miller, G.W. Perinatal heptachlor exposure increases expression of presynaptic dopaminergic markers in mouse striatum. Neurotoxicology 2005, 26, 721-728.
43. Hermanson, E.; Joseph, B.; Castro, D.; Lindqvist, E.; Aarnisalo, P.; Wallen, A.; Benoit, G.; Hengerer, B.; Olson, L.; Perlmann, T. Nurr1 regulates dopamine synthesis and storage in MN9D dopamine cells. Exp. Cell Res. 2003, 288, 324-334.
44. Smits, S.M.; Ponnio, T.; Conneely, O.M.; Burbach, J.P.; Smidt, M.P. Involvement of Nurr1 in specifying the neurotransmitter identity of ventral midbrain dopaminergic neurons. Eur. J. Neurosci. 2003, 18, 1731-1738.
45. LaVoie, M.J.; Hastings, T.G. Dopamine quinone formation and protein modification associated with the striatal neurotoxicity of methamphetamine: Evidence against a role for extracellular dopamine. J. Neurosci. 1999, 19, 1484-1491.
46. Miller, G.W.; Gainetdinov, R.R.; Levey, A.I.; Caron, M.G. Dopamine transporters and neuronal injury. Trends Pharmacol. Sci. 1999, 20, 424-429.
47. Chiueh, C.C.; Andoh, T.; Lai, A.R.; Lai, E.; Krishna, G. Neuroprotective strategies in Parkinson's disease: Protection against progressive nigral damage induced by free radicals. Neurotox. Res. 2000, 2, 293-310.
48. Berman, S.B.; Hastings, T.G. Dopamine oxidation alters mitochondrial respiration and induces permeability transition in brain mitochondria: Implications for Parkinson's disease. J. Neurochem. 1999, 73, 1127-1137.