Neonatal parathion exposure disrupts serotonin and dopamine synaptic function in rat brain regions: Modulation by a high-fat diet in adulthood

Neurotoxicology and Teratology

Volumn 31, Issue 6, 2009, Pages 390-399

  Slotkin, Theodore A ^a   Wrench, Nicola ^a   Ryde, Ian T ^a   Lassiter, T Leon ^a   Levin, Edward D ^a   Seidler, Frederic J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Brain development; Dopamine; High fat diet; Organophosphate insecticides; Parathion; Serotonin

Indexed keywords

PARATHION; SEROTONIN 1A RECEPTOR; SEROTONIN 2 RECEPTOR; SEROTONIN TRANSPORTER;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DOPAMINE BRAIN LEVEL; DOPAMINE METABOLISM; DOPAMINERGIC SYSTEM; FRONTAL CORTEX; HIPPOCAMPUS; LIPID DIET; NERVE PROJECTION; NEWBORN; NEWBORN PERIOD; NONHUMAN; OCCIPITAL CORTEX; PARIETAL LOBE; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; RECEPTOR UPREGULATION; SEROTONIN BRAIN LEVEL; SEROTONINERGIC SYSTEM; SYNAPTIC TRANSMISSION; TEMPORAL CORTEX;

ANIMALS; ANIMALS, NEWBORN; BRAIN; DOPAMINE; FEMALE; INSECTICIDES; KETOGENIC DIET; MALE; PARATHION; RADIOLIGAND ASSAY; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT1A; RECEPTORS, SEROTONIN, 5-HT2; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SYNAPTIC TRANSMISSION;

ANIMALIA; RATTUS;

EID: 70349740875     PISSN: 08920362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ntt.2009.07.003     Document Type: Article

References (57)

1. Aldridge J.E., Levin E.D., Seidler F.J., and Slotkin T.A. Developmental exposure of rats to chlorpyrifos leads to behavioral alterations in adulthood, involving serotonergic mechanisms and resembling animal models of depression. Environ. Health Perspect. 113 (2005) 527-531
2. Aldridge J.E., Meyer A., Seidler F.J., and Slotkin T.A. Alterations in central nervous system serotonergic and dopaminergic synaptic activity in adulthood after prenatal or neonatal chlorpyrifos exposure. Environ. Health Perspect. 113 (2005) 1027-1031
3. Aldridge J.E., Meyer A., Seidler F.J., and Slotkin T.A. Developmental exposure to terbutaline and chlorpyrifos: pharmacotherapy of preterm labor and an environmental neurotoxicant converge on serotonergic systems in neonatal rat brain regions. Toxicol. Appl. Pharmacol. 203 (2005) 134-144
4. Aldridge J.E., Seidler F.J., Meyer A., Thillai I., and Slotkin T.A. Serotonergic systems targeted by developmental exposure to chlorpyrifos: effects during different critical periods. Environ. Health Perspect. 111 (2003) 1736-1743
5. Aldridge J.E., Seidler F.J., and Slotkin T.A. Developmental exposure to chlorpyrifos elicits sex-selective alterations of serotonergic synaptic function in adulthood: critical periods and regional selectivity for effects on the serotonin transporter, receptor subtypes, and cell signaling. Environ. Health Perspect. 112 (2004) 148-155
6. Arango V., Underwood M.D., Boldrini M., Tamir H., Kassir S.A., Hsiung S., Chen J.J., and Mann J.J. Serotonin-1A receptors, serotonin transporter binding and serotonin transporter mRNA expression in the brainstem of depressed suicide victims. Neuropsychopharmacology 25 (2001) 892-903
7. Barr D.B., Allen R., Olsson A.O., Bravo R., Caltabiano L.M., Montesano A., Nguyen J., Udunka S., Walden D., Walker R.D., et al. Concentrations of selective metabolites of organophosphorus pesticides in the United States population. Environ. Res. 99 (2005) 314-326
8. Bough K.J., and Rho J.M. Anticonvulsant mechanisms of the ketogenic diet. Epilepsia 48 (2007) 43-58
9. Bradman A., Eskenazi B., Barr D.B., Bravo R., Castorina R., Chevrier J., Kogut K., Harnly M.E., and McKone T.E. Organophosphate urinary metabolite levels during pregnancy and after delivery in women living in an agricultural community. Environ. Health Perspect. 113 (2005) 1802-1807
10. Casida J.E., and Quistad G.B. Organophosphate toxicology: safety aspects of nonacetylcholinesterase secondary targets. Chem. Res. Toxicol. 17 (2004) 983-998
11. Clandinin M.T., Foot M., and Robson L. Plasma membrane: can its structure and function be modulated by dietary fat?. Comp. Biochem. Physiol. B 76 (1983) 335-339
12. Clegg D.J., and van Gemert M. Determination of the reference dose for chlorpyrifos: proceedings of an expert panel. J. Toxicol. Environ. Health 2 (1999) 211-255
13. Connolly M.B., Hendson G., and Steinbok P. Tuberous sclerosis complex: a review of the management of epilepsy with emphasis on surgical aspects. Childs Nervous System 22 (2006) 896-908
14. Costa L.G., Cole T.B., and Furlong C.E. Polymorphisms of paraoxonase (PON1) and their significance in clinical toxicology of organophosphates. J. Toxicol. Clin. Toxicol. 41 (2003) 37-45
15. Eskenazi B., Marks A.R., Bradman A., Harley K., Barr D.B., Johnson C., Morga N., and Jewell N.P. Organophosphate pesticide exposure and neurodevelopment in young Mexican-American children. Environ. Health Perspect. 115 (2007) 792-798
16. Evangeliou A., Vlachonikolis I., Mihailidou H., Spilioti M., Skarpalezou A., Makaronas N., Prokopiou A., Christodoulou P., Liapi-Adamidou G., Helidonis E., et al. Application of a ketogenic diet in children with autistic behavior: pilot study. J. Child Neurol. 18 (2003) 113-118
17. Fujita M., Charney D.S., and Innis R.B. Imaging serotonergic neurotransmission in depression: hippocampal pathophysiology may mirror global brain alterations. Biol. Psychiatry 48 (2000) 801-812
18. Furlong C.E., Cole T.B., Jarvik G.P., Pettan-Brewer C., Geiss G.K., Richter R.J., Shih D.M., Tward A.D., Lusis A.J., and Costa L.G. Role of paraoxonase (PON1) status in pesticide sensitivity: genetic and temporal determinants. Neurotoxicology 26 (2005) 651-659
19. Furlong C.E., Holland N.T., Richter R.J., Bradman A., Ho A., and Eskenazi B. PON1 status of farmworker mothers and children as a predictor of organophosphate sensitivity. Pharmacogen. Genomics 16 (2006) 183-190
20. Geiser F. Influence of polyunsaturated and saturated dietary lipids on adipose tissue, brain and mitochondrial membrane fatty acid composition of a mammalian hibernator. Biochim. Biophys. Acta 1046 (1990) 159-166
21. Grandjean P., and Landrigan P.J. Developmental neurotoxicity of industrial chemicals. Lancet 368 (2006) 2167-2178
22. Gudbjarnason S., and Benediktsdottir V.E. Regulation of β-adrenoceptor properties and the lipid milieu in heart muscle membranes during stress. Mol. Cell Biochem. 164 (1996) 137-143
23. Hallbook T., Lundgren J., and Rosen I. Ketogenic diet improves sleep quality in children with therapy-resistant epilepsy. Epilepsia 48 (2007) 59-65
24. Hartman A.L., and Vining E.P.G. Clinical aspects of the ketogenic diet. Epilepsia 48 (2007) 31-42
25. Kelly J.F., Joseph J.A., Denisova N.A., Erat S., Mason R.P., and Roth G.S. Dissociation of striatal GTPase and dopamine release responses to muscarinic cholinergic agonists in F344 rats: influence of age and dietary manipulation. J. Neurochem. 64 (1995) 2755-2764
26. Lassiter T.L., Ryde I.T., MacKillop E.A., Brown K.K., Levin E.D., Seidler F.J., and Slotkin T.A. Exposure of neonatal rats to parathion elicits sex-selective reprogramming of metabolism and alters the response to a high-fat diet in adulthood. Environ. Health Perspect. 116 (2008) 1456-1462
27. Lee W.J., Alavanja M.C.R., Hoppin J.A., Rusiecki J.A., Kamel F., Blair A., and Sandler D.P. Mortality among pesticide applicators exposed to chlorpyrifos in the agricultural health study. Environ. Health Perspect. 115 (2007) 528-534
28. London L., Flisher A.J., Wesseling C., Mergler D., and Kromhout H. Suicide and exposure to organophosphate insecticides: cause or effect?. Am. J. Ind. Med. 47 (2005) 308-321
29. Maes M., and Meltzer H. The Serotonin Hypothesis of Major Depression. In: Bloom F.E., Kupfer D.J., Bunney B.S., Ciaranello R.D., Davis K.L., Koob G.F., Meltzer H.Y., Schuster C.R., Shader R.I., and Watson S.J. (Eds). Psychopharmacology: The Fourth Generation of Progress (1995), Raven Press, New York 933-944
30. Nemeroff C.B. The neurobiology of depression. Sci. Am. 278 6 (1998) 42-49
31. Nutt D.J. The neuropharmacology of serotonin and noradrenaline in depression. Int. Clin. Psychopharmacol. 17 (2002) S1-S12
32. Ponsard B., Durot I., Delerive P., Oudot F., Cordelet C., Grynberg A., and Athias P. Cross-influence of membrane polyunsaturated fatty acids and hypoxia-reoxygenation on α- and β-adrenergic function of rat cardiomyocytes. Lipids 34 (1999) 457-466
33. Pulsifer M.B., Gordon J.M., Brandt J., Vining E.P., and Freeman J.M. Effects of ketogenic diet on development and behavior: preliminary report of a prospective study. Dev. Med. Child Neurol. 43 (2001) 301-306
34. Rauh V.A., Garfinkel R., Perera R., Andrews H., Hoepner L., Barr D., Whitehead D., Tang D., and Whyatt R.M. Impact of prenatal chlorpyrifos exposure on neurodevelopment in the first 3 years of life among inner-city children. Pediatrics 118 (2006) 1845-1859
35. Roegge C.S., Timofeeva O.A., Seidler F.J., Slotkin T.A., and Levin E.D. Developmental diazinon neurotoxicity in rats: later effects on emotional response. Brain Res. Bull. 75 (2008) 166-172
36. Slotkin T.A. Developmental Neurotoxicity of Organophosphates: A Case Study of Chlorpyrifos. In: Gupta R.C. (Ed). Toxicity of Organophosphate and Carbamate Pesticides (2005), Elsevier Academic Press, San Diego 293-314
37. Slotkin T.A., Lassiter T.L., Ryde I.T., Wrench N., Levin E.D., and Seidler F.J. Consumption of a high-fat diet in adulthood ameliorates the effects of neonatal parathion exposure on acetylcholine systems in rat brain regions. Environ. Health Perspect. 117 (2009) 916-922
38. Slotkin T.A., Levin E.D., and Seidler F.J. Comparative developmental neurotoxicity of organophosphate insecticides: effects on brain development are separable from systemic toxicity. Environ. Health Perspect. 114 (2006) 746-751
39. Slotkin T.A., Levin E.D., and Seidler F.J. Developmental neurotoxicity of parathion: progressive effects on serotonergic systems in adolescence and adulthood. Neurotoxicol. Teratol. 31 (2009) 11-17
40. Slotkin T.A., Ryde I.T., Levin E.D., and Seidler F.J. Developmental neurotoxicity of low-dose diazinon exposure of neonatal rats: effects on serotonin systems in adolescence and adulthood. Brain Res. Bull. 75 (2008) 640-647
41. Slotkin T.A., and Seidler F.J. Comparative developmental neurotoxicity of organophosphates in vivo: transcriptional responses of pathways for brain cell development, cell signaling, cytotoxicity and neurotransmitter systems. Brain Res. Bull. 72 (2007) 232-274
42. Slotkin T.A., and Seidler F.J. Developmental exposure to terbutaline and chlorpyrifos, separately or sequentially, elicits presynaptic serotonergic hyperactivity in juvenile and adolescent rats. Brain Res. Bull. 73 (2007) 301-309
43. Slotkin T.A., and Seidler F.J. Developmental neurotoxicants target neurodifferentiation into the serotonin phenotype: chlorpyrifos, diazinon, dieldrin and divalent nickel. Toxicol. Appl. Pharmacol. 233 (2008) 211-219
44. Slotkin T.A., and Seidler F.J. Prenatal chlorpyrifos exposure elicits presynaptic serotonergic and dopaminergic hyperactivity at adolescence: critical periods for regional and sex-selective effects. Reprod. Toxicol. 23 (2007) 421-427
45. Slotkin T.A., and Seidler F.J. The alterations in CNS serotonergic mechanisms caused by neonatal chlorpyrifos exposure are permanent. Dev. Brain Res. 158 (2005) 115-119
46. Slotkin T.A., and Seidler F.J. Transcriptional profiles reveal similarities and differences in the effects of developmental neurotoxicants on differentiation into neurotransmitter phenotypes in PC12 cells. Brain Res. Bull. 78 (2009) 211-225
47. Slotkin T.A., Seidler F.J., and Ali S.F. Cellular determinants of reduced adaptability of the aging brain: neurotransmitter utilization and cell signaling responses after MDMA lesions. Brain Res. 879 (2000) 163-173
48. Slotkin T.A., Tate C.A., Ryde I.T., Levin E.D., and Seidler F.J. Organophosphate insecticides target the serotonergic system in developing rat brain regions: disparate effects of diazinon and parathion at doses spanning the threshold for cholinesterase inhibition. Environ. Health Perspect. 114 (2006) 1542-1546
49. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., and Klenk D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150 (1985) 76-85
50. Teegarden S.L., Nestler E.J., and Bale T.L. DeltaFosB-mediated alterations in dopamine signaling are normalized by a palatable high-fat diet. Biol. Psychiatry 64 (2008) 941-950
51. Timofeeva O.A., Roegge C.S., Seidler F.J., Slotkin T.A., and Levin E.D. Persistent cognitive alterations in rats after early postnatal exposure to low doses of the organophosphate pesticide, diazinon. Neurotoxicol. Teratol. 30 (2008) 38-45
52. Timofeeva O.A., Sanders D., Seemann K., Yang L., Hermanson D., Regenbogen S., Agoos S., Kallepalli A., Rastogi A., Braddy D., et al. Persistent behavioral alterations in rats neonatally exposed to low doses of the organophosphate pesticide, parathion. Brain Res. Bull. 77 (2008) 404-411
53. Whitney K.D., Seidler F.J., and Slotkin T.A. Developmental neurotoxicity of chlorpyrifos: cellular mechanisms. Toxicol. Appl. Pharmacol. 134 (1995) 53-62
54. Whyatt R.M., Camann D., Perera F.P., Rauh V.A., Tang D., Kinney P.L., Garfinkel R., Andrews H., Hoepner L., and Barr D.B. Biomarkers in assessing residential insecticide exposures during pregnancy and effects on fetal growth. Toxicol. Appl. Pharmacol. 206 (2005) 246-254
55. Xu Z., Seidler F.J., Ali S.F., Slikker W., and Slotkin T.A. Fetal and adolescent nicotine administration: effects on CNS serotonergic systems. Brain Res. 914 (2001) 166-178
56. Yatham L.N., Liddle P.F., Dennie J., Shiah I.S., Adam M.J., Lane C.J., Lam R.W., and Ruth T.J. Decrease in brain serotonin-2 receptor binding in patients with major depression following desipramine treatment: a positron emission tomography study with fluorine-18-labeled setoperone. Arch. Gen. Psychiatry 56 (1999) 705-711
57. Yatham L.N., Liddle P.F., Shiah I.S., Scarrow G., Lam R.W., Adam M.J., Zis A.P., and Ruth T.J. Brain serotonin-2 receptors in major depression: a positron emission tomography study. Arch. Gen. Psychiatry 57 (2000) 850-858