Consumption of a high-fat diet in adulthood ameliorates the effects of neonatal parathion exposure on acetylcholine systems in rat brain regions

Environmental Health Perspectives

Volumn 117, Issue 6, 2009, Pages 916-922

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

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Acetylcholine; Brain development; High fat diet; Organophosphate insecticides; Parathion

Indexed keywords

CHOLINE ACETYLTRANSFERASE; HEMICHOLINIUM 3; NICOTINIC RECEPTOR; PARATHION;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN STEM; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; CORPUS STRIATUM; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; FAT INTAKE; FEMALE; FRONTAL CORTEX; HIPPOCAMPUS; LIPID DIET; MALE; MESENCEPHALON; NERVE CELL DIFFERENTIATION; NONHUMAN; OBESITY; OCCIPITAL CORTEX; PARIETAL LOBE; PRIORITY JOURNAL; PROTEIN DETERMINATION; RAT; RECEPTOR BINDING; SEX DIFFERENCE; SYNAPTIC TRANSMISSION; TEMPORAL CORTEX;

ACETYLCHOLINE; ANIMALS; ANIMALS, NEWBORN; BRAIN; CHOLINE O-ACETYLTRANSFERASE; DIETARY FATS; ENZYME ACTIVATION; FEMALE; HEMICHOLINIUM 3; INSECTICIDES; MALE; PARATHION; PREGNANCY; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC;

ANIMALIA; RATTUS;

EID: 67449159283     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.0800459     Document Type: Article

References (97)

1. Aldridge JE, Levin ED, Seidler FJ, Slotkin TA. 2005. Developmental exposure of rats to chlorpyrifos leads to behavioral alterations in adulthood, involving serotonergic mechanisms and resembling animal models of depression. Environ Health Perspect 113:527-531.
2. Aldridge JE, Seidler FJ, Slotkin TA. 2004. 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 112:148-155.
3. 2. J Neurosci 22:8586-8596.
4. Beer A, Slotkin TA, Seidler FJ, Aldridge JE, Yanai J. 2005. Nicotine therapy in adulthood reverses the synaptic and behavioral deficits elicited by prenatal exposure to phenobarbital. Neuropsychopharmacology 30:156-165.
5. Bough KJ, Rho JM. 2007. Anticonvulsant mechanisms of the ketogenic diet. Epilepsia 48:43-58.
6. Buisson B, Bertrand D. 2001. Chronic exposure to nicotine upregulates the human a4b2 nicotinic acetylcholine receptor function. J Neurosci 21:1819-1829.
7. Buisson B, Bertrand D. 2002. Nicotine addiction: the possible role of functional upregulation. Trends Pharmacol Sci 23:130-136.
8. Casida JE, Quistad GB. 2004. Organophosphate toxicology: safety aspects of nonacetylcholinesterase secondary targets. Chem Res Toxicol 17:983-998.
9. Clandinin MT, Foot M, Robson L. 1983. Plasma membrane: can its structure and function be modulated by dietary fat? Comp Biochem Physiol B 76:335-339.
10. Clegg DJ, van Gemert M. 1999. Determination of the reference dose for chlorpyrifos: proceedings of an expert panel. J Toxicol Environ Health 2:211-255.
11. Colborn T. 2006. A case for revisiting the safety of pesticides: a closer look at neurodevelopment. Environ Health Perspect 114:10-17.
12. Connolly MB, Hendson G, Steinbok P. 2006. Tuberous sclerosis complex: a review of the management of epilepsy with emphasis on surgical aspects. Childs Nervous System 22:896-908.
13. Costa LG. 2006. Current issues in organophosphate toxicology. Clin Chim Acta 366:1-13.
14. Dam K, Garcia SJ, Seidler FJ, Slotkin TA. 1999. Neonatal chlorpyrifos exposure alters synaptic development and neuronal activity in cholinergic and catecholaminergic pathways. Dev Brain Res 116:9-20.
15. Dam K, Seidler FJ, Slotkin TA. 2000. Chlorpyrifos exposure during a critical neonatal period elicits gender-selective deficits in the development of coordination skills and locomotor activity. Dev Brain Res 121:179-187.
16. Dani JA, De Biasi M. 2001. Cellular mechanisms of nicotine addiction. Pharmacol Biochem Behav 70:439-446.
17. Deas D, Brown ES. 2006. Adolescent substance abuse and psychiatric comorbidities. J Clin Psychiat 67:e02.
18. Evangeliou A, Vlachonikolis I, Mihailidou H, Spilioti M, Skarpalezou A, Makaronas N, et al. 2003. Application of a ketogenic diet in children with autistic behavior: pilot study. J Child Neurol 18:113-118.
19. 2 nicotinic receptors is initiated by receptor desensitization after chronic exposure to nicotine. J Neurosci 19:4804-4814.
20. 2 subunits and is upregulated by chronic nicotine treatment. Mol Pharmacol 41:31-37.
21. Geiser F. 1990. Influence of polyunsaturated and saturated dietary lipids on adipose tissue, brain and mitochondrial membrane fatty acid composition of a mammalian hibernator. Biochim Biophys Acta 1046:159-166.
22. Grandjean P, Landrigan PJ. 2006. Developmental neurotoxicity of industrial chemicals. Lancet 368:2167-2178.
23. Gudbjarnason S, Benediktsdottir VE. 1996. Regulation of β-adrenoceptor properties and the lipid milieu in heart muscle membranes during stress. Mol Cell Biochem 164:137-143.
24. Hallbook T, Lundgren J, Rosen I. 2007. Ketogenic diet improves sleep quality in children with therapy-resistant epilepsy. Epilepsia 48:59-65.
25. Happe HK, Murrin LC. 1992. High-affinity choline transport regulation by drug administration during postnatal development. J Neurochem 58:2053-2059.
26. Happe HK, Peters JL, Bergman DA, Murrin LC. 1994. Localization of nicotinic cholinergic receptors in rat brain: autoradiographic studies with [3H]cytisine. Neuroscience 62:929-944.
27. Hartman AL, Vining EPG. 2007. Clinical aspects of the ketogenic diet. Epilepsia 48:31-42.
28. Hilton GD, Ndubuizu AN, McCarthy MM. 2004. Neuroprotective effects of estradiol in newborn female rat hippocampus. Dev Brain Res 150:191-198.
29. Hohmann CF. 2003. A morphogenetic role for acetylcholine in mouse cerebral neocortex. Neurosci Biobehav Rev 27:351-363.
30. Izrael M, Van der Zee EA, Slotkin TA, Yanai J. 2004. Cholinergic synaptic signaling mechanisms underlying behavioral teratogenicity: effects of nicotine, chlorpyrifos and heroin converge on PKC translocation in the IMHV and on imprinting behavior in an avian model. J Neurosci Res 78:499-507.
31. Jacobsen LK, Slotkin TA, Mencl WE, Frost SJ, Pugh KR. 2007. Gender specific effects of prenatal and adolescent exposure to tobacco smoke on auditory and visual attention. Neuropsychopharmacology 32:2453-2464.
32. Kandel DB, Wu P, Davies M. 1994. Maternal smoking during pregnancy and smoking by adolescent daughters. Am J Public Health 84:1407-1413.
33. Kelly JF, Joseph JA, Denisova NA, Erat S, Mason RP, Roth GS. 1995. Dissociation of striatal GTPase and dopamine release responses to muscarinic cholinergic agonists in F344 rats: influence of age and dietary manipulation. J Neurochem 64:2755-2764.
34. Klemm N, Kuhar MJ. 1979. Post-mortem changes in high affinity choline uptake. J Neurochem 32:1487-1494.
35. Landrigan PJ, Graham DG, Thomas RD. 1994. Environmental neurotoxic illness: research for prevention. Environ Health Perspect 102(suppl 2):117-120.
36. Lassiter TL, Brimijoin S. 2008. Rats gain excess weight after developmental exposure to the organophosphorothionate pesticide, chlorpyrifos. Neurotoxicol Teratol 30:125-130.
37. Lassiter TL, Ryde IT, MacKillop EA, Brown KK, Levin ED, Seidler FJ, et al. 2008. 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 116:1456-1462.
38. Lauder JM, Schambra UB. 1999. Morphogenetic roles of acetylcholine. Environ Health Perspect 107(suppl 1):65-69.
39. Laviola G, Adriani W, Gaudino C, Marino R, Keller F. 2006. Paradoxical effects of prenatal acetylcholinesterase blockade on neuro-behavioral development and drug-induced stereotypies in reeler mutant mice. Psychopharmacology 187:331-344.
40. Levin ED, Addy N, Baruah A, Elias A, Christopher NC, Seidler FJ, et al. 2002. Prenatal chlorpyrifos exposure in rats causes persistent behavioral alterations. Neurotoxicol Teratol 24:733-741.
41. Levin ED, Addy N, Christopher NC, Seidler FJ, Slotkin TA. 2001. Persistent behavioral consequences of neonatal chlorpyrifos exposure in rats. Dev Brain Res 130:83-89.
42. McEwen BS. 2002. Sex, stress and the hippocampus: allostasis, allostatic load and the aging process. Neurobiol Aging 23:921-939.
43. Monnet-Tschudi F, Zurich MG, Schilter B, Costa LG, Honegger P. 2000. Maturation-dependent effects of chlorpyrifos and parathion and their oxygen analogs on acetylcholinesterase and neuronal and glial markers in aggregating brain cell cultures. Toxicol Appl Pharmacol 165:175-183.
44. Morgan MK, Sheldon LS, Croghan CW, Jones PA, Robertson GL, Chuang JC, et al. 2005. Exposures of preschool children to chlorpyrifos and its degradation product 3,5,6-trichloro-2-pyridinol in their everyday environments. J Expo Anal Environ Epidemiol 15:297-309.
45. Moser VC, Chanda SM, Mortensen SR, Padilla S. 1998. Age- and gender-related differences in sensitivity to chlorpyrifos in the rat reflect developmental profiles of esterase activities. Toxicol Sci 46:211-222.
46. Murphy P, Burnham WM. 2006. The ketogenic diet causes a reversible decrease in activity level in Long-Evans rats. Exp Neurol 201:84-89.
47. Murphy P, Likhodii SS, Hatamian M, McIntyre Burnham W. 2005. Effect of the ketogenic diet on the activity level of Wistar rats. Pediatr Res 57:353-357.
48. Nunez JL, McCarthy MM. 2003. Sex differences and hormonal effects in a model of preterm infant brain injury. Ann NY Acad Sci 1008:281-284.
49. Picciotto MR, Zoli M. 2008. Neuroprotection via nAChRs: the role of nAChRs in neurodegenerative disorders such as Alzheimer's and Parkinson's disease. Frontiers Biosci 13:492-504.
50. Pliszka SR, Pliszka SR. 2003. Psychiatric comorbidities in children with attention deficit hyperactivity disorder: implications for management. Paediatr Drugs 5:741-750.
51. Ponsard B, Durot I, Delerive P, Oudot F, Cordelet C, Grynberg A, et al. 1999. Cross-influence of membrane polyunsaturated fatty acids and hypoxia-reoxygenation on α- and β-adrenergic function of rat cardiomyocytes. Lipids 34:457-466.
52. Pope CN. 1999. Organophosphorus pesticides: do they all have the same mechanism of toxicity? J Toxicol Environ Health 2:161-181.
53. Pulsifer MB, Gordon JM, Brandt J, Vining EP, Freeman JM. 2001. Effects of ketogenic diet on development and behavior: preliminary report of a prospective study. Dev Med Child Neurol 43:301-306.
54. Qiao D, Seidler FJ, Abreu-Villaça Y, Tate CA, Cousins MM, Slotkin TA. 2004. Chlorpyrifos exposure during neurulation: cholinergic synaptic dysfunction and cellular alterations in brain regions at adolescence and adulthood. Dev Brain Res 148:43-52.
55. Qiao D, Seidler FJ, Tate CA, Cousins MM, Slotkin TA. 2003. Fetal chlorpyrifos exposure: adverse effects on brain cell development and cholinergic biomarkers emerge postnatally and continue into adolescence and adulthood. Environ Health Perspect 111:536-544.
56. Quick MW, Lester RA. 2002. Desensitization of neuronal nicotinic receptors. J Neurobiol 53:457-478.
57. Ricceri L, Venerosi A, Capone F, Cometa MF, Lorenzini P, Fortuna S, et al. 2006. Developmental neurotoxicity of organophosphorous pesticides: fetal and neonatal exposure to chlorpyrifos alters sex-specific behaviors at adulthood in mice. Toxicol Sci 93:105-113.
58. Richardson JR, Chambers JE. 2005. Effects of repeated oral postnatal exposure to chlorpyrifos on cholinergic neurochemistry in developing rats. Toxicol Sci 84:352-359.
59. Roegge CS, Timofeeva OA, Seidler FJ, Slotkin TA, Levin ED. 2008. Developmental diazinon neurotoxicity in rats: later effects on emotional response. Brain Res Bull 75:166-172.
60. Shahak H, Slotkin TA, Yanai J. 2003. Alterations in PKCg in the mouse hippocampus after prenatal exposure to heroin: a link from cell signaling to behavioral outcome. Dev Brain Res 140:117-125.
61. Simon JR, Atweh S, Kuhar MJ. 1976. Sodium-dependent high affinity choline uptake: a regulatory step in the synthesis of acetylcholine. J Neurochem 26:909-922.
62. Slotkin TA. 1999. Developmental cholinotoxicants: nicotine and chlorpyrifos. Environ Health Perspect 107(suppl 1):71-80.
63. Slotkin TA. 2004. Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates. Toxicol Appl Pharmacol 198:132-151.
64. Slotkin TA. 2005. Developmental neurotoxicity of organophosphates: a case study of chlorpyrifos. In: Toxicity of Organophosphate and Carbamate Pesticides (Gupta RC, ed). San Diego: Elsevier Academic Press, 293-314.
65. Slotkin TA, Bodwell BE, Levin ED, Seidler FJ. 2008a. Neonatal exposure to low doses of diazinon: long-term effects on neural cell development and acetylcholine systems. Environ Health Perspect 116:340-348.
66. Slotkin TA, Bodwell BE, Ryde IT, Levin ED, Seidler FJ. 2008b. Exposure of neonatal rats to parathion elicits sex-selective impairment of acetylcholine systems in brain regions during adolescence and adulthood. Environ Health Perspect 116:1308-1314.
67. Slotkin TA, Brown KK, Seidler FJ. 2005. Developmental exposure of rats to chlorpyrifos elicits sex-selective hyperlipidemia and hyperinsulinemia in adulthood. Environ Health Perspect 113:1291-1294.
68. Slotkin TA, Cousins MM, Tate CA, Seidler FJ. 2001a. Persistent cholinergic presynaptic deficits after neonatal chlorpyrifos exposure. Brain Res 902:229-243.
69. Slotkin TA, Levin ED, Seidler FJ. 2006a. Comparative developmental neurotoxicity of organophosphate insecticides: effects on brain development are separable from systemic toxicity. Environ Health Perspect 114:746-751.
70. Slotkin TA, Levin ED, Seidler FJ. 2009. Developmental neurotoxicity of parathion: progressive effects on serotonergic systems in adolescence and adulthood. Neurotoxicol Teratol 31:11-17.
71. Slotkin TA, MacKillop EA, Ryde IT, Tate CA, Seidler FJ. 2007a. Screening for developmental neurotoxicity using PC12 cells: comparisons of organophosphates with a carbamate, an organochlorine and divalent nickel. Environ Health Perspect 115:93-101.
72. Slotkin TA, Ryde IT, Levin ED, Seidler FJ. 2008c. Developmental neurotoxicity of low-dose diazinon exposure of neonatal rats: effects on serotonin systems in adolescence and adulthood. Brain Res Bull 75:640-647.
73. Slotkin TA, Ryde IT, Seidler FJ. 2007b. Separate or sequential exposure to nicotine prenatally and in adulthood: persistent effects on acetylcholine systems in rat brain regions. Brain Res Bull 74:91-103.
74. Slotkin TA, Seidler FJ. 2005. The alterations in CNS serotonergic mechanisms caused by neonatal chlorpyrifos exposure are permanent. Dev Brain Res 158:115-119.
75. Slotkin TA, Seidler FJ. 2007. Prenatal chlorpyrifos exposure elicits presynaptic serotonergic and dopaminergic hyperactivity at adolescence: critical periods for regional and sex-selective effects. Reprod Toxicol 23:421-427.
76. Slotkin TA, Seidler FJ, Yanai J. 2001b. Heroin neuroteratogenicity: targeting adenylyl cyclase as an underlying biochemical mechanism. Dev Brain Res 132:75-85.
77. Slotkin TA, Tate CA, Cousins MM, Seidler FJ. 2002. Functional alterations in CNS catecholamine systems in adolescence and adulthood after neonatal chlorpyrifos exposure. Dev Brain Res 133:163-173.
78. Slotkin TA, Tate CA, Ryde IT, Levin ED, Seidler FJ. 2006b. 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 114:1542-1546.
79. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, et al. 1985. Measurement of protein using bicinchoninic acid. Anal Biochem 150:76-85.
80. Steingart RA, Abou-Roumi M, Newman ME, Silverman WF, Slotkin TA, Yanai J. 2000a. Neurobehavioral damage to cholinergic systems caused by prenatal exposure to heroin or phenobarbital: cellular mechanisms and the reversal of deficits by neural grafting. Dev Brain Res 122:125-133.
81. Steingart RA, Silverman WF, Barron S, Slotkin TA, Awad Y, Yanai J. 2000b. Neural grafting reverses prenatal drug-induced alterations in hippocampal PKC and related behavioral deficits. Dev Brain Res 125:9-19.
82. Szpir M. 2006a. New thinking on neurodevelopment. Environ Health Perspect 114:A101-A107.
83. Szpir M. 2006b. Tracing the origins of autism: a spectrum of new studies. Environ Health Perspect 114:A412-A417.
84. Tanapat P, Hastings NB, Reeves AJ, Gould E. 1999. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19:5792-5801.
85. Teegarden SL, Nestler EJ, Bale TL. 2008. ΔFosB-mediated alterations in dopamine signaling are normalized by a palatable high-fat diet. Biol Psychiat 64:941-950.
86. Timofeeva OA, Roegge CS, Seidler FJ, Slotkin TA, Levin ED. 2008a. Persistent cognitive alterations in rats after early postnatal exposure to low doses of the organophosphate pesticide, diazinon. Neurotoxicol Teratol 30:38-45.
87. Timofeeva OA, Sanders D, Seemann K, Yang L, Hermanson D, Regenbogen S, et al. 2008b. Persistent behavioral alterations in rats neonatally exposed to low doses of the organophosphate pesticide, parathion. Brain Res Bull 77:404-411.
88. Weiss B, Amler S, Amler RW. 2004. Pesticides. Pediatrics 113:1030-1036.
89. Weiss B, Bellinger DC. 2006. Social ecology of children's vulnerability to environmental pollutants. Environ Health Perspect 114:1479-1485.
90. Weissman MM, Warner V, Wickramaratne PJ, Kandel DB. 1999. Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood. J Am Acad Child Adolesc Psychiat 38:892-899.
91. Whiting P, Lindstrom J. 1987. Purification and characterization of a nicotinic acetylcholine receptor from rat brain. Proc Natl Acad Sci 84:595-599.
92. Whiting PR, Lindstrom J. 1988. Characterization of bovine and human neuronal nicotinic acetylcholine receptors using monoclonal antibodies. J Neurosci 8:3395-3404.
93. Whitney KD, Seidler FJ, Slotkin TA. 1995. Developmental neurotoxicity of chlorpyrifos: cellular mechanisms. Toxicol Appl Pharmacol 134:53-62.
94. Wilens TE. 2004. Attention-deficit/hyperactivity disorder and the substance use disorders: the nature of the relationship, subtypes at risk, and treatment issues. Psychiat Clinics N Am 27:283-301.
95. Yanai J, Beer A, Huleihel R, Izrael M, Katz S, Levi Y, et al. 2004. Convergent effects on cell signaling mechanisms mediate the actions of different neurobehavioral teratogens: alterations in cholinergic regulation of PKC in chick and avian models. Ann NY Acad Sci 1025:595-601.
96. Yanai J, Ben-Hur T, Slotkin TA, Katz S. 2005. Neural progenitors for the reversal of heroin neurobehavioral teratogenicity. Proc Intl Soc Stem Cell Res 3:259.
97. Yanai J, Vatury O, Slotkin TA. 2002. Cell signaling as a target and underlying mechanism for neurobehavioral teratogenesis. Ann NY Acad Sci 965:473-478.