In utero and lactational exposure to PCBs in mice: Adult offspring show altered learning and memory depending on CYP1A2 and AHR genotypes

Environmental Health Perspectives

Volumn 119, Issue 9, 2011, Pages 1286-1293

  Curran, Christine P ^a   Nebert, Daniel W ^a   Genter, Mary Beth ^a   Patel, Krishna V ^a   Schaefer, Tori L ^a   Skelton, Matthew R ^a   Williams, Michael T ^a   Vorhees, Charles V ^a  

^a UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

Author keywords

Acoustic startle response; Aryl hydrocarbon receptor (AHR); Coplanar PCBs; Cytochrome P450 1A2 (CYP1A2); Developmental neurotoxicity; Locomotor activity; Long term potentiation; Morris water maze; Noncoplanar PCBs; Novel object recognition; PCB exposure in utero; PCB exposure via breast milk; Polychlorinated biphenyls (PCBs); Prepulse inhibition

Indexed keywords

POLYCHLORINATED BIPHENYL;

AHR GENE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CYP1A2 GENE; DEVELOPMENTAL GENE; FEMALE; GENETIC SUSCEPTIBILITY; GENOTYPE; GESTATIONAL AGE; LACTATION; LEARNING DISORDER; MALE; MAZE TEST; MEMORY DISORDER; MOUSE; NEUROTOXICITY; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; TOXICITY TESTING;

ANIMALS; BIOGENIC MONOAMINES; COMPLEX MIXTURES; CYTOCHROME P-450 CYP1A2; FEMALE; GENOTYPE; LONG-TERM POTENTIATION; MALE; MATERNAL EXPOSURE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MILK; MOTOR ACTIVITY; POLYCHLORINATED BIPHENYLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RECEPTORS, ARYL HYDROCARBON; STARTLE REACTION;

ANIMALIA; MUS;

EID: 80052323766     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1002965     Document Type: Article

References (57)

1. Abe S, Inoue Y, Takamatsu M. 1975. Polychlorinated biphenyl residues in plasma of Yusho children born to mothers who had consumed oil contaminated by PCB [in Japanese]. Fukuoka Igaku Zasshi 66:605-609.
2. Agency for Toxic Substances and Disease Registry. 2007. CERCLA Priority List of Hazardous Substances. Atlanta, GA:Agency for Toxic Substances and Disease Registry.
3. Altmann L, Mundy WR, Ward TR, Fastabend A, Lilienthal H. 2001. Developmental exposure of rats to a reconstituted PCB mixture or Aroclor 1254: effects on long-term potentiation and [3H]MK-801 binding in occipital cortex and hippocampus. Toxicol Sci 61:321-330.
4. Amin S, Moore RW, Peterson RE, Schantz SL. 2000. Gestational and lactational exposure to TCDD or coplanar PCBs alters adult expression of saccharin preference behavior in female rats. Neurotoxicol Teratol 22:675-682.
5. Branchi I, Capone F, Vitalone A, Madia F, Santucci D, Alleva E, et al. 2005. Early developmental exposure to BDE 99 or Aroclor 1254 affects neurobehavioural profile: interference from the administration route. Neurotoxicology 26:183-192.
6. Carpenter DO, Hussain RJ, Berger DF, Lombardo JP, Park HY. 2002. Electrophysiologic and behavioral effects of perinatal and acute exposure of rats to lead and polychlorinated biphenyls. Environ Health Perspect 110(suppl 3):377-386.
7. Chishti MA, Fisher JP, Seegal RF. 1996. Aroclors 1254 and 1260 reduce dopamine concentrations in rat striatal slices. Neurotoxicology 17:653-660.
8. Clancy B, Kersh B, Hyde J, Darlington RB, Anand KJ, Finlay BL. 2007. Web-based method for translating neurodevelopment from laboratory species to humans. Neuroinformatics 5:79-94.
9. Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, et al. 1997. Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl) 132:107-124.
10. Crews ST, Brenman JE. 2006. Spineless provides a little backbone for dendritic morphogenesis. Genes Dev 20:2773-2778.
11. Curran CP, Miller KA, Dalton TP, Vorhees CV, Miller ML, Shertzer HG, et al. 2006. Genetic differences in lethality of newborn mice treated in utero with coplanar versus non-coplanar hexabromobiphenyl. Toxicol Sci 89:454-464.
12. Curran CP, Vorhees CV, Williams MT, Genter MB, Miller ML, Nebert DW. 2011. In utero and lactational exposure to a complex mixture of polychlorinated biphenyls: toxicity in pups dependent on the Cyp1a2 and Ahr genotypes. Toxicol Sci 119:189-208.
13. Dragin N, Dalton TP, Miller ML, Shertzer HG, Nebert DW. 2006. For dioxin-induced birth defects, mouse or human CYP1A2 in maternal liver protects whereas mouse CYP1A1 and CYP1B1 are inconsequential. J Biol Chem 281:18591-18600.
14. Eriksson P. 1997. Developmental neurotoxicity of environmental agents in the neonate. Neurotoxicology 18:719-726.
15. Gilbert ME, Crofton KM. 1999 Developmental exposure to a commercial PCB mixture (Aroclor 1254) produces a persistent impairment in long-term potentiation in the rat dentate gyrus in vivo. Brain Res 850:87-95.
16. Gilbert ME, Mundy WR, Crofton KM. 2000. Spatial learning and long-term potentiation in the dentate gyrus of the hippocampus in animals developmentally exposed to Aroclor 1254. Toxicol Sci 57:102-111.
17. Goldey ES, Crofton KM. 1998. Thyroxine replacement attenuates hypothyroxemia, hearing loss, and motor deficits following developmental exposure to Aroclor 1254 in rats. Toxicol Sci 45:94-105.
18. Goldey ES, Kehn LS, Lau C, Rehnberg GL, Crofton KM. 1995. Developmental exposure to polychlorinated biphenyls (Aroclor 1254) reduces circulating thyroid hormone concentrations and causes hearing deficits in rats. Toxicol Appl Pharmacol 135:77-88.
19. Graham DL, Grace CE, Braun AA, Schaefer TL, Skelton MR, Tang PH, et al. 2011. Effects of developmental stress and lead (Pb) on corticosterone after chronic and acute stress, brain monoamines and blood Pb levels. Int J Dev Neurosci 29(1):45-55.
20. Gralewicz S, Wiaderna D, Lutz P, Sitarek K. 2009. Neurobehavioral functions in adult progeny of rat mothers exposed to methylmercury or 2,2',4,4',5,5'-hexachlorobiphenyl (PCB 153) alone or their combination during gestation and lactation. Int J Occup Med Environ Health 22:277-291.
21. Grandjean P, Weihe P, Burse VW, Needham LL, Storr-Hansen E, Heinzow B, et al. 2001. Neurobehavioral deficits associated with PCB in 7-year-old children prenatally exposed to seafood neurotoxicants. Neurotoxicol Teratol 23:305-317.
22. Guo YL, Lambert GH, Hsu CC, Hsu MM. 2004. Yucheng: health effects of prenatal exposure to polychlorinated biphenyls and dibenzofurans. Int Arch Occup Environ Health 77:153-158.
23. Guo YL, Ryan JJ, Lau BP, Yu ML, Hsu CC. 1997. Blood serum levels of PCBs and PCDFs in Yucheng women 14 years after exposure to a toxic rice oil. Arch Environ Contam Toxicol 33:104-108.
24. Gustavsson P, Hogstedt C. 1997. A cohort study of Swedish capacitor manufacturing workers exposed to polychlorinated biphenyls (PCBs). Am J Ind Med 32(3):234-239.
25. Hamm JT, Chen CY, Birnbaum LS. 2003. A mixture of dioxins, furans, and non-ortho PCBs based upon consensus toxic equivalency factors produces dioxin-like reproductive effects. Toxicol Sci 74:182-191.
26. Huwe JK, Larsen GL. 2005. Polychlorinated dioxins, furans, and biphenyls, and polybrominated diphenyl ethers in a U.S. meat market basket and estimates of dietary intake. Environ Sci Technol 39:5606-5611.
27. Jacobson JL, Jacobson SW. 1997. Evidence for PCBs as neurodevelopmental toxicants in humans. Neurotoxicology 18:415-424.
28. Jacobson JL, Jacobson SW. 2003. Prenatal exposure to polychlorinated biphenyls and attention at school age. J Pediatr 143:780-788.
29. Jacobson LH, Cryan JF. 2007. Feeling strained? Influence of genetic background on depression-related behavior in mice: a review. Behav Genet 37:171-213.
30. Jacobson SW, Fein GG, Jacobson JL, Schwartz PM, Dowler JK. 1985. The effect of intrauterine PCB exposure on visual recognition memory. Child Dev 56:853-860.
31. Kilburn KH. 2000. Visual and neurobehavioral impairment associated with polychlorinated biphenyls. Neurotoxicology 21:489-499.
32. Kodavanti PR, Kannan N, Yamashita N, Derr-Yellin EC, Ward TR, Burgin DE, et al. 2001. Differential effects of two lots of Aroclor 1254: congener-specific analysis and neurochemical end points. Environ Health Perspect 109:1153-1161.
33. Kostyniak PJ, Hansen LG, Widholm JJ, Fitzpatrick RD, Olson JR, Helferich JL, et al. 2005. Formulation and characterization of an experimental PCB mixture designed to mimic human exposure from contaminated fish. Toxicol Sci 88:400-411.
34. Liang HC, Li H, McKinnon RA, Duffy JJ, Potter SS, Puga A, et al. 1996. Cyp1a2(-/-) null mutant mice develop normally but show deficient drug metabolism. Proc Natl Acad Sci USA 93:1671-1676.
35. Nakai K, Suzuki K, Oka T, Murata K, Sakamoto M, Okamura K, et al. 2004. The Tohoku Study of Child Development: a cohort study of effects of perinatal exposures to methylmercury and environmentally persistent organic pollutants on neurobehavioral development in Japanese children. Tohoku J Exp Med 202:227-237.
36. Nebert DW, Dalton TP, Okey AB, Gonzalez FJ. 2004. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J Biol Chem 279:23847-23850.
37. Pavlides C, Westlind-Danielsson AI, Nyborg H, McEwen BS. 1991. Neonatal hyperthyroidism disrupts hippocampal LTP and spatial learning. Exp Brain Res 85:559-564.
38. Petersen MS, Halling J, Bech S, Wermuth L, Weihe P, Nielsen F, et al. 2008. Impact of dietary exposure to food contaminants on the risk of Parkinson disease. Neurotoxicology 29:584-590.
39. Poland A, Glover E. 1977. Chlorinated biphenyl induction of aryl hydrocarbon hydroxylase activity: a study of the structure-activity relationship. Mol Pharmacol 13:924-938.
40. Qin H, Powell-Coffman JA. 2004. The Caenorhabditis elegans aryl hydrocarbon receptor, AHR-1, regulates neuronal development. Dev Biol 270:64-75.
41. Rice DC. 1999. Effect of exposure to 3,3',4,4',5-pentachlorobiphenyl (PCB 126) throughout gestation and lactation on development and spatial delayed alternation performance in rats. Neurotoxicol Teratol 21:59-69.
42. Rice DC. 2000. Parallels between attention deficit hyperactivity disorder and behavioral deficits produced by neurotoxic exposure in monkeys. Environ Health Perspect 108(suppl 3):405-408.
43. Roegge CS, Schantz SL. 2006. Motor function following developmental exposure to PCBS and/or MEHG. Neurotoxicol Teratol 28:260-277.
44. Ryan JJ, Gasiewicz TA, Brown JF Jr. 1990. Human body burden of polychlorinated dibenzofurans associated with toxicity based on the Yusho and Yucheng incidents. Fundam Appl Toxicol 15:722-731.
45. Schantz SL, Gasior DM, Polverejan E, McCaffrey RJ, Sweeney AM, Humphrey HE, et al. 2001. Impairments of memory and learning in older adults exposed to polychlorinated biphenyls via consumption of Great Lakes fish. Environ Health Perspect 109:605-611.
46. Schantz SL, Levin ED, Bowman RE, Heironimus MP, Laughlin NK. 1989. Effects of perinatal PCB exposure on discrimination-reversal learning in monkeys. Neurotoxicol Teratol 11:243-250.
47. Schantz SL, Seo BW, Moshtaghian J, Peterson RE, Moore RW. 1996. Effects of gestational and lactational exposure to TCDD or coplanar PCBs on spatial learning. Neurotoxicol Teratol 18:305-313.
48. Schantz SL, Widholm JJ, Rice DC. 2003. Effects of PCBexposure on neuropsychological function in children. Environ Health Perspect 111:357-576.
49. Seegal RF, Brosch KO, Okoniewski RJ. 1997. Effects of in utero and lactational exposure of the laboratory rat to 2,4,2',4'- and 3,4,3',4'-tetrachlorobiphenyl on dopamine function. Toxicol Appl Pharmacol 146:95-103.
50. Seegal RF, Brosch KO, Okoniewski RJ. 2005. Coplanar PCB congeners increase uterine weight and frontal cortical dopamine in the developing rat: implications for developmental neurotoxicity. Toxicol Sci 86:125-131.
51. Seo BW, Sparks AJ, Medora K, Amin S, Schantz SL. 1999. Learning and memory in rats gestationally and lactationally exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Neurotoxicol Teratol 21:231-239.
52. Shepherd JK, Grewl SS, Fletcher A, Bill DJ, Dourish CT. 1994. Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacol (Berl) 116:56-64.
53. Shimono K, Baudry M, Ho L, Taketani M, Lynch G. 2002. Long-term recording of LTP in cultured hippocampal slices. Neural Plast 9:249-254.
54. Ulbrich B, Stahlmann R. 2004. Developmental toxicity of polychlorinated biphenyls (PCBs): a systematic review of experimental data. Arch Toxicol 78:252-268.
55. Vorhees CV, Williams MT. 2006. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1:848-858.
56. Vreugdenhil HJ, Mulder PG, Emmen HH, Weisglas-Kuperus N. 2004. Effects of perinatal exposure to PCBs on neuropsychological functions in the Rotterdam cohort at 9 years of age. Neuropsychology 18:185-193.
57. Widholm JJ. 2003. Effects of perinatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin on spatial and visual reversal learning in rats. Neurotoxicol Teratol 25:459-471.