PAH particles perturb prenatal processes and phenotypes: Protection from deficits in object discrimination afforded by dampening of brain oxidoreductase following In Utero exposure to inhaled benzo(a)pyrene

Toxicological Sciences

Volumn 125, Issue 1, 2012, Pages 233-247

  Li, Zhu ^a   Chadalapaka, Gayathri ^b,c   Ramesh, Aramandla ^a   Khoshbouei, Habibeh ^a   Maguire, Mark ^a   Safe, Stephen ^b,c   Rhoades, Raina E ^a   Clark, Ryan ^a   Jules, George ^a   McCallister, Monique ^a   Aschner, Michael ^d   Hood, Darryl B ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

B(a)P metabolites; Benzo(a)pyrene; Neurogenesis; Neuronal activity; NMDA receptor; Object discrimination task; Polycyclic aromatic hydrocarbon; Susceptibility exposure paradigm; Synaptogenesis

Indexed keywords

BENZO[A]PYRENE; CYP1B1 ASSOCIATED NADPH OXIDOREDUCTASE; CYTOCHROME P450 1B1; CYTOCHROME P450 REDUCTASE; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; OXIDOREDUCTASE; POLYCYCLIC AROMATIC HYDROCARBON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TRANSCRIPTION FACTOR SP4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NEUROPROTECTION; NEUROTOXICOLOGY; NONHUMAN; PERCEPTIVE DISCRIMINATION; PHENOTYPE; PRENATAL EXPOSURE; PROGENY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTOGENESIS; TARGET DISCRIMINATION; TASK PERFORMANCE;

MUS;

EID: 84555195336     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr261     Document Type: Article

References (60)

1. 450 oxidoreductase and human androgen synthesis: Analytical study. Lancet 363, 2128-2135.
2. Brigman, J., Feyder, M., Saksida, L., Bussey, T. J., Mishina, M., and Holmes, A. (2008). Impaired discrimination learning in mice lacking the NMDA receptor NR2A subunit. Learn. Mem. 15, 50-54.
3. Brown, L., Khoshbouei, H., Goodwin, J., Irvin-Wilson, C., Ramesh, A., Sheng, L., McCallister, M., Jiang, G., Aschner, M., and Hood, D. (2007). Down-regulation of early ionotrophic glutamate receptor subunit developmental expression as a mechanism for observed plasticity deficits following gestational exposure to benzo(a)pyrene. Neurotoxicology 28, 965-978.
4. Chefer, V., Meis, J., Wang, G., Kuzmin, A., Bakalkin, G., and Shippenberg, T. (2011). Repeated exposure tomoderate doses of ethanol augments hippocampal glutamate neurotransmission by increasing release. Addict. Biol. 16, 229-237.
5. Conroy, J. L., Fang, C., Gu, J., Zeitlin, S. O., Yang, W., Yang, J., VanAlstine, M. A., Nalwalk, J. W., Albrecht, P. J., Mazurkiewicz, J. E., et al. (2010). Opioids activate brain analgesic circuits through cytochrome P450/epoxygenase signaling. Nature Neurosci. 13, 284-286.
6. Cull-Candy, S., Brickley, S., and Farrant, M. (2001). NMDA receptor subunits: Diversity, development and disease. Curr. Opin. Neurobiol. 11, 327-335.
7. Cull-Candy, S., and Leszkiewicz, D. (2004). Role of distinct NMDA receptor subtypes at central synapses. Sci. STKE 2004, 16.
8. Dere, E., Huston, J. P., and De Souza Silva, M. A. (2007). The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci. Biobehav. Rev. 31, 673-704.
9. Devito, L. M., and Eichenbaum, H. (2011). Memory for the order of events in specific sequences: Contributions of the hippocampus and medial prefrontal cortex. J. Neurosci. 31, 3169-3175.
10. Ennaceur, A., and Delacour, J. (1988). A new one-trial test for neurobiological studies of memory in rats. 1, Behavioral data. Behav. Brain Res. 31, 47-59.
11. Feldman, D., and Knudsen, E. (1998). Pharmacological specialization of learned auditory responses in the inferior colliculus of the barn owl. J. Neurosci. 18, 3073-3087.
12. Floresco, S. B., and Phillips, A. G. (2001). Delay-dependent modulation of memory retrieval by infusion of a dopamine D1 agonist into the rat medial prefrontal cortex. Behav. Neurosci. 115, 934-939.
13. 450 oxidoreductase causes disordered steroidogenesis with and without Antley-Bixler syndrome. Nat. Genet. 36, 228-230.
14. Forwood, S. E., Winters, B. D., and Bussey, T. J. (2005). Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 h. Hippocampus 15, 347-355.
15. 450 oxidoreductase deficiency in three patients initially regarded as having 21-hydroxylase deficiency and/or aromatase deficiency: Diagnostic value of urine steroid hormone analysis. Pediatr. Res. 59, 276-280.
16. 450 oxidoreductase gene mutations and Antley-Bixler syndrome with abnormal genitalia and/or impaired steroidogenesis: Molecular and clinical studies in 10 patients. J. Clin. Endocrinol. Metab. 90, 414-426.
17. Fuster, J. M. (2001). The prefrontal cortex-an update, time is of the essence. Neuron 30, 319-333.
18. Grova, N., Valley, A., Turner, J., Morel, A., Muller, C., and Schroeder, H. (2007). Modulation of behavior and NMDA-R1 gene mRNA expression in adult female mice after sub-acute administration of benzo(a)pyrene. Neurotoxicology 28, 630-636.
19. 450 reductase gene: Characterization and utility for in vivo studies of cyclophosphamide disposition. J. Pharmacol. Exp. Ther. 321, 9-17.
20. Hlinak, Z., and Krejci, I. (1995). Kynurenic acid and 5,7-dichlorokynurenic acids improve social and object recognition in male rats. Psychopharmacology(Berlin) 120, 463-469.
21. Hood, D., Nayyar, T., Ramesh, A., Greenwood, M., and Inyang, F. (2000). Modulation in the developmental expression profile of Sp1 subsequent to transplacental exposure of fetal rats to desorbed benzo[a]pyrene following maternal inhalation. Inhal. Toxicol. 12, 511-535.
22. Hood, D., Woods, L., Brown, L., Johnson, S., and Ebner, F. (2006). Gestational 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure effects on sensory cortex function. Neurotoxicology 27, 1032-1042.
23. 450 oxidoreductase in patients with Antley-Bixler syndrome and disordered steroidogenesis. Am. J. Hum. Genet. 76, 729-749.
24. Iwama, H., and Gojobori, T. (2002). Identification of neurotransmitter receptor genes under significantly relaxed selective constraint by orthologous gene comparisons between humans and rodents. Mol. Biol. Evol. 19, 1891-1901.
25. Kemppainen, N., Laine, M., Laakso, M. P., Kaasinen, V., Någren, K., Vahlberg, T., Kurki, T., and Rinne, J. O. (2003). Hippocampal dopamine D2 receptors correlate with memory functions in Alzheimer's disease. Eur. J. Neurosci. 18, 149-154.
26. Kerzee, K., and Ramos, K. (2000). Activation of c-Ha-ras by benzo(a)pyrene in vascular smooth muscle cells involves redox stress and aryl hydrocarbon receptor. Mol. Pharmacol. 58, 152-158.
27. Kesner, R. P., and Holbrook, T. (1987). Dissociation of item and order spatial memory in rats following medial prefrontal cortex lesions. Neuropsychologia 25, 653-664.
28. Kesner, R. P., Hopkins, R. O., and Fineman, B. (1994). Item and order dissociation in humans with prefrontal cortex damage. Neuropsychologia 32, 881-891.
29. Kiruthiga, P., Shafreen, R., Pandian, S., Arun, S., Govindu, S., and Devi, K. (2007). Protective effect of silymarin on erythrocyte haemolysate against benzo(a)pyrene and exogenous reactive oxygen species (H2O2) induced oxidative stress. Chemosphere 68, 1511-1518.
30. Köhr, G. (2006). NMDA receptor function: Subunit composition versus spatial distribution. Cell Tissue Res. 326, 439-446.
31. Laube, B., Kuhse, J., and Betz, H. (1998). Evidence for a tetrameric structure of recombinant NMDA receptors. J. Neurosci. 18, 2954-2961.
32. Lenaers, E., De Feyter, H. M., Hoeks, J., Schrauwen, P., Schaart, G., Nabben, M., Nicolay, K., Prompers, J. J., and Hesselink, M. K. (2010). Adaptations in mitochondrial function parallel, but fail to rescue, the transition to severe hyperglycemia and hyperinsulinemia: A study in Zucker diabetic fatty rats. Obesity (Silver Spring) 18, 1100-1107.
33. Li, G., and Pleasure, S. (2005). Morphogenesis of the dentate gyrus: What we are learning from mouse mutants. Dev. Neurosci. 27, 93-99.
34. Liu, A., Zhuang, Z., Hoffman, P. W., and Bai, G. (2003). Functional analysis of the rat N-methyl-D-aspartate receptor 2A promoter: Multiple transcription start points, positive regulation by Sp factors, and translational regulation. J. Biol. Chem. 278, 26423-26434.
35. Liu, X.-B., Murray, K. D., and Jones, E. (2004). Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J. Neurosci. 24, 8885-8895.
36. McAndrews, M. P., and Milner, B. (1991). The frontal cortex and memory for temporal order. Neuropsychologia 29, 849-859.
37. McCallister, M., Maguire, M., Ramesh, A., Aimin, Q., Liu, S., Khoshbouei, H., Aschner, M., Ebner, F., and Hood, D. (2008). Prenatal exposure to benzo(a)pyrene impairs later-life cortical neuronal function. Neurotoxicology 29, 846-854.
38. Milatovic, D., and Aschner, M. (2009). Measurement of isoprostances as markers of oxidative stress in neuronal tissue. Curr. Protoc. Toxicol. (Suppl. 39), 12.14.1-12.14.12.
39. Mitchell, J. B., and Laiacona, J. (1998). The medial frontal cortex and temporal memory, tests using spontaneous exploratory behaviour in the rat. Behav. Brain Res. 97, 107-113.
40. Perera, F. P., Wang, S., Vishnevetsky, J., Zhang, B., Cole, K. J., Tang, D., Rauh, V., and Phillips, D. (2011). PAH/aromatic DNA adducts in cord blood and behavior scores in New York City children. Environ. Health Perspect. 118, 1176-1181.
41. Philpot, B., Weisberg, M., Ramos, M., Sawtell, N., Tang, Y., Tsien, J., and Bear, M. (2001). Effect of transgenic overexpression of NR2B on NMDA receptor function and synaptic plasticity in visual cortex. Neuropharmacology 41, 762-770.
42. Potter, M. C., Elmer, G. I., Bergeron, R., Albuquerque, E. X., Guidetti, P., Wu, H. Q., and Schwarcz, R. (2010). Reduction of endogenous kynurenic acid formation enhances extracellular glutamate, hippocampal plasticity, and cognitive behavior. Neuropsychopharmacology 35, 1734-1742.
43. Puma, C., and Bizot, J. C. (1998). Intraseptal infusions of a low dose of AP5, a NMDA receptor antagonist, improves memory in an object recognition task in rats. Neurosci. Lett. 248, 183-186.
44. Qiu, C., Cheng, S., Xia, Y., Peng, B., Tang, Q., and Tu, B. (2011). Effects of subchronic benzo(a)pyrene exposure on neurotransmitter receptor gene expression in the rats hippocampus related with spatial learning and memory change. Toxicology 289, 83-90.
45. Ramesh, A., Inyang, F., Hood, D., Archibong, A., Knuckles, M., and Nyanda, A. M. (2001). Metabolism, bioavailability, and toxicokinetics of benzo(alpha)pyrene in F-344 rats following oral administration. Exp. Toxicol. Pathol. 53, 275-290.
46. Ramos, B., Gaudillière, B., Bonni, A., and Gill, G. (2007). Transcription factor Sp4 regulates dendritic patterning during cerebellar maturation. Proc. Natl. Acad. Sci. U.S.A. 104, 9882-9887.
47. Riedel, G., Platt, B., and Micheau, J. (2003). Glutamate receptor function in learning and 570 memory. Behav. Brain Res. 140, 1-47.
48. Rodier, P. A. (1976). Critical periods for behavioral anomalies in mice. Environ. Health Perspect. 18, 79-83.
49. Sargolini, F., Roullet, P., Oliverio, A., and Mele, A. (2003). Effects of intraaccumbens focal administrations of glutamate antagonists on object recognition memory in mice. Behav. Brain Res. 138, 153-163.
50. Seamans, J. K., Floresco, S. B., and Phillips, A. G., (1998). D1 receptor modulation of 582 hippocampalprefrontal cortical circuits integrating spatial memory with executive functions in the rat. J. Neurosci. 18, 1613-1621.
51. Sheng, L., Ding, X., Ferguson, M., McCallister, M., Rhoades, R., Maguire, M., Ramesh, A., Aschner, M., Campbell, D., Levitt, P., et al. (2010). Prenatal polycyclic aromatic hydrocarbon exposure leads to behavioral deficits and downregulation of receptor tyrosine kinase, MET. Toxicol. Sci. 118, 625-634.
52. Silvers, J., Harrod, S., Mactutus, C., and Booze, R. (2007). Automation of the novel object recognition task for use in adolescent rodents. J. Neurosci. Methods 166, 99-103.
53. Wang, S., Chanock, S., Tang, D., Li, Z., Edwards, S., Jedrychowski, W., and Perera, F. P. (2010). Effect of gene-environment interactions on mental development in African American, Dominican, and Caucasian mothers and newborns. Ann. Hum. Genet. 74, 46-56.
54. Winters, B. D., and Bussey, T. J. (2005). Glutamate receptors in perirhinal cortex mediate encoding, retrieval, and consolidation of object recognition memory. J. Neurosci. 25, 4243-4251.
55. Winters, B. D., Forwood, S. E., Cowell, R. A., Saksida, L. M., and Bussey, T. J. (2004). Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory, heterogeneity of functionwithin the temporal lobe. J. Neurosci. 24, 5901-5908.
56. Wormley, D., Chirwa, S., Nayyar, T., Wu, J., Johnson, S., Brown, L., Harris, E., and Hood, D. (2004a). Inhaled benzo(a)pyrene impairs long-term potentiation in the F1 generation rat dentate gyrus. Cell Mol. Biol. (Noisy-legrand) 50, 715-721.
57. Wormley, D., Ramesh, A., and Hood, D. (2004b). Environmental contaminantmixture effects on CNS development, plasticity, and behavior. Toxicol. Appl. Pharmacol. 197, 49-65.
58. 450 oxidoreductase genes determines interindividual variability in basal expression and activity of a broad scope of xenobiotic metabolism genes in the human liver. Drug Metab. Dispos. 35, 1700-1710.
59. Wu, J., Ramesh, A., Nayyar, T., and Hood, D. (2003). Assessment of metabolites and AhR and CYP1A1 mRNA expression subsequent to prenatal exposure to inhaled benzo(a)pyrene. Int. J. Dev. Neurosci. 21, 333-346.
60. Zhou, X., Qyang, Y., Kelsoe, J., Masliah, E., and Geyer, M. (2007). Impaired postnatal development of hippocampal dentate gyrus in Sp4 null mutant mice. Genes Brain Behav. 6, 269-276.