Prenatal polycyclic aromatic hydrocarbon exposure leads to behavioral deficits and downregulation of receptor tyrosine kinase, MET

Toxicological Sciences

Volumn 118, Issue 2, 2010, Pages 716-731

  Sheng, Liu ^a   Ding, Xinxin ^b   Ferguson, Marcus ^a   Mccallister, Monique ^a   Rhoades, Raina ^a   Maguire, Mark ^a   Ramesh, Aramandla ^a   Aschner, Michael ^c   Campbell, Daniel ^d   Levitt, Pat ^d   Hood, Darryl B ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

^b WADSWORTH CENTER   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Autism spectrum disorders; Behavioral neurotoxicity; Benzo(a)pyrene; Gene environment interaction; In utero exposures; Novel object discrimination behavioral task; Polycyclic aromatic hydrocarbon; Susceptibility exposure paradigm

Indexed keywords

BENZO[A]PYRENE; POLYCYCLIC AROMATIC HYDROCARBON; PROTEIN TYROSINE KINASE; SCATTER FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTISM; BEHAVIOR DISORDER; COGNITIVE DEVELOPMENT; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE INTERACTION; GENETIC RISK; GENETIC SUSCEPTIBILITY; MOUSE; NEUROTOXICITY; NONHUMAN; PRENATAL EXPOSURE; SYNAPSE;

EID: 78549265510     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq303     Document Type: Article

References (48)

1. Akita, H., Takagi, N., Ishihara, N., Takagi, K., Murotomi, K., Funakoshi, H., Matsumoto, K., Nakamura, T., and Takeo, S. (2008). Hepatocyte growth factor improves synaptic localization of the NMDA receptor and intracellular signaling after excitotoxic injury in cultured hippocampal neurons. Exp. Neurol. 210, 83-94.
2. Arlt, W., Walker, E. A., Draper, N., Ivison, H., Ride, J., Hammer, F., Chalder, S., Borucka-Mankiewicz, M., Hauffa, B., Malunowicz, E., et al. (2004). Congenital adrenal hyperplasia caused by mutant P450 oxidoreductase and human androgen synthesis: analytical study. Lancet 363, 2128-2135.
3. Bill, B., and Geschwind, D. (2009). Genetic advances in autism: heterogeneity and convergence on shared pathways. Curr. Opin. Genet. Dev. 19, 271-278.
4. Bolton, J., Trush, M., Penning, T., Dryhurst, G., and Monks, T. (2000). Role of quinones in toxicology. Chem. Res. Toxicol. 13, 135-160.
5. Brown, L., Khousbouei, 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.
6. Campbell, D., Buie, T., Winter, H., Bauman, M., Sutcliffe, J., Perrin, J., and Levitt, P. (2009). Distinct genetic risk based on association of MET in families with co-occurring autism and gastrointestinal conditions. Pediatrics 123, 1018-1024.
7. Campbell, D., D'Oronzio, R., Garbett, K., Ebert, P., Mirnics, K., Levitt, P., and Persico, A. (2007). Disruption of cerebral cortex MET signaling in autism spectrum disorder. Ann. Neurol. 62, 243-250.
8. Campbell, D., Li, C., Sutcliffe, J., Persico, A., and Levitt, P. (2008). Genetic evidence implicating multiple genes in the MET receptor tyrosine kinase pathway in autism spectrum disorder. Autism Res. 1, 159-168.
9. Campbell, D., Sutcliffe, J., Ebert, P., Militerni, R., Bravaccio, C., Trillo, S., Elia, M., Schneider, C., Melmed, R., Sacco, R., et al. (2006). A genetic variant that disrupts MET transcription is associated with autism. Proc. Natl. Acad. Sci. U.S.A 103, 16834-16839.
10. Campbell, D., Warren, D., Sutcliffe, J., Lee, E., and Levitt, P. (2010). Association of MET with social and communication phenotypes in individuals with autism spectrum disorder. Am. J. Med. Genet. B Neuropsychiatr. Genet. 153B, 438-446.
11. Conroy, J., Fang, C., Gu, J., Zeitlin, S., Yang, W., Yang, J., VanAlstine, M., Nalwalk, J., Albrecht, P., Mazurkiewicz, J., et al. (2010). Opioids activate brain analgesic circuits through cytochrome P450/epoxygenase signaling. Nat. Neurosci. 13, 284-286.
12. Fluck, C., Tajima, T., Pandey, A., Arlt, W., Okuhara, K., Verge, C., Jabs, E., Mendonca, B., Fujieda, K., and Miller, W. (2004). Mutant P450 oxidoreductase causes disordered steroidogenesis with and without Antley-Bixler syndrome. Nat. Genet. 36, 228-230.
13. Fukami, M., Hasegawa, T., Horikawa, R., Ohashi, T., Nishimura, G., Homma, K., and Ogata, T. (2006). Cytochrome P450 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.
14. Fukami, M., Horikawa, R., Nagai, T., Tanaka, T., Naiki, Y., Sato, N., Okuyama, T., Nakai, H., Soneda, S., Tachibana, K., et al. (2005). Cytochrome P450 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.
15. Geschwind, D. (2009). Advances in autism. Annu. Rev. Med. 60, 367-380.
16. Geschwind, D., and Levitt, P. (2007). Autism spectrum disorders: developmental disconnection syndromes. Curr. Opin. Neurobiol. 17, 103-111.
17. Gu, J., Chen, C., Wei, Y., Fang, C., Xie, F., Kannan, K., Yang, W., Waxman, D., and Ding, X. (2007). A mouse model with liver-specific deletion and global suppression of the NADPH-cytochrome P450 reductase gene: characterization and utility for in vivo studies of cyclophosphamide disposition. J. Pharmacol. Exp. Ther. 321, 9-17.
18. Gu, J., Weng, Y., Zhang, Q., Cui, H., Behr, M., Wu, L., Yang, W., Zhang, L., and Ding, X. (2003). Liver-specific deletion of the NADPH-cytochrome P450 reductase gene: impact on plasma cholesterol homeostasis and the function and regulation of microsomal cytochrome P450 and heme oxygenase. J. Biol. Chem. 278, 25895-25901.
19. Gutierrez, H., Dolcet, X., Tolcos, M., and Davies, A. (2004). HGF regulates the development of cortical pyramidal dendrites. Development 131, 3717-3726.
20. 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.
21. Hood, D. B., Woods, L., Brown, L. A., and Ebner, F. F. (2006). Gestational 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin exposure effects on sensory cortex function. Neurotoxicology 27, 1032-1042.
22. Huang, N., Pandey, A., Agrawal, V., Reardon, W., Lapunzina, P., Mowat, D., Jabs, E., Van Vliet, G., Sack, J., Fluck, C., et al. (2005). Diversity and function of mutations in p450 oxidoreductase in patients with Antley-Bixler syndrome and disordered steroidogenesis. Am. J. Hum. Genet. 76, 729-749.
23. Jackson, P., Boccuto, L., Skinner, C., Collins, J., Neri, G., Gurrieri, F., and Schwartz, C. (2009). Further evidence that the rs1858830 C variant in the promoter region of the MET gene is associated with autistic disorder. Autism Res. 2, 232-236.
24. Judson, M., Bergman, M., Campbell, D., Eagleson, K., and Levitt, P. (2009). Dynamic gene and protein expression patterns of the autism-associated met receptor tyrosine kinase in the developing mouse forebrain. J. Comp. Neurol. 513, 511-531.
25. Kerzee, J., 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.
26. Levitt, P. (2003). Structural and functional maturation of the developing primate brain. J. Pediatr. 143, S35-S45.
27. Levitt, P., and Campbell, D. (2009). The genetic and neurobiologic compass points toward common signaling dysfunctions in autism spectrum disorders. J. Clin. Invest. 119, 747-754.
28. Li, Z., Dong, T., Pröschel, C., and Noble, M. (2007). Chemically diverse toxicants converge on Fyn and c-Cbl to disrupt precursor cell function. PLoS Biol. 5, e35.
29. Lioy, P. L., Waldman, J. M., Greenberg, A., Harkov, R., and Pietarinen, C. (1988). The Total Human Environmental Exposure Study (THEES) to benzo(a)pyrene: comparison of the inhalation and food pathways. Arch. Environ. Health 43, 304-312.
30. Liu, A., Zhuang, Z., Hoffman, P., and Bai, G. (2003). Functional analysis of the rat N-methyl-D-aspartate receptor 2A promoter: multiple transcription starts points, positive regulation by Sp factors, and translational regulation. J. Biol. Chem. 278, 26423-26434.
31. 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.
32. Morrow, E., Yoo, S., Flavell, S., Kim, T., Lin, Y., Hill, R., Mukaddes, N., Balkhy, S., Gascon, G., Hashmi, A., et al. (2008). Identifying autism loci and genes by tracing recent shared ancestry. Science 321, 218-223.
33. Nakano, M., Takagi, N., Takagi, K., Funakoshi, H., Matsumoto, K., Nakamura, T., and Takeo, S. (2007). Hepatocyte growth factor promotes the number of PSD-95 clusters in young hippocampal neurons. Exp. Neurol. 207, 195-202.
34. Nebert, D., Roe, A.,Dieter, M., Solis,W.,Yang,Y., andDalton, T. (2000). Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 59, 65-85.
35. Palmen, S., van Engeland, H., Hof, P., and Schmitz, C. (2004). Neuropathological finding in autism. Brain 127, 2572-2583.
36. Perera, F., Li, Z., Whyatt, R., Hoepner, L., Wang, S., Camann, D., and Rauh, V. (2009). Prenatal airborne polycyclic aromatic hydrocarbon exposure and child IQ at age 5 years. Pediatrics 124, e195-e202.
37. Perera, F., Rauh, V., Whyatt, R., Tsai, W., Tang, D., Diaz, D., Hoepner, L., Barr, D., Tu, Y., Camann, D., et al. (2006). Effect of prenatal exposure to airborne polycyclic aromatic hydrocarbons on neurodevelopment in the first 3 years of life among inner-city children. Environ. Health Perspect. 114, 1287-1292.
38. Powell, E., Campbell, D., Stanwood, G., Davis, C., Noebels, J., and Levitt, P. (2003). Genetic disruption of cortical interneuron development causes region- and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J. Neurosci. 23, 622-631.
39. Powell, E., Mars, W., and Levitt, P. (2001). Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 30, 79-89.
40. Ramesh, A., Inyang, F., Hood, D., Archibong, A., Knuckles, M., and Nyanda, A. (2001). Metabolism, bioavailability, and toxicokinetics of benzo(alpha)pyrene in F-344 rats following oral administration. Exp. Toxicol. Pathol. 53, 275-290.
41. Silvers, J., Harrod, S., Mactutu, C., and Booze, R. (2007). Automation of the novel object recognition task for use in adolescent rodents. J. Neurosci. Methods 166, 99-103.
42. Sousa, I., Clark, T., Toma, C., Kobayashi, K., Choma, M., Holt, R., Sykes, N., Lamb, J., Bailey, A., Battaglia, A., et al. (2009).MET and autism susceptibility: family and case-control studies. Eur. J. Hum. Genet. 17, 749-758.
43. Tyndall, S., and Walikonis, R. (2006). The receptor tyrosine kinase Met and its ligand hepatocyte growth factor are clustered at excitatory synapses and can enhance clustering of synaptic proteins. Cell Cycle 5, 1560-1568.
44. Wang, S., Chanock, S., Tang, D., Li, Z., Edwards, S., Jedrychowski, W., and Perera, F. (2010). Effect of gene-environment Interactions on mental development in African American, Dominican, and Caucasian mothers and newborns. Ann. Hum. Genet. 74, 46-56.
45. Wormley, D., Ramesh, A., and Hood, D. (2004). Environmental contaminantmixture effects on CNS development, plasticity, and behavior. Toxicol. Appl. Pharmacol. 197, 49-65.
46. Wortham, M., Czerwinski, M., He, L., Parkinson, A., and Wan, Y. (2007). Expression of constitutive androstane receptor, hepatic nuclear factor 4 alpha, and P450 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.
47. Wu, L., Gu, J., Weng, Y., Kluetzman, K., Swiatek, P., Behr, M., Zhang, Q., Zhuo, X., Xie, Q., and Ding, X. (2003). Conditional knockout of the mouse NADPH-cytochrome P450 reductase gene. Genesis 36, 177-181.
48. Wu, R., Zhao, J., Zhai, J., Guo, X., and Guo, W. (2007). Sex difference in effects of typical and atypical antipsychotics on glucose-insulin homeostasis and lipid metabolism in first-episode schizophrenia. J. Clin. Psychopharmacol. 27, 374-379.