mRNA expression is a relevant tool to identify developmental neurotoxicants using an in vitro approach

Toxicological Sciences

Volumn 113, Issue 1, 2009, Pages 95-115

  Hogberg, Helena T ^a,b   Kinsner Ovaskainen, Agnieszka ^a   Coecke, Sandra ^a   Hartung, Thomas ^c   Bal Price, Anna K ^a  

^a JOINT RESEARCH CENTRE   (Italy)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Developmental neurotoxicity; Gene expression; Primary cell culture

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; INDUSTRIAL CHEMICAL; LEAD CHLORIDE; MESSENGER RNA; METHYLMERCURIC CHLORIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NESTIN; NEUROTOXIN; PROTEIN S100B; TIN CHLORIDE; VALPROIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL MATURATION; CELL TYPE; CEREBELLUM; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GLIA CELL; GRANULE CELL; IN VITRO STUDY; NERVE CELL; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROTOXICITY; NONHUMAN; RAT; SCREENING; SENSITIVITY AND SPECIFICITY; TOXICITY TESTING;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; GENE EXPRESSION REGULATION; GENETIC MARKERS; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; INTERMEDIATE FILAMENT PROTEINS; LEAD; METHYLMERCURY COMPOUNDS; NERVE TISSUE PROTEINS; NEUROFILAMENT PROTEINS; NEUROGLIA; NEURONS; NEUROTOXICITY SYNDROMES; RATS; RATS, WISTAR; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; RISK ASSESSMENT; RISK FACTORS; RNA, MESSENGER; SOXE TRANSCRIPTION FACTORS; TIME FACTORS; TOXICITY TESTS; TRIMETHYLTIN COMPOUNDS; VALPROIC ACID;

RATTUS;

EID: 75249106472     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp175     Document Type: Article

References (126)

1. Altman, J. (1987). Morphological and behavioral markers of environmentally induced retardation of brain development: an animal model. Environ. Health Perspect. 74, 153-168.
2. Altman, J., and Bayer, S.A. (1978). Prenatal development of the cerebellar system in the rat. I. Cytogenesis and histogenesis of the deep nuclei and the cortex of the cerebellum. J. Comp. Neurol. 179, 23-48.
3. Amin-Zaki, L., Elhassani, S., Majeed, M.A., Clarkson, T.W., Doherty, R.A., Greenwood, M.R., and Giovanoli-Jakubczak, T. (1976). Perinatal methylmercury poisoning in Iraq. Am. J. Dis. Child 130, 1070-1076.
4. Amin-Zaki, L., Majeed, M.A., Greenwood, M.R., Elhassani, S.B., Clarkson, T.W., and Doherty, R.A. (1981). Methylmercury poisoning in the Iraqi suckling infant: a longitudinal study over five years. J. Appl. Toxicol. 1, 210-214.
5. Atchison, W.D., and Hare, M.F. (1994). Mechanisms of methylmercuryinduced neurotoxicity. FASEB J. 8, 622-629.
6. Bal-Price, A., and Brown, G.C. (2001). Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J. Neurosci. 21, 6480-6491.
7. Bal-Price, A.K., Hogberg, H.T., Buzanska, L., and Coecke, S. (2008). Relevance of in vitro neurotoxicity testing for regulatory requirements: challenges to be considered. Neurotoxicol. Teratol. doi:10/1016/j.ntt.2008.12.003.
8. Bellinger, D.C. (2008). Very low lead exposures and children's neurodevelopment. Curr. Opin. Pediatr. 20, 172-177.
9. Benke, D., Mertens, S., Trzeciak, A., Gillessen, D., and Mohler, H. (1991). Identification and immunohistochemical mapping of GABAA receptor subtypes containing the delta-subunit in rat brain. FEBS Lett. 283, 145-149.
10. Bernard, S., Enayati, A., Redwood, L., Roger, H., and Binstock, T. (2001). Autism: A novel form of mercury poisoning. Med. Hypotheses 56, 462-471.
11. Boyle, C.A., Decoufle, P., and Yeargin-Allsopp, M. (1994). Prevalence and health impact of developmental disabilities in US children. Pediatrics 93, 399-403.
12. Braman, R.S., and Tompkins, M.A. (1979). Separation and determination of nanogram amounts of inorganic tin and methyltin compounds in the environment. Anal. Chem. 51, 12-19.
13. Brook, G.A., Perez-Bouza, A., Noth, J., and Nacimiento, W. (1999). Astrocytes re-express nestin in deafferented target territories of the adult rat hippocampus. Neuroreport 10, 1007-1011.
14. Carden, M.J., Trojanowski, J.Q., Schlaepfer, W.W., and Lee, V.M. (1987). Two-stage expression of neurofilament polypeptides during rat neurogenesis with early establishment of adult phosphorylation patterns. J. Neurosci. 7, 3489-3504.
15. Centers for Disease Control. (1991). Preventing Lead Poisoning in Young Children. Centers for Disease Control, Atlanta, GA.
16. Chen, L.W., Wei, L.C., Qiu, Y., Liu, H.L., Rao, Z.R., Ju, G., and Chan, Y.S. (2002). Significant up-regulation of nestin protein in the neostriatum of MPTP-treated mice. Are the striatal astrocytes regionally activated after systemic MPTP administration? Brain Res. 925, 9-17.
17. Cheng, Y., Cheung, M., Abu-Elmagd, M.M., Orme, A., and Scotting, P.J. (2000). Chick sox10, a transcription factor expressed in both early neural crest cells and central nervous system. Brain Res. Dev. Brain Res. 121, 233-241.
18. Chiodo, L.M., Covington, C., Sokol, R.J., Hannigan, J.H., Jannise, J., Ager, J., Greenwald, M., and Delaney-Black, V. (2007). Blood lead levels and specific attention effects in young children. Neurotoxicol. Teratol. 29, 538-546.
19. Christianson, A.L., Chesler, N., and Kromberg, J.G. (1994). Fetal valproate syndrome: Clinical and neuro-developmental features in two sibling pairs. Dev. Med. Child Neurol. 36, 361-369.
20. Clarke, S.R., Shetty, A.K., Bradley, J.L., and Turner, D.A. (1994). Reactive astrocytes express the embryonic intermediate neurofilament nestin. Neuroreport 5, 1885-1888.
21. Clarkson, T.W. (1997). The toxicology of mercury. Crit. Rev. Clin. Lab. Sci. 34, 369-403.
22. Claudio, L., Kwa, W.C., Russell, A.L., and Wallinga, D. (2000). Testing methods for developmental neurotoxicity of environmental chemicals. Toxicol. Appl. Pharmacol. 164, 1-14.
23. Coecke, S., Goldberg, A.M., Allen, S., Buzanska, L., Calamandrei, G., Crofton, K., Hareng, L., Hartung, T., Knaut, H., Honegger, P., et al. (2007). Workgroup report: incorporating in vitro alternative methods for developmental neurotoxicity into international hazard and risk assessment strategies. Environ. Health Perspect. 115, 924-931.
24. Cory-Slechta, D.A. (1990). Lead exposure during advanced age: alterations in kinetics and biochemical effects. Toxicol. Appl. Pharmacol. 104, 67-78.
25. Cowan, W.M., Jessell, T.M., and Zipursky, S.L. (1997). In Molecular and Cellular Approaches to Neural Development. Oxford University Press, New York, NY.
26. Cunningham, M.O., Woodhall, G.L., and Jones, R.S. (2003). Valproate modifies spontaneous excitation and inhibition at cortical synapses in vitro. Neuropharmacology 45, 907-917.
27. David, O., Clark, J., and Voeller, K. (1972). Lead and hyperactivity. Lancet 2, 900-903.
28. Davis, L.E., Kornfeld, M., Mooney, H.S., Fiedler, K.J., Haaland, K.Y., Orrison, W.W., Cernichiari, E., and Clarkson, T.W. (1994). Methylmercury poisoning: Long-term clinical, radiological, toxicological, and pathological studies of an affected family. Ann. Neurol. 35, 680-688.
29. Dickinson, R.G., Harland, R.C., Lynn, R.K., Smith, W.B., and Gerber, N. (1979). Transmission of valproic acid (Depakene) across the placenta: Halflife of the drug in mother and baby. J. Pediatr. 94, 832-835.
30. Dolbec, J., Mergler, D., Sousa Passos, C.J., Sousad, M., and Lebel, J. (2000). Methylmercury exposure affects motor performance of a riverine population of the Tapajos river, Brazilian Amazon. Int. Arch. Occup. Environ. Health 73, 195-203.
31. El Fawal, H.A., and O'Callaghan, J.P. (2008). Autoantibodies to neurotypic and gliotypic proteins as biomarkers of neurotoxicity: assessment of trimethyltin (TMT). Neurotoxicology 29, 109-115.
32. Eriksson, P. (1997). Developmental neurotoxicity of environmental agents in the neonate. Neurotoxicology 18, 719-726.
33. Eskes, C., Juillerat-Jeanneret, L., Leuba, G., Honegger, P., and Monnet-Tschudi, F. (2003). Involvement of microglia-neuron interactions in the tumor necrosis factor-alpha release, microglial activation, and neurodegeneration induced by trimethyltin. J. Neurosci. Res. 71, 583-590.
34. Eto, K., Takizawa, Y., Akagi, H., Haraguchi, K., Asano, S., Takahata, N., and Tokunaga, H. (1999). Differential diagnosis between organic and inorganic mercury poisoning in human cases-the pathologic point of view. Toxicol. Pathol. 27, 664-671.
35. Feldman, R.G., White, R.F., and Eriator, I.I. (1993). Trimethyltin encephalopathy. Arch. Neurol. 50, 1320-1324.
36. Finkelstein, Y., Markowitz, M.E., and Rosen, J.F. (1998). Low-level lead-induced neurotoxicity in children: an update on central nervous system effects. Brain Res. Brain Res. Rev. 27, 168-176.
37. Foltinova, J., Foltin, V., and Neu, E. (2007). Occurrence of lead in placenta-important information for prenatal and postnatal development of child. Neuro Endocrinol. Lett. 28, 335-340.
38. Goldstein, G.W. (1992). Developmental neurobiology of lead toxicity. In Human Lead Exposure (H. L. Needleman, Ed.), pp. 125-135. CRC Press, Boca Raton.
39. Goritz, C., Mauch, D.H., Nagler, K., and Pfrieger, F.W. (2002). Role of glia-derived cholesterol in synaptogenesis: new revelations in the synapse-glia affair. J. Physiol. Paris 96, 257-263.
40. Grandjean, P., and Landrigan, P.J. (2006). Developmental neurotoxicity of industrial chemicals. Lancet 368, 2167-2178.
41. Grandjean, P., Weihe, P., White, R.F., Debes, F., Araki, S., Yokoyama, K., Murata, K., Sorensen, N., Dahl, R., and Jorgensen, P.J. (1997). Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicol. Teratol. 19, 417-428.
42. Harada, M. (1995). Minamata disease: Methylmercury poisoning in Japan caused by environmental pollution. Crit. Rev. Toxicol. 25, 1-24.
43. Hassett-Sipple, B., Swartout, J., Schoeny, R., Mahaffey, K.R., and Rice, G.E. (1997). Mercury Study Report to Congress Volume V: health Effects of Mercury and Mercury Compounds. United States Environmental Protection Agency, EPA-452/R-97-007.
44. Hatten, M.E., and Liem, R.K. (1981). Astroglial cells provide a template for the positioning of developing cerebellar neurons in vitro. J. Cell Biol. 90, 622-630.
45. Heizmann, C.W., and Cox, J.A. (1998). New perspectives on S100 proteins: a multi-functional Ca(2+)-, Zn(2+)- and Cu(2+)-binding protein family. Biometals 11, 383-397.
46. Hogberg, H.T., Kinsner-Ovaskainen, A., Hartung, T., Coecke, S., and Bal-Price, A.K. (2009). Gene expression as a sensitive endpoint to evaluate cell differentiation and maturation of the developing central nervous system in primary cultures of rat cerebellar granule cells (CGCs) exposed to pesticides. Toxicol. Appl. Pharmacol. 235, 268-286.
47. Hong, H.K., Takahashi, S., Min, B.Y., and Tanabe, S. (2002). Butyltin residues in blue mussels (Mytilus edulis) and arkshells (Scapharca broughtonii) collected from Korean coastal waters. Environ. Pollut. 117, 475-486.
48. Hu, H., Tellez-Rojo, M.M., Bellinger, D., Smith, D., Ettinger, A.S., Lamadrid-Figueroa, H., Schwartz, J., Schnaas, L., Mercado-Garcia, A., and Hernandez-Avila, M. (2006). Fetal lead exposure at each stage of pregnancy as a predictor of infant mental development. Environ. Health Perspect. 114, 1730-1735.
49. Ingels, M., Beauchamp, J., Clark, R.F., and Williams, S.R. (2002). Delayed valproic acid toxicity: A retrospective case series. Ann. Emerg. Med. 39, 616-621.
50. Ip, P., Wong, V., Ho, M., Lee, J., and Wong, W. (2004). Mercury exposure in children with autistic spectrum disorder: case-control study. J. Child Neurol. 19, 431-434.
51. Jenkins, S.M., Ehman, K., and Barone, S., Jr. (2004). Structure-activity comparison of organotin species: Dibutyltin is a developmental neuro-toxicant in vitro and in vivo. Brain Res. Dev. Brain Res. 151, 1-12.
52. Jergil, M., Kultima, K., Gustafson, A.L., Dencker, L., and Stigson, M. (2009). Valproic acid-induced deregulation in vitro of genes associated in vivo with neural tube defects. Toxicol. Sci. 108, 132-148.
53. Jusko, T.A., Henderson, C.R., Lanphear, B.P., Cory-Slechta, D.A., Parsons, P.J., and Canfield, R.L. (2008). Blood lead concentrations < 10 microg/dL and child intelligence at 6 years of age. Environ. Health Perspect. 116, 243-248.
54. Kalman, M., and Ajtai, B.M. (2001). A comparison of intermediate filament markers for presumptive astroglia in the developing rat neocortex: immunostaining against nestin reveals more detail, than GFAP or vimentin. Int. J. Dev. Neurosci. 19, 101-108.
55. Kaur, P., Aschner, M., and Syversen, T. (2006). Glutathione modulation influences methyl mercury induced neurotoxicity in primary cell cultures of neurons and astrocytes. Neurotoxicology 27, 492-500.
56. Kinsner, A., Pilotto, V., Deininger, S., Brown, G.C., Coecke, S., Hartung, T., and Bal-Price, A. (2005). Inflammatory neurodegeneration induced by lipoteichoic acid from Staphylococcus aureus is mediated by glia activation, nitrosative and oxidative stress, and caspase activation. J. Neurochem. 95, 1132-1143.
57. Kjellstrom, T., Kennedy, P., Wallis, S., and Mantell, C. (1986). In Physical and Mental Development of Children with Prenatal Exposure to Mercury from Fish. Stage 1: Preliminary Tests at Age 4. National Swedish Environmental Protection Board, Solna, Sweden.
58. Klotz, U., and Schweizer, C. (1980). Valproic acid in childhood epilepsy: Anticonvulsive efficacy in relation to its plasma levels. Int. J. Clin. Pharmacol. Ther. Toxicol. 18, 461-465.
59. Koch, S., Losche, G., Jager-Roman, E., Jakob, S., Rating, D., Deichl, A., and Helge, H. (1992). Major and minor birth malformations and antiepileptic drugs. Neurology 42, 83-88.
60. Kreyberg, S., Torvik, A., Bjorneboe, A., Wiik-Larsen, W., and Jacobsen, D. (1992). Trimethyltin poisoning: Report of a case with postmortem examination. Clin. Neuropathol. 11, 256-259.
61. Kuhlbrodt, K., Herbarth, B., Sock, E., Hermans-Borgmeyer, I., and Wegner, M. (1998). Sox10, a novel transcriptional modulator in glial cells. J. Neurosci. 18, 237-250.
62. Landrigan, P.J., Whitworth, R.H., Baloh, R.W., Staehling, N.W., Barthel, W.F., and Rosenblum, B.F. (1975). Neuropsychological dysfunction in children with chronic low-level lead absorption. Lancet 1, 708-712.
63. Lanphear, B.P., Hornung, R., Khoury, J., Yolton, K., Baghurst, P., Bellinger, D.C., Canfield, R.L., Dietrich, K.N., Bornschein, R., Greene, T., et al. (2005). Low-level environmental lead exposure and children's intellectual function: an international pooled analysis. Environ. Health Perspect. 113, 894-899.
64. Lauwerys, R., Buchet, J.P., Roels, H., and Hubermont, G. (1978). Placental transfer of lead, mercury, cadmium, and carbon monoxide in women. I. Comparison of the frequency distributions of the biological indices in maternal and umbilical cord blood. Environ. Res. 15, 278-289.
65. Lebel, J., Mergler, D., Branches, F., Lucotte, M., Amorim, M., Larribe, F., and Dolbec, J. (1998). Neurotoxic effects of low-level methylmercury contamination in the Amazonian Basin. Environ. Res. 79, 20-32.
66. Lee, J.A., and Cole, G.J. (2000). Localization of transitin mRNA, a nestin-like intermediate filament family member, in chicken radial glia processes. J. Comp. Neurol. 418, 473-483.
67. Lein, P., Locke, P., and Goldberg, A. (2007). Meeting report: alternatives for developmental neurotoxicity testing. Environ. Health Perspect. 115, 764-768.
68. Lin, R.C., Matesic, D.F., Marvin, M., McKay, R.D., and Brustle, O. (1995). Re-expression of the intermediate filament nestin in reactive astrocytes. Neurobiol. Dis. 2, 79-85.
69. Lindahl, L.S., Bird, L., Legare, M.E., Mikeska, G., Bratton, G.R., and Tiffany-Castiglioni, E. (1999). Differential ability of astroglia and neuronal cells to accumulate lead: dependence on cell type and on degree of differentiation. Toxicol. Sci. 50, 236-243.
70. Liu, J.Y., and Jiang, G.B. (2002). Survey on the presence of butyltin compounds in chinese alcoholic beverages, determined by using headspace solid-phase microextraction coupled with gas chromatography-flame photometric detection. J. Agric. Food Chem. 50, 6683-6687.
71. Liu, M.Y., Hsieh, W.C., and Yang, B.C. (2000). In vitro aberrant gene expression as the indicator of lead-induced neurotoxicity in U-373MG cells. Toxicology 147, 59-64.
72. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
73. Loscher, W., and Vetter, M. (1985). In vivo effects of aminooxyacetic acid and valproic acid on nerve terminal (synaptosomal) GABA levels in discrete brain areas of the rat. Correlation to pharmacological activities. Biochem. Pharmacol. 34, 1747-1756.
74. Lundberg, B., Nergardh, A., and Boreus, L.O. (1982). Plasma concentrations of valproate during maintenance therapy in epileptic children. J. Neurol. 228, 133-141.
75. Luthi, A., Schwyzer, L., Mateos, J.M., Gahwiler, B.H., and McKinney, R.A. (2001). NMDA receptor activation limits the number of synaptic connections during hippocampal development. Nat. Neurosci. 4, 1102-1107.
76. Maier, W.E., Brown, H.W., Tilson, H.A., Luster, M.I., and Harry, G.J. (1995). Trimethyltin increases interleukin (IL)-1 alpha, IL-6 and tumor necrosis factor alpha mRNA levels in rat hippocampus. J. Neuroimmunol. 59, 65-75.
77. Marsh, D.O., Clarkson, T.W., Cox, C., Myers, G.J., Amin-Zaki, L., and Al Tikriti, S. (1987). Fetal methylmercury poisoning. Relationship between concentration in single strands of maternal hair and child effects. Arch. Neurol. 44, 1017-1022.
78. McCann, M.J., O'Callaghan, J.P., Martin, P.M., Bertram, T., and Streit, W.J. (1996). Differential activation of microglia and astrocytes following trimethyl tin-induced neurodegeneration. Neuroscience 72, 273-281.
79. Messam, C.A., Hou, J., and Major, E.O. (2000). Coexpression of nestin in neural and glial cells in the developing human CNS defined by a humanspecific anti-nestin antibody. Exp. Neurol. 161, 585-596.
80. Moller-Madsen, B. (1990). Localization of mercury in CNS of the rat. II. Intraperitoneal injection of methylmercuric chloride (CH3HgCl) and mercuric chloride (HgCl2). Toxicol. Appl. Pharmacol. 103, 303-323.
81. Monnet-Tschudi, F., Zurich, M.G., Pithon, E., van Melle, G., and Honegger, P. (1995). Microglial responsiveness as a sensitive marker for trimethyltin (TMT) neurotoxicity. Brain Res. 690, 8-14.
82. Nau, H., Helge, H., and Luck, W. (1984). Valproic acid in the perinatal period: Decreased maternal serum protein binding results in fetal accumulation and neonatal displacement of the drug and some metabolites. J. Pediatr. 104, 627-634.
83. Needleman, H.L., Gunnoe, C., Leviton, A., Reed, R., Peresie, H., Maher, C., and Barrett, P. (1979). Deficits in psychologic and classroom performance of children with elevated dentine lead levels. N. Engl. J. Med. 300, 689-695.
84. Noland, E.A., Taylor, D.H., and Bull, R.J. (1982). Monomethyl-and trimethyltin compounds induce learning deficiencies in young rats. Neurobehav. Toxicol. Teratol. 4, 539-544.
85. The National Research Control (NRC). (2000). NRC: Toxicological Effects of Methylmercury. National Academy Press, Washington, DC.
86. O'Brien, J., Wilson, I., Orton, T., and Pognan, F. (2000). Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur. J. Biochem. 267, 5421-5426.
87. Organisation for Economic Co-operation and Development (OECD). (2007). Test Guideline 426. OECD Guideline for Testing of Chemicals. Developmental Neurotoxicity Study. Available at: http://masetto.sourceoecd.org/vl=7138526/cl=14/nw=1/rpsv/ij/oecdjournals/1607310x/v1n4/s27/p1. Accessed August 13, 2009.
88. Owens, M.J., and Nemeroff, C.B. (2003). Pharmacology of valproate. Psychopharmacol. Bull. 37(Suppl. 2), 17-24.
89. Pendergrass, J.C., Haley, B.E., Vimy, M.J., Winfield, S.A., and Lorscheider, F.L. (1997). Mercury vapor inhalation inhibits binding of GTP to tubulin in rat brain: similarity to a molecular lesion in Alzheimer diseased brain. Neurotoxicology 18, 315-324.
90. Pevny, L., and Placzek, M. (2005). SOX genes and neural progenitor identity. Curr. Opin. Neurobiol. 15, 7-13.
91. Pevny, L.H., and Lovell-Badge, R. (1997). Sox genes find their feet. Curr. Opin. Genet. Dev. 7, 338-344.
92. Pfrieger, F.W., and Barres, B.A. (1997). Synaptic efficacy enhanced by glial cells in vitro. Science 277, 1684-1687.
93. Privat, A., Drian, M.J., and Mandon, P. (1974). Synaptogenesis in the outgrowth of rat cerebellum in organized culture. J. Comp. Neurol. 153, 291-307.
94. Qiu, Z., Sweeney, D.D., Netzeband, J.G., and Gruol, D.L. (1998). Chronic interleukin-6 alters NMDA receptor-mediated membrane responses and enhances neurotoxicity in developing CNS neurons. J. Neurosci. 18, 10445-10456.
95. Radio, N.M., and Mundy, W.R. (2008). Developmental neurotoxicity testing in vitro: Models for assessing chemical effects on neurite outgrowth. Neurotoxicology 29, 361-376.
96. Rice, D., and Barone, S., Jr. (2000). Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ. Health Perspect. 108(Suppl. 3), 511-533.
97. Robert, E., and Rosa, F. (1983). Valproate and birth defects. Lancet 2, 1142.
98. Roda, E., Coccini, T., Acerbi, D., Castoldi, A., Bernocchi, G., and Manzo, L. (2008). Cerebellum cholinergic muscarinic receptor (subtype-2 and -3) and cytoarchitecture after developmental exposure to methylmercury: an immunohistochemical study in rat. J. Chem. Neuroanat. 35, 285-294.
99. Rodier, P.M. (1994). Vulnerable periods and processes during central nervous system development. Environ. Health Perspect. 102(Suppl. 2), 121-124.
100. Rodier, P.M. (1995). Developing brain as a target of toxicity. Environ. Health Perspect. 103(Suppl. 6), 73-76.
101. Ruppert, P.H., Dean, K.F., and Reiter, L.W. (1983). Developmental and behavioral toxicity following acute postnatal exposure of rat pups to trimethyltin. Neurobehav. Toxicol. Teratol. 5, 421-429.
102. Rutka, J.T., Ivanchuk, S., Mondal, S., Taylor, M., Sakai, K., Dirks, P., Jun, P., Jung, S., Becker, L.E., and Ackerley, C. (1999). Co-expression of nestin and vimentin intermediate filaments in invasive human astrocytoma cells. Int. J. Dev. Neurosci. 17, 503-515.
103. Sadiki, A.I., and Williams, D.T. (1999). A study on organotin levels in Canadian drinking water distributed through PVC pipes. Chemosphere 38, 1541-1548.
104. Sakamoto, M., Kubota, M., Liu, X.J., Murata, K., Nakai, K., and Satoh, H. (2004). Maternal and fetal mercury and n-3 polyunsaturated fatty acids as a risk and benefit of fish consumption to fetus. Environ. Sci. Technol. 38, 3860-3863.
105. Sanes, D.H., Reh, T.A., and Harris, W.A. (2005). In Development of the Nervous System. Academic Press, San Diego, CA.
106. Sass, J.B., Haselow, D.T., and Silbergeld, E.K. (2001). Methylmercury-induced decrement in neuronal migration may involve cytokine-dependent mechanisms: a novel method to assess neuronal movement in vitro. Toxicol. Sci. 63, 74-81.
107. Schionning, J.D., and Moller-Madsen, B. (1992). Autometallographic detection of mercury in rat spinal cord after treatment with organic mercury. Virchows Arch. B Cell. Pathol. Incl. Mol. Pathol. 61, 307-313.
108. Silbergeld, E.K. (1997). Preventing lead poisoning in children. Annu. Rev. Public Health 18, 187-210.
109. Stanton, M.E., Jensen, K.F., and Pickens, C.V. (1991). Neonatal exposure to trimethyltin disrupts spatial delayed alternation learning in preweanling rats. Neurotoxicol. Teratol. 13, 525-530.
110. Stolt, C.C., Rehberg, S., Ader, M., Lommes, P., Riethmacher, D., Schachner, M., Bartsch, U., and Wegner, M. (2002). Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev. 16, 165-170.
111. Sugimoto, T., Nishida, N., Yasuhara, A., Ono, A., Sakane, Y., and Matsumura, T. (1983). Reye-like syndrome associated with valproic acid. Brain Dev. 5, 334-337.
112. Surkan, P.J., Zhang, A., Trachtenberg, F., Daniel, D.B., McKinlay, S., and Bellinger, D.C. (2007). Neuropsychological function in children with blood lead levels <10 microg/dL. Neurotoxicology 28, 1170-1177.
113. Tiffany-Castiglion, E., and Qian, Y. (2001). Astroglia as metal depots: molecular mechanisms for metal accumulation, storage and release. Neurotoxicology 22, 577-592.
114. Tiffany-Castiglioni, E., Sierra, E.M., Wu, J.N., and Rowles, T.K. (1989). Lead toxicity in neuroglia. Neurotoxicology 10, 417-443.
115. Tilson, H.A. (2000). Neurotoxicology risk assessment guidelines: developmental neurotoxicology. Neurotoxicology 21, 189-194.
116. Trasande, L., Landrigan, P.J., and Schechter, C. (2005). Public health and economic consequences of methyl mercury toxicity to the developing brain. Environ. Health Perspect. 113, 590-596.
117. Tringali, G., Aubry, J.M., Moscianese, K., Zamori, C., Vairano, M., Preziosi, P., Navarra, P., and Pozzoli, G. (2004). Valproic acid inhibits corticotropin-releasing factor synthesis and release from the rat hypothalamus in vitro: evidence for the involvement of GABAergic neurotransmission. J. Psychiatry Neurosci. 29, 459-466.
118. Wang, L.C., Baird, D.H., Hatten, M.E., and Mason, C.A. (1994). Astroglial differentiation is required for support of neurite outgrowth. J. Neurosci. 14, 3195-3207.
119. Wei, L.C., Shi, M., Chen, L.W., Cao, R., Zhang, P., and Chan, Y.S. (2002). Nestin-containing cells express glial fibrillary acidic protein in the proliferative regions of central nervous system of postnatal developing and adult mice. Brain Res. Dev. Brain Res. 139, 9-17.
120. Whalen, M.M., Loganathan, B.G., and Kannan, K. (1999). Immunotoxicity of environmentally relevant concentrations of butyltins on human natural killer cells in vitro. Environ. Res. 81, 108-116.
121. World Health Organization. (1990). Environmental Health Criteria 101. Methylmercury. World Health Organization, Geneva.
122. Williams, G., King, J., Cunningham, M., Stephan, M., Kerr, B., and Hersh, J.H. (2001). Fetal valproate syndrome and autism: additional evidence of an association. Dev. Med. Child Neurol. 43, 202-206.
123. Williams, P.G., and Hersh, J.H. (1997). A male with fetal valproate syndrome and autism. Dev. Med. Child Neurol. 39, 632-634.
124. Yang, Q., Hamberger, A., Wang, S., and Haglid, K.G. (1996). Appearance of neuronal S-100 beta during development of the rat brain. Brain Res. Dev. Brain Res. 91, 181-189.
125. Yoo, C.I., Kim, Y., Jeong, K.S., Sim, C.S., Choy, N., Kim, J., Eum, J.B., Nakajima, Y., Endo, Y., and Kim, Y.J. (2007). A case of acute organotin poisoning. J. Occup. Health 49, 305-310.
126. Zurich, M.G., Eskes, C., Honegger, P., Berode, M., and Monnet-Tschudi, F. (2002). Maturation-dependent neurotoxicity of lead acetate in vitro: Implication of glial reactions. J. Neurosci. Res. 70, 108-116.