Gene expression profiles following exposure to a developmental neurotoxicant, Aroclor 1254: Pathway analysis for possible mode(s) of action

Toxicology and Applied Pharmacology

Volumn 231, Issue 2, 2008, Pages 179-196

  Royland, Joyce E ^a   Kodavanti, Prasada Rao S ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Aroclor 1254; Calcium signaling; Genomics; Learning and memory; Mode of action; Nervous system development; Polychlorinated biphenyls

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ARACHIDONATE 15 LIPOXYGENASE; AROCLOR 1254; CADHERIN; FOCAL ADHESION KINASE 1; HEMOGLOBIN BETA CHAIN; POLYCHLORINATED BIPHENYL; PROTEIN DERIVATIVE; RYANODINE RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; DNA MICROARRAY; GENE EXPRESSION; GENE EXPRESSION PROFILING; HIPPOCAMPUS; LEARNING; MEMORY; NERVOUS SYSTEM DEVELOPMENT; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; RAT; UNINDEXED SEQUENCE;

ANIMALS; ANIMALS, NEWBORN; ANTITHYROID AGENTS; AROCLOR 1254; CALCIUM; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBELLUM; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; HOMEOSTASIS; MALE; MATERNAL EXPOSURE; NEUROTOXINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; RATS; RATS, LONG-EVANS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

ANIMALIA; RATTUS;

EID: 49749109890     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2008.04.023     Document Type: Article

References (72)

1. Abeliovich A., Paylor R., Chen C., Kim J.J., Wehner J.M., and Tonegawa S. PKC gamma mutant mice exhibit mild deficits in spatial and contextual learning. Cell 75 (1993) 1263-1271
2. Backus K.H., Arigoni M., Drescher U., Scheurer L., Malherbe P., Mohler H., and Benson J.A. Stoichiometry of a recombinant GABAA receptor deduced from mutation-induced rectification. Neuroreport 5 (1993) 285-288
3. Barnard E.A. The molecular biology of GABAA receptors and their structural determinants. Adv. Biochem. Psychopharmacol. 48 (1995) 1-16
4. Basha M.R., Braddy N.S., Zawia N.H., and Kodavanti P.R. Ontogenetic alterations in prototypical transcription factors in the rat cerebellum and hippocampus following perinatal exposure to a commercial PCB mixture. Neurotoxicology 27 (2006) 118-124
5. Behar T.N., Li Y.X., Tran H.T., Ma W., Dunlap V., Scott C., and Barker J.L. GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms. J. Neurosci. 16 (1996) 1808-1818
6. Behar T.N., Scott C.A., Greene C.L., Wen X., Smith S.V., Maric D., Liu Q.Y., Colton C.A., and Barker J.L. Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J. Neurosci. 19 (1999) 4449-4461
7. Behar T.N., Schaffner A.E., Scott C.A., Greene C.L., and Barker J.L. GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. Cereb. Cortex 10 (2000) 899-909
8. Cooke B.M., and Woolley C.S. Sexually dimorphic synaptic organization of the medial amygdala. J. Neurosci. 25 (2005) 10759-10767
9. Crofton K.M., Kodavanti P.R., Derr-Yellin E.C., Casey A.C., and Kehn L.S. PCBs, thyroid hormones, and ototoxicity in rats: cross-fostering experiments demonstrate the impact of postnatal lactation exposure. Toxicol. Sci. 57 (2000) 131-140
10. Eriksson P. Developmental neurotoxicology in the neonate-effects of pesticides and polychlorinated organic substances. Arch. Toxicol. Suppl. 18 (1996) 81-88
11. Eriksson P., and Fredriksson A. Developmental neurotoxicity of four ortho-substituted poly-chlorinated byphenyls in the neonatal mouse. Environ. Toxicol. Pharmacol. 1 (1996) 155-165
12. Fiszman M.L., Borodinsky L.N., and Neale J.H. GABA induces proliferation of immature cerebellar granule cells grown in vitro. Brain Res. 115 (1999) 1-8
13. Geller A.M., Oshiro W.M., Haykal-Coates N., Kodavanti P.R., and Bushnell P.J. Gender-dependent behavioral and sensory effects of a commercial mixture of polychlorinated biphenyls (Aroclor 1254) in rats. Toxicol. Sci. 59 (2001) 268-277
14. Goldey E.S., Tilson H.A., and Crofton K.M. Implications of the use of neonatal birth weight, growth, viability, and survival data for predicting developmental neurotoxicity: a survey of the literature. Neurotoxicol. Teratol. 17 (1995) 313-332
15. Hagmar L. Polychlorinated biphenyls and thyroid status in humans: a review. Thyroid 13 (2003) 1021-1028
16. Hany J., Lilienthal H., Sarasin A., Roth-Harer A., Fastabend A., Dunemann L., Lichtensteiger W., and Winneke G. Developmental exposure of rats to a reconstituted PCB mixture or aroclor 1254: effects on organ weights, aromatase activity, sex hormone levels, and sweet preference behavior. Toxicol. Appl. Pharmacol. 158 (1999) 231-243
17. Harms K.J., and Dunaevsky A. Dendritic spine plasticity: Looking beyond development. Brain Res. 1184 (2007) 65-71
18. Herold S., and Fago A. Reactions of peroxynitrite with globin proteins and their possible physiological role. Comp. Biochem. Physiol., Part A. Mol. Integr. Physiol. 142 (2005) 124-129
19. Homanics G.E., DeLorey T.M., Firestone L.L., Quinlan J.J., Handforth A., Harrison N.L., Krasowski M.D., Rick C.E., Korpi E.R., Makela R., Brilliant M.H., Hagiwara N., Ferguson C., Snyder K., and Olsen R.W. Mice devoid of gamma-aminobutyrate type A receptor beta3 subunit have epilepsy, cleft palate, and hypersensitive behavior. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 4143-4148
20. Howard A.S., Fitzpatrick R., Pessah I., Kostyniak P., and Lein P.J. Polychlorinated biphenyls induce caspase-dependent cell death in cultured embryonic rat hippocampal but not cortical neurons via activation of the ryanodine receptor. Toxicol. Appl. Pharmacol. 190 (2003) 72-86
21. Inglefield J.R., and Shafer T.J. Perturbation by the PCB mixture aroclor 1254 of GABA(A) receptor-mediated calcium and chloride responses during maturation in vitro of rat neocortical cells. Toxicol. Appl. Pharmacol. 164 (2000) 184-195
22. Jacobson J.L., Janisse J., Banerjee M., Jester J., Jacobson S.W., and Ager J.W. A benchmark dose analysis of prenatal exposure to polychlorinated biphenyls. Environ. Health Perspect. 110 (2002) 393-398
23. Kater S.B., and Mills L.R. Regulation of growth cone behavior by calcium. J. Neurosci. 11 (1991) 891-899
24. Kaya H., Hany J., Fastabend A., Roth-Harer A., Winneke G., and Lilienthal H. Effects of maternal exposure to a reconstituted mixture of polychlorinated biphenyls on sex-dependent behaviors and steroid hormone concentrations in rats: dose-response relationship. Toxicol. Appl. Pharmacol. 178 (2002) 71-81
25. Kodavanti P.R. Intracellular signaling and developmental neurotoxicity. In: Zawia N.H. (Ed). Molecular Neurotoxicology Environmental Agents and Transcription-Transduction Coupling (2004), CRC Press, Boca Raton, FL 151-182
26. Kodavanti P.R. Neurotoxicity of persistant organic pollutants: possible modes(s) of action and further considerations. Dose-Response 3 (2005) 273-305
27. Kodavanti P.R., Kannan N., Yamashita N., Derr-Yellin E.C., Ward T.R., Burgin D.E., Tilson H.A., and Birnbaum L.S. Differential effects of two lots of aroclor 1254: congener-specific analysis and neurochemical end points. Environ. Health Perspect. 109 (2001) 1153-1161
28. Kodavanti P.R., and Tilson H.A. Neurochemical effects of environmental chemicals: in vitro and in vivo correlations on second messenger pathways. Ann. N. Y. Acad. Sci. 919 (2000) 97-105
29. Kodavanti P.R., Ward T.R., Derr-Yellin E.C., Mundy W.R., Casey A.C., Bush B., and Tilson H.A. Congener-specific distribution of polychlorinated biphenyls in brain regions, blood, liver, and fat of adult rats following repeated exposure to Aroclor 1254. Toxicol. Appl. Pharmacol. 153 (1998) 199-210
30. Lauder J.M. The effects of early hypo- and hyperthyroidism on the development of rat cerebellar cortex. III. Kinetics of cell proliferation in the external granular layer. Brain Res. 126 (1977) 31-51
31. Le Be J.V., and Markram H. Spontaneous and evoked synaptic rewiring in the neonatal neocortex. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 13214-13219
32. Lein P.J., Yang D., Bachstetter A.D., Tilson H.A., Harry G.J., Mervis R.F., and Kodavanti P.R. Ontogenetic alterations in molecular and structural correlates of dendritic growth after developmental exposure to polychlorinated biphenyls. Environ. Health Perspect. 115 (2007) 556-563
33. Leuner B., Mendolia-Loffredo S., Kozorovitskiy Y., Samburg D., Gould E., and Shors T.J. Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J. Neurosci. 24 (2004) 7477-7481
34. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001) 402-408
35. Longnecker M.P., Gladen B.C., Patterson Jr. D.G., and Rogan W.J. Polychlorinated biphenyl (PCB) exposure in relation to thyroid hormone levels in neonates. Epidemiology 11 (2000) 249-254
36. Mariussen E., Myhre O., Reistad T., and Fonnum F. The polychlorinated biphenyl mixture aroclor 1254 induces death of rat cerebellar granule cells: the involvement of the N-methyl-d-aspartate receptor and reactive oxygen species. Toxicol. Appl. Pharmacol. 179 (2002) 137-144
37. Mejia-Gervacio S., and Marty A. Control of interneurone firing pattern by axonal autoreceptors in the juvenile rat cerebellum. J. Physiol. 571 (2006) 43-55
38. Morreale de Escobar G., Obregon M.J., and Escobar del Rey F. Role of thyroid hormone during early brain development. Eur. J. Endocrinol. 151 Suppl 3 (2004) U25-U37
39. Morse D.C., Seegal R.F., Borsch K.O., and Brouwer A. Long-term alterations in regional brain serotonin metabolism following maternal polychlorinated biphenyl exposure in the rat. Neurotoxicology 17 (1996) 631-638
40. Morse D.C., Wehler E.K., Wesseling W., Koeman J.H., and Brouwer A. Alterations in rat brain thyroid hormone status following pre- and postnatal exposure to polychlorinated biphenyls (Aroclor 1254). Toxicol. Appl. Pharmacol. 136 (1996) 269-279
41. Padhi B.K., Pelletier G., Williams A., Berndt-Weis L., Yauk C., Bowers W.J., and Chu I. Gene expression profiling in rat cerebellum following in utero and lactational exposure to mixtures of methylmercury, polychlorinated biphenyls and organochlorine pesticides. Toxicol. Lett. 176 (2008) 93-103
42. Patandin S., Dagnelie P.C., Mulder P.G., Op de Coul E., van der Veen J.E., Weisglas-Kuperus N., and Sauer P.J. Dietary exposure to polychlorinated biphenyls and dioxins from infancy until adulthood: a comparison between breast-feeding, toddler, and long-term exposure. Environ. Health Perspect. 107 (1999) 45-51
43. Pessah I.N., Hansen L.G., Albertson T.E., Garner C.E., Ta T.A., Do Z., Kim K.H., and Wong P.W. Structure-activity relationship for noncoplanar polychlorinated biphenyl congeners toward the ryanodine receptor-Ca2+channel complex type 1 (RyR1). Chem. Res. Toxicol. 19 (2006) 92-101
44. Piomelli D., Feinmark S.J., Shapiro E., and Schwartz J.H. 12-keto-eicosatetraenoic acid. A biologically active eicosanoid in the nervous system of Aplysia. Ann. N.Y. Acad. Sci. 559 (1989) 208-218
45. Powers B.E., Widholm J.J., Lasky R.E., and Schantz S.L. Auditory deficits in rats exposed to an environmental PCB mixture during development. Toxicol. Sci. 89 (2006) 415-422
46. Pravettoni A., Colciago A., Negri-Cesi P., Villa S., and Celotti F. Ontogenetic development, sexual differentiation, and effects of Aroclor 1254 exposure on expression of the arylhydrocarbon receptor and of the arylhydrocarbon receptor nuclear translocator in the rat hypothalamus. Reprod. Toxicol. 20 (2005) 521-530
47. Ramadan E., Fu Z., Losi G., Homanics G.E., Neale J.H., and Vicini S. GABA(A) receptor beta3 subunit deletion decreases alpha2/3 subunits and IPSC duration. J. Neurophysiol. 89 (2003) 128-134
48. Rice D.C. Behavioral impairment produced by low-level postnatal PCB exposure in monkeys. Environ. Res. 80 (1999) S113-S121
49. Rice D.C., and Hayward S. Effects of postnatal exposure to a PCB mixture in monkeys on nonspatial discrimination reversal and delayed alternation performance. Neurotoxicology 18 (1997) 479-494
50. Rodier P.M. Developmental neurotoxicology. Toxicol. Pathol. 18 (1990) 89-95
51. Roegge C.S., Wang V.C., Powers B.E., Klintsova A.Y., Villareal S., Greenough W.T., and Schantz S.L. Motor impairment in rats exposed to PCBs and methylmercury during early development. Toxicol. Sci. 77 (2004) 315-324
52. Rogan W.J., and Gladen B.C. Neurotoxicology of PCBs and related compounds. Neurotoxicology 13 (1992) 27-35
53. Royland J.E., Wu J., Zawia N.H., and Kodavanti P.R.S. Gene expression profiles following exposure to a developmental neurotoxicant, Aroclor 1254: developmental effects. Toxicol. Appl. Pharmacol (2008) (companion paper)
54. Safe S.H. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit. Rev. Toxicol. 24 (1994) 87-149
55. Seegal R.F. Epidemiological and laboratory evidence of PCB-induced neurotoxicity. Crit. Rev. Toxicol. 26 (1996) 709-737
56. Seegal R.F., Brosch K.O., and Okoniewski R.J. 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 (1997) 95-103
57. Seo J.A.E.P.H. Probe set algorithms: is there a rational best bet?. BMC Bioinformatics vol. 7 (2006) 395-402
58. Shain W., Bush B., and Seegal R. Neurotoxicity of polychlorinated biphenyls: structure-activity relationship of individual congeners. Toxicol. Appl. Pharmacol. 111 (1991) 33-42
59. Sharma R., and Kodavanti P.R. In vitro effects of polychlorinated biphenyls and hydroxy metabolites on nitric oxide synthases in rat brain. Toxicol. Appl. Pharmacol. 178 (2002) 127-136
60. Sharma R., Derr-Yellin E.C., House D.E., and Kodavanti P.R. Age-dependent effects of Aroclor 1254R on calcium uptake by subcellular organelles in selected brain regions of rats. Toxicology 156 (2000) 13-25
61. Slikker Jr. W., and Bowyer J.F. Biomarkers of adult and developmental neurotoxicity. Toxicol. Appl. Pharmacol. 206 (2005) 255-260
62. Tilson H.A., and Kodavanti P.R. The neurotoxicity of polychlorinated biphenyls. Neurotoxicology 19 (1998) 517-525
63. Vreugdenhil H.J., Mulder P.G., Emmen H.H., and Weisglas-Kuperus N. Effects of perinatal exposure to PCBs on neuropsychological functions in the Rotterdam cohort at 9 years of age. Neuropsychology 18 (2004) 185-193
64. Waters M., Boorman G., Bushel P., Cunningham M., Irwin R., Merrick A., Olden K., Paules R., Selkirk J., Stasiewicz C., Weis B., Van Houten B., Walker N., and Tennant R. Systems toxicology and the chemical effects in biological systems knowledge base. Environ. Health Perspect. 111 (2003) 811-824
65. Widholm J.J., Villareal S., Seegal R.F., and Schantz S.L. Spatial alteration deficits following developmental exposure to Aroclor 1254 and/or methylmercury in rats. Toxicol. Sci. 82 (2004) 577-589
66. Winneke G., Walkowiak J., and Lilienthal H. PCB-induced neurodevelopmental toxicity in human infants and its potential mediation by endocrine dysfunction. Toxicology (2002) 161-165 181-182
67. Wu Z., Irizarry R.A., Gentleman R., Urillo F.M., and Spencer F. A model based background adjustment for oligonucliotide expression arrays. Technical Report. John Hopkins University, Dept. Biostatistics Working Papers, Baltimore (2003)
68. Yang J.H., Derr-Yellin E.C., and Kodavanti P.R. Alterations in brain protein kinase C isoforms following developmental exposure to a polychlorinated biphenyl mixture. Brain Res. Mol. Brain Res. 111 (2003) 123-135
69. Zoeller R.T. Environmental chemicals impacting the thyroid: targets and consequences. Thyroid 17 (2007) 811-817
70. Zoeller R.T., and Rovet J. Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J. Neuroendocrinol. 16 (2004) 809-818
71. Zoeller R.T., Dowling A.L., and Vas A.A. Developmental exposure to polychlorinated biphenyls exerts thyroid hormone-like effects on the expression of RC3/neurogranin and myelin basic protein messenger ribonucleic acids in the developing rat brain. Endocrinology 141 (2000) 181-189
72. Zoeller T.R., Dowling A.L., Herzig C.T., Iannacone E.A., Gauger K.J., and Bansal R. Thyroid hormone, brain development, and the environment. Environ. Health Perspect. 110 Suppl 3 (2002) 355-361