Modulation of cell viability, oxidative stress, calcium homeostasis, and voltage- and ligand-gated ion channels as common mechanisms of action of (mixtures of) non-dioxin-like polychlorinated biphenyls and polybrominated diphenyl ethers

Environmental Science and Pollution Research

Volumn 21, Issue 10, 2014, Pages 6373-6383

  Westerink, Remco H S ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Calcium homeostasis; Cell viability; Mixture toxicity; Neurotoxicity; Nicotinic acetylcholine receptors; Non Dioxin Like Polychlorinated Biphenyls; Oxidative stress; Polybrominated Diphenyl Ethers; Voltage gated calcium channels

Indexed keywords

CELL ORGANELLE; DATA SET; ETHER; HOMEOSTASIS; INHIBITOR; LIGAND; NEUROLOGY; ORGANIC COMPOUND; ORGANIC POLLUTANT; OXIDATION; TOXICITY;

ANIMALIA;

CALCIUM; DANGEROUS GOODS; DIPHENYL ETHER DERIVATIVE; LIGAND GATED ION CHANNEL; POLLUTANT; POLYBROMINATED BIPHENYL; POLYCHLORINATED BIPHENYL; TETRABROMOBISPHENOL A;

ANIMAL; CELL SURVIVAL; DANGEROUS GOODS; HOMEOSTASIS; HUMAN; METABOLISM; OXIDATIVE STRESS; POLLUTANT; TOXICITY;

ANIMALS; CALCIUM; CELL SURVIVAL; ENVIRONMENTAL POLLUTANTS; HALOGENATED DIPHENYL ETHERS; HAZARDOUS SUBSTANCES; HOMEOSTASIS; HUMANS; LIGAND-GATED ION CHANNELS; OXIDATIVE STRESS; POLYBROMINATED BIPHENYLS; POLYCHLORINATED BIPHENYLS;

EID: 84900852515     PISSN: 09441344     EISSN: 16147499     Source Type: Journal    
DOI: 10.1007/s11356-013-1759-x     Document Type: Review

References (111)

1. An J, Li S, Zhong Y, Wang Y, Zhen K, Zhang X, Wang Y, Wu M, Yu Z, Sheng G, Fu J, Huang Y (2011) The cytotoxic effects of synthetic 6-hydroxylated and 6-methoxylated polybrominated diphenyl ether 47 (BDE47). Environ Toxicol 26: 591-599.
2. Antunes Fernandes EC, Hendriks HS, van Kleef RG, van den Berg M, Westerink RH (2010a) Potentiation of the human GABA(A) receptor as a novel mode of action of lower-chlorinated non-dioxin-like PCBs. Environ Sci Technol 44: 2864-2869.
3. A receptors by non-dioxin-like PCBs depends on chlorination pattern. Toxicol Sci 118: 183-190.
4. ATSDR (2000) Toxicological profile for polychlorinated biphenyls (PCBs). Agency for toxic substances and disease registry, Atlanta.
5. Bae J, Stuenkel EL, Loch-Caruso R (1999) Stimulation of oscillatory uterine contraction by the PCB mixture Aroclor 1242 may involve increased [Ca2+]i through voltage-operated calcium channels. Toxicol Appl Pharmacol 155: 261-272.
6. Bemis JC, Seegal RF (1999) Polychlorinated biphenyls and methylmercury act synergistically to reduce rat brain dopamine content in vitro. Environ Health Perspect 107: 879-885.
7. Bemis JC, Seegal RF (2000) Polychlorinated biphenyls and methylmercury alter intracellular calcium concentrations in rat cerebellar granule cells. Neurotoxicology 21: 1123-1134.
8. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4: 517-529.
9. Boix J, Cauli O, Felipo V (2010) Developmental exposure to polychlorinated biphenyls 52, 138, or 180 affects differentially learning or motor coordination in adult rats. Mechanisms involved. Neuroscience 167: 994-1003.
10. Breivik K, Sweetman A, Pacyna JM, Jones KC (2002) Towards a global historical emission inventory for selected PCB congeners-a mass balance approach. 1. Global production and consumption. Sci Total Environ 290: 181-198.
11. Broding HC, Schettgen T, Goen T, Angerer J, Drexler H (2007) Development and verification of a toxicokinetic model of polychlorinated biphenyl elimination in persons working in a contaminated building. Chemosphere 68: 1427-1434.
12. Cantón RF, Sanderson JT, Nijmeijer S, Bergman A, Letcher RJ, van den Berg M (2006) In vitro effects of brominated flame retardants and metabolites on CYP17 catalytic activity: a novel mechanism of action? Toxicol Appl Pharmacol 216: 274-281.
13. Carpenter DO (2006) Polychlorinated biphenyls (PCBs): routes of exposure and effects on human health. Rev Environ Health 21: 1-23.
14. Carrasco MA, Hidalgo C (2006) Calcium microdomains and gene expression in neurons and skeletal muscle cells. Cell Calcium 40: 575-583.
15. Catterall WA, Few AP (2008) Calcium channel regulation and presynaptic plasticity. Neuron 59: 882-901.
16. 2+ and synaptic plasticity. Cell Calcium 38: 355-367.
17. Chishti MA, Fisher JP, Seegal RF (1996) Aroclors 1254 and 1260 reduce dopamine concentrations in rat striatal slices. Neurotoxicology 17: 653-660.
18. Coburn CG, Currás-Collazo MC, Kodavanti PRS (2008) In vitro effects of environmentally relevant polybrominated diphenyl ether (PBDE) congeners on calcium buffering mechanisms in rat brain. Neurochem Res 33: 355-364.
19. Collin T, Marty A, Llano I (2005) Presynaptic calcium stores and synaptic transmission. Curr Opin Neurobiol 15: 275-281.
20. Consonni D, Sindaco R, Bertazzi PA (2012) Blood levels of dioxins, furans, dioxin-like PCBs, and TEQs in general populations: a review, 1989-2010. Environ Int 44: 151-62.
21. Costa LG, Giordano G (2007) Developmental neurotoxicity of polybrominated diphenyl ether (PBDE) flame retardants. Neurotoxicology 28: 1047-1067.
22. Costa LG, Giordano G, Tagliaferri S, Caglieri A, Mutti A (2008) Polybrominated diphenyl ether (PBDE) flame retardants: environmental contamination, human body burden, and potential adverse health effects. Acta Biomed 79: 172-183.
23. D'Hulst C, Atack JR, Kooy RF (2009) The complexity of the GABAA receptor shapes unique pharmacological profiles. Drug Discov Today 14: 866-875.
24. Darnerud PO, Eriksen GS, Johannesson T, Larsen PB, Viluksela M (2001) Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology. Environ Health Perspect 109(1): 49-68.
25. Dickerson SM, Guevara E, Woller MJ, Gore AC (2009) Cell death mechanisms in GT1-7 GnRH cells exposed to polychlorinated biphenyls PCB74, PCB118, and PCB153. Toxicol Appl Pharmacol 237: 237-245.
26. Dingemans MM, Ramakers GM, Gardoni F, van Kleef RG, Bergman A, Di Luca M, van den Berg M, Westerink RH, Vijverberg HP (2007) Neonatal exposure to brominated flame retardant BDE-47 reduces long-term potentiation and postsynaptic protein levels in mouse hippocampus. Environ Health Perspect 115: 865-870.
27. Dingemans MM, de Groot A, van Kleef RG, Bergman A, van den Berg M, Vijverberg HP, Westerink RH (2008) Hydroxylation increases the neurotoxic potential of BDE-47 to affect exocytosis and calcium homeostasis in PC12 cells. Environ Health Perspect 116: 637-643.
28. Dingemans MM, Heusinkveld HJ, Bergman A, van den Berg M, Westerink RH (2010a) Bromination pattern of hydroxylated metabolites of BDE-47 affects their potency to release calcium from intracellular stores in PC12 cells. Environ Health Perspect 118: 519-525.
29. Dingemans MM, van den Berg M, Bergman A, Westerink RH (2010b) Calcium-related processes involved in the inhibition of depolarization-evoked calcium increase by hydroxylated PBDEs in PC12 cells. Toxicol Sci 114: 302-309.
30. Dingemans MM, van den Berg M, Westerink RH (2011) Neurotoxicity of brominated flame retardants: (in)direct effects of parent and hydroxylated polybrominated diphenyl ethers on the (developing) nervous system. Environ Health Perspect 119: 900-907.
31. Dreiem A, Rykken S, Lehmler HJ, Robertson LW, Fonnum F (2009) Hydroxylated polychlorinated biphenyls increase reactive oxygen species formation and induce cell death in cultured cerebellar granule cells. Toxicol Appl Pharmacol 240: 306-313.
32. Dwyer JB, McQuown SC, Leslie FM (2009) The dynamic effects of nicotine on the developing brain. Pharmacol Ther 122: 125-139.
33. EFSA (2005) Opinion of the scientific panel on contaminants in the food chain on a request from the comission related to the presence of non dioxin-like polychlorinated biphenyls (PCB) in feed and food. The EFSA Journal, 1-137.
34. Eriksson P, Fredriksson A (1996) Developmental neurotoxicity of four ortho-substituted polychlorinated biphenyls in the neonatal mouse. Environ Toxicol Pharmacol 1: 155-165.
35. Eriksson P, Viberg H, Jakobsson E, Orn U, Fredriksson A (2002) A brominated flame retardant, 2, 2′, 4, 4′, 5-pentabromodiphenyl ether: uptake, retention, and induction of neurobehavioral alterations in mice during a critical phase of neonatal brain development. Toxicol Sci 67: 98-103.
36. Fan CY, Besas J, Kodavanti PR (2010) Changes in mitogen-activated protein kinase in cerebellar granule neurons by polybrominated diphenyl ethers and polychlorinated biphenyls. Toxicol Appl Pharmacol 245: 1-8.
37. Faroon O, Jones D, de Rosa C (2001) Effects of polychlorinated biphenyls on the nervous system. Toxicol Ind Health 16: 305-333.
38. Ferrante MC, Mattace Raso G, Esposito E, Bianco G, Iacono A et al (2011) Effects of non-dioxin-like polychlorinated biphenyl congeners (PCB 101, PCB 153 and PCB 180) alone or mixed on J774A. 1 macrophage cell line: modification of apoptotic pathway. Toxicol Lett 202: 61-68.
39. Fischer D, Hooper K, Athanasiadou M, Athanassiadis I, Bergman A (2006) Children show highest levels of polybrominated diphenyl ethers in a California family of four: a case study. Environ Health Perspect 114: 1581-1584.
40. Fonnum F, Mariussen E (2009) Mechanisms involved in the neurotoxic effects of environmental toxicants such as polychlorinated biphenyls and brominated flame retardants. J Neurochem 111: 1327-1347.
41. Fonnum F, Mariussen E, Reistad T (2006) Molecular mechanisms involved in the toxic effects of polychlorinated biphenyls (PCBs) and brominated flame retardants (BFRs). J Toxicol Environ Health A 69: 21-35.
42. Frederiksen M, Vorkamp K, Thomsen M, Knudsen LE (2009) Human internal and external exposure to PBDEs-a review of levels and sources. Int J Hyg Environ Health 212: 109-134.
43. Fujii S, Jia Y, Yang A, Sumikawa K (2000) Nicotine reverses GABAergic inhibition of long-term potentiation induction in the hippocampal CA1 region. Brain Res 863: 259-265.
44. Gabrio T, Piechotowski I, Wallenhorst T, Klett M, Cott L, Friebel P, Link B, Schwenk M (2000) PCB-blood levels in teachers, working in PCB-contaminated schools. Chemosphere 40: 1055-1062.
45. Gao P, He P, Wang A, Xia T, Xu B, Xu Z, Niu Q, Guo L, Chen X (2009) Influence of PCB153 on oxidative DNA damage and DNA repair-related gene expression induced by PBDE-47 in human neuroblastoma cells in vitro. Toxicol Sci 107: 165-170.
46. Garcia AG, Garcia de Diego AM, Gandia L, Borges R, Garcia-Sancho J (2006) Calcium signaling and exocytosis in adrenal chromaffin cells. Physiol Rev 86: 1093-1131.
47. Gilbert ME (2003) Perinatal exposure to polychlorinated biphenyls alters excitatory synaptic transmission and short-term plasticity in the hippocampus of the adult rat. Neurotoxicology 24: 851-860.
48. He P, Wang AG, Xia T, Gao P, Niu Q, Guo LJ, Xu BY, Chen XM (2009) Mechanism of the neurotoxic effect of PBDE-47 and interaction of PBDE-47 and PCB153 in enhancing toxicity in SH-SY5Y cells. Neurotoxicology 30: 10-15.
49. He W, Wang A, Xia T, Gao P, Xu B, Xu Z, He P, Chen X (2010) Cytogenotoxicity induced by PBDE-47 combined with PCB153 treatment in SH-SY5Y cells. Environ Toxicol 25: 564-572.
50. A and alpha4beta2 nicotinic acetylcholine receptors. Toxicol Sci 118: 635-642.
51. Hendriks HS, van Kleef RG, Westerink RH (2012a) Modulation of human α4β2 nicotinic acetylcholine receptors by brominated and halogen-free flame retardants as a measure for in vitro neurotoxicity. Toxicol Lett 213: 266-274.
52. Hendriks HS, van Kleef RG, van den Berg M, Westerink RH (2012b) Multiple novel modes of action involved in the in vitro neurotoxic effects of tetrabromobisphenol-A. Toxicol Sci 128: 235-246.
53. Herbstman JB, Sjödin A, Kurzon M, Lederman SA, Jones RS, Rauh V et al (2010) Prenatal exposure to PBDEs and neurodevelopment. Environ Health Perspect 118: 712-719.
54. Heusinkveld HJ, Westerink RH (2011) Caveats and limitations of plate reader-based high-throughput kinetic measurements of intracellular calcium levels. Toxicol Appl Pharmacol 255: 1-8.
55. Hites RA (2004) Polybrominated diphenyl ethers in the environment and in people: a meta-analysis of concentrations. Environ Sci Technol 38: 945-956.
56. Howard AS, Fitzpatrick R, Pessah I, Kostyniak P, Lein PJ (2003) 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: 72-86.
57. Hu X, Adamcakova-Dodd A, Lehmler HJ, Hu D, Hornbuckle K, Thorne PS (2012) Subchronic inhalation exposure study of an airborne polychlorinated biphenyl mixture resembling the Chicago ambient air congener profile. Environ Sci Technol 46: 9653-9662.
58. Huang SC, Giordano G, Costa LG (2010) Comparative cytotoxicity and intracellular accumulation of five polybrominated diphenyl ether congeners in mouse cerebellar granule neurons. Toxicol Sci 114: 124-132.
59. Inglefield JR, Shafer TJ (2000a) Polychlorinated biphenyl-stimulation of Ca(2+) oscillations in developing neocortical cells: a role for excitatory transmitters and L-type voltage-sensitive Ca(2+) channels. J Pharmacol Exp Ther 295: 105-113.
60. Inglefield JR, Shafer TJ (2000b) 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: 184-195.
61. Inglefield JR, Mundy WR, Shafer TJ (2001) Inositol 1, 4, 5-triphosphate receptor-sensitive Ca(2+) release, store-operated Ca(2+) entry, and cAMP responsive element binding protein phosphorylation in developing cortical cells following exposure to polychlorinated biphenyls. J Pharmacol Exp Ther 297: 762-773.
62. Ji K, Choi K, Giesy JP, Musarrat J, Takeda S (2011) Genotoxicity of several polybrominated diphenyl ethers (PBDEs) and hydroxylated PBDEs, and their mechanisms of toxicity. Environ Sci Technol 45: 5003-5008.
63. Johansson C, Tofighi R, Tamm C, Goldoni M, Mutti A, Ceccatelli S (2006) Cell death mechanisms in AtT20 pituitary cells exposed to polychlorinated biphenyls (PCB 126 and PCB 153) and methylmercury. Toxicol Lett 167: 183-190.
64. Johansson N, Viberg H, Fredriksson A, Eriksson P (2008) Neonatal exposure to deca-brominated diphenyl ether (PBDE 209) causes dose-response changes in spontaneous behaviour and cholinergic susceptibility in adult mice. Neurotoxicology 29: 911-919.
65. Kim KH, Inan SY, Berman RF, Pessah IN (2009) Excitatory and inhibitory synaptic transmission is differentially influenced by two ortho-substituted polychlorinated biphenyls in the hippocampal slice preparation. Toxicol Appl Pharmacol 237: 168-177.
66. Kim KH, Bose DD, Ghogha A, Riehl J, Zhang R, Barnhart CD, Lein PJ, Pessah IN (2011) Para- and ortho-substitutions are key determinants of polybrominated diphenyl ether activity toward ryanodine receptors and neurotoxicity. Environ Health Perspect 119: 519-526.
67. Kodavanti PR, Ward TR (2005) Differential effects of commercial polybrominated diphenyl ether and polychlorinated biphenyl mixtures on intracellular signaling in rat brain in vitro. Toxicol Sci 85: 952-962.
68. Kodavanti PR, Shin DS, Tilson HA, Harry GJ (1993) Comparative effects of 2 polychlorinated biphenyl congeners on calcium homeostasis in rat cerebellar granule cells. Toxicol Appl Pharmacol 123: 97-106.
69. Kodavanti PR, Kannan N, Yamashita N, Derr-Yellin EC, Ward TR, Burgin DE, Tilson HA, Birnbaum LS (2001) Differential effects of two lots of aroclor 1254: congener-specific analysis and neurochemical end points. Environ Health Perspect 109: 1153-1161.
70. Kodavanti PR, Ward TR, Derr-Yellin EC, McKinney JD, Tilson HA (2003) Increased [3H]phorbol ester binding in rat cerebellar granule cells and inhibition of 45Ca(2+) buffering in rat cerebellum by hydroxylated polychlorinated biphenyls. Neurotoxicology 24: 187-198.
71. Kodavanti PR, Ward TR, Ludewig G, Robertson LW, Birnbaum LS (2005) Polybrominated diphenyl ether (PBDE) effects in rat neuronal cultures: 14C-PBDE accumulation, biological effects, and structure-activity relationships. Toxicol Sci 88: 181-192.
72. Langeveld WT, Meijer M, Westerink RH (2012) Differential effects of 20 non-dioxin-like PCBs on basal and depolarization-evoked intracellular calcium levels in PC12 cells. Toxicol Sci 126: 487-496.
73. Law RJ, Herzke D, Harrad S, Morris S, Bersuder P, Allchin CR (2008) Levels and trends of HBCD and BDEs in the European and Asian environments, with some information for other BFRs. Chemosphere 73: 223-241.
74. Lin CH, Lin PH (2006) Induction of ROS formation, poly(ADP-ribose) polymerase-1 activation, and cell death by PCB126 and PCB153 in human T47D and MDA-MB-231 breast cancer cells. Chem Biol Interact 162: 181-194.
75. Llansola M, Montoliu C, Boix J, Felipo V (2010) Polychlorinated biphenyls PCB 52, PCB 180, and PCB 138 impair the glutamate-nitric oxide-cGMP pathway in cerebellar neurons in culture by different mechanisms. Chem Res Toxicol 23: 813-820.
76. Londoño M, Shimokawa N, Miyazaki W, Iwasaki T, Koibuchi N (2010) Hydroxylated PCB induces Ca2+ oscillations and alterations of membrane potential in cultured cortical cells. J Appl Toxicol 30: 334-342.
77. Magi S, Castaldo P, Carrieri G, Scorziello A, Di Renzo G, Amoroso S (2005) Involvement of Na+-Ca2+ exchanger in intracellular Ca2+ increase and neuronal injury induced by polychlorinated biphenyls in human neuroblastoma SH-SY5Y cells. J Pharmacol Exp Ther 315: 291-296.
78. Mariussen E, Fonnum F (2006) Neurochemical targets and behavioral effects of organohalogen compounds: an update. Crit Rev Toxicol 36: 253-289.
79. Mariussen E, Myhre O, Reistad T, Fonnum F (2002) 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: 137-144.
80. Mohler H (2007) Molecular regulation of cognitive functions and developmental plasticity: impact of GABAA receptors. J Neurochem 102: 1-12.
81. Moody WJ, Bosma MM (2005) Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol Rev 85: 883-941.
82. Mundy WR, Freudenrich TM, Crofton KM, DeVito MJ (2004) Accumulation of PBDE-47 in primary cultures of rat neocortical cells. Toxicol Sci 82: 164-169.
83. Orrenius S, Nicotera P, Zhivotovsky B (2011) Cell death mechanisms and their implications in toxicology. Toxicol Sci 119: 3-19.
84. Pessah IN, Cherednichenko G, Lein PJ (2010) Minding the calcium store: ryanodine receptor activation as a convergent mechanism of PCB toxicity. Pharmacol Ther 125: 260-285.
85. Petrik J, Drobna B, Pavuk M, Jursa S, Wimmerova S, Chovancova J (2006) Serum PCBs and organochlorine pesticides in Slovakia: age, gender, and residence as determinants of organochlorine concentrations. Chemosphere 65: 410-418.
86. Reistad T, Mariussen E (2005) A commercial mixture of the brominated flame retardant pentabrominated diphenyl ether (DE-71) induces respiratory burst in human neutrophil granulocytes in vitro. Toxicol Sci 87: 57-65.
87. Reistad T, Mariussen E, Fonnum F (2006) Neurotoxicity of the pentabrominated diphenyl ether mixture, DE-71, and hexabromocyclododecane (HBCD) in rat cerebellar granule cells in vitro. Arch Toxicol 80: 785-796.
88. Represa A, Ben-Ari Y (2005) Trophic actions of GABA on neuronal development. Trends Neurosci 28: 278-283.
89. Roze E, Meijer L, Bakker A, van Braeckel KN, Sauer PJ (2009) Prenatal exposure to organohalogens, including brominated flame retardants, influences motor, cognitive, and behavioral performance at school age. Environ Health Perspect 117: 1953-1958.
90. Schantz SL, Widholm JJ, Rice DC (2003) Effects of PCB exposure on neuropsychological function in children. Environ Health Perspect 111: 357-376.
91. 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.
92. Shimokawa N, Miyazaki W, Iwasaki T, Koibuchi N (2006) Low-dose hydroxylated PCB induces c-Jun expression in PC12 cells. Neurotoxicology 27: 176-183.
93. Smaili SS, Pereira GJ, Costa MM, Rocha KK, Rodrigues L, do Carmo LG, Hirata H, Hsu YT (2013) The role of calcium stores in apoptosis and autophagy. Curr Mol Med 13: 252-265.
94. Spitzer NC (2006) Electrical activity in early neuronal development. Nature 444: 707-712.
95. Sugawara N, Nakai K, Nakamura T, Ohba T, Suzuki K, Kameo S, Satoh C, Satoh H (2006) Developmental and neurobehavioral effects of perinatal exposure to polychlorinated biphenyls in mice. Arch Toxicol 80: 286-292.
96. Tagliaferri S, Caglieri A, Goldoni M, Pinelli S, Alinovi R et al (2010) Low concentrations of the brominated flame retardants BDE-47 and BDE-99 induce synergistic oxidative stress-mediated neurotoxicity in human neuroblastoma cells. Toxicol In Vitro 24: 116-122.
97. Tilson HA, Kodavanti PR (1998) The neurotoxicity of polychlorinated biphenyls. Neurotoxicology 19: 517-525.
98. Tofighi R, Johansson C, Goldoni M, Ibrahim WN, Gogvadze V, Mutti A, Ceccatelli S (2011) Hippocampal neurons exposed to the environmental contaminants methylmercury and polychlorinated biphenyls undergo cell death via parallel activation of calpains and lysosomal proteases. Neurotox Res 19: 183-194.
99. Toms LM, Sjödin A, Harden F, Hobson P, Jones R et al (2009) Serum polybrominated diphenyl ether (PBDE) levels are higher in children (2-5 years of age) than in infants and adults. Environ Health Perspect 117: 1461-1465.
100. Ulbrich B, Stahlmann R (2004) Developmental toxicity of polychlorinated biphenyls (PCBs): a systematic review of experimental data. Arch Toxicol 78: 252-268.
101. Usenko CY, Hopkins DC, Trumble SJ, Bruce ED (2012) Hydroxylated PBDEs induce developmental arrest in zebrafish. Toxicol Appl Pharmacol 262: 43-51.
102. van den Berg M, Birnbaum LS, Denison M, De Vito M, Farland W et al (2006) The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci 93: 223-241.
103. Viberg H, Fredriksson A, Eriksson P (2003a) Neonatal exposure to polybrominated diphenyl ether (PBDE 153) disrupts spontaneous behaviour, impairs learning and memory, and decreases hippocampal cholinergic receptors in adult mice. Toxicol Appl Pharmacol 192: 95-106.
104. Viberg H, Fredriksson A, Jakobsson E, Orn U, Eriksson P (2003b) Neurobehavioral derangements in adult mice receiving decabrominated diphenyl ether (PBDE 209) during a defined period of neonatal brain development. Toxicol Sci 76: 112-120.
105. Voie ØA, Fonnum F (1998) Ortho-substituted polychlorinated biphenyls elevate intracellular [Ca2+] in human granulocytes. Environ Toxicol Pharmacol 5: 105-112.
106. Westerink RHS (2006) Targeting exocytosis: ins and outs of the modulation of quantal dopamine release. CNS Neurol Disord Drug Targets 5: 57-77.
107. Westerink RHS, Vijverberg HPM (2002) Vesicular catecholamine release from rat PC12 cells on acute and subchronic exposure to polychlorinated biphenyls. Toxicol Appl Pharmacol 183: 153-159.
108. Winneke G, Walkowiak J, Lilienthal H (2002) PCB-induced neurodevelopmental toxicity in human infants and its potential mediation by endocrine dysfunction. Toxicology 181-182: 161-165.
109. Xing T, Chen L, Tao Y, Wang M, Chen J, Ruan DY (2009) Effects of decabrominated diphenyl ether (PBDE 209) exposure at different developmental periods on synaptic plasticity in the dentate gyrus of adult rats in vivo. Toxicol Sci 110: 401-410.
110. Xing TR, Yong W, Chen L, Tang ML, Wang M, Chen JT, Ruan DY (2010) Effects of decabrominated diphenyl ether (PBDE 209) on voltage-gated sodium channels in primary cultured rat hippocampal neurons. Environ Toxicol 25: 400-408.
111. Yu K, He Y, Yeung LWY, Lam PKS, Wu RSS, Zhou B (2008) DE-71-induced apoptosis involving intracellular calcium and the Bax-mitochondria-caspase protease pathway in human neuroblastoma cells in vitro. Toxicol Sci 104: 341-351.