Neurodevelopmental effects of decabromodiphenyl ether (BDE-209) in APOE transgenic mice

Neurotoxicology and Teratology

Volumn 46, Issue , 2014, Pages 10-17

  Reverte, Ingrid ^a,b   Domingo, José L ^b   Colomina, Maria Teresa ^a,b  

^a UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^b INSTITUT D INVESTIGACIÓ SANITÀRIA PERE VIRGILI IISPV   (Spain)

Author keywords

Apolipoprotein E; BDE 209; Decabromodiphenyl ether; FOB; Neurodevelopment; PBDEs

Indexed keywords

APOLIPOPROTEIN E2; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; BDE 209; POLYBROMINATED DIPHENYL ETHER; UNCLASSIFIED DRUG; APOLIPOPROTEIN E; DECABROMOBIPHENYL ETHER; DIPHENYL ETHER DERIVATIVE; FLAME RETARDANT; NEUROTOXIN;

AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL SCREENING; DEVELOPMENTAL TOXICITY; DOSE RESPONSE; EYE DEVELOPMENT; FEMALE; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; MALE; MOTOR DEVELOPMENT; MOUSE; NERVE CELL DIFFERENTIATION; NEUROTOXICITY; NEWBORN; NONHUMAN; PERINATAL PERIOD; PROTEIN POLYMERIZATION; VULNERABLE POPULATION; AGE; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; DRUG EFFECTS; GENETICS; MOTOR ACTIVITY; TRANSGENIC MOUSE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; APOLIPOPROTEINS E; BEHAVIOR, ANIMAL; FEMALE; FLAME RETARDANTS; HALOGENATED DIPHENYL ETHERS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; NEUROTOXINS;

EID: 84908039732     PISSN: 08920362     EISSN: 18729738     Source Type: Journal    
DOI: 10.1016/j.ntt.2014.08.003     Document Type: Article

References (80)

1. Adgent M.A., Hoffman K., Goldman B.D., Sjödin A., Daniels J.L. Brominated flame retardants in breast milk and behavioural and cognitive development at 36months. Paediatr Perinat Epidemiol 2014, 28:48-57.
2. Alm H., Scholz B., Fischer C., Kultima K., Viberg H., Eriksson P., et al. Proteomic evaluation of neonatal exposure to 2,2,4,4,5-pentabromodiphenyl ether. Environ Health Perspect 2006, 114:254-259.
3. Bernal J. Thyroid hormone receptors in brain development and function. Nat Clin Pract Endocrinol Metab 2007, 3:249-259.
4. Bour A., Grootendorst J., Vogel E., Kelche C., Dodart J.C., Bales K., et al. Middle-aged human apoE4 targeted-replacement mice show retention deficits on a wide range of spatial memory tasks. Behav Brain Res 2008, 193:174-182.
5. Bradner J.M., Suragh T.A., Caudle W.M. Alterations to the circuitry of the frontal cortex following exposure to the polybrominated diphenyl ether mixture, DE-71. Toxicology 2013, 312:48-55.
6. Bradner J.M., Suragh T.A., Wilson W.W., Lazo C.R., Stout K.A., Kim H.M., et al. Exposure to the polybrominated diphenyl ether mixture DE-71 damages the nigrostriatal dopamine system: role of dopamine handling in neurotoxicity. Exp Neurol 2013, 241:138-147.
7. Branchi I., Alleva E., Costa L.G. Effects of perinatal exposure to a polybrominated diphenyl ether (PBDE 99) on mouse neurobehavioural development. Neurotoxicology 2002, 23:375-384.
8. Bu G. Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat Rev Neurosci 2009, 10:333-344.
9. Carrascal L., Nieto-Gonzalez J.L., Torres B., Nunez-Abades P. Changes in somatodendritic morphometry of rat oculomotor nucleus motoneurons during postnatal development. J Comp Neurol 2009, 514(2):189-202.
10. Chao H.R., Tsou T.C., Huang H.L., Chang-Chien G.P. Levels of breast milk PBDEs from southern Taiwan and their potential impact on neurodevelopment. Pediatr Res 2011, 70:596-600.
11. Colton C.A., Brown C.M., Vitek M.P. Sex steroids, APOE genotype and the innate immune system. Neurobiol Aging 2005, 26:363-372.
12. Costa L.G., Giordano G. Developmental neurotoxicity of polybrominated diphenyl ether (PBDE) flame retardants. Neurotoxicology 2007, 28:1047-1067.
13. Costa L.G., Giordano G. Is decabromodiphenyl ether (BDE-209) a developmental neurotoxicant?. Neurotoxicology 2011, 32:9-24.
14. Costa L.G., de Laat R., Tagliaferri S., Pellacani C. A mechanistic view of polybrominated diphenyl ether (PBDE) developmental neurotoxicity. Toxicol Lett 2014, [in press]. 10.1016/j.toxlet.2013.11.011.
15. Dietschy J.M., Turley S.D. Thematic review series: brain lipids. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J Lipid Res 2004, 45:1375-1397.
16. Dingemans M.M., Ramakers G.M., Gardoni F., van Kleef R.G., Bergman A., Di Luca M., et al. Neonatal exposure to brominated flame retardant BDE-47 reduces long-term potentiation and postsynaptic protein levels in mouse hippocampus. Environ Health Perspect 2007, 115:865-870.
17. Domingo J.L. Polybrominated diphenyl ethers in food and human dietary exposure: a review of the recent scientific literature. Food Chem Toxicol 2012, 50:238-249.
18. Du J., Chang J., Guo S., Zhang Q., Wang Z. ApoE 4 reduces the expression of Abeta degrading enzyme IDE by activating the NMDA receptor in hippocampal neurons. Neurosci Lett 2009, 464:140-145.
19. Dufault C., Poles G., Driscoll L.L. Brief postnatal PBDE exposure alters learning and the cholinergic modulation of attention in rats. Toxicol Sci 2005, 88:172-180.
20. EFSA . Scientific opinion on polybrominated diphenyl ethers (PBDEs) in food. EFSA J 2011, 9(15):1-274.
21. Eriksson P., Jakobsson E., Fredriksson A. Brominated flame retardants: a novel class of developmental neurotoxicants in our environment?. Environ Health Perspect 2001, 109:903-908.
22. Eriksson P., Viberg H., Jakobsson E., Orn U., Fredriksson A. 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 2002, 67:98-103.
23. Eskenazi B., Chevrier J., Rauch S.A., Kogut K., Harley K.G., Johnson C., et al. In utero and childhood polybrominated diphenyl ether (PBDE) exposures and neurodevelopment in the CHAMACOS study. Environ Health Perspect 2013, 121:257-262.
24. Fuentes S., Colomina M.T., Vicens P., Franco-Pons N., Domingo J.L. Concurrent exposure to perfluorooctane sulfonate and restraint stress during pregnancy in mice: effects on postnatal development and behavior of the offspring. Toxicol Sci 2007, 98:589-598.
25. Furman M., Crair M.C. Synapse maturation is enhanced in the binocular region of the retinocollicular map prior to eye opening. J Neurophysiol 2012, 107(11):3200-3216.
26. Gee J.R., Moser V.C. Acute postnatal exposure to brominated diphenylether 47 delays neuromotor ontogeny and alters motor activity in mice. Neurotoxicol Teratol 2008, 30:79-87.
27. Gee J.R., Moser V.C., McDanie K.L., Herr D.W. Neurochemical changes following a single dose of polybrominated diphenyl ether 47 in mice. Drug Chem Toxicol 2011, 34:213-219.
28. George Y., Derrien P., Lefranc G., Tusques J. Acceleration of keratinization in the process of opening of the palpebral fissure in the thyroxine-treated newborn rat. C R Seances Soc Biol Fil 1969, 163(4):947-949.
29. Gin D.W., Kim H.R., Lee D.M., Lee S.H., Seong A.R., Hwang J.A., et al. 2,3,7,8-Tetrachlorodibenzo-p-dioxin up-regulates stathmin 1 in the eye: suggestive evidence for the involvement of stathmin 1 in accelerated eye opening in mice induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Lett 2010, 196(2):87-94.
30. Gozes I., Bachar M., Bardea A., Davidson A., Rubinraut S., Fridkin M., et al. Protection against developmental retardation in apolipoprotein E-deficient mice by a fatty neuropeptide: implications for early treatment of Alzheimer's disease. J Neurobiol 1997, 33:329-342.
31. Grootendorst J., Bour A., Vogel E., Kelche C., Sullivan P.M., Dodart J.C., et al. Human apoE targeted replacement mouse lines: h-apoE4 and h-apoE3 mice differ on spatial memory performance and avoidance behavior. Behav Brain Res 2005, 159:1-14.
32. Gutzmann A., Ergül N., Engelhardt M. A period of structural plasticity at the axon initial segment in developing visual cortex. Front Neuroanat 2014, 8:11.
33. Haley G.E., Villasana L., Dayger C., Davis M.J., Raber J. Apolipoprotein e genotype-dependent paradoxical short-term effects of (56)fe irradiation on the brain. Int J Radiat Oncol Biol Phys 2012, 84:793-799.
34. Hardy M.L., Banasik M., Stedeford T. Toxicology and human health assessment of decabromodiphenyl ether. Crit Rev Toxicol 2009, 39(Suppl. 3):1-44.
35. Hatters D.M., Peters-Libeu C.A., Weisgraber K.H. Apolipoprotein E structure: insights into function. Trends Biochem Sci 2006, 31:445-454.
36. He P., Wang A., Niu Q., Guo L., Xia T., Chen X. Toxic effect of PBDE-47 on thyroid development, learning, and memory, and the interaction between PBDE-47 and PCB153 that enhances toxicity in rats. Toxicol Ind Health 2011, 27:279-288.
37. Herbstman J.B., Sjödin A., Kurzon M., Lederman S.A., Jones R.S., Rauh V., et al. Prenatal exposure to PBDEs and neurodevelopment. Environ Health Perspect 2010, 118:712-719.
38. Herlenius E., Lagercrantz H. Development of neurotransmitter systems during critical periods. Exp Neurol 2004, 190:S8-S21.
39. Herz J., Chen Y. Reelin, lipoprotein receptors and synaptic plasticity. Nat Rev Neurosci 2006, 7:850-859.
40. Hoffman K., Adgent M., Goldman B.D., Sjödin A., Daniels J.L. Lactational exposure to polybrominated diphenyl ethers and its relation to social and emotional development among toddlers. Environ Health Perspect 2012, 120:1438-1442.
41. Huang Y. Apolipoprotein E and Alzheimer disease. Neurology 2006, 66:S79-S85.
42. Hudry E., Dashkoff J., Roe A.D., Takeda S., Koffie R.M., Hashimoto T., et al. Gene transfer of human Apoe isoforms results in differential modulation of amyloid deposition and neurotoxicity in mouse brain. Sci Transl Med 2013, 5:212ra161.
43. Johansson N., Viberg H., Fredriksson A., Eriksson P. Neonatal exposure to deca-brominated diphenyl ether (PBDE 209) causes dose-response changes in spontaneous behaviour and cholinergic susceptibility in adult mice. Neurotoxicology 2008, 29:911-919.
44. Kapalanga J., Blecher S.R. Histological studies on eyelid opening in normal male mice and hemizygotes for the mutant gene Tabby (Ta) with and without epidermal growth factor treatment. Exp Eye Res 1991, 52(2):155-166.
45. Keppel G., Wickens T.D. Design and analysis: a researcher's handbook 2004, Pearson Prentice Hall, Upper Saddle River, NJ.
46. Lee E., Kim T.H., Choi J.S., Nabanata P., Kim N.Y., Ahn M.Y., et al. Evaluation of liver and thyroid toxicity in Sprague-Dawley rats after exposure to polybrominated diphenyl ether BDE-209. J Toxicol Sci 2010, 35:535-545.
47. Liraz O., Boehm-Cagan A., Michaelson D.M. ApoE4 induces Aβ42, tau, and neuronal pathology in the hippocampus of young targeted replacement apoE4 mice. Mol Neurodegener 2013, 8:16.
48. Liscovitch N., Chechik G. Specialization of gene expression during mouse brain development. PLoS Comput Biol 2013, 9(9):e1003185.
49. Miodovnik A. Environmental neurotoxicants and developing brain. Mt Sinai J Med 2011, 78:58-77.
50. Moncman C.L., Andrade M.E., McCool A.A., McMullen C.A., Andrade F.H. Development transitions of thin filament proteins in rat extraocular muscles. Exp Cell Res 2013, 319(3):23-31.
51. Moser V.C. The functional observational battery in adult and developing rats. Neurotoxicology 2000, 21:989-996.
52. Ng S., Lin C.C., Hwang Y.H., Hsieh W.S., Liao H.F., Chen P.C. Mercury, APOE, and children's neurodevelopment. Neurotoxicology 2013, 37:85-92.
53. Poirier J. Apolipoprotein E in animal models of CNS injury and in Alzheimer's disease. Trends Neurosci 1994, 17:525-530.
54. Reverte I., Klein A.B., Ratner C., Domingo J.L., Colomina M.T. Behavioral phenotype and BDNF differences related to apoE isoforms and sex in young transgenic mice. Exp Neurol 2012, 237:116-125.
55. Reverte I., Klein A.B., Domingo J.L., Colomina M.T. Long term effects of murine postnatal exposure to decabromodiphenyl ether (BDE-209) on learning and memory are dependent upon APOE polymorphism and age. Neurotoxicol Teratol 2013, 40C:17-27.
56. Reverte I., Pujol A., Domingo J.L., Colomina M.T. Thyroid hormones and fear learning but not anxiety are affected in adult APOE transgenic mice exposed postnatally to decabromodiphenyl ether (BDE-209). Physiol Behav 2014, 133:81-91.
57. Rice D.C., Reeve E.A., Herlihy A., Zoeller R.T., Thompson W.D., Markowski V.P. Developmental delays and locomotor activity in the C57BL6/J mouse following neonatal exposure to the fully-brominated PBDE, decabromodiphenyl ether. Neurotoxicol Teratol 2007, 29:511-520.
58. Rice D.C., Thompson W.D., Reeve E.A., Onos K.D., Assadollahzadeh M., Markowski V.P. Behavioral changes in aging but not young mice after neonatal exposure to the polybrominated flame retardant decaBDE. Environ Health Perspect 2009, 117:1903-1911.
59. Rochefort N.L., Garaschuk O., Milos R.I., Narushima M., Marandi N., Pichler B., et al. Sparsification of neuronal activity in the visual cortex at eye-opening. Proc Natl Acad Sci 2009, 106(35):15049-15054.
60. Roze E., Meijer L., Bakker A., Van Braeckel K.N., Sauer P.J., Bos A.F. Prenatal exposure to organohalogens, including brominated flame retardants, influences motor, cognitive, and behavioral performance at school age. Environ Health Perspect 2009, 117:1953-1958.
61. Schmidt M.V. Molecular mechanisms of early life stress-lessons from mouse models. Neurosci Biobehav Rev 2010, 34:845-852.
62. Seabrook T.A., El-Danaf R.N., Krahe T.E., Fox M.A., Guido W. Retinal input regulates the timing of corticogeniculate innervation. J Neurosci 2013, 33(24):10085-10097.
63. Siegel J.A., Haley G.E., Raber J. Apolipoprotein E isoform-dependent effects on anxiety and cognition in female TR mice. Neurobiol Aging 2012, 33:345-358.
64. Strittmatter W.J., Weisgraber K.H., Huang D.Y., Dong L.M., Salvesen G.S., Pericak-Vance M., et al. Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci U S A 1993, 90:8098-8102.
65. Strittmatter W.J., Saunders A.M., Goedert M., Weisgraber K.H., Dong L.M., Jakes R., et al. Isoform-specific interactions of apolipoprotein E with microtubule-associated protein tau: implications for Alzheimer disease. Proc Natl Acad Sci U S A 1994, 91:11183-11186.
66. Sullivan G.M., Feinn R. Using effect size-or why the p value is not enough. J Grad Med Educ 2012, 4(3):279-282.
67. Sullivan P.M., Mezdour H., Aratani Y., Knouff C., Najib J., Reddick R.L., et al. Targeted replacement of the mouse apolipoprotein E gene with the common human APOE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis. J Biol Chem 1997, 272:17972-17980.
68. Sullivan P.M., Han B., Liu F., Mace B.E., Ervin J.F., Wu S., et al. Reduced levels of human apoE4 protein in an animal model of cognitive impairment. Neurobiol Aging 2011, 32:791-801.
69. Viberg H., Fredriksson A., Eriksson P. Neonatal exposure to the brominated flame retardant 2,2',4,4',5-pentabromodiphenyl ether causes altered susceptibility in the cholinergic transmitter system in the adult mouse. Toxicol Sci 2002, 67:104-107.
70. Viberg H., Fredriksson A., Eriksson P. 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 2003, 192:95-106.
71. Viberg H., Fredriksson A., Jakobsson E., Orn U., Eriksson P. Neurobehavioral derangements in adult mice receiving decabrominated diphenyl ether (PBDE 209) during a defined period of neonatal brain development. Toxicol Sci 2003, 76:112-120.
72. Viberg H., Fredriksson A., Eriksson P. Neonatal exposure to the brominated flame-retardant, 2,2',4,4',5-pentabromodiphenyl ether, decreases cholinergic nicotinic receptors in hippocampus and affects spontaneous behaviour in the adult mouse. Environ Toxicol Pharmacol 2004, 17:61-65.
73. Viberg H., Fredriksson A., Eriksson P. Changes in spontaneous behaviour and altered response to nicotine in the adult rat, after neonatal exposure to the brominated flame retardant, decabrominated diphenyl ether (PBDE 209). Neurotoxicology 2007, 28:136-142.
74. Villasana L., Acevedo S., Poage C., Raber J. Sex- and APOE isoform-dependent effects of radiation on cognitive function. Radiat Res 2006, 166:883-891.
75. 56Fe irradiation on spatial memory of mice: role of sex and apolipoprotein E isoform. Int J Radiat Oncol Biol Phys 2011, 80:567-573.
76. Wan Y., Zhang K., Dong Z., Hu J. Distribution is a major factor affecting bioaccumulation of decabrominated diphenyl ether: Chinese sturgeon (Acipenser sinensis) as an example. Environ Sci Technol 2013, 47(5):2279-2286.
77. Watson R.E., DeSesso J.M., Hurtt M.E., Cappon G.D. Postnatal growth and morphological development of the brain: a species comparison. Birth Defects Res B 2006, 77:471-484.
78. Wright R.O., Hu H., Silverman E.K., Tsaih S.W., Schwartz J., Bellinger D., et al. Apolipoprotein E genotype predicts 24-month bayley scales infant development score. Pediatr Res 2003, 54:819-825.
79. Yan T., Xiang L., Xuejun J., Chengzhi C., Youbin Q., Xuelan Y., et al. Spatial learning and memory deficit of low level polybrominated diphenyl ethers-47 in male adult rat is modulated by intracellular glutamate receptors. J Toxicol Sci 2012, 37:223-233.
80. Zieske J.D. Corneal development associated with eyelid opening. Int J Dev Biol 2004, 48(8-9):903-911.