A hydroxylated metabolite of flame-retardant PBDE-47 decreases the survival, proliferation, and neuronal differentiation of primary cultured adult neural stem cells and interferes with signaling of ERK5 map kinase and neurotrophin 3

Toxicological Sciences

Volumn 134, Issue 1, 2013, Pages 111-124

  Li, Tan ^a,b   Wang, Wenbin ^a   Pan, Yung Wei ^a   Xu, Lihong ^b   Xia, Zhengui ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Adult neurogenesis; Apoptosis; Neuronal differentiation; Neurotoxicity; PBDE; Proliferation

Indexed keywords

FLAME RETARDANT; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 7; NEUROTROPHIN 3; ORGANOBROMINE DERIVATIVE; POLYBROMINATED DIPHENYLETHER 47 DERIVATIVE; UNCLASSIFIED DRUG; 2,2',4,4'-TETRABROMODIPHENYL ETHER; DIPHENYL ETHER DERIVATIVE;

ADULT STEM CELL; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL COUNT; CELL PROLIFERATION; CELL SURVIVAL; CYTOTOXICITY; ENZYME ACTIVATION; GLIA CELL; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROTOXICITY; NONHUMAN; OLIGODENDROGLIA; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE; ANIMAL; BRAIN; CELL CULTURE; CELL DIFFERENTIATION; DRUG EFFECTS; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; HYDROXYLATION; INBRED MOUSE STRAIN; METABOLISM; PATHOLOGY; PRIMARY CELL CULTURE; TOXICITY;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; FLAME RETARDANTS; HALOGENATED DIPHENYL ETHERS; HYDROXYLATION; MICE; MICE, INBRED STRAINS; MITOGEN-ACTIVATED PROTEIN KINASE 7; NEURAL STEM CELLS; NEUROTROPHIN 3; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION;

EID: 84880277731     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft083     Document Type: Article

References (67)

1. Ahmed, S., Reynolds, B. A., and Weiss, S. (1995). BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J. Neurosci. 15, 5765-5778.
2. Bath, K. G., and Lee, F. S. (2010). Neurotrophic factor control of adult SVZ neurogenesis. Dev. Neurobiol. 70, 339-349.
3. Costa, L. G., and Giordano, G. (2007). Developmental neurotoxicity of polybrominated diphenyl ether (PBDE) flame retardants. Neurotoxicology. 28, 1047-1067.
4. Costa, L. G., and Giordano, G. (2011). Is decabromodiphenyl ether (BDE-209) a developmental neurotoxicant? Neurotoxicology. 32, 9-24.
5. Costa, L. G., Giordano, G., Tagliaferri, S., Caglieri, A., and Mutti, A. (2008). Polybrominated diphenyl ether (PBDE) flame retardants: Environmental contamination, human body burden and potential adverse health effects. Acta Biomed. 79, 172-183.
6. Cundiff, P., Liu, L., Wang, Y., Zou, J., Pan, Y. W., Abel, G., Duan, X., Ming, G. L., Englund, C., Hevner, R., et al. (2009). ERK5 MAP kinase regulates neurogenin1 during cortical neurogenesis. PLoS One. 4, e5204.
7. de Wit, C. A. (2002). An overview of brominated flame retardants in the environment. Chemosphere. 46, 583-624.
8. Dingemans, M. M., de Groot, A., van Kleef, R. G., Bergman, A., van den Berg, M., Vijverberg, H. P., and Westerink, R. H. (2008). Hydroxylation increases the neurotoxic potential of BDE-47 to affect exocytosis and calcium homeostasis in PC12 cells. Environ. Health Perspect. 116, 637-643.
9. Dingemans, M. M., van den Berg, M., and Westerink, R. H. (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.
10. Eriksson, P., Viberg, H., Jakobsson, E., Orn, U., and 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.
11. Ernest, S. R., Wade, M. G., Lalancette, C., Ma, Y. Q., Berger, R. G., Robaire, B., and Hales, B. F. (2012). Effects of chronic exposure to an environmentally relevant mixture of brominated flame retardants on the reproductive and thyroid system in adult male rats. Toxicol. Sci. 127, 496-507.
12. Fan, C. Y., Besas, J., and Kodavanti, P. R. (2010). Changes in mitogen-activated protein kinase in cerebellar granule neurons by polybrominated diphenyl ethers and polychlorinated biphenyls. Toxicol. Appl. Pharmacol. 245, 1-8.
13. Fitzgerald, E. F., Shrestha, S., Gomez, M. I., McCaffrey, R. J., Zimmerman, E. A., Kannan, K., and Hwang, S. A. (2012). Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) and neuropsychological status among older adults in New York. Neurotoxicology 33, 8-15.
14. Frederiksen, M., Vorkamp, K., Thomsen, M., and Knudsen, L. E. (2009). Human internal and external exposure to PBDEs-a review of levels and sources. Int. J. Hyg. Environ. Health. 212, 109-134.
15. Gee, J. R., Moser, V. C., McDanie, K. L., and Herr, D. W. (2011). Neurochemical changes following a single dose of polybrominated diphenyl ether 47 in mice. Drug Chem. Toxicol. 34, 213-219.
16. Giordano, G., Kavanagh, T. J., and Costa, L. G. (2008). Neurotoxicity of a polybrominated diphenyl ether mixture (DE-71) in mouse neurons and astrocytes is modulated by intracellular glutathione levels. Toxicol. Appl. Pharmacol. 232, 161-168.
17. He, P., He, W., Wang, A., Xia, T., Xu, B., Zhang, M., and Chen, X. (2008a). PBDE-47-induced oxidative stress, DNA damage and apoptosis in primary cultured rat hippocampal neurons. Neurotoxicology. 29, 124-129.
18. He, P., Wang, A. G., Xia, T., Gao, P., Niu, Q., Guo, L. J., Xu, B. Y., and Chen, X. M. (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.
19. He, Y., Murphy, M. B., Yu, R. M., Lam, M. H., Hecker, M., Giesy, J. P., Wu, R. S., and Lam, P. K. (2008b). Effects of 20 PBDE metabolites on steroidogenesis in the H295R cell line. Toxicol. Lett. 176, 230-238.
20. Hendriks, H. S., Antunes Fernandes, E. C., Bergman, A., van den Berg, M., and Westerink, R. H. (2010). PCB-47, PBDE-47, and 6-OH-PBDE-47 differentially modulate human GABAA and alpha4beta2 nicotinic acetylcholine receptors. Toxicol. Sci. 118, 635-642.
21. Herbstman, J. B., Sjödin, A., Kurzon, M., Lederman, S. A., Jones, R. S., Rauh, V., Needham, L. L., Tang, D., Niedzwiecki, M., Wang, R. Y., et al. (2010). Prenatal exposure to PBDEs and neurodevelopment. Environ. Health Perspect. 118, 712-719.
22. Hertz-Picciotto, I., Bergman, A., Fängström, B., Rose, M., Krakowiak, P., Pessah, I., Hansen, R., and Bennett, D. H. (2011). Polybrominated diphenyl ethers in relation to autism and developmental delay: A case-control study. Environ. Health. 10, 1.
23. Hsieh, J., and Eisch, A. J. (2010). Epigenetics, hippocampal neurogenesis, and neuropsychiatric disorders: Unraveling the genome to understand the mind. Neurobiol. Dis. 39, 73-84.
24. Huang, S. C., Giordano, G., and Costa, L. G. (2010). Comparative cytotoxicity and intracellular accumulation of five polybrominated diphenyl ether congeners in mouse cerebellar granule neurons. Toxicol. Sci. 114, 124-132.
25. Johnson-Restrepo, B., and Kannan, K. (2009). An assessment of sources and pathways of human exposure to polybrominated diphenyl ethers in the United States. Chemosphere. 76, 542-548.
26. Kalantzi, O. I., Martin, F. L., Thomas, G. O., Alcock, R. E., Tang, H. R., Drury, S. C., Carmichael, P. L., Nicholson, J. K., and Jones, K. C. (2004). Different levels of polybrominated diphenyl ethers (PBDEs) and chlorinated compounds in breast milk from two U.K. Regions. Environ. Health Perspect. 112, 1085-1091.
27. Kato, Y., Kravchenko, V. V., Tapping, R. I., Han, J., Ulevitch, R. J., and Lee, J. D. (1997). BMK1/ERK5 regulates serum-induced early gene expression through transcription factor MEF2C. EMBO J. 16, 7054-7066.
28. Kempermann, G., Kuhn, H. G., and Gage, F. H. (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature. 386, 493-495.
29. Kodavanti, P. R., and Ward, T. R. (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.
30. Kuo, Y. M., Sepúlveda, M. S., Hua, I., Ochoa-Acuña, H. G., and Sutton, T. M. (2010). Bioaccumulation and biomagnification of polybrominated diphenyl ethers in a food web of Lake Michigan. Ecotoxicology. 19, 623-634.
31. Lee, J. D., Ulevitch, R. J., and Han, J. (1995). Primary structure of BMK1: A new mammalian map kinase. Biochem. Biophys. Res. Commun. 213, 715-724.
32. Li, L., Xie, S., Cai, H., Bai, X., and Xue, Z. (2008). Quantitative structure-property relationships for octanol-water partition coefficients of polybrominated diphenyl ethers. Chemosphere. 72, 1602-1606.
33. Li, T., Pan, Y. W., Wang, W., Abel, G., Zou, J., Xu, L., Storm, D. R., and Xia, Z. (2013). Targeted deletion of the ERK5 MAP kinase impairs neuronal differentiation, migration, and survival during adult neurogenesis in the olfactory bulb. PLoS One. 8, e61948.
34. Liang, J., and Slingerland, J. M. (2003). Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle. 2, 339-345.
35. Liu, L., Cavanaugh, J. E., Wang, Y., Sakagami, H., Mao, Z., and Xia, Z. (2003). ERK5 activation of MEF2-mediated gene expression plays a critical role in BDNF-promoted survival of developing but not mature cortical neurons. Proc. Natl. Acad. Sci. U. S. A. 100, 8532-8537.
36. Liu, L., Cundiff, P., Abel, G., Wang, Y., Faigle, R., Sakagami, H., Xu, M., and Xia, Z. (2006). Extracellular signal-regulated kinase (ERK) 5 is necessary and sufficient to specify cortical neuronal fate. Proc. Natl. Acad. Sci. U. S. A. 103, 9697-9702.
37. Mak, G. K., Enwere, E. K., Gregg, C., Pakarainen, T., Poutanen, M., Huhtaniemi, I., and Weiss, S. (2007). Male pheromone-stimulated neurogenesis in the adult female brain: Possible role in mating behavior. Nat. Neurosci. 10, 1003-1011.
38. Mazdai, A., Dodder, N. G., Abernathy, M. P., Hites, R. A., and Bigsby, R. M. (2003). Polybrominated diphenyl ethers in maternal and fetal blood samples. Environ. Health Perspect. 111, 1249-1252.
39. Messer, A. (2010). Mini-review: Polybrominated diphenyl ether (PBDE) flame retardants as potential autism risk factors. Physiol. Behav. 100, 245-249. Ming, G. L., and Song, H. (2011). Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron 70, 687-702.
40. Mirescu, C., Peters, J. D., Noiman, L., and Gould, E. (2006). Sleep deprivation inhibits adult neurogenesis in the hippocampus by elevating glucocorticoids. Proc. Natl. Acad. Sci. U. S. A. 103, 19170-19175.
41. Mitchell, M. M., Woods, R., Chi, L. H., Schmidt, R. J., Pessah, I. N., Kostyniak, P. J., and LaSalle, J. M. (2012). Levels of select PCB and PBDE congeners in human postmortem brain reveal possible environmental involvement in 15q11-q13 duplication autism spectrum disorder. Environ. Mol. Mutagen. 53, 589-598.
42. Morland, K. B., Landrigan, P. J., Sjödin, A., Gobeille, A. K., Jones, R. S., McGahee, E. E., Needham, L. L., and Patterson, D. G., Jr. (2005). Body burdens of polybrominated diphenyl ethers among urban anglers. Environ. Health Perspect. 113, 1689-1692.
43. Napoli, E., Hung, C., Wong, S., and Giulivi, C. (2013). Toxicity of the flameretardant BDE-49 on brain mitochondria and neuronal progenitor striatal cells enhanced by a PTEN-deficient background. Toxicol. Sci. 132, 196-210.
44. Pan, Y. W., Chan, G. C., Kuo, C. T., Storm, D. R., and Xia, Z. (2012a). Inhibition of adult neurogenesis by inducible and targeted deletion of ERK5 mitogen-activated protein kinase specifically in adult neurogenic regions impairs contextual fear extinction and remote fear memory. J. Neurosci. 32, 6444-6455.
45. Pan, Y. W., Kuo, C. T., Storm, D. R., and Xia, Z. (2012b). Inducible and targeted deletion of the ERK5 MAP kinase in adult neurogenic regions impairs adult neurogenesis in the olfactory bulb and several forms of olfactory behavior. PLoS One. 7, e49622.
46. Pan, Y. W., Storm, D. R., and Xia, Z. (2012c). The maintenance of established remote contextual fear memory requires ERK5 MAP kinase and ongoing adult neurogenesis in the hippocampus. PLoS One. 7, e50455.
47. Pan, Y. W., Zou, J., Wang, W., Sakagami, H., Garelick, M. G., Abel, G., Kuo, C.T., Storm, D. R., and Xia, Z. (2012d). Inducible and conditional deletion of extracellular signal-regulated kinase 5 disrupts adult hippocampal neurogenesis. J. Biol. Chem. 287, 23306-23317.
48. Qiu, X., Bigsby, R. M., and Hites, R. A. (2009). Hydroxylated metabolites of polybrominated diphenyl ethers in human blood samples from the United States. Environ. Health Perspect. 117, 93-98.
49. Raman, M., Chen, W., and Cobb, M. H. (2007). Differential regulation and properties of MAPKs. Oncogene. 26, 3100-3112.
50. Schecter, A., Päpke, O., Tung, K. C., Joseph, J., Harris, T. R., and Dahlgren, J. (2005). Polybrominated diphenyl ether flame retardants in the U.S. population: Current levels, temporal trends, and comparison with dioxins, dibenzofurans, and polychlorinated biphenyls. J. Occup. Environ. Med. 47, 199-211.
51. Schecter, A., Pavuk, M., Päpke, O., Ryan, J. J., Birnbaum, L., and Rosen, R. (2003). Polybrominated diphenyl ethers (PBDEs) in U.S. mothers' milk. Environ. Health Perspect. 111, 1723-1729.
52. Schreiber, T., Gassmann, K., Götz, C., Hübenthal, U., Moors, M., Krause, G., Merk, H. F., Nguyen, N. H., Scanlan, T. S., Abel, J., et al. (2010). Polybrominated diphenyl ethers induce developmental neurotoxicity in a human in vitro model: Evidence for endocrine disruption. Environ. Health Perspect. 118, 572-578.
53. Shao, J., White, C. C., Dabrowski, M. J., Kavanagh, T. J., Eckert, M. L., and Gallagher, E. P. (2008). The role of mitochondrial and oxidative injury in BDE 47 toxicity to human fetal liver hematopoietic stem cells. Toxicol. Sci. 101, 81-90.
54. Shaw, S. D., and Kannan, K. (2009). Polybrominated diphenyl ethers in marine ecosystems of the American continents: Foresight from current knowledge. Rev. Environ. Health. 24, 157-229.
55. Sjödin, A., Jones, R. S., Focant, J. F., Lapeza, C., Wang, R. Y., McGahee, E. E., 3rd, Zhang, Y., Turner, W. E., Slazyk, B., Needham, L. L., et al. (2004). Retrospective time-trend study of polybrominated diphenyl ether and polybrominated and polychlorinated biphenyl levels in human serum from the United States. Environ. Health Perspect. 112, 654-658.
56. Suhardja, A., and Hoffman, H. (2003). Role of growth factors and their receptors in proliferation of microvascular endothelial cells. Microsc. Res. Tech. 60, 70-75.
57. Tagliaferri, S., Caglieri, A., Goldoni, M., Pinelli, S., Alinovi, R., Poli, D., Pellacani, C., Giordano, G., Mutti, A., and Costa, L. G. (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.
58. van Praag, H., Kempermann, G., and Gage, F. H. (1999). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2, 266-270.
59. Verner, M. A., Bouchard, M., Fritsche, E., Charbonneau, M., and Haddad, S. (2011). In vitro neurotoxicity data in human risk assessment of polybrominated diphenyl ethers (PBDEs): Overview and perspectives. Toxicol. In Vitro. 25, 1509-1515.
60. Viberg, H., and Eriksson, P. (2011). Differences in neonatal neurotoxicity of brominated flame retardants, PBDE 99 and TBBPA, in mice. Toxicology. 289, 59-65.
61. Viberg, H., Fredriksson, A., Jakobsson, E., Orn, U., and Eriksson, P. (2003). Neurobehavioral derangements in adult mice receiving decabrominated diphenyl ether (PBDE 209) during a defined period of neonatal brain development. Toxicol. Sci. 76, 112-120.
62. Wang, W., Pan, Y. W., Wietecha, T., Zou, J., Abel, G. M., Kuo, C. T., and Xia, Z. (2013). Extracellular signal-regulated kinase 5 (ERK5) mediates prolactinstimulated adult neurogenesis in the subventricular zone and olfactory bulb. J. Biol. Chem. 288, 2623-2631.
63. Wiseman, S. B., Wan, Y., Chang, H., Zhang, X., Hecker, M., Jones, P. D., and Giesy, J. P. (2011). Polybrominated diphenyl ethers and their hydroxylated/methoxylated analogs: Environmental sources, metabolic relationships, and relative toxicities. Mar. Pollut. Bull. 63, 179-188.
64. Woods, R., Vallero, R. O., Golub, M. S., Suarez, J. K., Ta, T. A., Yasui, D. H., Chi, L. H., Kostyniak, P. J., Pessah, I. N., Berman, R. F., et al. (2012). Long-lived epigenetic interactions between perinatal PBDE exposure and Mecp2308 mutation. Hum. Mol. Genet. 21, 2399-2411.
65. Yan, T., Xiang, L., Xuejun, J., Chengzhi, C., Youbin, Q., Xuelan, Y., Yang, L., Changyan, P., and Hui, C. (2012). 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. 37, 223-233.
66. Zhao, C., Deng, W., and Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell. 132, 645-660.
67. Zou, J., Pan, Y. W., Wang, Z., Chang, S. Y., Wang, W., Wang, X., Tournier, C., Storm, D. R., and Xia, Z. (2012). Targeted deletion of ERK5 MAP kinase in the developing nervous system impairs development of GABAergic interneurons in the main olfactory bulb and behavioral discrimination between structurally similar odorants. J. Neurosci. 32, 4118-4132.