Effects of the brominated flame retardant hexabromocyclododecane (HBCD) on dopamine-dependent behavior and brainstem auditory evoked potentials in a one-generation reproduction study in Wistar rats

Toxicology Letters

Volumn 185, Issue 1, 2009, Pages 63-72

  Lilienthal, Hellmuth ^a   van der Ven, Leo T M ^b   Piersma, Aldert H ^b   Vos, Josephus G ^b  

^a INSTITUT DER RUHR UNIVERSITÄT BOCHUM IPA   (Germany)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

Author keywords

Benchmark analysis; Brominated flame retardants; Development; Hexabromocyclododecane; Neurotoxicity; Rats

Indexed keywords

DOPAMINE; HALOPERIDOL; HEXABROMOCYCLODODECANE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATALEPSY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DOPAMINERGIC SYSTEM; EVOKED BRAIN STEM AUDITORY RESPONSE; FEMALE; GESTATION PERIOD; LACTATION; MALE; MATING; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; REPRODUCTION; TISSUE LEVEL; WEANING; WISTAR RAT;

ANIMALS; BEHAVIOR, ANIMAL; CATALEPSY; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; FEMALE; FETUS; FLAME RETARDANTS; HYDROCARBONS, BROMINATED; MALE; PREGNANCY; RATS; RATS, WISTAR; REACTION TIME; REPRODUCTION;

RATTUS; RATTUS NORVEGICUS;

EID: 58349098956     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2008.12.002     Document Type: Article

References (73)

1. Antignac J.-P., Cariou R., Maume D., Marchand P., Monteau F., Zalko D., Berrebi A., Cravedi J.P., Andre F., and Le Bizec B. Exposure assessment of fetus and newborn to brominated flame retardants in France: preliminary data. Mol. Nutr. Food Res. 52 (2008) 258-265
2. Banjaw M.Y., Mayerhorfer A., and Schmidt W.J. Anticataleptic activity of cathinone and MDMA (ecstasy) upon acute and subchronic administration in rat. Synapse 49 (2003) 232-238
3. Birnbaum L.S., and Staskal D.F. Brominated flame retardants: cause for concern?. Environ. Health Perspects 112 (2004) 9-17
4. Bleecker M.L., Ford D.P., Lindgren K.N., Scheetz K., and Tiburzi M.J. Association of chronic and current measures of lead exposure with different components of brainstem auditory evoked potentials. Neurotoxicology 24 (2003) 625-631
5. Bogen I.L., Haug K.H., Myhre O., and Fonnum F. Short- and long-term effects of MDMA ("ecstasy") on synaptosomal and vesicular uptake of neurotransmitters in vitro andex vivo. Neurochem. Int. 43 (2003) 393-400
6. Bondioni S., Angioni A.R., Corbetta S., Locatelli M., Ferrero S., Ferrante E., Mantovani G., Olgiati L., Beck-Peccoz P., Spada A., and Lania A.G. Effect of 9-cis retinoic acid on dopamine D2 receptor expression in pituitary adenoma cells. Exp. Biol. Med. 233 (2008) 439-446
7. Bryant J., Goddyear R.J., and Richardson G.P. Sensory organ development in the inner ear: molecular and cellular mechanisms. Brit. Med. Bull. 63 (2002) 39-57
8. BSEF, 2006. Fact sheet, brominated flame retardant HBCD. Bromine Science and Environmental Forum: Brussels. Available www.bsef-site.com/.
9. Cecil H.C., Harris S.J., and Bitman H. Effects of polychlorinated biphenyls and terphenyls and polybrominated biphenyls on pentobarbital sleeping times of Japanese quail. Arch. Environ. Contam. Toxicol. 3 (1975) 183-192
10. Covaci A., Gerecke A.C., Law R.J., Voorspoels S., Kohler M., Heeb N.V., Leslie H., Allchin C.R., and de Boer J. Hexabromocyclododecanes (HBCDs) in the environment and humans: a review. Environ. Sci. Technol. 40 (2006) 3679-3688
11. Crofton K.M., Dean K.F., Menache M.G., and Janssen R. Trimethyltin effects on auditory function and cochlear morphology. Toxicol. Appl. Pharmacol. 105 (1990) 123-132
12. Crofton K.M., Ding D.-L., Padich R., Taylor M., and Henderson D. Hearing loss following exposure during development to polychlorinated biphenyls: a cochlear site of action. Hearing Res. 144 (2000) 196-204
13. Darnerud P.O. Toxic effects of brominated flame retardants in man and wildlife. Environ. Int. 29 (2003) 841-853
14. Dean S.L., and McCarthy M.M. Steroids, sex and the cerebellar cortex: implications for human disease. Cerebellum 7 (2008) 38-47
15. Ema M., Fuji S., Hirata-Koizumi M., and Matsumoto M. Two-generation reproductive toxicity study of the flame retardant hexabromocyclododecane in rats. Reprod. Toxicol. 25 (2008) 335-351
16. Eriksson P., Fischer C., Wallin M., Jakobsson E., and Fredriksson A. Impaired behaviour, learning and memory in adult mice neonatally exposed to hexabromocyclododecane (HBCDD). Environ. Toxicol. Pharmacol. 21 (2006) 317-322
17. Fang J., McKay G., Song J., Remillrd A., Li X., and Midha K. In vitro characterization of the metabolism of haloperidol using recombinant cytochrome p450 enzymes and human liver microsomes. Drug Metab. Dispos. 29 (2001) 1638-1643
18. Fängström B., Athanassiades I., Strid A., Odsjö T., Guvenius D., Noren K., and Bergman A. Temporal trends of PBDEs and HBCDD in milk from Stockholm mothers, 1980-2004. Organohalogen Compd. 68 (2006) 774-777
19. Fonnum F., Mariussen E., and Reistad T. Molecular mechanisms involved in the toxic effects of polychlorinated biphenyls (PCBs) and brominated flame retardants (BFRs). J. Toxicol. Environ. Health A 69 (2006) 21-35
20. Forrest D., Reh T.A., and Rüsch A. Neurodevelopmental control by thyroid hormone receptors. Curr. Opin. Neurobiol. 12 (2002) 49-56
21. Germer S., Piersma A.H., van der Ven L.T.M., Kamyschnikow A., Fery Y., Schmitz H.-J., and Schrenk D. Subacute effects of the brominated flame retardants hexabromocyclododecane and tetrabromobisphenol A on hepatic cytochrome P450 levels in rats. Toxicology 218 (2006) 229-236
22. Gillner S., Hellgren J., Menard A., Saitoh K., and Wikström M.A. Mechanism for selection of basic motor programs-roles for the striatum and pallidum. Trends Neurosci. 28 (2005) 364-370
23. Goldey E.S., and Crofton K.M. Thyroxine replacement attenuates hypothyroxinemia, hearing loss, and motor deficits following developmental exposure to Aroclor1254 in rats. Toxicol. Sci. 45 (1998) 94-105
24. Hamers T., Kamstra J.H., Sonneveld E., Murk A.J., Kester M.H.A., Andersson P.L., Legler J., and Brouwer A. In vitro profiling of the endocrine-disrupting potency of brominated flame retardants. Toxicol. Sci. 92 (2006) 157-173
25. Hiebl J., and Vetter W. Detection of hexabromocyclododecane and its metabolite pentabromocyclododecene in chicken egg and fish from the official food control. J. Agric. Food Chem. 55 (2007) 3319-3324
26. Johnson-Restrepo B., Adams D.H., and Kannan K. Tetrabromobisphenol A (TBBPA) and hexabromocyclododecanes (HBCDs) in tissues of humans, dolphins, and sharks from the United States. Chemosphere 70 (2008) 1935-1944
27. Kakimoto K., Akutsu K., Konishi Y., and Tanaka Y. Time trend of hexabromocyclododecane in the breast milk of Japanese women. Chemosphere 71 (2008) 1110-1114
28. Kaya H., Hany J., Fastabend A., Roth-Härer 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
29. Kipp M., Karakaya S., Pawlak J., Araujo-Wright G., Arnold S., and Beyer C. Estrogen and the development and protection of nigrostriatal dopaminergic neurons: concerted action of a multitude of signals, protective molecules, and growth factors. Front. Neuroendocrinol. 27 (2006) 376-390
30. Knipper M., Zinn C., Maier H., Praetorius M., Rohbock K., Köpschall I., and Zimmermann U. Thyroid hormone deficiency before the onset of hearing causes irreversible damage to peripheral and central auditory systems. J. Neurophysiol. 83 (2000) 3101-3112
31. Liao W.L., Tsai H.C., Wang H.F., Chang J., Lu K.M., Wu H.L., Lee Y.C., Tsai T.F., Takahashi H., Wagner M., Ghyselinck N.B., Chambon P., and Liu F.C. Modular patterning of structure and function of the striatum by retinoid receptor signaling. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 6765-6770
32. Lilienthal H., and Winneke G. Lead effects on the brain stem auditory evoked potential in monkeys during and after the treatment phase. Neurotoxicol. Teratol. 18 (1996) 17-32
33. Lilienthal H., Roth-Härer A., Hack A., Altmann L., and Winneke G. Developmental neurotoxicity of PHAHs: endocrine-mediated and general behavioral endpoints in adult male rats. Environ. Toxicol. Pharmacol. 19 (2005) 757-759
34. Lilienthal H., Hack A., Roth-Härer A., Wichert Grande S., and Talsness C. Effects of developmental exposure to 2,2′,4,4′,5-pentabromodiphenyl ether (PBDE-99) on sex steroids, sexual development, and sexually dimorphic behavior in rats. Environ. Health Perspects 114 (2006) 194-201
35. Lilienthal H., Verwer C., van der Ven L.T.M., Piersma A., and Vos J.G. Exposure to tetrabromobisphenol A (TBBPA) in Wistar rats: neurobehavioral effects in offspring from a one-generation reproduction study. Toxicology 246 (2008) 45-54
36. Lyng G.D., Snyder-Keller A., and Seegal R.F. Polychlorinated biphenyl-induced neurotoxicity in organotypic cocultures of developing rat ventral mesencephalon and striatum. Toxicol. Sci. 97 (2007) 128-139
37. Maden M. Retinoic acid in the development, regeneration and maintainance of the nervous system. Nat. Rev. Neurosci. 8 (2007) 755-765
38. Maguin K., Lataye R., Campo P., Cossec B., Burgart M., and Waniusiow D. Ototoxicity of the three xylene isomers in the rat. Neurotoxicol. Teratol. 28 (2006) 648-656
39. Mariussen E., and Fonnum F. The effect of brominated flame retardants on neurotransmitter uptake into rat brain synaptosomes and vesicles. Neurochem. Int. 43 (2003) 533-542
40. Mariussen E., and Fonnum F. Neurochemical targets and behavioral effects of organohalogen compounds: an update. Crit. Rev. Toxicol. 36 (2006) 253-289
41. McAlpine D. Creating a sense of auditory space. J. Physiol. (London) 566 (2005) 21-28
42. Meerts I.A.T.M., Lilienthal H., Hoving S., van den Berg J.H.J., Weijers B.M., Bergman A., Koeman J.H., and Brouwer A. Developmental exposure to 4-hydroxy-2,3,3′,4′,5-pentachlorobiphenyl (4-OH-CB107): long-term effects on brain development, behavior, and brain stem auditory evoked potentials in rats. Toxicol. Sci. 82 (2004) 207-218
43. Meethal S.V., and Atwood C.S. The role of hypothalamic-pituitary-gonadal hormones in the normal structure and functioning of the brain. Cell. Mol. Life Sci. 62 (2005) 257-270
44. Meijer L., Weiss J., van Velzen M., Brouwer A., Bergman A., and Sauer P. Serum concentration of neutral and phenolic organohalogens in pregnant women and some of their infants in the Netherlands. Environ. Sci. Technol. 42 (2008) 3428-3433
45. Morris S., Allchin C.R., Zegers B.N., Haftka J.J.H., Boon J.P., Belpaire C., Leonards P.E.G., van Leeuwen S.P.J., and de Boer J. Distribution and fate of HBCD and TBBPA brominated flame retardants in North Sea estuaries and aquatic food webs. Environ. Sci. Technol. 38 (2004) 5497-5504
46. Murray M. Role of CYP pharmacogenetics and drug-drug interactions in the efficacy and safety of atypical and other antipsychotic agents. J. Pharm. Pharmacol. 58 (2006) 871-885
47. Ng L., Goodyear R.J., Woods C.A., Schneider M.J., Diamond E., Richardson G.P., Kelley M.W., Germain D.L., Galton V.A., and Forrest D. Hearing loss and retarded cochlear development in mice lacking type 2 iodothyronine deiodinase. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 3474-3479
48. Oh-Nishi A., Saji M., Furudate S.-I., and Suzuki N. Dopamine D2-like receptor function is converted from excitatory to inhibitory by thyroxine in the developmental hippocampus. J. Neuroendocrinol. 17 (2005) 836-845
49. Pelkonen O., Turpeinen M., Hakkola J., Honkakoski P., Hukkanen J., and Raunio H. Inhibition and induction of human cytochrome P450 enzymes: current status. Arch. Toxicol. 82 (2008) 667-715
50. Pisani A., Bernardi G., Ding J., and Surmeier D.J. Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci. 30 (2007) 545-553
51. Rance G. Auditory neuropathy/dys-synchrony and its perceptual consequences. Trends Amplif. 9 (2005) 1-43
52. Raz Y., and Kelley M.W. Retinoic acid signaling is necessary for the development of the organ of Corti. Dev. Biol. 213 (1999) 180-193
53. Reistad T., Fonnum F., and Mariussen E. Neurotoxicity of the pentabrominated diphenyl ether mixture, DE-71, and hexabromocyclododecane (HBCD) in rat cerebellar granule cells in vitro. Arch. Toxicol. 80 (2006) 785-796
54. Romand R. The roles of retinoic acid during inner ear development. Curr. Top. Dev. Biol. 57 (2003) 261-291
55. Romand R., Kondo T., Fraulob V., Petkovich M., Dolle P., and Hasjoni E. Dynamic expression of retinoic acid-synthesizing and -metabolizing enzymes in the developing mouse inner ear. J. Comp. Neurol. 496 (2006) 643-654
56. Rovet J., Walker W., Bliss B., Buchanan L., and Ehrlich R. Long-term sequelae of hearing impairment in congenital hypothyroidism. J. Pediatr. 128 (1996) 776-783
57. Samad T.A., Krezel W., Chambon P., and Borrelli E. Regulation of dopaminergic pathways by retinoids: activation of the D2 receptor promoter by members of the retinoic acid receptor-retinoid X receptor family. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 14349-14354
58. Schecter A., Harris T.R., Shah N., Musumba A., and Päpke O. Brominated flame retardants in US food. Mol. Nutr. Food Res. 52 (2008) 266-272
59. Schriks M., Vrabie C.M., Gutleb A.C., Faasen E.J., Rietjens I.M.C.M., and Murk A.J. T-screen to quantify functional potentiating, antagonistic and thyroid hormone-like activities of polyhalogenated aromatic hydrocarbons (PHAHs). Toxicol. In Vitro 20 (2006) 490-498
60. Seegal R.F., Brosch K.O., and Okoniewski R.J. Coplanar PCB congeners increase uterine weight and frontal cortical dopamine in the developing rat: implications for developmental neurotoxicity. Toxicol. Sci. 86 (2005) 125-131
61. Simmons G.J., and McKee M.J. Alkoxyresorufin metabolism in white-footed mice at relevant environmental concentrations of Aroclor 1254. Fund. Appl. Toxicol. 19 (1992) 446-452
62. Slob W. dose-response modeling of continuous endpoints. Toxicol. Sci. 66 (2002) 298-312
63. Thomsen C., Molander P., Daae H.L., Janak K., Froshaug M., Liane V.H., Thorud S., Becher G., and Dybing E. Occupational exposure to hexabromocyclododecane at an industrial plant. Environ. Sci. Technol. 41 (2007) 5210-5216
64. Thomsen C., Knutsen H.K., Liane V.H., Froshaug M., Kvalem H.E., Haugen M., Meltzer H.M., Alexander J., and Becher G. Consumption of fish from a lake strongly affects the concentrations of polybrominated diphenyl ethers and hexabromocyclododecane in serum. Mol. Nutr. Food Res. 52 (2008) 228-237
65. van der Ven L.T.M., Verhoef A., van de Kuil T., Slob W., Leonards P.E.G., Visser T.J., Hamers T., Herlin M., Hakansson H., Olausson H., Piersma A.H., and Vos J.P. A 28-day oral dose toxicity study enhanced to detect endocrine effects of hexabromocyclododecane in Wistar rats. Toxicol. Sci. 94 (2006) 281-292
66. van der Ven L.T.M., van de Kuil T., Verhoef A., Verwer C.M., Lilienthal H., Leonards P.E.G., Schauer U.M.D., Canton R.F., Litens S., De Jong F.H., Visser T.J., Dekant W., Stern N., Hakansson H., Slob W., van den Berg M., Vos J.G., and Piersma A.H. Endocrine effects of tetrabromobisphenol-A (TBBPA) in Wistar rats as tested in a one-generation reproduction study and a subacute toxicity study. Toxicology 245 (2008) 76-89
67. van der Ven, L.T.M., van de Kuil, T., Slob, W., Leonards, P.E.G., Lilienthal, H., Visser, T.J., van Loveren, H., Vos, J.P., Piersma, A.H., in press. Endocrine effects of hexabromocyclododecane (HBCD) in a one-generation reproduction study in Wistar rats, Toxicol. Lett., doi:10.1016/j.toxlet.2008.12.003.
68. Villeneuve D.C., Grant D.L., and Phillips W.E. Modification of pentobarbital sleeping times in rats following chronic PCB ingestion. Bull. Environ. Contam. Toxicol. 7 (1972) 264-269
69. Wang H.F., and Liu F.C. Regulation of multiple dopamine signal transduction molecules by retinoids in the developing striatum. Neuroscience 134 (2005) 97-105
70. Weinand-Härer A., Lilienthal H., Bucholski K.-A., and Winneke G. Behavioral effects of maternal exposure to an ortho-chlorinated or a coplanar PCB congener in rats. Environ. Toxicol. Pharmacol. 3 (1997) 97-103
71. Weiss J., Wallin E., Axmon A., Jönsson B.A.G., Akeson H., Janak K., Halgmar L., and Bergman A. Hydroxy-PCBs, PBDEs, and HBCDDs in serum from an elderly population of Swedish fishermen's wives and associations with bone density. Environ. Sci. Technol. 40 (2006) 6282-6289
72. Yamada-Okabe T., Sakai H., Kashima Y., and Yamada-Okabe H. Modulation at a cellular level of the thyroid hormone receptor-mediated gene expression by 1,2,5,6,9,10-hexabromocyclododecane (HBCD), 4,4′-diiodobiphenyl (DIB), and nitrofen (NIP). Toxicol. Lett. 155 (2005) 127-133
73. Zegers B.N., Mets A., van Bommel R., Minkenberg C., Hamers T., Kamstra J.H., Pierce G.J., and Boon J.P. Levels of hexabromocyclododecane in harbor porpoises and common dolphins from Western European seas, with evidence for stereoisomer-specific biotransformation by cytochrome P450. Environ. Sci. Technol. 39 (2005) 2095-2100