Maternal transfer of BDE-47 to offspring and neurobehavioral development in C57BL/6J mice

Neurotoxicology and Teratology

Volumn 34, Issue 6, 2012, Pages 571-580

  Koenig, Claire M ^a   Lango, Jozsef ^a   Pessah, Isaac N ^a   Berman, Robert F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

BDE 47; Behavior; Bioaccumulation; Flame retardant; Neurodevelopment; Polybrominated diphenyl ether

Indexed keywords

FLAME RETARDANT; POLYBROMINATED DIPHENYL ETHER; POLYBROMINATED DIPHENYL ETHER 47; UNCLASSIFIED DRUG;

ACCLIMATIZATION; ANIMAL CELL; ARTICLE; BIOACCUMULATION; BLOOD; CALIBRATION; CONTROLLED STUDY; FEMALE; GAIT; GESTATIONAL AGE; GRIP STRENGTH; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LACTATION; LEARNING; LIMIT OF DETECTION; LITTER SIZE; LOCOMOTION; MALE; MAZE TEST; MEMORY; MOTOR PERFORMANCE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PERINATAL PERIOD; PLACENTAL TRANSFER; PRIORITY JOURNAL; PROGENY; REPRODUCTIVE SUCCESS; WEIGHT GAIN;

ANIMALS; BEHAVIOR, ANIMAL; ENVIRONMENTAL POLLUTANTS; FEMALE; MALE; MATERNAL-FETAL EXCHANGE; MICE; MICE, INBRED C57BL; MILK; MOTOR ACTIVITY; NERVOUS SYSTEM; POLYBROMINATED BIPHENYLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; TISSUE DISTRIBUTION;

MUS;

EID: 84867807477     PISSN: 08920362     EISSN: 18729738     Source Type: Journal    
DOI: 10.1016/j.ntt.2012.09.005     Document Type: Article

References (76)

1. 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.
2. Bannerman D.M., Good M.A., Butcher S.P., Ramsay M., Morris R.G. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature 1995, 378:182-186.
3. Beare J.E., Morehouse J.R., DeVries W.H., Enzmann G.U., Burke D.A., Magnuson D.S., et al. Gait analysis in normal and spinal contused mice using the TreadScan system. J Neurotrauma 2009, 26:2045-2056.
4. Binelli A., Guzzella L., Roscioli C. Levels and congener profiles of polybrominated diphenyl ethers (PBDEs) in Zebra mussels (D. polymorpha) from Lake Maggiore (Italy). Environ Pollut 2008, 153:610-617.
5. Cain D.P., Saucier D., Hall J., Hargreaves E.L., Boon F. Detailed behavioral analysis of water maze acquisition under APV or CNQX: contribution of sensorimotor disturbances to drug-induced acquisition deficits. Behav Neurosci 1996, 110:86-102.
6. Chen D., La Guardia M.J., Harvey E., Amaral M., Wohlfort K., Hale R.C. Polybrominated diphenyl ethers in peregrine falcon (Falco peregrinus) eggs from the northeastern U.S. Environ Sci Technol 2008, 42:7594-7600.
7. Clissold P.M., Hainey S., Bishop J.O. Messenger RNAs coding for mouse major urinary proteins are differentially induced by testosterone. Biochem Genet 1984, 22:379-387.
8. Darnerud P.O., Risberg S. Tissue localisation of tetra- and pentabromodiphenyl ether congeners (BDE-47, -85 and -99) in perinatal and adult C57BL mice. Chemosphere 2006, 62:485-493.
9. Davison A.N., Dobbing J. The developing brain. Appl Neurochem 1968, 253-286.
10. Depeters E.J., Hovey R.C. Methods for collecting milk from mice. J Mammary Gland Biol Neoplasia 2009, 14(4):397-400.
11. 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.
12. Elliott J.E., Wilson L.K., Wakeford B. Polybrominated diphenyl ether trends in eggs of marine and freshwater birds from British Columbia, Canada, 1979-2002. Environ Sci Technol 2005, 39:5584-5591.
13. Engelmann M., Ebner K., Landgraf R., Wotjak C.T. Effects of Morris water maze testing on the neuroendocrine stress response and intrahypothalamic release of vasopressin and oxytocin in the rat. Horm Behav 2006, 50:496-501.
14. 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.
15. Farr T.D., Liu L., Colwell K.L., Whishaw I.Q., Metz G.A. Bilateral alteration in stepping pattern after unilateral motor cortex injury: a new test strategy for analysis of skilled limb movements in neurological mouse models. J Neurosci Methods 2006, 153:104-113.
16. Finlay B.L., Darlington R.B. Linked regularities in the development and evolution of mammalian brains. Science 1995, 268:1578-1584.
17. Frederiksen M., Vorkamp K., Thomsen M., Knudsen L.E. Human internal and external exposure to PBDEs-a review of levels and sources. Int J Hyg Environ Health 2009, 212:109-134.
18. Gascon M., Vrijheid M., Martinez D., Forns J., Grimalt J.O., Torrent M., et al. Effects of pre and postnatal exposure to low levels of polybromodiphenyl ethers on neurodevelopment and thyroid hormone levels at 4years of age. Environ Int 2011, 37:605-611.
19. 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.
20. Golub M.S., Germann S.L., Lloyd K.C. Behavioral characteristics of a nervous system-specific erbB4 knock-out mouse. Behav Brain Res 2004, 153:159-170.
21. Gomara B., Herrero L., Ramos J.J., Mateo J.R., Fernandez M.A., Garcia J.F., et al. Distribution of polybrominated diphenyl ethers in human umbilical cord serum, paternal serum, maternal serum, placentas, and breast milk from Madrid population, Spain. Environ Sci Technol 2007, 41:6961-6968.
22. Haraguchi K., Hisamichi Y., Endo T. Accumulation and mother-to-calf transfer of anthropogenic and natural organohalogens in killer whales (Orcinus orca) stranded on the Pacific coast of Japan. Sci Total Environ 2009, 407:2853-2859.
23. Herbstman J.B., Sjodin A., Kurzon M., Lederman S.A., Jones R.S., Rauh V., et al. Prenatal exposure to PBDEs and neurodevelopment. Environ Health Perspect 2009, 118(5):712-719.
24. Hunsaker M.R., von Leden R.E., Ta B.T., Goodrich-Hunsaker N.J., Arque G., Kim K., et al. Motor deficits on a ladder rung task in male and female adolescent and adult CGG knock-in mice. Behav Brain Res 2011, 222:117-121.
25. Huwe J.K., West M. Polybrominated diphenyl ethers in U.S. meat and poultry from two statistically designed surveys showing trends and levels from 2002 to 2008. J Agric Food Chem 2011, 59:5428-5434.
26. Jin S., Yang F., Hui Y., Xu Y., Lu Y., Liu J. Cytotoxicity and apoptosis induction on RTG-2 cells of 2,2',4,4'-tetrabromodiphenyl ether (BDE-47) and decabrominated diphenyl ether (BDE-209). Toxicol In Vitro 2010, 24:1190-1196.
27. Johnson-Restrepo B., Kannan K., Rapaport D.P., Rodan B.D. Polybrominated diphenyl ethers and polychlorinated biphenyls in human adipose tissue from New York. Environ Sci Technol 2005, 39:5177-5182.
28. Johnson-Restrepo B., Addink R., Wong C., Arcaro K., Kannan K. Polybrominated diphenyl ethers and organochlorine pesticides in human breast milk from Massachusetts, USA. J Environ Monit 2007, 9:1205-1212.
29. Kim T.H., Lee Y.J., Lee E., Patra N., Lee J., Kwack S.J., et al. Exposure assessment of polybrominated diphenyl ethers (PBDE) in umbilical cord blood of Korean infants. J Toxicol Environ Health A 2009, 72:1318-1326.
30. Kim T.H., Bang du Y., Lim H.J., Won A.J., Ahn M.Y., Patra N., et al. Comparisons of polybrominated diphenyl ethers levels in paired South Korean cord blood, maternal blood, and breast milk samples. Chemosphere 2012, 87:97-104.
31. La A.G.M.J., Hale R.C., Harvey E. Detailed polybrominated diphenyl ether (PBDE) congener composition of the widely used penta-, octa-, and deca-PBDE technical flame-retardant mixtures. Environ Sci Technol 2006, 40:6247-6254.
32. Law R.J., Allchin C.R., de Boer J., Covaci A., Herzke D., Lepom P., Morris S., Tronczynski J., de Wit C.A. Levels and trends of brominated flame retardants in the European environment. Chemosphere 2006, 64(2):187-208.
33. Lorber M. Exposure of Americans to polybrominated diphenyl ethers. J Expo Sci Environ Epidemiol 2008, 18:2-19.
34. Luine V., Martinez C., Villegas M., Magarinos A.M., McEwen B.S. Restraint stress reversibly enhances spatial memory performance. Physiol Behav 1996, 59:27-32.
35. Lunder S., Hovander L., Athanassiadis I., Bergman A. Significantly higher polybrominated diphenyl ether levels in young U.S. children than in their mothers. Environ Sci Technol 2010, 44:5256-5262.
36. Macri S., Granstrem O., Shumilina M., Antunes Gomes dos Santos F.J., Berry A., Saso L., et al. Resilience and vulnerability are dose-dependently related to neonatal stressors in mice. Horm Behav 2009, 56:391-398.
37. Macri S., Zoratto F., Laviola G. Early-stress regulates resilience, vulnerability and experimental validity in laboratory rodents through mother-offspring hormonal transfer. Neurosci Biobehav Rev 2011, 35:1534-1543.
38. Marteau C., Chevolleau S., Jouanin I., Perdu E., De Sousa G., Rahmani R., et al. Development of a liquid chromatography/atmospheric pressure photo-ionization high-resolution mass spectrometry analytical method for the simultaneous determination of polybrominated diphenyl ethers and their metabolites: application to BDE-47 metabolism in human hepatocytes. Rapid Commun Mass Spectrom 2012, 26:599-610.
39. Masuda Y., Kagawa R., Tokudome S., Kuratsune M. Transfer of polychlorinated biphenyls to the foetuses and offspring of mice. Food Cosmet Toxicol 1978, 16:33-37.
40. McIntosh I., Bishop J.O. Differential expression in male and female mouse liver of very similar mRNAs specified by two group 1 major urinary protein genes. Mol Cell Biol 1989, 9:2202-2207.
41. McMullin T.S., Lowe E.R., Bartels M.J., Marty M.S. Dynamic changes in lipids and proteins of maternal, fetal, and pup blood and milk during perinatal development in CD and Wistar rats. Toxicol Sci 2008, 105:260-274.
42. Metz G.A., Whishaw I.Q. The ladder rung walking task: a scoring system and its practical application. J Vis Exp 2009, 28. pii: 1204.
43. Meyer O.A., Tilson H.A., Byrd W.C., Riley M.T. A method for the routine assessment of fore- and hindlimb grip strength of rats and mice. Neurobehav Toxicol 1979, 1:233-236.
44. Miller M.F., Chernyak S.M., Domino S.E., Batterman S.A., Loch-Caruso R. Concentrations and speciation of polybrominated diphenyl ethers in human amniotic fluid. Sci Total Environ 2012, 417-418:294-298.
45. Park J.S., She J., Holden A., Sharp M., Gephart R., Souders-Mason G., et al. High postnatal exposures to polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) via breast milk in California: does BDE-209 transfer to breast milk?. Environ Sci Technol 2011, 45:4579-4585.
46. Patil S.S., Sunyer B., Hoger H., Lubec G. Evaluation of spatial memory of C57BL/6J and CD1 mice in the Barnes maze, the multiple T-maze and in the Morris water maze. Behav Brain Res 2009, 198:58-68.
47. Pelletier C., Imbeault P., Tremblay A. Energy balance and pollution by organochlorines and polychlorinated biphenyls. Obes Rev 2003, 4:17-24.
48. Perez-Maldonado I.N., Ramirez-Jimenez Mdel R., Martinez-Arevalo L.P., Lopez-Guzman O.D., Athanasiadou M., Bergman A., et al. Exposure assessment of polybrominated diphenyl ethers (PBDEs) in Mexican children. Chemosphere 2009, 75:1215-1220.
49. Ramirez M.C., Luque G.M., Ornstein A.M., Becu-Villalobos D. Differential neonatal testosterone imprinting of GH-dependent liver proteins and genes in female mice. J Endocrinol 2010, 207:301-308.
50. 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.
51. Sanders J.M., Chen L.J., Lebetkin E.H., Burka L.T. Metabolism and disposition of 2,2',4,4'-tetrabromodiphenyl ether following administration of single or multiple doses to rats and mice. Xenobiotica 2006, 36:103-117.
52. Schecter A., Papke O., Tung K.C., Staskal D., Birnbaum L. Polybrominated diphenyl ethers contamination of United States food. Environ Sci Technol 2004, 38:5306-5311.
53. Schecter A., Haffner D., Colacino J., Patel K., Papke O., Opel M., et al. Polybrominated diphenyl ethers (PBDEs) and hexabromocyclodecane (HBCD) in composite U.S. food samples. Environ Health Perspect 2009, 118:357-362.
54. Shy C.G., Huang H.L., Chang-Chien G.P., Chao H.R., Tsou T.C. Neurodevelopment of infants with prenatal exposure to polybrominated diphenyl ethers. Bull Environ Contam Toxicol 2011, 87:643-648.
55. Staskal D.F., Diliberto J.J., DeVito M.J., Birnbaum L.S. Toxicokinetics of BDE 47 in female mice: effect of dose, route of exposure, and time. Toxicol Sci 2005, 83:215-223.
56. Staskal D.F., Diliberto J.J., Birnbaum L.S. Disposition of BDE 47 in developing mice. Toxicol Sci 2006, 90:309-316.
57. Staskal D.F., Diliberto J.J., Birnbaum L.S. Impact of repeated exposure on the toxicokinetics of BDE 47 in mice. Toxicol Sci 2006, 89:380-385.
58. Staskal D.F., Hakk H., Bauer D., Diliberto J.J., Birnbaum L.S. Toxicokinetics of polybrominated diphenyl ether congeners 47, 99, 100, and 153 in mice. Toxicol Sci 2006, 94:28-37.
59. Suvorov A., Takser L. Facing the challenge of data transfer from animal models to humans: the case of persistent organohalogens. Environ Health 2008, 7:58.
60. Suvorov A., Girard S., Lachapelle S., Abdelouahab N., Sebire G., Takser L. Perinatal exposure to low-dose BDE-47, an emergent environmental contaminant, causes hyperactivity in rat offspring. Neonatology 2009, 95:203-209.
61. Ta T.A., Koenig C.M., Golub M.S., Pessah I.N., Qi L., Aronov P.A., et al. Bioaccumulation and behavioral effects of 2,2',4,4'-tetrabromodiphenyl ether (BDE-47) in perinatally exposed mice. Neurotoxicol Teratol 2011, 33:393-404.
62. Thomsen C., Lundanes E., Becher G. Brominated flame retardants in archived serum samples from Norway: a study on temporal trends and the role of age. Environ Sci Technol 2002, 36:1414-1418.
63. Toms L.M., Harden F.A., Symons R.K., Burniston D., Furst P., Muller J.F. Polybrominated diphenyl ethers (PBDEs) in human milk from Australia. Chemosphere 2007, 68:797-803.
64. UNEP Commercial pentabromodiphenyl ether: risk management evaluation, Stockholm Convention on Persistent Organic Pollutants: Persistent Organic Pollutants Review Committee. Third meeting UNEP/POPS/POPRC3/20, Addendum1, Geneva 2007.
65. U.S.EPA Toxicological review of 2,2'4,4' tetrabromodiphenyl ether (BDE-47) 2008, U.S. Environmental Protection Agency, Washington, DC.
66. 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.
67. 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.
68. Viberg H., Fredriksson A., Eriksson P. Investigations of strain and/or gender differences in developmental neurotoxic effects of polybrominated diphenyl ethers in mice. Toxicol Sci 2004, 81:344-353.
69. Viberg H., Johansson N., Fredriksson A., Eriksson J., Marsh G., Eriksson P. Neonatal exposure to higher brominated diphenyl ethers, hepta-, octa-, or nonabromodiphenyl ether, impairs spontaneous behavior and learning and memory functions of adult mice. Toxicol Sci 2006, 92:211-218.
70. 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. Neurotoxicology 2007, 28:136-142.
71. Viberg H., Mundy W., Eriksson P. Neonatal exposure to decabrominated diphenyl ether (PBDE 209) results in changes in BDNF, CaMKII and GAP-43, biochemical substrates of neuronal survival, growth, and synaptogenesis. Neurotoxicology 2008, 29:152-159.
72. Zhang X., Diamond M.L., Ibarra C., Harrad S. Multimedia modeling of polybrominated diphenyl ether emissions and fate indoors. Environ Sci Technol 2009, 43:2845-2850.
73. Zhou Y., Rui L. Major urinary protein regulation of chemical communication and nutrient metabolism. Vitam Horm 2010, 83:151-163.
74. Zhu L., Ma B., Li J., Wu Y., Gong J. Distribution of polybrominated diphenyl ethers in breast milk from North China: implication of exposure pathways. Chemosphere 2009, 74:1429-1434.
75. Zota A.R., Park J.S., Wang Y., Petreas M., Zoeller R.T., Woodruff T.J. Polybrominated diphenyl ethers, hydroxylated polybrominated diphenyl ethers, and measures of thyroid function in second trimester pregnant women in California. Environ Sci Technol 2011, 45:7896-7905.
76. Zuurbier M., Leijs M., Schoeters G., ten Tusscher G., Koppe J.G. Children's exposure to polybrominated diphenyl ethers. Acta Paediatr Suppl 2006, 95:65-70.