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

Volumn 29, Issue 1, 2008, Pages 152-159

  Viberg, Henrik ^a   Mundy, William ^b   Eriksson, Per ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

BDNF; CaMKII; Decabrominated diphenyl ether; Flame retardants; GAP 43; Neonatal; Neurotoxicity; PBDE 209

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN PROTEIN; DECABROMINATED DIPHENYL ETHER; DIPHENYL ETHER; NEUROMODULIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN CORTEX; BRAIN LEVEL; BRAIN REGION; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENZYME LINKED IMMUNOSORBENT ASSAY; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NEUROTOXICITY; NEWBORN PERIOD; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; SYNAPTOGENESIS;

AGE FACTORS; ANIMALS; BRAIN; BRAIN CHEMISTRY; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL SURVIVAL; FEMALE; GAP-43 PROTEIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; NERVE TISSUE PROTEINS; NEURONS; PHENYL ETHERS; POLYBROMINATED BIPHENYLS; PREGNANCY; SYNAPSES;

ANIMALIA; MAMMALIA; MUS; RATTUS;

EID: 37849008239     PISSN: 0161813X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuro.2007.10.007     Document Type: Article

References (71)

1. Ahlbom J., Fredriksson A., and Eriksson P. Neonatal exposure to a type-I pyrethroid (bioallethrin) induces dose-response changes in brain muscarinic receptors and behaviour in neonatal and adult mice. Brain Res 645 (1994) 318-324
2. Ahlbom J., Fredriksson A., and Eriksson P. Exposure to an organophosphate (DFP) during a defined period in neonatal life induces permanent changes in brain muscarinic receptors and behaviour in adult mice. Brain Res 677 (1995) 13-19
3. Aziz M.H., Agrawal A.K., Adhami V.M., Ali M.M., Baig M.A., and Seth P.K. Methanol-induced neurotoxicity in pups exposed during lactation through mother: role of folic acid. Neurotoxicol Teratol 24 (2002) 519-527
4. Bolles R.C., and Woods P.J. The ontogeny of behaviour in the albino rat. Anim Behav 12 (1964) 427-441
5. Campbell B.A., Lytle L.D., and Fibiger H.C. Ontogeny of adrenergic arousal and cholinergic inhibitory mechanisms in the rat. Science 166 (1969) 635-637
6. Casoli T., Spagna C., Fattoretti P., Gesuita R., and Bertoni-Freddari C. Neuronal plasticity in aging: a quantitative immunohistochemical study of GAP-43 distribution in discrete regions of the rat brain. Brain Res 714 (1996) 111-117
7. Climent E., Pascual M., Renau-Piqueras J., and Guerri C. Ethanol exposure enhances cell death in the developing cerebral cortex: role of brain-derived neurotrophic factor and its signaling pathways. J Neurosci Res 68 (2002) 213-225
8. Coyle J.T., and Yamamura H.I. Neurochemical aspects of the ontogenesis of cholinergic neurons in the rat brain. Brain Res 118 (1976) 429-440
9. Cui Q. Actions of neurotrophic factors and their signaling pathways in neuronal survival and axonal regeneration. Mol Neurobiol 33 (2006) 155-179
10. Das K.P., Chao S.L., White L.D., Haines W.T., Harry G.J., Tilson H.A., et al. Differential patterns of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 mRNA and protein levels in developing regions of rat brain. Neuroscience 103 (2001) 739-761
11. Davison A.N., and Dobbing J. Applied neurochemistry (1968), Blackwell, Oxford p. 178-221, 253-316
12. 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 115 (2007) 865-870
13. Eriksson P. Developmental neurotoxicity of environmental agents in the neonate. Neurotoxicology 18 (1997) 719-726
14. Eriksson P. Perinatal developmental neurotoxicity of PCBs (1998), Swedish Environmental Protection Agency, Stockholm p. 56
15. Eriksson P., Ahlbom J., and Fredriksson A. Exposure to DDT during a defined period in neonatal life induces permanent changes in brain muscarinic receptors and behaviour in adult mice. Brain Res 582 (1992) 277-281
16. Eriksson P., Ankarberg E., and Fredriksson A. Exposure to nicotine during a defined period in neonatal life induces permanent changes in brain nicotinic receptors and in behaviour of adult mice. Brain Res 853 (2000) 41-48
17. Eriksson P., Jakobsson E., and Fredriksson A. Brominated flame retardants: a novel class of developmental neurotoxicants in our environment?. Environ Health Perspect 109 (2001) 903-908
18. Eriksson P., Viberg H., Jakobsson E., Orn U., and 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 67 (2002) 98-103
19. Erondu N.E., and Kennedy M.B. Regional distribution of type II Ca2+/calmodulin-dependent protein kinase in rat brain. J Neurosci 5 (1985) 3270-3277
20. Fibiger H.C., Damsma G., and Day J.C. Behavioral pharmacology and biochemistry of central cholinergic neurotransmission. Adv Exp Med Biol 295 (1991) 399-414
21. Fiedler E.P., Marks M.J., and Collins A.C. Postnatal development of cholinergic enzymes and receptors in mouse brain. J Neurochem 49 (1987) 983-990
22. Frankland P.W., O'Brien C., Ohno M., Kirkwood A., and Silva A.J. Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 411 (2001) 309-313
23. Garcia C.I., Paez P., Soto E.F., and Pasquini J.M. Differential effects of apotransferrin on two populations of oligodendroglial cells. Glia 42 (2003) 406-416
24. Glowinski J., and Iversen L.L. Regional studies of catecholamines in the rat brain. I. The disposition of [3H]norepinephrine, [3H]dopamine and [3H]dopa in various regions of the brain. J Neurochem 13 (1966) 655-669
25. Heist E.K., and Schulman H. The role of Ca2+/calmodulin-dependent protein kinases within the nucleus. Cell Calcium 23 (1998) 103-114
26. Hughes P.E., Alexi T., Walton M., Williams C.E., Dragunow M., Clark R.G., et al. Activity and injury-dependent expression of inducible transcription factors, growth factors and apoptosis-related genes within the central nervous system. Prog Neurobiol 57 (1999) 421-450
27. Hutzinger O., Sundström G., and Safe S. Environmental chemistry of flame retardants. Part I. Introduction and principles. Chemosphere 1 (1976) 3-10
28. Hutzinger O., and Thoma H. Polybrominated dibenzo-p-dioxins and dibenzofurans: the flame retardant issue. Chemosphere 16 (1987) 1877-1880
29. Jacobson R.D., Virag I., and Skene J.H. A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. J Neurosci 6 (1986) 1843-1855
30. Jones-Otazo H.A., Clarke J.P., Diamond M.L., Archbold J.A., Ferguson G., Harner T., et al. Is house dust the missing exposure pathway for PBDEs? An analysis of the urban fate and human exposure to PBDEs. Environ Sci Technol 39 (2005) 5121-5130
31. Kazama H., Morimoto-Tanifuji T., and Nose A. Postsynaptic activation of calcium/calmodulin-dependent protein kinase II promotes coordinated pre- and postsynaptic maturation of Drosophila neuromuscular junctions. Neuroscience 117 (2003) 615-625
32. Kazama H., Nose A., and Morimoto-Tanifuji T. Synaptic components necessary for retrograde signaling triggered by calcium/calmodulin-dependent protein kinase II during synaptogenesis. Neuroscience 145 (2007) 1007-1015
33. Keller W.C., and Yeary R.A. A comparison of the effects of mineral oil, vegetable oil and sodium sulfate on the intestinal absorption of DDT in rodents. Clin Toxicol 16 (1980) 223-231
34. Kelly P.T., Shields S., Conway K., Yip R., and Burgin K. Developmental changes in calmodulin-kinase II activity at brain synaptic junctions: alterations in holoenzyme composition. J Neurochem 49 (1987) 1927-1940
35. Kierstein G., Obst K., and Wahle P. Development and activity-dependent expression of neuronal marker proteins in organotypic cultures of rat visual cortex. Brain Res Dev Brain Res 92 (1996) 39-48
36. Kobayashi K., Tsuji R., Yoshioka T., Kushida M., Yabushita S., Sasaki M., et al. Effects of hypothyroidism induced by perinatal exposure to PTU on rat behavior and synaptic gene expression. Toxicology 212 (2005) 135-147
37. Kolb B., and Whishaw I.Q. Plasticity in the neocortex: mechanisms underlying recovery from early brain damage. Prog Neurobiol 32 (1989) 235-276
38. Kuhar M.J., Birdsall N.J.M., Burgen A.S.V., and Hulme E.C. Ontogeny of muscarinic receptors in rat brain. Brain Res 184 (1980) 375-383
39. Lessmann V., Gottmann K., and Malcangio M. Neurotrophin secretion: current facts and future prospects. Prog Neurobiol 69 (2003) 341-374
40. Lisman J.E., and Goldring M.A. Feasibility of long-term storage of graded information by the Ca2+/calmodulin-dependent protein kinase molecules of the postsynaptic density. Proc Natl Acad Sci USA 85 (1988) 5320-5324
41. Lustig R.H., Hua P., Wilson M.C., and Federoff H.J. Ontogeny, sex dimorphism, and neonatal sex hormone determination of synapse-associated messenger RNAs in rat brain. Brain Res Mol Brain Res 20 (1993) 101-110
42. Meironyté D., Norén K., and Bergman A. Analysis of polybrominated diphenyl ethers in Swedish human milk. a time dependent trend study, 1972-1997. J Toxicol Environ Health A 58 (1999) 329-341
43. Nawa H., Carnahan J., and Gall C. BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: partial disagreement with mRNA levels. Eur J Neurosci 7 (1995) 1527-1535
44. Newhouse P.A., Potter A., Corwin J., and Lenox R. Acute nicotinic blockade produces cognitive impairment in normal humans. Psychopharmacol Berl 108 (1992) 480-484
45. O'Callaghan J.P., and Miller D.B. Acute exposure of the neonatal rat to tributyltin results in decreases in biochemical indicators of synaptogenesis and myelinogenesis. J Pharmacol Exp Ther 246 (1988) 394-402
46. O'Callaghan J.P., and Miller D.B. Acute exposure of the neonatal rat to triethyltin results in persistent changes in neurotypic and gliotypic proteins. J Pharmacol Exp Ther 244 (1988) 368-378
47. Oestreicher A.B., De Graan P.N., Gispen W.H., Verhaagen J., and Schrama L.H. B-50, the growth associated protein-43: modulation of cell morphology and communication in the nervous system. Prog Neurobiol 53 (1997) 627-686
48. Oestreicher A.B., and Gispen W.H. Comparison of the immunocytochemical distribution of the phosphoprotein B-50 in the cerebellum and hippocampus of immature and adult rat brain. Brain Res 375 (1986) 267-279
49. Ohta S., Ishizuka D., Nishimura H., Nakao T., Aozasa O., Shimidzu Y., et al. Comparison of polybrominated diphenyl ethers in fish, vegetables, and meats and levels in human milk of nursing women in Japan. Chemosphere 46 (2002) 689-696
50. Palin K.J., Wilson C.G., Davis S.S., and Phillips A.J. The effects of oil on the lymphatic absorption of DDT. J Pharm Pharmacol 34 (1982) 707-710
51. Polli J.W., Patanow C.M., and Billingsley M.L. Developmental expression of neuronal calmodulin-binding proteins in rat brain. Brain Res Dev Brain Res 53 (1990) 62-70
52. Robinette B., and Mundy W.R. Ontogeny of proteins for use as biomarkers of developmental neurotoxicity. The Toxicologist 78 (2004) 1338
53. Rongo C., and Kaplan J.M. CaMKII regulates the density of central glutamatergic synapses in vivo. Nature 402 (1999) 195-199
54. Schecter A., Pavuk M., Papke O., Ryan J.J., Birnbaum L., and Rosen R. Polybrominated diphenyl ethers (PBDEs) in U.S. mothers' milk. Environ Health Perspect 111 (2003) 1723-1729
55. Shi Y., and Ethell I.M. Integrins control dendritic spine plasticity in hippocampal neurons through NMDA receptor and Ca2+/calmodulin-dependent protein kinase II-mediated actin reorganization. J Neurosci 26 (2006) 1813-1822
56. Shughrue P.J., and Dorsa D.M. The ontogeny of GAP-43 (neuromodulin) mRNA in postnatal rat brain: evidence for a sex dimorphism. J Comp Neurol 340 (1994) 174-184
57. Skene J.H. Axonal growth-associated proteins. Annu Rev Neurosci 12 (1989) 127-156
58. Sugiura H., and Yamauchi T. Developmental changes in the levels of Ca2+/calmodulin-dependent protein kinase II alpha and beta proteins in soluble and particulate fractions of the rat brain. Brain Res 593 (1992) 97-104
59. Webster M.J., Weickert C.S., Herman M.M., and Kleinman J.E. BDNF mRNA expression during postnatal development, maturation and aging of the human prefrontal cortex. Brain Res Dev Brain Res 139 (2002) 139-150
60. Viberg H., Fredriksson A., and 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 67 (2002) 104-107
61. Viberg H., Fredriksson A., and 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 192 (2003) 95-106
62. Viberg H., Fredriksson A., and Eriksson P. Investigations of strain and/or gender differences in developmental neurotoxic effects of polybrominated diphenyl ethers in mice. Toxicol Sci 81 (2004) 344-353
63. Viberg H., Fredriksson A., and 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 17 (2004) 61-65
64. Viberg H., Fredriksson A., and Eriksson P. Deranged spontaneous behaviour and decrease in cholinergic muscarinic receptors in hippocampus in the adult rat, after neonatal exposure to the brominated flame-retardant, 2,2′,4,4′,5-pentabromodiphenyl ether (PBDE 99). Environ Toxicol Pharmacol 20 (2005) 283
65. Viberg H., Fredriksson A., and 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 28 (2007) 136-142
66. Viberg H., Fredriksson A., Jakobsson E., Orn U., and Eriksson P. Neurobehavioral derangements in adult mice receiving decabrominated diphenyl ether (PBDE 209) during a defined period of neonatal brain development. Toxicol Sci 76 (2003) 112-120
67. Viberg H., Johansson N., Fredriksson A., Eriksson J., Marsh G., and 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 92 (2006) 211-218
68. WWF (2005). Generations X, p. 59. WWF DetoX Campaign, Brussels.
69. Xia Y.X., Ikeda T., Xia X.Y., and Ikenoue T. Differential neurotrophin levels in cerebrospinal fluid and their changes during development in newborn rat. Neurosci Lett 280 (2000) 220-222
70. Yamauchi T. Neuronal Ca2+/calmodulin-dependent protein kinase II-discovery, progress in a quarter of a century, and perspective: implication for learning and memory. Biol Pharm Bull 28 (2005) 1342-1354
71. Zou D.J., and Cline H.T. Postsynaptic calcium/calmodulin-dependent protein kinase II is required to limit elaboration of presynaptic and postsynaptic neuronal arbors. J Neurosci 19 (1999) 8909-8918