In Vitro Effects of Environmentally Relevant Polybrominated Diphenyl Ether (PBDE) Congeners on Calcium Buffering Mechanisms in Rat Brain
Tóm tắt
Polybrominated diphenyl ethers (PBDEs) are widely used as additive flame-retardants and have been detected in human blood, adipose tissue, and breast milk. Developmental and long-term exposures to these chemicals may pose a human health risk, especially to children. We have previously demonstrated that polychlorinated biphenyls (PCBs), which are structurally similar to PBDEs and cause neurotoxicity, perturb intracellular signaling events including calcium homeostasis and protein kinase C translocation, which are critical for neuronal function and development of the nervous system. The objective of the present study was to test whether environmentally relevant PBDE congeners 47 and 99 are also capable of disrupting Ca2 + homeostasis. Calcium buffering was determined by measuring 45Ca2 + -uptake by microsomes and mitochondria, isolated from adult male rat brain (frontal cortex, cerebellum, hippocampus, and hypothalamus). Results show that PBDEs 47 and 99 inhibit both microsomal and mitochondrial 45Ca2 + -uptake in a concentration-dependent manner. The effect of these congeners on 45Ca2 + -uptake is similar in all four brain regions though the hypothalamus seems to be slightly more sensitive. Among the two preparations, the congeners inhibited 45Ca2 + -uptake in mitochondria to a greater extent than in microsomes. These results indicate that PBDE 47 and PBDE 99 congeners perturb calcium signaling in rat brain in a manner similar to PCB congeners, suggesting a common mode of action of these persistent organic pollutants.
Tài liệu tham khảo
Kodavanti P (2005) Neurotoxicity of persistent organic pollutants: possible mode(s) of action and further considerations. Dose Response 3:273–305
Lang V (1992) Polychlorinated biphenyls in the environment. J Chromatogr 595:1–43
Hale R, Alaee M, Manchester-Neesvig J, Stapleton H, Ikonomou M (2003) Polybrominated diphenyl ether flame retardants in the North American environment. Env Int 29:771–779
Hale R, LaGuardia M, Harvey E, Gaylor M, Mainor T (2006) Brominated flame retardant concentrations and trends in abiotic media. Chemosphere 64:181–186
Wilford B, Shoeib M, Harner T, Zhu J, Jones K (2005) Polybrominated diphenyl ethers in indoor dust in Ottawa, Canada: implications for sources and exposure. Environ Sci Technol 39:7027–7035
Gill U, Chu I, Ryan J, Feeley M (2004) Polybrominated diphenyl ethers: human tissue levels and toxicology. Rev Environ Contam Toxicol 183:55–97
Hites R (2004) Polybrominated diphenyl ethers in the environment and in people: a meta-analysis of concentrations. Environ Sci Technol 38:945–956
Petreas M, She J, Brown F, Winkler J, Windham G, Rogers E, Zhao G, Bhatia R, Charles M (2003) High body burdens of 2,2′,4,4′-tetrabromobiphenyl ether (BDE-47) in California women. Environ Health Perspect 111:A480–481
McDonald T (2005) Polybrominated diphenyl ether levels among United States residents: daily intake and risk of harm to the developing brain and reproductive organs. Integr Environ Assess Manag 1:343–354
LaGuardia M, Hale R, Harvey E (2006) Detailed polybrominated diphenyl ether (PBDE) congener composition of the widely used Penta-, Octa-, and Deca-PBDE technical flame-retardant mixtures. Environ Sci Technol 40:6247–6254
Schecter A, Papke O, Tung K, Joseph J, Harris T, 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
Julander A, Karlsson M, Hagstrom K, Ohlson C, Engwall M, Bryngelsson I, Westberg H, vanBavel B (2005) Polybrominated diphenyl ethers—plasma levels and thyroid status of workers at an electronic recycling facility. Int Arch Occup Environ Health 78:584–592
Schecter A, Johnson-Welch S, Tung K, Harris T, Papke O, Rosen R (2007) Polybrominated diphenyl ether (PBDE) levels in livers of US human fetuses and newborns. J Toxicol and Env Health 70:1–6
Schecter A, Papke O, Tung K, Staskal D, Birnbaum L (2004) Polybrominated diphenyl ethers contamination of United States food. Environ Sci Technol 38:5306–5311
Dufault C, Poles G, Driscoll L (2005) Brief postnatal PBDE exposure alters learning and the cholinergic modulation of attention in rats. Toxicol Sci 88:172–180
Eriksson P, Jakobsson E, Fredriksson A (2001) Brominated flame retardants: a novel class of developmental neurotoxicants in our environments? Environ Health Perspect 109:903–908
Viberg H, Fredriksson A, Eriksson P (2003) Neonatal exposure to PBDE 153 disrupts spontaneous behavior, impairs learning and memory, and decreases hippocampal cholinergic receptors in adult mice. Toxicol Appl Pharmacol 192:95–106
Viberg H, Johansson N, Fredriksson A, Eriksson J, Marsh G, Eriksson P (2006) Neonatal exposure to higher brominated diphenyl ethers, hepta-, octa-, or nonabromodiphenyl ether, impairs spontaneous behavior and learning and memory functions in adult mice. Toxicol Sci 92:211–218
Kuriyama S, Talsness C, Grote K, Chahoud I (2005) Developmental exposure to low dose PBD 99: effects on male fertility and neurobehavior in rat offspring. Environ Health Perspect 113:149–54
Branchi I, Capone F, Alleva E, Costa L (2003) Polybrominated diphenyl ethers: neurobehavioral effects following developmental exposure. Neurotoxicology 24:449–462
Hallgren S, Darnerud P (2002) Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) and chlorinated paraffins (CPs) in rats-testing interactions and mechanisms for thyroid hormone effects. Toxicology 177:227–243
Zhou T, Taylor M, Devito M, Crofton K (2002) Developmental exposure to polybrominated diphenyl ethers results in thyroid hormone disruption. Toxicol Sci 66:105–116
Kodavanti P, Ward T (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
Kodavanti P, Ward T, Ludewig G, Robertson L, Birnbaum L (2005) Polybrominated diphenyl ether (PBDE) effects in rat neuronal cultures: 14C-PBDE accumulation, biological effects, and structure-activity relationships. Toxicol Sci 88:181–192
Abeliovich A, Paylor R, Chen C, Kim J, Wehner J, Tonegawa S (1993) PKC-gamma mutant mice exhibit mild deficit in spatial and contextual learning. Cell 75:1263–1271
Chen S, Sweatt J, Klann E (1997) Enhanced phosphorylation of the postsynaptic protein kinase C substrate RC3/neurogranin during long-term potentiation. Brain Res 749:181–187
Girard P, Kuo J (1990) Protein kinase C and its 80-kilodalton substrate protein in neuroblastoma cell neurite outgrowth. J Neurochem 54:300–306
Kater S, Mills L (1991) Regulation of growth cone behavior by calcium. J Neurosci 11:891–899
Murphy S, McCabe N, Morrow C, Pearce B (1987) Phorbol ester stimulates proliferation of astrocytes in primary cultures. Brain Res 428:133–135
Curtis J, Finkbeiner S (1999) Sending signals from the synapse to the nucleus: possible roles for CaMK, Ras/ERK, and SAPK pathways in the regulation of synaptic plasticity and neuronal growth. J Neurosci Res 58:88–95
Mariussen E, Fonnum F (2006) Neurochemical targets and behavioral effects of organohalogen compounds: an update. Crit Reviews in Toxicol 36:253–289
Berridge M (1998) Neuronal calcium signaling. Neuron 21:13–26
Gray E, Whittaker V (1962) The isolation of nerve endings from brain: an electron microscope study of cell fragments derived by homogenization and centrifugation. J Anat (Lond) 96:79–88
Dodd P, Hardy J, Oakley A, Edwardson J, Perry E, Delaunoy J (1981) A rapid method for preparing synaptosomes: comparison with alternate procedures. Brain Res 226:107–118
Kodavanti P, Mundy W, Tilson H, Harry G (1993) Effects of selected neuroactive chemicals on calcium transporting systems in rat cerebellum and on survival of cerebellar granule cells. Fundam Appl Toxicol 21:308–316
Kodavanti P, Shin D, Tilson H, Harry G (1993) Comparative effects of two polychlorinated biphenyl congeners on Ca2+-homeostasis in rat cerebellar granule cells. Toxicol Appl Pharmacol 123:97–106
Lowry O, Rosebrough N, Farr A, Randall R (1951) Protein measurement with folin-phenol reagent. J Biol Chem 193:265–275
Moore L, Chen T, Knapp H, Landon E (1975) Energy dependent calcium sequestration activity in rat liver microsomes. J Biol Chem 250:4562–4568
Sharma R, Derr-Yellin E, House D, Kodavanti P (2000) Age-dependent effects of Aroclor 1254 on calcium uptake by subcellular organelles in selected brain regions of rats. Toxicology 156:13–25
Kodavanti P, Ward T, Derr-Yellin E, McKinney J, Tilson H (2003) Increased [3H]phorbol ester binding in rat cerebellar granule cells and inhibition of 45Ca2+ buffering in rat cerebellum by hydroxylated polychlorinated biphenyls. Neurotoxicology 24:187–98
Tilson H, Kodavanti P, Mundy W, Bushnell P (1998) Neurotoxicity of environmental chemicals and their mechanism of action. Toxicol Lett 28:631–635
Noren K, Meironyte D (2000) Certain organochlorine and organobromine contaminants in Swedish milk in perspective of last 20–30 years. Chemosphere 40:1111–1123
Rayne S, Ikonomou M, Antcliffe B (2003) Rapidly increasing polybrominated diphenyl ether concentrations in the Columbia River system from 1992 to 2000. Environ Sci Technol 37:2847–2854
Stoker T, Cooper R, Lambright C, Wilson V, Furr J, Gray L (2005) In vivo and in vitro anti-androgenic effects of DE-71, a commercial polybrominated diphenyl ether (PBDE) mixture. Toxicol Sci 207:78–88
Stoker T, Laws S, Crofton K, Hedge J, Ferrell J, Cooper R (2004) Assessment of DE-71, a commercial polybrominated diphenyl ether (PBDE) mixture, in the EDSP male and female pubertal protocols. Toxicol Sci 78:144–155
Lilienthal H, Hack A, Roth-Harer A, Grande S, Talsness C (2006) 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 Perspect 114:194–201
Berridge M, Bootman M, Lipp P (1998) Calcium—a life and death signal. Nature 395:645–648
Zacharias D, DeMarco S, Strehler E (1997) mRNA expression of the four isoforms of the human plasma membrane Ca(2+)-ATPase in the human hippocampus. Brain Res Mol Brain Res 45:173–176
Voie OA, Fonnum F (2000) Effect of polychlorinated biphenyls on production of reactive oxygen species (ROS) in rat synaptosomes. Arch Toxicol 73:588–593
Mariussen E, Fonnum F (2001) The effect of polychlorinated biphenyls on the high affinity uptake of the neurotransmitters, dopamine, seratonin, glutamate, and GABA, into rat brain synaptosomes. Toxicology 159:11–21
Johnson-Restrepo B, Kannan K, Rapaport D, Rodan B (2005) Polybrominated diphenyl ethers and polychlorinated biphenyls in Human adipose tissue from New York. Environ Sci Technol 39:5177–5182
Fischer D, Hooper K, Athanasiadou M, Athanassiadis I, Bergman A (2006) Children show highest levels of polybrominated diphenyl ethers in a California family of four: a case study. Environ Health Perspect 114:1581–1584
Reistad T, Fonnum F, Mariussen E (2006) Neurotoxicity of the pentabrominated diphenyl ether mixture, DE-71, and hexabromocyclododecane (HBCD) in rat cerebellar granule cells in vitro. Arch Toxicol 80:785–796
Staskal D, Hakk H, Bauer D, Diliberto J, Birnbaum L (2006) Toxicokinetics of polybrominated diphenyl ether congeners 47, 99, 100, and 153 in mice. Toxicol Sci 94:28–37
Berridge M (1987) Inositol lipids and cell proliferation. Biochim Biophys Acta 907:33–45
Borle A (1981) Control, modulation and regulation of cell calcium. Rev Physiol Biochem Pharmacol 90:13–153
Carafoli E (1987) Intracellular calcium homeostasis. Annu Rev Biochem 56:395–433
Tan Y, Li D, Song R, Lawrence D, Carpenter D (2003) Ortho-Substituted PCBs kill thymocytes. Toxicol Sci 76:328–337
Tan Y, Chen C-H, Lawrence D, Carpenter D (2004) Ortho-Substituted PCBs kill cells by altering membrane structure. Toxicol Sci 80:54–59
Zacharias D, Dalrymple S, Strehler E (1995) Transcript distribution of plasma membrane Ca2+ pump isoforms and splice variants in the human brain. Brain Res Mol Brain Res 28:263–272
Burk S, Lyton J, MacLennan D, Shull G (1989) cDNA cloning, functional expression and mRNA tissue distribution of a third organellar Ca2+ pump. J Biol Chem 264:561–568
Rio Ed, Nicholls D, Downes C (1994) Involvement of calcium influx in muscarinic cholinergic regulation of phospholipase C in cerebellar granule cells. J Neurochem 63:535–543
Shafer T, Mundy W, Tilson H, Kodavanti P (1996) Disruption of inositol phosphate accumulation in cerebellar granule cells by polychlorinated biphenyls: a consequence of altered Ca2+ homeostasis. Toxicol Appl Pharmacol 141:448–455
Magi S, Castaldo P, Carrieri G, Scorziello A, DiRenzo G, Amoroso S (2005) Involvement of Na+-Ca2+ exchanger in intracellular Ca2+ increase and neuronal injury induced by polychlorinated biphenyls in human neuroblastoma SH-SY5Y cells. J Pharmacol Exp Ther 315:291–296
Inglefield J, Mundy W, Schafer T (2001) Inositol 1,4,5-triphosphate receptor-sensitive Ca(2+) release, store-operated Ca(2+) entry, and cAMP responsive element binding protein phosphorylation in developing cortical cells following exposure to polychlorinated biphenyls. J Pharmacol Exp Ther 297:762–773
Costa L, Guizzetti M, Lu H, Bordi F, Vitalone A, Tita B, Palmery M, Valeri P, Silvestrini B (2001) Intracellular signal transduction pathways as targets for neurotoxicants. Toxicology 160:19–26
Coburn C, Gillard E, Curras-Collazo M (2005) Dietary exposure to Aroclor 1254 alters central and peripheral vasopressin release in response to dehydration in the rat. Toxicol Sci 84:149–156
Coburn C, Curras-Collazo M, Kodavanti P (2007) Polybrominated diphenyl ethers (PBDEs) and ortho-substituted polychlorinated biphenyls (PCBs) as neuroendocrine disruptors of vasopressin release: effects during physiological activation in vitro and structure/activity relationships. Toxicol Sci 98:178–186
Ludwig M, Bull P, Toblin V, Sabatier N, Landgraf R, Dayanithi G, Leng G (2005) Regulation of activity-dependent dendritic vasopressin release from rat supraoptic neurones. J Physiol 564:515–522
Sabatier N, Shibuya I, Dayanithi G (2004) Intracellular calcium increase and somatodendritic vasopressin release by vasopressin receptor antagonists in the rat supraoptic nucleus: Involvement of multiple intracellular transduction signals. J Neuroendcrinol 16:221–236