Article pubs.acs.org/est
Selenomethionine Protects against Neuronal Degeneration by Methylmercury in the Developing Rat Cerebrum Mineshi Sakamoto,†,* Akira Yasutake,† Akiyoshi Kakita,‡ Masae Ryufuku,‡ Hing Man Chan,§ Megumi Yamamoto,† Sanae Oumi,∥ Sayaka Kobayashi,∥ and Chiho Watanabe∥ †
National Institute for Minamata Disease, Minamata, Kumamoto 867-0008, Japan Brain Research Institute, Niigata University, Asahimachi, Niigata 951-8122, Japan § University of Ottawa, Ottawa ON K1N 6N5, Canada ∥ University of Tokyo, Bunkyo-ku, Tokyo 113-8656, Japan ‡
ABSTRACT: Although many experimental studies have shown that selenium protects against methylmercury (MeHg) toxicity at different end points, the direct interactive effects of selenium and MeHg on neurons in the brain remain unknown. Our goal is to confirm the protective effects of selenium against neuronal degeneration induced by MeHg in the developing postnatal rat brain using a postnatal rat model that is suitable for extrapolating the effects of MeHg to the fetal brain of humans. As an exposure source of selenium, we used selenomethionine (SeMet), a food-originated selenium. Wistar rats of postnatal days 14 were orally administered with vehicle (control), MeHg (8 mg Hg/kg/day), SeMet (2 mg Se/kg/day), or MeHg plus SeMet coexposure for 10 consecutive days. Neuronal degeneration and reactive astrocytosis were observed in the cerebral cortex of the MeHg-group but the symptoms were prevented by coexposure to SeMet. These findings serve as a proof that dietary selenium can directly protect neurons against MeHg toxicity in the mammalian brain, especially in the developing cerebrum.
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INTRODUCTION Mercury is a naturally existing element throughout the environment. It is mainly released as Hg0 into the atmosphere from natural and anthropogenic sources. A recent study indicated that human activity contributes about 50−70% of the total emission into the environment making it a large contributor to the global mercury cycle.1 Hg0 emitted into the atmosphere is oxidized and transformed into Hg2+. Subsequently, it is changed to methylmercury (MeHg) mainly by aquatic bacteria and enters the aquatic food chain. MeHg is readily absorbed by the digestive tract in humans and enters the central nervous system after passing through the blood−brain barrier leading to degeneration and dysfunction of nerve cells.2,3 In MeHg pollution epidemics in Minamata, more than 20 infants were congenitally affected by MeHg, and the typical fetal-type Minamata disease patients had a severe cerebral palsylike syndrome, whereas their mothers had mild or no manifestations of poisoning.4 Historically, the occurrence of fetal-type Minamata disease was the landmark epidemic that brought worldwide attention to the high risk. In the natural course of events, most human exposure to MeHg occurs through consumption of fish and sea mammals. Therefore, the effects of MeHg exposure on pregnant women, especially those who frequently consume seafood, remain to be elucidated. The Governing Council of the United Nations Environment Programme (UNEP) started the global mercury assessment in 2003 and agreed to develop a global legally binding © 2013 American Chemical Society
instrument on mercury on January 2013 for the global control of mercury pollution. Selenium is an essential element that plays a role as a component of antioxidative enzymes, such as glutathione peroxidase and thioredoxin reductase. It is also well-known that selenium counteracts the toxicity of MeHg at different end points, such as survival and/or weight loss,5,6 hind limb crossing,7,8 neurodevelopment and neurobehavioral deficits,9−11 and degeneration of peripheral nerves.12,13 However, the direct protective effects of selenium against MeHg-induced neuronal degeneration in the developing brain, especially in the cerebrum, have not been proven. Dietary selenium can exist in multiple forms, for example selenomethionine (SeMet) and selenocysteine. In this study, we selected SeMet as an exposure source of selenium because it is a natural form of selenium that exists in fish14,15 and was reported to be less toxic than inorganic forms of selenium such as sodium selenite or sodium selenate.16,17 SeMet also shows higher intestinal absorption and brain accumulation than inorganic selenium.18−20 Several human and animal studies have indicated that the developing brain in its prenatal and early postnatal stages is at the highest risk for MeHg exposure. Although the results of the Received: Revised: Accepted: Published: 2862
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mercury determinations in tissue samples, DORM-2 (Dog fish muscle, National Research Council, Canada) was measured, and obtained results fell within the certified range of 4.64 ± 0.26 μg/g. The inorganic mercury portion in each tissue was determined using the method described by Yasutake and Hirayama.25 The selenium concentrations were measured using an inductively coupled plasma mass spectrometer equipped with a collision cell (Agilent 7500ce; Agilent Technologies). As the reference material of selenium determinations in tissue samples, NIST 1577b (Bovine Liver, Gainsberg, USA) was measured, and the obtained results fell within the certified rage of 0.73 ± 0.06 μg/g. The total bilirubin (T-Bil), alanine aminotransferase (ALT), and aspartate aminotransferase (AST) values in plasma samples were analyzed using a conventional method by SRL Inc. (Tokyo, Japan). For total glutathione (GSH) analysis, aliquots of tissue samples (0.05−0.1 g) were immediately homogenized in ice-cold 4% perchloric acid containing 1 mM EDTA (0.5 mL). After centrifugation (12 000 rpm, 1 min), the supernatants were analyzed for their GSH concentrations by an enzymatic recycling method.26 GSH-Px activity was determined by the NADPH oxidation rate27 using the tissue homogenates in phosphate buffer, with cumene hydroperoxide as a substrate. To evaluate plasma hydroperoxide concentrations, the N,N-diethylparaphenylendiamine reactive oxygen metabolites (d-ROM) were measured using a FREE Carpe Diem (Diacron International srl) according to previous study.28 Histopathologically, coronal sections were taken of the following three brain levels: frontal cortex/striatum, hippocampus/mesencephalon, and occipital cortex. Sagittal sections were prepared from the brainstem and cerebellum, and transverse sections were prepared from the spinal cord. The tissues were dehydrated using a graded ethanol series and embedded in paraffin wax. Serial 4 μm sections were cut from the embedded samples and subjected to hematoxylin and eosin (H&E) or Klüver−Barrera staining. Immunohistochemistry with a rabbit polyclonal antibody against glial fibrillary acidic protein (GFAP) (Dakopatts, 1:500 dilution) was performed. The rat brain atlas with anatomical explanations of the terminology adopted by Paxinos et al.29 was used to identify the brain regions. All animal procedures were approved by the Animal Research Committee at the National Institute for Minamata Disease, and all conducted with strict adherence to its guidelines for alleviation of suffering.
Seychelles Child Development Study and the Faroe Islands studies did not reach the same conclusion, Grandjean et al.21 described the prenatal MeHg exposure-related neuropsychological dysfunctions in a cohort study in Faroe Islands, indicating that the effects of prenatal MeHg exposure are critical to the cerebrum. In the epidemics studies in Minamata, Japan, more than 20 infants were congenitally affected by MeHg, and Takeuchi3 suggested that MeHg affected the nerve cells after considerable differentiation had occurred during the intermediate or later period of fetal life. Therefore, we conducted animal studies focusing on the effects of MeHg on the brain during the rapid growth period corresponding to the late gestation period in humans.22,23 As a result, we succeeded in the development of a rat model showing neuronal degeneration in the cerebral cortex and striatum by administering MeHg (8 mg Hg/kg/day) for 10 continuous days from postnatal day 14.22,23 We designed the present experiments to examine the protective effects of selenium against MeHg-induced neuronal degeneration in the developing brain using our postnatal rat model22,23 that is suitable to extrapolating the effects of MeHg to the fetal brain of humans during late gestation.
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MATERIALS AND METHODS Female Wistar rats with pups postnatal days 7 were supplied by CLEA Japan and were maintained on a 12 h light/12 h dark cycle at 23 °C. At postnatal day 14, a litter was randomly reduced to 8 male pups, which were then maintained by a dam until weaning on postnatal day 21 with γ-ray-sterilized CE-2 laboratory chow (CLEA, Japan), which contains 0.4 ppm of selenium. The four groups of eight rats at postnatal day 14 were as follows: (1) control, (2) MeHg-exposed, (3) SeMet-exposed, and (4) Co-exposed to MeHg and SeMet. A MeHg chloride (MMC) solution was prepared by dissolving 50 mg of MMC (98% purity, Tokyo Kasei Kogyo Co. Ltd.) and 147.5 mg of Lcysteine (Sigma) in 25 mL of distilled water and 25 mL of condensed milk every day before administration. The dose of MeHg administered was 8 mg Hg/kg/day. This MeHg level was selected as high enough to cause neurological degenerations mainly in the cerebral cortex in postnatal developing rats.18 A SeMet solution was prepared by dissolving 2.48 mg of L (+) SeMet (99>% purity, ACROS) in 1 mL of water every day before administration to avoid the destruction of SeMet. The dose of SeMet administered was 2 mg Se/kg/day. This was selected as the highest SeMet level, which does not show any toxic effects in adult mice24 to counteract the high dosage of MeHg, which can cause neuronal degenerations in the cerebrum. MeHg and/or SeMet solutions were orally administered to the infants, with the aid of a microman pipet (Gilson), according to the method of Sakamoto et al.23 SeMet was administered first and MeHg was administered approximately 30 min later to avoid the direct MeHg and selenium complex formation in digestive system. On day 11, at 24 h after the final dose of the 10 day consecutive administration of vehicle, MeHg, SeMet, or MeHg+SeMet coexposure, all infant rats were euthanized. For mercury analysis, aliquots of tissue samples (0.05−0.1 g) were homogenized in 50 mM potassium phosphate (pH 7.0, 0.5 mL). Total mercury concentrations in the tissue homogenates were determined by an oxygen combustion-gold amalgamation method using an atomic absorption mercury detector (MD-A, Nippon Instruments Co. Ltd.). As the reference material of
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STATISTICS Data are presented as means ± standard deviation. Differences among the four groups (control, SeMet-exposed, MeHgexposed, and MeHg+SeMet coexposed) were analyzed by one-way analysis of variance (ANOVA). When a significant difference was recognized among the groups, the group differences were evaluated by Tukey’s post hoc test. The significance level was set at P < 0.05.
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RESULTS Just before euthanasia (day 11), the MeHg-exposed, SeMetexposed, and MeHg+SeMet coexposed groups showed significantly (P < 0.01) lower body weights than the control group. However, the Co-exposed group showed a significantly higher body weight than the MeHg-exposed (P < 0.01) and SeMet-exposed (P < 0.05) groups (Figure 1). Significantly lower liver weights were observed in the SeMet-exposed (P < 2863
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Figure 1. Change in body weight (mean ± SD) of control, SeMetexposed, MeHg-exposed and Co-exposed groups (n = 8). On day at 11, MeHg-exposed, SeMet-exposed and Co-exposed groups showed significantly (P < 0.01) lower body weight than that of control. Coexposed group showed significantly higher body weight than those of MeHg-exposed (P < 0.05) and SeMet-exposed (P < 0.01) groups.
Figure 3. Total mercury concentrations in the cerebrum, liver, kidney and blood (mean ± SD) of MeHg-exposed and MeHg + SeMet coexposed groups (n = 5). Total mercury concentrations in the cerebrum of Co-exposed group were significantly (P < 0.01) higher than those of MeHg-exposed group. Total mercury concentrations in kidney and blood of Co-exposed group were significantly (P < 0.01 for kidney, P < 0.05 for blood) lower than those of MeHg-exposed group.
0.01) and MeHg-exposed (P < 0.05) groups compared with the control group. However, the Co-exposed group showed a significantly (P < 0.01) higher liver weight than the SeMetexposed group (Figure 2).
Figure 2. Brain, liver, and kidney weights (mean ± SD) of control, SeMet-exposed, MeHg-exposed, and Co-exposed groups (n = 5). Liver weights of SeMet-exposed and MeHg-exposed groups were significantly (P < 0.01 for SeMet-exposed, P < 0.05 for MeHg-exposed) lower than that of control. Liver weight of Co-exposed group was significantly (P < 0.01) higher than that of SeMet-exposed group.
Figure 4. Inorganic mercury concentrations in the cerebrum, liver and kidney (mean ± SD) of MeHg-exposed and MeHg + SeMet coexposed groups (n = 5). Inorganic mercury concentrations in the cerebrum and liver of Co-exposed group was significantly (P < 0.01) higher than those of MeHg-exposed group. Inorganic mercury concentrations in kidney of Co-exposed group were significantly (P < 0.05) lower those of MeHg-exposed group. The percentage of inorganic mercury in the cerebrum of Co-exposed group was significantly (P < 0.05) higher than that of MeHg-exposed group (data not shown).
The total and inorganic mercury concentrations in the cerebrum of the Co-exposed group were significantly (P < 0.01) higher (1.40 times for total mercury and 1.93 times for inorganic mercury) than those of the MeHg-exposed group (Figures 3 and 4). The inorganic mercury percentage in the cerebrum of the Co-exposed group was significantly (P < 0.01) higher (1.42 times) than those of the MeHg-exposed group (data not shown). The selenium concentrations in the cerebrum of the SeMet-exposed group were significantly (P < 0.01) higher (16.5 times) than those of control group (Figure 5). The selenium concentrations in the cerebrum of the Coexposed group were significantly (P < 0.01) higher (1.65 times) than those of SeMet group.
The plasma T-Bil, AST, and ALT values in the SeMetexposed group were significantly (P < 0.01 for T-Bil, P < 0.05 for AST and ALT) higher than those in the control group (Figure 6). The T-Bil, AST, and ALT values in the Co-exposed group were significantly (P < 0.01) lower than those in the SeMet-exposed group. The GSH levels in the cerebrum showed no significant differences among the groups (Figure 7). The GSH levels in the liver and blood in the MeHg-exposed group were significantly (P < 0.01) lower than those in the control group. The GSH levels in the Co-exposed group were 2864
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manifested by shrinkage and eosinophilic cytoplasm, and reactive astrocytosis were consistently observed in the cerebral cortex (primary motor and somatosensory areas and cingulate cortex) and neostriatum (parts I−L of Figure 10). Small numbers of degenerative neurons were also observed in Ammon’s horn and the brain stem. In other central nervous system regions, neuronal degeneration was not apparent. The distribution pattern of neuronal degeneration was consistent with that in our previous study.24 The MeHg+SeMet coexposed group did not show any signs of neuronal degeneration (parts M−P of Figure 10).
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DISCUSSION Our results first demonstrated that selenium in the form of SeMet protected the developing rat brain against MeHginduced neuronal degeneration. Selenium concentrations in the cerebrum of SeMet-exposed group showed 16.5 times higher than those of control indicating that selenium was efficiently incorporated in the brain by SeMet administration without showing neuronal degeneration in the brain. MeHg induced neuronal degenerations in the cerebrum and striatum as were observed in our previous study,9 and SeMet clearly protected against these MeHg effects. The protective effects were not mediated by inhibition of MeHg uptake into the cerebrum because the total and inorganic mercury concentrations in the cerebrum of the Co-exposed group were higher than those of the MeHg-exposed group. The selenium concentration in the cerebrum of the Co-exposed group was also higher than that of the SeMet-exposed group. Coexposure to MeHg and selenium has been shown to change the accumulation of mercury and/or selenium in the brain.7,30−33 Increased mercury concentrations in the brain after coexposure to selenium were observed when animals were euthanized shortly after continuous administration was completed.6,7,32 Increased selenium concentrations in the brain by coexposure to MeHg have also been reported.6,32 In addition to the alterations in mercury and selenium accumulation in the brain, we have shown for the first time an increase in the inorganic mercury concentration after coexposure to selenium. Ingested SeMet is either metabolized directly to a reactive form of selenium or stored in place of methionine in tissue proteins; then the reactive form of
Figure 5. Selenium concentrations in the cerebrum, liver, kidney and blood (mean ± SD) of control, MeHg exposed, SeMet exposed, and Co-exposed groups (n = 5). Selenium concentrations in the cerebrum, liver, kidney in SeMet-exposed group were significantly (P < 0.01) higher than those of control group. Selenium concentrations in the cerebrum and blood of Co-exposed group were significantly (P < 0.01) higher than those of SeMet-exposed group. Selenium concentrations in kidney of Co-exposed group were significantly (P < 0.01) lower than those of SeMet-exposed group.
significantly (P < 0.01 for liver, P < 0.05 for blood) higher than those in the MeHg-exposed group. The GSH-Px activities in the cerebrum and liver in the MeHg-exposed group were significantly (P < 0.01) lower than those in the control group (Figure 8). The GSH-Px activity in the cerebrum of the Coexposed group was significantly (P < 0.01) higher than that of the MeHg-exposed group. The plasma d-ROM level in MeHgexposed group was significantly (P < 0.05) higher than that of control group (Figure 9). The plasma d-ROM level of the Coexposed group was significantly (P < 0.01) lower than that of the MeHg-exposed group. In the brain and spinal cord of the control (parts A−D of Figure 10) and SeMet-exposed (parts E−H of Figure 10) groups, there were no features suggestive of neuronal damage. However, in the MeHg-exposed group, neuronal degeneration
Figure 6. T-Bil, AST, and ALT levels in plasma (mean ± SD) of control, SeMet-exposed, MeHg-exposed, and Co-exposed groups (n = 5). T-Bil, AST, and ALT values in SeMet-exposed group were significantly (P < 0.01 for T-Bil, P < 0.05 for AST and ALT) higher than those of control. T-Bil, AST, and ALT values in Co-exposed group were significantly (P < 0.01) lower than those of SeMe-exposed group. 2865
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Figure 7. GSH levels in the cerebrum, liver and blood (mean ± SD) of control, SeMet-exposed, MeHg-exposed, and Co-exposed groups (n = 5). GSH levels in the cerebrum showed no significant difference among the groups. GSH level in liver and blood in MeHg-treated group were significantly (P < 0.01) lower than those of control. GSH levels in liver and blood of Co-exposed group were significantly (P < 0.01) higher than those of the MeHg-exposed group.
Figure 8. GSH-Px activity in the cerebrum and liver (mean ± SD) of control, SeMet-exposed, MeHg-exposed, and Co-exposed groups (n = 5). GSH-Px activities in the cerebrum and liver in MeHg-exposed were significantly (P < 0.01) lower than those in control. GSH-Px activity in the cerebrum and liver of Co-exposed group was significantly (P < 0.01 for cerebrum, P < 0.05 for liver) higher than that of MeHgexposed group.
Figure 9. d-ROM level in plasma (mean ± SD) of control, SeMetexposed, MeHg-exposed, and Co-exposed groups (n = 8). d-ROM level in plasma in MeHg-treated group was significantly (P < 0.05) higher than that of control. d-ROM level in plasma of Co-exposed group was significantly (P < 0.05) lower than that of MeHg-exposed group.
selenium will make a complex with MeHg16 mainly in liver. Iwata et al.34 suggested that the mechanism of demethylation of MeHg might involve a reaction between MeHg and a selenoamino acid complex via the formation of bis-methylmercuric selenide. Bis-methylmercuric selenide is a lipid-soluble compound that can easily pass through the blood-brain barrier. Another possibility for a MeHg/selenium complex is MeHgselenocysteine (MeHg-Sec),35 which is similar to MeHgcysteine, the form in which MeHg enters the brain. The formation of these MeHg/selenium complexes might explain the protective effect of SeMet against MeHg-induced neuronal degeneration, although the mercury and selenium concentrations in the brain were increased by the coexposure compared to MeHg or SeMet alone administration. It is important to note that the liver damages, such as the decrease in liver weight and increases in serum T-Bil, AST, and ALT levels, induced by SeMet were also negated by coexposure to MeHg. These results showing that coexposure to MeHg
leads to lower selenium toxicity toward the liver further suggest that an inert MeHg/selenium complex, such as bis-methylmercuric selenide or MeHg-Sec, might have been formed. The SeMet administration level was selected as the highest SeMet level which does not show any toxic effects in adult mice 24 as described in the Materials and Methods section. However, SeMet caused the damage to the liver in this experiment suggesting that the developing liver is more sensitive to selenium than the adult liver. The strength of this study is that, different from the previously reported studies,5−13 our study has first clearly demonstrated the protective effects of SeMet against MeHginduced neurotoxicity in the developing rat cerebrum. The weakness of this study might be the short durations of the MeHg and SeMet dosing and experimental observation, since we observed the histopathological changes just at 24 h after the 2866
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Figure 10. Light micrographs of the motor cortex (A, B, E, F, I, J, M, and N) and striatum (C, D, G, H, K, L, O, and P) of the control (control, A− D), SeMet-exposed (SeMet, E−H), MeHg-exposed (MeHg, I−L), and Co-exposed (MeHg+SeMet, M−P) groups. No degenerative neurons and astrocytosis (A−H). Several degenerative neurons showing shrunken and eosinophilic cytoplasm and condensed nuclei (arrows) (I and K) and reactive astrocytosis (J and L). No apparent degenerative features were observed even in the cortex and striatum (M−P). A, C, E, G, I, K, M, and O: H&E; B, D, F, H, J, L, N, and P: GFAP immunostain. Bar = 50 μm for A−P.
final dose of the 10 day consecutive administration of MeHg and SeMet. Further studies using a lower and environmentally relevant dose of MeHg and SeMet and more sensitive end points on neurobehavior performance are needed. These findings may have significant implications for public health in the populations which consume much fish and shellfish, and the population such as Amazonians and Inuits, who are exposed to high levels of both MeHg and selenium.36−39 The beneficial effects of comparatively high selenium body burden on motor function in Brazilian Amazonians, who have elevated MeHg exposure,40 will partly be explained by the protective effects of selenium in the brain. Our findings emphasize the possibility that the food-originated selenium can protect the brain against MeHg toxicity, especially in the developing cerebrum.
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ACKNOWLEDGMENTS
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REFERENCES
We thank Dr. Atsuhiro Nakano, Ex-Director of Department of Basic Medical Sciences, and Dr. Komyo Eto, Ex-Director General, National Institute for Minamata Disease for their encouragements in the course of this study.
(1) UNEP, Global Mercury Assessment, UNEP Chemicals Mercury Programme. 2002. (2) WHO, Methylmercury. Environmental Health Criteria 101, Geneva: World Health Organization. 1990. (3) Takeuchi, T. Pathology of Minamata disease. With special reference to its pathogenesis. Acta Pathol. Jpn. 1982, 32 (Suppl 1), 73− 99. (4) Matsumoto, H.; Koya, G.; Takeuchi, T. Fetal Minamata disease. A neuropathological study of two cases of intrauterine intoxication by a methyl mercury compound. J. Neuropathol. Exp. Neurol. 1965, 24 (4), 563−74. (5) Ganther, H. E.; Goudie, C.; Sunde, M. L.; Kopecky, M. J.; Wagner, P. Selenium: Relation to decreased toxicity of methylmercury added to diets containing tuna. Science 1972, 175 (26), 1122−4. (6) Ohi, G.; Nishigaki, S.; Seki, H.; Tamura, Y.; Maki, T. Efficacy of selenium in tuna and selenite in modifying methylmercury intoxication. Environ. Res. 1976, 12 (1), 49−58. (7) Ralston, N. V.; Ralston, C. R.; Blackwell, J. L., 3rd; Raymond, L. J. Dietary and tissue selenium in relation to methylmercury toxicity. Neurotoxicology 2008, 29 (5), 802−11. (8) Chang, L. W.; Suber, R. Protective effect of selenium on methylmercury toxicity: A possible mechanism. Bull. Environ. Contam. Toxicol. 1982, 29 (3), 285−9. (9) Watanabe, C.; Yoshida, K.; Kasanuma, Y.; Kun, Y.; Satoh, H. In utero methylmercury exposure differentially affects the activities of
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[email protected]. Author Contributions
The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. The authors declare they have no competing financial interests. Funding
This work was supported by The Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Number 23510085. H. M. Chan was a recipient of a JSPS Fellowship. Notes
The authors declare no competing financial interest. 2867
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selenoenzymes in the fetal mouse brain. Environ. Res. 1999, 80 (3), 208−14. (10) Fowler, B. A.; Lucier, G. W. Phenobarbital protection against methyl mercury neophrotoxicity. Proc. Soc. Exp. Biol. Med. 1975, 149 (1), 75−9. (11) Satoh, H.; Yasuda, N.; Shimai, S. Development of reflexes in neonatal mice prenatally exposed to methylmercury and selenite. Toxicol. Lett. 1985, 25 (2), 199−203. (12) Chang, L. W. Protective effects of selenium against methylmercury neurotoxicity: a morphological and biochemical study. Exp. Pathol. 1983, 23 (3), 143−56. (13) Heath, J. C.; Banna, K. M.; Reed, M. N.; Pesek, E. F.; Cole, N.; Li, J.; Newland, M. C. Dietary selenium protects against selected signs of aging and methylmercury exposure. Neurotoxicology 2010, 31 (2), 169−79. (14) Onning, G.; Bergdahl, I. A. Fractionation of soluble selenium compounds from fish using size-exclusion chromatography with online detection by inductively coupled plasma mass spectrometry. Analyst 1999, 124 (10), 1435−8. (15) Cabanero, A. I.; Carvalho, C.; Madrid, Y.; Batoreu, C.; Camara, C. Quantification and speciation of mercury and selenium in fish samples of high consumption in Spain and Portugal. Biol. Trace. Elem. Res. 2005, 103 (1), 17−35. (16) Schrauzer, G. N. Selenomethionine: A review of its nutritional significance, metabolism and toxicity. J. Nutr. 2000, 130 (7), 1653−6. (17) Ammar, E. M.; Couri, D. Acute toxicity of sodium selenite and selenomethionine in mice after ICV or IV administration. Neurotoxicology 1981, 2 (2), 383−6. (18) Moser-Veillon, P. B.; Mangels, A. R.; Patterson, K. Y.; Veillon, C. Utilization of two different chemical forms of selenium during lactation using stable isotope tracers: an example of speciation in nutrition. Analyst 1992, 117 (3), 559−62. (19) Thomson, C. D.; Stewart, R. D. Metabolic studies of (75Se)selenomethionine and (75Se)selenite in the rat. Br. J. Nutr. 1973, 30 (1), 139−47. (20) Gronbaek, H.; Thorlacius-Ussing, O. Selenium in the central nervous system of rats exposed to 75-Se L-selenomethionine and sodium selenite. Biol. Trace Elem. Res. 1992, 35 (2), 119−27. (21) Grandjean, P.; Weihe, P.; White, R. F.; Debes, F.; Araki, S.; Yokoyama, K.; Murata, K.; Sorensen, N.; Dahl, R.; Jorgensen, P. J. Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicol. Teratol. 1997, 19 (6), 417−28. (22) Wakabayashi, K.; Kakita, A.; Sakamoto, M.; Su, M.; Iwanaga, K.; Ikuta, F. Variability of brain lesions in rats administered methylmercury at various postnatal development phases. Brain Res. 1995, 705 (1−2), 267−72. (23) Sakamoto, M.; Nakano, A.; Kajiwara, Y.; Naruse, I.; Fujisaki, T. Effects of methyl mercury in postnatal developing rats. Environ Res 1993, 61 (1), 43−50. (24) Tsunoda, M.; Johnson, V. J.; Sharma, R. P. Increase in dopamine metabolites in murine striatum after oral exposure to inorganic but not organic form of selenium. Arch. Environ. Contam. Toxicol. 2000, 39 (1), 32−7. (25) Yasutake, A.; Hirayama, K. Selective quantification of inorganic mercury in tissues of methylmercury-treated rats. Bull. Environ. Contam. Toxicol. 1990, 45 (5), 662−6. (26) Tietze, F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 1969, 27 (3), 502−22. (27) Lawrence, R. A.; Burk, R. F. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 1976, 71 (4), 952−8. (28) Cesarone, M. R.; Belcaro, G.; Carratelli, M.; Cornelli, U.; De Sanctis, M. T.; Incandela, L.; Barsotti, A.; Terranova, R.; Nicolaides, A. A simple test to monitor oxidative stress. International Angiology: A Journal of the International Union of Angiology 1999, 18 (2), 127−30.
(29) Paxinos, G.; Watson, C. R.; Emson, P. C. AChE-stained horizontal sections of the rat brain in stereotaxic coordinates. J Neurosci Methods 1980, 3 (2), 129−49. (30) Alexander, J.; Norseth, T. The effect of selenium on the biliary excretion and organ distribution of mercury in the rat after exposure to methyl mercuric chloride. Acta Pharmacol. Toxicol. (Copenh) 1979, 44 (3), 168−76. (31) Dos Santos, A. P.; Mateus, M. L.; Carvalho, C. M.; Batoreu, M. C. Biomarkers of exposure and effect as indicators of the interference of selenomethionine on methylmercury toxicity. Toxicol. Lett. 2007, 169 (2), 121−8. (32) Magos, L.; Webb, M. The effect of selenium on the brain uptake of methylmercury. Arch. Toxicol. 1977, 38 (3), 201−7. (33) Komsta-Szumska, E.; Reuhl, K. R.; Miller, D. R. The effect of methylmercury on the distribution and excretion of selenium by the guinea pig. Arch. Toxicol. 1983, 54 (4), 303−10. (34) Iwata, H.; Masukawa, T.; Kito, H.; Hayashi, M. Degradation of methylmercury by selenium. Life Sci. 1982, 31 (9), 859−66. (35) Ralston, N. V.; Raymond, L. J. Dietary selenium’s protective effects against methylmercury toxicity. Toxicology 2010, 278 (1), 112− 23. (36) Hansen, J. C.; Deutch, B.; Pedersen, H. S. Selenium status in Greenland Inuit. Sci. Total Environ. 2004, 331 (1−3), 207−14. (37) Dewailly, E.; Ayotte, P.; Bruneau, S.; Lebel, G.; Levallois, P.; Weber, J. P. Exposure of the Inuit population of Nunavik (Arctic Quebec) to lead and mercury. Arch. Environ. Health 2001, 56 (4), 350−7. (38) Kehrig, H. A.; Malm, O.; Akagi, H.; Guimaraes, J. R.; Torres, J. P. Methylmercury in fish and hair samples from the Balbina Feservoir, Brazilian Amazon. Environ. Res. 1998, 77 (2), 84−90. (39) Lemire, M.; Mergler, D.; Fillion, M.; Passos, C. J.; Guimaraes, J. R.; Davidson, R.; Lucotte, M. Elevated blood selenium levels in the Brazilian Amazon. Sci. Total Environ. 2006, 366 (1), 101−11. (40) Lemire, M.; Fillion, M.; Frenette, B.; Passos, C. J.; Guimaraes, J. R.; Barbosa, F., Jr.; Mergler, D. Selenium from dietary sources and motor functions in the Brazilian Amazon. Neurotoxicology 2011, 32 (6), 944−53.
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NOTE ADDED AFTER ASAP PUBLICATION This article was published ASAP on February 25, 2013, with an error in the abstract and Table of Contents graphics and the legend of Figure 10. The corrected version was published ASAP on February 26, 2013.
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dx.doi.org/10.1021/es304226h | Environ. Sci. Technol. 2013, 47, 2862−2868
