Behavioral effects of developmental methylmercury drinking water exposure in rodents

Journal of Trace Elements in Medicine and Biology

Volumn 28, Issue 2, 2014, Pages 117-124

  Bisen Hersh, Emily B ^a   Farina, Marcelo ^c   Barbosa, Fernando ^d   Rocha, Joao B T ^e   Aschner, Michael ^a,b  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^d Departament of Pharmaceutical Sciences   (Brazil)

^e FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

Author keywords

Behavior; Developmental neurotoxicity; Learning; Mercury; Rodents

Indexed keywords

DRINKING WATER; METHYLMERCURY; PERFLUOROOCTANOIC ACID; POLYCHLORINATED BIPHENYL DERIVATIVE; TRANSCRIPTION FACTOR NRF2;

ANIMAL BEHAVIOR; BLOOD LEVEL; BRAIN LEVEL; DEVELOPMENTAL TOXICITY; FLUID INTAKE; IN VIVO STUDY; LEARNING DISORDER; MEMORY DISORDER; MOLECULAR MECHANICS; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; REINFORCEMENT; REVIEW; RISK ASSESSMENT; TASK PERFORMANCE;

RODENTIA;

EID: 84898029376     PISSN: 0946672X     EISSN: 18783252     Source Type: Journal    
DOI: 10.1016/j.jtemb.2013.09.008     Document Type: Review

References (101)

1. Water quality criterion for the protection of human health: methylmercury 2001, Environmental Protection Agency, Office of Science and Technology, Office of Water, Environmental Protection Agency, Washington, DC, [EPA-823-R-01-001].
2. Davidson P.W., Myers G.J., Cox C., Axtell C., Shamlaye C., Sloane-Reeves J., et al. Effects of prenatal and postnatal methylmercury exposure from fish consumption on neurodevelopment: outcomes at 66 months of age in the Seychelles Child Development Study. J Am Med Assoc 1998, 280:701-707.
3. Davidson P.W., Myers G.J., Cox C., Wilding G.E., Shamlaye C.F., Huang L.S., et al. Methylmercury and neurodevelopment: longitudinal analysis of the Seychelles child development cohort. Neurotoxicol Teratol 2006, 28:529-535.
4. Davidson P.W., Strain J.J., Myers G.J., Thurston S.W., Bonham M.P., Shamlaye C.F., et al. Neurodevelopmental effects of maternal nutritional status and exposure to methylmercury from eating fish during pregnancy. Neurotoxicology 2008, 29:767-775.
5. Davidson P.W., Jean Sloane R., Myers G.J., Hansen O.N., Huang L.S., Georger L.A., et al. Association between prenatal exposure to methylmercury and visuospatial ability at 10.7 years in the Seychelles child development study. Neurotoxicology 2008, 29:453-459.
6. Myers G.J., Thurston S.W., Pearson A.T., Davidson P.W., Cox C., Shamlaye C.F., et al. Postnatal exposure to methylmercury from fish consumption: a review and new data from the Seychelles Child Development Study. Neurotoxicology 2009, 30:338-349.
7. Davidson P.W., Leste A., Benstrong E., Burns C.M., Valentin J., Sloane-Reeves J., et al. Fish consumption, mercury exposure, and their associations with scholastic achievement in the Seychelles Child Development Study. Neurotoxicology 2010, 31:439-447.
8. Grandjean P., Budtz-Jorgensen E., Jorgensen P.J., Weihe P. Umbilical cord mercury concentration as biomarker of prenatal exposure to methylmercury. Environ Health Perspect 2005, 113:905-908.
9. Grandjean P., Budtz-Jorgensen E., Steuerwald U., Heinzow B., Needham L.L., Jorgensen P.J., et al. Attenuated growth of breast-fed children exposed to increased concentrations of methylmercury and polychlorinated biphenyls. FASEB J 2003, 17:699-701.
10. Grandjean P., Weihe P., White R.F., Debes F., Araki S., Yokoyama K., et al. Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicol Teratol 1997, 19:417-428.
11. Debes F., Budtz-Jørgensen E., Weihe P., White R.F., Grandjean P. Impact of prenatal methylmercury exposure on neurobehavioral function at age 14 years. Neurotoxicol Teratol 2006, 28:363-375.
12. Toxicological Effect of Methylmercury 2000, National Academy of Science, Committee on the Toxicological Effects of Methylmercury, Board on Environmental Studies and Toxicology, National Research Council, National Academies Press, Washington, DC.
13. US EPA Health effects of mercury and mercury compounds 1997, vol. V. Mercury Study Report to Congress, Office of Air Quality Planning & Standards and Office of Research and Development, [EPA-452/R-97-007].
14. Björnberg K.A., Vahter M., Berglund B., Niklasson B., Blennow M., Sandborgh-Englund G. Transport of methylmercury and inorganic mercury to the fetus and breast-fed infant. Environ Health Perspect 2005, 113:1381-1385.
15. Watanabe C., Yoshida K., Kasanuma Y., Kun Y., Satoh H. In utero methylmercury exposure differentially affects the activities of selenoenzymes in the fetal mouse brain. Environ Res 1999, 80:208-214.
16. Grandjean P., Landrigan P.J. Developmental neurotoxicity of industrial chemicals. Lancet 2006, 368:2167-2178.
17. Harada M. Minamata disease: methylmercury poisoning in Japan caused by environmental pollution. Crit Rev Toxicol 1995, 25:1-24.
18. Amin-Zaki L., Elhassani S., Majeed M.A., Clarkson T.W., Doherty R.A., Greenwood M. Intra-uterine methylmercury poisoning in Iraq. Pediatrics 1974, 54:587-595.
19. Julvez J., Yorifuji T., Choi A.L., Grandjean P. Epidemiological evidence on methylmercury neurotoxicity. Methylmercury and neurotoxicity 2012, 13-35. Springer, New York. S. Ceccatelli, M. Aschner (Eds.).
20. Grandjean P., Weihe P., White R.F., Debes F. Cognitive performance of children prenatally exposed to "safe" levels of methylmercury. Environ Res 1998, 77:165-172.
21. Gimenez-Llort L., Ahlbom E., Dare E., Vahter M., Ogren S., Ceccatelli S. Prenatal exposure to methylmercury changes dopamine-modulated motor activity during early ontogeny: age and gender-dependent effects. Environ Toxicol Pharmacol 2001, 9:61-70.
22. Malagutti K.S., da Silva A.P., Braga H.C., Mitozo P.A., Soares Dos Santos A.R., Dafre A.L., et al. 17β-estradiol decreases methylmercury-induced neurotoxicity in male mice. Environ Toxicol Pharmacol 2009, 27:293-297.
23. Rossi A.D., Ahlbom E., Ogren S.O., Nicotera P., Ceccatelli S. Prenatal exposure to methylmercury alters locomotor activity of male but not female rats. Exp Brain Res 1997, 117:428-436.
24. Myers G.J., Davidson P.W., Cox C., Shamlaye C.F., Palumbo D., Cernichiari E., et al. Prenatal methylmercury exposure from ocean fish consumption in the Seychelles Child Development Study. Lancet 2003, 361:1686-1692.
25. Rice D.C. Effects of pre-plus postnatal exposure to methylmercury in the monkey on fixed interval and discrimination reversal performance. Neurotoxicology 1992, 13:443-452.
26. Rice D.C. Sensory and cognitive effects of developmental methylmercury exposure in monkeys, and a comparison to effects in rodents. Neurotoxicology 1996, 17:139-154.
27. Magos L. The absorption, distribution, and excretion of methylmercury. The toxicity of methyl mercury 1987, 24-44. Johns Hopkins University Press, Baltimore.
28. Newland M.C., Reile P.A. Blood and brain mercury levels after chronic gestational exposure to methylmercury in rats. Toxicol Sci 1999, 50:106-116.
29. Dietrich M.O., Mantese C.E., Anjos G.D., Souza D.O., Farina M. Motor impairment induced by oral exposure to methylmercury in adult mice. Environ Toxicol Pharmacol 2005, 19:169-175.
30. Reed M.N., Newland M.C. Prenatal methylmercury exposure increases responding under clocked and unclocked fixed interval schedules of reinforcement. Neurotoxicol Teratol 2007, 29:492-502.
31. Rasmussen E.B., Newland M.C. Developmental exposure to methylmercury alters behavioral sensitivity to d-amphetamine and pentobarbital in adult rats. Neurotoxicol Teratol 2001, 23:45-55.
32. Reed M.N., Newland M.C. Gestational methylmercury exposure selectively increases the sensitivity of operant behavior to cocaine. Behav Neurosci 2009, 123:408-417.
33. Newland M.C., Hoffman D., Heath J.C., Donlin W.D. Response inhibition is impaired by developmental methylmercury exposure: acquisition of low-rate lever-pressing. Behav Brain Res 2013, 253:196-205.
34. Onishchenko N., Tamm C., Vahter M., Hokfelt T., Johnson J.A., Johnson D.A., et al. Developmental exposure to methylmercury alters learning and induces depression-like behavior in male mice. Toxicol Sci 2007, 97:428-437.
35. Stringari J., Nunes A.K.C., Franco J.L., Bohrer D., Garcia S.C., Dafre A.L., et al. Prenatal methylmercury exposure hampers glutathione antioxidant system ontogenesis and causes long-lasting oxidative stress in the mouse brain. Toxicol Appl Pharmacol 2008, 227:147-154.
36. Goulet S., Dore F.Y., Mirault M.E. Neurobehavioral changes in mice chronically exposed to methylmercury during fetal and early postnatal development. Neurotoxicol Teratol 2003, 25:335-347.
37. Vitalone A., Catalani A., Chiodi V., Cinque C., Fattori V., Goldoni M., et al. Neurobehavioral assessment of rats exposed to low doses of PCB126 and methyl mercury during development. Environ Toxicol Pharmacol 2008, 25:103-113.
38. Vitalone A., Catalani A., Cinque C., Fattori V., Matteucci P., Zuena A.R., et al. Long-term effects of developmental exposure to low doses of PCB126 and methylmercury. Toxicol Lett 2010, 197:38-45.
39. Fujimura M., Cheng J., Zhao W. Perinatal exposure to low-dose methylmercury induces dysfunction of motor coordination with decreases in synaptophysin expression in the cerebellar granule cells of rats. Brain Res 2012, 1464:1-7.
40. Cheng J., Fujimura M., Zhao W., Wang W. Neurobehavioral effects, c-Fos/Jun expression and tissue distribution in rat offspring prenatally co-exposed to MeHg and PFOA: PFOA impairs Hg retention. Chemosphere 2013, 91:758-764.
41. Manfroi C.B., Schwalm F.D., Cereser V., Abreu F., Oliveira A., Bizarro L., et al. Maternal milk as methylmercury source for suckling mice: neurotoxic effects involved with the cerebellar glutamatergic system. Toxicol Sci 2004, 81:172-178.
42. Stern S., Cox C., Cernichiari E., Balys M., Weiss B. Methylmercury in the mouse: blood and brain concentrations of mercury to 26 months of age. Neurotoxicology 2001, 22:467-477.
43. Weiss B., Stern S., Cox C., Balys M. Perinatal and lifetime exposure to methylmercury in the mouse: behavioral effects. Neurotoxicology 2005, 26:675-690.
44. Castoldi A.F., Onishchenko N., Johansson C., Coccini T., Roda E., Vahter M., et al. Neurodevelopmental toxicity of methylmercury: laboratory animal data and their contribution to human risk assessment. Regul Toxicol Pharmacol 2008, 51:215-229.
45. Burbacher T.M., Rodier P.M., Weiss B. Methylmercury developmental neurotoxicity: a comparison of effects in humans and animals. Neurotoxicol Teratol 1990, 12:191-202.
46. Newland M.C., Rasmussen E.B. Aging unmasks adverse effects of gestational exposure to methylmercury in rats. Neurotoxicol Teratol 2000, 22:819-828.
47. Newland M.C., Reed M.N., LeBlanc A., Donlin W.D. Brain and blood mercury and selenium after chronic and developmental exposure to methylmercury. Neurotoxicology 2006, 27:710-720.
48. Lewandowski T.A., Ponce R.A., Charleston J.S., Hong S., Faustman E.M. Effect of methylmercury on midbrain cell proliferation during organogenesis: potential cross-species differences and implications for risk assessment. Toxicol Sci 2003, 75:124-133.
49. Lapham L.W., Cernichiari E., Cox C., Myers G.J., Baggs R.B., Brewer R., et al. An analysis of autopsy brain tissue from infants prenatally exposed to methylmercury. Neurotoxicology 1995, 16:689-704.
50. Takeuchi T. Human effects of methylmercury as an environmental neurotoxicant. Neurotoxicology 1985, 345-367. Marcel Dekker, New York. K. Blum, L. Manzo (Eds.).
51. Takizawa Y. Mercury content in recognized patients and non-recognized patients exposed to methylmercury from Minamata Bay in the last ten years. Recent advances in minamata disease studies 1986, 1-39. Kodansha Ltd, Tokyo. T. Tsubaki, H. Takahashi (Eds.).
52. Choi B.H., Lapham L.W., Amin-Zaki L., Saleem T. Abnormal neuronal migration, deranged cerebral cortical organization, and diffuse white matter astrocytosis of human fetal brain: a major effect of methylmercury poisoning in utero. J Neuropathol Exp Neurol 1978, 37:719-733.
53. Day J.J., Reed M.N., Newland M.C. Neuromotor deficits and mercury concentrations in rats exposed to methyl mercury and fish oil. Neurotoxicol Teratol 2005, 27:629-641.
54. Roegge C.S., Wang V.C., Powers B.E., Klintsova A.Y., Villareal S., Greenough W.T., et al. Motor impairment in rats exposed to PCBs and methylmercury during early development. Toxicol Sci 2004, 77:315-324.
55. Grandjean P. Methylmercury toxicity and functional programming. Reprod Toxicol 2007, 23:414-420.
56. Cagiano R., De Salvia M.A., Renna G., Tortella E., Braghiroli D., Parenti C., et al. Evidence that exposure to methyl mercury during gestation induces behavioral and neurochemical changes in offspring of rats. Neurotoxicol Teratol 1990, 12:23-28.
57. Eccles C.U., Annau Z. Prenatal methyl mercury exposure: I. Alterations in neonatal activity. Neurobehav Toxicol Teratol 1982, 4:371-376.
58. Heath J.C., Banna K.M., Reed M.N., Pesek E.F., Cole N., Li J., et al. Dietary selenium protects against selected signs of aging and methylmercury exposure. Neurotoxicology 2010, 31:169-179.
59. Motz B.A., Alberts J.R. The validity and utility of geotaxis in young rodents. Neurotoxicol Teratol 2005, 27:529-533.
60. Paletz E.M., Craig-Schmidt M.C., Newland M.C. Gestational exposure to methylmercury and n-3 fatty acids: effects on high- and low-rate operant behavior in adulthood. Neurotoxicol Teratol 2006, 28:59-73.
61. Newland M.C., Paletz E.M. Animal studies of methylmercury and PCBs: what do they tell us about expected effects in humans. Neurotoxicology 2000, 21:1003-1027.
62. Reed M.N., Paletz E.M., Newland M.C. Gestational exposure to methylmercury and selenium: effects on a spatial discrimination reversal in adulthood. Neurotoxicology 2006, 27:721-732.
63. Paletz E.M., Day J.J., Craig-Schmidt M.C., Newland M.C. Spatial and visual discrimination reversals in adult and geriatric rats exposed during gestation to methylmercury and n-3 polyunsaturated fatty acids. Neurotoxicology 2007, 28:707-719.
64. Reed M.N., Banna K.M., Donlin W.D., Newland M.C. Effects of gestational exposure to methylmercury and dietary selenium on reinforcement efficacy in adulthood. Neurotoxicol Teratol 2008, 30:29-37.
65. Newland M.C., Reile P.A., Langston J.L. Gestational exposure to methylmercury retards choice in transition in aging rats. Neurotoxicol Teratol 2004, 26:179-194.
66. Barone S., Haykal-Coates N., Parran D.K., Tilson H.A. Gestational exposure to methylmercury alters the developmental pattern of trk-like immunoreactivity in the rat brain and results in cortical dysmorphology. Dev Brain Res 1998, 109:13-31.
67. Onishchenko N., Karpova N., Sabri F., Castrén E., Ceccatelli S. Long-lasting depression-like behavior and epigenetic changes of BDNF gene expression induced by perinatal exposure to methylmercury. J Neurochem 2008, 106:1378-1387.
68. Burk R.F. Selenium: an antioxidant nutrient. Nutr Clin Care 2002, 5:75-79.
69. Uchikawa T., Yasutake A., Kumamoto Y.T., Maruyama I., Kumamoto S., Ando Y. The influence of Parachlorella beyerinckii CK-5 on the absorption and excretion of methylmercury in mice. J Toxicol Sci 2010, 35:101-105.
70. Uchikawa T., Kumamoto Y.T., Maruyama I., Kumamoto S., Ando Y., Yasutake A. The enhanced elimination of tissue methylmercury in Parachlorella beijerinckii-fed mice. J Toxicol Sci 2011, 36:121-126.
71. Uchikawa T., Maruyama I., Kumamoto S., Ando Y., Yasutake A. Chlorella suppresses methylmercury transfer to the fetus in pregnant mice. J Toxicol Sci 2011, 36:675-680.
72. Aschner M., Syversen T., Souza D.O., Rocha J.B., Farina M. Involvement of glutamate and reactive oxygen species in methylmercury neurotoxicity. Braz J Med Biol Res 2007, 40:285-291.
73. Farina M., Aschner M., Rocha J.B. Oxidative stress in MeHg-induced neurotoxicity. Toxicol Appl Pharmacol 2011, 256:405-417.
74. Khan J.Y., Black S.M. Developmental changes in murine brain antioxidant enzymes. Pediatr Res 2003, 54:77-82.
75. Farina M., Avila D.S., da Rocha J.B., Aschner M. Metals, oxidative stress and neurodegeneration: a focus on iron, manganese and mercury. Neurochem Int 2013, 62:575-594.
76. Toyama T., Sumi D., Shinkai Y., Yasutake A., Taguchi K., Tong K.I., et al. Cytoprotective role of Nrf2/Keap1 system in methylmercury toxicity. Biochem Biophys Res Commun 2007, 363:645-650.
77. Rand M.D., Dao J.C., Clason T.A. Methylmercury disruption of embryonic neural development in Drosophila. Neurotoxicology 2009, 30:794-802.
78. Wang L., Jiang H., Yin Z., Aschner M., Cai J. Methylmercury toxicity and Nrf2-dependent detoxification in astrocytes. Toxicol Sci 2009, 107:135-143.
79. Ni M., Li X., Yin Z., Sidoryk-Wegrzynowicz M., Jiang H., Farina M., et al. Comparative study on the response of rat primary astrocytes and microglia to methylmercury toxicity. Glia 2011, 59:810-820.
80. Toyama T., Shinkai Y., Yasutake A., Uchida K., Yamamoto M., Kumagai Y. Isothiocyanates reduce mercury accumulation via an Nrf2-dependent mechanism during exposure of mice to methylmercury. Environ Health Perspect 2011, 119:1117-1122.
81. Hwang G.W. Role of intracellular defense factors against methylmercury toxicity. Biol Pharm Bull 2012, 35:1881-1884.
82. Kumagai Y., Kanda H., Shinkai Y., Toyama T. The role of the keap1/nrf2 pathway in the cellular response to methylmercury. Oxid Med Cell Longev 2013, 10.1155/2013/848279.
83. Huang H.C., Nguyen T., Pickett C.B. Phosphorylation of Nrf2 at ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. J Biol Chem 2002, 277:42769-42774.
84. Bloom D.A., Jaiswal A.K. Phosphorylation of Nrf2 at Ser40 by protein kinase c in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H:quinone oxidoreductase-1 gene expression. J Biol Chem 2003, 278:44675-44682.
85. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 2007, 47:89-116.
86. Kell A., Ventura N., Kahn N., Johnson T.E. Activation of SKN-1 by novel kinases in Caenorhabditis elegans. Free Radic Biol Med 2007, 43:1560-1566.
87. Tullet J.M., Hertweck M., An J.H., Baker J., Hwang J.Y., Liu S., et al. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 2008, 132:1025-1038.
88. Morito N., Yoh K., Itoh K., Hirayama A., Koyama A., Yamamoto M., et al. Nrf2 regulates the sensitivity of death receptor signals by affecting intracellular glutathione levels. Oncogene 2003, 22:9275-9281.
89. Sherratt P.J., Huang H.C., Nguyen T., Pickett C.B. Role of protein phosphorylation in the regulation of NF-E2-related factor 2 activity. Methods Enzymol 2004, 378:286-301.
90. Chen X.L., Dodd G., Thomas S., Zhang X., Wasserman M.A., Rovin B.H., et al. Activation of Nrf2/ARE pathways protects endothelial cells from oxidant injury and inhibits inflammatory gene expression. Am J Physiol Heart Circ Physiol 2006, 290:H1862-H1870.
91. Fayard E., Tintignac L.A., Baudry A., Hemmings B.A. Protein kinase B/Akt at a glance. J Cell Sci 2005, 118:5675-5678.
92. Malstrom S., Tili E., Kappes D., Ceci J.D., Tsichlis P.N. Tumor induction by an Lck-MyrAkt transgene is delayed by mechanisms controlling the size of the thymus. Proc Natl Acad Sci USA 2001, 98:14967-14972.
93. Rathmell J.C., Elstrom R.L., Cinalli R.M., Thompson C.B. Activated Akt promotes increased resting T cell size, CD28-independent T cell growth, and development of autoimmunity and lymphoma. Eur J Immunol 2003, 33:2223-2232.
94. Yang Z.Z., Tschopp O., Hemmings-Mieszczak M., Feng J., Brodbeck D., Perentes E., et al. Protein kinase B alpha/Akt1 regulates placental development and fetal growth. J Biol Chem 2003, 278:32124-32131.
95. Garofalo R.S., Orena S.J., Radidi K., Torchia A.J., Stock J.L., Hildebrandt A.L., et al. Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB. J Clin Invest 2003, 112:197-208.
96. Tschopp O., Yang Z., Brodbeck D., Dummler B.A., Hemings-Mieszczak M., Watanabe T., et al. Essential role of protein kinase B gamma (PKB gamma/Akt3) in postnatal brain development but not in glucose homeostasis. Development 2005, 132:2943-2954.
97. Easton R.M., Cho H., Roovers K., Shineman D.W., Mizrahi M., Forman M.S., et al. Role for Akt3/protein kinase B gamma in attainment of normal brain size. Mol Cell Biol 2005, 25:1869-1878.
98. Report on mercury. Nord Hyg Tidskr 1971, 4:1-357. Swedish Expert Group.
99. Philbert M.A., Billingsley M.L., Reuhl K.R. Mechanisms of injury in the central nervous system. Toxicol Pathol 2000, 28:43-53.
100. Costa L.G., Aschner M., Vitalone A., Syversen T., Soldin O.P. Developmental neuropathology of environmental agents. Annu Rev Pharmacol Toxicol 2004, 44:87-110.
101. Mergler D., Anderson H.A., Chan L.H., Mahaffey K.R., Murray M., Sakamoto M., et al. The panel on health risks and toxicological effects of methylmercury. Methylmercury exposure and health effects in humans: a worldwide concern. Ambio 2007, 36:3-11.