Age-dependent susceptibility to manganese-induced neurological dysfunction

Toxicological Sciences

Volumn 112, Issue 2, 2009, Pages 394-404

  Moreno, Julie A ^a   Yeomans, Elizabeth C ^a   Streifel, Karin M ^a   Brattin, Bryan L ^b   Taylor, Robert J ^b   Tjalkens, Ronald B ^b  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Behavior; Development; Manganese; Metals; Neurochemistry

Indexed keywords

COPPER; DOPAMINE; IRON; MANGANESE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS;

AGE DISTRIBUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; C57BL 6 MOUSE; CONTROLLED STUDY; FEEDING; FEMALE; HELP SEEKING BEHAVIOR; HYPERACTIVITY; JUVENILE ANIMAL; LOCOMOTION; MALE; MASS SPECTROMETRY; MOUSE; NEUROCHEMISTRY; NEUROLOGIC DISEASE; NONHUMAN; OCCUPATIONAL EXPOSURE; SENSITIVITY ANALYSIS; SEX DETERMINATION; STRIATE CORTEX; SUBSTANTIA NIGRA; AGE; ANIMAL; ANIMAL BEHAVIOR; BRAIN; C57BL MOUSE; DRUG EFFECT; ELECTROCHEMISTRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; PATHOPHYSIOLOGY; TISSUE DISTRIBUTION;

ANIMALIA; MUS; RODENTIA;

AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROCHEMISTRY; FEMALE; MALE; MANGANESE; MICE; MICE, INBRED C57BL; NEUROTRANSMITTER AGENTS; TISSUE DISTRIBUTION;

EID: 74949109351     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp220     Document Type: Article

References (43)

1. Bader, M., Dietz, M. C., Ihrig, A., and Triebig, G. (1999). Biomonitoring of manganese in blood, urine and axillary hair following low-dose exposure during the manufacture of dry cell batteries. Int. Arch. Occup. Environ. Health 72, 521-527.
2. Bird, E. D., Anton, A. H., and Bullock, B. (1984). The effect of manganese inhalation on basal ganglia dopamine concentrations in rhesus monkey. Neurotoxicology 5(1), 59-65.
3. Bowler, R. M., Koller, W., and Schulz, P. E. (2006). Parkinsonism due to manganism in a welder: neurological and neuropsychological sequelae. Neurotoxicology 27, 327-332.
4. Cersosimo, M. G., and Koller, W. C. (2006). The diagnosis of manganese-induced parkinsonism. Neurotoxicology 27, 340-346.
5. Champney, T. H., Hanneman, W. H., and Nichols, M. A. (1992). gamma-Aminobutyric acid, catecholamine and indoleamine determinations from the same brain region by high-performance liquid chromatography with electrochemical detection. J. Chromatogr. 579, 334-339.
6. Cotzias, G. C., Miller, S. T., Papavasiliou, P. S., and Tang, L. C. (1976). Interactions between manganese and brain dopamine. Med. Clin. North Am. 60, 729-738.
7. D'Astous, M., Morissette, M., and Di Paolo, T. (2004). Effect of estrogen receptor agonists treatment in MPTP mice: evidence of neuroprotection by an ER alpha agonist. Neuropharmacology 47, 1180-1188.
8. Dodd, C. A., Ward, D. L., and Klein, B. G. (2005). Basal ganglia accumulation and motor assessment following manganese chloride exposure in the C57BL/6 mouse. Int. J. Toxicol. 24, 389-397.
9. Dorman, D. C., Struve, M. F., Marshall, M. W., Parkinson, C. U., James, R. A., and Wong, B. A. (2006a). Tissue manganese concentrations in young male rhesus monkeys following subchronic manganese sulfate inhalation. Toxicol. Sci. 92, 201-210.
10. Dorman, D. C., Struve, M. F., Vitarella, D., Byerly, F. L., Goetz, J., and Miller, R. (2000). Neurotoxicity of manganese chloride in neonatal and adult CD rats following subchronic (21-day) high-dose oral exposure. J. Appl. Toxicol. 20, 179-187.
11. Dorman, D. C., Struve, M. F., and Wong, B. A. (2002). Brain manganese concentrations in rats following manganese tetroxide inhalation are unaffected by dietary manganese intake. Neurotoxicology 23, 185-195.
12. Eriksson,H.,Magiste,K.,Plantin,L.O.,Fonnum,F.,Hedstrom,K.G.,Theodorsson-Norheim, E., Kristensson, K., Stalberg, E., and Heilbronn, E. (1987). Effects of manganese oxide on monkeys as revealed by a combined neurochemical, histological and neurophysiological evaluation. Arch. Toxicol. 61, 46-52.
13. Flurkey, K. C. J., and Harrison, D. E. (2007). The mouse in aging research. In The Mouse in Biomedical Research, 2nd ed (J. G. Fox, S. Barthold, M. Davisson, C. E. Newcomer, F. W. Quimby, and A. Smith, Eds.), pp. 637-672. American College Laboratory Animal Medicine, Elsevier, Burlington, MA.
14. George, S., van den Buuse, M., San Mok, S., Masters, C. L., Li, Q. X., and Culvenor, J. G. (2008). Alpha-synuclein transgenic mice exhibit reduced anxiety-like behaviour. Exp. Neurol. 210, 788-792.
15. Golub, M. S., Hogrefe, C. E., Germann, S. L., Tran, T. T., Beard, J. L., Crinella, F. M., and Lonnerdal, B. (2005). Neurobehavioral evaluation of rhesus monkey infants fed cow's milk formula, soy formula, or soy formula with added manganese. Neurotoxicol. Teratol. 27, 615-627.
16. Guilarte, T. R., Burton, N. C., McGlothan, J. L., Verina, T., Zhou, Y., Alexander, M., Pham, L., Griswold, M., Wong, D. F., Syversen, T., et al. (2008a). Impairment of nigrostriatal dopamine neurotransmission by manganese is mediated by pre-synaptic mechanism(s): implications to manganese-induced parkinsonism. J. Neurochem. 107, 1236-1247.
17. Guilarte, T. R., Burton, N. C., Verina, T., Prabhu, V. V., Becker, K. G., Syversen, T., and Schneider, J. S. (2008b). Increased APLP1 expression and neurodegeneration in the frontal cortex of manganese-exposed non-human primates. J. Neurochem. 105, 1948-1959.
18. Guilarte, T. R., McGlothan, J. L., Degaonkar, M., Chen, M. K., Barker, P. B., Syversen, T., and Schneider, J. S. (2006). Evidence for cortical dysfunction and widespread manganese accumulation in the nonhuman primate brain following chronic manganese exposure: a 1H-MRS and MRI study. Toxicol. Sci. 94, 351-358.
19. Hearn, A. S., Stroupe, M. E., Cabelli, D. E., Ramilo, C. A., Luba, J. P., Tainer, J. A., Nick, H. S., and Silverman, D. N. (2003). Catalytic and structural effects of amino acid substitution at histidine 30 in human manganese superoxide dismutase: insertion of valine C gamma into the substrate access channel. Biochemistry 42, 2781-2789.
20. Helms, C. M., Gubner, N. R., Wilhelm, C. J., Mitchell, S. H., and Grandy, D. K. (2008). D4 receptor deficiency in mice has limited effects on impulsivity and novelty seeking. Pharmacol. Biochem. Behav. 90, 387-393.
21. Hirata, Y., Kiuchi, K., and Nagatsu, T. (2001). Manganese mimics the action of 1-methyl-4-phenylpyridinium ion, a dopaminergic neurotoxin, in rat striatal tissue slices. Neurosci. Lett. 311, 53-56.
22. Josephs, K. A., Ahlskog, J. E., Klos, K. J., Kumar, N., Fealey, R. D., Trenerry, M. R., and Cowl, C. T. (2005). Neurologic manifestations in welders with pallidal MRI T1 hyperintensity. Neurology 64, 2033-2039.
23. Keen, C. L. (1984). Manganese. In Biochemical of the Essential Ultratrace Elements (E. Frieden, Ed.), pp. 89-132. New York Plenum Press, New York.
24. Kimura, M., Yagi, N., and Itokawa, Y. (1978). Effect of subacute manganese feeding on serotonin metabolism in the rat. J. Toxicol. Environ. Health. 4, 701-707.
25. Krachler, M., Domej, W., and Irgolic, K. J. (2000). Concentrations of trace elements in osteoarthritic knee-joint effusions. Biol.TraceElem.Res.75, 253-263.
26. Lesch, K. P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S., Benjamin, J., Muller, C. R., Hamer, D. H., and Murphy, D. L. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527-1531.
27. Liu, X., Sullivan, K. A., Madl, J. E., Legare, M., and Tjalkens, R. B. (2006). Manganese-induced neurotoxicity: the role of astroglial-derived nitric oxide in striatal interneuron degeneration. Toxicol. Sci. 91, 521-531.
28. Mergler,D., Huel, G., Bowler, R., Iregren, A., Belanger, S.,Baldwin,M.,Tardif, R., Smargiassi, A., and Martin, L. (1994). Nervous system dysfunction among workers with long-term exposure to manganese. Environ. Res. 64, 151-180.
29. Miczek, K. A., Fish, E. W., De Bold, J. F., and De Almeida, R. M. (2002). Social and neural determinants of aggressive behavior: pharmacotherapeutic targets at serotonin, dopamine and gamma-aminobutyric acid systems. Psychopharmacology (Berl.) 163, 434-458.
30. Morello, M., Canini, A., Mattioli, P., Sorge, R. P., Alimonti, A., Bocca, B., Forte, G., Martorana, A., Bernardi, G., and Sancesario, G. (2008). Sub-cellular localization of manganese in the basal ganglia of normal and manganese-treated rats an electron spectroscopy imaging and electron energy-loss spectroscopy study. Neurotoxicology 29, 60-72.
31. Mustafa, S. J., and Chandra, S. V. (1971). Levels of 5-hydroxytryptamine, dopamine and norepinephrine in whole brain of rabbits in chronic manganese toxicity. J. Neurochem. 18, 931-933.
32. Neff, N. H., Barrett, R. E., and Costa, E. (1969). Selective depletion of caudate nucleus dopamine and serotonin during chronic manganese dioxide administration to squirrel monkeys. Experientia 25, 1140-1141.
33. National Research Council. (1989). Recommended dietary allowances. NRC, Ed. 1989. Food and Nutrition Board, 10th ed., pp. 230-235. National Academy Press, Washington, DC.
34. Perl, D. P., and Olanow, C. W. (2007). The neuropathology of manganese-induced Parkinsonism. J. Neuropathol. Exp. Neurol. 66, 675-682.
35. Schneider, J. S., Decamp, E., Koser, A. J., Fritz, S., Gonczi, H., Syversen, T., and Guilarte, T. R. (2006). Effects of chronic manganese exposure on cognitive and motor functioning in non-human primates. Brain Res. 1118, 222-231.
36. Struve, M. F., McManus, B. E., Wong, B. A., and Dorman, D. C. (2007). Basal ganglia neurotransmitter concentrations in rhesus monkeys following subchronic manganese sulfate inhalation. Am. J. Ind. Med. 50, 772-778.
37. Takeda, A. (2003). Manganese action in brain function. Brain Res. Brain Res. Rev. 41(1), 79-87.
38. Tripanichkul, W., Sripanichkulchai, K., Duce, J. A., and Finkelstein, D. I. (2007). 17Beta-estradiol reduces nitrotyrosine immunoreactivity and increases SOD1 and SOD2 immunoreactivity in nigral neurons in male mice following MPTP insult. Brain Res. 1164, 24-31.
39. Uversky, V. N., Li, J., and Fink, A. L. (2001). Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson's disease and heavy metal exposure. J. Biol. Chem. 276, 44284-44296.
40. Wasserman, G. A., Liu, X., Parvez, F., Ahsan, H., Levy, D., Factor-Litvak, P., Kline, J., van Geen, A., Slavkovich, V., LoIacono, N. J., et al. (2006). Water manganese exposure and children's intellectual function in Araihazar, Bangladesh. Environ. Health Perspect. 114, 124-129.
41. Wolters, E. C., Huang, C. C., Clark, C., Peppard, R. F., Okada, J., Chu, N. S., Adam, M. J., Ruth, T. J., Li, D., and Calne, D. B. (1989). Positron emission tomography in manganese intoxication. Ann. Neurol. 26, 647-651.
42. Woolf, A., Wright, R., Amarasiriwardena, C., and Bellinger, D. (2002). A child with chronic manganese exposure from drinking water. Environ. Health Perspect. 110, 613-616.
43. Yamada, M., Ohno, S., Okayasu, I., Okeda, R., Hatakeyama, S., Watanabe, H., Ushio, K., and Tsukagoshi, H. (1986). Chronic manganese poisoning: a neuropathological study with determination of manganese distribution in the brain. Acta Neuropathol. (Berl.) 70, 273-278.