Chronic exposure to manganese alters brain responses to amphetamine: A pharmacological magnetic resonance imaging study

Toxicological Sciences

Volumn 114, Issue 2, 2010, Pages 310-322

  Williams, Jason M ^a,b   Milatovic, Dejan ^a   Gore, John C ^a,b   Aschner, Michael ^a,c   Avison, Malcolm J ^a,b,c  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Basal ganglia; Dopamine; Magnetic resonance imaging; Manganese; Neurodegeneration; Parkinson's disease

Indexed keywords

AMPHETAMINE; DOPAMINE; MANGANESE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BLOOD LEVEL; BRAIN FUNCTION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; GLOBUS PALLIDUS; INNERVATION; INTOXICATION; LONG TERM EXPOSURE; MALE; MESENCEPHALON; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARKINSONISM; PUTAMEN; RAT; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; SUBSTANTIA NIGRA; THALAMUS DORSOMEDIAL NUCLEUS;

AMPHETAMINE; ANIMALS; BRAIN; BRAIN MAPPING; CHLORIDES; DOPAMINE UPTAKE INHIBITORS; DRUG ANTAGONISM; INJECTIONS, INTRAVENOUS; MAGNETIC RESONANCE IMAGING; MALE; MANGANESE COMPOUNDS; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY;

ANIMALIA; PARKINSONIA; RATTUS;

EID: 77951577455     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq002     Document Type: Article

References (82)

1. Al-Bader, A. A., Mosawi, M. H., Hussain, T. A., and Dashti, H. M. (1997). Effect of dietary selenium, zinc and allopurinol supplements on plasma and tissue manganese levels in rats with thioacetamide [correction of thiocetamide]-induced liver cirrhosis. Mol. Cell. Biochem. 173, 121-125.
2. Amara, S. G., and Sonders, M. S. (1998). Neurotransmitter transporters as molecular targets for addictive drugs. Drug Alcohol Depend. 51, 87-96.
3. Anderson, J. G., Cooney, P. T., and Erikson, K. M. (2007). Inhibition of DAT function attenuates manganese accumulation in the globus pallidus. Environ. Toxicol. Pharmacol. 23, 179-184.
4. Arthurs, O. J., and Boniface, S. (2002). How well do we understand the neural origins of the fMRI BOLD signal? Trends Neurosci. 25, 27-31.
5. Aschner, M., and Aschner, J. L. (1991). Manganese neurotoxicity: cellular effects and blood-brain barrier transport. Neurosci. Biobehav. Rev. 15, 333-340.
6. Aschner, M., Guilarte, T. R., Schneider, J. S., and Zheng, W. (2007). Manganese: recent advances in understanding its transport and neurotoxicity. Toxicol. Appl. Pharmacol. 221, 131-147.
7. 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, 59-65.
8. Brooks, D. J., Ibanez, V., Sawle, G. V., Quinn, N., Lees, A. J., Mathias, C. J., Bannister, R., Marsden, C. D., and Frackowiak, R. S. (1990). Differing patterns of striatal 18F-dopa uptake in Parkinson's disease, multiple system atrophy, and progressive supranuclear palsy. Ann. Neurol. 28, 547-555.
9. Brouillet, E. P., Shinobu, L., McGarvey, U., Hochberg, F., and Beal, M. F. (1993). Manganese injection into the rat striatum produces excitotoxic lesions by impairing energy metabolism. Exp. Neurol. 120, 89-94.
10. Burton, N. C., and Guilarte, T. R. (2009). Manganese neurotoxicity: lessons learned from longitudinal studies in nonhuman primates. Environ. Health Perspect. 117, 325-332.
11. Buxton, R. B., Uludag, K., Dubowitz, D. J., and Liu, T. T. (2004). Modeling the hemodynamic response to brain activation. Neuroimage 23(Suppl. 1), S220-S233.
12. Calne, D. B., Chu, N. S., Huang, C. C., Lu, C. S., and Olanow, W. (1994). Manganism and idiopathic parkinsonism: similarities and differences. Neurology 44, 1583-1586.
13. Cass, W. A., Gerhardt, G. A., Mayfield, R. D., Curella, P., and Zahniser, N. R. (1992). Differences in dopamine clearance and diffusion in rat striatum and nucleus accumbens following systemic cocaine administration. J. Neurochem. 59, 259-266.
14. Chandra, S. V., and Shukla, G. S. (1981). Concentrations of striatal catecholamines in rats given manganese chloride through drinking water. J. Neurochem. 36, 683-687.
15. Chen, M. K., Lee, J. S., McGlothan, J. L., Furukawa, E., Adams, R. J., Alexander, M., Wong, D. F., and Guilarte, T. R. (2006). Acute manganese administration alters dopamine transporter levels in the non-human primate striatum. Neurotoxicology 27, 229-236.
16. Chen, Y. C., Galpern, W. R., Brownell, A. L., Matthews, R. T., Bogdanov, M., Isacson, O., Keltner, J. R., Beal, M. F., Rosen, B. R., and Jenkins, B. G. (1997). Detection of dopaminergic neurotransmitter activity using pharmacologic MRI: correlation with PET, microdialysis, and behavioral data. Magn. Reson. Med. 38, 389-398.
17. Chen, Y. I., Brownell, A. L., Galpern, W., Isacson, O., Bogdanov, M., Beal, M. F., Livni, E., Rosen, B. R., and Jenkins, B. G. (1999). Detection of dopaminergic cell loss and neural transplantation using pharmacological MRI, PET and behavioral assessment. Neuroreport 10, 2881-2886.
18. Ciliax, B. J., Heilman, C., Demchyshyn, L. L., Pristupa, Z. B., Ince, E., Hersch, S. M., Niznik, H. B., and Levey, A. I. (1995). The dopamine transporter: immunochemical characterization and localization in brain. J. Neurosci. 15, 1714-1723.
19. Cotterill, R. M. (2001). Cooperation of the basal ganglia, cerebellum, sensory cerebrum and hippocampus: possible implications for cognition, consciousness, intelligence and creativity. Prog. Neurobiol. 64, 1-33.
20. Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162-173.
21. Daniels, A. J., and Abarca, J. (1991). Effect of intranigral Mn2+ on striatal and nigral synthesis and levels of dopamine and cofactor. Neurotoxicol. Teratol. 13, 483-487.
22. Di Monte, D. A. (2003). The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins? Lancet Neurol. 2, 531-538.
23. Dixon, A. L., Prior, M., Morris, P. M., Shah, Y. B., Joseph, M. H., and Young, A. M. (2005). Dopamine antagonist modulation of amphetamine response as detected using pharmacological MRI. Neuropharmacology 48, 236-245.
24. Easton, N., Marshall, F., Fone, K. C., and Marsden, C. A. (2007). Differential effects of the D-and L-isomers of amphetamine on pharmacological MRI BOLD contrast in the rat. Psychopharmacology (Berl.) 193, 11-30.
25. Erikson, K. M., Dorman, D. C., Lash, L. H., and Aschner, M. (2007). Manganese inhalation by rhesus monkeys is associated with brain regional changes in biomarkers of neurotoxicity. Toxicol. Sci. 97, 459-466.
26. Eriksson, H., Gillberg, P. G., Aquilonius, S. M., Hedstrom, K. G., and Heilbronn, E. (1992a). Receptor alterations in manganese intoxicated monkeys. Arch. Toxicol. 66, 359-364.
27. Eriksson, H., Tedroff, J., Thuomas, K. A., Aquilonius, S. M., Hartvig, P., Fasth, K. J., Bjurling, P., Langstrom, B., Hedstrom, K. G., and Heilbronn, E. (1992b). Manganese induced brain lesions in Macaca fascicularis as revealed by positron emission tomography and magnetic resonance imaging. Arch. Toxicol. 66, 403-407.
28. Ferraz, H. B., Bertolucci, P. H., Pereira, J. S., Lima, J. G., and Andrade, L. A. (1988). Chronic exposure to the fungicide maneb may produce symptoms and signs of CNS manganese intoxication. Neurology 38, 550-553.
29. Fitsanakis, V. A., Au, C., Erikson, K. M., and Aschner, M. (2006). The effects of manganese on glutamate, dopamine and gamma-aminobutyric acid regulation. Neurochem. Int. 48, 426-433.
30. Fitsanakis, V. A., Zhang, N., Anderson, J. G., Erikson, K. M., Avison, M. J., Gore, J. C., and Aschner, M. (2008). Measuring brain manganese and iron accumulation in rats following 14 weeks of low-dose manganese treatment using atomic absorption spectroscopy and magnetic resonance imaging. Toxicol. Sci. 103, 116-124.
31. Giros, B., Jaber, M., Jones, S. R., Wightman, R. M., and Caron, M. G. (1996). Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379, 606-612.
32. Gore, J. C. (2003). Principles and practice of functional MRI of the human brain. J. Clin. Invest. 112, 4-9.
33. 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. (2008). Impairment of nigrostriatal dopamine neurotransmission by manganese is mediated by pre-synaptic mechanism(s): implications to manganese-induced parkinsonism. J. Neurochem. 107, 1236-1247.
34. Guilarte, T. R., Chen, M. K., McGlothan, J. L., Verina, T., Wong, D. F., Zhou, Y., Alexander, M., Rohde, C. A., Syversen, T., Decamp, E., et al. (2006). Nigrostriatal dopamine system dysfunction and subtle motor deficits in manganese-exposed non-human primates. Exp. Neurol. 202, 381-390.
35. Huang, C. C., Chu, N. S., Lu, C. S., Chen, R. S., and Calne, D. B. (1998). Long-term progression in chronic manganism: ten years of follow-up. Neurology 50, 698-700.
36. Huang, C. C., Weng, Y. H., Lu, C. S., Chu, N. S., and Yen, T. C. (2003). Dopamine transporter binding in chronic manganese intoxication. J. Neurol. 250, 1335-1339.
37. Ingersoll, R. T., Montgomery, E. B. J., and Aposhian, H. V. (1999). Central nervous system toxicity of manganese. II: cocaine or reserpine inhibit manganese concentration in the rat brain. Neurotoxicology 20, 467-476.
38. Kahlig, K. M., and Galli, A. (2003). Regulation of dopamine transporter function and plasma membrane expression by dopamine, amphetamine, and cocaine. Eur. J. Pharmacol. 479, 153-158.
39. Kim, Y. (2006). Neuroimaging in manganism. Neurotoxicology 27, 369-372.
40. Kim, Y., Kim, J. M., Kim, J. W., Yoo, C. I., Lee, C. R., Lee, J. H., Kim, H. K., Yang, S. O., Chung, H. K., Lee, D. S., et al. (2002). Dopamine transporter density is decreased in parkinsonian patients with a history of manganese exposure: what does it mean? Mov. Disord. 17, 568-575.
41. Klockgether, T., and Turski, L. (1989). Excitatory amino acids and the basal ganglia: implications for the therapy of Parkinson's disease. Trends Neurosci. 12, 285-286.
42. Koob, G. F. (2006). The neurobiology of addiction: a neuroadaptational view relevant for diagnosis. Addiction 101(Suppl. 1), 23-30.
43. Kuo, Y. T., Herlihy, A. H., So, P. W., Bhakoo, K. K., and Bell, J. D. (2005). In vivo measurements of T1 relaxation times in mouse brain associated with different modes of systemic administration of manganese chloride. J. Magn. Reson. Imaging 21, 334-339.
44. Leenders, K. L., Salmon, E. P., Tyrrell, P., Perani, D., Brooks, D. J., Sager, H., Jones, T., Marsden, C. D., and Frackowiak, R. S. (1990). The nigrostriatal dopaminergic system assessed in vivo by positron emission tomography in healthy volunteer subjects and patients with Parkinson's disease. Arch. Neurol. 47, 1290-1298.
45. Logothetis, N. K. (2003). The underpinnings of the BOLD functional magnetic resonance imaging signal. J Neurosci 23, 3963-3971.
46. Logothetis, N. K., and Pfeuffer, J. (2004). On the nature of the BOLD fMRI contrast mechanism. Magn. Reson. Imaging 22, 1517-1531.
47. Mahoney, J. P., and Small, W. J. (1968). Studies on manganese. 3. The biological half-life of radiomanganese in man and factors which affect this half-life. J. Clin. Invest. 47, 643-653.
48. McDonald, M. C., d'Emmanuele di Villa Bianca, R., Wayman, N. S., Pinto, A., Sharpe, M. A., Cuzzocrea, S., Chatterjee, P. K., and Thiemermann, C. (2003). A superoxide dismutase mimetic with catalase activity (EUK-8) reduces the organ injury in endotoxic shock. Eur. J. Pharmacol. 466, 181-189.
49. Mergler, D. (1999). Neurotoxic effects of low level exposure to manganese in human populations. Environ. Res. 80, 99-102.
50. Muller-Gartner, H. W. (1998). Imaging techniques in the analysis of brain function and behaviour. Trends Biotechnol. 16, 122-130.
51. Nam, J., and Kim, K. (2008). Abnormal motor function and the expression of striatal dopamine D2 receptors in manganese-treated mice. Biol. Pharm. Bull. 31, 1894-1897.
52. Narita, K., Kawasaki, F., and Kita, H. (1990). Mn and Mg influxes through Ca channels of motor nerve terminals are prevented by verapamil in frogs. Brain Res. 510, 289-295.
53. Newland, M. C., Ceckler, T. L., Kordower, J. H., and Weiss, B. (1989). Visualizing manganese in the primate basal ganglia with magnetic resonance imaging. Exp. Neurol. 106, 251-258.
54. Nirenberg, M. J., Vaughan, R. A., Uhl, G. R., Kuhar, M. J., and Pickel, V. M. (1996). The dopamine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons. J. Neurosci. 16, 436-447.
55. Ogawa, S., Lee, T. M., Kay, A. R., and Tank, D. W. (1990). Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. U.S.A 87, 9868-9872.
56. Olanow, C. W. (2004). Manganese-induced parkinsonism and Parkinson's disease. Ann. N. Y. Acad. Sci. 1012, 209-223.
57. Pal, P. K., Samii, A., and Calne, D. B. (1999). Manganese neurotoxicity: a review of clinical features, imaging and pathology. Neurotoxicology 20, 227-238.
58. Park, N. H., Park, J. K., Choi, Y., Yoo, C. I., Lee, C. R., Lee, H., Kim, H. K., Kim, S. R., Jeong, T. H., Park, J., et al. (2003). Whole blood manganese correlates with high signal intensities on T1-weighted MRI in patients with liver cirrhosis. Neurotoxicology 24, 909-915.
59. Paxinos, G., and Watson, C. (1998). The Rat Brain in Stereotaxic Coordinates, (4th ed). Academic Press, New York.
60. Perl, D. P., and Olanow, C. W. (2007). The neuropathology of manganese-induced parkinsonism. J. Neuropathol. Exp. Neurol. 66, 675-682.
61. Pirker, W., Djamshidian, S., Asenbaum, S., Gerschlager, W., Tribl, G., Hoffmann, M., and Brucke, T. (2002). Progression of dopaminergic degeneration in Parkinson's disease and atypical parkinsonism: a longitudinal beta-CIT SPECT study. Mov. Disord. 17, 45-53.
62. Racette, B. A., Antenor, J. A., McGee-Minnich, L., Moerlein, S. M., Videen, T. O., Kotagal, V., and Perlmutter, J. S. (2005). [18F]FDOPA PET and clinical features in parkinsonism due to manganism. Mov. Disord. 20, 492-496.
63. Racette, B. A., McGee-Minnich, L., Moerlein, S. M., Mink, J. W., Videen, T. O., and Perlmutter, J. S. (2001). Welding-related parkinsonism: clinical features, treatment, and pathophysiology. Neurology 56, 8-13.
64. Shinotoh, H., Snow, B. J., Chu, N. S., Huang, C. C., Lu, C. S., Lee, C., Takahashi, H., and Calne, D. B. (1997). Presynaptic and postsynaptic striatal dopaminergic function in patients with manganese intoxication: a positron emission tomography study. Neurology 48, 1053-1056.
65. Shinotoh, H., Snow, B. J., Hewitt, K. A., Pate, B. D., Doudet, D., Nugent, R., Perl, D. P., Olanow, W., and Calne, D. B. (1995). MRI and PET studies of manganese-intoxicated monkeys. Neurology 45, 1199-1204.
66. Sloot, W. N., and Gramsbergen, J. B. (1994). Axonal transport of manganese and its relevance to selective neurotoxicity in the rat basal ganglia. Brain Res. 657, 124-132.
67. Sloot, W. N., van der Sluijs-Gelling, A. J., and Gramsbergen, J. B. (1994). Selective lesions by manganese and extensive damage by iron after injection into rat striatum or hippocampus. J. Neurochem. 62, 205-216.
68. Stepens, A., Logina, I., Liguts, V., Aldins, P., Eksteina, I., Platkajis, A., Martinsone, I., Terauds, E., Rozentale, B., and Donaghy, M. (2008). A parkinsonian syndrome in methcathinone users and the role of manganese. N. Engl. J. Med. 358, 1009-1017.
69. Steward, C. A., Marsden, C. A., Prior, M. J., Morris, P. G., and Shah, Y. B. (2005). Methodological considerations in rat brain BOLD contrast pharmacological MRI. Psychopharmacology (Berl.) 180, 687-704.
70. Sulzer, D., Sonders, M. S., Poulsen, N. W., and Galli, A. (2005). Mechanisms of neurotransmitter release by amphetamines: a review. Prog. Neurobiol. 75, 406-433.
71. Suzuki, H., Takanashi, J., Saeki, N., and Kohno, Y. (2003). Temporal parenteral nutrition in children causing T1 shortening in the anterior pituitary gland and globus pallidus. Neuropediatrics 34, 200-204.
72. Takeda, A. (2003). Manganese action in brain function. Brain Res. Brain Res. Rev. 41, 79-87.
73. Takeda, A., Sotogaku, N., and Oku, N. (2002). Manganese influences the levels of neurotransmitters in synapses in rat brain. Neuroscience 114, 669-674.
74. Wichmann, T., and DeLong, M. R. (2003). Functional neuroanatomy of the basal ganglia in Parkinson's disease. Adv. Neurol. 91, 9-18.
75. Williams, J. M., and Galli, A. (2006). The dopamine transporter: a vigilant border control for psychostimulant action. Handb. Exp. Pharmacol. 175, 215-232.
76. Williams, J. M., Owens, W. A., Turner, G. H., Saunders, C., Dipace, C., Blakely, R. D., France, C. P., Gore, J. C., Daws, L. C., Avison, M. J., et al. (2007). Hypoinsulinemia regulates amphetamine-induced reverse transport of dopamine. PLoS Biol. 5, 2369-2378.
77. Wise, R. A. (2004). Dopamine, learning and motivation. Nat. Rev. Neurosci. 5, 483-494.
78. Wise, R. A. (2005). Forebrain substrates of reward and motivation. J. Comp. Neurol. 493, 115-121.
79. Wise, R. G., and Tracey, I. (2006). The role of fMRI in drug discovery. J. Magn. Reson. Imaging 23, 862-876.
80. 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.
81. Xu, X. R., Li, H. B., Wang, W. H., and Gu, J. D. (2005). Decolorization of dyes and textile wastewater by potassium permanganate. Chemosphere 59, 893-898.
82. Zhang, N., Fitsanakis, V. A., Erikson, K. M., Aschner, M., Avison, M. J., and Gore, J. C. (2009). A model for the analysis of competitive relaxation effects of manganese and iron in vivo. NMR Biomed. 22, 391-404.