Subacute manganese exposure in rats is a neurochemical model of early manganese toxicity

NeuroToxicology

Volumn 44, Issue , 2014, Pages 303-313

  O'Neal, Stefanie L ^a   Lee, Jang Won ^a   Zheng, Wei ^a   Cannon, Jason R ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Dopamine; GABA; Manganese; Manganism; Neurobehavior; Serotonin

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 4 AMINOBUTYRIC ACID; DOPAMINE; HOMOVANILLIC ACID; MANGANESE; NEUROTRANSMITTER; NORADRENALIN; SEROTONIN; BIOGENIC AMINE; 5 HYDROXYINDOLEACETIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE BRAIN LEVEL; DOPAMINERGIC SYSTEM; EXPOSURE; GABAERGIC SYSTEM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; INTOXICATION; MALE; METABOLITE; NEUROCHEMISTRY; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; RAT; SEROTONINERGIC SYSTEM; SUBSTANTIA NIGRA; TOXICITY TESTING; WEIGHT REDUCTION; ANIMAL; BODY WEIGHT; BRAIN; CHEMISTRY; DRUG EFFECTS; METABOLISM; MOTOR ACTIVITY; SPRAGUE DAWLEY RAT; BRAIN TOXICITY; DOSE RESPONSE; HYPOACTIVITY; IMMUNOHISTOCHEMISTRY; LOCOMOTION; NEUROTRANSMISSION; SUBACUTE MANGANESE EXPOSURE;

ANIMALS; BIOGENIC MONOAMINES; BODY WEIGHT; BRAIN; CORPUS STRIATUM; DOPAMINE; HIPPOCAMPUS; MALE; MANGANESE; MOTOR ACTIVITY; NOREPINEPHRINE; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; SUBSTANTIA NIGRA;

RATTUS;

EID: 84907339453     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2014.08.001     Document Type: Article

References (64)

1. Andersen M.E., Dorman D.C., Clewell H.J., Taylor M.D., Nong A. Multi-dose-route, multi-species pharmacokinetic models for manganese and their use in risk assessment. J Toxicol Environ Health A 2010, 73(2):217-234. 10.1080/15287390903340849.
2. Aschner M., Vrana K.E., Zheng W. Manganese uptake and distribution in the central nervous system. Neurotoxicology 1999, 20(2-3):173-180.
3. Aschner M., Erikson K.M., Herrero Hernández E., Hernández E.H., Tjalkens R. Manganese and its role in Parkinson's disease: from transport to neuropathology. Neuromol Med 2009, 11(4):252-266. 10.1007/s12017-009-8083-0.
4. Aschner M., Guilarte T.R., Schneider J.S., Zheng W. Manganese: recent advances in understanding its transport and neurotoxicity. Toxicol Appl Pharmacol 2007, 221(2):131-147.
5. Autissier N., Rochette L., Dumas P., Beley A., Loireau A., Bralet J. Dopamine and norepinephrine turnover in various regions of the rat brain after chronic manganese chloride administration. Toxicology 1982, 24:175-182.
6. Blecharz-Klin K., Piechal A., Joniec-Maciejak I., Pyrzanowska J., Widy-Tyszkiewicz E. Effect of intranasal manganese administration on neurotransmission and spatial learning in rats. Toxicol Appl Pharmacol 2012, 265(1):1-9. 10.1016/j.taap.2012.09.015.
7. Bonilla E. L-tyrosine hydroxylase activity in the rat brain after chronic oral administration of manganese chloride. Neurobehav Toxicol 1980, 2(1):37-41.
8. Bouchard M., Laforest F., Vandelac L., Bellinger D., Mergler D. Hair manganese and hyperactive behaviors: pilot study of school-age children exposed through tap water. Environ Health Perspect 2007, 115(1):122-127.
9. Bowman A.B., Kwakye G.F., Hernández E.H., Aschner M. Role of manganese in neurodegenerative diseases. J Trace Elem Med Biol 2011, 25(4):191-203. 10.1016/j.jtemb.2011.08.144.
10. Bradford M.A. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
11. Calabresi P., Ammassari-Teule M., Gubellini P., Sancesario G., Morello M., Centonze D., et al. A synaptic mechanism underlying the behavioral abnormalities induced by manganese intoxication. Neurobiol Dis 2001, 8(3):419-432. 10.1006/nbdi.2000.0379.
12. Cannon J.R., Geghman K.D., Tapias V., Sew T., Dail M.K., Li C., et al. Expression of human E46K-mutated a-synuclein in BAC-transgenic rats replicates early-stage Parkinson's disease features and enhances vulnerability to mitochondrial impairment. Exp Neurol 2013, 240:44-56. PMID: 23153578. 10.1016/j.expneurol.2012.11.007.
13. Cannon J.R., Tapias V., Na H.M., Honick A.S., Drolet R.E., Greenamyre J.T. A highly reproducible rotenone model of Parkinson's disease. Neurobiol Dis 2009, 34(2):279-290.
14. Cannon J.R., Nakamura T., Keep R.F., Richardson R.J., Hua Y., Xi G. Dopamine changes in a rat model of intracerebral hemorrhage. Acta Neurochir Suppl (Wien) 2006, 96:222-226. PMID: 16671459.
15. Careau V., Bininda-Emonds O.R., Ordonez G., Garland T. Are Voluntary wheel running and open-field behavior correlated in mice? Different answers from comparative and artificial selection approaches. Behav Genet 2012, 42(5):830-844.
16. Chandra S.V., Shukla G.S. Concentrations of striatal catecholamines in rats given manganese chloride through drinking water. J Neurochem 1981, 36(2):683-687. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/7463083.
17. Chandra S.V., Shukla G.S., Murthy R.C. Effect of stress on the response of rat brain to manganese. Toxicol Appl Pharmacol 1979, 47(3):603-608. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/442097.
18. Chandra S.V., Shukla G.S., Saxena D.K. Manganese-induced behavioral dysfunction and its neurochemical mechanism in growing mice. J Neurochem 1979, 33(6):1217-1221. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/552401.
19. Cotzias G.C., Papavasiliou P.S., Mena I., Tang L.C., Miller S.T. Manganese and catecholamines. Adv Neurol 1974, 5:235-243.
20. Cotzias G.C. Manganese in health and disease. Physiol Rev 1958, 38:503-532.
21. Crossgrove J., Zheng W. Manganese toxicity upon overexposure. NMR Biomed 2004, 17(8):544-553. 10.1002/nbm.931.
22. Dobson A.W., Erikson K.M., Aschner M. Manganese neurotoxicity. Ann NY Acad Sci 2004, 1012:115-128. 10.1196/annals.1306.009.
23. Dodd C.A., Bloomquist J.R., Klein B.G. Consequences of manganese administration for striatal dopamaine and motor behavior in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposed C57BL/6 mice. Hum Exp Toxicol 2013, 32(8):865-880.
24. Faul F., Edrfelder E., Lang A.-G., Buchner A. G * Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 2007, 39:175-191.
25. Fitsanakis V.A., Zhang N., Anderson J.G., Erikson K.M., Avison M.J., Gore J.C., et al. 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 2008, 103(1):116-124. 10.1093/toxsci/kfn019.
26. Gianutsos G., Murray M.T. Alterations in brain dopamine and GABA following inorganic or organic manganese administration. Neurotoxicology 1982, 3(3):75-82.
27. Guilarte T.R. Manganese and Parkinson's disease: a critical review and new findings. Environ Health Perspect 2010, 118(8):1071-1080. 10.1289/ehp.0901748.
28. Guilarte T., Chen M.K., McGlothan J.L., Verina T., Wong D.F., Zhou Y. Nigrostriatal dopamine system dysfunction and subtle motor deficits in manganese-exposed non-human primates. Exp Neurol 2006, 202:381-390.
29. Gwiazda R., Lucchini R., Smith D. Adequacy and consistency of animal studies to evaluate the neurotoxicity of chronic low-level manganese exposure in humans. J Toxicol Environ Health A 2007, 70(7):594-605. 10.1080/10937400600882897.
30. Gwiazda R.H., Lee D., Sheridan J., Smith D.R. Low cumulative manganese exposure affects striatal GABA but not dopamine. Neurotoxicology 2002, 23:69-76.
31. Hastings T.G., Zigmond M.J. Identification of catechol-protein conjugates in neostriatal slices incubated with [3H]dopamine: impact of ascorbic acid and glutathione. J Neurochem 1994, 63:1126-1132. PMID: 8051554.
32. Hong J.S., Hung C.R., Seth P.K., Mason G., Bondy S.C. Effect of manganese treatment on the levels of neurotransmitters, hormones, and neuropeptides: modulation by stress. Environ Res 1984, 34(2):242-249.
33. Husain M., Khanna V.K., Roy A., Tandon R., Pradeep S., Set P.K. Platelet dopamine receptors and oxidative stress parameters as markers of manganese toxicity. Hum Exp Toxicol 2001, 20(12):631-636.
34. Khalid M., Aoun R.A., Mathews T.A. Altered striatal dopamine release following a sub-acute exposure to manganese. J Neurosci Methods 2011, 202:182-191.
35. Klassen C.D. Biliary excretion of metals. Drug Metab Rev 1976, 5:165-196.
36. Kunar M.J., Couceyro P.R., Lambert P.D. Catecholamines. Basic neurochemistry molecular, cellular, and medical aspects 1999, 243-261. Lippincott-Raven, Philadelphia, PA. G.J. Siegel, B.W. Agranoff, R.W. Albers, S.K. Fisher, M.D. Uhler (Eds.).
37. Lebda M.A., El-Neweshy M.S., El-Sayed Y.S. Neurotoxicology 2012, 33(1):98-104.
38. Madison J.L., Wegrzynowicz M., Aschner M., Bowman A.B. Disease-toxicant interactions in manganese exposed Huntington Disease mice: early changes in striatal neuron morphology and dopamine metabolism. PLoS ONE 2012, 7(2).
39. McMillian D.E. A brief history of the neurobehavioral toxicity of manganese: some unanswered questions. Neurotoxicology 1999, 20(2-3):499-508.
40. Meerlo P., Overkamp G.J., Benning M.A., Koolhaas J.M., Van den Hoofdakker R.H. Long-term changes in open field behavior following a single social defeat in rats can be reversed by sleep deprivation. Physiol Behav 1996, 60(1):115-119.
41. Mergler D., Baldwin M., Belanger S., Larribe F., Beuter A., Bowler R., et al. Manganese neurotoxicity, a continuum of dysfunction: results from a community based study. Neurotoxicology 1999, 20(2-3):327-342.
42. Nachtman J.P., Tubben R.E., Commissaris R.L. Behavioral effects of chronic manganese administration in rats: locomotor activity studies. Neurobehav Toxicol Teratol 1986, 8(6):711-715. PMID: 3808186.
43. Newland M.C. Animal models of manganese's neurotoxicity. Neurotoxicology 1999, 20(2-3):415-432.
44. O'Neal S.L., Hong L., Fu S., Jiang W., Jones A., Nie L.H., et al. Manganese accumulation in bone following chronic exposure in rats: Steady-state concentration and half-life in bone. Toxicol Lett 2014, 229:93-100.
45. Ordoñez-Librado J.L., Gutierrez-Valdez L., Colín-Barenque L., Anaya-Martínez V., Díaz-Bech P., Avila-Costa M.R. Inhalation of divalent and trivalent manganese mixture induces a Parkinson's disease model: immunocytochemical and behavioral evidences. Neuroscience 2008, 155(1):7-16. 10.1016/j.neuroscience.2008.05.012.
46. Oszlanczi G., Vezer T., Sarkozi L., Horvath E., Szabo A., Horvath E., et al. Metal disposition and functional neurotoxicity in rats after 3-6 weeks nasal exposure by two physicochemical forms of manganese. Environ Toxicol Pharmacol 2010, 30(2):121-126.
47. Ou C.Y., Huang M.L., Jiang Y.M., Luo H.L., Deng X.F., Wang C., et al. Effect of sodium-paraminosalicylic acid on concentrations of amino acid neurotransmitters in basal ganglia of manganese-exposed rats. Zhonghua Yu Fang Yi Xue Za Zhi 2011, 45(5):422-425.
48. Pechlivanova D., Tchekalarova J., Nikolov R., Yakimova K. Dose-dependent effects of caffeine on behavior and thermoregulation in a chronic unpredictable stress model of depression in rats. Behav Brain Res 2010, 19(2):205-211.
49. Pothos E.N., Hernandez L., Hoebel B.G. Chronic food deprivation decreases extracellular dopamine in the nucleus accumbens: implications for a possible neurochemical link between weight loss and drug abuse. Obes Res 1995, 3(Suppl 4):525S-529S.
50. Robison G., Zakharova T., Fu S., Jiang W., Fulper R., Barrea R., et al. X-ray fluorescence imaging: a new tool for studying manganese neurotoxicity. PLoS ONE 2012, 7(11):1-9.
51. Rodier J. Manganese poisoning in Moroccan miners. Br J Ind Med 1955, 12:21-35.
52. Roth J.A. Are there common biochemical and molecular mechanisms controlling manganism and parkinsonism. Neuromol Med 2009, 11(4):281-296. 10.1007/s12017-009-8088-8.
53. Sarkar S., Schmued L. The fluoro-jade dyes: novel, sensitive, and reliable fluorochromes for the histochemical localization of degenerating neurons. Fundamental neuropathology for pathologists and toxicologists principles and techniques 2011, 171-179. Wiley & Sons, Inc., Hoboken, NJ. B. Bolon, M.T. Butt (Eds.).
54. Schneider J.S., Decamp E., Clark K., Bouquio C., Syversen T., Guilarte T.R. Effects of chronic manganese exposure on working memory in non-human primates. Brain Res 2009, 1258:86-95. 10.1016/j.brainres.2008.12.035.
55. Schwarting R.K., Huston J.P. Unilateral 6-hydroxydopamine lesions of meso-striatal dopamine neurons and their physiological sequelae. Prog Neurobiol 1996, 49(3):215-266. PMID: 8878304.
56. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., et al. Measurement of protein using bicinchoninic acid. Anal Biochem 1985, 150:76-85.
57. Tapias V., Cannon J.R., Greenamyre J.T. Pomegranate juice exacerbates oxidative stress and nigrostriatal degeneration in Parkinson's disease. Neurobiol Aging 2014, 35(5):1162-1176. PMID: 24315037.
58. Torrente M., Colomina M.T., Domingo J.L. Behavioral effects of adult rats concurrently exposed to high doses of oral manganese and restraint stress. Toxicology 2005, 211(1-2):59-69.
59. Vezér T., Kurunczi A., Naray M., Papp A., Nagymajtenyi L. Behavioral effects of subchronic inorganic manganese exposure in rats. Am J Ind Med 2007, 50:841-852. 10.1002/ajim.20485.
60. Vidal L., Alfonso M., Campos F., Faro L.R.F., Cervantes R.C., Duran R. Effects of manganese on extracellular levels of dopamine in rat striatum: an analysis in vivo by brain microdialysis. Neurochem Res 2005, 30(9):1147-1154.
61. Wang Y., Lee J.W., Oh G., Grady S.R., McIntosh J.M., Brunzell D.H., et al. Enhanced synthesis and release of dopamine in transgenic mice with gain-of-function α6* nAChRs. J Neurochem 2014, 10.1111/jnc.12616.
62. Williams J.M., Milatovic D., Gore J.C., Aschner M., Avison M.J. Chronic exposure to manganese alters brain responses to amphetamine: a pharmacological magnetic resonance imaging study. Toxicol Sci 2010, 114(2):310-322.
63. Zheng W., Jiang Y.-M., Zhang Y., Jiang W., Wang X., Cowan D.M. Chelation therapy of manganese intoxication with para-aminosalicylic acid (PAS) in Sprague-Dawley rats. Neurotoxicology 2009, 30(2):240-248. 10.1016/j.neuro.2008.12.007.
64. Zheng W., Zhao Q., Slavkovich V., Aschner M., Graziano J.H. Alteration of iron homeostasis following chronic exposure to manganese in rats. Brain Res 1999, 833:125-132.