Gender and manganese exposure interactions on mouse striatal neuron morphology

NeuroToxicology

Volumn 32, Issue 6, 2011, Pages 896-906

  Madison, Jennifer L ^a,b   Wegrzynowicz, Michal ^b   Aschner, Michael ^a,b   Bowman, Aaron B ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Gender; Manganese; Medium spiny neuron; Neuron morphology

Indexed keywords

MANGANESE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL FUNCTION; CELL LEVEL; CELL STRUCTURE; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITIC SPINE; FEMALE; MALE; MOUSE; NEUROPATHOLOGY; NEUROTOXICOLOGY; NONHUMAN; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SEX DIFFERENCE;

ANALYSIS OF VARIANCE; ANIMALS; BASAL GANGLIA; CELL SHAPE; CHLORIDES; DENDRITES; ENVIRONMENTAL POLLUTANTS; FEMALE; MALE; MANGANESE COMPOUNDS; MICE; NEURONS; RISK ASSESSMENT; RISK FACTORS; SEX FACTORS; TIME FACTORS;

ANIMALIA; MUS;

EID: 80055075460     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2011.05.007     Document Type: Article

References (91)

1. Akesson A., Berglund M., Schutz A., Bjellerup P., Bremme K., Vahter M. Cadmium exposure in pregnancy and lactation in relation to iron status. Am J Public Health 2002, 92:284-287.
2. Akesson A., Lundh T., Vahter M., Bjellerup P., Lidfeldt J., Nerbrand C., et al. Tubular and glomerular kidney effects in Swedish women with low environmental cadmium exposure. Environ Health Perspect 2005, 113:1627-1631.
3. Aschner M., Erikson K.M., Dorman D.C. Manganese dosimetry: species differences and implications for neurotoxicity. Crit Rev Toxicol 2005, 35:1-32.
4. Aschner M., Guilarte T.R., Schneider J.S., Zheng W. Manganese: recent advances in understanding its transport and neurotoxicity. Toxicol Appl Pharmacol 2007, 221:131-147.
5. Baraka A.M., Korish A.A., Soliman G.A., Kamal H. The possible role of estrogen and selective estrogen receptor modulators in a rat model of Parkinson's disease. Life Sci 2011.
6. Bjorkman L., Vahter M., Pedersen N.L. Both the environment and genes are important for concentrations of cadmium and lead in blood. Environ Health Perspect 2000, 108:719-722.
7. Bonate P.L. Gender-related differences in xenobiotic metabolism. J Clin Pharmacol 1991, 31:684-690.
8. Bowler R.M., Gysens S., Diamond E., Nakagawa S., Drezgic M., Roels H.A. Manganese exposure: neuropsychological and neurological symptoms and effects in welders. Neurotoxicology 2006, 27:315-326.
9. Bowler R.M., Nakagawa S., Drezgic M., Roels H.A., Park R.M., Diamond E., et al. Sequelae of fume exposure in confined space welding: a neurological and neuropsychological case series. Neurotoxicology 2007, 28:298-311.
10. Bowler R.M., Roels H.A., Nakagawa S., Drezgic M., Diamond E., Park R., et al. Dose-effect relationships between manganese exposure and neurological, neuropsychological and pulmonary function in confined space bridge welders. Occup Environ Med 2007, 64:167-177.
11. Calne D.B., Chu N.S., Huang C.C., Lu C.S., Olanow W. Manganism and idiopathic parkinsonism: similarities and differences. Neurology 1994, 44:1583-1586.
12. Clewell H.J., Teeguarden J., McDonald T., Sarangapani R., Lawrence G., Covington T., et al. Review and evaluation of the potential impact of age- and gender-specific pharmacokinetic differences on tissue dosimetry. Crit Rev Toxicol 2002, 32:329-389.
13. Davis C.D., Greger J.L. Longitudinal changes of manganese-dependent superoxide dismutase and other indexes of manganese and iron status in women. Am J Clin Nutr 1992, 55:747-752.
14. Day M., Wang Z., Ding J., An X., Ingham C.A., Shering A.F., et al. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat Neurosci 2006, 9:251-259.
15. Deutch A.Y., Colbran R.J., Winder D.J. Striatal plasticity and medium spiny neuron dendritic remodeling in parkinsonism. Parkinsonism Relat Disord. 2007, 3(13 Suppl.):S251-S258.
16. Diaz C., Lopez F., Henriquez P., Rodriguez E., Serra-MaJem L. Serum manganese concentrations in a representative sample of the Canarian population. Biol Trace Elem Res 2001, 80:43-51.
17. Dobson A.W., Erikson K.M., Aschner M. Manganese neurotoxicity. Ann N Y Acad Sci 2004, 1012:115-128.
18. Dodd C.A., Ward D.L., Klein B.G. Basal Ganglia accumulation and motor assessment following manganese chloride exposure in the C57BL/6 mouse. Int J Toxicol 2005, 24:389-397.
19. Dorman D.C., McManus B.E., Marshall M.W., James R.A., Struve M.F. Old age and gender influence the pharmacokinetics of inhaled manganese sulfate and manganese phosphate in rats. Toxicol Appl Pharmacol 2004, 197:113-124.
20. Erikson K.M., Dorman D.C., Lash L.H., Dobson A.W., Aschner M. Airborne manganese exposure differentially affects end points of oxidative stress in an age- and sex-dependent manner. Biol Trace Elem Res 2004, 100:49-62.
21. Erikson K.M., Shihabi Z.K., Aschner J.L., Aschner M. Manganese accumulates in iron-deficient rat brain regions in a heterogeneous fashion and is associated with neurochemical alterations. Biol Trace Elem Res 2002, 87:143-156.
22. Erikson K.M., Syversen T., Steinnes E., Aschner M. Globus pallidus: a target brain region for divalent metal accumulation associated with dietary iron deficiency. J Nutr Biochem 2004, 15:335-341.
23. Finley J.W., Johnson P.E., Johnson L.K. Sex affects manganese absorption and retention by humans from a diet adequate in manganese. Am J Clin Nutr 1994, 60:949-955.
24. 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, 103:116-124.
25. Fletcher C.V., Acosta E.P., Strykowski J.M. Gender differences in human pharmacokinetics and pharmacodynamics. J Adolesc Health 1994, 15:619-629.
26. Fortoul T.I., Moncada-Hernandez S., Saldivar-Osorio L., Espejel-Maya G., Mussali-Galante P., del Carmen Avila-Casado M., et al. Sex differences in bronchiolar epithelium response after the inhalation of lead acetate (Pb). Toxicology 2005, 207:323-330.
27. Galea L.A., McEwen B.S., Tanapat P., Deak T., Spencer R.L., Dhabhar F.S. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 1997, 81:689-697.
28. Garcia B.G., Neely M.D., Deutch A.Y. Cortical regulation of striatal medium spiny neuron dendritic remodeling in parkinsonism: modulation of glutamate release reverses dopamine depletion-induced dendritic spine loss. Cereb Cortex 2010, 20:2423-2432.
29. George S., van den Buuse M., San Mok S., Masters C.L., Li Q.X., Culvenor J.G. Alpha-synuclein transgenic mice exhibit reduced anxiety-like behaviour. Exp Neurol 2008, 210:788-792.
30. Gorell J.M., Johnson C.C., Rybicki B.A., Peterson E.L., Kortsha G.X., Brown G.G., et al. Occupational exposures to metals as risk factors for Parkinson's disease. Neurology 1997, 48:650-658.
31. Gorell J.M., Rybicki B.A., Cole Johnson C., Peterson E.L. Occupational metal exposures and the risk of Parkinson's disease. Neuroepidemiology, Switzerland 1999, 303-308.
32. Grandjean P., Weihe P., White R.F., Debes F. Cognitive performance of children prenatally exposed to " safe" levels of methylmercury. Environ Res 1998, Academic Press, United States, p. 165-72.
33. Greger J.L., Davis C.D., Suttie J.W., Lyle B.J. Intake, serum concentrations, and urinary excretion of manganese by adult males. Am J Clin Nutr 1990, 51:457-461.
34. Guilarte T.R., Burton N.C., McGlothan J.L., Verina T., Zhou Y., Alexander M., et al. Impairment of nigrostriatal dopamine neurotransmission by manganese is mediated by pre-synaptic mechanism(s): implications to manganese-induced parkinsonism. J Neurochem 2008, 107:1236-1247.
35. Guilarte T.R., Chen M.K., McGlothan J.L., Verina T., Wong D.F., Zhou Y., et al. Nigrostriatal dopamine system dysfunction and subtle motor deficits in manganese-exposed non-human primates. Exp Neurol 2006, 202:381-390.
36. Gulson B.L., Mahaffey K.R., Jameson C.W., Mizon K.J., Korsch M.J., Cameron M.A., et al. Mobilization of lead from the skeleton during the postnatal period is larger than during pregnancy. J Lab Clin Med 1998, 131:324-329.
37. Haaxma C.A., Bloem B.R., Borm G.F., Oyen W.J., Leenders K.L., Eshuis S., et al. Gender differences in Parkinson's disease. J Neurol Neurosurg Psychiatry 2007, 78:819-824.
38. Harris R.Z., Benet L.Z., Schwartz J.B. Gender effects in pharmacokinetics and pharmacodynamics. Drugs 1995, 50:222-239.
39. Huang C.C., Chu N.S., Lu C.S., Wang J.D., Tsai J.L., Tzeng J.L., et al. Chronic manganese intoxication. Arch Neurol 1989, 46:1104-1106.
40. Huang C.C., Weng Y.H., Lu C.S., Chu N.S., Yen T.C. Dopamine transporter binding in chronic manganese intoxication. J Neurol 2003, 250:1335-1339.
41. Jiang Y., Zheng W., Long L., Zhao W., Li X., Mo X., et al. Brain magnetic resonance imaging and manganese concentrations in red blood cells of smelting workers: search for biomarkers of manganese exposure. Neurotoxicology 2007, 28:126-135.
42. Jin T., Wu X., Tang Y., Nordberg M., Bernard A., Ye T., et al. Environmental epidemiological study and estimation of benchmark dose for renal dysfunction in a cadmium-polluted area in China. Biometals 2004, 17:525-530.
43. Juraska J.M. Sex differences in dendritic response to differential experience in the rat visual cortex. Brain Res 1984, 295:27-34.
44. Juraska J.M., Fitch J.M., Henderson C., Rivers N. Sex differences in the dendritic branching of dentate granule cells following differential experience. Brain Res 1985, 333:73-80.
45. Juraska J.M., Fitch J.M., Washburne D.L. The dendritic morphology of pyramidal neurons in the rat hippocampal CA3 area II. Effects of gender and the environment. Brain Res 1989, 479:115-119.
46. Kessler K.R., Wunderlich G., Hefter H., Seitz R.J. Secondary progressive chronic manganism associated with markedly decreased striatal D2 receptor density. Mov Disord 2003, 18:217-218.
47. Kim Y., Kim J.M., Kim J.W., Yoo C.I., Lee C.R., Lee J.H., et al. Dopamine transporter density is decreased in parkinsonian patients with a history of manganese exposure: what does it mean?. Mov Disord 2002, 17:568-575.
48. Kobayashi E., Suwazono Y., Uetani M., Inaba T., Oishi M., Kido T., et al. Estimation of benchmark dose for renal dysfunction in a cadmium non-polluted area in Japan. J Appl Toxicol 2006, 26:351-355.
49. Kusnoor S.V., Parris J., Muly E.C., Morgan J.I., Deutch A.Y. Extracerebellar role for Cerebellin1: modulation of dendritic spine density and synapses in striatal medium spiny neurons. J Comp Neurol 2010, 518:2525-2537.
50. Lee E.S., Sidoryk M., Jiang H., Yin Z., Aschner M. Estrogen and tamoxifen reverse manganese-induced glutamate transporter impairment in astrocytes. J Neurochem 2009, 110:530-544.
51. Lee E.S., Yin Z., Milatovic D., Jiang H., Aschner M. Estrogen and tamoxifen protect against Mn-induced toxicity in rat cortical primary cultures of neurons and astrocytes. Toxicol Sci 2009, 110:156-167.
52. Leranth C., Roth R.H., Elsworth J.D., Naftolin F., Horvath T.L., Redmond D.E. Estrogen is essential for maintaining nigrostriatal dopamine neurons in primates: implications for Parkinson's disease and memory. J Neurosci 2000, 20:8604-8609.
53. Lucchini R.G., Martin C.J., Doney B.C. From manganism to manganese-induced parkinsonism: a conceptual model based on the evolution of exposure. Neuromolecular Med 2009, 11:311-321.
54. Magos L., Peristianis G.C., Clarkson T.W., Brown A., Preston S., Snowden R.T. Comparative study of the sensitivity of male and female rats to methylmercury. Arch Toxicol 1981, 48:11-20.
55. Manton W.I., Angle C.R., Stanek K.L., Kuntzelman D., Reese Y.R., Kuehnemann T.J. Release of lead from bone in pregnancy and lactation. Environ Res 2003, 92:139-151.
56. McKeown-Eyssen G.E., Ruedy J., Neims A. Methyl mercury exposure in northern Quebec II. Neurologic findings in children. Am J Epidemiol 1983, 118:470-479.
57. Meding B., Liden C., Berglind N. Self-diagnosed dermatitis in adults, results from a population survey in Stockholm. Contact Dermatitis 2001, 45:341-345.
58. Milatovic D., Zaja-Milatovic S., Gupta R.C., Yu Y., Aschner M. Oxidative damage and neurodegeneration in manganese-induced neurotoxicity. Toxicol Appl Pharmacol 2009, 240:219-225.
59. Miller D.B., Ali S.F., O'Callaghan J.P., Laws S.C. The impact of gender and estrogen on striatal dopaminergic neurotoxicity. Ann N Y Acad Sci 1998, 844:153-165.
60. Miller I.N., Cronin-Golomb A. Gender differences in Parkinson's disease: clinical characteristics and cognition. Mov Disord 2010, 25:2695-2703.
61. Morale M.C., L'Episcopo F., Tirolo C., Giaquinta G., Caniglia S., Testa N., et al. Loss of aromatase cytochrome P450 function as a risk factor for Parkinson's disease?. Brain Res Rev 2008, 57:431-443.
62. Moreno J.A., Streifel K.M., Sullivan K.A., Hanneman W.H., Tjalkens R.B. Manganese-induced NF-{kappa}B activation and nitrosative stress is decreased by estrogen in juvenile mice. Toxicol Sci 2011.
63. Moreno J.A., Yeomans E.C., Streifel K.M., Brattin B.L., Taylor R.J., Tjalkens R.B. Age-dependent susceptibility to manganese-induced neurological dysfunction. Toxicol Sci 2009, 112:394-404.
64. Nicolson T.J., Mellor H.R., Roberts R.R. Gender differences in drug toxicity. Trends Pharmacol Sci 2010, 31:108-114.
65. Nielsen N.H., Linneberg A., Menne T., Madsen F., Frolund L., Dirksen A., et al. Incidence of allergic contact sensitization in Danish adults between 1990 and 1998; the Copenhagen Allergy Study, Denmark. Br J Dermatol 2002, 147:487-492.
66. Olanow C.W. Manganese-induced Parkinsonism and Parkinson's disease. Ann N Y Acad Sci 2004, 1012:209-223.
67. Olanow C.W., Good P.F., Shinotoh H., Hewitt K.A., Vingerhoets F., Snow B.J., et al. Manganese intoxication in the rhesus monkey: a clinical, imaging, pathologic, and biochemical study. Neurology 1996, 46:492-498.
68. Ono K., Komai K., Yamada M. Myoclonic involuntary movement associated with chronic manganese poisoning. J Neurol Sci 2002, 199:93-96.
69. Ookubo M., Yokoyama H., Takagi S., Kato H., Araki T. Effects of estrogens on striatal damage after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) neurotoxicity in male and female mice. Mol Cell Endocrinol 2008, 296:87-93.
70. Perl D.P., Olanow C.W. The neuropathology of manganese-induced Parkinsonism. J Neuropathol Exp Neurol 2007, 66:675-682.
71. Pounds J.G., Long G.J., Rosen J.F. Cellular and molecular toxicity of lead in bone. Environ Health Perspect 1991, 91:17-32.
72. Richardson J.R., Caudle W.M., Wang M.Z., Dean E.D., Pennell K.D., Miller G.W. Developmental heptachlor exposure increases susceptibility of dopamine neurons to N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in a gender-specific manner. Neurotoxicology 2008, 29:855-863.
73. Riojas-Rodriguez H., Solis-Vivanco R., Schilmann A., Montes S., Rodriguez S., Rios C., et al. Intellectual function in Mexican children living in a mining area and environmentally exposed to manganese. Environ Health Perspect 2010, 118:1465-1470.
74. Rukgauer M., Klein J., Kruse-Jarres J.D. Reference values for the trace elements copper, manganese, selenium, and zinc in the serum/plasma of children, adolescents, and adults. J Trace Elem Med Biol 1997, 11:92-98.
75. Sager P.R., Aschner M., Rodier P.M. Persistent, differential alterations in developing cerebellar cortex of male and female mice after methylmercury exposure. Brain Res 1984, 314:1-11.
76. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 1953, 87:387-406.
77. Shulman L.M. Gender differences in Parkinson's disease. Gend Med 2007, 4:8-18.
78. Simon P., Dupuis R., Costentin J. Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res 1994, 61:59-64.
79. Smith C.P., Oh J.D., Bibbiani F., Collins M.A., Avila I., Chase T.N. Tamoxifen effect on l-DOPA induced response complications in parkinsonian rats and primates. Neuropharmacology 2007, 52:515-526.
80. Stanwood G.D., Leitch D.B., Savchenko V., Wu J., Fitsanakis V.A., Anderson D.J., et al. Manganese exposure is cytotoxic and alters dopaminergic and GABAergic neurons within the basal ganglia. J Neurochem 2009, 110:378-389.
81. Stroppolo A., Tian C., Guinea B., Olm V., Sheffield R., Sommer J., et al. 17beta-Estradiol promotes striatal medium size spiny neuronal maturation in vitro. Neuroendocrinology 2004, 79:259-267.
82. Tamas A., Lubics A., Szalontay L., Lengvari I., Reglodi D. Age and gender differences in behavioral and morphological outcome after 6-hydroxydopamine-induced lesion of the substantia nigra in rats. Behav Brain Res 2005, 158:221-229.
83. Uno T., Kobayashi E., Suwazono Y., Okubo Y., Miura K., Sakata K., et al. Health effects of cadmium exposure in the general environment in Japan with special reference to the lower limit of the benchmark dose as the threshold level of urinary cadmium. Scand J Work Environ Health 2005, 31:307-315.
84. Vahter M., Akesson A., Liden C., Ceccatelli S., Berglund M. Gender differences in the disposition and toxicity of metals. Environ Res 2007, 104:85-95.
85. Vahter M., Berglund M., Akesson A., Liden C. Metals and women's health. Environ Res 2002, 88:145-155.
86. Wang J.D., Huang C.C., Hwang Y.H., Chiang J.R., Lin J.M., Chen J.S. Manganese induced parkinsonism: an outbreak due to an unrepaired ventilation control system in a ferromanganese smelter. Br J Ind Med 1989, 46:856-859.
87. Williams B.B., Li D., Wegrzynowicz M., Vadodaria B.K., Anderson J.G., Kwakye G.F., et al. Disease-toxicant screen reveals a neuroprotective interaction between Huntington's disease and manganese exposure. J Neurochem 2010, 112:227-237.
88. Wright A.K., Garcia-Munoz M., Arbuthnott G.W. Slowly progressive dopamine cell loss-a model on which to test neuroprotective strategies for Parkinson's disease?. Rev Neurosci 2009, 20:85-94.
89. Zaja-Milatovic S., Milatovic D., Schantz A.M., Zhang J., Montine K.S., Samii A., et al. Dendritic degeneration in neostriatal medium spiny neurons in Parkinson disease. Neurology 2005, 64:545-547.
90. Zayed J., Guessous A., Lambert J., Carrier G., Philippe S. Estimation of annual Mn emissions from MMT source in the Canadian environment and the Mn pollution index in each province. Sci Total Environ 2003, 312:147-154.
91. Zheng W., Kim H., Zhao Q. Comparative toxicokinetics of manganese chloride and methylcyclopentadienyl manganese tricarbonyl (MMT) in Sprague-Dawley rats. Toxicol Sci 2000, 54:295-301.