Manganese-induced NF-κB activation and nitrosative stress is decreased by estrogen in juvenile mice

Toxicological Sciences

Volumn 122, Issue 1, 2011, Pages 121-133

  Moreno, Julie A ^a   Streifel, Karin M ^a   Sullivan, Kelly A ^a   Hanneman, William H ^a   Tjalkens, Ronald B ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

Author keywords

17 estradiol; Astrocyte; Manganese; Microglia; Neuroinflammation; Neuroprotection; Nitric oxide

Indexed keywords

DOPAMINE; ENHANCED GREEN FLUORESCENT PROTEIN; ESTRADIOL BENZOATE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MANGANESE; SILASTIC; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BASAL GANGLION; CONTROLLED STUDY; CORPUS STRIATUM; DEGENERATIVE DISEASE; DEVELOPMENTAL STAGE; FEMALE; GENE EXPRESSION; INFLAMMATION; JUVENILE ANIMAL; MALE; MICROGLIA; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NITRATION; NITROSATIVE STRESS; NONHUMAN; PARKINSON DISEASE; PROTEIN EXPRESSION; SEX DIFFERENCE; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

EID: 79960993418     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr091     Document Type: Article

References (54)

1. Aschner, M., Erikson, K. M., and Dorman, D. C. (2005). Manganese dosimetry: species differences and implications for neurotoxicity. Crit. Rev. Toxicol. 35, 1-32.
2. Aschner, M., Erikson, K. M., Hernandez, E. H., and Tjalkens, R. (2009). Manganese and its role in Parkinson's disease: from transport to neuropathology. Neuromolecular Med 11, 252-266.
3. Aschner, M., Gannon, M., and Kimelberg, H. K. (1992). Manganese uptake and efflux in cultured rat astrocytes. J. Neurochem. 58, 730-735.
4. Bouchard, M., Mergler, D., Baldwin, M., Panisset, M., and Roels, H. A. (2007). Neuropsychiatric symptoms and past manganese exposure in a ferroalloy plant. Neurotoxicology. 28, 290-297.
5. Bouchard, M. F., Sauve, S., Barbeau, B., Legrand, M., Brodeur, M. E., Bouffard, T., Limoges, E., Bellinger, D. C., and Mergler, D. (2011). Intellectual impairment in school-age children exposed to manganese from drinking water. Environ. Health Perspect. 119, 138-143.
6. Callier, S., Morissette, M., Grandbois, M., Pelaprat, D., and Di Paolo, T. (2001). Neuroprotective properties of 17beta-estradiol, progesterone, and raloxifene in MPTP C57Bl/6 mice. Synapse. 41, 131-138.
7. Carbone, D. L., Popichak, K. A., Moreno, J. A., Safe, S., and Tjalkens, R. B. (2009). Suppression of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridineinduced nitric-oxide synthase 2 expression in astrocytes by a novel diindolylmethane analog protects striatal neurons against apoptosis. Mol. Pharmacol. 75, 35-43.
8. Carreno-Muller, E., Herrera, A. J., de Pablos, R. M., Tomas-Camardiel, M., Venero, J. L., Cano, J., and Machado, A. (2003). Thrombin induces in vivo degeneration of nigral dopaminergic neurones along with the activation of microglia. J. Neurochem. 84, 1201-1214.
9. Chua, A. C., and Morgan, E. H. (1996). Effects of iron deficiency and iron overload on manganese uptake and deposition in the brain and other organs of the rat. Biol. Trace Elem. Res. 55, 39-54.
10. Cockell, K. A., Bonacci, G., and Belonje, B. (2004). Manganese content of soy or rice beverages is high in comparison to infant formulas. J. Am. Coll. Nutr. 23, 124-130.
11. Collipp, P. J., Chen, S. Y., and Maitinsky, S. (1983). Manganese in infant formulas and learning disability. Ann. Nutr. Metab. 27, 488-494.
12. D'Astous, M., Morissette, M., Tanguay, B., Callier, S., and Di Paolo, T. (2003). Dehydroepiandrosterone (DHEA) such as 17beta-estradiol prevents MPTP-induced dopamine depletion in mice. Synapse. 47, 10-14.
13. Dluzen, D. E., McDermott, J. L., and Liu, B. (1996). Estrogen alters MPTPinduced neurotoxicity in female mice: effects on striatal dopamine concentrations and release. J. Neurochem. 66, 658-666.
14. Dobbing, J., and Sands, J. (1979). Comparative aspects of the brain growth spurt. Early Hum. Dev. 3, 79-83.
15. Flurkey, K. C. J., and Harrison, D. E. (2007). The mouse in aging research. In The Mouse in Biomedical Research (J. G. Fox, et al.), pp. 637-672. American College Laboratory Animal Medicine, Burlington, MA.
16. Ghisletti, S., Huang,W., Jepsen, K., Benner, C., Hardiman, G., Rosenfeld, M. G., and Glass, C. K. (2009). Cooperative NCoR/SMRT interactions establish a corepressor-based strategy for integration of inflammatory and antiinflammatory signaling pathways. Genes Dev. 23, 681-693.
17. Greger, J. L. (1998). Dietary standards for manganese: overlap between nutritional and toxicological studies. J. Nutr. 128, 368S-371S.
18. 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.
19. Hafeman, D., Factor-Litvak, P., Cheng, Z., van Geen, A., and Ahsan, H. (2007). Association between manganese exposure through drinking water and infant mortality in Bangladesh. Environ. Health Perspect. 115, 1107-1112.
20. He, P., Liu, D. H., and Zhang, G. Q. (1994). [Effects of high-level-manganese sewage irrigation on children's neurobehavior]. Zhonghua Yu Fang Yi Xue Za Zhi. 28, 216-218.
21. Hirsch, E. C., and Hunot, S. (2000). Nitric oxide, glial cells and neuronal degeneration in parkinsonism. Trends Pharmacol. Sci. 21, 163-165.
22. Kern, C. H., Stanwood, G. D., and Smith, D. R. (2010). Preweaning manganese exposure causes hyperactivity, disinhibition, and spatial learning and memory deficits associated with altered dopamine receptor and transporter levels. Synapse. 64, 363-378.
23. Koop, M., Rilling, G., Herrmann, A., and Kretschmann, H. J. (1986). Volumetric development of the fetal telencephalon, cerebral cortex, diencephalon, and rhombencephalon including the cerebellum in man. Bibl. Anat. 28, 53-78.
24. Krachler, M., Prohaska, T., Koellensperger, G., Rossipal, E., and Stingeder, G. (2000). Concentrations of selected trace elements in human milk and in infant formulas determined by magnetic sector field inductively coupled plasma-mass spectrometry. Biol. Trace Elem. Res. 76, 97-112.
25. Kudwa, A. E., Harada, N., Honda, S. I., and Rissman, E. F. (2007). Effects of organisational oestradiol on adult immunoreactive oestrogen receptors (alpha and beta) in the male mouse brain. J. Neuroendocrinol. 19, 767-772.
26. Lee, B., Hiney, J. K., Pine, M. D., Srivastava, V. K., and Dees, W. L. (2007). Manganese stimulates luteinizing hormone releasing hormone secretion in prepubertal female rats: hypothalamic site and mechanism of action. J. Physiol. 578, 765-772.
27. Lee, E. S., Sidoryk, M., Jiang, H., Yin, Z., and Aschner, M. (2009a). Estrogen and tamoxifen reverse manganese-induced glutamate transporter impairment in astrocytes. J. Neurochem. 110, 530-544.
28. Lee, E. S., Yin, Z., Milatovic, D., Jiang, H., and Aschner, M. (2009b). Estrogen and tamoxifen protect against Mn-induced toxicity in rat cortical primary cultures of neurons and astrocytes. Toxicol. Sci. 110, 156-167.
29. Liberatore, G. T., Jackson-Lewis, V., Vukosavic, S., Mandir, A. S., Vila, M., McAuliffe, W. G., Dawson, V. L., Dawson, T. M., and Przedborski, S. (1999). Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat. Med. 5, 1403-1409.
30. Liu, M., Cai, T., Zhao, F., Zheng, G., Wang, Q., Chen, Y., Huang, C., Luo, W., and Chen, J. (2009). Effect of microglia activation on dopaminergic neuronal injury induced by manganese, and its possible mechanism. Neurotox. Res. 16, 42-49.
31. 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.
32. Magness, S. T., Jijon, H., Van Houten Fisher, N., Sharpless, N. E., Brenner, D. A., and Jobin, C. (2004). In vivo pattern of lipopolysaccharide and anti-CD3-induced NF-kappa B activation using a novel gene-targeted enhanced GFP reporter gene mouse. J. Immunol. 173, 1561-1570.
33. Miller, D. B., Ali, S. F., O'Callaghan, J. P., and Laws, S. C. (1998). The impact of gender and estrogen on striatal dopaminergic neurotoxicity. Ann. N Y Acad. Sci. 844, 153-165.
34. Morale, M. C., Serra, P. A., L'Episcopo, F., Tirolo, C., Caniglia, S., Testa, N., Gennuso, F., Giaquinta, G., Rocchitta, G., Desole, M. S., et al. (2006). Estrogen, neuroinflammation and neuroprotection in Parkinson's disease: glia dictates resistance versus vulnerability to neurodegeneration. Neuroscience. 138, 869-878.
35. Moreno, J. A., Streifel, K. M., Sullivan, K. A., Legare, M. E., and Tjalkens, R. B. (2009a). Developmental exposure to manganese increases adult susceptibility to inflammatory activation of glia and neuronal protein nitration. Toxicol. Sci. 112, 405-415.
36. Moreno, J. A., Sullivan, K. A., Carbone, D. L., Hanneman, W. H., and Tjalkens, R. B. (2008). Manganese potentiates nuclear factor-kappa B-dependent expression of nitric oxide synthase 2 in astrocytes by activating soluble guanylate cyclase and extracellular responsive kinase signaling pathways. J. Neurosci. Res. 86, 2028-2038.
37. Moreno, J. A., Yeomans, E. C., Streifel, K. M., Brattin, B. L., Taylor, R. J., and Tjalkens, R. B. (2009b). Age-dependent susceptibility to manganese-induced neurological dysfunction. Toxicol. Sci. 112, 394-404.
38. Murray, H. E., Pillai, A. V., McArthur, S. R., Razvi, N., Datla, K. P., Dexter, D. T., and Gillies, G. E. (2003). Dose- and sex-dependent effects of the neurotoxin 6-hydroxydopamine on the nigrostriatal dopaminergic pathway of adult rats: differential actions of estrogen in males and females. Neuroscience. 116, 213-222.
39. Olanow, C. W. (2004). Manganese-induced parkinsonism and Parkinson's disease. Ann. N Y Acad. Sci. 1012, 209-223.
40. Pihl, R. O., and Parkes, M. (1977). Hair element content in learning disabled children. Science. 198, 204-206.
41. Ramirez, A. D., Liu, X., and Menniti, F. S. (2003). Repeated estradiol treatment prevents MPTP-induced dopamine depletion in male mice. Neuroendocrinology. 77, 223-231.
42. Rapoport, J. L., and Gogtay, N. (2008). Brain neuroplasticity in healthy, hyperactive and psychotic children: insights from neuroimaging. Neuropsychopharmacology. 33, 181-197.
43. Riojas-Rodriguez, H., Solis-Vivanco, R., Schilmann, A., Montes, S., Rodriguez, S., Rios, C., and Rodriguez-Agudelo, Y. (2010). Intellectual function in Mexican children living in a mining area and environmentally exposed to manganese. Environ. Health Perspect. 118, 1465-1470.
44. Spranger, M., Schwab, S., Desiderato, S., Bonmann, E., Krieger, D., and Fandrey, J. (1998). Manganese augments nitric oxide synthesis in murine astrocytes: a new pathogenetic mechanism in manganism? Exp. Neurol. 149, 277-283.
45. 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.
46. Tripanichkul, W., Sripanichkulchai, K., and Finkelstein, D. I. (2006). Estrogen down-regulates glial activation in male mice following 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine intoxication. Brain Res 1084, 28-37.
47. Tsujimoto, S. (2008). The prefrontal cortex: functional neural development during early childhood. Neuroscientist. 14, 345-358.
48. 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.
49. 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.
50. Wu, D. C., Jackson-Lewis, V., Vila, M., Tieu, K., Teismann, P., Vadseth, C., Choi, D. K., Ischiropoulos, H., and Przedborski, S. (2002). Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 22, 1763-1771.
51. Xie, Q. W., Kashiwabara, Y., and Nathan, C. (1994). Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269, 4705-4708.
52. Xie, Q. W., Whisnant, R., and Nathan, C. (1993). Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J. Exp. Med. 177, 1779-1784.
53. 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.
54. Zhang, D., Kanthasamy, A., and Anantharam, V. (2011). Effects of manganese on tyrosine hydroxylase (TH) activity and TH-phosphorylation in a dopaminergic neural cell line. Toxicol. Appl. Pharmacol. Advance Access published on February 15, 2011; doi:10.1016/j.taap.2010.03.023.