Developmental exposure to manganese increases adult susceptibility to inflammatory activation of glia and neuronal protein nitration

Toxicological Sciences

Volumn 112, Issue 2, 2009, Pages 405-415

  Moreno, Julie A ^a   Streifel, Karin M ^a   Sullivan, Kelly A ^a   Legare, Marie E ^a   Tjalkens, Ronald B ^a  

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

Author keywords

Astrocyte; Development; Manganese; Microglia; Neurotoxicity; Nitric oxide

Indexed keywords

3 NITROTYROSINE; CYCLIC AMP; DOPAMINE; MANGANESE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHOSPHOPROTEIN; PHOSPHOPROTEIN 32; UNCLASSIFIED DRUG; NERVE PROTEIN; NITRATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; C57BL 6 MOUSE; CELL ACTIVATION; CELL STRESS; CHEMICAL ANALYSIS; CONTROLLED STUDY; CORPUS STRIATUM; GLIA CELL; GLIOSIS; GLOBUS PALLIDUS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; JUVENILE ANIMAL; MICROGLIA; MOUSE; NEUROPATHOLOGY; NONHUMAN; PROTEIN EXPRESSION; SUBSTANTIA NIGRA; AGING; ANIMAL; C57BL MOUSE; FEMALE; GLIA; METABOLISM; NERVE CELL; PATHOLOGY; PREGNANCY;

MUS; PARKINSONIA;

AGING; ANIMALS; FEMALE; IMMUNOHISTOCHEMISTRY; MANGANESE; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; NITRATES; PREGNANCY;

EID: 74949127037     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp221     Document Type: Article

References (57)

1. Albin, R. L. (2000). Basal ganglia neurotoxins. Neurol. Clin. 18, 665-680.
2. Aschner, M. (1998). Astrocytic functions and physiological reactions to injury: The potential to induce and/or exacerbate neuronal dysfunction-A forum position paper. Neurotoxicology 19, 7-17; discussion 37-18
3. Aschner, M., Mullaney, K. J., Wagoner, D., Lash, L. H., and Kimelberg, H. K. (1994). Intracellular glutathione (GSH) levels modulate mercuric chloride (MC)-and methylmercuric chloride (MeHgCl)-induced amino acid release from neonatal rat primary astrocytes cultures. Brain Res. 664, 133-140.
4. Bae, J. H., Jang, B. C., Suh, S. I., Ha, E., Baik, H. H., Kim, S. S., Lee, M. Y., and Shin, D. H. (2006). Manganese induces inducible nitric oxide synthase (iNOS) expression via activation of both MAP kinase and PI3K/Akt pathways in BV2 microglial cells. Neurosci. Lett. 398, 151-154.
5. Bouchard, M., Laforest, F., Vandelac, L., Bellinger, D., and Mergler, D. (2007). Hair manganese and hyperactive behaviors: Pilot study of school-age children exposed through tap water. Environ. Health Perspect. 115, 122-127.
6. 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.
7. 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.
8. Carbone, D. L., Moreno, J. A., and Tjalkens, R. B. (2008). Nuclear factor kappa-B mediates selective induction of neuronal nitric oxide synthase in astrocytes during low-level inflammatory stimulation with MPTP. Brain Res. 1217, 1-9.
9. 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.
10. Chang, J. Y., and Liu, L. Z. (1999). Manganese potentiates nitric oxide production by microglia. Brain Res. Mol. Brain Res. 68, 22-28.
11. Cowan, D. M., Fan, Q., Zou, Y., Shi, X., Chen, J., Aschner, M., Rosenthal, F. S., and Zheng, W. (2009). Manganese exposure among smelting workers: blood manganese-iron ratio as a novel tool for manganese exposure assessment. Biomarkers 14, 3-16.
12. Dobbing, J., and Sands, J. (1979). Comparative aspects of the brain growth spurt. Early Hum. Dev. 3, 79-83.
13. Dorman, D. C., Struve, M. F., Marshall, M. W., Parkinson, C. U., James, R. A., and Wong, B. A. (2006). Tissue manganese concentrations in young male rhesus monkeys following subchronic manganese sulfate inhalation. Toxicol. Sci. 92, 201-210.
14. Filipov, N. M., Seegal, R. F., and Lawrence, D. A. (2005). Manganese potentiates in vitro production of proinflammatory cytokines and nitric oxide by microglia through a nuclear factor kappa B-dependent mechanism. Toxicol. Sci. 84, 139-148.
15. Flurkey, K., Currer, J. M., and Harrison, D. E. (2007). The mouse in aging research. In In the Mouse in Biomedical Research (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.
16. Garcia, S. J., Gellein, K., Syversen, T., and Aschner, M. (2007). Iron deficient and manganese supplemented diets alter metals and transporters in the developing rat brain. Toxicol. Sci. 95, 205-214.
17. Giovannini, M. G., Scali, C., Prosperi, C., Bellucci, A., Vannucchi, M. G., Rosi, S., Pepeu, G., and Casamenti, F. (2002). Beta-amyloid-induced inflammation and cholinergic hypofunction in the rat brain in vivo: Involvement of the p38MAPK pathway. Neurobiol. Dis. 11, 257-274.
18. Gonzalez-Scarano, F., and Baltuch, G. (1999). Microglia as mediators of inflammatory and degenerative diseases. Annu. Rev. Neurosci. 22, 219-240.
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. Henriksson, J., and Tjalve, H. (2000). Manganese taken up into the CNS via the olfactory pathway in rats affects astrocytes. Toxicol. Sci. 55, 392-398.
21. Hensley, K., Maidt, M. L., Yu, Z., Sang, H., Markesbery, W. R., and Floyd, R. A. (1998). Electrochemical analysis of protein nitrotyrosine and dityrosine in the Alzheimer brain indicates region-specific accumulation. J. Neurosci. 18, 8126-8132.
22. Hirsch, E. C., Hunot, S., Damier, P., and Faucheux, B. (1998). Glial cells and inflammation in Parkinson's disease: A role in neurodegeneration? Ann. Neurol. 44, S115-S120.
23. Huie, R. E., and Padmaja, S. (1993). The reaction of no with superoxide. Free Radic. Res. Commun. 18, 195-199.
24. Ischiropoulos, H. (2003). Biological selectivity and functional aspects of protein tyrosine nitration. Biochem. Biophys. Res. Commun. 305, 776-783.
25. 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.
26. Kim, W. G., Mohney, R. P., Wilson, B., Jeohn, G. H., Liu, B., and Hong, J. S. (2000). Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: Role of microglia. J. Neurosci. 20, 6309-6316.
27. 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.
28. Koppenol, W. H., Moreno, J. J., Pryor, W. A., Ischiropoulos, H., and Beckman, J. S. (1992). Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem. Res. Toxicol. 5, 834-842.
29. Krachler, M., Domej, W., and Irgolic, K. J. (2000). Concentrations of trace elements in osteoarthritic knee-joint effusions. Biol. Trace Elem. Res. 75, 253-263.
30. Kuhn, D. M., Sakowski, S. A., Sadidi, M., and Geddes, T. J. (2004). Nitrotyrosine as a marker for peroxynitrite-induced neurotoxicity: The beginning or the end of the end of dopamine neurons? J. Neurochem. 89, 529-536.
31. Lawson, L. J., Perry, V. H., Dri, P., and Gordon, S. (1990). Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39, 151-170.
32. 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.
33. 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.
34. Liu, X., Buffington, J. A., and Tjalkens, R. B. (2005). NF-kappaB-dependent production of nitric oxide by astrocytes mediates apoptosis in differentiated PC12 neurons following exposure to manganese and cytokines. Brain Res. Mol. Brain Res. 141, 39-47.
35. 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.
36. Ma, T. C., Mihm, M. J., Bauer, J. A., and Hoyt, K. R. (2007). Bioenergetic and oxidative effects of free 3-nitrotyrosine in culture: Selective vulnerability of dopaminergic neurons and increased sensitivity of non-dopaminergic neurons to dopamine oxidation. J. Neurochem. 103, 131-144.
37. Martinez-Hernandez, A., Bell, K. P., and Norenberg, M. D. (1977). Glutamine synthetase: Glial localization in brain. Science 195, 1356-1358.
38. Moreno, J. A., Sullivan, K. A., Carbone, D. L., Hanneman, W. H., and Tjalkens, R. B. (2008). Manganese potentiates nuclear factor-kappaB-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.
39. Moreno, J. A., Yeomans, E. C., Streifel, K. M., Sullivan, K. A., Brattin, B., Taylor, R., and Tjalkens, R. B. (2009). Age-dependent susceptibility to manganese-induced neurological dysfunction. Toxicol. Sci. Advance Access published on October 7, 2009; doi:10.1093/toxsci/kfp220.
40. Norton, W. T. (1999). Cell reactions following acute brain injury: A review. Neurochem. Res. 24, 213-218.
41. Olanow, C. W. (2004). Manganese-induced parkinsonism and Parkinson's disease. Ann. N.Y. Acad. Sci. 1012, 209-223.
42. Pal, P. K., Samii, A., and Calne, D. B. (1999). Manganese neurotoxicity: A review of clinical features, imaging and pathology. Neurotoxicology 20, 227-238.
43. Pekny, M., and Nilsson, M. (2005). Astrocyte activation and reactive gliosis. Glia 50, 427-434.
44. Reiner, A., Perera, M., Paullus, R., and Medina, L. (1998). Immunohistochemical localization of DARPP32 in striatal projection neurons and striatal interneurons in pigeons. J. Chem. Neuroanat. 16, 17-33.
45. Rice, D., and Barone, S., Jr. (2000). Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environ. Health Perspect 108(Suppl. 3), 511-533.
46. Rodier, J. (1955). Manganese poisoning in Moroccan miners. Br. J. Ind. Med. 12, 21-35.
47. Saka, E., Iadarola, M., Fitzgerald, D. J., and Graybiel, A. M. (2002). Local circuit neurons in the striatum regulate neural and behavioral responses to dopaminergic stimulation. Proc. Natl. Acad. Sci. U.S.A. 99, 9004-9009.
48. Soiza-Reilly, M., and Azcurra, J. M. (2009). Developmental striatal critical period of activity-dependent plasticity is also a window of susceptibility for haloperidol induced adult motor alterations. Neurotoxicol. Teratol. 31, 191-197.
49. 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.
50. Stuehr, D. J., and Griffith, O. W. (1992). Mammalian nitric oxide synthases. Adv. Enzymol. Relat. Areas Mol. Biol. 65, 287-346.
51. Takeda, A. (2003). Manganese action in brain function. Brain Res. Brain Res. Rev. 41, 79-87.
52. Tran, T. T., Chowanadisai, W., Crinella, F. M., Chicz-DeMet, A., and Lonnerdal, B. (2002). Effect of high dietary manganese intake of neonatal rats on tissue mineral accumulation, striatal dopamine levels, and neurodevelopmental status. Neurotoxicology 23, 635-643.
53. Verity, M. A. (1999). Manganese neurotoxicity: A mechanistic hypothesis. Neurotoxicology 20, 489-497.
54. 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.
55. 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.
56. 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.
57. 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. 70, 273-278.