Manganese inhibits the ability of astrocytes to promote neuronal differentiation

Toxicology and Applied Pharmacology

Volumn 240, Issue 2, 2009, Pages 226-235

  Giordano, Gennaro ^a   Pizzurro, Daniella ^a   VanDeMark, Kathryn ^a   Guizzetti, Marina ^a   Costa, Lucio G ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF PARMA MEDICAL SCHOOL   (Italy)

Author keywords

Manganese; Neurotoxicity

Indexed keywords

2,3 DIMETHOXY 1,4 NAPHTHOQUINONE; FIBRONECTIN; GLUTATHIONE; HYDROGEN PEROXIDE; MANGANESE; MELATONIN; N TERT BUTYL ALPHA PHENYLNITRONE;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL INTERACTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; FETUS; GENE EXPRESSION; HIPPOCAMPUS; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT;

ANIMALS; ANTIOXIDANTS; ASTROCYTES; AXONS; CELL COMMUNICATION; CELLS, CULTURED; CEREBRAL CORTEX; CHLORIDES; COCULTURE TECHNIQUES; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBRONECTINS; GLUTATHIONE; HIPPOCAMPUS; MANGANESE COMPOUNDS; NEURITES; NEUROGENESIS; NEURONS; OXIDANTS; OXIDATIVE STRESS; RATS; RNA, MESSENGER;

RATTUS;

EID: 70349263353     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2009.06.004     Document Type: Article

References (71)

1. In: Aschner M., and Costa L.G. (Eds). The Role of Glia in Neurotoxicity (2004), CRC Press, Boca Raton 456
2. Aschner M., Gannon M., and Kimelberg H.K. Manganese uptake and efflux in cultured rat astrocytes. J. Neurochem. 68 (1992) 730-735
3. Aschner M., Vrana K.E., and Zhang W. Manganese uptake and distribution in the central nervous system (CNS). NeuroToxicology 20 (1999) 173-180
4. Aschner M., Guilarte T.R., Schneider J.S., and Zheng W. Manganese: recent advances in understanding its transport and neurotoxicity. Toxicol. Appl. Pharmacol. 221 (2007) 131-147
5. Asher R.A., Morgenstern D.A., Fidler P.S., Adcock K.H., Oohira A., Braistead J.E., Levine J.M., Margolis R.U., Rogers J.H., and Fawcett J.W. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J. Neurosci. 20 (2000) 2427-2438
6. ATSDR (Agency for Toxic Substances and Disease Registry). Toxicological Profile for Manganese (2000)
7. Barbeau A. Manganese and extrapyramidal disorders. NeuroToxicology 5 (1984) 13-36
8. Bondy S.C., and Lee D.K. Oxidative stress induced by glutamate receptor agonists. Brain Res. 610 (1993) 229-233
9. Brewer G.J., Torricelli J.R., Evege E.K., and Price P.J. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35 (1993) 567-576
10. Chen C.J., and Liao S.L. Oxidative stress involved in astrocytic alterations induced by manganese. Exp. Neurol. 175 (2002) 216-225
11. Christopherson K.S., Ullian E.M., Stokes C.C., Mullowney C.E., Hell J.W., Agah A., Lawler J., Mosher D.F., Bornstein P., and Barres B.A. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120 (2005) 421-433
12. Das S.K., and Vasudevan D.M. Alcohol-induced oxidative stress. Life Sci. 81 (2007) 177-187
13. Deb S., Zhang J.W., and Gottschall P.E. Beta-amyloid induces the production of active, matrix-degrading proteases in cultured rat astrocytes. Brain Res. 970 (2003) 205-213
14. DiProspero N.A., Meiners S., and Geller H.M. Inflammatory cytokines interact to modulate extracellular matrix and astrocytic support of neurite outgrowth. Exp. Neurol. 148 (1997) 628-639
15. Dotti C.G., Sullivan C.A., and Banker G.A. The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8 (1988) 1454-1468
16. Dunn Keene S., Greco T.M., Parastatidis I., Lee S.H., Hughes E.G., Balice-Gordon R.J., Speicher D.W., and Ischiropoulos H. Mass spectrometric and computational analysis of cytokine-induced alterations in the astrocyte secretome. Proteomics 9 (2009) 768-782
17. Elder A., Gelein R., Silva V., Feikert T., Opanashuk L., Carter J., et al. Translocation of inhaled ultrafine manganese oxide particles to the central nervous system. Environ. Health Perspect. 114 (2006) 1172-1178
18. Erikson K.M., and Aschner M. Manganese causes differential regulation of glutamate transporter (GLAST), taurine transporter, and methallothionein in cultured rat astrocytes. Neurotoxicology 23 (2002) 595-602
19. Erikson K.M., and Aschner M. Manganese neurotoxicity and glutamate-GABA interaction. Neurochem. Int. 43 (2003) 475-480
20. Erikson K.M., Dobson A.W., Dorman D.C., and Aschner M. Manganese exposure and induced oxidative stress in the rat brain. Sci. Total Environ. 334-335 (2004) 409-416
21. Erikson K.M., Thompson K., Aschner J., and Aschner M. Manganese neurotoxicity: a focus on the neonate. Pharmacol. Ther. 113 (2007) 369-377
22. Fitsanakis V.A., Au C., Erikson K.M., and Aschner M. The effects of manganese on glutamate, dopamine and gamma-aminobutyric acid regulation. Neurochem. Int. 48 (2006) 426-433
23. Giordano G., White C.C., McConnachie L.A., Fernandez C., Kavanagh T.J., and Costa L.G. Neurotoxicity of domoic acid in cerebellar granule neurons in a genetic model of glutathione deficiency. Mol. Pharmacol. 70 (2006) 2116-2126
24. Gomes F.C., Spohr T.C., Martinez R., and Moura Nieto V. Cross-talk between neurons and glia: highlights on soluble factors. Braz. J. Med. Res. 34 (2001) 611-620
25. Greger J.L. Nutrition versus toxicology of manganese in humans: evaluation of potential biomarkers. NeuroToxicology 20 (1999) 205-212
26. Gris P., Tighe A., Levin D., Sharma R., and Brown A. Transcriptional regulation of scar gene expression in primary astrocytes. Glia 55 (2007) 1145-1155
27. Guizzetti M., Costa P., Peters J., and Costa L.G. Actylcholine as a mitogen: muscarinic receptor-mediated proliferation of rat astrocytes and human astrocytoma cells. Eur. J. Pharmacol. 197 (1996) 265-273
28. Guizzetti M., Moore N.H., Giordano G., and Costa L.G. . Modulation of neuritogenesis by astrocyte muscarinic receptors. J. Biol. Chem. 283 (2008) 31884-31897
29. Gunter T.E., Gavin C.E., Aschner M., and Gunter K.K. Speciation of manganese in cells and mitochondria: a search for the proximal cause of manganese neurotoxicity. NeuroToxicology 27 (2006) 765-776
30. HaMai D., and Bondy S.C. Oxidative basis of manganese neurotoxicity. Ann. N.Y. Acad. Sci. 1012 (2004) 129-141
31. Haydon P.G. Glia: listening and talking to the synapse. Nat. Rev., Neurosci. 2 (2001) 185-193
32. Hazell A.S. Astrocytes and manganese neurotoxicity. Neurochem. Int. 41 (2002) 271-277
33. Ihnat M.A., Thorpe J.E., Kamat C.D., Szabo C., Gree D.E., Warnke L.A., Lacza Z., Cselenyak A., Ross K., Shakir S., Piconi L., Kaltreider R.C., and Ceriello A. Reactive oxygen species mediate a cellular "memory" of high glucose stress signaling. Diabetologia 50 (2007) 1523-1530
34. IOM (Institute of Medicine). Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium and Zinc (2001), National Academy Press, Washington DC
35. Irigoyen J.P., Munoz-Canoves P., Montero L., Koziczak M., and Nagamine Y. The plasminogen activator system: biology and regulation. Cell. Mol. Life Sci. 56 (1999) 104-132
36. Kimelberg H.K., and Aschner M. Functions of astrocytes. In: Schipper H.M. (Ed). Astrocytes in Brain Aging and Neurodegeneration (1998), Landes Bioscience, Montreal, Canada 15-39
37. Kiryushko D., Berezin V., and Bock E. Regulators of neurite outgrowth: role of cell adhesion molecules. Ann. N.Y. Acad. Sci. 1014 (2004) 140-154
38. Lee H.B., Yu M.R., Song J.S., and Ha H. Reactive oxygen species amplify protein kinase C signaling in high glucose-induced fibronectin expression by human peritoneal mesothelial cells. Kidney Int. 65 (2004) 1170-1179
39. v integrins. Brain Res. 885 (2000) 220-230
40. Levy B.S., and Nassetta W.J. Neurologic effects of manganese in humans: a review. Int. J. Occup. Environ. Health 9 (2003) 153-163
41. Liao S.L., Ou Y.C., Chen S.Y., Chiang A.N., and Chen C.J. Induction of cyclooxygenase-2 expression by manganese in cultured astrocytes. Neurochem. Int. 50 (2007) 905-915
42. Lin W.H., Higgins D., Pacheco M., Aletta J., Perini S., Marcucci K.A., and Roth J.A. Manganese induces spreading and process outgrowth in rat pheochromocytoma (PC12) cells. J. Neurosci. Res. 34 (1993) 546-561
43. Lindsley T.A., Comstock L.L., and Rising L.J. Morphologic and neurotoxic effects of ethanol vary with timing of exposure in vitro. Alcohol 28 (2002) 197-203
44. Liu X., Sullivan K.A., Madl J.E., Legare M., and Tjalkens R.B. Manganese-induced neurotoxicity: the role of astroglial-derived nitric oxide in striatal interneuron degeneration. Toxicol. Sci. 91 (2006) 521-531
45. Ljung K., and Vahter M. Time to re-evaluate the guideline value for manganese in drinking water?. Environ. Health Perspect. 115 (2007) 1533-1538
46. Mahler M., Ben-Ari Y., and Represa A. Differential expression of fibronectin, tenascin-C, and NCAMs in cultured hippocampal astrocytes activated by kainite, bacterial lipopolysaccharide or basic fibroblast growth factor. Brain Res. 775 (1997) 63-73
47. Martinez R., and Gomes F.C. Neuritogenesis induced by thyroid hormone-treated astrocytes is mediated by epidermal growth factor/mitogen-activated protein kinase-phosphatidylinositol 3-kinase pathways and involves modulation of extracellular matrix. J. Biol. Chem. 277 (2002) 49311-49318
48. McMillan D.E. A brief history of the neurobehavioral toxicity of manganese: some unanswered questions. NeuroToxicology 20 (1999) 499-507
49. Milatovic D., Yin Z., Gupta R.C., Sidoryk M., Albrecht J., Aschner J.L., and Aschner M. Manganese induces oxidative impairment in cultured rat astrocytes. Toxicol. Sci. 98 (2007) 198-205
50. Moore N.H., Costa L.G., Shaffer S.A., Goodlett D.R., and Guizzetti M. Shotgun proteomics implicates extracellular matrix proteins and protease systems in neuronal development induced by astrocyte cholinergic stimulation. J. Neurochem. 108 (2009) 891-908
51. Morello M., Canini A., Mattioli P., Sorge R.P., Alimonti A., Bocca B., Forte G., Martorana A., Bernardi G., and Sancesario G. Subcellular localization of manganese in the basal ganglia of normal and manganese-treated rats. An electron spectroscopy imaging and electron energy-loss spectroscopy study. NeuroToxicology 29 (2008) 60-72
52. Moreno J.A., Sullivan K.A., Carbone D.L., Hanneman W.H., and Tjalkens R.B. Manganese potentiates nuclear factor-kB-dependent expression of nitric oxide synthase 2 in astrocytes by activating soluble guanylate cyclase and extracellular responsive kinase signaling pathways. J. Neurosci. Res. 86 (2008) 2028-2038
53. Muller H.W., Junghans U., and Kappler J. Astroglial neurotrophic and neurite-promoting factors. Pharmacol. Ther. 65 (1995) 1-18
54. Muscoli C., Fresta M., Cardile V., Palumbo M., Renis M., Puglisi G., Paolino D., Nistico S., Rotiroti D., and Mollace V. Ethanol-induced injury in rat primary cortical astrocytes involves oxidative stress: effect of idebenone. Neurosci. Lett. 329 (2002) 21-24
55. Obara Y., and Nakahata N. The signaling pathway of neurotrophic factor biosynthesis. Drug News Perspect. 15 (2002) 290-298
56. Perl D.P., and Olanow C.W. The neuropathology of manganese-induced parkinsonism. J. Neuropathol. Exp. Neurol. 66 (2007) 675-682
57. Rama Rao K.V., Reddy P.V.B., Hazell A.S., and Norenberg M.D. Manganese induces cell swelling in cultured astrocytes. NeuroToxicology 28 (2007) 807-812
58. Ren L.Q., Garrett D.K., Syapin M., and Syapin P.J. Differential fibronectin expression in activated C6 glial cells treated with ethanol. Mol. Pharmacol. 58 (2000) 1303-1309
59. Sengupta A., Mense S.M., Lan C., Zhou M., Mauro R.E., Kellerman L., Bentsman G., Volsky D.J., Lois E.D., Graziano J.H., and Zhang L. Gene expression profiling of human primary astrocytes exposed to manganese chloride indicates selective effects on several functions of the cells. NeuroToxicology 28 (2007) 478-489
60. Thibault T.C., Kennedy G., Gareau L., and Zayed J. Preliminary assessment of atmospheric methylcyclopentadienyl manganese tricarbonyl and particulate manganese in selected urban sites. J. Toxicol. Environ. Health 65 (2002) 503-511
61. Tjalkens R.B., Zoran M.J., Mohl B., and Barhoumi R. Manganese suppresses ATP-dependent intercellular calcium waves in astrocyte networks through alteration of mitochondrial and endoplasmic reticulum calcium dynamics. Brain Res. 1113 (2006) 210-219
62. Tom V.J., Doller C.M., Malouf A.T., and Silver J. Astrocyte-associated fibronectin is critical for axonal regeneration in adult white matter. J. Neurosci. 24 (2004) 9282-9290
63. USEPA (US Environmental Protection Agency). Drinking Water Health Advisory for Manganese. Report 822R04003 (2004), US Environmental Protection Agency, Washington DC
64. VanDeMark K.L., Guizzetti M., Giordano G., and Costa L.G. The activation of M1 muscarinic receptor signaling induces neuronal differentiation of pyramidal hippocampal neurons. J. Pharmacol. Exp. Ther. 329 (2009) 532-542
65. Viviani B., Corsini E., Galli C.L., and Marinovich M. Glia increase degeneration of hippocampal neurons through release of tumor necrosis factor-alpha. Toxicol. Appl. Pharmacol. 150 (1998) 271-276
66. Wasserman G.A., Liu X., Parvez F., Ahsan H., Levy D., Factor-Ltvak P., Kline J., van Green A., Slavkovich V., Lolacono N.J., Cheng Z., Zheng Y., and Graziano J.H. Water manganese exposure and children's intellectual function in Araihazar, Bangladesh. Environ. Health Perspect. 114 (2006) 124-129
67. Watts L.T., Rathinam M.L., Schenker S., and Henderson G.I. Astrocytes protect neurons from ethanol-induced oxidative stress and apoptotic death. J. Neurosci. Res. 80 (2005) 655-666
68. WHO (World Health Organization). Guidelines for Drinking Water (2006)
69. Yamada H., Fredette B., Shitara K., Hagihara K., Miura R., Ranscht B., Stallcup W.B., and Yamaguchi Y. The brain chondroitin sulfate proteoglycan brevican associates with astrocytes ensheathing cerebellar glomeruli and inhibits neurite outgrowth from granule neurons. J. Neurosci. 17 (1997) 7784-7795
70. Yeh C.H., Chang C.K., Cheng M.F., Lin H.J., and Cheng J.T. The antioxidative effect of bone morphogenetic protein-7 against high glucose-induced oxidative stress in mesangial cells. Biochem. Biophys. Res. Commun. 382 (2009) 292-297
71. Yin Z., Aschner J.L., dos Santos A.P., and Aschner M. Mitochondrial-dependent manganese neurotoxicity in rat primary astrocyte cultures. Brain Res. 1203 (2008) 1-11