Estrogen and tamoxifen protect against Mn-induced toxicity in rat cortical primary cultures of neurons and astrocytes

Toxicological Sciences

Volumn 110, Issue 1, 2009, Pages 156-167

  Lee, Eun Sook Y ^a   Yin, ZZhaobao ^b   Milatovic, Dejan ^b   Jiang, Haiyan ^b   Aschner, Michael ^b  

^a MEHARRY MEDICAL COLLEGE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

17 estradiol; Kinase (MAPK ERK); Neuroprotection; Oxidative stress; PI3K Akt; Tamoxifen

Indexed keywords

ESTROGEN; MANGANESE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; TAMOXIFEN;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; ASTROCYTE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENVIRONMENTAL EXPOSURE; GENE ACTIVATION; IMMUNOCYTOCHEMISTRY; LONG TERM EXPOSURE; NERVE CELL CULTURE; NEUROPROTECTION; NEUROTOXICITY; NEWBORN; NONHUMAN; OXIDATIVE STRESS; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIOXIDANTS; ASTROCYTES; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; ENZYME ACTIVATION; ESTRADIOL; MANGANESE; MANGANESE POISONING; MITOGEN-ACTIVATED PROTEIN KINASES; NEURONS; NEUROPROTECTIVE AGENTS; ONCOGENE PROTEIN V-AKT; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TAMOXIFEN;

RATTUS;

EID: 67649221617     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp081     Document Type: Article

References (48)

1. 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.
2. Barbeau, A. (1984). Manganese and extrapyramidal disorders (a critical review and tribute to Dr. George C. Cotzias). Neurotoxicology 5 13-35.
3. Barron, A. M., Fuller, S. J., Verdile, G., and Martins, R. N. (2006). Reproductive hormones modulate oxidative stress in Alzheimer's disease. Antioxid. Redox Signal. 8, 2047-2059.
4. Brouillet, E. P., Shinobu, L., McGarvey, U., Hochberg, F., and Beal, M. F. (1993). Manganese injection into the rat striatum produces excitotoxic lesions by impairing energy metabolism. Exp. Neurol. 120, 89-94.
5. Bryant, W., Snowhite, A. E., Rice, L. W., and Shupnik, M. A. (2005). The estrogen receptor (ER) alpha variant Delta5 exhibits dominant positive activity on ER-regulated promoters in endometrial carcinoma cells. Endocrinology 146, 751-759.
6. Chen, C. J., and Liao, S. L. (2002). Oxidative stress involves in astrocytic alterations induced by manganese. Exp. Neurol. 175 216-225.
7. Desagher, S., Glowinski, J., and Premont, J. (1996). Astrocytes protect neurons from hydrogen peroxide toxicity. J. Neurosci. 16, 2553-2562.
8. Desole, M. S., Sciola, L., Delogu, M. R., Sircana, S., Migheli, R., and Miele, E. (1997). Role of oxidative stress in the manganese and 1-methyl-4-(2′- ethylphenyl)-1,2,3,6-tetrahydropyridine-induced apoptosis in PC12 cells. Neurochem. Int. 31, 169-176.
9. Dhandapani, K. M., and Brann, D. W. (2002). Protective effects of estrogen and selective estrogen receptor modulators in the brain. Biol. Reprod. 67, 1379-1385.
10. Dhandapani, K. M., Wade, F. M., Mahesh, V. B., and Brann, D. W. (2005). Astrocyte-derived transforming growth factor-{beta} mediates the neuroprotective effects of 17{beta}-estradiol: Involvement of nonclassical genomic signaling pathways. Endocrinology 146, 2749-2759.
11. Dominguez, R., Liu, R., and Baudry, M. (2007). 17-Beta-estradiol-mediated activation of extracellular-signal regulated kinase, phosphatidylinositol 3-kinase/protein kinase B-Akt and N-methyl-D-aspartate receptor phosphorylation in cortical synaptoneurosomes. J. Neurochem. 101, 232-240.
12. 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.
13. Ebadi, M., Srinivasan, S. K., and Baxi, M. D. (1996). Oxidative stress and antioxidant therapy in Parkinson's disease. Prog. Neurobiol. 48, 1-19.
14. Fu, W., Luo, H., Parthasarathy, S., and Mattson, M. P. (1998). Catecholamines potentiate amyloid beta-peptide neurotoxicity: Involvement of oxidative stress, mitochondrial dysfunction, and perturbed calcium homeostasis. Neurobiol. Dis. 5, 229-243.
15. Gorovits, R., Avidan, N., Avisar, N., Shaked, I., and Vardimon, L. (1997). Glutamine synthetase protects against neuronal degeneration in injured retinal tissue. Proc. Natl. Acad. Sci. U. S. A. 94, 7024-7029.
16. Guilarte, T. R., Burton, N. C., Verina, T., Prabhu, V. V., Becker, K. G., Syversen, T., and Schneider, J. S. (2008). Increased APLP1 expression and neurodegeneration in the frontal cortex of manganese-exposed non-human primates. J. Neurochem. 105, 1948-1959.
17. Guilarte, T. R., and Chen, M. K. (2007). Manganese inhibits NMDA receptor channel function: Implications to psychiatric and cognitive effects. Neurotoxicology 28, 1147-1152.
18. Gunter, K. K., Aschner, M., Miller, L. M., Eliseev, R., Salter, J., Anderson, K., Hammond, S., and Gunter, T. E. (2005). Determining the oxidation states of manganese in PC12 and nerve growth factor-induced PC12 cells. Free Radic. Biol. Med. 39, 164-181.
19. Hazell, A. S. (2002). Astrocytes and manganese neurotoxicity. Neurochem. Int. 41, 271-277.
20. Honda, K., Sawada, H., Kihara, T., Urushitani, M., Nakamizo, T., Akaike, A., and Shimohama, S. (2000). Phosphatidylinositol 3-kinase mediates neuroprotection by estrogen in cultured cortical neurons. J. Neurosci. Res. 60, 321-327.
21. Jover-Mengual, T., Zukin, R. S., and Etgen, A. M. (2007). MAPK signaling is critical to estradiol protection of CA1 neurons in global ischemia. Endocrinology 148, 1131-1143.
22. Kimelberg, H. K. (2005). Astrocytic swelling in cerebral ischemia as a possible cause of injury and target for therapy. Glia 50, 389-397.
23. Kimelberg, H. K., Feustel, P. J., Jin, Y., Paquette, J., Boulos, A., Keller, R. W., Jr., and Tranmer, B. I. (2000). Acute treatment with tamoxifen reduces ischemic damage following middle cerebral artery occlusion. Neuroreport. 11, 2675-2679.
24. Kuroki, Y., Fukushima, K., Kanda, Y., Mizuno, K., and Watanabe, Y. (2001). Neuroprotection by estrogen via extracellular signal-regulated kinase against quinolinic acid-induced cell death in the rat hippocampus. Eur. J. Neurosci. 13, 472-476.
25. Liao, S. L., Ou, Y. C., Chen, S. Y., Chiang, A. N., and Chen, C. J. (2007). Induction of cyclooxygenase-2 expression by manganese in cultured astrocytes. Neurochem. Int. 50, 905-915.
26. Mannella, P., and Brinton, R. D. (2006). Estrogen receptor protein interaction with phosphatidylinositol 3-kinase leads to activation of phosphorylated Akt and extracellular signal-regulated kinase 1/2 in the same population of cortical neurons: A unified mechanism of estrogen action. J. Neurosci. 26, 9439-9447.
27. Milatovic, D., Yin, Z., Gupta, R. C., Sidoryk, M., Albrecht, J., Aschner, J. L., and Aschner, M. (2007). Manganese induces oxidative impairment in cultured rat astrocytes. Toxicol. Sci. 98, 198-205.
28. Moosmann, B., and Behl, C. (1999). The antioxidant neuroprotective effects of estrogens and phenolic compounds are independent from their estrogenic properties. Proc. Natl. Acad. Sci. U. S. A. 96, 8867-8872.
29. Normandin, L., and Hazell, A. S. (2002). Manganese neurotoxicity: An update of pathophysiologic mechanisms. Metab. Brain Dis. 17, 375-387.
30. Numakawa, Y., Matsumoto, T., Yokomaku, D., Taguchi, T., Niki, E., Hatanaka, H., Kunugi, H., and Numakawa, T. (2007). 17Beta-estradiol protects cortical neurons against oxidative stress-induced cell death through reduction in the activity of mitogen-activated protein kinase and in the accumulation of intracellular calcium. Endocrinology 148, 627-637.
31. O'Lone, R., Frith, M. C., Karlsson, E. K., and Hansen, U. (2004). Genomic targets of nuclear estrogen receptors. Mol. Endocrinol. 18, 1859-1875.
32. O'Neill, K., Chen, S., and Brinton, R. D. (2004). Impact of the selective estrogen receptor modulator, raloxifene, on neuronal survival and outgrowth following toxic insults associated with aging and Alzheimer's disease. Exp. Neurol. 185, 63-80.
33. 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.
34. Raz, L., Khan, M. M., Mahesh, V. B., Vadlamudi, R. K., and Brann, D. W. (2008). Rapid estrogen signaling in the brain. Neurosignals 16 140-153.
35. Rice, M. E., and Russo-Menna, I. (1998). Differential compartmentalization of brain ascorbate and glutathione between neurons and glia. Neuroscience 82, 1213-1223.
36. Singer, C. A., Figueroa-Masot, X. A., Batchelor, R. H., and Dorsa, D. M. (1999). The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J. Neurosci. 19, 2455-2463.
37. Singh, M., Setalo, G., Jr., Guan, X., Warren, M., and Toran-Allerand, C. D. (1999). Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: Convergence of estrogen and neurotrophin signaling pathways. J. Neurosci. 19, 1179-1188.
38. Stokes, A. H., Lewis, D. Y., Lash, L. H., Jerome, W. G., III, Grant, K. W., Aschner, M., and Vrana, K. E. (2000). Dopamine toxicity in neuroblastoma cells: Role of glutathione depletion by L-BSO and apoptosis. Brain Res. 858, 1-8.
39. Sun, A. Y., Yang, W. L., and Kim, H. D. (1993). Free radical and lipid peroxidation in manganese-induced neuronal cell injury. Ann. N. Y. Acad. Sci. 679, 358-363.
40. Taylor, M. D., Erikson, K. M., Dobson, A. W., Fitsanakis, V. A., Dorman, D. C., and Aschner, M. (2006). Effects of inhaled manganese on biomarkers of oxidative stress in the rat brain. Neurotoxicology 27, 788-797.
41. Tholey, G., Ledig, M., Mandel, P., Sargentini, L., Frivold, A. H., Leroy, M., Grippo, A. A., and Wedler, F. C. (1988). Concentrations of physiologically important metal ions in glial cells cultured from chick cerebral cortex. Neurochem. Res. 13, 45-50.
42. Wakade, C., Khan, M. M., De Sevilla, L. M., Zhang, Q. G., Mahesh, V. B., and Brann, D. W. (2008). Tamoxifen neuroprotection in cerebral ischemia involves attenuation of kinase activation and superoxide production and potentiation of mitochondrial superoxide dismutase. Endocrinology 149, 367-379.
43. Wang, X., Dykens, J. A., Perez, E., Liu, R., Yang, S., Covey, D. F., and Simpkins, J. W. (2006). Neuroprotective effects of 17beta-estradiol and nonfeminizing estrogens against H2O2 toxicity in human neuroblastoma SK-N-SH cells. Mol. Pharmacol. 70, 395-404.
44. Watters, J. J., Campbell, J. S., Cunningham, M. J., Krebs, E. G., and Dorsa, D. M. (1997). Rapid membrane effects of steroids in neuroblastoma cells: Effects of estrogen on mitogen activated protein kinase signalling cascade and c-fos immediate early gene transcription. Endocrinology 138, 4030-4033.
45. Wilson, M. E., Liu, Y., and Wise, P. M. (2002). Estradiol enhances Akt activation in cortical explant cultures following neuronal injury. Brain Res. Mol. Brain Res. 102, 48-54.
46. Worley, C. G., Bombick, D., Allen, J. W., Suber, R. L., and Aschner, M. (2002). Effects of manganese on oxidative stress in CATH.a cells. Neurotoxicology 23, 159-164.
47. 2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: A potential initiation mechanism for estrogen-induced neuroprotection. Neuroscience 135, 59-72.
48. Zhang, Y., Milatovic, D., Aschner, M., Feustel, P. J., and Kimelberg, H. K. (2007). Neuroprotection by tamoxifen in focal cerebral ischemia is not mediated by an agonist action at estrogen receptors but is associated with antioxidant activity. Exp. Neurol. 204, 819-827.