Elevated adult neurogenesis in brain subventricular zone following in vivo manganese exposure: Roles of copper and DMT1

Toxicological Sciences

Volumn 143, Issue 2, 2015, Pages 482-498

  Fu, Sherleen ^a   O'Neal, Stefanie ^a   Hong, Lan ^a   Jiang, Wendy ^a   Zheng, Wei ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Adult neurogenesis; Copper; Divalent metal transporter 1; Manganese; Rostral migratory stream; Subventricular zone

Indexed keywords

BROXURIDINE; COPPER; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; MANGANESE; MESSENGER RNA; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; NESTIN; CATION TRANSPORT PROTEIN; CHLORIDE; MANGANESE CHLORIDE; MANGANESE DERIVATIVE; SOLUTE CARRIER FAMILY 11- (PROTON-COUPLED DIVALENT METAL ION TRANSPORTERS), MEMBER 2;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ATOMIC ABSORPTION SPECTROMETRY; BRAIN REGION; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NEUROTOXICITY; NONHUMAN; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROSTRAL MIGRATORY STREAM; SUBVENTRICULAR ZONE; WESTERN BLOTTING; ANIMAL; CELL PROLIFERATION; DRUG EFFECTS; GENETICS; INTRAPERITONEAL DRUG ADMINISTRATION; LATERAL BRAIN VENTRICLE; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; TISSUE DISTRIBUTION;

ANIMALIA; RATTUS;

ANIMALS; BLOTTING, WESTERN; CATION TRANSPORT PROTEINS; CELL PROLIFERATION; CHLORIDES; COPPER; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAPERITONEAL; LATERAL VENTRICLES; MALE; MANGANESE COMPOUNDS; NEUROGENESIS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; SPECTROPHOTOMETRY, ATOMIC; TISSUE DISTRIBUTION;

EID: 84924742286     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfu249     Document Type: Article

References (45)

1. Andrews, N. C. (1999). The iron transporter DMT1. Int. J. Biochem. Cell Biol. 31, 991-994.
2. Barnham, K. J., and Bush, A. I. (2008). Metals in Alzheimer's and Parkinson's diseases. Curr. Opin. Chem. Biol. 12, 222-228.
3. Burdo, J. R., Menzies, S. L., Simpson, I. A., Garrick, L. M., Garrick, M. D., Dolan, K. G., Haile, D. J., Beard, J. L., and Connor, J. R. (2001). Distribution of divalent metal transporter 1 and metal transport protein 1 in the normal and Belgrade rat. J. Neurosci. 66, 1198-1207.
4. Choi, B. S., and Zheng, W. (2009). Copper transport to the brain by the blood-brain barrier and blood-CSF barrier. Brain Res. 1248, 14-21.
5. Curtis, M. A., Faull, R. L. M., and Eriksson, P. S. (2007). The effect of neurodegenerative diseases on the subventricular zone. Nat. Rev. Neurosci. 8, 712-723.
6. Deibel, M. A., Ehmann, W. D., and Markesbery, W. R. (1996). Copper, iron, and zinc imbalances in severely degenerated brain regions in Alzheimer's disease: possible relation to oxidative stress. J. Neurol. Sci. 143, 137-142.
7. Doetsch, F., Caillé, I., Lim, D. A., García-Verdugo, J. M., and Alvarez-Buylla, A. (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716.
8. Doetsch, F., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (1997). Cellular composition and three-dimensional organization of the subventricular geminal zone in the adult mammalian brain. J. Neurosci. 17, 5046-5061.
9. El Meskini, R., Crabtree, K. L., Cline, L. B., Mains, R. E., Eipper, B. A., and Ronnett, G. V. (2007). ATP7A (Menkes protein) functions in axonal targeting and synaptogenesis. Mol. Cell Neurosci. 34, 409-421.
10. Fu, X., Zhang, Y., Jiang, W., Monnot, A. D., Bates, C. A., and Zheng, W. (2014). Regulation of copper transport crossing brain barrier systems by Cu-ATPases: effect of manganese exposure. Toxicol Sci. 139, 432-451.
11. Gaggelli, E., Kozlowski, H., Valensin, D., and Valensin, G. (2006). Copper homeostasis and neurodegenerative disorders (Alzheimer's, prion, and Parkinson's diseases and amyotrophic lateral sclerosis). Chem. Rev. 106, 1995-2044.
12. Ghashghaei, H. T., Lai, C., and Anton, E. S. (2007). Neuronal migration in the adult brain: are we there yet? Nat. Rev. Neurosci. 8, 141-151.
13. Gruenheid, S., Cellier, M., Vidal, S., and Gros, P. (1995). Identification and characterization of a second mouse Nramp gene. Genomics 25, 514-525.
14. Gunshin, H., Mackenzie, B., Berger, U. V., Gunshin, Y., Romero, M. F., Boron, W. F., Nussberger, S., Gollan, J. L., and Hediger, M. A. (1997). Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388, 482-488.
15. Haremaki, T., Fraser, S. T., Kuo, Y. M., Baron, M. H., and Weinstein, D. C. (2007). Vertebrate Ctr1 coordinates morphogenesis and progenitor cell fate and regulates embryonic stem cell differentiation. Proc. Natl Acad. Sci. U. S. A. 104, 12029-12034.
16. Harris, E. D. (2001). Copper homeostasis: the role of cellular transporters. Nutr. Rev. 59, 281-285.
17. Imura, T., Nakano, I., Kornblum, H. I., and Sofroniew, M. V. (2006). Phenotypic and functional heterogeneity of GFAP-expressing cells in vitro: differential expression of LeX/CD15 by GFAP-expressing multipotent neural stem cells and nonneurogenic astrocytes. Glia 53, 277-293.
18. Joseph, R. P., Bruce, B. (2001). Dietary copper deficiency alters protein levels of rat dopamine ß-monooxygenase and tyrosine monooxygenase. Exp. Biol. Med. 226, 199-207.
19. Klausner, R. D., Rouault, T. A., and Harford, J. B. (1993). Regulating the fate of mRNA: the control of cellular iron metabolism. Cell 72, 19-28.
20. Li, G. J., Zhao, Q., and Zheng, W. (2005). Alteration at translational but not transcriptional level of transferrin receptor expression following manganese exposure at the blood-CSF barrier in vitro. Toxicol. Appl. Pharmacol. 205, 188-200.
21. Lledo, P. M., Alonso, M., and Grubb, M. S. (2006). Adult neurogenesis and functional plasticity in neuronal circuits. Nat. Rev. Neurosci. 7, 179-193.
22. Lois, C., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (1996). Chain migration of neuronal precursors. Science 271, 978-981.
23. Lorraine, G., Christine, K., and Harry, J. M. (2011). Iron and copper in fetal development. Semin. Cell Dev. Biol. 22, 637-644.
24. Luskin, M. B. (1993). Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11, 173-189.
25. Martino, G., and Pluchino, S. (2006). The therapeutic potential of neural stem cells. Nat. Rev. Neurosci. 7, 395-406.
26. Matés, J. M., Segura, J. A., Alonso, F. J., and Márquez, J. (2010). Roles of dioxins and heavy metals in cancer and neurological diseases using ROS-mediated mechanisms. Free Radic. Biol. Med. 49, 1328-1341.
27. Matusch,A., Depboylu,C., Palm,C.,Wu, B., Höglinger, G. U., Schäfer, M. K., and Becker, J. S. (2010). Cerebral bioimaging of Cu, Fe, Zn, and Mn in the MPTP mouse model of Parkinson's disease using laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). J.Am. Soc.Mass Spectrom. 21, 161-171.
28. Menezes, J. R., Smith, C. M., Nelson, K. C., and Luskin, M. B. (1995). The division of neuronal progenitor cells during migration in the neuonatal mammalian forebrain. Mol. Cell. Neurosci. 6, 496-508.
29. Michalczyk, K., and Ziman, M. (2005). Nestin structure and predicted function in cellular cytoskeletal organisation. Histol. Histopathol. 20, 665-671.
30. Monnot, A. D., Zheng, G., and Zheng, W. (2012). Mechanism of copper transport at the blood-cerebrospinal fluid barrier: influence of iron deficiency. Exp. Biol. Med. 237, 327-333.
31. Niciu, M. J., Ma, X. M., El Meskini, R., Pachter, J. S., Mains, R. E., and Eipper, B. A. (2007). Altered ATP7A expression and other compensatory responses in a murine model of Menkes disease. Neurobiol. Dis. 27, 278-291.
32. O'Neal, S. L., Lee, J. W., Zheng, W., and Cannon, J. R. (2014). Subchronic manganese exposure in rats is a neurochemical model of early manganese toxicity. Neurotoxicology 44, 303-313.
33. Pushie, M. J., Pickering, I. J., Martin, G. R., Tsutsui, S., Jirik, F. R., and George, G. N. (2011). Prion protein expression level alters regional copper, iron and zinc content in the mouse brain. Metallomics 3, 206-214.
34. Pushkar, Y., Robison, G., Sullivan, B., Fu, S. X., Kohne, M., Jiang, W., Rohr, S., Lai, B., Marcus, M. A., Zakharova, T., et al. (2013). Aging results in copper accumulations in glial fibrillary acidic protein-positive cells in the subventricular zone. Aging Cell 12, 823-832.
35. Robison, G., Zakharova, T., Fu, X., Jiang, W., Fulper, R., Barrea, R., Marcus, M. A., Zheng, W., and Pushkar, Y. (2012). X-ray fluorescence imaging: a new tool for studying manganese neurotoxicity. PLoS One 7, e48899.
36. Skjorringe, T., Moller, L., and Moos, T. (2012). Impairment of interrelated iron- and copper homeostatic mechanisms in brain contributes to the pathogenesis of neurodegenerative disorders. Front. Pharmacol. 3, 169.
37. Takahashi, Y., Kako, K., Kashiwabara, S., Takehara, A., Inada, Y., Arai, H., Nakada, K., Kodama, H., Hayashi, J., Baba, T., et al. (2002). Mammalian copper chaperone cox17p has an essential role in activation of cytochrome C oxidase and embryonic development. Mol. Cell Biol. 22, 7614-7621.
38. Turski, M. L., and Thiele, D. J. (2009). New roles for copper metabolism in cell proliferation, signaling, and disease. J. Biol. Chem. 284, 717-721.
39. Uriu-Adams, J., Scherr, R., Lanoue, L., and Keen, C. L. (2010). Influence of copper on early development: prenatal and postnatal considerations. Biofactors 36, 136-152.
40. Wang, L., Ohishi, T., Shiraki, A., Morita, R., Akane, H., Ikarashi, Y., Mitsumori, K., and Shibutani, M. (2012). Developmental exposure to manganese chloride induces sustained aberration of neurogenesis in the hippocampal dentate gyrus of mice. Toxicol. Sci. 127, 508-521.
41. Wang, X., Li, G. J., and Zheng, W. (2006). Up-regulation of DMT1 expression in choroidal epithelial cells following manganese exposure. Brain Res. 1097, 1-10.
42. Zheng, W., Jiang, Y. M., Zhang, Y., Jiang, W., Wang, X., and Cowan, D. M. (2009). Chelation therapy of manganese intoxication with para-aminosalicylic acid (PAS) in Sprague-Dawley rats. Neurotoxicology 30, 240-248.
43. Zheng, W., and Monnot, A. D. (2012). Regulation of brain iron and copper homeostasis by brain barrier systems: implication in neurodegenerative diseases. Pharmacol. Ther. 133, 177-188.
44. Zheng, W., Ren, S., and Graziano, J. H. (1998). Manganese inhibits mitochondrial aconitase: a mechanism of manganese neurotoxicity. Brain Res. 799, 334-342.
45. Zheng, W., Zhao, Q., Slavkovich, V., Aschner, M., and Graziano, J. H. (1999). Alteration of iron homeostasis following chronic exposure to manganese in rats. Brain Res. 833, 125-132.