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BioMed Research International
Volume 2013 (2013), Article ID 769295, 12 pages
http://dx.doi.org/10.1155/2013/769295
Research Article

In Vitro Manganese Exposure Disrupts MAPK Signaling Pathways in Striatal and Hippocampal Slices from Immature Rats

1Departamento de Bioquímica, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Campus Universitário, 88040-900 Florianópolis, SC, Brazil
2Escola de Medicina Veterinária e Zootecnia, Universidade Federal do Tocantins, 77804-970 Araguaína, TO, Brazil
3Departamento de Biologia Celular, Embriologia e Genética, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Campus Universitário, 88040-900 Florianópolis, SC, Brazil
4Departamento de Clínica Médica, Centro de Ciências da Saúde, Universidade Federal de Santa Catarina, Hospital Universitário (HU), 88036-800 Florianópolis, SC, Brazil
5Department of Pediatrics, Vanderbilt University Medical Center, Nashville, TN 37232, USA

Received 31 July 2013; Accepted 7 October 2013

Academic Editor: Wilma De Grava Kempinas

Copyright © 2013 Tanara Vieira Peres et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Aschner, K. M. Erikson, E. H. Hernández, and R. Tjalkens, “Manganese and its role in Parkinson's disease: from transport to neuropathology,” NeuroMolecular Medicine, vol. 11, no. 4, pp. 252–266, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. T. R. Guilarte, “Manganese and Parkinson's disease: a critical review and new findings,” Environmental Health Perspectives, vol. 118, no. 8, pp. 1071–1080, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. T. E. Gunter, C. E. Gavin, M. Aschner, and K. K. Gunter, “Speciation of manganese in cells and mitochondria: a search for the proximal cause of manganese neurotoxicity,” NeuroToxicology, vol. 27, no. 5, pp. 765–776, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. T. R. Guilarte, N. C. Burton, T. Verina et al., “Increased APLP1 expression and neurodegeneration in the frontal cortex of manganese-exposed non-human primates,” Journal of Neurochemistry, vol. 105, no. 5, pp. 1948–1959, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. R. M. Molina, S. Phattanarudee, J. Kim et al., “Ingestion of Mn and Pb by rats during and after pregnancy alters iron metabolism and behavior in offspring,” NeuroToxicology, vol. 32, no. 4, pp. 413–422, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. C. H. Kern and D. R. Smith, “Preweaning Mn exposure leads to prolonged astrocyte activation and lasting effects on the dopaminergic system in adult male rats,” Synapse, vol. 65, no. 6, pp. 532–544, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. J. A. Moreno, E. C. Yeomans, K. M. Streifel, B. L. Brattin, R. J. Taylor, and R. B. Tjalkens, “Age-dependent susceptibility to manganese-induced neurological dysfunction,” Toxicological Sciences, vol. 112, no. 2, pp. 394–404, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. L. E. Gonzalez, A. A. Juknat, A. J. Venosa, N. Verrengia, and M. L. Kotler, “Manganese activates the mitochondrial apoptotic pathway in rat astrocytes by modulating the expression of proteins of the Bcl-2 family,” Neurochemistry International, vol. 53, no. 6–8, pp. 408–415, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. Y. Liu, D. S. Barber, P. Zhang, and B. Liu, “Complex II of the mitochondrial respiratory chain is the key mediator of divalent manganese-induced hydrogen peroxide production in microglia,” Toxicological Sciences, vol. 132, no. 2, pp. 298–306, 2013. View at Publisher · View at Google Scholar
  10. H. Yoon, D.-S. Kim, G.-H. Lee, K.-W. Kim, H.-R. Kim, and H.-J. Chae, “Apoptosis induced by manganese on neuronal SK-N-MC cell line: Endoplasmic Reticulum (ER) stress and mitochondria dysfunction,” Environmental Health and Toxicology, vol. 26, Article ID e2011017, 2011. View at Publisher · View at Google Scholar
  11. D. Milatovic, S. Zaja-Milatovic, R. C. Gupta, Y. Yu, and M. Aschner, “Oxidative damage and neurodegeneration in manganese-induced neurotoxicity,” Toxicology and Applied Pharmacology, vol. 240, no. 2, pp. 219–225, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. F. M. Cordova, A. S. Aguiar Jr., T. V. Peres et al., “In vivo manganese exposure modulates Erk, Akt and Darpp-32 in the striatum of developing rats, and impairs their motor function,” PLoS ONE, vol. 7, no. 3, Article ID e33057, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. F. M. Cordova, A. S. Aguiar Jr., T. V. Peres, et al., “Manganese-exposed developing rats display motor deficits and striatal oxidative stress that are reversed by Trolox,” vol. 87, no. 7, pp. 1231–1244, 2013. View at Publisher · View at Google Scholar
  14. Y. Hirata, T. Meguro, and K. Kiuchi, “Differential effect of nerve growth factor on dopaminergic neurotoxin-induced apoptosis,” Journal of Neurochemistry, vol. 99, no. 2, pp. 416–425, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Ito, K. Oh-hashi, K. Kiuchi, and Y. Hirata, “p44/42 MAP kinase and c-Jun N-terminal kinase contribute to the up-regulation of caspase-3 in manganese-induced apoptosis in PC12 cells,” Brain Research, vol. 1099, no. 1, pp. 1–7, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. K. Prabhakaran, G. D. Chapman, and P. G. Gunasekar, “α-synuclein overexpression enhances manganese-induced neurotoxicity through the NF-κB-mediated pathway,” Toxicology Mechanisms and Methods, vol. 21, no. 6, pp. 435–443, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. Z. Yin, J. L. Aschner, A. P. dos Santos, and M. Aschner, “Mitochondrial-dependent manganese neurotoxicity in rat primary astrocyte cultures,” Brain Research, vol. 1203, pp. 1–11, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. E. K. Kim and E.-J. Choi, “Pathological roles of MAPK signaling pathways in human diseases,” Biochimica et Biophysica Acta, vol. 1802, no. 4, pp. 396–405, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. G. M. Thomas and R. L. Huganir, “MAPK cascade signalling and synaptic plasticity,” Nature Reviews Neuroscience, vol. 5, no. 3, pp. 173–183, 2004. View at Scopus
  20. T. R. Guilarte, N. C. Burton, J. L. McGlothan et al., “Impairment of nigrostriatal dopamine neurotransmission by manganese is mediated by pre-synaptic mechanism(s): implications to manganese-induced parkinsonism,” Journal of Neurochemistry, vol. 107, no. 5, pp. 1236–1247, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. K. M. Erikson, K. Thompson, J. Aschner, and M. Aschner, “Manganese neurotoxicity: a focus on the neonate,” Pharmacology & Therapeutics, vol. 113, no. 2, pp. 369–377, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. S. C. Sistrunk, M. K. Ross, and N. M. Filipov, “Direct effects of manganese compounds on dopamine and its metabolite Dopac: an in vitro study,” Environmental Toxicology and Pharmacology, vol. 23, no. 3, pp. 286–296, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Posser, J. L. Franco, L. Bobrovskaya, R. B. Leal, P. W. Dickson, and P. R. Dunkley, “Manganese induces sustained Ser40 phosphorylation and activation of tyrosine hydroxylase in PC12 cells,” Journal of Neurochemistry, vol. 110, no. 3, pp. 848–856, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Sengupta, “The laboratory rat: relating its age with human's,” International Journal of Preventive Medicine, vol. 4, no. 6, pp. 624–630, 2013.
  25. F. M. Cordova, A. L. S. Rodrigues, M. B. O. Giacomelli et al., “Lead stimulates ERK1/2 and p38MAPK phosphorylation in the hippocampus of immature rats,” Brain Research, vol. 998, no. 1, pp. 65–72, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. A. V. Jacques, D. K. Rieger, M. Maestri, et al., “Lectin from Canavalia brasiliensis (ConBr) protects hippocampal slices against glutamate neurotoxicity in a manner dependent of PI3K/Akt pathway,” Neurochemistry International, vol. 62, no. 6, pp. 836–842, 2013. View at Publisher · View at Google Scholar
  27. S. Molz, H. Decker, T. Dal-Cim et al., “Glutamate-induced toxicity in hippocampal slices involves apoptotic features and p38MAPK signaling,” Neurochemical Research, vol. 33, no. 1, pp. 27–36, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Suzuki, T. Mouri, and Y. Suzuki, “Study of subacute toxicity of manganese dioxide in monkeys,” Tokushima Journal of Experimental Medicine, vol. 22, pp. 5–10, 1975. View at Scopus
  29. Y. Liu, D. A. Peterson, H. Kimura, and D. Schubert, “Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5- diphenyltetrazolium bromide (MTT) reduction,” Journal of Neurochemistry, vol. 69, no. 2, pp. 581–593, 1997. View at Scopus
  30. A. P. Rigon, F. M. Cordova, C. S. Oliveira et al., “Neurotoxicity of cadmium on immature hippocampus and a neuroprotective role for p38MAPK,” NeuroToxicology, vol. 29, no. 4, pp. 727–734, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. R. B. Leal, F. M. Cordova, L. Herd, L. Bobrovskaya, and P. R. Dunkley, “Lead-stimulated p38MAPK-dependent Hsp27 phosphorylation,” Toxicology and Applied Pharmacology, vol. 178, no. 1, pp. 44–51, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. G. L. Peterson, “A simplification of the protein assay method of Lowry et al. Which is more generally applicable,” Analytical Biochemistry, vol. 83, no. 2, pp. 346–356, 1977. View at Scopus
  33. P. R. Dunkley, L. Bobrovskaya, M. E. Graham, E. I. Von Nagy-Felsobuki, and P. W. Dickson, “Tyrosine hydroxylase phosphorylation: regulation and consequences,” Journal of Neurochemistry, vol. 91, no. 5, pp. 1025–1043, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. S. C. Kumer and K. E. Vrana, “Intricate regulation of tyrosine hydroxylase activity and gene expression,” Journal of Neurochemistry, vol. 67, no. 2, pp. 443–462, 1996. View at Scopus
  35. T. Cai, H. Che, T. Yao et al., “Manganese induces Tau hyperphosphorylation through the activation of ERK MAPK pathway in PC12 cells,” Toxicological Sciences, vol. 119, no. 1, pp. 169–177, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. J.-H. Bae, B.-C. Jang, S.-I. Suh et al., “Manganese induces inducible nitric oxide synthase (iNOS) expression via activation of both MAP kinase and PI3K/Akt pathways in BV2 microglial cells,” Neuroscience Letters, vol. 398, no. 1-2, pp. 151–154, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. P. L. Crittenden and N. M. Filipov, “Manganese modulation of MAPK pathways: effects on upstream mitogen activated protein kinase kinases and mitogen activated kinase phosphatase-1 in microglial cells,” Journal of Applied Toxicology, vol. 31, no. 1, pp. 1–10, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. P. Grandjean and P. Landrigan, “Developmental neurotoxicity of industrial chemicals,” The Lancet, vol. 368, no. 9553, pp. 2167–2178, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Zhang, A. Kanthasamy, V. Anantharam, and A. Kanthasamy, “Effects of manganese on Tyrosine Hydroxylase (TH) activity and TH-phosphorylation in a dopaminergic neural cell line,” Toxicology and Applied Pharmacology, vol. 254, no. 2, pp. 65–71, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. N. M. Filipov and C. A. Dodd, “Role of glial cells in manganese neurotoxicity,” Journal of Applied Toxicology, vol. 32, no. 5, pp. 310–317, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. F. Zhao, T. Cai, M. Liu, G. Zheng, W. Luo, and J. Chen, “Manganese induces dopaminergic neurodegeneration via microglial activation in a rat model of manganism,” Toxicological Sciences, vol. 107, no. 1, pp. 156–164, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. C.-X. Gong, T. Lidsky, J. Wegiel, I. Grundke-Iqbal, and K. Iqbal, “Metabolically active rat brain slices as a model to study the regulation of protein phosphorylation in mammalian brain,” Brain Research Protocols, vol. 6, no. 3, pp. 134–140, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Hirata and T. Nagatsu, “Rotenone and CCCP inhibit tyrosine hydroxylation in rat striatal tissue slices,” Toxicology, vol. 216, no. 1, pp. 9–14, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Rodnight and R. Leal, “Regional variations in protein phosphorylating activity in rat brain studied in micro-slices labeled with [32P]phosphate,” Journal of Molecular Neuroscience, vol. 2, no. 2, pp. 115–122, 1990. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Díaz-Véliz, S. Mora, P. Gómez et al., “Behavioral effects of manganese injected in the rat substantia nigra are potentiated by dicumarol, a DT-diaphorase inhibitor,” Pharmacology Biochemistry and Behavior, vol. 77, no. 2, pp. 245–251, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. E. J. Martinez-Finley, C. E. Gavin, M. Aschner, and T. E. Gunter, “Manganese neurotoxicity and the role of reactive oxygen species,” Free Radical Biology and Medicine, vol. 62, pp. 65–75, 2013. View at Publisher · View at Google Scholar
  47. K. Prabhakaran, D. Ghosh, G. D. Chapman, and P. G. Gunasekar, “Molecular mechanism of manganese exposure-induced dopaminergic toxicity,” Brain Research Bulletin, vol. 76, no. 4, pp. 361–367, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Benedetto, C. Au, D. S. Avila, D. Milatovic, and M. Aschner, “Extracellular dopamine potentiates Mn-induced oxidative stress, lifespan reduction, and dopaminergic neurodegeneration in a BLI-3-dependent manner in caenorhabditis elegans,” PLoS Genetics, vol. 6, no. 8, Article ID e1001084, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Au, A. Benedetto, and M. Aschner, “Manganese transport in eukaryotes: the role of DMT1,” NeuroToxicology, vol. 29, no. 4, pp. 569–576, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. E. N. Martins, N. T. C. Pessano, L. Leal et al., “Protective effect of Melissa officinalis aqueous extract against Mn-induced oxidative stress in chronically exposed mice,” Brain Research Bulletin, vol. 87, no. 1, pp. 74–79, 2012. View at Publisher · View at Google Scholar · View at Scopus