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Journal of Toxicology
Volume 2015, Article ID 532691, 10 pages
http://dx.doi.org/10.1155/2015/532691
Research Article

MeHg Developing Exposure Causes DNA Double-Strand Breaks and Elicits Cell Cycle Arrest in Spinal Cord Cells

1Departamento de Biologia Celular, Embriologia e Genética, Centro de Ciências Biológicas, UFSC, Campus Universitário, Trindade, 88040-900 Florianópolis, SC, Brazil
2Instituto de Ciências Naturais Humanas e Sociais, UFMT, Avenida Alexandre Ferronato 1200, Setor Industrial, 78557287 Sinop, MT, Brazil
3Centro Universitário Católica de Santa Catarina, Rua Visconde de Taunay 427, Centro, 89203-005 Joinville, SC, Brazil
4Departamento de Fisioterapia, Centro de Ciências da Saúde e do Esporte, UDESC, Rua Pascoal Simone 358, Coqueiros, 88080-350 Florianópolis, SC, Brazil

Received 3 September 2015; Revised 22 November 2015; Accepted 23 November 2015

Academic Editor: Lucio Guido Costa

Copyright © 2015 Fabiana F. Ferreira 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. F. M. M. Morel, A. M. L. Kraepiel, and M. Amyot, “The chemical cycle and bioaccumulation of mercury,” Annual Review of Ecology and Systematics, vol. 29, no. 1, pp. 543–566, 1998. View at Publisher · View at Google Scholar · View at Scopus
  2. R. A. Bernhoft, “Mercury toxicity and treatment: a review of the literature,” Journal of Environmental and Public Health, vol. 2012, Article ID 460508, 10 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Grandjean, P. Weihe, R. F. White et al., “Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury,” Neurotoxicology and Teratology, vol. 19, no. 6, pp. 417–428, 1997. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Kakita, K. Wakabayashi, M. Su, M. Sakamoto, F. Ikuta, and H. Takahashi, “Distinct pattern of neuronal degeneration in the fetal rat brain induced by consecutive transplacental administration of methylmercury,” Brain Research, vol. 859, no. 2, pp. 233–239, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Bertossi, F. Girolamo, M. Errede et al., “Effects of methylmercury on the microvasculature of the developing brain,” Neurotoxicology, vol. 25, no. 5, pp. 849–857, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Sakamoto, A. Kakita, R. B. De Oliveira, H. Sheng Pan, and H. Takahashi, “Dose-dependent effects of methylmercury administered during neonatal brain spurt in rats,” Developmental Brain Research, vol. 152, no. 2, pp. 171–176, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. P. M. Rodier, M. Aschner, and P. R. Sager, “Mitotic arrest in the developing CNS after prenatal exposure to methylmercury,” Neurobehavioral Toxicology and Teratology, vol. 6, no. 5, pp. 379–385, 1984. View at Google Scholar · View at Scopus
  8. M. Aschner and J. L. Aschner, “Mercury neurotoxicity: mechanisms of blood-brain barrier transport,” Neuroscience and Biobehavioral Reviews, vol. 14, no. 2, pp. 169–176, 1990. View at Publisher · View at Google Scholar · View at Scopus
  9. K. Yurdakök, “Environmental pollution and the fetus,” Journal of Pediatric and Neonatal Individualized Medicine, vol. 1, no. 1, pp. 33–42, 2012. View at Google Scholar
  10. S. Bose-O'Reilly, K. M. McCarty, N. Steckling, and B. Lettmeier, “Mercury exposure and children's health,” Current Problems in Pediatric and Adolescent Health Care, vol. 40, no. 8, pp. 186–215, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Farina, J. B. T. Rocha, and M. Aschner, “Mechanisms of methylmercury-induced neurotoxicity: evidence from experimental studies,” Life Sciences, vol. 89, no. 15-16, pp. 555–563, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. E. Patel and M. Reynolds, “Methylmercury impairs motor function in early development and induces oxidative stress in cerebellar granule cells,” Toxicology Letters, vol. 222, no. 3, pp. 265–272, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Sokolowski, M. Obiorah, K. Robinson, E. Mccandlish, B. Buckley, and E. Dicicco-Bloom, “Neural stem cell apoptosis after low-methylmercury exposures in postnatal hippocampus produce persistent cell loss and adolescent memory deficits,” Developmental Neurobiology, vol. 73, no. 12, pp. 936–949, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Burke, Y. Cheng, B. Li et al., “Methylmercury elicits rapid inhibition of cell proliferation in the developing brain and decreases cell cycle regulator, cyclin E,” NeuroToxicology, vol. 27, no. 6, pp. 970–981, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Aschner, C. P. Yao, J. W. Allen, and K. H. Tan, “Methylmercury alters glutamate transport in astrocytes,” Neurochemistry International, vol. 37, no. 2-3, pp. 199–206, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. T. L. Limke, S. R. Heidemann, and W. D. Atchison, “Disruption of intraneuronal divalent cation regulation by methylmercury: are specific targets involved in altered neuronal development and cytotoxicity in methylmercury poisoning?” NeuroToxicology, vol. 25, no. 5, pp. 741–760, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. J. L. Franco, T. Posser, P. R. Dunkley et al., “Methylmercury neurotoxicity is associated with inhibition of the antioxidant enzyme glutathione peroxidase,” Free Radical Biology and Medicine, vol. 47, no. 4, pp. 449–457, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Farina, M. Aschner, and J. B. T. Rocha, “Oxidative stress in MeHg-induced neurotoxicity,” Toxicology and Applied Pharmacology, vol. 256, no. 3, pp. 405–417, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Polunas, A. Halladay, R. B. Tjalkens, M. A. Philbert, H. Lowndes, and K. Reuhl, “Role of oxidative stress and the mitochondrial permeability transition in methylmercury cytotoxicity,” NeuroToxicology, vol. 32, no. 5, pp. 526–534, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Tamm, J. Duckworth, O. Hermanson, and S. Ceccatelli, “High susceptibility of neural stem cells to methylmercury toxicity: effects on cell survival and neuronal differentiation,” Journal of Neurochemistry, vol. 97, no. 1, pp. 69–78, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. T.-H. Lu, S.-Y. Hsieh, C.-C. Yen et al., “Involvement of oxidative stress-mediated ERK1/2 and p38 activation regulated mitochondria-dependent apoptotic signals in methylmercury-induced neuronal cell injury,” Toxicology Letters, vol. 204, no. 1, pp. 71–80, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Sokolowski, A. Falluel-Morel, X. Zhou, and E. DiCicco-Bloom, “Methylmercury (MeHg) elicits mitochondrial-dependent apoptosis in developing hippocampus and acts at low exposures,” NeuroToxicology, vol. 32, no. 5, pp. 535–544, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. M. C. Carvalho, E. M. Nazari, M. Farina, and Y. M. R. Muller, “Behavioral, morphological, and biochemical changes after in ovo exposure to methylmercury in chicks,” Toxicological Sciences, vol. 106, no. 1, pp. 180–185, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. V. Hamburger and H. L. Hamilton, “A series of normal stages in the development of the chick embryo,” Journal of Morphology, vol. 88, no. 1, pp. 49–92, 1951. View at Publisher · View at Google Scholar
  25. G. H. Heinz, D. J. Hoffman, S. L. Kondrad, and C. A. Erwin, “Factors affecting the toxicity of methylmercury injected into eggs,” Archives of Environmental Contamination and Toxicology, vol. 50, no. 2, pp. 264–279, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. G. H. Heinz, D. J. Hoffman, J. D. Klimstra, K. R. Stebbins, S. L. Kondrad, and C. A. Erwin, “Species differences in the sensitivity of avian embryos to methylmercury,” Archives of Environmental Contamination and Toxicology, vol. 56, no. 1, pp. 129–138, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. G. Danscher, “Autometallography: a new technique for light and electron microscopic visualization of metals in biological tissues (gold, silver, metal sulphides and metal selenides),” Histochemistry, vol. 81, no. 4, pp. 331–335, 1984. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. M. R. Müller, K. Kobus, J. C. Schatz, D. Ammar, and E. M. Nazari, “Prenatal lead acetate exposure induces apoptosis and changes GFAP expression during spinal cord development,” Ecotoxicology and Environmental Safety, vol. 75, no. 1, pp. 223–229, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. C. A. Mandarim-de-Lacerda, “Stereological tools in biomedical research,” Anais da Academia Brasileira de Ciências, vol. 75, no. 4, pp. 469–486, 2003. View at Google Scholar
  30. G. F. Bourckhardt, M. S. Cecchini, D. Ammar, K. Kobus-Bianchini, Y. M. R. Müller, and E. M. Nazari, “Effects of homocysteine on mesenchymal cell proliferation and differentiation during chondrogenesis on limb development,” Journal of Applied Toxicology, vol. 35, pp. 1390–1397, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. M. R. Müller, L. B. D. Rivero, M. C. Carvalho, K. Kobus, M. Farina, and E. M. Nazari, “Behavioral impairments related to lead-induced developmental neurotoxicity in chicks,” Archives of Toxicology, vol. 82, no. 7, pp. 445–451, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Matsumoto, G. Koya, and T. Takeuchi, “Fetal Minamata disease: a neuropathological study of two cases of intrauterine intoxication by a methyl mercury compound,” Journal of Neuropathology and Experimental Neurology, vol. 24, no. 4, pp. 563–574, 1965. View at Publisher · View at Google Scholar · View at Scopus
  33. B. H. Choi, L. W. Lapham, L. Amin-Zaki, and T. Saleem, “Abnormal neuronal migration, deranged cerebral cortical organization, and diffuse white matter astrocytosis of human fetal brain: a major effect of methylmercury poisoning in utero,” Journal of Neuropathology and Experimental Neurology, vol. 37, no. 6, pp. 719–733, 1978. View at Publisher · View at Google Scholar · View at Scopus
  34. P. R. Sager, R. A. Doherty, and P. M. Rodier, “Effects of methylmercury on developing mouse cerebellar cortex,” Experimental Neurology, vol. 77, no. 1, pp. 179–193, 1982. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Falluel-Morel, K. Sokolowski, H. M. Sisti, X. Zhou, T. J. Shors, and E. DiCicco-Bloom, “Developmental mercury exposure elicits acute hippocampal cell death, reductions in neurogenesis, and severe learning deficits during puberty,” Journal of Neurochemistry, vol. 103, no. 5, pp. 1968–1981, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Ceccatelli, R. Bose, K. Edoff, N. Onishchenko, and S. Spulber, “Long-lasting neurotoxic effects of exposure to methylmercury during development,” Journal of Internal Medicine, vol. 273, no. 5, pp. 490–497, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. S. A. Hassan, E. A. Moussa, and L. C. Abbott, “The effect of methylmercury exposure on early central nervous system development in the zebrafish (Danio rerio) embryo,” Journal of Applied Toxicology, vol. 32, no. 9, pp. 707–713, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. R. W. Huyck, M. Nagarkar, N. Olsen, S. E. Clamons, and M. S. Saha, “Methylmercury exposure during early Xenopus laevis development affects cell proliferation and death but not neural progenitor specification,” Neurotoxicology and Teratology, vol. 47, pp. 102–113, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. R. A. Ponce, T. J. Kavanagh, N. K. Mottet, S. G. Whittaker, and E. M. Faustman, “Effects of methyl mercury on the cell cycle of primary rat CNS cells in vitro,” Toxicology and Applied Pharmacology, vol. 127, no. 1, pp. 83–90, 1994. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Xu, C. Yan, Y. Tian, X. Yuan, and X. Shen, “Effects of low level of methylmercury on proliferation of cortical progenitor cells,” Brain Research, vol. 1359, pp. 272–280, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Fujimura and F. Usuki, “Low concentrations of methylmercury inhibit neural progenitor cell proliferation associated with up-regulation of glycogen synthase kinase 3β and subsequent degradation of cyclin E in rats,” Toxicology and Applied Pharmacology, vol. 288, no. 1, pp. 19–25, 2015. View at Publisher · View at Google Scholar
  42. Y. C. Ou, S. A. Thompson, R. A. Ponce, J. Schroeder, T. J. Kavanagh, and E. M. Faustman, “Induction of the cell cycle regulatory gene p21 (waf1, cip1) following methylmercury exposure in vitro and in vivo,” Toxicology and Applied Pharmacology, vol. 157, no. 3, pp. 203–212, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. E. M. Faustman, R. A. Ponce, Y. C. Ou, M. A. C. Mendoza, T. Lewandowski, and T. Kavanagh, “Investigations of methylmercury-induced alterations in neurogenesis,” Environmental Health Perspectives, vol. 110, no. 5, pp. 859–864, 2002. View at Google Scholar · View at Scopus
  44. M. Kunimoto, “Methylmercury induces apoptosis of rat cerebellar neurons in primary culture,” Biochemical and Biophysical Research Communications, vol. 204, no. 1, pp. 310–317, 1994. View at Publisher · View at Google Scholar · View at Scopus
  45. A. F. Castoldi, S. Barni, I. Turin, C. Gandini, and L. Manzo, “Early acute necrosis, delayed apoptosis and cytoskeletal breakdown in cultured cerebellar granule neurons exposed to methylmercury,” Journal of Neuroscience Research, vol. 59, no. 6, pp. 775–787, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Ceccatelli, E. Daré, and M. Moors, “Methylmercury-induced neurotoxicity and apoptosis,” Chemico-Biological Interactions, vol. 188, no. 2, pp. 301–308, 2010. View at Publisher · View at Google Scholar · View at Scopus