Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2018, Article ID 7878050, 11 pages
https://doi.org/10.1155/2018/7878050
Research Article

Hippocampal Dysfunction Provoked by Mercury Chloride Exposure: Evaluation of Cognitive Impairment, Oxidative Stress, Tissue Injury and Nature of Cell Death

1Laboratory of Functional and Structural Biology, Institute of Biological Sciences, Federal University of Pará, Belém, PA, Brazil
2Laboratory of Pharmacology of Inflammation and Behavior, Institute of Health Sciences, Federal University of Pará, Belém, PA, Brazil
3Laboratory of Ecotoxicology, Institute of Biological Sciences, Federal University of Pará, Belém, PA, Brazil
4Laboratory of Tissue Culture and Cytogenetics, Evandro Chagas Institute, Ananindeua, PA, Brazil
5Laboratory of Molecular Pharmacology, Institute of Biological Sciences, Federal University of Pará, Belém, PA, Brazil

Correspondence should be addressed to Rafael Rodrigues Lima; rb.apfu@amilafar

Received 22 November 2017; Revised 31 January 2018; Accepted 21 February 2018; Published 10 April 2018

Academic Editor: Julia Bornhorst

Copyright © 2018 Walessa Alana Bragança Aragão 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. K. M. Rice, E. M. Walker Jr., M. Wu, C. Gillette, and E. R. Blough, “Environmental mercury and its toxic effects,” Journal of Preventive Medicine and Public Health, vol. 47, no. 2, pp. 74–83, 2014. 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. Holmes, K. A. James, and L. S. Levy, “Is low-level environmental mercury exposure of concern to human health?” Science of The Total Environment, vol. 408, no. 2, pp. 171–182, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Kothari, D. Kruse, R. Karimi et al., “High mercury seafood consumption associated with fatigue at specialty medical clinics on Long Island, NY,” Preventive Medicine Reports, vol. 2, pp. 798–802, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. R. C. Marques, J. V. Bernardi, M. P. Cunha, and J. G. Dorea, “Impact of organic mercury exposure and home delivery on neurodevelopment of Amazonian children,” International Journal of Hygiene and Environmental Health, vol. 219, no. 6, pp. 498–502, 2016. View at Publisher · View at Google Scholar · View at Scopus
  6. J. J. Berzas Nevado, R. C. Rodríguez Martín-Doimeadios, M. Jiménez Moreno, J. L. Martins do Nascimento, A. M. Herculano, and M. E. Crespo-López, “Mercury speciation analysis on cell lines of the human central nervous system to explain genotoxic effects,” Microchemical Journal, vol. 93, no. 1, pp. 12–16, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. M. E. Crespo-López, A. M. Herculano, T. C. Corvelo, and J. L. Do Nascimento, “Mercury and neurotoxicity,” Revue Neurologique, vol. 40, no. 7, pp. 441–447, 2005. View at Google Scholar
  8. J. J. Berzas Nevado, R. C. Rodríguez Martín-Doimeadios, F. J. Guzmán Bernardo et al., “Mercury in the Tapajós River basin, Brazilian Amazon: a review,” Environment International, vol. 36, no. 6, pp. 593–608, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Ruggieri, C. Majorani, F. Domanico, and A. Alimonti, “Mercury in children: current state on exposure through human biomonitoring studies,” International Journal of Environmental Research and Public Health, vol. 14, no. 12, p. 519, 2017. View at Publisher · View at Google Scholar · View at Scopus
  10. G. P. F. Arrifano, R. C. R. Martín-Doimeadios, M. Jiménez-Moreno et al., “Large-scale projects in the amazon and human exposure to mercury: the case-study of the Tucuruí dam,” Ecotoxicology and Environmental Safety, vol. 147, pp. 299–305, 2018. View at Publisher · View at Google Scholar · View at Scopus
  11. R. C. Rodríguez Martín-Doimeadios, J. J. Berzas Nevado, F. J. Guzmán Bernardo et al., “Comparative study of mercury speciation in commercial fishes of the Brazilian Amazon,” Environmental Science and Pollution Research International, vol. 1, pp. 1–6, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. L. K. R. Leão, A. M. Herculano, C. Maximino et al., “Mauritia flexuosa L. protects against deficits in memory acquisition and oxidative stress in rat hippocampus induced by methylmercury exposure,” Nutritional Neuroscience, vol. 20, no. 5, pp. 297–304, 2017. View at Publisher · View at Google Scholar · View at Scopus
  13. A. L. Milioni, B. V. Nagy, A. L. Moura, E. C. Zachi, M. T. Barboni, and D. F. Ventura, “Neurotoxic impact of mercury on the central nervous system evaluated by neuropsychological tests and on the autonomic nervous system evaluated by dynamic pupillometry,” NeuroToxicology, vol. 59, pp. 263–269, 2017. View at Publisher · View at Google Scholar · View at Scopus
  14. M. R. Drew and K. A. Huckleberry, “Modulation of aversive memory by adult hippocampal neurogenesis,” Neurotherapeutics, vol. 14, no. 3, pp. 646–661, 2017. View at Publisher · View at Google Scholar · View at Scopus
  15. F. B. Teixeira, R. M. Fernandes, P. M. Farias-Junior et al., “Evaluation of the effects of chronic intoxication with inorganic mercury on memory and motor control in rats,” International Journal of Environmental Research and Public Health, vol. 11, no. 12, pp. 9171–9185, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. Udo Albus, Guide for the Care and Use of Laboratory Animals, National Research Council of the National Academies, Washington, DC, 2011.
  17. A. C. Oliveira, M. C. Pereira, L. N. Santana et al., “Chronic ethanol exposure during adolescence through early adulthood in female rats induces emotional and memory deficits associated with morphological and molecular alterations in hippocampus,” Journal of Psychopharmacology, vol. 29, no. 6, pp. 712–724, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Suzuki, H. Akagi, K. Akimura et al., Manual of Analyzes of Mercury, Ministry of the Environment, Japan, 2004.
  19. L. L. Amado, M. L. Garcia, P. B. Ramos et al., “A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity,” Science of The Total Environment, vol. 407, no. 6, pp. 2115–2123, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Esterbauer and K. H. Cheeseman, “[42] Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal,” Methods in Enzymology, vol. 186, pp. 407–421, 1990. View at Publisher · View at Google Scholar · View at Scopus
  21. L. C. Green, S. R. Tannenbaum, and P. Goldman, “Nitrate synthesis in the germfree and conventional rat,” Science, vol. 212, no. 4490, pp. 56–58, 1981. View at Publisher · View at Google Scholar
  22. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976. View at Publisher · View at Google Scholar · View at Scopus
  23. A. F. Silva, M. S. Aguiar, O. S. Carvalho et al., “Hippocampal neuronal loss, decreased GFAP immunoreactivity and cognitive impairment following experimental intoxication of rats with aluminum citrate,” Brain Research, vol. 1491, pp. 23–33, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. G. B. Oliveira, A. Fontes Ede Jr, S. de Carvalho et al., “Minocycline mitigates motor impairments and cortical neuronal loss induced by focal ischemia in rats chronically exposed to ethanol during adolescence,” Brain Research, vol. 1561, pp. 23–34, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. R. R. Lima, J. Guimaraes-Silva, J. L. Oliveira et al., “Diffuse axonal damage, myelin impairment, astrocytosis and inflammatory response following microinjections of NMDA into the rat striatum,” Inflammation, vol. 31, no. 1, pp. 24–35, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. R. R. Lima, L. N. Santana, R. M. Fernandes et al., “Neurodegeneration and glial response after acute striatal stroke: histological basis for neuroprotective studies,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 3173564, 15 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  27. L. O. Bittencourt, B. Puty, S. Charone et al., “Oxidative biochemistry disbalance and changes on proteomic profile in salivary glands of rats induced by chronic exposure to methylmercury,” Oxidative Medicine and Cellular Longevity, vol. 2017, Article ID 5653291, 15 pages, 2017. View at Publisher · View at Google Scholar · View at Scopus
  28. C. C. Bridges and R. K. Zalups, “Mechanisms involved in the transport of mercuric ions in target tissues,” Archives of Toxicology, vol. 91, no. 1, pp. 63–81, 2017. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Szász, B. Barna, Z. Gajda, G. Galbács, M. Kirsch-Volders, and M. Szente, “Effects of continuous low-dose exposure to organic and inorganic mercury during development on epileptogenicity in rats,” Neurotoxicology, vol. 23, no. 2, pp. 197–206, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. E. Atucha and B. Roozendaal, “The inhibitory avoidance discrimination task to investigate accuracy of memory,” Frontiers in Behavioral Neuroscience, vol. 9, p. 60, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. P. B. Mello-Carpes, W. Barros, S. Borges et al., “Chronic exposure to low mercury chloride concentration induces object recognition and aversive memories deficits in rats,” International Journal of Developmental Neuroscience, vol. 31, no. 7, pp. 468–472, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Karl, R. Pabst, and S. von Horsten, “Behavioral phenotyping of mice in pharmacological and toxicological research,” Experimental and Toxicologic Pathology, vol. 55, no. 1, pp. 69–83, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. I. Izquierdo, C. R. Furini, and J. C. Myskiw, “Fear memory,” Physiological Reviews, vol. 96, no. 2, pp. 695–750, 2016. View at Publisher · View at Google Scholar · View at Scopus
  34. M. S. Fanselow and H. W. Dong, “Are the dorsal and ventral hippocampus functionally distinct structures?” Neuron, vol. 65, no. 1, pp. 7–19, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. M. C. Chan, E. Bautista, I. Alvarado-Cruz, B. Quintanilla-Vega, and J. Segovia, “Inorganic mercury prevents the differentiation of SH-SY5Y cells: amyloid precursor protein, microtubule associated proteins and ROS as potential targets,” Journal of Trace Elements in Medicine and Biology, vol. 41, pp. 119–128, 2017. View at Publisher · View at Google Scholar · View at Scopus
  36. M. E. Crespo-Lopez, A. Costa-Malaquias, E. H. Oliveira et al., “Is low non-lethal concentration of methylmercury really safe? A report on genotoxicity with delayed cell proliferation,” PLoS One, vol. 11, no. 9, article e0162822, 2016. View at Publisher · View at Google Scholar · View at Scopus
  37. M. E. Crespo-Lopez, A. Lima de Sa, A. M. Herculano, R. Rodriguez Burbano, and J. L. Martins do Nascimento, “Methylmercury genotoxicity: a novel effect in human cell lines of the central nervous system,” Environment International, vol. 33, no. 2, pp. 141–146, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. T. L. Limke, J. J. Bearss, and W. D. Atchison, “Acute exposure to methylmercury causes Ca2+ dysregulation and neuronal death in rat cerebellar granule cells through an M3 muscarinic receptor-linked pathway,” Toxicological Sciences, vol. 80, no. 1, pp. 60–68, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. N. Ercal, H. Gurer-Orhan, and N. Aykin-Burns, “Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage,” Current Topics in Medicinal Chemistry, vol. 1, no. 6, pp. 529–539, 2001. View at Publisher · View at Google Scholar
  40. A. E. Abdel Moneim, “The neuroprotective effect of berberine in mercury-induced neurotoxicity in rats,” Metabolic Brain Disease, vol. 30, no. 4, pp. 935–942, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Ceccatelli, E. Dare, 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
  42. E. Fonfria, M. T. Vilaro, Z. Babot, E. Rodriguez-Farre, and C. Sunol, “Mercury compounds disrupt neuronal glutamate transport in cultured mouse cerebellar granule cells,” Journal of Neuroscience Research, vol. 79, no. 4, pp. 545–553, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. L. L. Gutierrez, N. G. Mazzotti, A. S. Araujo et al., “Peripheral markers of oxidative stress in chronic mercuric chloride intoxication,” Brazilian Journal of Medical and Biological Research, vol. 39, no. 6, pp. 767–772, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Sumathi, C. Shobana, J. Christinal, and C. Anusha, “Protective effect of Bacopa monniera on methyl mercury-induced oxidative stress in cerebellum of rats,” Cellular and Molecular Neurobiology, vol. 32, no. 6, pp. 979–987, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. D. A. Rizzetti, F. Fernandez, S. Moreno et al., “Egg white hydrolysate promotes neuroprotection for neuropathic disorders induced by chronic exposure to low concentrations of mercury,” Brain Research, vol. 1646, pp. 482–489, 2016. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Lohren, L. Blagojevic, R. Fitkau et al., “Toxicity of organic and inorganic mercury species in differentiated human neurons and human astrocytes,” Journal of Trace Elements in Medicine and Biology, vol. 32, pp. 200–208, 2015. View at Publisher · View at Google Scholar · View at Scopus
  47. S. H. Kim and R. P. Sharma, “Mercury-induced apoptosis and necrosis in murine macrophages: role of calcium-induced reactive oxygen species and p38 mitogen-activated protein kinase signaling,” Toxicology and Applied Pharmacology, vol. 196, no. 1, pp. 47–57, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Nakaizumi, T. Horie, T. Kida et al., “Nitric oxide potentiates TNF-α-induced neurotoxicity through suppression of NF-κB,” Cellular and Molecular Neurobiology, vol. 32, no. 1, pp. 95–106, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. O. Sveinsson, L. Herrman, and M. A. Hietala, “Heroin-induced acute myelopathy with extreme high levels of CSF glial fibrillar acidic protein indicating a toxic effect on astrocytes,” BMJ Case Reports, vol. 2017, 2017. View at Publisher · View at Google Scholar · View at Scopus
  50. R. M. Ransohoff and M. A. Brown, “Innate immunity in the central nervous system,” The Journal of Clinical Investigation, vol. 122, no. 4, pp. 1164–1171, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. J. S. Charleston, R. L. Body, R. P. Bolender, N. K. Mottet, M. E. Vahter, and T. M. Burbacher, “Changes in the number of astrocytes and microglia in the thalamus of the monkey Macaca fascicularis following long-term subclinical methylmercury exposure,” Neurotoxicology, vol. 17, no. 1, pp. 127–138, 1996. View at Google Scholar
  52. R. H. Garman, B. Weiss, and H. L. Evans, “Alkylmercurial encephalopathy in the monkey (Saimiri sciureus and Macaca arctoides): a histopathologic and autoradiographic study,” Acta Neuropathologica, vol. 32, no. 1, pp. 61–74, 1975. View at Publisher · View at Google Scholar · View at Scopus
  53. J. W. Allen, G. Shanker, K. H. Tan, and M. Aschner, “The consequences of methylmercury exposure on interactive functions between astrocytes and neurons,” Neurotoxicology, vol. 23, no. 6, pp. 755–759, 2002. View at Publisher · View at Google Scholar · View at Scopus
  54. F. T. Crews, M. A. Collins, C. Dlugos et al., “Alcohol-induced neurodegeneration: when, where and why?” Alcoholism, Clinical and Experimental Research, vol. 28, no. 2, pp. 350–364, 2004. View at Publisher · View at Google Scholar · View at Scopus