Evidences for a role of glutathione peroxidase 4 (GPx4) in methylmercury induced neurotoxicity in vivo

Toxicology

Volumn 302, Issue 1, 2012, Pages 60-67

  Zemolin, A P P ^a   Meinerz, D F ^b   de Paula, M T ^b   Mariano, D O C ^b   Rocha, J B T ^b   Pereira, A B ^a   Posser, T ^a,b   Franco, J L ^a,b  

^a UNIVERSIDADE FEDERAL DO PAMPA   (Brazil)

^b FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

Author keywords

Enzyme activity; Glutathione peroxidase; Methylmercury; Protein expression; Selenoproteins; Thioredoxin reductase

Indexed keywords

ACTIN; ANTIBODY; CATALASE; DRINKING WATER; GLUTATHIONE PEROXIDASE 1; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN 70; METHYLMERCURY; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; SUPEROXIDE DISMUTASE; THIOREDOXIN REDUCTASE; THIOREDOXIN REDUCTASE 1;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CEREBELLUM; CONTROLLED STUDY; DRUG EXPOSURE; ENZYME ACTIVITY; IN VIVO STUDY; LOCOMOTION; MALE; MOUSE; NEUROTOXICITY; NONHUMAN; OPEN FIELD BEHAVIOR; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; REARING; SPECTROPHOTOMETRY;

ANIMALIA; MUS;

EID: 84984548718     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2012.07.013     Document Type: Article

References (64)

1. Aebi H. Catalase in vitro. Method Enzymol. 1984, 105:121-126.
2. Arner E.S., Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 2000, 267:6102-6109.
3. Arteel G.E., Sies H. The biochemistry of selenium and the glutathione system. Environ. Toxicol. Pharmacol. 2001, 10:153-158.
4. Arthur J.R. The glutathione peroxidases. Cell. Mol. Life Sci. 2000, 57:1825-1835.
5. Aschner M., Syversen T., Souza D.O., Rocha J.B., Farina M. Involvement of glutamate and reactive oxygen species in methylmercury neurotoxicity. Braz. J. Med. Biol. Res. 2007, 40:285-291.
6. Barkay T., Poulain A.J. Mercury (micro)biogeochemistry in polar environments. FEMS Microbiol. Ecol. 2007, 59:232-241.
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
8. Branco V., Canario J., Holmgren A., Carvalho C. Inhibition of the thioredoxin system in the brain and liver of zebra-seabreams exposed to waterborne methylmercury. Toxicol. Appl. Pharmacol. 2011, 251:95-103.
9. Branco V., Canario J., Lu J., Holmgren A., Carvalho C. Mercury and selenium interaction in vivo: effects on thioredoxin reductase and glutathione peroxidase. Free Radical Biol. Med. 2012, 52:781-793.
10. Brigelius-Flohe R. Glutathione peroxidases and redox-regulated transcription factors. Biol. Chem. 2006, 387:1329-1335.
11. Carlberg I., Mannervik B. Glutathione reductase. Method Enzymol. 1985, 113:484-490.
12. Carvalho C.M., Lu J., Zhang X., Arner E.S., Holmgren A. Effects of selenite and chelating agents on mammalian thioredoxin reductase inhibited by mercury: implications for treatment of mercury poisoning. FASEB J. 2011, 25:370-381.
13. Carvalho M.C., Nazari E.M., Farina M., Muller Y.M. Behavioral, morphological, and biochemical changes after in ovo exposure to methylmercury in chicks. Toxicol. Sci. 2008, 106:180-185.
14. Cecatelli S., Daré E., Moors M. Methylmercury-induced neurotoxicity and apoptosis. Chem. Biol. Interact. 2010, 188:301-308.
15. Clarkson T.W., Magos L., Myers G.J. The toxicology of mercury-current exposures and clinical manifestations. N. Engl. J. Med. 2003, 349:1731-1737.
16. Conrad M. Transgenic mouse models for the vital selenoenzymes cytosolic thioredoxin reductase, mitochondrial thioredoxin reductase and glutathione peroxidase 4. Biochim. Biophys. Acta 2009, 1790:1575-1585.
17. Conrad M., Moreno S.G., Sinowatz F., Ursini F., Kolle S., Roveri A., Brielmeier M., Wurst W., Maiorino M., Bornkamm G.W. The nuclear form of phospholipid hydroperoxide glutathione peroxidase is a protein thiol peroxidase contributing to sperm chromatin stability. Mol. Cell. Biol. 2005, 25:7637-7644.
18. Conrad M., Schneider M., Seiler A., Bornkamm G.W. Physiological role of phospholipid hydroperoxide glutathione peroxidase in mammals. Biol. Chem. 2007, 388:1019-1025.
19. Dietrich M.O., Mantese C.E., Anjos G.D., Souza D.O., Farina M. Motor impairment induced by oral exposure to methylmercury in adult mice. Environ. Toxicol. Pharmacol. 2005, 19:169-175.
20. Dringen R. Glutathione metabolism and oxidative stress in neurodegeneration. Eur. J. Biochem. 2000, 267:4903.
21. Farina M., Aschner M., Rocha J.B. Oxidative stress in MeHg-induced neurotoxicity. Toxicol. Appl. Pharmacol. 2011, 256:405-417.
22. Farina M., Campos F., Vendrell I., Berenguer J., Barzi M., Pons S., Sunol C. Probucol increases glutathione peroxidase-1 activity and displays long-lasting protection against methylmercury toxicity in cerebellar granule cells. Toxicol. Sci. 2009, 112:416-426.
23. Farina M., Franco J.L., Ribas C.M., Meotti F.C., Missau F.C., Pizzolatti M.G., Dafre A.L., Santos A.R. Protective effects of Polygala paniculata extract against methylmercury-induced neurotoxicity in mice. J. Pharm. Pharmacol. 2005, 57:1503-1508.
24. Farina M., Rocha J.B., Aschner M. Mechanisms of methylmercury-induced neurotoxicity: evidence from experimental studies. Life Sci. 2011, 89:555-563.
25. Finkel T., Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408:239-247.
26. Franco J., Prediger R.D., Pandolfo P., Takahashi R.N., Farina M., Dafre A.L. Antioxidant responses and lipid peroxidation following intranasal 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) administration in rats: increased susceptibility of olfactory bulb. Life Sci. 2007, 80:1906-1914.
27. Franco J.L., Posser T., Dunkley P.R., Dickson P.W., Mattos J.J., Martins R., Bainy A.C., Marques M.R., Dafre A.L., Farina M. Methylmercury neurotoxicity is associated with inhibition of the antioxidant enzyme glutathione peroxidase. Free Radical Biol. Med. 2009, 47:449-457.
28. Franco J.L., Posser T., Gordon S.L., Bobrovskaya L., Schneider J.J., Farina M., Dafre A.L., Dickson P.W., Dunkley P.R. Expression of tyrosine hydroxylase increases the resistance of human neuroblastoma cells to oxidative insults. Toxicol. Sci. 2010, 113:150-157.
29. Franco J.L., Posser T., Missau F., Pizzolatti M.G., Dos Santos A.R., Souza D.O., Aschner M., Rocha J.B., Dafre A.L., Farina M. Structure-activity relationship of flavonoids derived from medicinal plants in preventing methylmercury-induced mitochondrial dysfunction. Environ. Toxicol. Pharmacol. 2010, 30:272-278.
30. Glaser V., Nazari E.M., Muller Y.M., Feksa L., Wannmacher C.M., Rocha J.B., de Bem A.F., Farina M., Latini A. Effects of inorganic selenium administration in methylmercury-induced neurotoxicity in mouse cerebral cortex. Int. J. Dev. Neurosci. 2010, 28:631-637.
31. Grandjean P., Herz K.T. Methylmercury and brain development: imprecision and underestimation of developmental neurotoxicity in humans. Mt. Sinai J. Med. 2011, 78:107-118.
32. Habig W.H., Jakoby W.B. Assays for differentiation of glutathione S-transferases. Method Enzymol. 1981, 77:398-405.
33. Halliwell B., Gutteridge J. Free Radicals in Biology and Medicine 2007, Oxford University Press.
34. Holmgren A., Bjornstedt M. Thioredoxin and thioredoxin reductase. Method Enzymol. 1995, 252:199-208.
35. Honda S., Hylander L., Sakamoto M. Recent advances in evaluation of health effects on mercury with special reference to methylmercury: a minireview. Environ. Health Prev. Med. 2006, 11:171-176.
36. Hughes J.A., Sparber S.B. Reduction of methylmercury concentration in neonatal rat brains after administration of dimercaptosuccinic acid to dams while pregnant. Res. Commun. Chem. Pathol. Pharmacol. 1978, 22:357-363.
37. Hylander L.D., Goodsite M.E. Environmental costs of mercury pollution. Sci. Total Environ. 2006, 368:352-370.
38. Johansson C., Castoldi A.F., Onishchenko N., Manzo L., Vahter M., Ceccatelli S. Neurobehavioural and molecular changes induced by methylmercury exposure during development. Neurotox. Res. 2007, 11:241-260.
39. Kostyuk V.A., Potapovich A.I. Superoxide-driven oxidation of quercetin and a simple sensitive assay for determination of superoxide dismutase. Biochem. Int. 1989, 19:1117-1124.
40. Lee J.M., Li J., Johnson D.A., Stein T.D., Kraft A.D., Calkins M.J., Jakel R.J., Johnson J.A. Nrf2, a multi-organ protector?. FASEB J. 2005, 19:1061-1066.
41. Leyshon K., Morgan A.J. An integrated study of the morphological and gross-elemental consequences of methyl mercury intoxication in rats, with particular attention on the cerebellum. Scanning Microsc. 1991, 5:895-904.
42. Leyshon-Sorland K., Jasani B., Morgan A.J. The localization of mercury and metallothionein in the cerebellum of rats experimentally exposed to methylmercury. Histochem. J. 1994, 26:161-169.
43. Liang H., Ran Q., Jang Y.C., Holstein D., Lechleiter J., McDonald-Marsh T., Musatov A., Song W., Van Remmen H., Richardson A. Glutathione peroxidase 4 differentially regulates the release of apoptogenic proteins from mitochondria. Free Radical Biol. Med. 2009, 47:312-320.
44. Manto M. Toxic agents causing cerebellar ataxias. Handb. Clin. Neurol. 2012, 103:201-213.
45. Mori N., Yasutake A., Hirayama K. Comparative study of activities in reactive oxygen species production/defense system in mitochondria of rat brain and liver, and their susceptibility to methylmercury toxicity. Arch. Toxicol. 2007, 81:769-776.
46. Mugesh G., Singh H. Synthetic organoselenium compounds as antioxidants: glutathione peroxidase activity. Chem. Soc. Rev. 2000, 29:347-357.
47. Nagashima K. A review of experimental methylmercury toxicity in rats: neuropathology and evidence for apoptosis. Toxicol. Pathol. 1997, 25:624-631.
48. Ni M., Li X., Yin Z., Sidoryk-Wegrzynowicz M., Jiang H., Farina M., Rocha J.B., Syversen T., Aschner M. Comparative study on the response of rat primary astrocytes and microglia to methylmercury toxicity. Glia 2011, 59:810-820.
49. Onyido I., Norris A.R., Buncel E. Biomolecule-mercury interactions: modalities of DNA base-mercury binding mechanisms remediation strategies. Chem. Rev. 2004, 104:5911-5929.
50. Paula M.T., Zemolin A.P., Vargas A.P., Golombieski R.M., Loreto E.L., Saidelles A.P., Picoloto R.S., Flores E.M., Pereira A.B., Rocha J.B., Merritt T.J., Franco J.L., Posser T. Effects of Hg(II) Exposure on MAPK Phosphorylation and Antioxidant System in D. melanogaster. Environ. Toxicol. 2012.
51. Pfeifer H., Conrad M., Roethlein D., Kyriakopoulos A., Brielmeier M., Bornkamm G.W., Behne D. Identification of a specific sperm nuclei selenoenzyme necessary for protamine thiol cross-linking during sperm maturation. Faseb J. 2001, 15:1236-1238.
52. Reeves M.A., Hoffmann P.R. The human selenoproteome: recent insights into functions and regulation. Cell. Mol. Life Sci. 2009, 66:2457-2478.
53. Roveri A., Maiorino M., Nisii C., Ursini F. Purification and characterization of phospholipid hydroperoxide glutathione peroxidase from rat testis mitochondrial membranes. Biochim. Biophys. Acta 1994, 1208:211-221.
54. Rundlof A.K., Arner E.S. Regulation of the mammalian selenoprotein thioredoxin reductase 1 in relation to cellular phenotype, growth, and signaling events. Antioxid. Redox. Signal. 2004, 6:41-52.
55. Schulke S., Dreidax D., Malik A., Burmester T., Nevo E., Band M., Avivi A., Hankeln T. Living with stress: regulation of antioxidant defense genes in the subterranean, hypoxia-tolerant mole rat, Spalax. Gene 2012, 500:199-206.
56. Shanker G., Syversen T., Aschner J.L., Aschner M. Modulatory effect of glutathione status and antioxidants on methylmercury-induced free radical formation in primary cultures of cerebral astrocytes. Brain Res. Mol. Brain Res. 2005, 137:11-22.
57. Sugiura Y., Hojo Y., Tamai Y., Tanaka H. Letter: selenium protection against mercury toxicity. binding of methylmercury by the selenohydryl-containing ligand. J. Am. Chem. Soc. 1976, 98:2339-2341.
58. Sunde R.A. Selenium. Handbook of Nutritionally Essential Mineral Elements 1997, Marcel Dekker, New York, NY, pp. 493-556. B.L. O'Dell, R.A. Sunde (Eds.).
59. Tanito M., Agbaga M.P., Anderson R.E. Upregulation of thioredoxin system via Nrf2-antioxidant responsive element pathway in adaptive-retinal neuroprotection in vivo and in vitro. Free Radic. Biol. Med. 2007, 42:1838-1850.
60. Usuki F., Yamashita A., Fujimura M. Post-transcriptional defects of antioxidant selenoenzymes cause oxidative stress under methylmercury exposure. J. Biol. Chem. 2011, 286:6641-6649.
61. Wagner C., Sudati J.H., Nogueira C.W., Rocha J.B. In vivo and in vitro inhibition of mice thioredoxin reductase by methylmercury. Biometals 2010, 23:1171-1177.
62. Wang X.J., Zhang D.D. Ectodermal-neural cortex 1 down-regulates Nrf2 at the translational level. PLoS One 2009, 4:e5492.
63. Wendel A. Glutathione peroxidase. Method Enzymol. 1981, 77:325-333.
64. Yant L.J., Ran Q., Rao L., Van Remmen H., Shibatani T., Belter J.G., Motta L., Richardson A., Prolla T.A. The selenoprotein GPX4 is essential for mouse development and protects from radiation and oxidative damage insults. Free Radical Biol. Med. 2003, 34:496-502.