SKN-1/Nrf2 inhibits dopamine neuron degeneration in a Caenorhabditis elegans model of methylmercury toxicity

Toxicological Sciences

Volumn 118, Issue 2, 2010, Pages 613-624

  VanDuyn, Natalia ^a   Settivari, Raja ^a   Wong, Garry ^b   Nass, Richard ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

C. elegans; Dopamine neurodegeneration; Genetics; Methylmercury; Nematode; Nrf2; Oxidative stress; Parkinson's disease; SKN 1

Indexed keywords

GLUTATHIONE TRANSFERASE; GLUTATHIONE TRANSFERASE 38; GLUTATHIONE TRANSFERASE 4; METHYLMERCURY; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL SIZE; CELL VIABILITY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYO DEVELOPMENT; NERVE CELL DEGENERATION; NONHUMAN; PROTEIN EXPRESSION;

ANIMAL TESTING ALTERNATIVES; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DOPAMINE; EMBRYO, NONMAMMALIAN; LARVA; LONGEVITY; MERCURY POISONING, NERVOUS SYSTEM; METHYLMERCURY COMPOUNDS; NERVE DEGENERATION; NEURONS; NF-E2-RELATED FACTOR 2; REPRODUCTION; TRANSCRIPTION FACTORS; WATER POLLUTANTS, CHEMICAL;

ANIMALIA; CAENORHABDITIS ELEGANS; MAMMALIA; VERTEBRATA;

EID: 78549234350     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq285     Document Type: Article

References (72)

1. An, J.H., and Blackwell, T.K. (2003). SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 17, 1882-1893.
2. Aschner, M., and Aschner, J.L. (1990). Mercury neurotoxicity: mechanisms of blood-brain barrier transport. Neurosci. Biobehav. Rev. 14, 169-176.
3. Audhya, A., Hyndman, F., McLeod, I.X., Maddox, A.S., Yates, J.R., III., Desai, A., and Oegema, K. (2005). A complex containing the Sm protein CAR-1 and the RNA helicase CGH-1 is required for embryonic cytokinesis in Caenorhabditis elegans. J. Cell. Biol. 171, 267-279.
4. Bakir, F., Damluji, S.F., Amin-Zaki, L., Murtadha, M., Khalidi, A., al-Rawi, N.Y., Tikriti, S., Dahahir, H.I., Clarkson, T.W., Smith, J.C., et al. (1973). Methylmercury poisoning in Iraq. Science 181, 230-241.
5. Beyrouty, P., Stamler, C.J., Liu, J.N., Loua, K.M., Kubow, S., and Chan, H.M. (2006). Effects of prenatal methylmercury exposure on brain monoamine oxidase activity and neurobehaviour of rats. Neurotoxicol. Teratol. 28, 251-259.
6. Bianchi, L., and Driscoll, M. (2006). Culture of embryonic C. elegans cells for electrophysiological and pharmacological analyses (September 30, 2006). WormBook. (The C. elegans Research Community, WormBook Ed.). doi/10.1895/wormbook.1.122.1. Available at: http://www.wormbook.org.
7. Bishop, N.A., and Guarente, L. (2007). Genetic links between diet and lifespan: shared mechanisms from yeast to humans. Nat. Rev. Genet. 8, 835-844.
8. Blau, N., Bonafe, L., and Thony, B. (2001). Tetrahydrobiopterin deficiencies without hyperphenylalaninemia: diagnosis and genetics of dopa-responsive dystonia and sepiapterin reductase deficiency. Mol. Genet. Metab. 74, 172-185.
9. Boulin, T., Etchberger, J., and Hobert, O. (2006). Reporter gene fusions (April 5, 2006). WormBook. (The C. elegans Research Community, WormBook Ed.). doi/10.1895/wormbook.1.122.1. Available at: http://www.wormbook.org.
10. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
11. Bridges, C.C., and Zalups, R.K. (2005). Molecular and ionic mimicry and the transport of toxic metals. Toxicol. Appl. Pharmacol. 204, 274-308.
12. Budtz-Jorgensen, E., Grandjean, P., and Weihe, P. (2007). Separation of risks and benefits of seafood intake. Environ. Health Perspect. 115, 323-327.
13. Carvalho, M.C., Nazari, E.M., Farina, M., and Muller, Y.M. (2008). Behavioral, morphological, and biochemical changes after in ovo exposure to methylmercury in chicks. Toxicol. Sci. 106, 180-185.
14. Carvelli, L., McDonald, P.W., Blakely, R.D., and Defelice, L.J. (2004). Dopamine transporters depolarize neurons by a channel mechanism. Proc. Natl. Acad. Sci. U.S.A. 101, 16046-16051.
15. Clarkson, T.W., and Magos, L. (2006). The toxicology of mercury and its chemical compounds. Crit. Rev. Toxicol. 36, 609-662.
16. Curle, D.C., Ray, M., and Persaud, T.V. (1987). In vivo evaluation of teratogenesis and cytogenetic changes following methylmercuric chloride treatment. Anat. Rec. 219, 286-295.
17. Di Simplicio, P., Gorelli, M., Vignani, R., and Leonzio, C. (1993). The differential modulation of the enzymes of glutathione metabolism. Indication of overlapping effects of toxicity and repair in mouse liver and kidney after dietary treatment with methylmercury and sodium selenite. Biol. Trace Elem. Res. 36, 167-181.
18. Dreiem, A., Shan, M., Okoniewski, R.J., Sanchez-Morrissey, S., and Seegal, R.F. (2009). Methylmercury inhibits dopaminergic function in rat pup synaptosomes in an age-dependent manner. Neurotoxicol. Teratol. 31, 312-317.
19. Friberg, L., and Mottet, N.K. (1989). Accumulation of methylmercury and inorganic mercury in the brain. Biol. Trace Elem. Res. 21, 201-206.
20. Glover, C.N., Zheng, D., Jayashankar, S., Sales, G.D., Hogstrand, C., and Lundebye, A.K. (2009). Methylmercury speciation influences brain gene expression and behavior in gestationally-exposed mice pups. Toxicol. Sci. 110, 389-400.
21. Goering, P.L., Fisher, B.R., Noren, B.T., Papaconstantinou, A., Rojko, J.L., and Marler, R.J. (2000). Mercury induces regional and cell-specific stress protein expression in rat kidney. Toxicol. Sci. 53, 447-457.
22. Grandjean, P., Weihe, P., White, R.F., Debes, F., Araki, S., Yokoyama, K., Murata, K., Sorensen, N., Dahl, R., and Jorgensen, P.J. (1997). Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicol. Teratol. 19, 417-428.
23. Hasegawa, K., Miwa, S., Isomura, K., Tsutsumiuchi, K., Taniguchi, H., and Miwa, J. (2008). Acrylamide-responsive genes in the nematode Caenorhabditis elegans. Toxicol. Sci. 101, 215-225.
24. Helmcke, K.J., Syversen, T., Miller, D.M., III., and Aschner, M. (2009). Characterization of the effects of methylmercury on Caenorhabditis elegans. Toxicol. Appl. Pharmacol. 240, 265-272.
25. Hope, I., Ed. (1999). C. elegans: A Practical Approach. New York, Oxford University Press.
26. Hughes, J.A., and Annau, Z. (1976). Postnatal behavioral effects in mice after prenatal exposure to methylmercury. Pharmacol. Biochem. Behav. 4, 385-391.
27. InSug, O., Datar, S., Koch, C.J., Shapiro, I.M., and Shenker, B.J. (1997). Mercuric compounds inhibit human monocyte function by inducing apoptosis: evidence for formation of reactive oxygen species, development of mitochondrial membrane permeability transition and loss of reductive reserve. Toxicology 124, 211-224.
28. Jakel, R.J., Townsend, J.A., Kraft, A.D., and Johnson, J.A. (2007). Nrf2-mediated protection against 6-hydroxydopamine. Brain Res. 1144, 192-201.
29. Kamath, R.S., and Ahringer, J. (2003). Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321.
30. Kampkotter, A., Pielarski, T., Rohrig, R., Timpel, C., Chovolou, Y., Watjen, W., and Kahl, R. (2007). The Ginkgo biloba extract EGb761 reduces stress sensitivity, ROS accumulation and expression of catalase and glutathione S-transferase 4 in Caenorhabditis elegans. Pharmacol. Res. 55, 139-147.
31. Kensler, T.W., Wakabayashi, N., and Biswal, S. (2007). Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47, 89-116.
32. Kunimoto, M., and Suzuki, T. (1997). Migration of granule neurons in cerebellar organotypic cultures is impaired by methylmercury. Neurosci. Lett. 226, 183-186.
33. Lakowicz, J.R., and Anderson, C.J. (1980). Permeability of lipid bilayers to methylmercuric chloride: quantification by fluorescence quenching of a carbazole-labeled phospholipid. Chem. Biol. Interact. 30, 309-323.
34. Lee, J.M., Shih, A.Y., Murphy, T.H., and Johnson, J.A. (2003). NF-E2-related factor-2 mediates neuroprotection against mitochondrial complex I inhibitors and increased concentrations of intracellular calcium in primary cortical neurons. J. Biol. Chem. 278, 37948-37956.
35. Liao, V.H., and Freedman, J.H. (1998). Cadmium-regulated genes from the nematode Caenorhabditis elegans. Identification and cloning of new cadmium-responsive genes by differential display. J. Biol. Chem. 273, 31962-31970.
36. Limke, T.L., Heidemann, S.R., and Atchison, W.D. (2004). Disruption of intraneuronal divalent cation regulation by methylmercury: are specific targets involved in altered neuronal development and cytotoxicity in methylmercury poisoning? Neurotoxicology 25, 741-760.
37. Lovenberg, W., Levine, R.A., Robinson, D.S., Ebert, M., Williams, A.C., and Calne, D.B. (1979). Hydroxylase cofactor activity in cerebrospinal fluid of normal subjects and patients with Parkinson's disease. Science 204, 624-626.
38. Murata, K., Weihe, P., Budtz-Jorgensen, E., Jorgensen, P.J., and Grandjean, P. (2004). Delayed brainstem auditory evoked potential latencies in 14-year-old children exposed to methylmercury. J. Pediatr. 144, 177-183.
39. Myers, G.J., and Davidson, P.W. (1998). Prenatal methylmercury exposure and children: neurologic, developmental, and behavioral research. Environ. Health Perspec.t 106(Suppl. 3), 841-847.
40. Nakada, S., and Imura, N. (1982). Uptake of methylmercury and inorganic mercury by mouse glioma and mouse neuroblastoma cells. Neurotoxicology 3, 249-258.
41. Nass, R., Hall, D.H., Miller, D.M., III., and Blakely, R.D. (2002). Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 99, 3264-3269.
42. Nass, R., and Hamza, I. (2007). The nematode Caenorhabditis elegans as a model to explore toxicology in vivo: solid and axenic growth culture conditions and compound exposure parameters. Curr. Protoc. Toxicol. 1.9.1-1.9.18.
43. Nass, R., Merchant, K.M., and Ryan, T. (2008). Caenohabditis elegans in Parkinson's disease drug discovery: addressing an unmet medical need. Mol. Interv. 8, 284-293.
44. Nass, R. and Przedborski, S., Eds. (2008). Parkinson's Disease: Molecular and Therapeutic Insights from Model Systems, 1st ed. Elsevier Academic Press.
45. Newland, M.C., Paletz, E.M., and Reed, M.N. (2008). Methylmercury and nutrition: adult effects of fetal exposure in experimental models. Neurotoxicology 29, 783-801.
46. Novillo, A., Won, S.-J., Li, C., and Callard, I.P. (2005). Changes in nuclear receptor and vitellogenin gene expression in response to steroids and heavy metal in Caenorhabditis elegans. Int. Comp. Biol. 45, 61-71.
47. Nygaard, T.G., Takahashi, H., Heiman, G.A., Snow, B.J., Fahn, S., and Calne, D.B. (1992). Long-term treatment response and fluorodopa positron emission tomographic scanning of parkinsonism in a family with doparesponsive dystonia. Annu. Neurol. 32, 603-608.
48. Oliveira, R.P., Porter Abate, J., Dilks, K., Landis, J., Ashraf, J., Murphy, C.T., and Blackwell, T.K. (2009). Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell 8, 524-541.
49. Park, S.K., Tedesco, P.M., and Johnson, T.E. (2009). Oxidative stress and longevity in Caenorhabditis elegans as mediated by SKN-1. Aging Cell 8, 258-269.
50. Parran, D.K., Mundy, W.R., and Barone, S., Jr. (2001). Effects of methylmercury and mercuric chloride on differentiation and cell viability in PC12 cells. Toxicol. Sci. 59, 278-290.
51. Petersen, M.S., Halling, J., Bech, S., Wermuth, L., Weihe, P., Nielsen, F., Jorgensen, P.J., Budtz-Jorgensen, E., and Grandjean, P. (2008). Impact of dietary exposure to food contaminants on the risk of Parkinson's disease. Neurotoxicology 29, 584-590.
52. Rand, J.B., and Johnson, C.D. (1995). Genetic pharmacology: interactions between drugs and gene products in Caenorhabditis elegans. Methods Cell. Biol. 48, 187-204.
53. Rand, M.D., Dao, J.C., and Clason, T.A. (2009). Methylmercury disruption of embryonic neural development in Drosophila. Neurotoxicology 30, 794-802.
54. Rodier, P.M. (1995). Developing brain as a target of toxicity. Environ. Health Perspect. 103(Suppl. 6), 73-76.
55. Samali, A., and Orrenius, S. (1998). Heat shock proteins: regulators of stress response and apoptosis. Cell Stress Chaperones 3, 228-236.
56. Scherzer, C.R., Jensen, R.V., Gullans, S.R., and Feany, M.B. (2003). Gene expression changes presage neurodegeneration in a Drosophila model of Parkinson's disease. Hum. Mol. Genet. 12, 2457-2466.
57. Schulz, T.J., Zarse, K., Voigt, A., Urban, N., Birringer, M., and Ristow, M. (2007). Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 6, 280-293.
58. Settivari, R., Levora, J., and Nass, R. (2009). The divalent metal transporter homologues SMF-1/2 mediate dopamine neuron sensitivity in Caenorhabditis elegans models of manganism and parkinson disease. J. Biol. Chem. 284, 35758-35768.
59. Siebert, A., Desai, V., Chandrasekaran, K., Fiskum, G., and Jafri, M.S. (2009). Nrf2 activators provide neuroprotection against 6-hydroxydopamine toxicity in rat organotypic nigrostriatal cocultures. J. Neurosci. Res. 87, 1659-1669.
60. Simmer, F., Moorman, C., van der Linden, A.M., Kuijk, E., van den Berghe, P.V., Kamath, R.S., Fraser, A.G., Ahringer, J., and Plasterk, R.H. (2003). Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol. 1, E12.
61. Sykiotis, G.P., and Bohmann, D. (2010). Stress-activated cap′n′collar transcription factors in aging and human disease. Sci. Signal 3, re3.
62. Takeuchi, T. (1982). Pathology of Minamata disease. With special reference to its pathogenesis. Acta Pathol. Jpn 32(Suppl. 1), 73-99.
63. Taylor, R.C., Acquaah-Mensah, G., Singhal, M., Malhotra, D., and Biswal, S. (2008). Network inference algorithms elucidate Nrf2 regulation of mouse lung oxidative stress. PLoS Comput. Biol. 4, e1000166.
64. Thompson, S.A., White, C.C., Krejsa, C.M., Eaton, D.L., and Kavanagh, T.J. (2000). Modulation of glutathione and glutamate-L-cysteine ligase by methylmercury during mouse development. Toxicol. Sci. 57, 141-146.
65. Timmons, L., and Fire, A. (1998). Specific interference by ingested dsRNA. Nature 395, 854.
66. Toyama, T., Sumi, D., Shinkai, Y., Yasutake, A., Taguchi, K., Tong, K.I., Yamamoto, M., and Kumagai, Y. (2007). Cytoprotective role of Nrf2/Keap1 system in methylmercury toxicity. Biochem. Biophys. Res. Commun. 363, 645-650.
67. Tullet, J.M., Hertweck, M., An, J.H., Baker, J., Hwang, J.Y., Liu, S., Oliveira, R.P., Baumeister, R., and Blackwell, T.K. (2008). Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132, 1025-1038.
68. von Otter, M., Landgren, S., Nilsson, S., Celojevic, D., Bergstrom, P., Hakansson, A., Nissbrandt, H., Drozdzik, M., Bialecka, M., Kurzawski, M., et al. (2010). Association of Nrf2-encoding NFE2L2 haplotypes with Parkinson's disease. BMC Med. Genet. 11, 36.
69. Wang, L., Jiang, H., Yin, Z., Aschner, M., and Cai, J. (2009). Methylmercury toxicity and Nrf2-dependent detoxification in astrocytes. Toxicol. Sci. 107, 135-143.
70. Weis, J.S. (2009). Reproductive, developmental, and neurobehavioral effects of methylmercury in fishes. J. Environ. Sci. Health C Environ. Carcinog. Ecotoxicol. Rev. 27, 212-225.
71. Wilce, M.C.J., and Parker, M.W. (1994). Structure and function of glutathione S-transferases. Biochim. Biophys. Acta 1205, 1-18.
72. Yu, X., Robinson, J.F., Sidhu, J.S., Hong, S., and Faustman, E.M. (2010). A system-based comparison of gene expression reveals alterations in oxidative stress, disruption of ubiquitin-proteasome system and altered cell cycle regulation after exposure to cadmium and methylmercury in mouse embryonic fibroblast. Toxicol. Sci. 114, 356-377.