Glutathione deficiency in Gclm null mice results in complex I inhibition and dopamine depletion following paraquat administration

Toxicological Sciences

Volumn 134, Issue 2, 2013, Pages 366-373

  Liang, Li Ping ^a   Kavanagh, Terrance J ^b   Patel, Manisha ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Complex I; Dopamine; Glutathione; Paraquat; Parkinson'S disease

Indexed keywords

3 NITROTYROSINE; ACONITATE HYDRATASE; DOPAMINE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; HERBICIDE; PARAQUAT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TYROSINE;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; FEMALE; GLUTATHIONE DEFICIENCY; MALE; MOUSE; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PROTEIN DEFICIENCY;

COMPLEX I.; DOPAMINE; GLUTATHIONE; PARAQUAT; PARKINSON'S DISEASE;

ANIMALS; BASE SEQUENCE; DNA PRIMERS; DOPAMINE; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; HERBICIDES; MICE; MICE, KNOCKOUT; PARAQUAT; SUCCINATE CYTOCHROME C OXIDOREDUCTASE;

EID: 84880679138     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft112     Document Type: Article

References (60)

1. Andersen, J. K., Mo, J. Q., Hom, D. G., Lee, F. Y., Harnish, P., Hamill, R. W., and McNeill, T. H. (1996). Effect of buthionine sulfoximine, a synthesis inhibitor of the antioxidant glutathione, on the murine nigrostriatal neurons. J. Neurochem. 67, 2164-2171.
2. Beal, M. F. (2001). Experimental models of Parkinson's disease. Nat. Rev. Neurosci. 2, 325-334.
3. Beal, M. F., Matson, W. R., Swartz, K. J., Gamache, P. H., and Bird, E. D. (1990). Kynurenine pathway measurements in Huntington's disease striatum: Evidence for reduced formation of kynurenic acid. J. Neurochem. 55, 1327-1339.
4. Betarbet, R., Sherer, T. B., MacKenzie, G., Garcia-Osuna, M., Panov, A. V., and Greenamyre, J. T. (2000). Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3, 1301-1306.
5. Birch-Machin, M. A., and Turnbull, D. M. (2001). Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Methods Cell Biol. 65, 97-117.
6. Brooks, A. I., Chadwick, C. A., Gelbard, H. A., Cory-Slechta, D. A., and Federoff, H. J. (1999). Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss. Brain Res. 823, 1-10.
7. Brown, T. P., Rumsby, P. C., Capleton, A. C., Rushton, L., and Levy, L. S. (2006). Pesticides and Parkinson's disease-is there a link? Environ. Health Perspect. 114, 156-164.
8. Bus, J. S., and Gibson, J. E. (1984). Paraquat: Model for oxidant-initiated toxicity. Environ. Health Perspect. 55, 37-46.
9. Calne, D. B., and Langston, J. W. (1983). Aetiology of Parkinson's disease. Lancet 2, 1457-1459.
10. Castello, P. R., Drechsel, D. A., and Patel, M. (2007). Mitochondria are a major source of paraquat-induced reactive oxygen species production in the brain. J. Biol. Chem. 282, 14186-14193.
11. Chinta, S. J., and Andersen, J. K. (2006). Reversible inhibition of mitochondrial complex I activity following chronic dopaminergic glutathione depletion in vitro: Implications for Parkinson's disease. Free Radic. Biol. Med. 41, 1442-1448.
12. Chinta, S. J., Kumar, M. J., Hsu, M., Rajagopalan, S., Kaur, D., Rane, A., Nicholls, D. G., Choi, J., and Andersen, J. K. (2007). Inducible alterations of glutathione levels in adult dopaminergic midbrain neurons result in nigrostriatal degeneration. J. Neurosci. 27, 13997-14006.
13. Ciliax, B. J., Drash, G. W., Staley, J. K., Haber, S., Mobley, C. J., Miller, G. W., Mufson, E. J., Mash, D. C., and Levey, A. I. (1999). Immunocytochemical localization of the dopamine transporter in human brain. J. Comp. Neurol. 409, 38-56.
14. Cochemé, H. M., and Murphy, M. P. (2008). Complex I is the major site of mitochondrial superoxide production by paraquat. J. Biol. Chem. 283, 1786-1798.
15. Dalton, T. P., Chen, Y., Schneider, S. N., Nebert, D. W., and Shertzer, H. G. (2004). Genetically altered mice to evaluate glutathione homeostasis in health and disease. Free Radic. Biol. Med. 37, 1511-1526.
16. Dauer, W., and Przedborski, S. (2003). Parkinson's disease: Mechanisms and models. Neuron 39, 889-909.
17. Drechsel, D. A., and Patel, M. (2009a). Chapter 21 Paraquat-induced production of reactive oxygen species in brain mitochondria. Methods Enzymol. 456, 381-393.
18. Drechsel, D. A., and Patel, M. (2009b). Differential contribution of the mitochondrial respiratory chain complexes to reactive oxygen species production by redox cycling agents implicated in parkinsonism. Toxicol. Sci. 112, 427-434.
19. Franklin, C. C., Backos, D. S., Mohar, I., White, C. C., Forman, H. J., and Kavanagh, T. J. (2009). Structure, function, and post-translational regulation of the catalytic and modifier subunits of glutamate cysteine ligase. Mol. Aspects Med. 30, 86-98.
20. Fukushima, T., Yamada, K., Isobe, A., Shiwaku, K., and Yamane, Y. (1993). Mechanism of cytotoxicity of paraquat. I. NADH oxidation and paraquat radical formation via complex I. Exp. Toxicol. Pathol. 45, 345-349.
21. Gardner, P. R., and Fridovich, I. (1992). Inactivation-reactivation of aconitase in Escherichia coli. A sensitive measure of superoxide radical. J. Biol. Chem. 267, 8757-8763.
22. Grant, H., Lantos, P. L., and Parkinson, C. (1980). Cerebral damage in paraquat poisoning. Histopathology 4, 185-195.
23. Greenamyre, J. T., Sherer, T. B., Betarbet, R., and Panov, A. V. (2001). Complex I and Parkinson's disease. IUBMB Life 52, 135-141.
24. Griffith, O. W., and Meister, A. (1979). Glutathione: Interorgan translocation, turnover, and metabolism. Proc. Natl. Acad. Sci. U. S. A. 76, 5606-5610.
25. Heales, S. J., Davies, S. E., Bates, T. E., and Clark, J. B. (1995). Depletion of brain glutathione is accompanied by impaired mitochondrial function and decreased N-acetyl aspartate concentration. Neurochem. Res. 20, 31-38.
26. Heales, S. J., Menzes, A., and Davey, G. P. (2011). Depletion of glutathione does not affect electron transport chain complex activity in brain mitochondria: Implications for Parkinson disease and postmortem studies. Free Radic. Biol. Med. 50, 899-902.
27. Hensley, K., Maidt, M. L., Yu, Z., Sang, H., Markesbery, W. R., and Floyd, R. A. (1998). Electrochemical analysis of protein nitrotyrosine and dityrosine in the Alzheimer brain indicates region-specific accumulation. J. Neurosci. 18, 8126-8132.
28. Hertzman, C., Wiens, M., Bowering, D., Snow, B., and Calne, D. (1990). Parkinson's disease: A case-control study of occupational and environmental risk factors. Am. J. Ind. Med. 17, 349-355.
29. Hsu, M., Srinivas, B., Kumar, J., Subramanian, R., and Andersen, J. (2005). Glutathione depletion resulting in selective mitochondrial complex I inhibition in dopaminergic cells is via an NO-mediated pathway not involving peroxynitrite: Implications for Parkinson's disease. J. Neurochem. 92, 1091-1103.
30. Hughes, J. T. (1988). Brain damage due to paraquat poisoning: A fatal case with neuropathological examination of the brain. Neurotoxicology 9, 243-248.
31. Jain, A., Mårtensson, J., Stole, E., Auld, P. A., and Meister, A. (1991). Glutathione deficiency leads to mitochondrial damage in brain. Proc. Natl. Acad. Sci. U. S. A. 88, 1913-1917.
32. Jenner, P., Dexter, D. T., Sian, J., Schapira, A. H., and Marsden, C. D. (1992). Oxidative stress as a cause of nigral cell death in Parkinson's disease and incidental Lewy body disease. The Royal Kings and Queens Parkinson's Disease Research Group. Ann. Neurol. 32(Suppl), S82-S87.
33. Jha, N., Jurma, O., Lalli, G., Liu, Y., Pettus, E. H., Greenamyre, J. T., Liu, R. M., Forman, H. J., and Andersen, J. K. (2000). Glutathione depletion in PC12 results in selective inhibition of mitochondrial complex I activity. Implications for Parkinson's disease. J. Biol. Chem. 275, 26096-26101.
34. Keeney, P. M., Xie, J., Capaldi, R. A., and Bennett, J. P., Jr. (2006). Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. J. Neurosci. 26, 5256-5264.
35. Langston, J. W. (1996). The etiology of Parkinson's disease with emphasis on the MPTP story. Neurology 47, S153-S160.
36. Lenaz, G., Bovina, C., Castelluccio, C., Fato, R., Formiggini, G., Genova, M. L., Marchetti, M., Pich, M. M., Pallotti, F., Parenti Castelli, G., et al. (1997). Mitochondrial complex I defects in aging. Mol. Cell Biochem. 174, 329-333.
37. Liang, L. P., Huang, J., Fulton, R., Day, B. J., and Patel, M. (2007). An orally active catalytic metalloporphyrin protects against 1-methyl-4-phenyl- 1,2,3,6-tetrahydropyridine neurotoxicity in vivo. J. Neurosci. 27, 4326-4333.
38. Liang, L. P., Jarrett, S., and Patel, M. (2009). Paraquat-induced mitochondrial oxidative stress and dopaminergic neuronal loss in vivo. Free Radic. Biol. Med. 47, S113.
39. Liang, L. P., and Patel, M. (2004). Iron-sulfur enzyme mediated mitochondrial superoxide toxicity in experimental Parkinson's disease. J. Neurochem. 90, 1076-1084.
40. Liang, L. P., and Patel, M. (2006). Seizure-induced changes in mitochondrial redox status. Free Radic. Biol. Med. 40, 316-322.
41. Liou, H. H., Tsai, M. C., Chen, C. J., Jeng, J. S., Chang, Y. C., Chen, S. Y., and Chen, R. C. (1997). Environmental risk factors and Parkinson's disease: A case-control study in Taiwan. Neurology 48, 1583-1588.
42. McConnachie, L. A., Mohar, I., Hudson, F. N., Ware, C. B., Ladiges, W. C., Fernandez, C., Chatterton-Kirchmeier, S., White, C. C., Pierce, R. H., and Kavanagh, T. J. (2007). Glutamate cysteine ligase modifier subunit deficiency and gender as determinants of acetaminophen-induced hepatotoxicity in mice. Toxicol. Sci. 99, 628-636.
43. McCormack, A. L., Thiruchelvam, M., Manning-Bog, A. B., Thiffault, C., Langston, J. W., Cory-Slechta, D. A., and Di Monte, D. A. (2002). Environmental risk factors and Parkinson's disease: Selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat. Neurobiol. Dis. 10, 119-127.
44. O'Donovan, D. J., Rogers, L. K., Kelley, D. K., Welty, S. E., Ramsay, P. L., and Smith, C. V. (2002). CoASH and CoASSG levels in lungs of hyperoxic rats as potential biomarkers of intramitochondrial oxidant stresses. Pediatr. Res. 51, 346-353.
45. Paixão, P., Costa, P., Bugalho, T., Fidalgo, C., and Pereira, L. M. (2002). Simple method for determination of paraquat in plasma and serum of human patients by high-performance liquid chromatography. J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci. 775, 109-113.
46. Patel, M., Day, B. J., Crapo, J. D., Fridovich, I., and McNamara, J. O. (1996). Requirement for superoxide in excitotoxic cell death. Neuron 16, 345-355.
47. Pearce, R. K., Owen, A., Daniel, S., Jenner, P., and Marsden, C. D. (1997). Alterations in the distribution of glutathione in the substantia nigra in Parkinson's disease. J. Neural Transm. 104, 661-677.
48. Perry, T. L., Godin, D. V., and Hansen, S. (1982). Parkinson's disease: A disorder due to nigral glutathione deficiency? Neurosci. Lett. 33, 305-310.
49. Perry, T. L., and Yong, V. W. (1986). Idiopathic Parkinson's disease, progressive supranuclear palsy and glutathione metabolism in the substantia nigra of patients. Neurosci. Lett. 67, 269-274.
50. Purisai, M. G., McCormack, A. L., Cumine, S., Li, J., Isla, M. Z., and Di Monte, D. A. (2007). Microglial activation as a priming event leading to paraquatinduced dopaminergic cell degeneration. Neurobiol. Dis. 25, 392-400.
51. Rappold, P. M., Cui, M., Chesser, A. S., Tibbett, J., Grima, J. C., Duan, L., Sen, N., Javitch, J. A., and Tieu, K. (2011). Paraquat neurotoxicity is mediated by the dopamine transporter and organic cation transporter-3. Proc. Natl. Acad. Sci. U. S. A. 108, 20766-20771.
52. Riederer, P., Sofic, E., Rausch, W. D., Schmidt, B., Reynolds, G. P., Jellinger, K., and Youdim, M. B. (1989). Transition metals, ferritin, glutathione, and ascorbic acid in parkinsonian brains. J. Neurochem. 52, 515-520.
53. Schapira, A. H., Cooper, J. M., Dexter, D., Clark, J. B., Jenner, P., and Marsden, C. D. (1990). Mitochondrial complex I deficiency in Parkinson's disease. J. Neurochem. 54, 823-827.
54. Schapira, A. H., Mann, V. M., Cooper, J. M., Krige, D., Jenner, P. J., and Marsden, C. D. (1992). Mitochondrial function in Parkinson's disease. The Royal Kings and Queens Parkinson's Disease Research Group. Ann. Neurol. 32(Suppl), S116-S124.
55. Seaton, T. A., Jenner, P., and Marsden, C. D. (1996). Mitochondrial respiratory enzyme function and superoxide dismutase activity following brain glutathione depletion in the rat. Biochem. Pharmacol. 52, 1657-1663.
56. Sian, J., Dexter, D. T., Lees, A. J., Daniel, S., Agid, Y., Javoy-Agid, F., Jenner, P., and Marsden, C. D. (1994). Alterations in glutathione levels in Parkinson's disease and other neurodegenerative disorders affecting basal ganglia. Ann. Neurol. 36, 348-355.
57. Sofic, E., Lange, K. W., Jellinger, K., and Riederer, P. (1992). Reduced and oxidized glutathione in the substantia nigra of patients with Parkinson's disease. Neurosci. Lett. 142, 128-130.
58. Toffa, S., Kunikowska, G. M., Zeng, B. Y., Jenner, P., and Marsden, C. D. (1997). Glutathione depletion in rat brain does not cause nigrostriatal pathway degeneration. J. Neural Transm. 104, 67-75.
59. Weldy, C. S., Luttrell, I. P., White, C. C., Morgan-Stevenson, V., Bammler, T. K., Beyer, R. P., Afsharinejad, Z., Kim, F., Chitaley, K., and Kavanagh, T. J. (2012). Glutathione (GSH) and the GSH synthesis gene Gclm modulate vascular reactivity in mice. Free Radic. Biol. Med. 53, 1264-1278.
60. Zhang, Y., Marcillat, O., Giulivi, C., Ernster, L., and Davies, K. J. (1990). The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J. Biol. Chem. 265, 16330-16336.