DJ-1 changes in G93A-SOD1 transgenic mice: Implications for oxidative stress in ALS

Journal of Molecular Neuroscience

Volumn 38, Issue 2, 2009, Pages 94-102

  Lev, Nirit ^a   Ickowicz, Debby ^a   Barhum, Yael ^a   Melamed, Eldad ^a   Offen, Daniel ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Amyotrophic lateral sclerosis (ALS); Cu Zn superoxide dismutase (SOD1); DJ 1; Oxidative stress

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; DJ 1 PROTEIN; DJ 1 PROTEIN, MOUSE; DJ-1 PROTEIN, MOUSE; ISOPROTEIN; ONCOPROTEIN; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; SPINAL CORD; TRANSGENIC MOUSE; UPREGULATION; WILD TYPE; ANIMAL; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; PATHOPHYSIOLOGY; POINT MUTATION; ROTAROD TEST;

ANIMALIA; MUS; MUS MUSCULUS;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; HUMANS; MICE; MICE, TRANSGENIC; ONCOGENE PROTEINS; OXIDATIVE STRESS; POINT MUTATION; PROTEIN ISOFORMS; ROTAROD PERFORMANCE TEST; SPINAL CORD; SUPEROXIDE DISMUTASE;

EID: 69249214308     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12031-008-9138-7     Document Type: Article

References (53)

1. Abe, K., Pan, L. H., Watanabe, M., Kato, T., & Itoyama, Y. (1995). Induction of nitrotyrosine-like immunoreactivity in the lower motor neuron of amyotrophic lateral sclerosis. Neuroscience Letters, 199, 152-154. doi:10.1016/0304-3940(95)12039-7.
2. Abe, K., Pan, L. H., Watanabe, M., Konno, H., Kato, T., & Itoyama, Y. (1997). Upregulation of protein-tyrosine nitration in the anterior horn cells of amyotrophic lateral sclerosis. Neurological Research, 19, 124-128.
3. Agar, J., & Durham, H. (2003). Relevance of oxidative injury in the pathogenesis of motor neuron diseases. Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders, 4, 232-242. doi:10.1080/14660820310011278. (Pubitemid 37428478)
4. Aguirre, N., Beal, M. F., Matson, W. R., & Bogdanov, M. B. (2005). Increased oxidative damage to DNA in an animal model of amyotrophic lateral sclerosis. Free Radical Research, 39, 383-388. doi:10.1080/10715760400027979. (Pubitemid 40613717)
5. Andrus, P. K., Fleck, T. J., Gurney, M. E., & Hall, E. D. (1998). Protein oxidative damage in a transgenic mouse model of familial amyotrophic lateral sclerosis. Journal of Neurochemistry, 71, 2041-2048.
6. Annesi, G., Savettieri, G., Pugliese, P., et al. (2005). DJ-1 mutations and parkinsonism-dementia-amyotrophic lateral sclerosis complex. Annals of Neurology, 58, 803-807. doi:10.1002/ana.20666. (Pubitemid 41552561)
7. Aoyama, K., Matsubara, K., Fujikawa, Y., et al. (2000). Nitration of manganese superoxide dismutase in cerebrospinal fluids is a marker for peroxynitritemediated oxidative stress in neurodegenerative diseases. Annals of Neurology, 47, 524-527. doi:10.1002/1531-8249(200004)474<524::AID-ANA19>3.0.CO;2-5.
8. Bader, V., Ran Zhu, X., Lubbert, H., & Stichel, C. C. (2005). Expression of DJ-1 in the adult mouse CNS. Brain Research, 1041, 102-111. doi:10.1016/j.brainres.2005.02.006. (Pubitemid 40445394)
9. Bandopadhyay, R., Kingsbury, A. E., Cookson, M. R., et al. (2004). The expression of DJ-1 (PARK7) in normal human CNS and idiopathic Parkinson's disease. Brain, 127, 420-430. doi:10.1093/brain/awh054. (Pubitemid 38160326)
10. Barber, S. C., Mead, R. J., & Shaw, P. J. (2006). Oxidative stress in ALS: a mechanism of neurodegeneration and a therapeutic target. Biochimica et Biophysica Acta, 1762, 1051-1067.
11. Beal, M. F., Ferrante, R. J., Browne, S. E., Mathews, R. T., Kowall, N. W., & Brown Jr., R. H. (1997). Increased 3-nitrotyrosine in both sporadic and familial amyotrophic lateral sclerosis. Annals of Neurology, 42, 644-654. doi:10.1002/ana.410420416. (Pubitemid 27439028)
12. Bogdanov, M., Brown, R. H., Matson, W., et al. (2000). Increased oxidative damage to DNA in ALS patients. Free Radical Biology & Medicine, 29, 652-658. doi:10.1016/S0891-5849(00)00349-X. (Pubitemid 30741807)
13. Bonifati, V., Rizzu, P., van Baren, M. J., et al. (2003). Mutations in the DJ1 gene associated with autosomal recessive early-onset parkinsonism. Science, 299, 256-259. doi:10.1126/science.1077209. (Pubitemid 36131051)
14. Canet-Aviles, R. M., Wilson, M. A., Miller, D. W., et al. (2004). The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proceedings of the National Academy of Sciences of the United States of America, 101, 9103-9108. doi:10.1073/pnas.0402959101. (Pubitemid 38781618)
15. Carri, M. T., Ferri, A., Cozzolino, M., Calabrese, L., & Rotilio, G. (2003). Neurodegeneration in amyotrophic lateral sclerosis: the role of oxidative stress and altered homeostasis of metals. Brain Research Bulletin, 61, 365-374. doi:10.1016/S0361-9230(03)00179-5. (Pubitemid 36945467)
16. Casoni, F., Basso, M., Massignan, T., et al. (2005). Protein nitration in a mouse model of familial amyotrophic lateral sclerosis: possible multifunctional role in the pathogenesis. The Journal of Biological Chemistry, 280, 16295-16304. doi:10.1074/jbc.M413111200. (Pubitemid 40616757)
17. Cha, C. I., Chung, Y. H., Shin, C. M., et al. (2000). Immunochemical study on the distribution of nitrotyrosine in the brain of the transgenic mice expressing a human Cu/Zn SOD mutation. Brain Research, 853, 156-161. doi:10.1016/S0006-8993(99)02302-1. (Pubitemid 30016011)
18. Choi, J., Sullards, M. C., Olzmann, J. A., et al. (2006). Oxidative damage of DJ-1 is linked to sporadic Parkinson and Alzheimer diseases. The Journal of Biological Chemistry, 281, 10816-10824. doi:10.1074/jbc.M509079200. (Pubitemid 43855504)
19. Clements, C. M., McNally, R. S., Conti, B. J., Mak, T. W., & Ting, J. P. (2006). DJ-1, a cancer- and Parkinson's disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2. Proceedings of the National Academy of Sciences of the United States of America, 103, 15091-15096. doi:10.1073/pnas.0607260103. (Pubitemid 44583169)
20. Ferrante, R. J., Browne, S. E., Shinobu, L. A., et al. (1997a). Evidence of increased oxidative damage in both sporadic and familial amyotrophic lateral sclerosis. Journal of Neurochemistry, 69, 2064-2074.
21. Ferrante, R. J., Shinobu, L. A., Schulz, J. B., et al. (1997b). Increased 3-nitrotyrosine and oxidative damage in mice with a human copper/zinc superoxide dismutase mutation. Annals of Neurology, 42, 326-334. doi:10.1002/ana.410420309. (Pubitemid 27391116)
22. Fitzmaurice, P. S., Shaw, I. C., Kleiner, H. E., et al. (1996). Evidence for DNA damage in amyotrophic lateral sclerosis. Muscle & Nerve, 19, 797-798.
23. Gurney, M. E., Pu, H., Chiu, A. Y., et al. (1994). Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science, 264, 1772-1775. doi:10.1126/science.8209258. (Pubitemid 24227760)
24. Hall, E. D., Andrus, P. K., Oostveen, J. A., Fleck, T. J., & Gurney, M. E. (1998). Relationship of oxygen radical-induced lipid peroxidative damage to disease onset and progression in a transgenic model of familial ALS. Journal of Neuroscience Research, 53, 66-77. doi:10.1002/(SICI)1097-4547(19980701)53:1<66::AIDJNR7>3.0.CO;2-H.
25. Harraz, M. M., Marden, J. J., Zhou, W., et al. (2008). SOD1 mutations disrupt redox-sensitive Rac regulation of NADPH oxidase in a familial ALS model. The Journal of Clinical Investigation, 118, 659-670.
26. Hensley, K., Fedynyshyn, J., Ferrel, S., et al. (2003). Message and protein level elevations of tumor necrosis factor alpha and TNFmodulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiology of Disease, 14, 74-80. doi:10.1016/S0969-9961(03)00087-1. (Pubitemid 37103181)
27. Hensley, K., Mhatre, M., Mou, S., et al. (2006). On the relation of oxidative stress to neuroinflammation: lessons learned from the G93A-SOD1 mouse model of amyotrophic lateral sclerosis. Antioxidants & Redox Signalling, 8, 2075-2087. doi:10.1089/ars.2006.8.2075.
28. Ihara, Y., Nobukuni, K., Takata, H., & Hayabara, T. (2005). Oxidative stress and metal content in blood and cerebrospinal fluid of amyotrophic lateral sclerosis patients with and without a Cu,Znsuperoxide dismutase mutation. Neurological Research, 27, 105-108. doi:10.1179/016164105X18430. (Pubitemid 40189615)
29. Ilieva, E. V., Ayala, V., Jove, M., et al. (2007). Oxidative and endoplasmic reticulum stress interplay in sporadic amyotrophic lateral sclerosis. Brain, 130, 3111-3123. doi:10.1093/brain/awm190. (Pubitemid 350209064)
30. Jokic, N., Di Scala, F., Dupuis, L., et al. (2003). Early activation of antioxidant mechanisms in muscle of mutant Cu/Zn-superoxide dismutase-linked amyotrophic lateral sclerosis mice. Annals of the New York Academy of Sciences, 1010, 552-556. doi:10.1196/annals.1299.102. (Pubitemid 38265043)
31. Kim, R. H., Smith, P. D., Aleyasin, H., et al. (2005). Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine (MPTP) and oxidative stress. Proceedings of the National Academy of Sciences of the United States of America, 102, 5215-5220. doi:10.1073/pnas.0501282102.
32. Kraft, A. D., Resch, J. M., Johnson, D. A., & Johnson, J. A. (2007). Activation of the Nrf2-ARE pathway in muscle and spinal cord during ALS-like pathology in mice expressing mutant SOD1. Experimental Neurology, 207, 107-117. doi:10.1016/j.expneurol.2007.05.026. (Pubitemid 47332487)
33. Lev, N., Ickowicz, D., Melamed, E., & Offen, D. (2008). Oxidative insults induce DJ-1 upregulation and redistribution: implications for neuroprotection. Neurotoxicology, 29, 397-405. doi:10.1016/j.neuro.2008.01.007.
34. Liu, R., Althaus, J. S., Ellerbrock, B. R., Becker, D. A., & Gurney, M. E. (1998). Enhanced oxygen radical production in a transgenic mouse model of familial amyotrophic lateral sclerosis. Annals of Neurology, 44, 763-770. doi:10.1002/ana.410440510.
35. Liu, J., Lillo, C., Jonsson, P. A., et al. (2004). Toxicity of familial ALS-Linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron, 43, 5-17. doi:10.1016/j.neuron.2004.06.016. (Pubitemid 38952815)
36. Liu, D., Wen, J., Liu, J., & Li, L. (1999). The roles of free radicals in amyotrophic lateral sclerosis: reactive oxygen species and elevated oxidation of protein, DNA, and membrane phospholipids. The FASEB Journal, 13, 2318-2328.
37. Mahoney, D. J., Kaczor, J. J., Bourgeois, J., Yasuda, N., & Tarnopolsky, M. A. (2006). Oxidative stress and antioxidant enzyme upregulation in SOD1-G93A mouse skeletal muscle. Muscle & Nerve, 33, 809-816. doi:10.1002/mus.20542. (Pubitemid 43856799)
38. Martinat, C., Shendelman, S., Jonason, A., et al. (2004). Sensitivity to oxidative stress in DJ-1-deficient dopamine neurons: an ESderived cell model of primary Parkinsonism. PLoS Biology, 2, e327. doi:10.1371/journal.pbio.0020327. (Pubitemid 40280475)
39. Menzies, F. M., Yenisetti, S. C., & Min, K. T. (2005). Roles of Drosophila DJ-1 in survival of dopaminergic neurons and oxidative stress. Current Biology, 15, 1578-1582. doi:10.1016/j.cub.2005.07.036. (Pubitemid 41219598)
40. Meulener, M., Whitworth, A. J., Armstrong-Gold, C. E., et al. (2005). Drosophila DJ-1 mutants are selectively sensitive to environmental toxins associated with Parkinson's disease. Current Biology, 15, 1572-1577. doi:10.1016/j.cub.2005.07.064. (Pubitemid 41219597)
41. Mitsumoto, A., Nakagawa, Y., Takeuchi, A., Okawa, K., Iwamatsu, A., & Takanezawa, Y. (2001). Oxidized forms of peroxiredoxins and DJ-1 on two-dimensional gels increased in response to sublethal levels of paraquat. Free Radical Research, 35, 301-310. doi:10.1080/10715760100300831.
42. Nagakubo, D., Taira, T., Kitaura, H., et al. (1997). DJ-1, a novel oncogene which transforms mouse NIH3T3 cells in cooperation with ras. Biochemical and Biophysical Research Communications, 231, 509-513. doi:10.1006/bbrc.1997.6132. (Pubitemid 27214343)
43. Perluigi, M., Poon, H. F., Hensley, K., et al. (2005). Proteomic analysis of 4-hydroxy-2-nonenal-modified proteins in G93ASOD1 transgenic mice: a model of familial amyotrophic lateral sclerosis. Free Radical Biology & Medicine, 38, 960-968. doi:10.1016/j.freeradbiomed.2004.12.021. (Pubitemid 40321087)
44. Poon, H. F., Hensley, K., Thongboonkerd, V., et al. (2005). Redox proteomics analysis of oxidatively modified proteins in G93ASOD1 transgenic mice-a model of familial amyotrophic lateral sclerosis. Free Radical Biology & Medicine, 39, 453-462. doi:10.1016/j.freeradbiomed.2005.03.030. (Pubitemid 41021644)
45. Sekito, A., Koide-Yoshida, S., Niki, T., Taira, T., Iguchi-Ariga, S. M., & Ariga, H. (2006). DJ-1 interacts with HIPK1 and affects H2O2-induced cell death. Free Radical Research, 40, 155-165. doi:10.1080/10715760500456847. (Pubitemid 43050878)
46. Shaw, P. J., Ince, P. G., Falkous, G., & Mantle, D. (1995). Oxidative damage to protein in sporadic motor neuron disease spinal cord. Annals of Neurology, 38, 691-695. doi:10.1002/ana.410380424.
47. Shibata, N., Kawaguchi, M., Uchida, K., et al. (2007). Protein-bound crotonaldehyde accumulates in the spinal cord of superoxide dismutase-1 mutation-associated familial amyotrophic lateral sclerosis and its transgenic mouse model. Neuropathology, 27, 49-61. doi:10.1111/j.1440-1789.2006.00746.x. (Pubitemid 46146613)
48. Shibata, N., Nagai, R., Uchida, K., et al. (2001). Morphological evidence for lipid peroxidation and protein glycoxidation in spinal cords from sporadic amyotrophic lateral sclerosis patients. Brain Research, 917, 97-104. doi:10.1016/S0006-8993(01) 02926-2.
49. Simpson, E. P., Henry, Y. K., Henkel, J. S., Smith, R., & Appel, S. H. (2004). Increased lipid peroxidation in sera of ALS patients: a potential biomarker of disease burden. Neurology, 62, 1758-1765.
50. Smith, R. G., Henry, Y. K., Mattson, M. P., & Appel, S. H. (1998). Presence of 4-hydroxynonenal in cerebrospinal fluid of patients with sporadic amyotrophic lateral sclerosis. Annals of Neurology, 44, 696-699. doi:10.1002/ana.410440419. (Pubitemid 28477861)
51. Taira, T., Saito, Y., Niki, T., Iguchi-Ariga, S. M., Takahashi, K., & Ariga, H. (2004). DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Reports, 5, 213-218. doi:10.1038/sj.embor.7400074. (Pubitemid 38401204)
52. Tohgi, H., Abe, T., Yamazaki, K., Murata, T., Ishizaki, E., & Isobe, C. (1999). Remarkable increase in cerebrospinal fluid 3-nitrotyrosine in patients with sporadic amyotrophic lateral sclerosis. Annals of Neurology, 46, 129-131. doi:10.1002/1531-8249(199907)461<129::AID-ANA21>3.0.CO;2-Y.
53. Yokota, T., Sugawara, K., Ito, K., Takahashi, R., Ariga, H., & Mizusawa, H. (2003). Down regulation of DJ-1 enhances cell death by oxidative stress, ER stress, and proteasome inhibition. Biochemical and Biophysical Research Communications, 312, 1342-1348. doi:10.1016/j.bbrc.2003.11.056. (Pubitemid 37490964)