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Original Article

Free radicals impair the anti-oxidative stress activity of DJ-1 through the formation of SDS-resistant dimer

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Pages 397-412 | Received 27 Jan 2017, Accepted 24 Apr 2017, Published online: 16 May 2017

References

  • Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998;392:605–608.
  • Bonifati V, Rizzu P, van Baren MJ, Schaap O, Breedveld GJ, Krieger E, et al. Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 2003;299:256–259.
  • Valente EM, Abou-Sleiman PM, Caputo V, Muqit MMK, Harvey K, Gispert S, et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004;304:1158–1160.
  • Abou-Sleiman PM, Healy DG, Quinn N, Quinn N, Lees AJ, Wood NW, et al. The role of pathogenic DJ-1 mutations in Parkinson's disease. Ann Neurol 2003;54:283–286.
  • Hague S, Rogaeva E, Hernandez D, Hernandez D, Gulick C, Singleton A, Hanson M, et al. Early-onset Parkinson's disease caused by a compound heterozygous DJ-1 mutation. Ann Neurol 2003;54:271–274.
  • Hering R, Strauss KM, Tao X, Bauer A, Woitalla D, Mietz E-M, et al. Novel homozygous p.E64D mutation in DJ1 in early onset Parkinson disease (PARK7). Hum Mutat 2004;24:321–329.
  • Hedrich K, Djarmati A, Schäfer N, Hering R, Wellenbrock C, Weiss PH, et al. DJ-1 (PARK7) mutations are less frequent than Parkin (PARK2) mutations in early-onset Parkinson disease. Neurology 2004;62:389–394.
  • Annesi G, Savettieri G, Pugliese P, D'Amelio M, Tarantino P, Ragonese P, et al. DJ-1 mutations and parkinsonism-dementia-amyotrophic lateral sclerosis complex. Ann Neurol 2005;58:803–807.
  • Guo JF, Xiao B, Liao B, Zhang X-W, Nie L-L, Zhang Y-H, et al. Mutation analysis of Parkin, PINK1, DJ-1 and ATP13A2 genes in Chinese patients with autosomal recessive early-onset Parkinsonism. Mov Disord 2008;23:2074–2079.
  • Macedo MG, Verbaan D, Fang Y, van Rooden SM, Visser M, Anar B, et al. Genotypic and phenotypic characteristics of Dutch patients with early onset Parkinson's disease. Mov Disord 2009;24:196–203.
  • Ghazavi F, Fazlali Z, Banihosseini SS, Hosseini S-R, Kazemi MH, Shojaee S, et al. PRKN, DJ-1, and PINK1 screening identifies novel splice site mutation in PRKN and two novel DJ-1 mutations. Mov Disord 2011;26:80–89.
  • Nagakubo D, Taira T, Kitaura H, Ikeda M, Tamai K, Iguchi-Ariga SM, et al. DJ-1, a novel oncogene which transforms mouse NIH3T3 cells in cooperation with ras. Biochem Biophys Res Commun 1997;231:509–513.
  • Kim RH, Peters M, Jang Y, Shi W, Pintilie M, Fletcher GC, et al. DJ-1, a novel regulator of the tumor suppressor PTEN. Cancer Cell 2005;7:263–273.
  • Takahashi-Niki K, Kato-Ose I, Murata H, Maita H, Iguchi-Ariga SM, Ariga H. Epidermal growth factor-dependent activation of the extracellular signal-regulated kinase pathway by DJ-1 protein through its direct binding to c-Raf protein. J Biol Chem 2015;290:17838–17847.
  • Takahashi K, Taira T, Niki T, Seino C, Iguchi-Ariga SM, Ariga H, et al. DJ-1 positively regulates the androgen receptor by impairing the binding of PIASx alpha to the receptor. J Biol Chem 2001;276:37556–37563.
  • Niki T, Takahashi-Niki K, Taira T, Iguchi-Ariga SM, Ariga H. DJBP: a novel DJ-1-binding protein, negatively regulates the androgen receptor by recruiting histone deacetylase complex, and DJ-1 antagonizes this inhibition by abrogation of this complex. Mol Cancer Res 2003;1:247–261.
  • Zhong N, Kim CY, Rizzu P, Geula C, Porter DR, Pothos EN, et al. DJ-1 transcriptionally up-regulates the human tyrosine hydroxylase by inhibiting the sumoylation of pyrimidine tract-binding protein-associated splicing factor. J Biol Chem 2006;281:20940–20948.
  • Clements CM, McNally RS, Conti BJ, Mak TW, Ting JP-Y. DJ-1, a cancer- and Parkinson's disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2. Proc Natl Acad Sci USA 2006;103:15091–15096.
  • Fan J, Ren H, Jia N, Fei E, Zhou T, Jiang P, et al. DJ-1 decreases Bax expression through repressing p53 transcriptional activity. J Biol Chem 2008;283:4022–4030.
  • Olzmann JA, Brown K, Wilkinson KD, Rees HD, Huai Q, Ke H, et al. Familial Parkinson's disease-associated L166P mutation disrupts DJ-1 protein folding and function. J Biol Chem 2004;279:8506–8515.
  • Koide-Yoshida S, Niki T, Ueda M, Himeno S, Taira T, Iguchi-Ariga SM, et al. DJ-1 degrades transthyretin and an inactive form of DJ-1 is secreted in familial amyloidotic polyneuropathy. Int J Mol Med 2007;19:885–893.
  • Chen J, Li L, Chin LS. Parkinson disease protein DJ-1 converts from a zymogen to a protease by carboxyl-terminal cleavage. Hum Mol Genet 2010;19:2395–2408.
  • Mitsugi H, Niki T, Takahashi-Niki K, Tanimura K, Yoshizawa-Kumagaye K, Tsunemi M, et al. Identification of the recognition sequence and target proteins for DJ-1 protease. FEBS Lett 2013;587:2493–2499.
  • Canet-Avilés RM, Wilson MA, Miller DW, Ahmad R, McLendon C, Bandyopadhyay S, et al. The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc Natl Acad Sci USA 2004;101:9103–9108.
  • Hayashi T, Ishimori C, Takahashi-Niki K, Taira T, KimY-C, Maita H, et al. DJ-1 binds to mitochondrial complex I and maintains its activity. Biochem Biophys Res Commun 2009;390:667–672.
  • Hao L-Y, Giasson BI, Bonini NM. DJ-1 is critical for mitochondrial function and rescues PINK1 loss of function. Proc Natl Acad Sci USA 2010;107:9747–9752.
  • Krebiehl G, Ruckerbauer S, Burbulla LF, Kieper N, Maurer B, Waak J, et al. Reduced basal autophagy and impaired mitochondrial dynamics due to loss of Parkinson's disease-associated protein DJ-1. PLoS One 2010;5:e9367.
  • Thomas KJ, McCoy MK, Blackinton J, Beilina A, van der Brug M, Sandebring A, et al. DJ-1 acts in parallel to the PINK1/parkin pathway to control mitochondrial function and autophagy. Hum Mol Genet 2011;20:40–50.
  • Shendelman S, Jonason A, Martinat C, Leete T, Abeliovich A. DJ-1 is a redox-dependent molecular chaperone that inhibits alpha-synuclein aggregate formation. PLoS Biol 2004;2:e362.
  • Zhou W, Zhu M, Wilson MA, Petsko GA, Fink AL. The oxidation state of DJ-1 regulates its chaperone activity toward alpha-synuclein. J Mol Biol 2006;356:1036–1048.
  • Taira T, Saito Y, Niki T, Iguchi-Ariga SMM, Takahashi K, Ariga H, et al. DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep 2004;5:213–218.
  • Martinat C, Shendelman S, Jonason A, Leete T, Beal MF, Yang L, et al. Sensitivity to oxidative stress in DJ-1-deficient dopamine neurons: an ES-derived cell model of primary Parkinsonism. PLoS Biol 2004;2:e327.
  • Inden M, Taira T, Kitamura Y, Yanagida T, Tsuchiya D, Takata K, et al. PARK7 DJ-1 protects against degeneration of nigral dopaminergic neurons in Parkinson's disease rat model. Neurobiol Dis 2006;24:144–158.
  • Yasuda T, Kaji Y, Agatsuma T, Niki T, Arisawa M, Shuto S, et al. DJ-1 cooperates with PYCR1 in cell protection against oxidative stress. Biochem Biophys Res Commun 2013;436:289–294.
  • Takahashi-Niki K, Niki T, Taira T, Taira T, Iguchi-Ariga SMM, Ariga H, et al. Reduced anti-oxidative stress activities of DJ-1 mutants found in Parkinson's disease patients. Biochem Biophys Res Commun 2004;320:389–397.
  • Junn E, Taniguchi H, Jeong BS, Zhao X, Ichijo H, Mouradian MM, et al. Interaction of DJ-1 with Daxx inhibits apoptosis signal-regulating kinase 1 activity and cell death. Proc Natl Acad Sci USA 2005;102:9691–9696.
  • Görner K, Holtorf E, Waak J, Pham T-T, Vogt-Weisenhorn DM, Wurst W, et al. Structural determinants of the C-terminal helix-kink-helix motif essential for protein stability and survival promoting activity of DJ-1. J Biol Chem 2007;282:13680–13691.
  • Waak J, Weber SS, Görner K, Schall C, Ichijo H, Stehle T, et al. Oxidizable residues mediating protein stability and cytoprotective interaction of DJ-1 with apoptosis signal-regulating kinase 1. J Biol Chem 2009;284:14245–14257.
  • Kim YC, Kitaura H, Taira T, Iguchi-Ariga SMM, Ariga H. Oxidation of DJ-1-dependent cell transformation through direct binding of DJ-1 to PTEN. Int J Oncol 2009;35:1331–1341.
  • Kinumi T, Kimata J, Taira T, Ariga H, Niki E. Cysteine-106 of DJ-1 is the most sensitive cysteine residue to hydrogen peroxide-mediated oxidation in vivo in human umbilical vein endothelial cells. Biochem Biophys Res Commun 2004;317:722–728.
  • Kim RH, Smith PD, Aleyasin H, Hayley S, Mount MP, Pownall S, et al. Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine (MPTP) and oxidative stress. Proc Natl Acad Sci USA 2005;102:5215–5220.
  • Wilson MA, Collins JL, Hod Y, Ringe D, Petsko GA. The 1.1-A resolution crystal structure of DJ-1, the protein mutated in autosomal recessive early onset Parkinson's disease. Proc Natl Acad Sci USA 2003;100:9256–9261.
  • Takahashi-Niki K, Ganaha Y, Niki T, Nakagawa S, Kato-Ose I, Iguchi-Ariga SMM, et al. DJ-1 activates SIRT1 through its direct binding to SIRT1. Biochem Biophys Res Commun 2016;474:131–136.
  • Maita C, Maita H, Iguchi-Ariga SM, Ariga H, Waller RF. Monomer DJ-1 and its N-terminal sequence are necessary for mitochondrial localization of DJ-1 mutants. PLoS One 2013;8:e54087.
  • Ishikawa S, Taira T, Niki T, Takahashi-Niki K, Maita C, Maita H, et al. Oxidative status of DJ-1-dependent activation of dopamine synthesis through interaction of tyrosine hydroxylase and 4-dihydroxy-L-phenylalanine (L-DOPA) decarboxylase with DJ-1. J Biol Chem 2009;284:28832–28844.
  • Clejan L, Cederbaum AI. Synergistic interactions between NADPH-cytochrome P-450 reductase, paraquat, and iron in the generation of active oxygen radicals. Biochem Pharmacol 1989;38:1779–1786.
  • Kitazawa Y, Matsubara M, Takeyama N, Tanaka T. The role of xanthine oxidase in paraquat intoxication. Arch Biochem Biophys 1991;288:220–224.
  • Cristóvão AC, Choi DH, Baltazar G, Beal MF, Kim YS. The role of NADPH oxidase 1-derived reactive oxygen species in paraquat-mediated dopaminergic cell death. Antioxid Redox Signal 2009;11:2105–2118.
  • Bus JS, Gibson JE. Paraquat: model for oxidant-initiated toxicity. Environ Health Perspect 1984;55:37–46.
  • Rappold PM, Cui M, Chesser AS, Grima JC, Duan L. Paraquat neurotoxicity is mediated by the dopamine transporter and organic cation transporter-3. Proc Natl Acad Sci USA 2011;108:20766–20771.
  • Lev N, Ickowicz D, Melamed E, Offen D. Oxidative insults induce DJ-1 upregulation and redistribution: implications for neuroprotection. Neurotoxicology 2008;29:397–405.
  • Bandopadhyay R, Kingsbury AE, Cookson MR, Reid AR, Evans IM, Hope AD, et al. The expression of DJ-1 (PARK7) in normal human CNS and idiopathic Parkinson's disease. Brain 2003;127:420–430.
  • Ariga H, Takahashi-Niki K, Kato I, Maita H, Niki T, Iguchi-Ariga SMM, et al. Neuroprotective function of DJ-1 in Parkinson's disease. Oxid Med Cell Longev 2013;2013:683920.
  • Choi J, Sullards MC, Olzmann JA, Rees HD, Weintraub ST, Bostwick DE, et al. Oxidative damage of DJ-1 is linked to sporadic Parkinson and Alzheimer diseases. J Biol Chem 2006;281:10816–10824.
  • Tanner CM, Kamel F, Ross GW, Hoppin JA, Goldman SM, Korell M, et al. Rotenone, paraquat, and Parkinson's disease. Environ Health Perspect 2011;119:866–872.

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