Oxidized DJ-1 inhibits p53 by sequestering p53 from promoters in a DNA-binding affinity-dependent manner

Molecular and Cellular Biology

Volumn 33, Issue 2, 2013, Pages 340-359

  Kato, Izumi ^a   Maita, Hiroshi ^a   Takahashi Niki, Kazuko ^a   Saito, Yoshiro ^b   Noguchi, Noriko ^b   Iguchi Ariga, Sanae M M ^a   Arigaa, Hiroyoshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b DOSHISHA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DJ 1 PROTEIN; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; MUTANT PROTEIN; PROTEIN P21; PROTEIN P53;

AMINO ACID SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; BINDING AFFINITY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE REPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; WILD TYPE;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE, TUMOR; CYSTEINE; DOWN-REGULATION; DUAL SPECIFICITY PHOSPHATASE 1; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HEK293 CELLS; HUMANS; HYDROGEN PEROXIDE; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ONCOGENE PROTEINS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PARKINSON DISEASE; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84871877899     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01350-12     Document Type: Article

References (53)

1. Nagakubo D, Taira T, Kitaura H, Ikeda M, Tamai K, Iguchi-Ariga SM, Ariga H. 1997. DJ-1, a novel oncogene which transforms mouse NIH3T3 cells in cooperation with ras. Biochem. Biophys. Res. Commun. 231:509-513.
2. Bonifati V, Rizzu P, van Baren MJ, Schaap O, Breedveld GJ, Krieger E, Dekker MC, Squitieri F, Ibanez P, Joosse M, van Dongen JW, Vanacore N, van Swieten JC, Brice A, Meco G, van Duijn CM, Oostra BA, Heutink P. 2003. Mutations in the DJ-1 gene associated with autosomal recessive early-onset Parkinsonism. Science 299:256-259.
3. Kinumi T, Kimata J, Taira T, Ariga H, Niki E. 2004. 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. 317:722-728.
4. Takahashi-Niki K, Niki T, Taira T, Iguchi-Ariga SM, Ariga H. 2004. Reduced anti-oxidative stress activities of DJ-1 mutants found in Parkinson's disease patients. Biochem. Biophys. Res. Commun. 320:389-397.
5. Canet-Aviles RM, Wilson MA, Miller DW, Ahmad R, McLendon C, Bandyopadhyay S, Baptista MJ, Ringe D, Petsko GA, Cookson MR. 2004. The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine- sulfinic acid-driven mitochondrial localization. Proc. Natl. Acad. Sci. U. S. A. 101:9103-9108.
6. Kim RH, Peters M, Jang Y, Shi W, Pintilie M, Fletcher GC, DeLuca C, Liepa J, Zhou L, Snow B, Binari RC, Manoukian AS, Bray MR, Liu FF, Tsao MS, Mak TW. 2005. DJ-1, a novel regulator of the tumor suppressor PTEN. Cancer Cell 7:263-273.
7. Martinat C, Shendelman S, Jonason A, Leete T, Beal MF, Yang L, Floss T, Abeliovich A. 2004. Sensitivity to oxidative stress in DJ-1-deficient dopamine neurons: an ES- derived cell model of primary Parkinsonism. PLoS Biol. 2:e327. doi:10.1371/journal.pbio.0020327.
8. Taira T, Saito Y, Niki T, Iguchi-Ariga SM, Takahashi K, Ariga H. 2004. DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep. 5:213-218.
9. Bandopadhyay R, Kingsbury AE, Cookson MR, Reid AR, Evans IM, Hope AD, Pittman AM, Lashley T, Canet-Aviles R, Miller DW, Mc-Lendon C, Strand C, Leonard AJ, Abou-Sleiman PM, Healy DG, Ariga H, Wood NW, de Silva R, Revesz T, Hardy JA, Lees AJ. 2004. The expression of DJ-1 (PARK7) in normal human CNS and idiopathic Parkinson's disease. Brain 127:420-430.
10. Niki T, Takahashi-Niki K, Taira T, Iguchi-Ariga SM, Ariga H. 2003. 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. 1:247-261.
11. Takahashi K, Taira T, Niki T, Seino C, Iguchi-Ariga SM, Ariga H. 2001. DJ-1 positively regulates the androgen receptor by impairing the binding of PIASx alpha to the receptor. J. Biol. Chem. 276:37556-37563.
12. Fan J, Ren H, Jia N, Fei E, Zhou T, Jiang P, Wu M, Wang G. 2008. DJ-1 decreases Bax expression through repressing p53 transcriptional activity. J. Biol. Chem. 283:4022-4030.
13. Shinbo Y, Taira T, Niki T, Iguchi-Ariga SM, Ariga H. 2005. DJ-1 restores p53 transcription activity inhibited by Topors/p53BP3. Int. J. Oncol. 26:641-648.
14. Xu J, Zhong N, Wang H, Elias JE, Kim CY, Woldman I, Pifl C, Gygi SP, Geula C, Yankner BA. 2005. The Parkinson's disease-associated DJ-1 protein is a transcriptional co-activator that protects against neuronal apoptosis. Hum. Mol. Genet. 14:1231-1241.
15. Clements CM, McNally RS, Conti BJ, Mak TW, Ting JP. 2006. DJ-1, a cancer-and Parkinson's disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2. Proc. Natl. Acad. Sci. U. S.A. 103:15091-15096.
16. Das S, Raj L, Zhao B, Kimura Y, Bernstein A, Aaronson SA, Lee SW. 2007. Hzf determines cell survival upon genotoxic stress by modulating p53 transactivation. Cell 130:624-637.
17. Samuels-Lev Y, O'Connor DJ, Bergamaschi D, Trigiante G, Hsieh JK, Zhong S, Campargue I, Naumovski L, Crook T, Lu X. 2001. ASPP proteins specifically stimulate the apoptotic function of p53. Mol. Cell 8:781-794.
18. Tanaka T, Ohkubo S, Tatsuno I, Prives C. 2007. hCAS/CSE1L associates with chromatin and regulates expression of select p53 target genes. Cell 130:638-650.
19. Weger S, Hammer E, Engstler M. 2003. The DNA topoisomerase I binding protein topors as a novel cellular target for SUMO-1 modification: characterization of domains necessary for subcellular localization and sumolation. Exp. Cell Res. 290:13-27.
20. Shinbo Y, Niki T, Taira T, Ooe H, Takahashi-Niki K, Maita C, Seino C, Iguchi-Ariga SM, Ariga H. 2006. Proper SUMO-1 conjugation is essential to DJ-1 to exert its full activities. Cell Death Differ. 13:96-108.
21. Fan J, Ren H, Fei E, Jia N, Ying Z, Jiang P, Wu M, Wang G. 2008. Sumoylation is critical for DJ-1 to repress p53 transcriptional activity. FEBS Lett. 582:1151-1156.
22. Goldberg MS, Pisani A, Haburcak M, Vortherms TA, Kitada T, Costa C, Tong Y, Martella G, Tscherter A, Martins A, Bernardi G, Roth BL, Pothos EN, Calabresi P, Shen J. 2005. Nigrostriatal dopaminergic deficits and hypokinesia caused by inactivation of the familial Parkinsonismlinked gene DJ-1. Neuron 45:489-496.
23. Graham FL, van der Eb AJ. 1973. Transformation of rat cells by DNA of human adenovirus 5. Virology 54:536-539.
24. Saito Y, Hamakubo T, Yoshida Y, Ogawa Y, Hara Y, Fujimura H, Imai Y, Iwanari H, Mochizuki Y, Shichiri M, Nishio K, Kinumi T, Noguchi N, Kodama T, Niki E. 2009. Preparation and application of monoclonal antibodies against oxidized DJ-1. Significant elevation of oxidized DJ-1 in erythrocytes of early-stage Parkinson disease patients. Neurosci. Lett. 465: 1-5.
25. Ishikawa S, Taira T, Niki T, Takahashi-Niki K, Maita C, Maita H, Ariga H, Iguchi-Ariga SM. 2009. 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. 284:28832-28844.
26. Li HM, Niki T, Taira T, Iguchi-Ariga SM, Ariga H. 2005. Association of DJ-1 with chaperones and enhanced association and co-localization with mitochondrial Hsp70 by oxidative stress. Free Radic. Res. 39:1091-1099.
27. Liu YX, Wang J, Guo J, Wu J, Lieberman HB, Yin Y. 2008. DUSP1 is controlled by p53 during the cellular response to oxidative stress. Mol. Cancer Res. 6:624-633.
28. Sun H, Charles CH, Lau LF, Tonks NK. 1993. MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell 75:487-493.
29. Freed-Pastor WA, Prives C. 2012. Mutant p53: one name, many proteins. Genes Dev. 26:1268-1286.
30. Santibanez-Koref MF, Birch JM, Hartley AL, Jones PH, Craft AW, Eden T, Crowther D, Kelsey AM, Harris M. 1991. p53 germline mutations in Li-Fraumeni syndrome. Lancet 338:1490-1491.
31. Schlereth K, Beinoraviciute-Kellner R, Zeitlinger MK, Bretz AC, Sauer M, Charles JP, Vogiatzi F, Leich E, Samans B, Eilers M, Kisker C, Rosenwald A, Stiewe T. 2010. DNA binding cooperativity of p53 modulates the decision between cell-cycle arrest and apoptosis. Mol. Cell 38: 356-368.
32. Choi J, Sullards MC, Olzmann JA, Rees HD, Weintraub ST, Bostwick DE, Gearing M, Levey AI, Chin LS, Li L. 2006. Oxidative damage of DJ-1 is linked to sporadic Parkinson and Alzheimer diseases. J. Biol. Chem. 281:10816-10824.
33. Zhou W, Zhu M, Wilson MA, Petsko GA, Fink AL. 2006. The oxidation state of DJ-1 regulates its chaperone activity toward alpha-synuclein. J. Mol. Biol. 356:1036-1048.
34. Gu W, Roeder RG. 1997. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90:595-606.
35. Rahman-Roblick R, Hellman U, Becker S, Bader FG, Auer G, Wiman KG, Roblick UJ. 2008. Proteomic identification of p53-dependent protein phosphorylation. Oncogene 27:4854-4859.
36. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T, Nishimori H, Tamai K, Tokino T, Nakamura Y, Taya Y. 2000. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102:849-862.
37. Freeman J, Schmidt S, Scharer E, Iggo R. 1994. Mutation of conserved domain II alters the sequence specificity of DNA binding by the p53 protein. EMBO J. 13:5393-5400.
38. Miyashita T, Reed JC. 1995. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80:293-299.
39. Bulavin DV, Saito S, Hollander MC, Sakaguchi K, Anderson CW, Appella E, Fornace AJ, Jr. 1999. Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J. 18:6845-6854.
40. Shono T, Tofilon PJ, Schaefer TS, Parikh D, Liu TJ, Lang FF. 2002. Apoptosis induced by adenovirus-mediated p53 gene transfer in human glioma correlates with site-specific phosphorylation. Cancer Res. 62: 1069-1076.
41. Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME. 1999. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286: 1358-1362.
42. Wang JK, Gao G, Goldfarb M. 1994. Fibroblast growth factor receptors have different signaling and mitogenic potentials. Mol. Cell. Biol. 14:181-188.
43. Lange-Carter CA, Pleiman CM, Gardner AM, Blumer KJ, Johnson GL. 1993. A divergence in theMAPkinase regulatory network defined byMEK kinase and Raf. Science 260:315-319.
44. Kim GS, Choi YK, Song SS, Kim WK, Han BH. 2005. MKP-1 contributes to oxidative stress-induced apoptosis via inactivation of ERK1/2 in SH-SY5Y cells. Biochem. Biophys. Res. Commun. 338:1732-1738.
45. Jacobsen KX, MacDonald H, Lemonde S, Daigle M, Grimes DA, Bulman DE, Albert PR. 2008. A Nurr1 point mutant, implicated in Parkinson's disease, uncouples ERK1/2-dependent regulation of tyrosine hydroxylase transcription. Neurobiol. Dis. 29:117-122.
46. Lu L, Sun X, Liu Y, Zhao H, Zhao S, Yang H. 2012. DJ-1 upregulates tyrosine hydroxylase gene expression by activating its transcriptional factor Nurr1 via the ERK1/2 pathway. Int. J. Biochem. Cell Biol. 44:65-71.
47. Mo JS, Jung J, Yoon JH, Hong JA, Kim MY, Ann EJ, Seo MS, Choi YH, Park HS. 2010. DJ-1 modulates the p38 mitogen-activated protein kinase pathway through physical interaction with apoptosis signal-regulating kinase 1. J. Cell. Biochem. 110:229-237.
48. Chow SN, Chen RJ, Chen CH, Chang TC, Chen LC, Lee WJ, Shen J, Chow LP. 2010. Analysis of protein profiles in human epithelial ovarian cancer tissues by proteomic technology. Eur. J. Gynaecol. Oncol. 31:55-62.
49. Le Naour F, Misek DE, Krause MC, Deneux L, Giordano TJ, Scholl S, Hanash SM. 2001. Proteomics-based identification of RS/DJ-1 as a novel circulating tumor antigen in breast cancer. Clin. Cancer Res. 7:3328-3335.
50. Melle C, Ernst G, Escher N, Hartmann D, Schimmel B, Bleul A, Thieme H, Kaufmann R, Felix K, Friess HM, Settmacher U, Hommann M, Richter KK, Daffner W, Taubig H, Manger T, Claussen U, von Eggeling F. 2007. Protein profiling of microdissected pancreas carcinoma and identification of HSP27 as a potential serum marker. Clin. Chem. 53:629-635.
51. Yuen HF, Chan YP, Law S, Srivastava G, El-Tanani M, Mak TW, Chan KW. 2008. DJ-1 could predict worse prognosis in esophageal squamous cell carcinoma. Cancer Epidemiol. Biomarkers Prev. 17:3593-3602.
52. Zhu XL, Wang ZF, Lei WB, Zhuang HW, Jiang HY, Wen WP. 2010. DJ-1: a novel independent prognostic marker for survival in glottic squamous cell carcinoma. Cancer Sci. 101:1320-1325.
53. Kim YC, Kitaura H, Taira T, Iguchi-Ariga SM, Ariga H. 2009. Oxidation of DJ-1-dependent cell transformation through direct binding of DJ-1 to PTEN. Int. J. Oncol. 35:1331-1341. Oxidative Stress-Dependent Repression of p53 by DJ-1