Reactive oxygen species-mediated DJ-1 monomerization modulates intracellular trafficking involving karyopherin β2

Molecular and Cellular Biology

Volumn 34, Issue 16, 2014, Pages 3024-3040

  Björkblom, Benny ^a,b,e   Maple Grødem, Jodi ^a,b   Puno, Marc Rhyan ^c   Odell, Mark ^c   Larsen, Jan Petter ^a   Møller, Simon Geir ^a,d  

^a STAVANGER UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF STAVANGER   (Norway)

^c UNIVERSITY OF WESTMINSTER   (United Kingdom)

^d ST JOHN'S UNIVERSITY   (United States)

^e UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DJ 1 PROTEIN; HETERODIMER; KARYOPHERIN BETA; KARYOPHERIN BETA2; MONOMER; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; CELLULAR DISTRIBUTION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CYTOSOL; DEVELOPMENTAL STAGE; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR TRANSPORT; MITOCHONDRION; MOUSE; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOGENESIS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; WILD TYPE;

ANIMALS; BETA KARYOPHERINS; CELL LINE, TUMOR; CELL NUCLEUS; CYTOSOL; FEMALE; HUMANS; MICE; MITOCHONDRIA; NEURONS; ONCOGENE PROTEINS; OXIDATIVE STRESS; PARKINSON DISEASE; PROTEIN TRANSPORT; REACTIVE OXYGEN SPECIES; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84904505245     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00286-14     Document Type: Article

References (57)

1. Martin I, Dawson VL, Dawson TM. 2011. Recent advances in the genetics of Parkinson's disease. Annu. Rev. Genomics Hum. Genet. 12:301-325. http://dx.doi.org/10.1146/annurev-genom-082410-101440
2. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N. 1998. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392: 605-608. http://dx.doi.org/10.1038/33416
3. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, Albanese A, Nussbaum R, Gonzalez-Maldonado R, Deller T, Salvi S, Cortelli P, Gilks WP, Latchman DS, Harvey RJ, Dallapiccola B, Auburger G, Wood NW. 2004. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304:1158-1160. http://dx.doi.org/10.1126/science.1096284
4. 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. http://dx.doi.org/10.1126/science.1077209
5. Olzmann JA, Bordelon JR, Muly EC, Rees HD, Levey AI, Li L, Chin LS. 2007. Selective enrichment of DJ-1 protein in primate striatal neuronal processes: implications for Parkinson's disease. J. Comp. Neurol. 500: 585-599. http://dx.doi.org/10.1002/cne.21191
6. Andres-Mateos E, Perier C, Zhang L, Blanchard-Fillion B, Greco TM, Thomas B, Ko HS, Sasaki M, Ischiropoulos H, Przedborski S, Dawson TM, Dawson VL. 2007. DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase. Proc. Natl. Acad. Sci. U. S. A. 104:14807-14812. http://dx.doi.org/10.1073/pnas.0703219104
7. 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. http://dx.doi.org/10.1073/pnas.0402959101
8. Mitsumoto A, Nakagawa Y, Takeuchi A, Okawa K, Iwamatsu A, Takanezawa Y. 2001. Oxidized forms of peroxiredoxins and DJ-1 on twodimensional gels increased in response to sublethal levels of paraquat. Free Radic. Res. 35:301-310. http://dx.doi.org/10.1080/10715760100300831
9. 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. http://dx.doi.org/10.1038/sj.embor.7400074
10. 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. http://dx.doi.org/10.1371/journal.pbio.0020327
11. Menzies FM, Yenisetti SC, Min KT. 2005. Roles of Drosophila DJ-1 in survival of dopaminergic neurons and oxidative stress. Curr. Biol. 15: 1578-1582. http://dx.doi.org/10.1016/j.cub.2005.07.036
12. Kim RH, Smith PD, Aleyasin H, Hayley S, Mount MP, Pownall S, Wakeham A, You-Ten AJ, Kalia SK, Horne P, Westaway D, Lozano AM, Anisman H, Park DS, Mak TW. 2005. Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine (MPTP) and oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 102:5215-5220. http://dx.doi.org/10.1073/pnas.0501282102
13. Meulener MC, Xu K, Thomson L, Ischiropoulos H, Bonini NM. 2006. Mutational analysis of DJ-1 in Drosophila implicates functional inactivation by oxidative damage and aging. Proc. Natl. Acad. Sci. U. S. A. 103: 12517-12522. http://dx.doi.org/10.1073/pnas.0601891103
14. Inden M, Taira T, Kitamura Y, Yanagida T, Tsuchiya D, Takata K, Yanagisawa D, Nishimura K, Taniguchi T, Kiso Y, Yoshimoto K, Agatsuma T, Koide-Yoshida S, Iguchi-Ariga SM, Shimohama S, Ariga H. 2006. PARK7 DJ-1 protects against degeneration of nigral dopaminergic neurons in Parkinson's disease rat model. Neurobiol. Dis. 24:144-158. http://dx.doi.org/10.1016/j.nbd.2006.06.004
15. 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. http://dx.doi.org/10.1016/j.bbrc.2004.03.110
16. 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. http://dx.doi.org/10.1006/bbrc.1997.6132
17. Zhang L, Shimoji M, Thomas B, Moore DJ, Yu SW, Marupudi NI, Torp R, Torgner IA, Ottersen OP, Dawson TM, Dawson VL. 2005. Mitochondrial localization of the Parkinson's disease related protein DJ-1: implications for pathogenesis. Hum. Mol. Genet. 14:2063-2073. http://dx.doi.org/10.1093/hmg/ddi211
18. Junn E, Jang WH, Zhao X, Jeong BS, Mouradian MM. 2009. Mitochondrial localization of DJ-1 leads to enhanced neuroprotection. J. Neurosci. Res. 87:123-129. http://dx.doi.org/10.1002/jnr.21831
19. Hayashi T, Ishimori C, Takahashi-Niki K, Taira T, Kim YC, Maita H, Maita C, Ariga H, Iguchi-Ariga SM. 2009. DJ-1 binds to mitochondrial complex I and maintains its activity. Biochem. Biophys. Res. Commun. 390:667-672. http://dx.doi.org/10.1016/j.bbrc.2009.10.025
20. Maita C, Maita H, Iguchi-Ariga SM, Ariga H. 2013. Monomer DJ-1 and its N-terminal sequence are necessary for mitochondrial localization of DJ-1 mutants. PLoS One 8:e54087. http://dx.doi.org/10.1371/journal.pone.0054087
21. van der Brug MP, Blackinton J, Chandran J, Hao LY, Lal A, Mazan-Mamczarz K, Martindale J, Xie C, Ahmad R, Thomas KJ, Beilina A, Gibbs JR, Ding J, Myers AJ, Zhan M, Cai H, Bonini NM, Gorospe M, Cookson MR. 2008. RNA binding activity of the recessive parkinsonism protein DJ-1 supports involvement in multiple cellular pathways. Proc. Natl. Acad. Sci. U. S. A. 105:10244-10249. http://dx.doi.org/10.1073/pnas.0708518105
22. Blackinton J, Lakshminarasimhan M, Thomas KJ, Ahmad R, Greggio E, Raza AS, Cookson MR, Wilson MA. 2009. Formation of a stabilized cysteine sulfinic acid is critical for the mitochondrial function of the parkinsonism protein DJ-1. J. Biol. Chem. 284:6476-6485. http://dx.doi.org/10.1074/jbc. M806599200
23. Junn E, Taniguchi H, Jeong BS, Zhao X, Ichijo H, Mouradian MM. 2005. Interaction of DJ-1 with Daxx inhibits apoptosis signal-regulating kinase 1 activity and cell death. Proc. Natl. Acad. Sci. U. S. A. 102:9691-9696. http://dx.doi.org/10.1073/pnas.0409635102
24. 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. http://dx.doi.org/10.1074/jbc. M101730200
25. 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. http://mcr.aacrjournals.org/content/1/4/247
26. 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. http://dx.doi.org/10.1073/pnas.0607260103
27. 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. http://dx.doi.org/10.3892/ijo.26.3.641
28. Kato I, Maita H, Takahashi-Niki K, Saito Y, Noguchi N, Iguchi-Ariga SM, Ariga H. 2013. Oxidized DJ-1 inhibits p53 by sequestering p53 from promoters in a DNA-binding affinity-dependent manner. Mol. Cell. Biol. 33:340-359. http://dx.doi.org/10.1128/MCB.01350-12
29. Zhong N, Kim CY, Rizzu P, Geula C, Porter DR, Pothos EN, Squitieri F, Heutink P, Xu J. 2006. DJ-1 transcriptionally up-regulates the human tyrosine hydroxylase by inhibiting the sumoylation of pyrimidine tractbinding protein-associated splicing factor. J. Biol. Chem. 281:20940-20948. http://dx.doi.org/10.1074/jbc. M601935200
30. Ishikawa S, Taira T, Takahashi-Niki K, Niki T, Ariga H, Iguchi-Ariga SM. 2010. Human DJ-1-specific transcriptional activation of tyrosine hydroxylase gene. J. Biol. Chem. 285:39718-39731. http://dx.doi.org/10.1074/jbc. M110.137034
31. Moore DJ, Zhang L, Dawson TM, Dawson VL. 2003. A missense mutation (L166P) in DJ-1, linked to familial Parkinson's disease, confers reduced protein stability and impairs homo-oligomerization. J. Neurochem. 87:1558-1567. http://dx.doi.org/10.1111/j.1471-4159.2003.02265.x
32. Chandran JS, Lin X, Zapata A, Hoke A, Shimoji M, Moore SO, Galloway MP, Laird FM, Wong PC, Price DL, Bailey KR, Crawley JN, Shippenberg T, Cai H. 2008. Progressive behavioral deficits in DJ-1-deficient mice are associated with normal nigrostriatal function. Neurobiol Dis. 29:505-514. http://dx.doi.org/10.1016/j.nbd.2007.11.011
33. Johnston AJ, Hoogenraad J, Dougan DA, Truscott KN, Yano M, Mori M, Hoogenraad NJ, Ryan MT. 2002. Insertion and assembly of human tom7 into the preprotein translocase complex of the outer mitochondrial membrane. J. Biol. Chem. 277:42197-42204. http://dx.doi.org/10.1074/jbc. M205613200
34. Bjorkblom B, Ostman N, Hongisto V, Komarovski V, Filen JJ, Nyman TA, Kallunki T, Courtney MJ, Coffey ET. 2005. Constitutively active cytoplasmic c-Jun N-terminal kinase 1 is a dominant regulator of dendritic architecture: role of microtubule-associated protein 2 as an effector. J. Neurosci. 25:6350-6361. http://dx.doi.org/10.1523/JNEUROSCI.1517-05.2005
35. Bjorkblom B, Vainio JC, Hongisto V, Herdegen T, Courtney MJ, Coffey ET. 2008. All JNKs can kill, but nuclear localization is critical for neuronal death. J. Biol. Chem. 283:19704-19713. http://dx.doi.org/10.1074/jbc. M707744200
36. Waetzig V, Wacker U, Haeusgen W, Bjorkblom B, Courtney MJ, Coffey ET, Herdegen T. 2009. Concurrent protective and destructive signaling of JNK2 in neuroblastoma cells. Cell. Signal. 21:873-880. http://dx.doi.org/10.1016/j.cellsig.2009.01.032
37. Xia Z, Dudek H, Miranti CK, Greenberg ME. 1996. Calcium influx via theNMDAreceptor induces immediate early gene transcription by aMAP kinase/ERK-dependent mechanism. J. Neurosci. 16:5425-5436.
38. Coffey ET, Hongisto V, Dickens M, Davis RJ, Courtney MJ. 2000. Dual roles for c-Jun N-terminal kinase in developmental and stress responses in cerebellar granule neurons. J. Neurosci. 20:7602-7613.
39. Vonsattel JP, Del Amaya MP, Keller CE. 2008. Twenty-first century brain banking. Processing brains for research: the Columbia University methods. Acta Neuropathol. 115:509-532. http://dx.doi.org/10.1007/s00401-007-0311-9
40. Burgoyne RD, Cambray-Deakin MA. 1988. The cellular neurobiology of neuronal development: the cerebellar granule cell. Brain Res. 472: 77-101.
41. Macedo MG, Anar B, Bronner IF, Cannella M, Squitieri F, Bonifati V, Hoogeveen A, Heutink P, Rizzu P. 2003. The DJ-1L166P mutant protein associated with early onset Parkinson's disease is unstable and forms higher-order protein complexes. Hum. Mol. Genet. 12:2807-2816. http://dx.doi.org/10.1093/hmg/ddg304
42. Blackinton J, Ahmad R, Miller DW, van der Brug MP, Canet-Aviles RM, Hague SM, Kaleem M, Cookson MR. 2005. Effects of DJ-1 mutations and polymorphisms on protein stability and subcellular localization. Brain Res. Mol. Brain Res. 134:76-83. http://dx.doi.org/10.1016/j.molbrainres.2004.09.004
43. Lange A, Mills RE, Lange CJ, Stewart M, Devine SE, Corbett AH. 2007. Classical nuclear localization signals: definition, function, and interaction with importin alpha. J. Biol. Chem. 282:5101-5105. http://dx.doi.org/10.1074/jbc. R600026200
44. Lee BJ, Cansizoglu AE, Suel KE, Louis TH, Zhang Z, Chook YM. 2006. Rules for nuclear localization sequence recognition by karyopherin beta 2. Cell 126:543-558. http://dx.doi.org/10.1016/j.cell.2006.05.049
45. Kumaran R, Vandrovcova J, Luk C, Sharma S, Renton A, Wood NW, Hardy JA, Lees AJ, Bandopadhyay R. 2009. Differential DJ-1 gene expression in Parkinson's disease. Neurobiol Dis. 36:393-400. http://dx.doi.org/10.1016/j.nbd.2009.08.011
46. Joselin AP, Hewitt SJ, Callaghan SM, Kim RH, Chung YH, Mak TW, Shen J, Slack RS, Park DS. 2012. ROS-dependent regulation of Parkin and DJ-1 localization during oxidative stress in neurons. Hum. Mol. Genet. 21:4888-4903. http://dx.doi.org/10.1093/hmg/dds325
47. Tao X, Tong L. 2003. Crystal structure of human DJ-1, a protein associated with early onset Parkinson's disease. J. Biol. Chem. 278:31372-31379. http://dx.doi.org/10.1074/jbc. M304221200
48. Lakshminarasimhan M, Maldonado MT, Zhou W, Fink AL, Wilson MA. 2008. Structural impact of three Parkinsonism-associated missense mutations on human DJ-1. Biochemistry 47:1381-1392. http://dx.doi.org/10.1021/bi701189c
49. Hulleman JD, Mirzaei H, Guigard E, Taylor KL, Ray SS, Kay CM, Regnier FE, Rochet JC. 2007. Destabilization of DJ-1 by familial substitution and oxidative modifications: implications for Parkinson's disease. Biochemistry 46:5776-5789. http://dx.doi.org/10.1021/bi7001778
50. Repici M, Straatman KR, Balduccio N, Enguita FJ, Outeiro TF, Giorgini F. 2013. Parkinson's disease-associated mutations in DJ-1 modulate its dimerization in living cells. J. Mol. Med. 91:599-611. http://dx.doi.org/10.1007/s00109-012-0976-y
51. Hu CD, Kerppola TK. 2003. Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat. Biotechnol. 21:539-545. http://dx.doi.org/10.1038/nbt816
52. Xiong H, Wang D, Chen L, Choo YS, Ma H, Tang C, Xia K, Jiang W, Ronai Z, Zhuang X, Zhang Z. 2009. Parkin, PINK1, and DJ-1 form a ubiquitin E3 ligase complex promoting unfolded protein degradation. J. Clin. Invest. 119:650-660. http://dx.doi.org/10.1172/JCI37617
53. Hao LY, Giasson BI, Bonini NM. 2010. DJ-1 is critical for mitochondrial function and rescues PINK1 loss of function. Proc. Natl. Acad. Sci. U. S. A. 107:9747-9752. http://dx.doi.org/10.1073/pnas.0911175107
54. Annesi G, Savettieri G, Pugliese P, D'Amelio M, Tarantino P, Ragonese P, La Bella V, Piccoli T, Civitelli D, Annesi F, Fierro B, Piccoli F, Arabia G, Caracciolo M, Ciro Candiano IC, Quattrone A. 2005. DJ-1 mutations and Parkinsonism-dementia-amyotrophic lateral sclerosis complex. Ann. Neurol. 58:803-807. http://dx.doi.org/10.1002/ana.20666
55. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K, Ichijo H. 1998. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17:2596-2606. http://dx.doi.org/10.1093/emboj/17.9.2596
56. Im JY, Lee KW, Junn E, Mouradian MM. 2010. DJ-1 protects against oxidative damage by regulating the thioredoxin/ASK1 complex. Neurosci. Res. 67:203-208. http://dx.doi.org/10.1016/j.neures.2010.04.002
57. Kim SJ, Park YJ, Hwang IY, Youdim MB, Park KS, Oh YJ. 2012. Nuclear translocation of DJ-1 during oxidative stress-induced neuronal cell death. Free Radic. Biol. Med. 53:936-950. http://dx.doi.org/10.1016/j.freeradbiomed.2012.05.035