The Parkinson disease-related protein DJ-1 counteracts mitochondrial impairment induced by the tumour suppressor protein p53 by enhancing endoplasmic reticulum-mitochondria tethering

Human Molecular Genetics

Volumn 22, Issue 11, 2013, Pages 2152-2168

  Ottolini, Denis ^a   Calì, Tito ^a   Negro, Alessandro ^a   Brini, Marisa ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

1,4,5 INOSITOL TRIS PHOSPHATE AGONIST; CALCIUM; DJ 1 PROTEIN; DYNAMIN RELATED PROTEIN 1; INOSITOL 1,4,5 TRISPHOSPHATE; MITOFUSIN 2; PROTEIN P53; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL PROTECTION; CELL STIMULATION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM; HELA CELL; MITOCHONDRION; MORPHOLOGY; MOUSE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BIOLOGICAL TRANSPORT; BRAIN; CALCIUM; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GTP PHOSPHOHYDROLASES; HELA CELLS; HUMANS; INTRACELLULAR MEMBRANES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; ONCOGENE PROTEINS; PHENOTYPE; PROTEOLYSIS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SUBCELLULAR FRACTIONS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84876098997     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt068     Document Type: Article

References (58)

1. Bonifati, V., Rizzu, P., van Baren, M.J., Schaap, O., Breedveld, G.J., Krieger, E., Dekker, M.C., Squitieri, F., Ibanez, P., Joosse, M. et al. (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science, 299, 256-259.
2. Hinkle, D.A., Mullett, S.J., Gabris, B.E. and Hamilton, R.L. (2011) DJ-1 expression in glioblastomas shows positive correlation with p53 expression and negative correlation with epidermal growth factor receptor amplification. Neuropathology, 31, 29-37.
3. Chen, J., Li, L. and Chin, L.S. (2010) Parkinson disease protein DJ-1 converts from a zymogen to a protease by carboxyl-terminal cleavage. Hum. Mol. Genet., 19, 2395-2408.
4. Lucas, J.I. and Marin, I. (2007) A new evolutionary paradigm for the Parkinson disease gene DJ-1. Mol. Biol. Evol., 24, 551-561.
5. Shendelman, S., Jonason, A., Martinat, C., Leete, T. and Abeliovich, A. (2004) DJ-1 is a redox-dependent molecular chaperone that inhibits alpha-synuclein aggregate formation. PLoS Biol., 2, e362.
6. Xu, J., Zhong, N., Wang, H., Elias, J.E., Kim, C.Y., Woldman, I., Pifl, C., Gygi, S.P., Geula, C. and Yankner, B.A. (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.
7. Andres-Mateos, E., Perier, C., Zhang, L., Blanchard-Fillion, B., Greco, T.M., Thomas, B., Ko, H.S., Sasaki, M., Ischiropoulos, H., Przedborski, S. et al. (2007) DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase. Proc. Natl Acad. Sci., 104, 14807-14812.
8. Taira, T., Saito, Y., Niki, T., Iguchi-Ariga, S.M., Takahashi, K. and Ariga, H. (2004) DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep., 5, 213-218.
9. Martinat, C., Shendelman, S., Jonason, A., Leete, T., Beal, M.F., Yang, L., Floss, T. and 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.
10. Blackinton, J., Lakshminarasimhan, M., Thomas, K.J., Ahmad, R., Greggio, E., Raza, A.S., Cookson, M.R. and Wilson, M.A. (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.
11. Kim, R.H., Peters, M., Jang, Y., Shi, W., Pintilie, M., Fletcher, G.C., DeLuca, C., Liepa, J., Zhou, L., Snow, B. et al. (2005) DJ-1, a novel regulator of the tumor suppressor PTEN. Cancer Cell, 7, 263-273.
12. Giaime, E., Sunyach, C., Druon, C., Scarzello, S., Robert, G., Grosso, S., Auberger, P., Goldberg, M.S., Shen, J., Heutink, P. et al. (2010) Loss of function of DJ-1 triggered by Parkinson's disease-associated mutation is due to proteolytic resistance to caspase-6. Cell. Death Differ., 17, 158-169.
13. Gu, L., Cui, T., Fan, C., Zhao, H., Zhao, C., Lu, L. and Yang, H. (2009) Involvement of ERK1/2 signaling pathway in DJ-1-induced neuroprotection against oxidative stress. Biochem. Biophys. Res. Commun., 383, 469-474.
14. Bretaud, S., Allen, C., Ingham, P.W. and Bandmann, O. (2007) p53-dependent neuronal cell death in a DJ-1-deficient zebrafish model of Parkinson's disease. J. Neurochem., 100, 1626-1635.
15. Ren, H., Fu, K., Wang, D., Mu, C. and Wang, G. (2011) Oxidized DJ-1 interacts with the mitochondrial protein BCL-XL. J. Biol. Chem., 286, 35308-35317.
16. Exner, N., Lutz, A.K., Haass, C. and Winklhofer, K.F. (2012) Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences. EMBO J., 31, 3038-3062.
17. Calì, T., Ottolini, D. and Brini, M. (2011) Mitochondria, calcium, and endoplasmic reticulum stress in Parkinson's disease. Biofactors, 37, 228- 240.
18. Canet-Aviles, R.M., Wilson, M.A., Miller, D.W., Ahmad, R., McLendon, C., Bandyopadhyay, S., Baptista, M.J., Ringe, D., Petsko, G.A. and Cookson, M.R. (2004) The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc. Natl Acad. Sci., 101, 9103-9108.
19. Zhang, L., Shimoji, M., Thomas, B., Moore, D.J., Yu, S.W., Marupudi, N.I., Torp, R., Torgner, I.A., Ottersen, O.P., Dawson, T.M. et al. (2005) Mitochondrial localization of the Parkinson's disease related protein DJ-1: implications for pathogenesis. Hum. Mol. Genet., 14, 2063-2073.
20. Shinbo, Y., Niki, T., Taira, T., Ooe, H., Takahashi-Niki, K., Maita, C., Seino, C., Iguchi-Ariga, S.M. and Ariga, H. (2006) Proper SUMO-1 conjugation is essential to DJ-1 to exert its full activities. Cell Death Differ., 13, 96-108.
21. Junn, E., Jang, W.H., Zhao, X., Jeong, B.S. and Mouradian, M.M. (2009) Mitochondrial localization of DJ-1 leads to enhanced neuroprotection. J. Neurosci. Res., 87, 123-129.
22. Kim, S.J., Park, Y.J., Hwang, I.Y., Youdim, M.B., Park, K.S. and Oh, Y.J. (2012) Nuclear translocation of DJ-1 during oxidative stress-induced neuronal cell death. Free Rad. Biol. Med, 15, 936-950.
23. Thomas, K.J., McCoy, M.K., Blackinton, J., Beilina, A., van der Brug, M., Sandebring, A., Miller, D., Maric, D., Cedazo-Minguez, A. and Cookson, M.R. (2011) DJ-1 acts in parallel to the PINK1/parkin pathway to control mitochondrial function and autophagy. Hum. Mol. Genet., 20, 40-50.
24. Irrcher, I., Aleyasin, H., Seifert, E.L., Hewitt, S.J., Chhabra, S., Phillips, M., Lutz, A.K., Rousseaux, M.W., Bevilacqua, L., Jahani-Asl, A. et al. (2010) Loss of the Parkinson's disease-linked gene DJ-1 perturbs mitochondrial dynamics. Hum. Mol. Genet., 19, 3734-3746.
25. Wang, X., Petrie, T.G., Liu, Y., Liu, J., Fujioka, H. and Zhu, X. (2012) Parkinson's disease-associated DJ-1 mutations impair mitochondrial dynamics and cause mitochondrial dysfunction. J. Neurochem., 121, 830-839.
26. Krebiehl, G., Ruckerbauer, S., Burbulla, L.F., Kieper, N., Maurer, B., Waak, J., Wolburg, H., Gizatullina, Z., Gellerich, F.N., Woitalla, D. et al. (2010) Reduced basal autophagy and impaired mitochondrial dynamics due to loss of Parkinson's disease-associated protein DJ-1. PLoS ONE, 5, e9367.
27. Li, J., Donath, S., Li, Y., Qin, D., Prabhakar, B.S. and Li, P. (2010) miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS Genet., 6, e1000795.
28. Fan, J., Ren, H., Jia, N., Fei, E., Zhou, T., Jiang, P., Wu, M. and Wang, G. (2008) DJ-1 decreases Bax expression through repressing p53 transcriptional activity. J. Biol. Chem., 283, 4022-4030.
29. Vasseur, S., Afzal, S., Tomasini, R., Guillaumond, F., Tardivel-Lacombe, J., Mak, T.W. and Iovanna, J.L. (2012) Consequences of DJ-1 upregulation following p53 loss and cell transformation. Oncogene, 31, 664-670.
30. Vaseva, A.V. and Moll, U.M. (2009) The mitochondrial p53 pathway. Biochim. Biophys. Acta, 1787, 414-420.
31. Marchenko, N.D., Zaika, A. and Moll, U.M. (2000) Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J. Biol. Chem., 275, 16202-16212.
32. Mihara, M., Erster, S., Zaika, A., Petrenko, O., Chittenden, T., Pancoska, P. and Moll, U.M. (2003) p53 has a direct apoptogenic role at the mitochondria. Mol. Cell, 11, 577-590.
33. Talos, F., Petrenko, O., Mena, P. and Moll, U.M. (2005) Mitochondrially targeted p53 has tumor suppressor activities in vivo. Cancer Res., 65, 9971-9981.
34. Brini, M. (2008) Calcium-sensitive photoproteins. Methods, 46, 160-166.
35. de Brito, O.M. and Scorrano, L. (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature, 456, 605-610.
36. Cereghetti, G.M., Stangherlin, A., Martins de Brito, O., Chang, C.R., Blackstone, C., Bernardi, P. and Scorrano, L. (2008) Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc. Natl Acad. Sci., 105, 15803-15808.
37. Calì, T., Ottolini, D., Negro, A. and Brini, M. (2012) alpha-Synuclein controls mitochondrial calcium homeostasis by enhancing endoplasmic reticulum-mitochondria interactions. J. Biol. Chem., 287, 17914-17929.
38. 2+ transfer to sustain cell bioenergetics. Biochim. Biophy. Acta, 1832, 495-508.
39. Hayashi, T., Rizzuto, R., Hajnoczky, G. and Su, T.P. (2009) MAM: more than just a housekeeper. Trends Cell Biol., 19, 81-88.
40. Csordas, G., Renken, C., Varnai, P., Walter, L., Weaver, D., Buttle, K.F., Balla, T., Mannella, C.A. and Hajnoczky, G. (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol., 174, 915-921.
41. 2+ channels. J. Cell Biol., 175, 901-911.
42. Hoppe-Seyler, F. and Butz, K. (1993) Repression of endogenous p53 transactivation function in HeLa cervical carcinoma cells by human papillomavirus type 16 E6, human mdm-2, and mutant p53. J. Virol., 67, 3111-3117.
43. Marchenko, N.D., Wolff, S., Erster, S., Becker, K. and Moll, U.M. (2007) Monoubiquitylation promotes mitochondrial p53 translocation. EMBO J., 26, 923-934.
44. Smirnova, E., Griparic, L., Shurland, D.L. and van der Bliek, A.M. (2001) Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell, 12, 2245-2256.
45. Chan, D.C. (2012) Fusion and fission: interlinked processes critical for mitochondrial health. Ann. Rev. Genet., 46, 265-287.
46. Harder, Z., Zunino, R. and McBride, H. (2004) Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission. Curr. Biol., 14, 340-345.
47. Braschi, E., Zunino, R. and McBride, H.M. (2009) MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep., 10, 748-754.
48. Zhong, N., Kim, C.Y., Rizzu, P., Geula, C., Porter, D.R., Pothos, E.N., Squitieri, F., Heutink, P. and Xu, J. (2006) DJ-1 transcriptionally up-regulates the human tyrosine hydroxylase by inhibiting the sumoylation of pyrimidine tract-binding protein-associated splicing factor. J. Biol. Chem., 281, 20940-20948.
49. Zhong, N. and Xu, J. (2008) Synergistic activation of the human MnSOD promoter by DJ-1 and PGC-1alpha: regulation by SUMOylation and oxidation. Hum. Mol. Genet., 17, 3357-3367.
50. Wasiak, S., Zunino, R. and McBride, H.M. (2007) Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell Biol., 177, 439-450.
51. Guzman, J.N., Sanchez-Padilla, J., Wokosin, D., Kondapalli, J., Ilijic, E., Schumacker, P.T. and Surmeier, D.J. (2010) Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature, 468, 696-700.
52. Surmeier, D.J., Guzman, J.N., Sanchez-Padilla, J. and Schumacker, P.T. (2011) The role of calcium and mitochondrial oxidant stress in the loss of substantia nigra pars compacta dopaminergic neurons in Parkinson's disease. Neuroscience, 198, 221-231.
53. Grimm, S. (2012) The ER-mitochondria interface: the social network of cell death. Biochim. Biophys. Acta, 1823, 327-334.
54. 2+ transfer to mitochondria. Cell, 142, 270-283.
55. Rizzuto, R., Brini, M., Bastianutto, C., Marsault, R. and Pozzan, T. (1995) Photoprotein-mediated measurement of calcium ion concentration in mitochondria of living cells. Methods Enzymol., 260, 417-428.
56. c). A critical evaluation. J. Biol. Chem., 270, 9896-9903.
57. 2+ ] in the endoplasmic reticulum and cytoplasm of intact HeLa cells. A comparative study. J. Biol. Chem., 272, 27694-27699.
58. Manders, E.M., Verbeek, F.J. and Aten, J.A. (1993) Measurement of co-localization of objects in dual-colour confocal images J. Microsc., 169, 375-382.