DJ-1 interactions with a-synuclein attenuate aggregation and cellular toxicity in models of Parkinson's disease

Cell Death and Disease

Volumn 5, Issue 7, 2014, Pages

  Zondler, L ^a   Miller Fleming, L ^b,c   Repici, M ^c   Goncalves S ^b   Tenreiro, S ^b   Rosado Ramos, R ^b   Betzer, C ^d   Straatman, K R ^c   Jensen, P H ^d   Giorgini, F ^c   Outeiro, T F ^a,b  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; DJ 1 PROTEIN; MONOMER; OLIGOMER; DJ-1 PROTEIN, MOUSE; ONCOPROTEIN; PARK7 PROTEIN, HUMAN; PEROXIREDOXIN; PROTEIN AGGREGATE; PROTEIN BINDING; SIGNAL PEPTIDE; SNCA PROTEIN, HUMAN; SNCA PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; BRAIN HOMOGENATE; CONTROLLED STUDY; CYTOTOXICITY; DIMERIZATION; GENE MUTATION; GENE OVEREXPRESSION; HEK293 CELL LINE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; MOUSE; NONHUMAN; OLIGOMERIZATION; ORTHOLOGY; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; TURNOVER TIME; YEAST; ANIMAL; BRAIN; C57BL MOUSE; CELL LINE; CHEMISTRY; GENETICS; METABOLISM; MUTATION;

ALPHA-SYNUCLEIN; ANIMALS; BRAIN; CELL LINE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; MUTATION; ONCOGENE PROTEINS; PARKINSON DISEASE; PEROXIREDOXINS; PROTEIN AGGREGATES; PROTEIN BINDING;

EID: 84905494974     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.307     Document Type: Article

References (57)

1. Bonifati V, Rizzu P, Squitieri F, Krieger E, Vanacore N, van Swieten JC et al. DJ-1( PARK7), a novel gene for autosomal recessive, early onset parkinsonism. Neurol Sci 2003; 24: 159-160
2. Marques O, Outeiro TF. Alpha-synuclein: From secretion to dysfunction and death. Cell Death Dis 2012; 3: e350
3. Wales P, Pinho R, Lazaro DF, Outeiro TF. Limelight on alpha-synuclein: pathological and mechanistic implications in neurodegeneration. J Parkinsons Dis 2013; 3: 415-459
4. Paleologou KE, El-Agnaf OM. alpha-Synuclein aggregation and modulating factors. Subcell Biochem 2012; 65: 109-164
5. Outeiro TF, Putcha P, Tetzlaff JE, Spoelgen R, Koker M, Carvalho F et al. Formation of toxic oligomeric alpha-synuclein species in living cells. PloS One 2008; 3: e1867
6. Winkler S, Hagenah J, Lincoln S, Heckman M, Haugarvoll K, Lohmann-Hedrich K et al. alpha-Synuclein and Parkinson disease susceptibility. Neurology 2007; 69: 1745-1750
7. Cooper AA, Gitler AD, Cashikar A, Haynes CM, Hill KJ, Bhullar B et al. Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 2006; 313: 324-328
8. Gitler AD, Bevis BJ, Shorter J, Strathearn KE, Hamamichi S, Su LJ et al. The Parkinson's disease protein alpha-synuclein disrupts cellular Rab homeostasis. Proc Natl Acad Sci USA 2008; 105: 145-150
9. Outeiro TF, Lindquist S. Yeast cells provide insight into alpha-synuclein biology and pathobiology. Science 2003; 302: 1772-1775
10. Fasano M, Lopiano L. Alpha-synuclein and Parkinson's disease: A proteomic view. Expert Rev Proteomics 2008; 5: 239-248
11. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M. Alphasynuclein in Lewy bodies. Nature 1997; 388: 839-840
12. Canet-Aviles 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
13. Blackinton J, Ahmad R, Miller DW, van der Brug MP, Canet-Aviles RM, Hague SM et al. Effects of DJ-1 mutations and polymorphisms on protein stability and subcellular localization. Brain Research Mol Brain Res 2005; 134: 76-83
14. Zhang L, Shimoji M, Thomas B, Moore DJ, Yu SW, Marupudi NI et al. Mitochondrial localization of the Parkinson's disease related protein DJ-1: Implications for pathogenesis. Hum Mol Genet 2005; 14: 2063-2073
15. 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
16. Gorner K, Holtorf E, Waak J, Pham TT, 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
17. Repici M, Straatman KR, Balduccio N, Enguita FJ, Outeiro TF, Giorgini F. Parkinson's disease-associated mutations in DJ-1 modulate its dimerization in living cells. J Mol Med (Berl) 2013; 91: 599-611
18. Cookson MR. DJ-1, PINK1, and their effects on mitochondrial pathways. Mov Disord 2010; 25: S44-S48
19. 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
20. Zhou W, Bercury K, Cummiskey J, Luong N, Lebin J, Freed CR. Phenylbutyrate up-regulates the DJ-1 protein and protects neurons in cell culture and in animal models of Parkinson disease. J Biol Chem 2011; 286: 14941-14951
21. Sun SY, An CN, Pu XP. DJ-1 protein protects dopaminergic neurons against 6-OHDA/MG-132-induced neurotoxicity in rats. Brain Research Bull 2012; 88: 609-616
22. Zhou W, Freed CR. DJ-1 up-regulates glutathione synthesis during oxidative stress and inhibits A53T alpha-synuclein toxicity. J Biol Chem 2005; 280: 43150-43158
23. Mysling S, Betzer C, Jensen PH, Jorgensen TJ. Characterizing the dynamics of alpha-synuclein oligomers using hydrogen/deuterium exchange monitored by mass spectrometry. Biochemistry 2013; 52: 9097-9103
24. Goncalves SA, Matos JE, Outeiro TF. Zooming into protein oligomerization in neurodegeneration using BiFC. Trends Biochem Sci 2010; 35: 643-651
25. Hu CD, Kerppola TK. Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat Biotechnol 2003; 21: 539-545
26. Honbou K, Suzuki NN, Horiuchi M, Niki T, Taira T, Ariga H et al. The crystal structure of DJ-1, a protein related to male fertility and Parkinson's disease. J Biol Chem 2003; 278: 31380-31384
27. Miller-Fleming L, Giorgini F, Outeiro TF. Yeast as a model for studying human neurodegenerative disorders. Biotechnol J 2008; 3: 325-338
28. Tenreiro S, Munder MC, Alberti S, Outeiro TF. Harnessing the power of yeast to unravel the molecular basis of neurodegeneration. J Neurochem 2013; 127: 438-452
29. Wilson MA, St Amour CV, Collins JL, Ringe D, Petsko GA. The 1.8-A resolution crystal structure of YDR533Cp from Saccharomyces cerevisiae: A member of the DJ-1/ThiJ/PfpI superfamily. Proc Natl Acad Sci USA 2004; 101: 1531-1536
30. Basso E, Antas P, Marijanovic Z, Goncalves S, Tenreiro S, Outeiro TF. PLK2 modulates alpha-synuclein aggregation in yeast and mammalian cells. Mol Neurobiol 2013; 48: 854-862
31. Olanow CW, Perl DP, DeMartino GN, McNaught KS. Lewy-body formation is an aggresome-related process: A hypothesis. Lancet Neurol 2004; 3: 496-503
32. Bonini NM, Giasson BI. Snaring the function of alpha-synuclein. Cell 2005; 123: 359-361
33. Vekrellis K, Xilouri M, Emmanouilidou E, Rideout HJ, Stefanis L. Pathological roles of alpha-synuclein in neurological disorders. Lancet Neurol 2011; 10: 1015-1025
34. Cremades N, Cohen SI, Deas E, Abramov AY, Chen AY, Orte A et al. Direct observation of the interconversion of normal and toxic forms of alpha-synuclein. Cell 2012; 149: 1048-1059
35. Brown DR. Oligomeric alpha-synuclein and its role in neuronal death. IUBMB Life 2010; 62: 334-339
36. Celej MS, Sarroukh R, Goormaghtigh E, Fidelio GD, Ruysschaert JM, Raussens V. Toxic prefibrillar alpha-synuclein amyloid oligomers adopt a distinctive antiparallel beta-sheet structure. Biochem J 2012; 443: 719-726
37. Colla E, Jensen PH, Pletnikova O, Troncoso JC, Glabe C, Lee MK. Accumulation of toxic alpha-synuclein oligomer within endoplasmic reticulum occurs in alpha-synucleinopathy in vivo. J Neurosci 2012; 32: 3301-3305
38. Roostaee A, Beaudoin S, Staskevicius A, Roucou X. Aggregation and neurotoxicity of recombinant alpha-synuclein aggregates initiated by dimerization. Mol Neurodegener 2013; 8: 5
39. 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
40. Aleyasin H, Rousseaux MW, Marcogliese PC, Hewitt SJ, Irrcher I, Joselin AP et al. DJ-1 protects the nigrostriatal axis from the neurotoxin MPTP by modulation of the AKT pathway. Proc Natl Acad Sci USA 2010; 107: 3186-3191
41. Irrcher I, Aleyasin H, Seifert EL, Hewitt SJ, Chhabra S, Phillips M et al. Loss of the Parkinson's disease-linked gene DJ-1 perturbs mitochondrial dynamics. Hum Mol Genet 2010; 19: 3734-3746
42. Wang X, Petrie TG, Liu Y, Liu J, Fujioka H, Zhu X. Parkinson's disease-associated DJ-1 mutations impair mitochondrial dynamics and cause mitochondrial dysfunction. J Neurochem 2012; 121: 830-839
43. van Duijn CM, Dekker MC, Bonifati V, Galjaard RJ, Houwing-Duistermaat JJ, Snijders PJ et al. Park7, a novel locus for autosomal recessive early-onset parkinsonism, on chromosome 1p36. Am J Hum Genet 2001; 69: 629-634
44. Irwin DJ, Lee VM, Trojanowski JQ. Parkinson's disease dementia: Convergence of alpha-synuclein, tau and amyloid-beta pathologies. Nat Rev Neurosci 2013; 14: 626-636
45. Nixon RA. The role of autophagy in neurodegenerative disease. Nat Med 2013; 19: 983-997
46. Sajjad MU, Green EW, Miller-Fleming L, Hands S, Herrera F, Campesan S et al. DJ-1 modulates aggregation and pathogenesis in models of Huntington's disease. Hum Mol Genet 2014; 23: 755-766
47. 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
48. Girotto S, Cendron L, Bisaglia M, Tessari I, Mammi S, Zanotti G et al. DJ-1 is a copper chaperone acting on SOD1 activation. J Biol Chem 2014; 289: 10887-10899
49. Yamashita S, Mori A, Kimura E, Mita S, Maeda Y, Hirano T et al. DJ-1 forms complexes with mutant SOD1 and ameliorates its toxicity. J Neurochem 2010; 113: 860-870
50. Jin J, Li GJ, Davis J, Zhu D, Wang Y, Pan C et al. Identification of novel proteins associated with both alpha-synuclein and DJ-1. Mol Cell Proteomics 2007; 6: 845-859
51. Badiola N, de Oliveira RM, Herrera F, Guardia-Laguarta C, Goncalves SA, Pera M et al. Tau enhances alpha-synuclein aggregation and toxicity in cellular models of synucleinopathy. PLoS One 2011; 6: e26609
52. Jellinger KA. Interaction between alpha-synuclein and other proteins in neurodegenerative disorders. ScientificWorldJournal 2011; 11: 1893-1907
53. Nakamura K, Nemani VM, Azarbal F, Skibinski G, Levy JM, Egami K et al. Direct membrane association drives mitochondrial fission by the Parkinson diseaseassociated protein alpha-synuclein. J Biol Chem 2011; 286: 20710-20726
54. Malgieri G, Eliezer D. Structural effects of Parkinson's disease linked DJ-1 mutations. Protein Sci 2008; 17: 855-868
55. Ramsey CP, Giasson BI. L10p and P158DEL DJ-1 mutations cause protein instability, aggregation, and dimerization impairments. J Neurosci Res 2010; 88: 3111-3124
56. Jensen PH, Islam K, Kenney J, Nielsen MS, Power J, Gai WP. Microtubule-associated protein 1B is a component of cortical Lewy bodies and binds alpha-synuclein filaments. J Biol Chem 2000; 275: 21500-21507
57. Tanese N. Small-scale density gradient sedimentation to separate and analyze multiprotein complexes. Methods 1997; 12: 224-234.