Parkinson's disease-associated mutations in DJ-1 modulate its dimerization in living cells

Journal of Molecular Medicine

Volumn 91, Issue 5, 2013, Pages 599-611

  Repici, Mariaelena ^a   Straatman, Kornelis R ^a   Balduccio, Nadia ^a   Enguita, Francisco J ^b   Outeiro, Tiago F ^b,c   Giorgini, Flaviano ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^c INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

Author keywords

Bimolecular fluorescence complementation; Dimerization; DJ 1; Parkinson's disease

Indexed keywords

ALOXISTATIN; DJ 1 PROTEIN; HETERODIMER; MUTANT PROTEIN;

AGGRESOME; ARTICLE; CELL INCLUSION; CONTROLLED STUDY; DIMERIZATION; FLUORESCENCE; GENE DISRUPTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; OXIDATIVE STRESS; PARKINSON DISEASE; TRANSIENT TRANSFECTION; WILD TYPE;

AMINO ACID SUBSTITUTION; GENE EXPRESSION; GENETIC VECTORS; HEK293 CELLS; HUMANS; HYDROGEN PEROXIDE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROSCOPY, CONFOCAL; MODELS, MOLECULAR; MUTATION; ONCOGENE PROTEINS; OXIDATIVE STRESS; PARKINSON DISEASE; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; TRANSFECTION;

EID: 84879076109     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-012-0976-y     Document Type: Article

References (40)

1. Bonifati V (2012) Autosomal recessive parkinsonism. Parkinsonism Relat Disord 18(Suppl 1):S4-6
2. Nuytemans K, Theuns J, Cruts M, Van Broeckhoven C (2010) Genetic etiology of Parkinson disease associated with mutations in the SNCA, PARK2, PINK1, PARK7, and LRRK2 genes: a mutation update. Hum Mutat 31:763-780
3. Corti O, Lesage S, Brice A (2011) What genetics tells us about the causes and mechanisms of Parkinson's disease. Physiol Rev 91:1161-1218
4. 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
5. Bonifati V, Rizzu P, Squitieri F, Krieger E, Vanacore N, van Swieten JC, Brice A, van Duijn CM, Oostra B, Meco G et al (2003) DJ-1(PARK7), a novel gene for autosomal recessive, early onset parkinsonism. Neurol Sci 24:159-160
6. 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
7. Zhang L, Shimoji M, Thomas B, Moore DJ, Yu SW, Marupudi NI, Torp R, Torgner IA, Ottersen OP, Dawson TM et al (2005) Mitochondrial localization of the Parkinson's disease related protein DJ-1: implications for pathogenesis. Hum Mol Genet 14:2063-2073
8. 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
9. Wilson MA, Collins JL, Hod Y, Ringe D, Petsko GA (2003) 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 U S A 100:9256-9261
10. Gorner K, Holtorf E, Waak J, Pham TT, Vogt-Weisenhorn DM, Wurst W, Haass C, Kahle PJ (2007) Structural determinants of the C-terminal helix-kink-helix motif essential for protein stability and survival promoting activity of DJ-1. J Biol Chem 282:13680-13691
11. Honbou K, Suzuki NN, Horiuchi M, Niki T, Taira T, Ariga H, Inagaki F (2003) The crystal structure of DJ-1, a protein related to male fertility and Parkinson's disease. J Biol Chem 278:31380-31384
12. Cookson MR (2010) DJ-1, PINK1, and their effects on mitochondrial pathways. Mov Disord: Off J Mov Disord Soc 25(Suppl 1):S44-48
13. Martin I, Dawson VL, Dawson TM (2011) Recent advances in the genetics of Parkinson's disease. Annu Rev Genomics Hum Genet 12:301-325
14. Olzmann JA, Brown K, Wilkinson KD, Rees HD, Huai Q, Ke H, Levey AI, Li L, Chin LS (2004) Familial Parkinson's disease-associated L166P mutation disrupts DJ-1 protein folding and function. J Biol Chem 279:8506-8515
15. Gorner K, Holtorf E, Odoy S, Nuscher B, Yamamoto A, Regula JT, Beyer K, Haass C, Kahle PJ (2004) Differential effects of Parkinson's disease-associated mutations on stability and folding of DJ-1. J Biol Chem 279:6943-6951
16. 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
17. Miller DW, Ahmad R, Hague S, Baptista MJ, Canet-Aviles R, McLendon C, Carter DM, Zhu PP, Stadler J, Chandran J et al (2003) L166P mutant DJ-1, causative for recessive Parkinson's disease, is degraded through the ubiquitin-proteasome system. J Biol Chem 278:36588-36595
18. 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
19. Malgieri G, Eliezer D (2008) Structural effects of Parkinson's disease linked DJ-1 mutations. Protein Sci: Publ Protein Soc 17:855-868
20. 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. Biochem 46:5776-5789
21. Ramsey CP, Giasson BI (2010) L10p and P158DEL DJ-1 mutations cause protein instability, aggregation, and dimerization impairments. J Neurosci Res 88:3111-3124
22. Hering R, Strauss KM, Tao X, Bauer A, Woitalla D, Mietz EM, Petrovic S, Bauer P, Schaible W, Muller T et al (2004) Novel homozygous p.E64D mutation in DJ1 in early onset Parkinson disease (PARK7). Hum Mutat 24:321-329
23. Bonny C, Oberson A, Negri S, Sauser C, Schorderet DF (2001) Cell-permeable peptide inhibitors of JNK: novel blockers of beta-cell death. Diabetes 50:77-82
24. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D: Biol Crystallogr 66:486-501
25. Steinkellner G, Rader R, Thallinger GG, Kratky C, Gruber K (2009) VASCo: computation and visualization of annotated protein surface contacts. BMC Bioinformatics 10:32
26. Pettit FK, Bare E, Tsai A, Bowie JU (2007) HotPatch: a statistical approach to finding biologically relevant features on protein surfaces. J Mol Biol 369:863-879
27. Kerppola TK (2006) Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells. Nat Protoc 1:1278-1286
28. Hu CD, Kerppola TK (2003) Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat Biotechnol 21:539-545
29. Hu CD, Grinberg AV, Kerppola TK (2006) Visualization of protein interactions in living cells using bimolecular fluorescence complementation (BiFC) analysis. Current protocols in cell biology / editorial board, Juan S Bonifacino [et al.] Chapter 21: Unit 21 23
30. Kim RH, Smith PD, Aleyasin H, Hayley S, Mount MP, Pownall S, Wakeham A, You-Ten AJ, Kalia SK, Horne P et al (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
31. 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
32. Anderson PC, Daggett V (2008) Molecular basis for the structural instability of human DJ-1 induced by the L166P mutation associated with Parkinson's disease. Biochem 47:9380-9393
33. Herrera FE, Zucchelli S, Jezierska A, Lavina ZS, Gustincich S, Carloni P (2007) On the oligomeric state of DJ-1 protein and its mutants associated with Parkinson Disease. A combined computational and in vitro study. J Biol Chem 282:24905-24914
34. 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
35. Waak J, Weber SS, Gorner K, Schall C, Ichijo H, Stehle T, Kahle PJ (2009) Oxidizable residues mediating protein stability and cytoprotective interaction of DJ-1 with apoptosis signal-regulating kinase 1. J Biol Chem 284:14245-14257
36. Liu F, Nguyen JL, Hulleman JD, Li L, Rochet JC (2008) Mechanisms of DJ-1 neuroprotection in a cellular model of Parkinson's disease. J Neurochem 105:2435-2453
37. Krebiehl G, Ruckerbauer S, Burbulla LF, Kieper N, Maurer B, Waak J, Wolburg H, Gizatullina Z, Gellerich FN, 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
38. Neumann M, Muller V, Gorner K, Kretzschmar HA, Haass C, Kahle PJ (2004) Pathological properties of the Parkinson's disease-associated protein DJ-1 in alpha-synucleinopathies and tauopathies: relevance for multiple system atrophy and Pick's disease. Acta Neuropathol 107:489-496
39. Moore DJ, Zhang L, Troncoso J, Lee MK, Hattori N, Mizuno Y, Dawson TM, Dawson VL (2005) Association of DJ-1 and parkin mediated by pathogenic DJ-1 mutations and oxidative stress. Hum Mol Genet 14:71-84
40. Cha SS, Jung HI, Jeon H, An YJ, Kim IK, Yun S, Ahn HJ, Chung KC, Lee SH, Suh PG et al (2008) Crystal structure of filamentous aggregates of human DJ-1 formed in an inorganic phosphate-dependent manner. J Biol Chem 283:34069-34075