The mitochondrial chaperone protein TRAP1 mitigates α-synuclein toxicity

PLoS Genetics

Volumn 8, Issue 2, 2012, Pages

  Butler, Erin K ^a,b,c   Voigt, Aaron ^a   Lutz, A Kathrin ^d   Toegel, Jane P ^a   Gerhardt, Ellen ^b   Karsten, Peter ^a   Falkenburger, Björn ^a   Reinartz, Andrea ^e   Winklhofer, Konstanze F ^d,f   Schulz, Jörg B ^a,g  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c Göttingen Graduate School for Neurosciences and Molecular Biosciences   (Germany)

^d UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF AACHEN MEDICAL CENTER   (Germany)

^f GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^g Juelich Aachen Research Alliance JARA Section JARA Brain   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; CHAPERONE; DOPAMINE; MITOCHONDRIAL PROTEIN; PROTEIN TRAP1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; HEAT SHOCK PROTEIN 90; TRAP1 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL COUNT; CELL STRUCTURE; CLIMBING; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; GENETIC SCREENING; HUMAN; HUMAN CELL; MITOCHONDRION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PROTEIN EXPRESSION; RAT; ANIMAL; BIOSYNTHESIS; CELL STRAIN; CELL STRAIN HEK293; CELL SURVIVAL; DOPAMINERGIC NERVE CELL; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MUTATION; PARKINSON DISEASE; PHYSIOLOGY;

DROSOPHILA MELANOGASTER; RATTUS;

ADENOSINE TRIPHOSPHATE; ALPHA-SYNUCLEIN; ANIMALS; CELL SURVIVAL; DOPAMINE; DOPAMINERGIC NEURONS; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENE SILENCING; HEK293 CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MOLECULAR CHAPERONES; MUTATION; OXIDATIVE STRESS; PARKINSON DISEASE; PC12 CELLS; RATS; RNA, SMALL INTERFERING; ROTENONE;

EID: 84859169870     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002488     Document Type: Article

References (86)

1. Mayeux R, (2003) Epidemiology of neurodegeneration. Annu Rev Neurosci 26: 81-104.
2. Marsden CD, (1983) Neuromelanin and Parkinson's disease. J Neural Transm Suppl 19: 121-141.
3. Lee FJ, Liu F, (2008) Genetic factors involved in the pathogenesis of Parkinson's disease. Brain Res Rev 58: 354-364.
4. Keeney PM, Xie J, Capaldi RA, Bennett JP Jr, (2006) Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. J Neurosci 26: 5256-5264.
5. Schapira AH, Cooper JM, Dexter D, Clark JB, Jenner P, et al. (1990) Mitochondrial complex I deficiency in Parkinson's disease. J Neurochem 54: 823-827.
6. Mizuno Y, Ikebe S, Hattori N, Nakagawa-Hattori Y, Mochizuki H, et al. (1995) Role of mitochondria in the etiology and pathogenesis of Parkinson's disease. Biochim Biophys Acta 1271: 265-274.
7. Semchuk KM, Love EJ, Lee RG, (1992) Parkinson's disease and exposure to agricultural work and pesticide chemicals. Neurology 42: 1328-1335.
8. Liou HH, Tsai MC, Chen CJ, Jeng JS, Chang YC, et al. (1997) Environmental risk factors and Parkinson's disease: a case-control study in Taiwan. Neurology 48: 1583-1588.
9. Costello S, Cockburn M, Bronstein J, Zhang X, Ritz B, (2009) Parkinson's disease and residential exposure to maneb and paraquat from agricultural applications in the central valley of California. Am J Epidemiol 169: 919-926.
10. Wood-Kaczmar A, Gandhi S, Wood NW, (2006) Understanding the molecular causes of Parkinson's disease. Trends in Molecular Medicine 12: 521-528.
11. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, et al. (2003) alpha-Synuclein locus triplication causes Parkinson's disease. Science 302: 841.
12. Chartier-Harlin MC, Kachergus J, Roumier C, Mouroux V, Douay X, et al. (2004) Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet 364: 1167-1169.
13. Farrer M, Kachergus J, Forno L, Lincoln S, Wang DS, et al. (2004) Comparison of kindreds with parkinsonism and alpha-synuclein genomic multiplications. Ann Neurol 55: 174-179.
14. Fuchs J, (2007) Phenotypic variation in a large Swedish pedigree due to SNCA duplication and triplication. Neurology 68: 916-922.
15. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, et al. (1997) Alpha-synuclein in Lewy bodies. Nature 388: 839-840.
16. Lakso M, Vartiainen S, Moilanen AM, Sirvio J, Thomas JH, et al. (2003) Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human alpha-synuclein. J Neurochem 86: 165-172.
17. Smith WW, Jiang H, Pei Z, Tanaka Y, Morita H, et al. (2005) Endoplasmic reticulum stress and mitochondrial cell death pathways mediate A53T mutant alpha-synuclein-induced toxicity. Hum Mol Genet 14: 3801-3811.
18. Norris EH, Uryu K, Leight S, Giasson BI, Trojanowski JQ, et al. (2007) Pesticide exposure exacerbates alpha-synucleinopathy in an A53T transgenic mouse model. Am J Pathol 170: 658-666.
19. Martin LJ, Pan Y, Price AC, Sterling W, Copeland NG, et al. (2006) Parkinson's Disease {alpha}-Synuclein Transgenic Mice Develop Neuronal Mitochondrial Degeneration and Cell Death. J Neurosci 26: 41-50.
20. Hsu LJ, Sagara Y, Arroyo A, Rockenstein E, Sisk A, et al. (2000) {alpha}-Synuclein Promotes Mitochondrial Deficit and Oxidative Stress. Am J Pathol 157: 401-410.
21. Feany MB, Bender WW, (2000) A Drosophila model of Parkinson's disease. Nature 404: 394-398.
22. Lo Bianco C, Ridet JL, Schneider BL, Deglon N, Aebischer P, (2002) alpha-Synucleinopathy and selective dopaminergic neuron loss in a rat lentiviral-based model of Parkinson's disease. Proc Natl Acad Sci U S A 99: 10813-10818.
23. Eslamboli A, Romero-Ramos M, Burger C, Bjorklund T, Muzyczka N, et al. (2007) Long-term consequences of human alpha-synuclein overexpression in the primate ventral midbrain. Brain 130: 799-815.
24. Conway KA, Lee SJ, Rochet JC, Ding TT, Williamson RE, et al. (2000) Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc Natl Acad Sci U S A 97: 571-576.
25. Volles MJ, Lansbury JPT, (2007) Relationships between the Sequence of [alpha]-Synuclein and its Membrane Affinity, Fibrillization Propensity, and Yeast Toxicity. Journal of Molecular Biology 366: 1510-1522.
26. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D, (2004) Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 305: 1292-1295.
27. Martinez-Vicente M, Talloczy Z, Kaushik S, Massey AC, Mazzulli J, et al. (2008) Dopamine-modified alpha-synuclein blocks chaperone-mediated autophagy. J Clin Invest 118: 777-788.
28. Petrucelli L, O'Farrell C, Lockhart PJ, Baptista M, Kehoe K, et al. (2002) Parkin protects against the toxicity associated with mutant alpha-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36: 1007-1019.
29. Stefanis L, Larsen KE, Rideout HJ, Sulzer D, Greene LA, (2001) Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J Neurosci 21: 9549-9560.
30. Snyder H, Mensah K, Theisler C, Lee J, Matouschek A, et al. (2003) Aggregated and monomeric alpha-synuclein bind to the S6′ proteasomal protein and inhibit proteasomal function. J Biol Chem 278: 11753-11759.
31. Tanaka Y, Engelender S, Igarashi S, Rao RK, Wanner T, et al. (2001) Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria-dependent apoptosis. Hum Mol Genet 10: 919-926.
32. Li WW, Yang R, Guo JC, Ren HM, Zha XL, et al. (2007) Localization of alpha-synuclein to mitochondria within midbrain of mice. Neuroreport 18: 1543-1546.
33. Liu G, Zhang C, Yin J, Li X, Cheng F, et al. (2009) alpha-Synuclein is differentially expressed in mitochondria from different rat brain regions and dose-dependently down-regulates complex I activity. Neurosci Lett 454: 187-192.
34. Loeb V, Yakunin E, Saada A, Sharon R, The Transgenic Overexpression of α-Synuclein and Not Its Related Pathology Associates with Complex I Inhibition. Journal of Biological Chemistry 285: 7334-7343.
35. Parihar MS, Parihar A, Fujita M, Hashimoto M, Ghafourifar P, (2008) Mitochondrial association of alpha-synuclein causes oxidative stress. Cell Mol Life Sci 65: 1272-1284.
36. Parihar MS, Parihar A, Fujita M, Hashimoto M, Ghafourifar P, (2009) Alpha-synuclein overexpression and aggregation exacerbates impairment of mitochondrial functions by augmenting oxidative stress in human neuroblastoma cells. The International Journal of Biochemistry & Cell Biology 41: 2015-2024.
37. Shavali S, Brown-Borg HM, Ebadi M, Porter J, (2008) Mitochondrial localization of alpha-synuclein protein in alpha-synuclein overexpressing cells. Neurosci Lett 439: 125-128.
38. Devi L, Raghavendran V, Prabhu BM, Avadhani NG, Anandatheerthavarada HK, (2008) Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. J Biol Chem 283: 9089-9100.
39. Pridgeon JW, Olzmann JA, Chin L-S, Li L, (2007) PINK1 Protects against Oxidative Stress by Phosphorylating Mitochondrial Chaperone TRAP1. PLoS Biol 5: e172 doi:10.1371/journal.pbio.0050172.
40. Muqit MM, Feany MB, (2002) Modelling neurodegenerative diseases in Drosophila: a fruitful approach? Nat Rev Neurosci 3: 237-243.
41. Karpinar DP, Balija MB, Kugler S, Opazo F, Rezaei-Ghaleh N, et al. (2009) Pre-fibrillar alpha-synuclein variants with impaired beta-structure increase neurotoxicity in Parkinson's disease models. EMBO J 28: 3256-3268.
42. Chen J, Shi X, Padmanabhan R, Wang Q, Wu Z, et al. (2008) Identification of novel modulators of mitochondrial function by a genome-wide RNAi screen in Drosophila melanogaster. Genome Res 18: 123-136.
43. Du G, Liu X, Chen X, Song M, Yan Y, et al. Drosophila Histone Deacetylase 6 Protects Dopaminergic Neurons Against {alpha}-Synuclein Toxicity by Promoting Inclusion Formation. Mol Biol Cell pp. E10-03-0200.
44. Bilen J, Bonini NM, (2007) Genome-wide screen for modifiers of ataxin-3 neurodegeneration in Drosophila. PLoS Genet 3: e177 doi:10.1371/journal.pgen.0030177.
45. Shulman JM, Feany MB, (2003) Genetic modifiers of tauopathy in Drosophila. Genetics 165: 1233-1242.
46. Hua G, Zhang Q, Fan Z, (2007) Heat shock protein 75 (TRAP1) antagonizes reactive oxygen species generation and protects cells from granzyme M-mediated apoptosis. J Biol Chem 282: 20553-20560.
47. Im CN, Lee JS, Zheng Y, Seo JS, (2007) Iron chelation study in a normal human hepatocyte cell line suggests that tumor necrosis factor receptor-associated protein 1 (TRAP1) regulates production of reactive oxygen species. J Cell Biochem 100: 474-486.
48. Masuda Y, Shima G, Aiuchi T, Horie M, Hori K, et al. (2004) Involvement of Tumor Necrosis Factor Receptor-associated Protein 1 (TRAP1) in Apoptosis Induced by Î-Hydroxyisovalerylshikonin. Journal of Biological Chemistry 279: 42503-42515.
49. Xiang F, Huang YS, Shi XH, Zhang Q, Mitochondrial chaperone tumour necrosis factor receptor-associated protein 1 protects cardiomyocytes from hypoxic injury by regulating mitochondrial permeability transition pore opening. FEBS J 277: 1929-1938.
50. Panaretou B, Prodromou C, Roe SM, O'Brien R, Ladbury JE, et al. (1998) ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J 17: 4829-4836.
51. Kamp F, Exner N, Lutz AK, Wender N, Hegermann J, et al. (2010) Inhibition of mitochondrial fusion by alpha-synuclein is rescued by PINK1, Parkin and DJ-1. EMBO J 29: 3571-3589.
52. Leav I, Plescia J, Goel HL, Li J, Jiang Z, et al. Cytoprotective Mitochondrial Chaperone TRAP-1 As a Novel Molecular Target in Localized and Metastatic Prostate Cancer. Am J Pathol 176: 393-401.
53. Costantino E, Maddalena F, Calise S, Piscazzi A, Tirino V, et al. (2009) TRAP1, a novel mitochondrial chaperone responsible for multi-drug resistance and protection from apoptotis in human colorectal carcinoma cells. Cancer letters 279: 39-46.
54. Gesualdi NM, Chirico G, Pirozzi G, Costantino E, Landriscina M, et al. (2007) Tumor necrosis factor-associated protein 1 (TRAP-1) protects cells from oxidative stress and apoptosis. Stress: The International Journal on the Biology of Stress 10: 342-350.
55. Takahashi M, Kanuka H, Fujiwara H, Koyama A, Hasegawa M, et al. (2003) Phosphorylation of [alpha]-synuclein characteristic of synucleinopathy lesions is recapitulated in [alpha]-synuclein transgenic Drosophila. Neuroscience Letters 336: 155-158.
56. Botella JA, Bayersdorfer F, Schneuwly S, (2008) Superoxide dismutase overexpression protects dopaminergic neurons in a Drosophila model of Parkinson's disease. Neurobiol Dis 30: 65-73.
57. Shaltiel-Karyo R, Frenkel-Pinter M, Egoz-Matia N, Frydman-Marom A, Shalev DE, et al. Inhibiting α-Synuclein Oligomerization by Stable Cell-Penetrating α-Synuclein Fragments Recovers Phenotype of Parkinson's Disease Model Flies. PLoS ONE 5: e13863 doi:10.1371/journal.pone.0013863.
58. van Ham TJ, Thijssen KL, Breitling R, Hofstra RMW, Plasterk RHA, et al. (2008) C. elegans Model Identifies Genetic Modifiers of α-Synuclein Inclusion Formation During Aging. PLoS Genetics 4: e1000027 doi:10.1371/journal.pgen.1000027.
59. Montesano Gesualdi N, Chirico G, Pirozzi G, Costantino E, Landriscina M, et al. (2007) Tumor necrosis factor-associated protein 1 (TRAP-1) protects cells from oxidative stress and apoptosis. Stress 10: 342-350.
60. Choi WS, Eom DS, Han BS, Kim WK, Han BH, et al. (2004) Phosphorylation of p38 MAPK induced by oxidative stress is linked to activation of both caspase-8- and-9-mediated apoptotic pathways in dopaminergic neurons. J Biol Chem 279: 20451-20460.
61. Hwang S, Kim D, Choi G, An SW, Hong YK, et al. (2010) Parkin suppresses c-Jun N-terminal kinase-induced cell death via transcriptional regulation in Drosophila. Mol Cells 29: 575-580.
62. Novikova L, Garris BL, Garris DR, Lau YS, (2006) Early signs of neuronal apoptosis in the substantia nigra pars compacta of the progressive neurodegenerative mouse 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine/probenecid model of Parkinson's disease. Neuroscience 140: 67-76.
63. Singh S, Kumar S, Dikshit M, (2010) Involvement of the mitochondrial apoptotic pathway and nitric oxide synthase in dopaminergic neuronal death induced by 6-hydroxydopamine and lipopolysaccharide. Redox Rep 15: 115-122.
64. Abou-Sleiman PM, Muqit MM, Wood NW, (2006) Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat Rev Neurosci 7: 207-219.
65. Büeler H, (2009) Impaired mitochondrial dynamics and function in the pathogenesis of Parkinson's disease. Experimental Neurology 218: 235-246.
66. Parker WD Jr, Boyson SJ, Parks JK, (1989) Abnormalities of the electron transport chain in idiopathic Parkinson's disease. Ann Neurol 26: 719-723.
67. Patki G, Che Y, Lau YS, (2009) Mitochondrial dysfunction in the striatum of aged chronic mouse model of Parkinson's disease. Front Aging Neurosci 1: 3.
68. Schapira AHV, (2008) Mitochondria in the aetiology and pathogenesis of Parkinson's disease. The Lancet Neurology 7: 97-109.
69. Song DD, Shults CW, Sisk A, Rockenstein E, Masliah E, (2004) Enhanced substantia nigra mitochondrial pathology in human alpha-synuclein transgenic mice after treatment with MPTP. Exp Neurol 186: 158-172.
70. Vila M, Ramonet D, Perier C, (2008) Mitochondrial alterations in Parkinson's disease: new clues. J Neurochem 107: 317-328.
71. Winklhofer KF, Haass C, (2010) Mitochondrial dysfunction in Parkinson's disease. Biochim Biophys Acta 1802: 29-44.
72. Dagda RK, Chu CT, (2009) Mitochondrial quality control: insights on how Parkinson's disease related genes PINK1, parkin, and Omi/HtrA2 interact to maintain mitochondrial homeostasis. J Bioenerg Biomembr 41: 473-479.
73. Exner N, Treske B, Paquet D, Holmstrom K, Schiesling C, et al. (2007) Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin. J Neurosci 27: 12413-12418.
74. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, et al. (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392: 605-608.
75. Lutz AK, Exner N, Fett ME, Schlehe JS, Kloos K, et al. (2009) Loss of parkin or PINK1 function increases Drp1-dependent mitochondrial fragmentation. J Biol Chem 284: 22938-22951.
76. Morais VA, Verstreken P, Roethig A, Smet J, Snellinx A, et al. (2009) Parkinson's disease mutations in PINK1 result in decreased Complex I activity and deficient synaptic function. EMBO Mol Med 1: 99-111.
77. Sandebring A, Dehvari N, Perez-Manso M, Thomas KJ, Karpilovski E, et al. (2009) Parkin deficiency disrupts calcium homeostasis by modulating phospholipase C signalling. FEBS J 276: 5041-5052.
78. Sandebring A, Thomas KJ, Beilina A, van der Brug M, Cleland MM, et al. (2009) Mitochondrial alterations in PINK1 deficient cells are influenced by calcineurin-dependent dephosphorylation of dynamin-related protein 1. PLoS ONE 4: e5701 doi:10.1371/journal.pone.0005701.
79. Strauss KM, Martins LM, Plun-Favreau H, Marx FP, Kautzmann S, et al. (2005) Loss of function mutations in the gene encoding Omi/HtrA2 in Parkinson's disease. Hum Mol Genet 14: 2099-2111.
80. Valente EM, Salvi S, Ialongo T, Marongiu R, Elia AE, et al. (2004) PINK1 mutations are associated with sporadic early-onset parkinsonism. Ann Neurol 56: 336-341.
81. Voigt A, Herholz D, Fiesel FC, Kaur K, Muller D, et al. (2010) TDP-43-mediated neuron loss in vivo requires RNA-binding activity. PLoS ONE 5: e12247 doi:10.1371/journal.pone.0012247.
82. Auluck PK, Chan HY, Trojanowski JQ, Lee VM, Bonini NM, (2002) Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295: 865-868.
83. Bayersdorfer F, Voigt A, Schneuwly S, Botella JA, Dopamine-dependent neurodegeneration in Drosophila models of familial and sporadic Parkinson's disease. Neurobiology of Disease In Press, Corrected Proof.
84. Livak KJ, Schmittgen TD, (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-[Delta][Delta]CT Method. Methods 25: 402-408.
85. Reich A, Spering C, Gertz K, Harms C, Gerhardt E, et al. (2011) Fas/CD95 Regulatory Protein Faim2 Is Neuroprotective after Transient Brain Ischemia. J Neurosci 31: 225-233.
86. Gegg ME, Cooper JM, Schapira AHV, Taanman J-W, (2009) Silencing of PINK1 Expression Affects Mitochondrial DNA and Oxidative Phosphorylation in DOPAMINERGIC Cells. PLoS ONE 4: e4756 doi:10.1371/journal.pone.0004756.