TRAP1 rescues PINK1 loss-of-function phenotypes

Human Molecular Genetics

Volumn 22, Issue 14, 2013, Pages 2829-2841

  Zhang, Li ^a   Karsten, Peter ^a   Hamm, Sabine ^a   Pogson, Joe H ^b   Mü ller Rischart, A Kathrin ^c,d   Exner, Nicole ^c   Haass, Christian ^c,d,e   Whitworth, Alexander J ^b   Winklhofer, Konstanze F ^c,d,e   Schulz, Jö rg B ^a,f   Voigt, Aaron ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF MUNICH   (Germany)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^e Germany 3 Munich Cluster for Systems Neurology   (Germany)

^f Julich Aachen Research Alliance JARA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; PARKIN; PROTEIN SERINE THREONINE KINASE; PTEN INDUCED KINASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; DROSOPHILA; FEMALE; GENE OVEREXPRESSION; GENOTYPE PHENOTYPE CORRELATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MALE; MITOCHONDRION; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA INTERFERENCE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL LINE; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE KNOCKOUT TECHNIQUES; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MALE; PARKINSON DISEASE; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; UBIQUITIN-PROTEIN LIGASES;

EID: 84878529485     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt132     Document Type: Article

References (67)

1. 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.
2. Schapira, A.H. (1998) Human complex I defects in neurodegenerative diseases. Biochim. Biophys. Acta, 1364, 261-270.
3. Parker, W.D. Jr, Parks, J.K. and Swerdlow, R.H. (2008) Complex I deficiency in Parkinson's disease frontal cortex. Brain Res., 1189, 215-218.
4. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y. and Shimizu, N. (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature, 392, 605-608.
5. Valente, E.M., Abou-Sleiman, P.M., Caputo, V., Muqit, M.M., Harvey, K., Gispert, S., Ali, Z., Del Turco, D., Bentivoglio, A.R., Healy, D.G. et al. (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science, 304, 1158-1160.
6. Clark, I.E., Dodson, M.W., Jiang, C., Cao, J.H., Huh, J.R., Seol, J.H., Yoo, S.J., Hay, B.A. and Guo, M. (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature, 441, 1162-1166.
7. Park, J., Lee, S.B., Lee, S., Kim, Y., Song, S., Kim, S., Bae, E., Kim, J., Shong, M., Kim, J.M. et al. (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature, 441, 1157-1161.
8. Narendra, D., Tanaka, A., Suen, D.F. and Youle, R.J. (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol., 183, 795-803.
9. Dagda, R.K., Cherra, S.J. III, Kulich, S.M., Tandon, A., Park, D. and Chu, C.T. (2009) Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J. Biol. Chem., 284, 13843-13855.
10. Exner, N., Treske, B., Paquet, D., Holmstrom, K., Schiesling, C., Gispert, S., Carballo-Carbajal, I., Berg, D., Hoepken, H.H., Gasser, T. et al. (2007) Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin. J. Neurosci., 27, 12413-12418.
11. Geisler, S., Holmstrom, K.M., Skujat, D., Fiesel, F.C., Rothfuss, O.C., Kahle, P.J. and Springer, W. (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol., 12, 119-131.
12. Chartier-Harlin, M.C., Kachergus, J., Roumier, C., Mouroux, V., Douay, X., Lincoln, S., Levecque, C., Larvor, L., Andrieux, J., Hulihan, M. 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, D.S., Hulihan, M., Maraganore, D., Gwinn-Hardy, K., Wszolek, Z., Dickson, D. et al. (2004) Comparison of kindreds with parkinsonism and alpha-synuclein genomic multiplications. Ann. Neurol., 55, 174-179.
14. Polymeropoulos, M.H., Lavedan, C., Leroy, E., Ide, S.E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R. et al. (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science, 276, 2045-2047.
15. Singleton, A.B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R. et al. (2003) alpha-Synuclein locus triplication causes Parkinson's disease. Science, 302, 841.
16. Kamp, F., Exner, N., Lutz, A.K., Wender, N., Hegermann, J., Brunner, B., Nuscher, B., Bartels, T., Giese, A., Beyer, K. et al. (2010) Inhibition of mitochondrial fusion by alpha-synuclein is rescued by PINK1, Parkin and DJ-1. EMBO J., 29, 3571-3589.
17. Butler, E.K., Voigt, A., Lutz, A.K., Toegel, J.P., Gerhardt, E., Karsten, P., Falkenburger, B., Reinartz, A., Winklhofer, K.F. and Schulz, J.B. (2012) The mitochondrial chaperone protein TRAP1 mitigates alpha-Synuclein toxicity. PLoS Genet., 8, e1002488.
18. Costantino, E., Maddalena, F., Calise, S., Piscazzi, A., Tirino, V., Fersini, A., Ambrosi, A., Neri, V., Esposito, F. and Landriscina, M. (2009) TRAP1, a novel mitochondrial chaperone responsible for multi-drug resistance and protection from apoptotis in human colorectal carcinoma cells. Cancer Lett., 279, 39-46.
19. Fang, W., Li, X., Jiang, Q., Liu, Z., Yang, H., Wang, S., Xie, S., Liu, Q., Liu, T., Huang, J. et al. (2008) Transcriptional patterns, biomarkers and pathways characterizing nasopharyngeal carcinoma of Southern China. J. Transl. Med., 6, 32.
20. Song, H.Y., Dunbar, J.D., Zhang, Y.X., Guo, D. and Donner, D.B. (1995) Identification of a protein with homology to hsp90 that binds the type 1 tumor necrosis factor receptor. J. Biol. Chem., 270, 3574-3581.
21. Pridgeon, J.W., Olzmann, J.A., Chin, L.S. and Li, L. (2007) PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol., 5, e172.
22. Chien, W.L., Lee, T.R., Hung, S.Y., Kang, K.H., Lee, M.J. and Fu, W.M. (2011) Impairment of oxidative stress-induced heme oxygenase-1 expression by the defect of Parkinson-related gene of PINK1. J. Neurochem., 117, 643-653.
23. McCoy, M.K. and Cookson, M.R. (2012) Mitochondrial quality control and dynamics in Parkinson's disease. Antioxid. Redox Signal., 16, 869-882.
24. Anders, S., Sack, B., Pohl, A., Munte, T., Pramstaller, P., Klein, C. and Binkofski, F. (2012) Compensatory premotor activity during affective face processing in subclinical carriers of a single mutant Parkin allele. Brain, 135, 1128-1140.
25. Keeney, P.M., Xie, J., Capaldi, R.A. and Bennett, J.P. Jr (2006) Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. J. Neurosci., 26, 5256-5264.
26. Mizuno, Y., Ikebe, S., Hattori, N., Nakagawa-Hattori, Y., Mochizuki, H., Tanaka, M. and Ozawa, T. (1995) Role of mitochondria in the etiology and pathogenesis of Parkinson's disease. Biochim. Biophys. Acta, 1271, 265-274.
27. Parker, W.D. Jr and Swerdlow, R.H. (1998) Mitochondrial dysfunction in idiopathic Parkinson disease. Am. J. Hum. Genet., 62, 758-762.
28. Schapira, A.H., Cooper, J.M., Dexter, D., Clark, J.B., Jenner, P. and Marsden, C.D. (1990) Mitochondrial complex I deficiency in Parkinson's disease. J. Neurochem., 54, 823-827.
29. Bezard, E. and Przedborski, S. (2011) A tale on animal models of Parkinson's disease. Mov. Disord., 26, 993-1002.
30. Cannon, J.R. and Greenamyre, J.T. (2011) The role of environmental exposures in neurodegeneration and neurodegenerative diseases. Toxicol. Sci., 124, 225-250.
31. Hirsch, E.C. (2007) Animal models in neurodegenerative diseases. J. Neural. Transm. Suppl., 72, 87-90.
32. Vilain, S., Esposito, G., Haddad, D., Schaap, O., Dobreva, M.P., Vos, M., Van Meensel, S., Morais, V.A., De Strooper, B. and Verstreken, P. (2012) The yeast complex I equivalent NADH dehydrogenase rescues pink1 mutants. PLoS Genet., 8, e1002456.
33. Bonifati, V., Rohe, C.F., Breedveld, G.J., Fabrizio, E., De Mari, M., Tassorelli, C., Tavella, A., Marconi, R., Nicholl, D.J., Chien, H.F. et al. (2005) Early-onset parkinsonism associated with PINK1 mutations: frequency, genotypes, and phenotypes. Neurology, 65, 87-95.
34. Klein, C., Djarmati, A., Hedrich, K., Schafer, N., Scaglione, C., Marchese, R., Kock, N., Schule, B., Hiller, A., Lohnau, T. et al. (2005) PINK1, Parkin, and DJ-1 mutations in Italian patients with early-onset parkinsonism. Eur. J. Hum. Genet., 13, 1086-1093.
35. Duvezin-Caubet, S., Jagasia, R., Wagener, J., Hofmann, S., Trifunovic, A., Hansson, A., Chomyn, A., Bauer, M.F., Attardi, G., Larsson, N.G. et al. (2006) Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. J. Biol. Chem., 281, 37972-37979.
36. Jeyaraju, D.V., Xu, L., Letellier, M.C., Bandaru, S., Zunino, R., Berg, E.A., McBride, H.M. and Pellegrini, L. (2006) Phosphorylation and cleavage of presenilin-associated rhomboid-like protein (PARL) promotes changes in mitochondrial morphology. Proc. Natl Acad. Sci. USA, 103, 18562-18567.
37. Lutz, A.K., Exner, N., Fett, M.E., Schlehe, J.S., Kloos, K., Lammermann, K., Brunner, B., Kurz-Drexler, A., Vogel, F., Reichert, A.S. et al. (2009) Loss of parkin or PINK1 function increases Drp1-dependent mitochondrial fragmentation. J. Biol. Chem., 284, 22938-22951.
38. Taguchi, N., Ishihara, N., Jofuku, A., Oka, T. and Mihara, K. (2007) Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem., 282, 11521-11529.
39. Weihofen, A., Thomas, K.J., Ostaszewski, B.L., Cookson, M.R. and Selkoe, D.J. (2009) Pink1 forms a multiprotein complex with Miro and Milton, linking Pink1 function to mitochondrial trafficking. Biochemistry, 48, 2045-2052.
40. Mitra, K., Wunder, C., Roysam, B., Lin, G. and Lippincott-Schwartz, J. (2009) A hyperfused mitochondrial state achieved at G1-S regulates cyclin E buildup and entry into S phase. Proc. Natl Acad. Sci. USA, 106, 11960-11965.
41. Haque, M.E., Mount, M.P., Safarpour, F., Abdel-Messih, E., Callaghan, S., Mazerolle, C., Kitada, T., Slack, R.S., Wallace, V., Shen, J. et al. (2012) Inactivation of Pink1 gene in vivo sensitizes dopamine-producing neurons to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) and can be rescued by autosomal recessive Parkinson disease genes, Parkin or DJ-1. J. Biol. Chem., 287, 23162-23170.
42. Yang, Y.,Gehrke, S., Imai, Y., Huang, Z., Ouyang, Y.,Wang, J.W.,Yang, L., Beal, M.F., Vogel, H. and Lu, B. (2006) Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc. Natl Acad. Sci. USA, 103, 10793-10798.
43. Chu, C.T. (2010) A pivotal role for PINK1 and autophagy in mitochondrial quality control: implications for Parkinson disease. Hum. Mol. Genet., 19, R28-R37.
44. Dagda, R.K. and Chu, C.T. (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.
45. Pilsl, A. and Winklhofer, K.F. (2012) Parkin, PINK1 and mitochondrial integrity: emerging concepts of mitochondrial dysfunction in Parkinson's disease. Acta Neuropathol., 123, 173-188.
46. Deas, E., Plun-Favreau, H., Gandhi, S., Desmond, H., Kjaer, S., Loh, S.H., Renton, A.E., Harvey, R.J., Whitworth, A.J., Martins, L.M. et al. (2011) PINK1 cleavage at position A103 by the mitochondrial protease PARL. Hum. Mol. Genet., 20, 867-879.
47. Greene, A.W., Grenier, K., Aguileta, M.A., Muise, S., Farazifard, R., Haque, M.E., McBride, H.M., Park, D.S. and Fon, E.A. (2012) Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep., 13, 378-385.
48. Jin, S.M., Lazarou, M., Wang, C., Kane, L.A., Narendra, D.P. and Youle, R.J. (2010) Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol., 191, 933-942.
49. Meissner, C., Lorenz, H., Weihofen, A., Selkoe, D.J. and Lemberg, M.K. (2011) The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking. J. Neurochem., 117, 856-867.
50. Matsuda, N., Sato, S., Shiba, K., Okatsu, K., Saisho, K., Gautier, C.A., Sou, Y.S., Saiki, S., Kawajiri, S., Sato, F. et al. (2010) PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J. Cell Biol., 189, 211-221.
51. Narendra, D.P., Jin, S.M., Tanaka, A., Suen, D.F., Gautier, C.A., Shen, J., Cookson, M.R. and Youle, R.J. (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol., 8, e1000298.
52. Lazarou, M., Jin, S.M., Kane, L.A. and Youle, R.J. (2012) Role of PINK1 binding to the TOM complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin. Dev. Cell, 22, 320-333.
53. 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.
54. Vives-Bauza, C., Zhou, C., Huang, Y., Cui, M., de Vries, R.L., Kim, J., May, J., Tocilescu, M.A., Liu, W., Ko, H.S. et al. (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc. Natl Acad. Sci. USA, 107, 378-383.
55. Kondapalli, C., Kazlauskaite, A., Zhang, N., Woodroof, H.I., Campbell, D.G., Gourlay, R., Burchell, L., Walden, H., Macartney, T.J., Deak, M. et al. (2012) PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol., 2, 120080.
56. Shiba-Fukushima, K., Imai, Y., Yoshida, S., Ishihama, Y., Kanao, T., Sato, S. and Hattori, N. (2012) PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci. Rep., 2, 1002.
57. Springer, W. and Kahle, P.J. (2011) Regulation of PINK1-Parkin-mediated mitophagy. Autophagy, 7, 266-278.
58. Hao, L.Y., Giasson, B.I. and Bonini, N.M. (2010) DJ-1 is critical for mitochondrial function and rescues PINK1 loss of function. Proc. Natl Acad. Sci. USA, 107, 9747-9752.
59. Koh, H., Kim, H., Kim, M.J., Park, J., Lee, H.J. and Chung, J. (2012) Silent information regulator 2 (Sir2) and Forkhead box O (FOXO) complement mitochondrial dysfunction and dopaminergic neuron loss in Drosophila PTEN-induced kinase 1 (PINK1) null mutant. J. Biol. Chem., 287, 12750-12758.
60. Tain, L.S., Chowdhury, R.B., Tao, R.N., Plun-Favreau, H., Moisoi, N., Martins, L.M., Downward, J., Whitworth, A.J. and Tapon, N. (2009) Drosophila HtrA2 is dispensable for apoptosis but acts downstream of PINK1 independently from Parkin. Cell Death Differ., 16, 1118-1125.
61. Vos, M., Esposito, G., Edirisinghe, J.N., Vilain, S., Haddad, D.M., Slabbaert, J.R., Van Meensel, S., Schaap, O., De Strooper, B., Meganathan, R. et al. (2012) Vitamin K2 is a mitochondrial electron carrier that rescues pink1 deficiency. Science, 336, 1306-1310.
62. Costa, A.C., Loh, S.H. and Martins, L.M. (2013) Drosophila Trap1 protects against mitochondrial dysfunction in a PINK1/parkin model of Parkinson's disease. Cell Death Dis., 4, e467.
63. Muller-Rischart, A.K., Pilsl, A., Beaudette, P., Patra, M., Hadian, K., Funke, M., Peis, R., Deinlein, A., Schweimer, C., Kuhn, P.H. et al. (2013) The E3 ligase parkin maintains mitochondrial integrity by increasing linear ubiquitination of NEMO. Mol. Cell, 49, 908-921.
64. Seibler, P., Graziotto, J., Jeong, H., Simunovic, F., Klein, C. and Krainc, D. (2011) Mitochondrial Parkin recruitment is impaired in neurons derived from mutant PINK1 induced pluripotent stem cells. J. Neurosci., 31, 5970-5976.
65. Greene, J.C., Whitworth, A.J., Kuo, I., Andrews, L.A., Feany, M.B. and Pallanck, L.J. (2003) Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc. Natl Acad. Sci. USA, 100, 4078-4083.
66. Liu, S. and Lu, B. (2010) Reduction of protein translation and activation of autophagy protect against PINK1 pathogenesis in Drosophila melanogaster. PLoS Genet., 6, e1001237.
67. Bouman, L., Schlierf, A., Lutz, A.K., Shan, J., Deinlein, A., Kast, J., Galehdar, Z., Palmisano, V., Patenge, N., Berg, D. et al. (2011) Parkin is transcriptionally regulated by ATF4: evidence for an interconnection between mitochondrial stress and ER stress. Cell Death Differ., 18, 769-782.