PINK1 Primes Parkin-Mediated Ubiquitination of PARIS in Dopaminergic Neuronal Survival

Cell Reports

Volumn 18, Issue 4, 2017, Pages 918-932

  Lee, Yunjong ^a,c   Stevens, Daniel A ^a   Kang, Sung Ung ^a,b,d   Jiang, Haisong ^a,b,d   Lee, Yun Il ^a   Ko, Han Seok ^a,b,d   Scarffe, Leslie A ^a   Umanah, George E ^a   Kang, Hojin ^c   Ham, Sangwoo ^c   Kam, Tae In ^a   Allen, Kathleen ^a,b,d   Brahmachari, Saurav ^a,b   Kim, Jungwoo Wren ^a   Neifert, Stewart ^a,b,d   Yun, Seung Pil ^a   Fiesel, Fabienne C ^e,f   Springer, Wolfdieter ^e,f   Dawson, Valina L ^a,b,d   Shin, Joo Ho ^a,c   Dawson, Ted M ^a,b,d   more..

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ADRIENNE HELIS MALVIN MEDICAL RESEARCH FOUNDATION   (United States)

^c Sungkyunkwan University School of Medicine   (South Korea)

^d Diana Helis Henry Medical Research Foundation   (United States)

^e MAYO GRADUATE SCHOOL   (United States)

^f MAYO CLINIC   (United States)

Author keywords

PARIS; parkin; Parkinson's disease; PGC 1 ; PINK1; ubiquitin; ZNF746

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE TRANSFERASE; PARKIN; PARKIN INTERACTING SUBSTRATE; PEPTIDES AND PROTEINS; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PHOSPHOTRANSFERASE; PTEN INDUCED PUTATIVE KINASE 1; UNCLASSIFIED DRUG; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE; REPRESSOR PROTEIN; SMALL INTERFERING RNA; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; ZNF746 PROTEIN, MOUSE;

ADULT; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DOPAMINERGIC NERVE CELL; DOWN REGULATION; ENZYME ACTIVITY; IMMUNOREACTIVITY; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NECROSIS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SUBSTANTIA NIGRA; UBIQUITINATION; ANIMAL; C57BL MOUSE; CHEMISTRY; CHROMATIN IMMUNOPRECIPITATION; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PROMOTER REGION; RNA INTERFERENCE; SITE DIRECTED MUTAGENESIS; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; DOPAMINERGIC NEURONS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTAGENESIS, SITE-DIRECTED; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN KINASES; PROTEOLYSIS; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 85010461607     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.12.090     Document Type: Article

References (78)

1. Baldelli, S., Aquilano, K., Ciriolo, M.R., PGC-1α buffers ROS-mediated removal of mitochondria during myogenesis. Cell Death Dis., 5, 2014, e1515.
2. Byrd, R.A., Weissman, A.M., Compact Parkin only: insights into the structure of an autoinhibited ubiquitin ligase. EMBO J. 32 (2013), 2087–2089.
3. Ciron, C., Zheng, L., Bobela, W., Knott, G.W., Leone, T.C., Kelly, D.P., Schneider, B.L., PGC-1α activity in nigral dopamine neurons determines vulnerability to α-synuclein. Acta Neuropathol. Commun., 3, 2015, 16.
4. Clark, I.E., Dodson, M.W., Jiang, C., Cao, J.H., Huh, J.R., Seol, J.H., Yoo, S.J., Hay, B.A., Guo, M., Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441 (2006), 1162–1166.
5. Clark, J., Reddy, S., Zheng, K., Betensky, R.A., Simon, D.K., Association of PGC-1alpha polymorphisms with age of onset and risk of Parkinson's disease. BMC Med. Genet., 12, 2011, 69.
6. Corti, O., Brice, A., Mitochondrial quality control turns out to be the principal suspect in parkin and PINK1-related autosomal recessive Parkinson's disease. Curr. Opin. Neurobiol. 23 (2013), 100–108.
7. Corti, O., Lesage, S., Brice, A., What genetics tells us about the causes and mechanisms of Parkinson's disease. Physiol. Rev. 91 (2011), 1161–1218.
8. da Costa, C.A., Sunyach, C., Giaime, E., West, A., Corti, O., Brice, A., Safe, S., Abou-Sleiman, P.M., Wood, N.W., Takahashi, H., et al. Transcriptional repression of p53 by parkin and impairment by mutations associated with autosomal recessive juvenile Parkinson's disease. Nat. Cell Biol. 11 (2009), 1370–1375.
9. Dagda, R.K., Pien, I., Wang, R., Zhu, J., Wang, K.Z., Callio, J., Banerjee, T.D., Dagda, R.Y., Chu, C.T., Beyond the mitochondrion: cytosolic PINK1 remodels dendrites through protein kinase A. J. Neurochem. 128 (2014), 864–877.
10. Eschbach, J., von Einem, B., Müller, K., Bayer, H., Scheffold, A., Morrison, B.E., Rudolph, K.L., Thal, D.R., Witting, A., Weydt, P., et al. Mutual exacerbation of peroxisome proliferator-activated receptor γ coactivator 1α deregulation and α-synuclein oligomerization. Ann. Neurol. 77 (2015), 15–32.
11. Fallon, L., Bélanger, C.M., Corera, A.T., Kontogiannea, M., Regan-Klapisz, E., Moreau, F., Voortman, J., Haber, M., Rouleau, G., Thorarinsdottir, T., et al. A regulated interaction with the UIM protein Eps15 implicates parkin in EGF receptor trafficking and PI(3)K-Akt signalling. Nat. Cell Biol. 8 (2006), 834–842.
12. Fedorowicz, M.A., de Vries-Schneider, R.L., Rüb, C., Becker, D., Huang, Y., Zhou, C., Alessi Wolken, D.M., Voos, W., Liu, Y., Przedborski, S., Cytosolic cleaved PINK1 represses Parkin translocation to mitochondria and mitophagy. EMBO Rep. 15 (2014), 86–93.
13. Fiesel, F.C., Moussaud-Lamodière, E.L., Ando, M., Springer, W., A specific subset of E2 ubiquitin-conjugating enzymes regulate Parkin activation and mitophagy differently. J. Cell Sci. 127 (2014), 3488–3504.
14. Fiesel, F.C., Ando, M., Hudec, R., Hill, A.R., Castanedes-Casey, M., Caulfield, T.R., Moussaud-Lamodière, E.L., Stankowski, J.N., Bauer, P.O., Lorenzo-Betancor, O., et al. (Patho-)physiological relevance of PINK1-dependent ubiquitin phosphorylation. EMBO Rep. 16 (2015), 1114–1130.
15. Geisler, S., Holmström, K.M., Skujat, D., Fiesel, F.C., Rothfuss, O.C., Kahle, P.J., Springer, W., PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12 (2010), 119–131.
16. Goldberg, M.S., Fleming, S.M., Palacino, J.J., Cepeda, C., Lam, H.A., Bhatnagar, A., Meloni, E.G., Wu, N., Ackerson, L.C., Klapstein, G.J., et al. Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J. Biol. Chem. 278 (2003), 43628–43635.
17. Haque, M.E., Thomas, K.J., D'Souza, C., Callaghan, S., Kitada, T., Slack, R.S., Fraser, P., Cookson, M.R., Tandon, A., Park, D.S., Cytoplasmic Pink1 activity protects neurons from dopaminergic neurotoxin MPTP. Proc. Natl. Acad. Sci. USA 105 (2008), 1716–1721.
18. Helton, T.D., Otsuka, T., Lee, M.C., Mu, Y., Ehlers, M.D., Pruning and loss of excitatory synapses by the parkin ubiquitin ligase. Proc. Natl. Acad. Sci. USA 105 (2008), 19492–19497.
19. Hunter, T., The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol. Cell 28 (2007), 730–738.
20. Imai, Y., Soda, M., Hatakeyama, S., Akagi, T., Hashikawa, T., Nakayama, K.I., Takahashi, R., CHIP is associated with Parkin, a gene responsible for familial Parkinson's disease, and enhances its ubiquitin ligase activity. Mol. Cell 10 (2002), 55–67.
21. Itier, J.M., Ibanez, P., Mena, M.A., Abbas, N., Cohen-Salmon, C., Bohme, G.A., Laville, M., Pratt, J., Corti, O., Pradier, L., et al. Parkin gene inactivation alters behaviour and dopamine neurotransmission in the mouse. Hum. Mol. Genet. 12 (2003), 2277–2291.
22. Jiang, H., Kang, S.U., Zhang, S., Karuppagounder, S., Xu, J., Lee, Y.K., Kang, B.G., Lee, Y., Zhang, J., Pletnikova, O., et al. Adult conditional knockout of PGC-1α leads to loss of dopamine neurons. eNeuro 3 (2016), 1–8.
23. Kageyama, Y., Zhang, Z., Roda, R., Fukaya, M., Wakabayashi, J., Wakabayashi, N., Kensler, T.W., Reddy, P.H., Iijima, M., Sesaki, H., Mitochondrial division ensures the survival of postmitotic neurons by suppressing oxidative damage. J. Cell Biol. 197 (2012), 535–551.
24. Kageyama, Y., Hoshijima, M., Seo, K., Bedja, D., Sysa-Shah, P., Andrabi, S.A., Chen, W., Höke, A., Dawson, V.L., Dawson, T.M., et al. Parkin-independent mitophagy requires Drp1 and maintains the integrity of mammalian heart and brain. EMBO J. 33 (2014), 2798–2813.
25. Kane, L.A., Lazarou, M., Fogel, A.I., Li, Y., Yamano, K., Sarraf, S.A., Banerjee, S., Youle, R.J., PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J. Cell Biol. 205 (2014), 143–153.
26. Kazlauskaite, A., Kondapalli, C., Gourlay, R., Campbell, D.G., Ritorto, M.S., Hofmann, K., Alessi, D.R., Knebel, A., Trost, M., Muqit, M.M., Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem. J. 460 (2014), 127–139.
27. Kazlauskaite, A., Martínez-Torres, R.J., Wilkie, S., Kumar, A., Peltier, J., Gonzalez, A., Johnson, C., Zhang, J., Hope, A.G., Peggie, M., et al. Binding to serine 65-phosphorylated ubiquitin primes Parkin for optimal PINK1-dependent phosphorylation and activation. EMBO Rep. 16 (2015), 939–954.
28. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., Shimizu, N., Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392 (1998), 605–608.
29. Kitada, T., Pisani, A., Porter, D.R., Yamaguchi, H., Tscherter, A., Martella, G., Bonsi, P., Zhang, C., Pothos, E.N., Shen, J., Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc. Natl. Acad. Sci. USA 104 (2007), 11441–11446.
30. Koyano, F., Okatsu, K., Kosako, H., Tamura, Y., Go, E., Kimura, M., Kimura, Y., Tsuchiya, H., Yoshihara, H., Hirokawa, T., et al. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 510 (2014), 162–166.
31. Kumar, A., Aguirre, J.D., Condos, T.E., Martinez-Torres, R.J., Chaugule, V.K., Toth, R., Sundaramoorthy, R., Mercier, P., Knebel, A., Spratt, D.E., et al. Disruption of the autoinhibited state primes the E3 ligase parkin for activation and catalysis. EMBO J. 34 (2015), 2506–2521.
32. Lee, S.B., Kim, J.J., Nam, H.J., Gao, B., Yin, P., Qin, B., Yi, S.Y., Ham, H., Evans, D., Kim, S.H., et al. Parkin regulates mitosis and genomic stability through Cdc20/Cdh1. Mol. Cell 60 (2015), 21–34.
33. Lin, W., Kang, U.J., Characterization of PINK1 processing, stability, and subcellular localization. J. Neurochem. 106 (2008), 464–474.
34. Lin, W., Kang, U.J., Structural determinants of PINK1 topology and dual subcellular distribution. BMC Cell Biol., 11, 2010, 90.
35. Liu, S., Sawada, T., Lee, S., Yu, W., Silverio, G., Alapatt, P., Millan, I., Shen, A., Saxton, W., Kanao, T., et al. Parkinson's disease-associated kinase PINK1 regulates Miro protein level and axonal transport of mitochondria. PLoS Genet., 8, 2012, e1002537.
36. Martin, I., Dawson, V.L., Dawson, T.M., Recent advances in the genetics of Parkinson's disease. Annu. Rev. Genomics Hum. Genet. 12 (2011), 301–325.
37. Matenia, D., Hempp, C., Timm, T., Eikhof, A., Mandelkow, E.M., Microtubule affinity-regulating kinase 2 (MARK2) turns on phosphatase and tensin homolog (PTEN)-induced kinase 1 (PINK1) at Thr-313, a mutation site in Parkinson disease: effects on mitochondrial transport. J. Biol. Chem. 287 (2012), 8174–8186.
38. Mudò, G., Mäkelä, J., Di Liberto, V., Tselykh, T.V., Olivieri, M., Piepponen, P., Eriksson, O., Mälkiä, A., Bonomo, A., Kairisalo, M., et al. Transgenic expression and activation of PGC-1α protect dopaminergic neurons in the MPTP mouse model of Parkinson's disease. Cell. Mol. Life Sci. 69 (2012), 1153–1165.
39. Murata, H., Sakaguchi, M., Jin, Y., Sakaguchi, Y., Futami, J., Yamada, H., Kataoka, K., Huh, N.H., A new cytosolic pathway from a Parkinson disease-associated kinase, BRPK/PINK1: activation of AKT via mTORC2. J. Biol. Chem. 286 (2011), 7182–7189.
40. Narendra, D.P., Jin, S.M., Tanaka, A., Suen, D.F., Gautier, C.A., Shen, J., Cookson, M.R., Youle, R.J., PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol., 8, 2010, e1000298.
41. Ordureau, A., Sarraf, S.A., Duda, D.M., Heo, J.M., Jedrychowski, M.P., Sviderskiy, V.O., Olszewski, J.L., Koerber, J.T., Xie, T., Beausoleil, S.A., et al. Quantitative proteomics reveal a feedforward mechanism for mitochondrial PARKIN translocation and ubiquitin chain synthesis. Mol. Cell 56 (2014), 360–375.
42. Park, J., Lee, S.B., Lee, S., Kim, Y., Song, S., Kim, S., Bae, E., Kim, J., Shong, M., Kim, J.M., Chung, J., Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441 (2006), 1157–1161.
43. Pickrell, A.M., Youle, R.J., The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson's disease. Neuron 85 (2015), 257–273.
44. Pickrell, A.M., Huang, C.H., Kennedy, S.R., Ordureau, A., Sideris, D.P., Hoekstra, J.G., Harper, J.W., Youle, R.J., Endogenous Parkin preserves dopaminergic substantia nigral neurons following mitochondrial DNA mutagenic stress. Neuron 87 (2015), 371–381.
45. Rochet, J.C., Hay, B.A., Guo, M., Molecular insights into Parkinson's disease. Prog. Mol. Biol. Transl. Sci. 107 (2012), 125–188.
46. Sauvé, V., Lilov, A., Seirafi, M., Vranas, M., Rasool, S., Kozlov, G., Sprules, T., Wang, J., Trempe, J.F., Gehring, K., A Ubl/ubiquitin switch in the activation of Parkin. EMBO J. 34 (2015), 2492–2505.
47. Scarffe, L.A., Stevens, D.A., Dawson, V.L., Dawson, T.M., Parkin and PINK1: much more than mitophagy. Trends Neurosci. 37 (2014), 315–324.
48. Sha, D., Chin, L.S., Li, L., Phosphorylation of parkin by Parkinson disease-linked kinase PINK1 activates parkin E3 ligase function and NF-kappaB signaling. Hum. Mol. Genet. 19 (2010), 352–363.
49. Shan, Y., Liu, B., Li, L., Chang, N., Li, L., Wang, H., Wang, D., Feng, H., Cheung, C., Liao, M., et al. Regulation of PINK1 by NR2B-containing NMDA receptors in ischemic neuronal injury. J. Neurochem. 111 (2009), 1149–1160.
50. Shiba, K., Arai, T., Sato, S., Kubo, S., Ohba, Y., Mizuno, Y., Hattori, N., Parkin stabilizes PINK1 through direct interaction. Biochem. Biophys. Res. Commun. 383 (2009), 331–335.
51. Shin, J.H., Ko, H.S., Kang, H., Lee, Y., Lee, Y.I., Pletinkova, O., Troconso, J.C., Dawson, V.L., Dawson, T.M., PARIS (ZNF746) repression of PGC-1α contributes to neurodegeneration in Parkinson's disease. Cell 144 (2011), 689–702.
52. Siddiqui, A., Bhaumik, D., Chinta, S.J., Rane, A., Rajagopalan, S., Lieu, C.A., Lithgow, G.J., Andersen, J.K., Mitochondrial quality control via the PGC1α-TFEB signaling pathway is compromised by Parkin Q311X mutation but independently restored by rapamycin. J. Neurosci. 35 (2015), 12833–12844.
53. Siddiqui, A., Rane, A., Rajagopalan, S., Chinta, S.J., Andersen, J.K., Detrimental effects of oxidative losses in parkin activity in a model of sporadic Parkinson's disease are attenuated by restoration of PGC1alpha. Neurobiol. Dis. 93 (2016), 115–120.
54. Song, P., Trajkovic, K., Tsunemi, T., Krainc, D., Parkin modulates endosomal organization and function of the endo-lysosomal pathway. J. Neurosci. 36 (2016), 2425–2437.
55. Sterky, F.H., Lee, S., Wibom, R., Olson, L., Larsson, N.G., Impaired mitochondrial transport and Parkin-independent degeneration of respiratory chain-deficient dopamine neurons in vivo. Proc. Natl. Acad. Sci. USA 108 (2011), 12937–12942.
56. Stevens, D.A., Lee, Y., Kang, H.C., Lee, B.D., Lee, Y.I., Bower, A., Jiang, H., Kang, S.U., Andrabi, S.A., Dawson, V.L., et al. Parkin loss leads to PARIS-dependent declines in mitochondrial mass and respiration. Proc. Natl. Acad. Sci. USA 112 (2015), 11696–11701.
57. Su, X., Chu, Y., Kordower, J.H., Li, B., Cao, H., Huang, L., Nishida, M., Song, L., Wang, D., Federoff, H.J., PGC-1α promoter methylation in Parkinson's disease. PLoS ONE, 10, 2015, e0134087.
58. Trempe, J.F., Sauvé, V., Grenier, K., Seirafi, M., Tang, M.Y., Ménade, M., Al-Abdul-Wahid, S., Krett, J., Wong, K., Kozlov, G., et al. Structure of parkin reveals mechanisms for ubiquitin ligase activation. Science 340 (2013), 1451–1455.
59. Vainshtein, A., Desjardins, E.M., Armani, A., Sandri, M., Hood, D.A., PGC-1α modulates denervation-induced mitophagy in skeletal muscle. Skelet. Muscle, 5, 2015, 9.
60. Vainshtein, A., Tryon, L.D., Pauly, M., Hood, D.A., Role of PGC-1α during acute exercise-induced autophagy and mitophagy in skeletal muscle. Am. J. Physiol. Cell Physiol. 308 (2015), C710–C719.
61. 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. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304 (2004), 1158–1160.
62. 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. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc. Natl. Acad. Sci. USA 107 (2010), 378–383.
63. Voigt, A., Berlemann, L.A., Winklhofer, K.F., The mitochondrial kinase PINK1: functions beyond mitophagy. J. Neurochem. 139 (2016), S232–S239.
64. von Coelln, R., Dawson, V.L., Dawson, T.M., Parkin-associated Parkinson's disease. Cell Tissue Res. 318 (2004), 175–184.
65. Von Coelln, R., Thomas, B., Savitt, J.M., Lim, K.L., Sasaki, M., Hess, E.J., Dawson, V.L., Dawson, T.M., Loss of locus coeruleus neurons and reduced startle in parkin null mice. Proc. Natl. Acad. Sci. USA 101 (2004), 10744–10749.
66. Wauer, T., Komander, D., Structure of the human Parkin ligase domain in an autoinhibited state. EMBO J. 32 (2013), 2099–2112.
67. Wauer, T., Simicek, M., Schubert, A., Komander, D., Mechanism of phospho-ubiquitin-induced PARKIN activation. Nature 524 (2015), 370–374.
68. Wauer, T., Swatek, K.N., Wagstaff, J.L., Gladkova, C., Pruneda, J.N., Michel, M.A., Gersch, M., Johnson, C.M., Freund, S.M., Komander, D., Ubiquitin Ser65 phosphorylation affects ubiquitin structure, chain assembly and hydrolysis. EMBO J. 34 (2015), 307–325.
69. Weihofen, A., Ostaszewski, B., Minami, Y., Selkoe, D.J., Pink1 Parkinson mutations, the Cdc37/Hsp90 chaperones and Parkin all influence the maturation or subcellular distribution of Pink1. Hum. Mol. Genet. 17 (2008), 602–616.
70. West, A.B., Dawson, V.L., Dawson, T.M., The role of PARKIN in Parkinson's disease. Dawson, T.M., (eds.) Parkinson's Disease: Genetics and Pathogenesis, 2007, Informa Healthcare, 199–218.
71. Winklhofer, K.F., Parkin and mitochondrial quality control: toward assembling the puzzle. Trends Cell Biol. 24 (2014), 332–341.
72. Woodroof, H.I., Pogson, J.H., Begley, M., Cantley, L.C., Deak, M., Campbell, D.G., van Aalten, D.M., Whitworth, A.J., Alessi, D.R., Muqit, M.M., Discovery of catalytically active orthologues of the Parkinson's disease kinase PINK1: analysis of substrate specificity and impact of mutations. Open Biol., 1, 2011, 110012.
73. Yamano, K., Queliconi, B.B., Koyano, F., Saeki, Y., Hirokawa, T., Tanaka, K., Matsuda, N., Site-specific interaction mapping of phosphorylated ubiquitin to uncover Parkin activation. J. Biol. Chem. 290 (2015), 25199–25211.
74. Yang, Y., Gehrke, S., Imai, Y., Huang, Z., Ouyang, Y., Wang, J.W., Yang, L., Beal, M.F., Vogel, H., Lu, B., Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc. Natl. Acad. Sci. USA 103 (2006), 10793–10798.
75. Yogev, O., Pines, O., Dual targeting of mitochondrial proteins: mechanism, regulation and function. Biochim. Biophys. Acta 1808 (2011), 1012–1020.
76. Zheng, B., Liao, Z., Locascio, J.J., Lesniak, K.A., Roderick, S.S., Watt, M.L., Eklund, A.C., Zhang-James, Y., Kim, P.D., Hauser, M.A., et al., Global PD Gene Expression (GPEX) Consortium. PGC-1α, a potential therapeutic target for early intervention in Parkinson's disease. Sci. Transl. Med., 2, 2010, 52ra73.
77. Zhou, C., Huang, Y., Shao, Y., May, J., Prou, D., Perier, C., Dauer, W., Schon, E.A., Przedborski, S., The kinase domain of mitochondrial PINK1 faces the cytoplasm. Proc. Natl. Acad. Sci. USA 105 (2008), 12022–12027.
78. Zhou, H., Falkenburger, B.H., Schulz, J.B., Tieu, K., Xu, Z., Xia, X.G., Silencing of the Pink1 gene expression by conditional RNAi does not induce dopaminergic neuron death in mice. Int. J. Biol. Sci. 3 (2007), 242–250.