Trumping neurodegeneration: Targeting common pathways regulated by autosomal recessive Parkinson's disease genes

Experimental Neurology

Volumn 298, Issue , 2017, Pages 191-201

  Scott, Laura ^a,b   Dawson, Valina L ^a,b   Dawson, Ted M ^a,b  

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

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

Author keywords

Autosomal recessive Parkinson's disease; Mitochondria; Oxidative stress; Parkin; PINK1; Protein degradation

Indexed keywords

ADENOSINE TRIPHOSPHATASE; PARKIN; PROTEIN ATP13A2; UNCLASSIFIED DRUG; SIGNAL PEPTIDE;

APOPTOSIS; AUTOSOMAL RECESSIVE DISORDER; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CELL FUSION; CELL TRANSPORT; DNAJC6 GENE; DOPAMINERGIC NERVE CELL; EXON; FBXO7 GENE; GENE; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENE REARRANGEMENT; GENETIC CODE; HETEROZYGOSITY; HUMAN; MITOCHONDRIAL BIOGENESIS; MITOCHONDRION; MITOPHAGY; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PARK7 GENE; PARKIN GENE; PARKINSON DISEASE; PINK1 GENE; PLA2G6 GENE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; REVIEW; SYNJ1 GENE; ANIMAL; GENETICS; METABOLISM; MUTATION; PARKINSONISM; PATHOLOGY;

ANIMALS; DOPAMINERGIC NEURONS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOCHONDRIA; MUTATION; PARKINSON DISEASE; PARKINSONIAN DISORDERS;

EID: 85018169957     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2017.04.008     Document Type: Review

References (93)

1. Andres-Mateos, E., Perier, C., Zhang, L., Blanchard-Fillion, B., Greco, T.M., Thomas, B., Ko, H.S., Sasaki, M., Ischiropoulos, H., Przedborski, S., Dawson, T.M., Dawson, V.L., DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 14807–14812.
2. Ashrafi, G., Schlehe, J.S., LaVoie, M.J., Schwarz, T.L., Mitophagy of damaged mitochondria occurs locally in distal neuronal axons and requires PINK1 and Parkin. J. Cell Biol. 206 (2014), 655–670.
3. Bento, C.F., Ashkenazi, A., Jimenez-Sanchez, M., Rubinsztein, D.C., The Parkinson's disease-associated genes ATP13A2 and SYT11 regulate autophagy via a common pathway. Nat. Commun., 7, 2016, 11803.
4. Blackinton, J., Lakshminarasimhan, M., Thomas, K.J., Ahmad, R., Greggio, E., Raza, A.S., Cookson, M.R., Wilson, M.A., Formation of a stabilized cysteine sulfinic acid is critical for the mitochondrial function of the Parkinsonism protein DJ-1. J. Biol. Chem. 284 (2009), 6476–6485.
5. Bonifati, V., Genetics of Parkinson's disease – state of the art, 2013. Parkinsonism Relat. Disord. 20 (2014), S23–S28.
6. Bonifati, V., Rizzu, P., van Baren, M.J., Schaap, O., Breedveld, G.J., Krieger, E., Dekker, M.C., Squitieri, F., Ibanez, P., Joosse, M., van Dongen, J.W., Vanacore, N., van Swieten, J.C., Brice, A., Meco, G., van Duijn, C.M., Oostra, B.A., Heutink, P., Mutations in the DJ-1 gene associated with autosomal recessive early-onset Parkinsonism. Science 299 (2003), 256–259.
7. Burchell, V.S., Nelson, D.E., Sanchez-Martinez, A., Delgado-Camprubi, M., Ivatt, R.M., Pogson, J.H., Randle, S.J., Wray, S., Lewis, P.A., Houlden, H., Abramov, A.Y., Hardy, J., Wood, N.W., Whitworth, A.J., Laman, H., Plun-Favreau, H., The Parkinson's disease–linked proteins Fbxo7 and Parkin interact to mediate mitophagy. Nat. Neurosci. 16 (2013), 1257–1265.
8. Calabrese, V.P., Dorsey, E.R., Constantinescu, R., Thompson, J.P., Biglan, K.M., Holloway, R.G., Kieburtz, K., Marshall, F.J., Ravina, B.M., Schifitto, G., Siderowf, A., Tanner, C.M., Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology 69 (2007), 223–224.
9. Chan, J.Y.H., Chan, S.H.H., Activation of endogenous antioxidants as a common therapeutic strategy against cancer, neurodegeneration and cardiovascular diseases: a lesson learnt from DJ-1. Pharmacol. Ther. 156 (2015), 69–74.
10. Charan, R.A., Johnson, B.N., Zaganelli, S., Nardozzi, J.D., LaVoie, M.J., Inhibition of apoptotic Bax translocation to the mitochondria is a central function of parkin. Cell Death Dis., 5, 2014, e1313.
11. Charan, R.A., LaVoie, M.J., Pathologic and therapeutic implications for the cell biology of parkin. Mol. Cell. Neurosci. 66 (2015), 62–71.
12. Chaturvedi, R.K., Beal, M.F., Mitochondria targeted therapeutic approaches in Parkinson's and Huntington's diseases. Mol. Cell. Neurosci. 55 (2013), 101–114.
13. Chen, H., Chan, D.C., Mitochondrial dynamics—fusion, fission, movement, and mitophagy—in neurodegenerative diseases. Hum. Mol. Genet. 18 (2009), R169–R176.
14. Choubey, V., Cagalinec, M., Liiv, J., Safiulina, D., Hickey, M.A., Kuum, M., Liiv, M., Anwar, T., Eskelinen, E.-L., Kaasik, A., BECN1 is involved in the initiation of mitophagy. Autophagy 10 (2014), 1105–1119.
15. Cornelissen, T., Haddad, D., Wauters, F., Van Humbeeck, C., Mandemakers, W., Koentjoro, B., Sue, C., Gevaert, K., De Strooper, B., Verstreken, P., Vandenberghe, W., The deubiquitinase USP15 antagonizes Parkin-mediated mitochondrial ubiquitination and mitophagy. Hum. Mol. Genet. 23 (2014), 5227–5242.
16. Cunningham, C.N., Baughman, J.M., Phu, L., Tea, J.S., Yu, C., Coons, M., Kirkpatrick, D.S., Bingol, B., Corn, J.E., USP30 and parkin homeostatically regulate atypical ubiquitin chains on mitochondria. Nat. Cell Biol. 17 (2015), 160–169.
17. Di Fonzo, A., Dekker, M.C., Montagna, P., Baruzzi, A., Yonova, E.H., Correia Guedes, L., Szczerbinska, A., Zhao, T., Dubbel-Hulsman, L.O., Wouters, C.H., de Graaff, E., Oyen, W.J., Simons, E.J., Breedveld, G.J., Oostra, B.A., Horstink, M.W., Bonifati, V., FBXO7 mutations cause autosomal recessive, early-onset parkinsonian-pyramidal syndrome. Neurology 72 (2009), 240–245.
18. Drouet, V.A.S.L., Synaptojanin 1 mutation in Parkinson's disease brings further insight into the neuropathological mechanisms. Biomed. Res. Int., 2014, 2014.
19. Durcan, T.M., Kontogiannea, M., Bedard, N., Wing, S.S., Fon, E.A., Ataxin-3 deubiquitination is coupled to Parkin ubiquitination via E2 ubiquitin-conjugating enzyme. J. Biol. Chem. 287 (2011), 531–541.
20. Durcan, T.M., Tang, M.Y., Perusse, J.R., Dashti, E.A., Aguileta, M.A., McLelland, G.L., Gros, P., Shaler, T.A., Faubert, D., Coulombe, B., Fon, E.A., USP8 regulates mitophagy by removing K6-linked ubiquitin conjugates from parkin. EMBO J. 33 (2014), 2473–2491.
21. Esposito, G., Vos, M., Vilain, S., Swerts, J., De Sousa Valadas, J., Van Meensel, S., Schaap, O., Verstreken, P., Aconitase causes iron toxicity in Drosophila pink1 mutants. PLoS Genet., 9, 2013, e1003478.
22. Gautier, C.A., Kitada, T., Shen, J., Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc. Natl. Acad. Sci. 105 (2008), 11364–11369.
23. Gegg, M.E., Cooper, J.M., Schapira, A.H.V., Taanman, J.-W., Silencing of PINK1 expression affects mitochondrial DNA and oxidative phosphorylation in DOPAMINERGIC cells. PLoS One, 4, 2009, e4756.
24. Grenier, K., McLelland, G.-L., Fon, E.A., Parkin- and PINK1-dependent mitophagy in neurons: will the real pathway please stand up?. Front. Neurol., 4, 2013.
25. Grünewald, A., Arns, B., Seibler, P., Rakovic, A., Münchau, A., Ramirez, A., Sue, C.M., Klein, C., ATP13A2 mutations impair mitochondrial function in fibroblasts from patients with Kufor-Rakeb syndrome. Neurobiol. Aging 33 (2012), 1843.e1841–1843.e1847.
26. Gusdon, A.M., Zhu, J., Van Houten, B., Chu, C.T., ATP13A2 regulates mitochondrial bioenergetics through macroautophagy. Neurobiol. Dis. 45 (2012), 962–972.
27. Hasegawa, K., Yasuda, T., Shiraishi, C., Fujiwara, K., Przedborski, S., Mochizuki, H., Yoshikawa, K., Promotion of mitochondrial biogenesis by necdin protects neurons against mitochondrial insults. Nat. Commun., 7, 2016, 10943.
28. Hayashi, T., Ishimori, C., Takahashi-Niki, K., Taira, T., Kim, Y.-C., Maita, H., Maita, C., Ariga, H., Iguchi-Ariga, S.M.M., DJ-1 binds to mitochondrial complex I and maintains its activity. Biochem. Biophys. Res. Commun. 390 (2009), 667–672.
29. Heo, J.-M., Ordureau, A., Paulo, Joao A., Rinehart, J., Harper, J.W., The PINK1-PARKIN mitochondrial ubiquitylation pathway drives a program of OPTN/NDP52 recruitment and TBK1 activation to promote Mitophagy. Mol. Cell 60 (2015), 7–20.
30. Hernandez, D.G., Reed, X., Singleton, A.B., Genetics in Parkinson disease: Mendelian versus non-Mendelian inheritance. J. Neurochem. 139:Suppl. 1 (2016), 59–74.
31. Hertz, Nicholas T., Berthet, A., Sos, Martin L., Thorn, Kurt S., Burlingame, Al L., Nakamura, K., Shokat, Kevan M., A neo-substrate that amplifies catalytic activity of Parkinson's-disease-related kinase PINK1. Cell 154 (2013), 737–747.
32. Imam, S.Z., Trickler, W., Kimura, S., Binienda, Z.K., Paule, M.G., Slikker, W., Li, S., Clark, R.A., Ali, S.F., Neuroprotective efficacy of a new brain-penetrating C-Abl inhibitor in a Murine Parkinson's disease model. PLoS One, 8, 2013, e65129.
33. Jiang, H., Kang, S.U., Zhang, S., Karuppagounder, S., Xu, J., Lee, Y.K., Kang, B.G., Zhang, J., Pletnikova, O., Troncoso, J.C., Pirooznia, S., Andrabi, S.A., Dawson, V.L., Dawson, T.M., Adult conditional knockout of PGC-1 leads to loss of dopamine neurons. eNeuro, 3, 2016.
34. Karunakaran, S., Diwakar, L., Saeed, U., Agarwal, V., Ramakrishnan, S., Iyengar, S., Ravindranath, V., Activation of apoptosis signal regulating kinase 1 (ASK1) and translocation of death-associated protein, Daxx, in substantia nigra pars compacta in a mouse model of Parkinson's disease: protection by -lipoic acid. FASEB J. 21 (2007), 2226–2236.
35. Karuppagounder, S.S., Brahmachari, S., Lee, Y., Dawson, V.L., Dawson, T.M., Ko, H.S., The c-Abl inhibitor, nilotinib, protects dopaminergic neurons in a preclinical animal model of Parkinson's disease. Sci. Rep., 4, 2014, 4874.
36. Kett, L.R., Dauer, W.T., Endolysosomal dysfunction in Parkinson's disease: recent developments and future challenges. Mov. Disord. 31 (2016), 1433–1443.
37. Kett, L.R., Stiller, B., Bernath, M.M., Tasset, I., Blesa, J., Jackson-Lewis, V., Chan, R.B., Zhou, B., Di Paolo, G., Przedborski, S., Cuervo, A.M., Dauer, W.T., Synuclein-independent histopathological and motor deficits in mice lacking the endolysosomal Parkinsonism protein Atp13a2. J. Neurosci. 35 (2015), 5724–5742.
38. Khandelwal, P., The relationship between parkin and protein aggregation in neurodegenerative diseases. Front. Psychiatry, 1, 2010.
39. Kim, G.H., Kim, J.E., Rhie, S.J., Yoon, S., The role of oxidative stress in neurodegenerative diseases. Exp. Neurobiol. 24 (2015), 325–340.
40. 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.
41. Ko, H.S., Lee, Y., Shin, J.H., Karuppagounder, S.S., Gadad, B.S., Koleske, A.J., Pletnikova, O., Troncoso, J.C., Dawson, V.L., Dawson, T.M., Phosphorylation by the c-Abl protein tyrosine kinase inhibits parkin's ubiquitination and protective function. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 16691–16696.
42. Kostic, M., Ludtmann, Marthe H.R., Bading, H., Hershfinkel, M., Steer, E., Chu, Charleen T., Abramov, Andrey Y., Sekler, I., PKA phosphorylation of NCLX reverses mitochondrial calcium overload and depolarization, promoting survival of PINK1-deficient dopaminergic neurons. Cell Rep. 13 (2015), 376–386.
43. Krebiehl, G., Ruckerbauer, S., Burbulla, L.F., Kieper, N., Maurer, B., Waak, J., Wolburg, H., Gizatullina, Z., Gellerich, F.N., Woitalla, D., Riess, O., Kahle, P.J., Proikas-Cezanne, T., Krüger, R., Reduced basal autophagy and impaired mitochondrial dynamics due to loss of Parkinson's disease-associated protein DJ-1. PLoS One, 5, 2010, e9367.
44. Kuroda, Y., Parkin enhances mitochondrial biogenesis in proliferating cells. Hum. Mol. Genet. 15 (2006), 883–895.
45. Lee, Y., Karuppagounder, S.S., Shin, J.H., Lee, Y.I., Ko, H.S., Swing, D., Jiang, H., Kang, S.U., Lee, B.D., Kang, H.C., Kim, D., Tessarollo, L., Dawson, V.L., Dawson, T.M., Parthanatos mediates AIMP2-activated age-dependent dopaminergic neuronal loss. Nat. Neurosci. 16 (2013), 1392–1400.
46. Lee, Y., Stevens, D.A., Kang, S.-U., Jiang, H., Lee, Y.-I., Ko, H.S., Scarffe, L.A., Umanah, G.E., Kang, H., Ham, S., Kam, T.-I., Allen, K., Brahmachari, S., Kim, J.W., Neifert, S., Yun, S.P., Fiesel, F.C., Springer, W., Dawson, V.L., Shin, J.-H., Dawson, T.M., PINK1 primes parkin-mediated ubiquitination of PARIS in dopaminergic neuronal survival. Cell Rep., 2017.
47. Li, W., Bengtson, M.H., Ulbrich, A., Matsuda, A., Reddy, V.A., Orth, A., Chanda, S.K., Batalov, S., Joazeiro, C.A.P., Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the Organelle's dynamics and signaling. PLoS One, 3, 2008, e1487.
48. Li, X., Wang, H., Gao, Y., Li, L., Tang, C., Wen, G., Zhou, Y., Zhou, M., Mao, L., Fan, Y., Protective effects of Quercetin on mitochondrial biogenesis in experimental traumatic brain injury via the Nrf2 signaling pathway. PLoS One, 11, 2016, e0164237.
49. Lill, C.M., Genetics of Parkinson's disease. Mol. Cell. Probes 30 (2016), 386–396.
50. Lin, W., Kang, U., Structural determinants of PINK1 topology and dual subcellular distribution. BMC Cell Biol., 11, 2010, 90.
51. Liu, S., Sawada, T., Lee, S., Yu, W., Silverio, G., Alapatt, P., Millan, I., Shen, A., Saxton, W., Kanao, T., Takahashi, R., Hattori, N., Imai, Y., Lu, B., Parkinson's disease–associated kinase PINK1 regulates Miro protein level and axonal transport of mitochondria. PLoS Genet., 8, 2012, e1002537.
52. Miki, Y., Tanji, K., Mori, F., Kakita, A., Takahashi, H., Wakabayashi, K., PLA2G6 accumulates in Lewy bodies in PARK14 and idiopathic Parkinson's disease. Neurosci. Lett. 645 (2017), 40–45.
53. Misko, A., Jiang, S., Wegorzewska, I., Milbrandt, J., Baloh, R.H., Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J. Neurosci. 30 (2010), 4232–4240.
54. Moore, D.J., Dawson, V.L., Dawson, T.M., Lessons from Drosophila models of DJ-1 deficiency. Sci. Aging Knowl. Environ., 2006, 2006, pe2.
55. Moore, D.J., West, A.B., Dawson, V.L., Dawson, T.M., Molecular pathophysiology of Parkinson's disease. Annu. Rev. Neurosci. 28 (2005), 57–87.
56. Müftüoglu, M., Elibol, B., Dalmızrak, Ö., Ercan, A., Kulaksız, G., Ögüs, H., Dalkara, T., Özer, N., Mitochondrial complex I and IV activities in leukocytes from patients with parkin mutations. Mov. Disord. 19 (2003), 544–548.
57. Müller-Rischart, Anne K., Pilsl, A., Beaudette, P., Patra, M., Hadian, K., Funke, M., Peis, R., Deinlein, A., Schweimer, C., Kuhn, P.-H., Lichtenthaler, Stefan F., Motori, E., Hrelia, S., Wurst, W., Trümbach, D., Langer, T., Krappmann, D., Dittmar, G., Tatzelt, J., Winklhofer, Konstanze F., The E3 ligase Parkin maintains mitochondrial integrity by increasing linear Ubiquitination of NEMO. Mol. Cell 49 (2013), 908–921.
58. Narendra, D., Tanaka, A., Suen, D.-F., Youle, R.J., Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183 (2008), 795–803.
59. Olgiati, S., Quadri, M., Fang, M., Rood, J.P., Saute, J.A., Chien, H.F., Bouwkamp, C.G., Graafland, J., Minneboo, M., Breedveld, G.J., Zhang, J., International Parkinsonism Genetics, N, Verheijen, F.W., Boon, A.J., Kievit, A.J., Jardim, L.B., Mandemakers, W., Barbosa, E.R., Rieder, C.R., Leenders, K.L., Wang, J., Bonifati, V., DNAJC6 mutations associated with early-onset Parkinson's disease. Ann. Neurol. 79 (2016), 244–256.
60. Park, J.S., Koentjoro, B., Veivers, D., Mackay-Sim, A., Sue, C.M., Parkinson's disease-associated human ATP13A2 (PARK9) deficiency causes zinc dyshomeostasis and mitochondrial dysfunction. Hum. Mol. Genet. 23 (2014), 2802–2815.
61. Periquet, M., Parkin mutations are frequent in patients with isolated early-onset Parkinsonism. Brain 126 (2003), 1271–1278.
62. Pickrell, Alicia M., Youle, Richard J., The roles of PINK1, Parkin, and mitochondrial fidelity in Parkinson's disease. Neuron 85 (2015), 257–273.
63. Pryde, K.R., Smith, H.L., Chau, K.-Y., Schapira, A.H.V., PINK1 disables the anti-fission machinery to segregate damaged mitochondria for mitophagy. J. Cell Biol. 213 (2016), 163–171.
64. Ramirez, A., Heimbach, A., Grundemann, J., Stiller, B., Hampshire, D., Cid, L.P., Goebel, I., Mubaidin, A.F., Wriekat, A.L., Roeper, J., Al-Din, A., Hillmer, A.M., Karsak, M., Liss, B., Woods, C.G., Behrens, M.I., Kubisch, C., Hereditary Parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase. Nat. Genet. 38 (2006), 1184–1191.
65. Ren, H., Fu, K., Mu, C., Li, B., Wang, D., Wang, G., DJ-1, a cancer and Parkinson's disease associated protein, regulates autophagy through JNK pathway in cancer cells. Cancer Lett. 297 (2010), 101–108.
66. Requejo-Aguilar, R., Lopez-Fabuel, I., Jimenez-Blasco, D., Fernandez, E., Almeida, A., Bolaños, Juan P., DJ1 represses glycolysis and cell proliferation by transcriptionally up-regulating pink1. Biochem. J. 467 (2015), 303–310.
67. Ross, J., Brough, D., Gibson, R., Loddick, S., Rothwell, N., A selective, non-peptide caspase-1 inhibitor, VRT-018858, markedly reduces brain damage induced by transient ischemia in the rat. Neuropharmacology 53 (2007), 638–642.
68. Rothfuss, O., Fischer, H., Hasegawa, T., Maisel, M., Leitner, P., Miesel, F., Sharma, M., Bornemann, A., Berg, D., Gasser, T., Patenge, N., Parkin protects mitochondrial genome integrity and supports mitochondrial DNA repair. Hum. Mol. Genet. 18 (2009), 3832–3850.
69. Savitt, J.M., Dawson, V.L., Dawson, T.M., Diagnosis and treatment of Parkinson's disease: molecules to medicine. J. Clin. Invest. 116 (2006), 1744–1754.
70. 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.
71. Shadrach, K.G., Rayborn, M.E., Hollyfield, J.G., Bonilha, V.L., DJ-1-dependent regulation of oxidative stress in the retinal pigment epithelium (RPE). PLoS One, 8, 2013, e67983.
72. Shin, J.-H., Ko, Han S., Kang, H., Lee, Y., Pletinkova, O., Troconso, Juan C., Dawson, Valina L., Dawson, Ted M., PARIS (ZNF746) repression of PGC-1α contributes to neurodegeneration in Parkinson's disease. Cell 144 (2011), 689–702.
73. 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., Shin, J.H., Dawson, T.M., Parkin loss leads to PARIS-dependent declines in mitochondrial mass and respiration. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 11696–11701.
74. Strappazzon, F., Nazio, F., Corrado, M., Cianfanelli, V., Romagnoli, A., Fimia, G.M., Campello, S., Nardacci, R., Piacentini, M., Campanella, M., Cecconi, F., AMBRA1 is able to induce mitophagy via LC3 binding, regardless of PARKIN and p62/SQSTM1. Cell Death Differ. 22 (2015), 419–432.
75. Szargel, R., Shani, V., Abd Elghani, F., Mekies, L.N., Liani, E., Rott, R., Engelender, S., The PINK1, synphilin-1 and SIAH-1 complex constitutes a novel mitophagy pathway. Hum. Mol. Genet. 25 (2016), 3476–3490.
76. Thomas, K.J., McCoy, M.K., Blackinton, J., Beilina, A., van der Brug, M., Sandebring, A., Miller, D., Maric, D., Cedazo-Minguez, A., Cookson, M.R., DJ-1 acts in parallel to the PINK1/parkin pathway to control mitochondrial function and autophagy. Hum. Mol. Genet. 20 (2010), 40–50.
77. Trempe, J.-F., Fon, E.A., Structure and function of Parkin, PINK1, and DJ-1, the three musketeers of neuroprotection. Front. Neurol., 4, 2013.
78. Valente, E.M., Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304 (2004), 1158–1160.
79. Van Humbeeck, C., Cornelissen, T., Hofkens, H., Mandemakers, W., Gevaert, K., De Strooper, B., Vandenberghe, W., Parkin interacts with Ambra1 to induce Mitophagy. J. Neurosci. 31 (2011), 10249–10261.
80. van Veen, S., Sø Rensen, D.M., Holemans, T., Holen, H.W., Palmgren, M.G., Vangheluwe, P., Cellular function and pathological role of ATP13A2 and related p-type transport ATPases in Parkinson's disease and other neurological disorders. Front. Mol. Neurosci., 7, 2014.
81. Vandiver, M.S., Paul, B.D., Xu, R., Karuppagounder, S., Rao, F., Snowman, A.M., Seok Ko, H., Il Lee, Y., Dawson, V.L., Dawson, T.M., Sen, N., Snyder, S.H., Sulfhydration mediates neuroprotective actions of Parkin. Nat. Commun., 4, 2013, 1626.
82. von Coelln, R., Dawson, V.L., Dawson, T.M., Parkin-associated Parkinson's disease. Cell Tissue Res. 318 (2004), 175–184.
83. Wang, H.-L., Chou, A.-H., Wu, A.-S., Chen, S.-Y., Weng, Y.-H., Kao, Y.-C., Yeh, T.-H., Chu, P.-J., Lu, C.-S., PARK6 PINK1 mutants are defective in maintaining mitochondrial membrane potential and inhibiting ROS formation of substantia nigra dopaminergic neurons. Biochim. Biophys. Acta (BBA) - Mol. Basis Dis. 1812 (2011), 674–684.
84. Wang, X., Winter, D., Ashrafi, G., Schlehe, J., Wong, Y.L., Selkoe, D., Rice, S., Steen, J., LaVoie, M.J., Schwarz, T.L., PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 147 (2011), 893–906.
85. Wang, Y., An, R., Umanah, G.K., Park, H., Nambiar, K., Eacker, S.M., Kim, B., Bao, L., Harraz, M.M., Chang, C., Chen, R., Wang, J.E., Kam, T.I., Jeong, J.S., Xie, Z., Neifert, S., Qian, J., Andrabi, S.A., Blackshaw, S., Zhu, H., Song, H., Ming, G.L., Dawson, V.L., Dawson, T.M., A nuclease that mediates cell death induced by DNA damage and poly(ADP-ribose) polymerase-1. Science, 354, 2016.
86. Wang, Y., Serricchio, M., Jauregui, M., Shanbhag, R., Stoltz, T., Di Paolo, C.T., Kim, P.K., McQuibban, G.A., Deubiquitinating enzymes regulate PARK2-mediated mitophagy. Autophagy 11 (2015), 595–606.
87. Xu, Q., Guo, H., Zhang, X., Tang, B., Cai, F., Zhou, W., Song, W., Hypoxia regulation of ATP13A2 (PARK9) gene transcription. J. Neurochem. 122 (2012), 251–259.
88. Yu, W., Sun, Y., Guo, S., Lu, B., The PINK1/Parkin pathway regulates mitochondrial dynamics and function in mammalian hippocampal and dopaminergic neurons. Hum. Mol. Genet. 20 (2011), 3227–3240.
89. Zhang, C.-W., Hang, L., Yao, T.-P., Lim, K.-L., Parkin regulation and neurodegenerative disorders. Front. Aging Neurosci., 7, 2016.
90. Zhang, L., Karsten, P., Hamm, S., Pogson, J.H., Muller-Rischart, A.K., Exner, N., Haass, C., Whitworth, A.J., Winklhofer, K.F., Schulz, J.B., Voigt, A., TRAP1 rescues PINK1 loss-of-function phenotypes. Hum. Mol. Genet. 22 (2013), 2829–2841.
91. 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. 105 (2008), 12022–12027.
92. Zhou, Z.D., Sathiyamoorthy, S., Angeles, D.C., Tan, E.K., Linking f-box protein 7 and parkin to neuronal degeneration in Parkinson's disease (PD). Mol. Brain, 9, 2016.
93. Ziviani, E., Tao, R.N., Whitworth, A.J., Drosophila Parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc. Natl. Acad. Sci. 107 (2010), 5018–5023.