PINK1-Mediated Phosphorylation of Parkin Boosts Parkin Activity in Drosophila

PLoS Genetics

Volumn 10, Issue 6, 2014, Pages

  Shiba Fukushima, Kahori ^a   Inoshita, Tsuyoshi ^a   Hattori, Nobutaka ^a   Imai, Yuzuru ^a  

^a JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; MIRO PROTEIN; MITOCHONDRIAL PROTEIN; MITOFUSIN; OUTER MEMBRANE PROTEIN; PARKIN; PINK1 PROTEIN; PROTEIN KINASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; MEMBRANE PROTEIN; MFN2 PROTEIN, DROSOPHILA; MIRO PROTEIN, DROSOPHILA; PARKIN PROTEIN, DROSOPHILA; PINK1 PROTEIN, DROSOPHILA; PROTEIN SERINE THREONINE KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UBIQUITIN PROTEIN LIGASE;

ADULT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL DEGENERATION; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; DROSOPHILA; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; LIFESPAN; MALE; MITOCHONDRIAL RESPIRATION; MUSCLE FUNCTION; MUSCLE MITOCHONDRION; NONHUMAN; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; WILD TYPE; ANIMAL; BIOSYNTHESIS; DROSOPHILA MELANOGASTER; FORELIMB; GENETICS; INNERVATION; METABOLISM; MITOCHONDRION; PARKINSON DISEASE; PATHOLOGY; PHOSPHORYLATION; SKELETAL MUSCLE; TRANSGENIC ANIMAL; UBIQUITINATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ELECTRON TRANSPORT COMPLEX I; MEMBRANE PROTEINS; MITOCHONDRIA; MUSCLE, SKELETAL; PARKINSON DISEASE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RHO GTP-BINDING PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; WING;

EID: 84903485895     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004391     Document Type: Article

References (48)

1. 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.
2. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, et al. (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304: 1158-1160.
3. Imai Y, Soda M, Takahashi R, (2000) Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity. J Biol Chem 275: 35661-35664.
4. Shimura H, Hattori N, Kubo S, Mizuno Y, Asakawa S, et al. (2000) Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat Genet 25: 302-305.
5. Zhang Y, Gao J, Chung KK, Huang H, Dawson VL, et al. (2000) Parkin functions as an E2-dependent ubiquitin- protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc Natl Acad Sci U S A 97: 13354-13359.
6. Silvestri L, Caputo V, Bellacchio E, Atorino L, Dallapiccola B, et al. (2005) Mitochondrial import and enzymatic activity of PINK1 mutants associated to recessive parkinsonism. Hum Mol Genet 14: 3477-3492.
7. Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, et al. (2003) Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci U S A 100: 4078-4083.
8. Pesah Y, Pham T, Burgess H, Middlebrooks B, Verstreken P, et al. (2004) Drosophila parkin mutants have decreased mass and cell size and increased sensitivity to oxygen radical stress. Development 131: 2183-2194.
9. Clark IE, Dodson MW, Jiang C, Cao JH, Huh JR, et al. (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441: 1162-1166.
10. Park J, Lee SB, Lee S, Kim Y, Song S, et al. (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441: 1157-1161.
11. Yang Y, Gehrke S, Imai Y, Huang Z, Ouyang Y, et al. (2006) Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc Natl Acad Sci U S A 103: 10793-10798.
12. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, et al. (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A 107: 378-383.
13. Geisler S, Holmstrom KM, Skujat D, Fiesel FC, Rothfuss OC, et al. (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 12: 119-131.
14. Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, 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.
15. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, et al. (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 8: e1000298.
16. Kawajiri S, Saiki S, Sato S, Sato F, Hatano T, et al. (2010) PINK1 is recruited to mitochondria with parkin and associates with LC3 in mitophagy. FEBS Lett 584: 1073-1079.
17. Okatsu K, Oka T, Iguchi M, Imamura K, Kosako H, et al. (2012) PINK1 autophosphorylation upon membrane potential dissipation is essential for Parkin recruitment to damaged mitochondria. Nat Commun 3: 1016.
18. Tanaka A, Cleland MM, Xu S, Narendra DP, Suen DF, et al. (2010) Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol 191: 1367-1380.
19. Rakovic A, Grunewald A, Kottwitz J, Bruggemann N, Pramstaller PP, et al. (2011) Mutations in PINK1 and Parkin impair ubiquitination of Mitofusins in human fibroblasts. PLoS One 6: e16746.
20. Liu S, Sawada T, Lee S, Yu W, Silverio G, et al. (2012) Parkinson's disease-associated kinase PINK1 regulates Miro protein level and axonal transport of mitochondria. PLoS Genet 8: e1002537.
21. Wang X, Winter D, Ashrafi G, Schlehe J, Wong YL, et al. (2011) PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 147: 893-906.
22. Shiba-Fukushima K, Imai Y, Yoshida S, Ishihama Y, Kanao T, et al. (2012) PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci Rep 2: 1002.
23. Kondapalli C, Kazlauskaite A, Zhang N, Woodroof HI, Campbell DG, 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.
24. Rana A, Rera M, Walker DW, (2013) Parkin overexpression during aging reduces proteotoxicity, alters mitochondrial dynamics, and extends lifespan. Proc Natl Acad Sci U S A 110: 8638-8643.
25. Ziviani E, Tao RN, Whitworth AJ, (2010) Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc Natl Acad Sci U S A 107: 5018-5023.
26. Poole AC, Thomas RE, Yu S, Vincow ES, Pallanck L, (2010) The mitochondrial fusion-promoting factor mitofusin is a substrate of the PINK1/parkin pathway. PLoS One 5: e10054.
27. Gandhi S, Wood-Kaczmar A, Yao Z, Plun-Favreau H, Deas E, et al. (2009) PINK1-associated Parkinson's disease is caused by neuronal vulnerability to calcium-induced cell death. Mol Cell 33: 627-638.
28. Wu Z, Sawada T, Shiba K, Liu S, Kanao T, et al. (2013) Tricornered/NDR kinase signaling mediates PINK1-directed mitochondrial quality control and tissue maintenance. Genes Dev 27: 157-162.
29. Pimenta de Castro I, Costa AC, Lam D, Tufi R, Fedele V, et al. (2012) Genetic analysis of mitochondrial protein misfolding in Drosophila melanogaster. Cell Death Differ 19: 1308-1316.
30. Yang Y, Ouyang Y, Yang L, Beal MF, McQuibban A, et al. (2008) Pink1 regulates mitochondrial dynamics through interaction with the fission/fusion machinery. Proc Natl Acad Sci U S A 105: 7070-7075.
31. Wu TH, Lu YN, Chuang CL, Wu CL, Chiang AS, et al. (2013) Loss of vesicular dopamine release precedes tauopathy in degenerative dopaminergic neurons in a Drosophila model expressing human tau. Acta Neuropathol 125: 711-725.
32. Iguchi M, Kujuro Y, Okatsu K, Koyano F, Kosako H, et al. (2013) Parkin-catalyzed Ubiquitin-Ester Transfer Is Triggered by PINK1-dependent Phosphorylation. J Biol Chem 288: 22019-22032.
33. Vincow ES, Merrihew G, Thomas RE, Shulman NJ, Beyer RP, et al. (2013) The PINK1-Parkin pathway promotes both mitophagy and selective respiratory chain turnover in vivo. Proc Natl Acad Sci U S A 110: 6400-6405.
34. Lazarou M, Narendra DP, Jin SM, Tekle E, Banerjee S, et al. (2013) PINK1 drives Parkin self-association and HECT-like E3 activity upstream of mitochondrial binding. J Cell Biol 200: 163-172.
35. Sato S, Chiba T, Nishiyama S, Kakiuchi T, Tsukada H, et al. (2006) Decline of striatal dopamine release in parkin-deficient mice shown by ex vivo autoradiography. J Neurosci Res 84: 1350-1357.
36. Kitada T, Pisani A, Karouani M, Haburcak M, Martella G, et al. (2009) Impaired dopamine release and synaptic plasticity in the striatum of parkin-/- mice. J Neurochem 110: 613-621.
37. Oyama G, Yoshimi K, Natori S, Chikaoka Y, Ren YR, et al. (2010) Impaired in vivo dopamine release in parkin knockout mice. Brain Res 1352: 214-222.
38. Kitada T, Pisani A, Porter DR, Yamaguchi H, Tscherter A, et al. (2007) Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc Natl Acad Sci U S A 104: 11441-11446.
39. Fallon L, Belanger CM, Corera AT, Kontogiannea M, Regan-Klapisz E, et al. (2006) A regulated interaction with the UIM protein Eps15 implicates parkin in EGF receptor trafficking and PI(3)K-Akt signalling. Nat Cell Biol 8: 834-842.
40. Lu XH, Fleming SM, Meurers B, Ackerson LC, Mortazavi F, et al. (2009) Bacterial artificial chromosome transgenic mice expressing a truncated mutant parkin exhibit age-dependent hypokinetic motor deficits, dopaminergic neuron degeneration, and accumulation of proteinase K-resistant alpha-synuclein. J Neurosci 29: 1962-1976.
41. Riemensperger T, Isabel G, Coulom H, Neuser K, Seugnet L, et al. (2011) Behavioral consequences of dopamine deficiency in the Drosophila central nervous system. Proc Natl Acad Sci U S A 108: 834-839.
42. Hindle S, Afsari F, Stark M, Middleton CA, Evans GJ, et al. (2013) Dopaminergic expression of the Parkinsonian gene LRRK2-G2019S leads to non-autonomous visual neurodegeneration, accelerated by increased neural demands for energy. Hum Mol Genet 22: 2129-2140.
43. MacLeod DA, Rhinn H, Kuwahara T, Zolin A, Di Paolo G, et al. (2013) RAB7L1 interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson's disease risk. Neuron 77: 425-439.
44. Tricoire H, Battisti V, Trannoy S, Lasbleiz C, Pret AM, et al. (2009) The steroid hormone receptor EcR finely modulates Drosophila lifespan during adulthood in a sex-specific manner. Mech Ageing Dev 130: 547-552.
45. Shiba K, Arai T, Sato S, Kubo S, Ohba Y, et al. (2009) Parkin stabilizes PINK1 through direct interaction. Biochem Biophys Res Commun 383: 331-335.
46. Imai Y, Kanao T, Sawada T, Kobayashi Y, Moriwaki Y, et al. (2010) The loss of PGAM5 suppresses the mitochondrial degeneration caused by inactivation of PINK1 in Drosophila. PLoS Genet 6: e1001229.
47. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF, (1994) Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol A 175: 179-191.
48. Imai Y, Gehrke S, Wang HQ, Takahashi R, Hasegawa K, et al. (2008) Phosphorylation of 4E-BP by LRRK2 affects the maintenance of dopaminergic neurons in Drosophila. EMBO J 27: 2432-2443.