PINK1 and Parkin - Mitochondrial interplay between phosphorylation and ubiquitylation in Parkinson's disease

FEBS Journal

Volumn 282, Issue 2, 2015, Pages 215-223

  Kazlauskaite, Agne ^a   Muqit, Miratul M K ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

kinase; mitochondria; parkin; Parkinson's disease; PINK1; ubiquitin

Indexed keywords

PARKIN; PROTEIN PINK1; PROTEIN SERINE KINASE; UNCLASSIFIED DRUG; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

AUTOPHOSPHORYLATION; BINDING AFFINITY; BINDING SITE; CELL DAMAGE; ENZYME ACTIVITY; HUMAN; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MITOPHAGY; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; UBIQUITINATION; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION; NERVE DEGENERATION; PATHOLOGY; PHOSPHORYLATION;

HUMANS; MITOCHONDRIA; MUTATION; NERVE DEGENERATION; PARKINSON DISEASE; PHOSPHORYLATION; PROTEIN KINASES; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84925940926     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13127     Document Type: Review

References (59)

1. Schulz JB, &, Beal MF, (1994) Mitochondrial dysfunction in movement disorders. Curr Opin Neurol 7, 333-339.
2. Langston JW, Ballard P, Tetrud JW, &, Irwin I, (1983) Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219, 979-980.
3. Nicklas WJ, Vyas I, &, Heikkila RE, (1985) Inhibition of NADH-linked oxidation in brain mitochondria by 1-methyl-4-phenyl-pyridine, a metabolite of the neurotoxin, 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. Life Sci 36, 2503-2508.
4. Mizuno Y, Ohta S, Tanaka M, Takamiya S, Suzuki K, Sato T, Oya H, Ozawa T, &, Kagawa Y, (1989) Deficiencies in complex I subunits of the respiratory chain in Parkinson's disease. Biochem Biophys Res Commun 163, 1450-1455.
5. Schapira AH, Cooper JM, Dexter D, Jenner P, Clark JB, &, Marsden CD, (1989) Mitochondrial complex I deficiency in Parkinson's disease. Lancet 1, 1269.
6. Beal MF, (1995) Aging, energy, and oxidative stress in neurodegenerative diseases. Ann Neurol 38, 357-366.
7. Singleton AB, Farrer MJ, &, Bonifati V, (2013) The genetics of Parkinson's disease: progress and therapeutic implications. Mov Disord 28, 14-23.
8. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, &, Healy DG, et al,. (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304, 1158-1160.
9. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, &, Shimizu N, (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605-608.
10. Cohen P, (2002) The origins of protein phosphorylation. Nat Cell Biol 4, E127-E130.
11. Cohen P, (2002) Protein kinases-the major drug targets of the twenty-first century? Nat Rev Drug Discovery 1, 309-315.
12. Lazarou M, Jin SM, Kane LA, &, Youle RJ, (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.
13. Deas E, Plun-Favreau H, Gandhi S, Desmond H, Kjaer S, Loh SH, Renton AE, Harvey RJ, Whitworth AJ, &, Martins LM, et al,. (2011) PINK1 cleavage at position A103 by the mitochondrial protease PARL. Hum Mol Genet 20, 867-879.
14. Jin SM, Lazarou M, Wang C, Kane LA, Narendra DP, &, Youle RJ, (2010) Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J Cell Biol 191, 933-942.
15. Whitworth AJ, Lee JR, Ho VM, Flick R, Chowdhury R, &, McQuibban GA, (2008) Rhomboid-7 and HtrA2/Omi act in a common pathway with the Parkinson's disease factors Pink1 and Parkin. Dis Model Mech, 1, 168-174. discussion 173.
16. Greene AW, Grenier K, Aguileta MA, Muise S, Farazifard R, Haque ME, McBride HM, Park DS, &, Fon EA, (2012) Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep 13, 378-385.
17. Yamano K, &, Youle RJ, (2013) PINK1 is degraded through the N-end rule pathway. Autophagy 9, 1758-1769.
18. Lin W, &, Kang UJ, (2008) Characterization of PINK1 processing, stability, and subcellular localization. J Neurochem 106, 464-474.
19. Zhou C, Huang Y, Shao Y, May J, Prou D, Perier C, Dauer W, Schon EA, &, Przedborski S, (2008) The kinase domain of mitochondrial PINK1 faces the cytoplasm. Proc Natl Acad Sci USA 105, 12022-12027.
20. Kondapalli C, Kazlauskaite A, Zhang N, Woodroof HI, Campbell DG, Gourlay R, Burchell L, Walden H, Macartney TJ, &, 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.
21. Okatsu K, Oka T, Iguchi M, Imamura K, Kosako H, Tani N, Kimura M, Go E, Koyano F, &, Funayama M, et al,. (2012) PINK1 autophosphorylation upon membrane potential dissipation is essential for Parkin recruitment to damaged mitochondria. Nat Commun 3, 1016.
22. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, &, Youle RJ, (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 8, e1000298.
23. Geisler S, Holmström KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, &, Springer W, (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 12, 119-131.
24. Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gautier CA, Sou YS, 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.
25. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J, May J, Tocilescu MA, Liu W, &, Ko HS, et al,. (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci USA 107, 378-383.
26. Nolen B, Taylor S, &, Ghosh G, (2004) Regulation of protein kinases; controlling activity through activation segment conformation. Mol Cell 15, 661-675.
27. Gandhi S, Wood-Kaczmar A, Yao Z, Plun-Favreau H, Deas E, Klupsch K, Downward J, Latchman DS, Tabrizi SJ, &, Wood NW, et al,. (2009) PINK1-associated Parkinson's disease is caused by neuronal vulnerability to calcium-induced cell death. Mol Cell 33, 627-638.
28. Peng YY, (1998) Effects of mitochondrion on calcium transients at intact presynaptic terminals depend on frequency of nerve firing. J Neurophysiol 80, 186-195.
29. Lücking CB, Dürr A, Bonifati V, Vaughan J, De Michele G, Gasser T, Harhangi BS, Meco G, Denèfle P, &, Wood NW, et al,. (2000) Association between early-onset Parkinson's disease and mutations in the parkin gene. N Engl J Med 342, 1560-1567.
30. Walden H, &, Martinez-Torres RJ, (2012) Regulation of Parkin E3 ubiquitin ligase activity. Cell Mol Life Sci 69, 3053-3067.
31. Spratt DE, Walden H, &, Shaw GS, (2014) RBR E3 ubiquitin ligases: new structures, new insights, new questions. Biochem J 458, 421-437.
32. Wenzel DM, Lissounov A, Brzovic PS, &, Klevit RE, (2011) UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids. Nature 474, 105-108.
33. Chaugule VK, Burchell L, Barber KR, Sidhu A, Leslie SJ, Shaw GS, &, Walden H, (2011) Autoregulation of Parkin activity through its ubiquitin-like domain. EMBO J 30, 2853-2867.
34. Riley BE, Lougheed JC, Callaway K, Velasquez M, Brecht E, Nguyen L, Shaler T, Walker D, Yang Y, &, Regnstrom K, et al,. (2013) Structure and function of Parkin E3 ubiquitin ligase reveals aspects of RING and HECT ligases. Nat Commun 4, 1982.
35. Trempe JF, Sauvé V, Grenier K, Seirafi M, Tang MY, Ménade M, Al-Abdul-Wahid S, Krett J, Wong K, &, Kozlov G, et al,. (2013) Structure of parkin reveals mechanisms for ubiquitin ligase activation. Science 340, 1451-1455.
36. Wauer T, &, Komander D, (2013) Structure of the human Parkin ligase domain in an autoinhibited state. EMBO J 32, 2099-3112.
37. Khan NL, Valente EM, Bentivoglio AR, Wood NW, Albanese A, Brooks DJ, &, Piccini P, (2002) Clinical and subclinical dopaminergic dysfunction in PARK6-linked parkinsonism: an 18F-dopa PET study. Ann Neurol 52, 849-853.
38. Clark IE, Dodson MW, Jiang C, Cao JH, Huh JR, Seol JH, Yoo SJ, Hay BA, &, Guo M, (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441, 1162-1166.
39. Park J, Lee SB, Lee S, Kim Y, Song S, Kim S, Bae E, Kim J, Shong M, Kim JM, &, Chung J, (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441, 1157-1161.
40. Darios F, Corti O, Lücking CB, Hampe C, Muriel MP, Abbas N, Gu WJ, Hirsch EC, Rooney T, Ruberg M, &, Brice A, (2003) Parkin prevents mitochondrial swelling and cytochrome c release in mitochondria-dependent cell death. Hum Mol Genet 12, 517-526.
41. Narendra D, Tanaka A, Suen DF, &, Youle RJ, (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183, 795-803.
42. Woodroof HI, Pogson JH, Begley M, Cantley LC, Deak M, Campbell DG, van Aalten DM, Whitworth AJ, Alessi DR, &, Muqit MM, (2011) Discovery of catalytically active orthologues of the Parkinson's disease kinase PINK1: analysis of substrate specificity and impact of mutations. Open Biol 1, 110012.
43. Shiba-Fukushima K, Imai Y, Yoshida S, Ishihama Y, Kanao T, Sato S, &, Hattori N, (2012) PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci Rep 2, 1002.
44. Kazlauskaite A, Kondapalli C, Gourlay R, Campbell DG, Ritorto MS, Hofmann K, Alessi DR, Knebel A, Trost M, &, Muqit MM, (2014) Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem J 460, 127-139.
45. Kane LA, Lazarou M, Fogel AI, Li Y, Yamano K, Sarraf SA, Banerjee S, &, Youle RJ, (2014) PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J Cell Biol 205, 143-153.
46. Koyano F, Okatsu K, Kosako H, Tamura Y, Go E, Kimura M, Kimura Y, Tsuchiya H, Yoshihara H, &, Hirokawa T, et al,. (2014) Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 510, 162-166.
47. Sarraf SA, Raman M, Guarani-Pereira V, Sowa ME, Huttlin EL, Gygi SP, &, Harper JW, (2013) Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature 496, 372-376.
48. Chan NC, Salazar AM, Pham AH, Sweredoski MJ, Kolawa NJ, Graham RL, Hess S, &, Chan DC, (2011) Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum Mol Genet 20, 1726-1737.
49. Allen GF, Toth R, James J, &, Ganley IG, (2013) Loss of iron triggers PINK1/Parkin-independent mitophagy. EMBO Rep 14, 1127-1135.
50. McLelland GL, Soubannier V, Chen CX, McBride HM, &, Fon EA, (2014) Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control. EMBO J 33, 282-295.
51. Kazlauskaite A, Kelly V, Johnson C, Baillie C, Peggie M, Hastie CJ, Macartney T, Woodroof HI, Alessi DR, Pedrioli PG, et al,. (2014) Phosphorylation of Parkin at Serine65 is essential for activation: elaboration of a Miro1substrate-based assay of Parkin E3 ligase activity. Open Biol 4, 130213.
52. Schwarz TL, (2013) Mitochondrial trafficking in neurons. Cold Spring Harb Perspect Biol 5, a011304.
53. Cornelissen T, Haddad D, Wauters F, Van Humbeeck C, Mandemakers W, Koentjoro B, Sue C, Gevaert K, De Strooper B, &, Verstreken P, et al,. (2014) The deubiquitinase USP15 antagonizes Parkin-mediated mitochondrial ubiquitination and mitophagy. Hum Mol Genet 23, 5227-5242.
54. Bingol B, Tea JS, Phu L, Reichelt M, Bakalarski CE, Song Q, Foreman O, Kirkpatrick DS, &, Sheng M, (2014) The mitochondrial deubiquitinase USP30 opposes parkin-mediated mitophagy. Nature 509, 370-375.
55. Dave KD, De Silva S, Sheth NP, Ramboz S, Beck MJ, Quang C, Switzer RC III, Ahmad SO, Sunkin SM, &, Walker D, et al,. (2014) Phenotypic characterization of recessive gene knockout rat models of Parkinson's disease. Neurobiol Dis, 70, 190-203.
56. Liang H, He S, Yang J, Jia X, Wang P, Chen X, Zhang Z, Zou X, McNutt MA, &, Shen WH, et al,. (2014) PTENalpha, a PTEN isoform translated through alternative initiation, regulates mitochondrial function and energy metabolism. Cell Metab 19, 836-848.
57. Gong Y, Zack TI, Morris LG, Lin K, Hukkelhoven E, Raheja R, Tan IL, Turcan S, Veeriah S, &, Meng S, et al,. (2010) Somatic mutations of the Parkinson's disease-associated gene PARK2 in glioblastoma and other human malignancies. Nat Genet 42, 77-82.
58. O'Flanagan CH, Morais VA, Wurst W, De Strooper B, &, O'Neill C, (2014) The Parkinson's gene PINK1 regulates cell cycle progression and promotes cancer-associated phenotypes. Oncogene doi: 10.1038/onc.2014.81.
59. Deas E, Piipari K, Machhada A, Li A, Gutierrez-del-Arroyo A, Withers DJ, Wood NW, &, Abramov AY, (2014) PINK1 deficiency in beta-cells increases basal insulin secretion and improves glucose tolerance in mice. Open Biol 4, 140051.