A Ubl/ubiquitin switch in the activation of Parkin

EMBO Journal

Volumn 34, Issue 20, 2015, Pages 2492-2505

  Sauvé, Véronique ^a   Lilov, Asparouh ^a   Seirafi, Marjan ^a   Vranas, Marta ^a   Rasool, Shafqat ^a   Kozlov, Guennadi ^a   Sprules, Tara ^b   Wang, Jimin ^c   Trempe, Jean François ^a   Gehring, Kalle ^a  

^a MCGILL UNIVERSITY   (Canada)

^b Quebec/Eastern Canada High Field NMR Facility   (Canada)

^c YALE UNIVERSITY   (United States)

Author keywords

mitochondria; mitophagy; Parkinson's disease; phosphorylation; ubiquitination

Indexed keywords

PARKIN; RING FINGER PROTEIN; RING1 PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; PROTEIN BINDING; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE; UBE2L3 PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR INTERACTION; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; RING FINGER MOTIF; SIZE EXCLUSION CHROMATOGRAPHY; X RAY CRYSTALLOGRAPHY; CHEMISTRY; CRYSTALLIZATION; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; MOLECULAR CLONING; MOLECULAR MODEL; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; SMALL ANGLE SCATTERING;

CLONING, MOLECULAR; CRYSTALLIZATION; ENZYME ACTIVATION; HUMANS; MITOCHONDRIA; MODELS, MOLECULAR; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SCATTERING, SMALL ANGLE; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES;

EID: 84944441112     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201592237     Document Type: Article

References (54)

1. Ashrafi G, Schlehe JS, LaVoie MJ, Schwarz TL, (2014) Mitophagy of damaged mitochondria occurs locally in distal neuronal axons and requires PINK1 and Parkin. J Cell Biol 206: 655-670
2. Beasley SA, Hristova VA, Shaw GS, (2007) Structure of the Parkin in-between-ring domain provides insights for E3-ligase dysfunction in autosomal recessive Parkinson's disease. Proc Natl Acad Sci USA 104: 3095-3100
3. Caulfield TR, Fiesel FC, Moussaud-Lamodiere EL, Dourado DF, Flores SC, Springer W, (2014) Phosphorylation by PINK1 releases the UBL domain and initializes the conformational opening of the E3 ubiquitin ligase Parkin. PLoS Comput Biol 10: e1003935
4. 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
5. 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
6. Deas E, Plun-Favreau H, Gandhi S, Desmond H, Kjaer S, Loh SH, Renton AE, Harvey RJ, Whitworth AJ, Martins LM, Abramov AY, Wood NW, (2011) PINK1 cleavage at position A103 by the mitochondrial protease PARL. Hum Mol Genet 20: 867-879
7. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A, (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293
8. Emsley P, Lohkamp B, Scott WG, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501
9. Gegg ME, Cooper JM, Chau KY, Rojo M, Schapira AH, Taanman JW, (2010) Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum Mol Genet 19: 4861-4870
10. Geisler S, Holmstrom 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
11. 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
12. 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
13. Jin SM, Youle RJ, (2013) The accumulation of misfolded proteins in the mitochondrial matrix is sensed by PINK1 to induce PARK2/Parkin-mediated mitophagy of polarized mitochondria. Autophagy 9: 1750-1757
14. Kabsch W, (2010a) Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr D Biol Crystallogr 66: 133-144
15. Kabsch W, (2010b) Xds. Acta Crystallogr D Biol Crystallogr 66: 125-132
16. 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
17. Karplus PA, Diederichs K, (2012) Linking crystallographic model and data quality. Science 336: 1030-1033
18. Kazlauskaite A, Kelly V, Johnson C, Baillie C, Hastie CJ, Peggie M, Macartney T, Woodroof HI, Alessi DR, Pedrioli PG, Muqit MM, (2014a) Phosphorylation of Parkin at Serine65 is essential for activation: elaboration of a Miro1 substrate-based assay of Parkin E3 ligase activity. Open Biol 4: 130213
19. Kazlauskaite A, Kondapalli C, Gourlay R, Campbell DG, Ritorto MS, Hofmann K, Alessi DR, Knebel A, Trost M, Muqit MM, (2014b) Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem J 460: 127-139
20. Kazlauskaite A, Martinez-Torres RJ, Wilkie S, Kumar A, Peltier J, Gonzalez A, Johnson C, Zhang J, Hope AG, Peggie M, Trost M, van Aalten DM DM, Alessi DR, Prescott AR, Knebel A, Walden H, Muqit MM, (2015) Binding to serine 65-phosphorylated ubiquitin primes Parkin for optimal PINK1-dependent phosphorylation and activation. EMBO Rep 16: 939-954
21. 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
22. Kondapalli C, Kazlauskaite A, Zhang N, Woodroof HI, Campbell DG, Gourlay R, Burchell L, Walden H, Macartney TJ, Deak M, Knebel A, Alessi DR, Muqit MM, (2012) PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol 2: 120080
23. Koyano F, Okatsu K, Kosako H, Tamura Y, Go E, Kimura M, Kimura Y, Tsuchiya H, Yoshihara H, Hirokawa T, Endo T, Fon EA, Trempe JF, Saeki Y, Tanaka K, Matsuda N, (2014) Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 510: 162-166
24. Martin I, Dawson VL, Dawson TM, (2011) Recent advances in the genetics of Parkinson's disease. Annu Rev Genomics Hum Genet 12: 301-325
25. Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gautier CA, Sou YS, Saiki S, Kawajiri S, Sato F, Kimura M, Komatsu M, Hattori N, Tanaka K, (2010) PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J Cell Biol 189: 211-221
26. 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
27. Meissner C, Lorenz H, Weihofen A, Selkoe DJ, Lemberg MK, (2011) The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking. J Neurochem 117: 856-867
28. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255
29. 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
30. 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
31. Narendra D, Walker JE, Youle R, (2012) Mitochondrial quality control mediated by PINK1 and Parkin: links to parkinsonism. Cold Spring Harb Perspect Biol 4: a011338
32. Okatsu K, Koyano F, Kimura M, Kosako H, Saeki Y, Tanaka K, Matsuda N, (2015) Phosphorylated ubiquitin chain is the genuine Parkin receptor. J Cell Biol 209: 111-128
33. Ordureau A, Sarraf SA, Duda DM, Heo JM, Jedrychowski MP, Sviderskiy VO, Olszewski JL, Koerber JT, Xie T, Beausoleil SA, Wells JA, Gygi SP, Schulman BA, Harper JW, (2014) Quantitative proteomics reveal a feedforward mechanism for mitochondrial PARKIN translocation and ubiquitin chain synthesis. Mol Cell 56: 360-375
34. Ordureau A, Heo JM, Duda DM, Paulo JA, Olszewski JL, Yanishevski D, Rinehart J, Schulman BA, Harper JW, (2015) Defining roles of PARKIN and ubiquitin phosphorylation by PINK1 in mitochondrial quality control using a ubiquitin replacement strategy. Proc Natl Acad Sci USA 112: 6637-6642
35. 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
36. Petoukhov MV, Franke D, Shkumatov AV, Tria G, Kikhney AG, Gajda M, Gorba C, Mertens HD, Konarev PV, Svergun DI, (2012) New developments in the program package for small-angle scattering data analysis. J Appl Crystallogr 45: 342-350
37. Rambo RP, Tainer JA, (2013) Accurate assessment of mass, models and resolution by small-angle scattering. Nature 496: 477-481
38. Riley BE, Lougheed JC, Callaway K, Velasquez M, Brecht E, Nguyen L, Shaler T, Walker D, Yang Y, Regnstrom K, Diep L, Zhang Z, Chiou S, Bova M, Artis DR, Yao N, Baker J, Yednock T, Johnston JA, (2013) Structure and function of Parkin E3 ubiquitin ligase reveals aspects of RING and HECT ligases. Nat Commun 4: 1982
39. Serniwka SA, Shaw GS, (2008) 1H, 13C and 15N resonance assignments for the human E2 conjugating enzyme, UbcH7. Biomol NMR Assign 2: 21-23
40. 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
41. Svergun DI, (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Cryst 25: 495-503
42. Svergun D, Barberato C, Koch MHJ, (1995) CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atom ic coordinates. J Appl Cryst 28: 768-773
43. Tanaka A, Cleland MM, Xu S, Narendra DP, Suen DF, Karbowski M, Youle RJ, (2010) Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol 191: 1367-1380
44. Trempe JF, Sauve V, Grenier K, Seirafi M, Tang MY, Menade M, Al-Abdul-Wahid S, Krett J, Wong K, Kozlov G, Nagar B, Fon EA, Gehring K, (2013) Structure of parkin reveals mechanisms for ubiquitin ligase activation. Science 340: 1451-1455
45. Vagin A, Teplyakov A, (2010) Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr 66: 22-25
46. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, Albanese A, Nussbaum R, Gonzalez-Maldonado R, Deller T, Salvi S, Cortelli P, Gilks WP, Latchman DS, Harvey RJ, Dallapiccola B, et al, (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304: 1158-1160
47. Wang X, Winter D, Ashrafi G, Schlehe J, Wong YL, Selkoe D, Rice S, Steen J, LaVoie MJ, Schwarz TL, (2011) PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 147: 893-906
48. Wauer T, Komander D, (2013) Structure of the human Parkin ligase domain in an autoinhibited state. EMBO J 32: 2099-2112
49. Wauer T, Simicek M, Schubert A, Komander D, (2015a) Mechanism of phospho-ubiquitin-induced PARKIN activation. Nature 524: 370-374
50. Wauer T, Swatek KN, Wagstaff JL, Gladkova C, Pruneda JN, Michel MA, Gersch M, Johnson CM, Freund SM, Komander D, (2015b) Ubiquitin Ser65 phosphorylation affects ubiquitin structure, chain assembly and hydrolysis. EMBO J 34: 307-325
51. 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
52. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS, (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235-242
53. 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
54. Ziviani E, Tao RN, Whitworth AJ, (2010) Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc Natl Acad Sci USA 107: 5018-5023