Structure of the human Parkin ligase domain in an autoinhibited state

EMBO Journal

Volumn 32, Issue 15, 2013, Pages 2099-2112

  Wauer, Tobias ^a   Komander, David ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

E3 ligase; neurodegenerative disease; Parkin; ubiquitin; X ray crystallography

Indexed keywords

PARKIN;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STRUCTURE; PRIORITY JOURNAL;

CRYSTALLOGRAPHY, X-RAY; HUMANS; MUTATION; PARKINSON DISEASE; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; UBIQUITIN-PROTEIN LIGASES; URIDINE DIPHOSPHATE; ZINC;

EID: 84881477223     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.125     Document Type: Article

References (76)

1. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Echols N, Headd JJ, Hung L-W, Jain S, Kapral GJ, Grosse Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner RD, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2011) The Phenix software for automated determination of macromolecular structures. Methods 55: 94-106
2. Aguilera M, Oliveros M, Mart́inez-Padrón M, Barbas JA, Ferrús A (2000) Ariadne-1: a vital Drosophila gene is required in development and defines a new conserved family of ring-finger proteins. Genetics 155: 1231-1244
3. Akutsu M, Ye Y, Virdee S, Chin JW, Komander D (2011) Molecular basis for ubiquitin and ISG15 cross-reactivity in viral ovarian tumor domains. Proc Natl Acad Sci 108: 2228-2233
4. 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
5. Berrow NS, Alderton D, Sainbury S, Nettkeship J, Assenberg R, Rahman N, Stuart DI, Owens RJ (2007) A versatile ligation-independent cloning method suitable for high-throughput expression screening applications. Nucleic acids research 35, e45
6. Biondi RM, Komander D, Thomas CC, Lizcano JM, Deak M, Alessi DR, van Aalten DM (2002) High resolution crystal structure of the human PDK1 catalytic domain defines the regulatory phospho-peptide docking site. EMBO J 21: 4219-4248
7. Bonifati V, Rizzu P, van Baren MJ, Schaap O, Breedveld GJ, Krieger E, Dekker MCJ, Squitieri F, Ibanez P, Joosse M, van Dongen JW, Vanacore N, van Swieten JC, Brice A, Meco G, van Duijn CM, Oostra BA, Heutink P (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinson-ism. Science 299: 256-259
8. Borodovsky A, Ovaa H, Kolli N, Gan-Erdene T, Wilkinson KD, Ploegh HL, Kessler BM (2002) Chemistry-based functional pro-teomics reveals novel members of the deubiquitinating enzyme family. Chem Biol 9: 1149-1159
9. Capili AD, Edghill EL, Wu K, Borden KLB (2004) Structure of the C-terminal RING finger from a RING-IBR-RING/TRIAD motif reveals a novel zinc-binding domain distinct from a RING. J Mol Biol 340: 1117-1129
10. Cha G-H, Kim S, Park J, Lee E, Kim M, Lee SB, Kim J-M, Chung J, Cho KS (2005) Parkin negatively regulates JNK pathway in the dopaminergic neurons of Drosophila. Proc Natl Acad Sci USA 102: 10345-10350
11. 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
12. Chen Y, Dorn GW (2013) PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science 340: 471-475
13. Chew KCM, Matsuda N, Saisho K, Lim GGY, Chai C, Tan H-M, Tanaka K, Lim KL (2011) Parkin mediates apparent E2-indepen-dent monoubiquitination in vitro and contains an intrinsic activity that catalyzes polyubiquitination. PLoS ONE 6: e19720
14. Corti O, Hampe C, Koutnikova H, Darios F, Jacquier S, Prigent A, Robinson J-C, Pradier L, Ruberg M, Mirande M, Hirsch E, Rooney T, Fournier A, Brice A (2003) The p38 subunit of the aminoacyl-tRNA synthetase complex is a Parkin substrate: linking protein biosynthesis and neurodegeneration. Hum Mol Genet 12: 1427-1437
15. Corti O, Lesage S, Brice A (2011) What genetics tells us about the causes and mechanisms of Parkinson's disease. Physiol Rev 91: 1161-1218
16. Dou H, Buetow L, Sibbet GJ, Cameron K, Huang DT (2012) BIRC7-E2 ubiquitin conjugate structure reveals the mechanism of ubi-quitin transfer by a RING dimer. Nat Struct Mol Biol 19: 876-883
17. Dye BT, Schulman BA (2007) Structural mechanisms underlying posttranslational modification by ubiquitin-like proteins. Annu Rev Biophys Biomol Struct 36: 131-150
18. Eisenhaber B, Chumak N, Eisenhaber F, Hauser M-T (2007) The ring between ring fingers (RBR) protein family. Genome Biol 8: 209
19. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501
20. 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
21. Goedert M, Spillantini MG, Del Tredici K, Braak H (2013) 100 years of Lewy pathology. Nat Rev Neurol 9: 13-24
22. Gu W-J, Corti O, Araujo F, Hampe C, Jacquier S, Lücking CB, Abbas N, Duyckaerts C, Rooney T, Pradier L, Ruberg M, Brice A (2003) The C289G and C418R missense mutations cause rapid sequestration of human Parkin into insoluble aggregates. Neurobiol Dis 14: 357-364
23. Hampe C, Ardila-Osorio H, Fournier M, Brice A, Corti O (2006) Biochemical analysis of Parkinson's disease-causing variants of Parkin, an E3 ubiquitin-protein ligase with monoubiquitylation capacity. Hum Mol Genet 15: 2059-2075
24. Henn IH, Bouman L, Schlehe JS, Schlierf A, Schramm JE, Wegener E, Nakaso K, Culmsee C, Berninger B, Krappmann D, Tatzelt J, Winklhofer KF (2007) Parkin mediates neuroprotection through activation of IkappaB kinase/nuclear factor-kappaB signaling. J. Neurosci 27: 1868-1878
25. Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67: 425-479
26. Hoeller D, Hecker C-M, Wagner S, Rogov V, Dötsch V, Dikic I (2007) E3-independent monoubiquitination of ubiquitin-binding proteins. Mol Cell 26: 891-898
27. Hristova VA, Beasley SA, Rylett RJ, Shaw GS (2009) Identification of a novel Zn2 +-binding domain in the autosomal recessive juvenile Parkinson-related E3 ligase parkin. J Biol Chem 284: 14978-14986
28. Kirisako T, Kamei K, Murata S, Kato M, Fukumoto H, Kanie M, Sano S, Tokunaga F, Tanaka K, Iwai K (2006) A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J 25: 4877-4887
29. 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
30. Komander D, Rape M (2012) The ubiquitin code. Annu Rev Biochem 81: 203-229
31. Komander D, Clague MJ, Urbé S (2009) Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10: 550-563
32. 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 MMK (2012) PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol 2: 120080
33. Langer G, Cohen SX, Lamzin VS, Perrakis A (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 3: 1171-1179
34. Lazarou M, Narendra DP, Jin SM, Tekle E, Banerjee S, Youle RJ (2013) PINK1 drives Parkin self-association and HECT-like E3 activity upstream of mitochondrial binding. J Cell Biol 200: 163-172
35. Lima CD, Schulman BA (2012) Structural biology: a protein engagement RING. Nature 489: 43-44
36. Maŕin I (2009) RBR ubiquitin ligases: diversification and streamlining in animal lineages. J Mol Evol 69: 54-64
37. Matsuda N, Kitami T, Suzuki T, Mizuno Y, Hattori N, Tanaka K (2006) Diverse effects of pathogenic mutations of Parkin that catalyze multiple monoubiquitylation in vitro. J Biol Chem 281: 3204-3209
38. Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gautier CA, Sou Y-S, 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
39. Moynihan TP, Ardley HC, Nuber U, Rose SA, Jones PF, Markham AF, Scheffner M, Robinson PA (1999) The ubiquitin-conjugating enzymes UbcH7 and UbcH8 interact with RING finger/IBR motif-containing domains of HHARI and H7-AP1. J Biol Chem 274: 30963-30968
40. Müller-Rischart AK, Pilsl A, Beaudette P, Patra M, Hadian K, Funke M, Peis R, Deinlein A, Schweimer C, Kuhn PH, Linchtenthaler SF, Motori E, Hrelia S, Wurst W, Trümbach D, Langer T, Krappmann D, Dittmar G, Tatzelt J, Winklhofer KF (2013) The E3 ligase parkin maintains mitochondrial integrity by increasing linear ubiquitination of NEMO. Mol Cell 149: 908-921
41. Narendra D, Walker JE, Youle R (2012) Mitochondrial quality control mediated by PINK1 and Parkin: links to parkinsonism. Cold Spring Harb Perspect Biol 4: pii: a011338
42. Narendra DP, Jin SM, Tanaka A, Suen D-F, Gautier CA, Shen J, Cookson MR, Youle RJ (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 8: e1000298
43. Okatsu K, Oka T, Iguchi M, Imamura K, Kosako H, Tani N, Kimura M, Go E, Koyano F, Funayama M, Shiba-Fukushima K, Sato S, Shimizu H, Fukunaga Y, Taniguchi H, Komatsu M, Hattori N, Mihara K, Tanaka K, Matsuda N (2012) PINK1 autophosphorylation upon membrane potential dissipation is essential for Parkin recruitment to damaged mitochondria. Nat Commun 3: 1016
44. Plechanovova A, Jaffray EG, Tatham MH, Naismith JH, Hay RT (2012) Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis. Nature 489: 115-120
45. 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
46. Poulogiannis G, McIntyre RE, Dimitriadi M, Apps JR, Wilson CH, Ichimura K, Luo F, Cantley LC, Wyllie AH, Adams DJ, Arends MJ (2010) PARK2 deletions occur frequently in sporadic colorectal cancer and accelerate adenoma development in Apc mutant mice. Proc Natl Acad Sci 107: 15145-15150
47. Pruneda JN, Littlefield PJ, Soss SE, Nordquist KA, Chazin WJ, Brzovic PS, Klevit RE (2012) Structure of an E3:E2BUb complex reveals an allosteric mechanism shared among RING/U-box ligases. Mol Cell 47: 933-942
48. Rawal N, Corti O, Sacchetti P, Ardilla-Osorio H, Sehat B, Brice A, Arenas E (2009) Parkin protects dopaminergic neurons from excessive Wnt/beta-catenin signaling. Biochem Biophys Res Commun 388: 473-478
49. Rodŕiguez D, Grosse C, Himmel S, González C, de Ilarduya I, Becker S, Sheldrick G, Usón I (2009) Crystallographic ab initio protein structure solution below atomic resolution. Nat Methods 6: 651-653
50. 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
51. Schlehe JS, Lutz AK, Pilsl A, Lämmermann K, Grgur K, Henn IH, Tatzelt J, Winklhofer KF (2008) Aberrant folding of pathogenic Parkin mutants: aggregation versus degradation. J Biol Chem 283: 13771-13779
52. Shimura H, Hattori N, Kubo SI, Mizuno Y, Asakawa S, Minoshima S, Shimizu N, Iwai K, Chiba T, Tanaka K, Suzuki T (2000) Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat Genet 25: 302-305
53. Smit JJ, Monteferrario D, Noordermeer SM, van Dijk WJ, van der Reijden BA, Sixma TK (2012) The E3 ligase HOIP specifies linear ubiquitin chain assembly through its RING-IBR-RING domain and the unique LDD extension. EMBO J 31: 3833-3844
54. Sriram SR, Li X, Ko HS, Chung KKK, Wong E, Lim KL, Dawson VL, Dawson TM (2005) Familial-associated mutations differentially disrupt the solubility, localization, binding and ubiquitination properties of parkin. Hum Mol Genet 14: 2571-2586
55. Stieglitz B, Morris-Davies AC, Koliopoulos MG, Christodoulou E, Rittinger K (2012) LUBAC synthesizes linear ubiquitin chains via a thioester intermediate. EMBO Rep 13: 840-846
56. Sun M, Latourelle JC, Wooten GF, Lew MF, Klein C, Shill HA, Golbe LI, Mark MH, Racette BA, Perlmutter JS, Parsian A, Guttman M, Nicholson G, Xu G, Wilk JB, Saint-Hilaire MH, DeStefano AL, Prakash R, Williamson S, Suchowersky O et al. (2006) Influence of heterozygosity for parkin mutation on onset age in familial Parkinson disease: the GenePD study. Arch Neurol 63: 826-832
57. Tanaka A, Cleland MM, Xu S, Narendra DP, Suen D-F, Karbowski M, Youle RJ (2010) Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol 191: 1367-1380
58. Trempe J-F, Sauvé V, Grenier K, Seirafi M, Tang MY, Ménade M, Al-Abdul-Wahid S, Krett J, Wong K, Kozlov G, Nagar B, Fon EA, Geherng K (2013) Structure of Parkin Reveals Mechanisms for Ubiquitin Ligase Activation. Science. (advance online publication 9 May 2013; doi:10.1126/science.1237908)
59. Tsai YC, Fishman PS, Thakor NV, Oyler GA (2003) Parkin facilitates the elimination of expanded polyglutamine proteins and leads to preservation of proteasome function. J Biol Chem 278: 22044-22055
60. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MMK, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, Albanese A, Nussbaum R, González-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
61. Van Humbeeck C, Waelkens E, Corti O, Brice A, Vandenberghe W (2008) Parkin occurs in a stable, non-covalent, approximately 110-kDa complex in brain. Eur J Neurosci 27: 284-293
62. Veeriah S, Taylor BS, Meng S, Fang F, Yilmaz E, Vivanco I, Janakiraman M, Schultz N, Hanrahan AJ, Pao W, Ladanyi M, Sander C, Heguy A, Holland EC, Paty PB, Mischel PS, Liau L, Cloughesy TF, Mellinghoff IK, Solit DB et al. (2010) Somatic mutations of the Parkinson's disease-associated gene PARK2 in glioblastoma and other human malignancies. Nat Genet 42: 77-82
63. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RLA, Kim J, May J, Tocilescu MA, Liu W, Ko HS, Magrané J, Moore DJ, Dawson VL, Grailhe R, Dawson TM, Li C, Tieu K, Przedborski S (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci 107: 378-383
64. Walden H, Martinez-Torres RJ (2012) Regulation of Parkin E3 ubiquitin ligase activity. Cell Mol Life Sci 69: 3053-3067
65. Wang C, Tan JMM, Ho MWL, Zaiden N, Wong SH, Chew CLC, Eng PW, Lim TM, Dawson TM, Lim KL (2005) Alterations in the solubility and intracellular localization of parkin by several familial Parkinson's disease-linked point mutations. J Neurochem 93: 422-431
66. 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
67. Wang Y, Clark LN, Louis ED, Mejia-Santana H, Harris J, Cote LJ, Waters C, Andrews H, Ford B, Frucht S, Fahn S, Ottman R, Rabinowitz D, Marder K (2008) Risk of Parkinson disease in carriers of parkin mutations: estimation using the kin-cohort method. Arch Neurol 65: 467-474
68. Wenzel DM, Klevit RE (2012) Following Ariadne's thread: a new perspective on RBR ubiquitin ligases. BMC Biol 10: 24
69. 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
70. Wong ESP, Tan JMM, Wang C, Zhang Z, Tay S-P, Zaiden N, Ko HS, Dawson VL, Dawson TM, Lim KL (2007) Relative sensitivity of parkin and other cysteine-containing enzymes to stress-induced solubility alterations. J Biol Chem 282: 12310-12318
71. Xiong H, Wang D, Chen L, Choo YS, Ma H, Tang C, Xia K, Jiang W, Ronai Z, Zhuang X, Zhang Z (2009) Parkin, PINK1, and DJ-1 form a ubiquitin E3 ligase complex promoting unfolded protein degradation. J Clin Invest 119: 650-660
72. Yang Y, Lorick KL, Jensen JP, Weissman AM (2005) Expression and evaluation of RING finger proteins. Methods Enzymol 398: 103-112
73. Youle RJ, Narendra DP (2011) Mechanisms of mitophagy. Nat Rev Mol Cell Biol 12: 9-14
74. Zhang Y, Gao J, Chung KK, Huang H, Dawson VL, Dawson TM (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 USA 97: 13354-13359
75. Zheng N, Wang P, Jeffrey PD, Pavletich NP (2000) Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-pro-tein ligases. Cell 102: 533-539
76. Ziviani E, Tao RN, Whitworth AJ (2010) Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofu-sin. Proc Natl Acad Sci 107: 5018-5023