Phosphorylation by PINK1 Releases the UBL Domain and Initializes the Conformational Opening of the E3 Ubiquitin Ligase Parkin

PLoS Computational Biology

Volumn 10, Issue 11, 2014, Pages

  Caulfield, Thomas R ^a   Fiesel, Fabienne C ^a   Moussaud Lamodière, Elisabeth L ^a   Dourado, Daniel F A R ^c   Flores, Samuel C ^c   Springer, Wolfdieter ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYST ACTIVITY; CONFORMATIONS; CONTROLLED DRUG DELIVERY; ENZYMES; MITOCHONDRIA; MOLECULAR DYNAMICS; MONTE CARLO METHODS; TARGETED DRUG DELIVERY;

DYNAMICS SIMULATION; E3 UBIQUITIN LIGASES; ENZYMATIC FUNCTIONS; GENE PRODUCTS; MITOCHONDRIAS; MOLECULAR MECHANISM; PARKINSON'S DISEASE; STEADY STATE; STRUCTURAL MODELING; UBIQUITINATION;

PHOSPHORYLATION;

PARKIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE INDUCED PUTATIVE KINASE 1; SERINE; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE E3 PARKIN; UNCLASSIFIED DRUG; PROTEIN BINDING; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE; UBIQUITIN PROTEIN LIGASE;

ALGORITHM; AMINO ACID SUBSTITUTION; ARTICLE; CALCULATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME RELEASE; ENZYME STRUCTURE; HUMAN; HUMAN CELL; MATHEMATICAL ANALYSIS; MOLECULAR DYNAMICS; MONTE CARLO METHOD; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; UBIQUITINATION; CHEMICAL STRUCTURE; CHEMISTRY; HELA CELL LINE; METABOLISM; PARKINSON DISEASE; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

HELA CELLS; HUMANS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PARKINSON DISEASE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; UBIQUITIN-PROTEIN LIGASES;

EID: 84912127688     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003935     Document Type: Article

References (100)

1. 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.
2. Springer W, Kahle PJ, (2011) Regulation of PINK1-Parkin-mediated mitophagy. Autophagy 7: 266–278.
3. 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.
4. 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.
5. 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.
6. 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.
7. Chan NC, Salazar AM, Pham AH, Sweredoski MJ, Kolawa NJ, et al. (2011) Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum Mol Genet 20: 1726–1737.
8. Sarraf SA, Raman M, Guarani-Pereira V, Sowa ME, Huttlin EL, et al. (2013) Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature 496: 372–376.
9. Okatsu K, Saisho K, Shimanuki M, Nakada K, Shitara H, et al. (2010) p62/SQSTM1 cooperates with Parkin for perinuclear clustering of depolarized mitochondria. Genes Cells 15: 887–900.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. Zheng X, Hunter T, (2013) Parkin mitochondrial translocation is achieved through a novel catalytic activity coupled mechanism. Cell Res 23: 886–897.
16. Kane LA, Lazarou M, Fogel AI, Li Y, Yamano K, et al. (2014) PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J Cell Biol 205: 143–153.
17. Kazlauskaite A, Kondapalli C, Gourlay R, Campbell DG, Ritorto MS, et al. (2014) Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem J 460: 127–139.
18. Koyano F, Okatsu K, Kosako H, Tamura Y, Go E, et al. (2014) Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 510: 162–166.
19. Zhang C, Lee S, Peng Y, Bunker E, Giaime E, et al. (2014) PINK1 Triggers Autocatalytic Activation of Parkin to Specify Cell Fate Decisions. Curr Biol
20. 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.
21. 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.
22. Wenzel DM, Klevit RE, (2012) Following Ariadne's thread: a new perspective on RBR ubiquitin ligases. BMC Biol 10: 24.
23. Berndsen CE, Wolberger C, (2014) New insights into ubiquitin E3 ligase mechanism. Nat Struct Mol Biol 21: 301–307.
24. Riley BE, Lougheed JC, Callaway K, Velasquez M, Brecht E, et al. (2013) Structure and function of Parkin E3 ubiquitin ligase reveals aspects of RING and HECT ligases. Nat Commun 4: 1982.
25. Spratt DE, Julio Martinez-Torres R, Noh YJ, Mercier P, Manczyk N, et al. (2013) A molecular explanation for the recessive nature of parkin-linked Parkinson's disease. Nat Commun 4: 1983.
26. Trempe JF, Sauve V, Grenier K, Seirafi M, Tang MY, et al. (2013) Structure of Parkin Reveals Mechanisms for Ubiquitin Ligase Activation. Science 340: 1451–1455.
27. Wauer T, Komander D, (2013) Structure of the human Parkin ligase domain in an autoinhibited state. EMBO J 32: 2099–2112.
28. Byrd RA, Weissman AM, (2013) Compact Parkin only: insights into the structure of an autoinhibited ubiquitin ligase. EMBO J 32: 2087–2089.
29. Lorenz S, Cantor AJ, Rape M, Kuriyan J, (2013) Macromolecular juggling by ubiquitylation enzymes. BMC Biol 11: 65.
30. Kales SC, Ryan PE, Lipkowitz S, (2012) Cbl exposes its RING finger. Nat Struct Mol Biol 19: 131–133.
31. Dou H, Buetow L, Hock A, Sibbet GJ, Vousden KH, et al. (2012) Structural basis for autoinhibition and phosphorylation-dependent activation of c-Cbl. Nat Struct Mol Biol 19: 184–192.
32. Gallagher E, Gao M, Liu YC, Karin M, (2006) Activation of the E3 ubiquitin ligase Itch through a phosphorylation-induced conformational change. Proc Natl Acad Sci U S A 103: 1717–1722.
33. Chaugule VK, Burchell L, Barber KR, Sidhu A, Leslie SJ, et al. (2011) Autoregulation of Parkin activity through its ubiquitin-like domain. EMBO J 30: 2853–2867.
34. Zhang YJ, Caulfield T, Xu YF, Gendron TF, Hubbard J, et al. (2013) The dual functions of the extreme N-terminus of TDP-43 in regulating its biological activity and inclusion formation. Hum Mol Genet 22: 3112–3122.
35. Caulfield T, Devkota B, (2012) Motion of transfer RNA from the A/T state into the A-site using docking and simulations. Proteins 80: 2489–2500.
36. Caulfield TR, Devkota B, Rollins GC, (2011) Examinations of tRNA Range of Motion Using Simulations of Cryo-EM Microscopy and X-Ray Data. J Biophys 2011: 219515.
37. Dourado DF, Flores SC, (2014) A multiscale approach to predicting affinity changes in protein-protein interfaces. Proteins 82: 2681–2690.
38. Ruben Abagyan MT, Kuznetzov Dmitry, (1993) ICM - A New Method for Protein Modeling and Design: Applications to Docking and Structure Prediction from the Distorted Native Conformation. Journal of Computational Chemistry 15.
39. Fiesel FC, Moussaud-Lamodiere EL, Ando M, Springer W, (2014) A specific subset of E2 ubiquitin-conjugating enzymes regulate Parkin activation and mitophagy differently. J Cell Sci 127: 3488–3504.
40. Engels M, Jacoby E, Kruger P, Schlitter J, Wollmer A, (1992) The T<–>R structural transition of insulin; pathways suggested by targeted energy minimization. Protein Eng 5: 669–677.
41. Schlitter J, Engels M, Kruger P, (1994) Targeted molecular dynamics: a new approach for searching pathways of conformational transitions. J Mol Graph 12: 84–89.
42. Schrödinger (2012) Suite 2012. BioLuminate, version 1.0 ed. New York, NY: Schrödinger, LLC.
43. Schrödinger (2013) Biologics Suite. In: Schrodinger, editor. BioLuminate, version 11. BioLuminate, version 1.1 ed. New York, NY, 2013: Schrödinger, LLC.
44. Krieger E, Joo K, Lee J, Lee J, Raman S, et al. (2009) Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins 77 Suppl 9: 114–122.
45. Krieger E, Koraimann G, Vriend G, (2002) Increasing the precision of comparative models with YASARA NOVA–a self-parameterizing force field. Proteins 47: 393–402.
46. Krieger E, Nabuurs SB, Vriend G, (2003) Homology modeling. Methods Biochem Anal 44: 509–523.
47. 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.
48. Hasson SA, Kane LA, Yamano K, Huang CH, Sliter DA, et al. (2013) High-content genome-wide RNAi screens identify regulators of parkin upstream of mitophagy. Nature 504: 291–295.
49. Beveridge DL, DiCapua FM, (1989) Free energy via molecular simulation: applications to chemical and biomolecular systems. Annu Rev Biophys Biophys Chem 18: 431–492.
50. Madej T, Addess KJ, Fong JH, Geer LY, Geer RC, et al. (2012) MMDB: 3D structures and macromolecular interactions. Nucleic Acids Res 40: D461–464.
51. Kollman PA, Massova I, Reyes C, Kuhn B, Huo S, et al. (2000) Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc Chem Res 33: 889–897.
52. Hamelberg D, Mongan J, McCammon JA, (2004) Accelerated molecular dynamics: a promising and efficient simulation method for biomolecules. J Chem Phys 120: 11919–11929.
53. Wang Y, Harrison CB, Schulten K, McCammon JA, (2011) Implementation of Accelerated Molecular Dynamics in NAMD. Comput Sci Discov 4.
54. Dawson TM, Dawson VL, (2014) Parkin plays a role in sporadic Parkinson's disease. Neurodegener Dis 13: 69–71.
55. Birsa N, Norkett R, Wauer T, Mevissen TE, Wu HC, et al. (2014) Lysine 27 ubiquitination of the mitochondrial transport protein miro is dependent on serine 65 of the parkin ubiquitin ligase. J Biol Chem 289: 14569–14582.
56. Shiba-Fukushima K, Inoshita T, Hattori N, Imai Y, (2014) PINK1-mediated phosphorylation of Parkin boosts Parkin activity in Drosophila. PLoS Genet 10: e1004391.
57. Kazlauskaite A, Kelly V, Johnson C, Baillie C, Hastie CJ, et al. (2014) 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.
58. Geisler S, Vollmer S, Golombek S, Kahle PJ, (2014) The ubiquitin-conjugating enzymes UBE2N, UBE2L3 and UBE2D2/3 are essential for Parkin-dependent mitophagy. J Cell Sci 127: 3280–3293.
59. Sandebring A, Cedazo-Mínguez A, (2012) Parkin - An E3 Ubiquitin Ligase with Multiple Substrates. J Alzheimers Dis Parkinsonism
60. Spratt DE, Walden H, Shaw GS, (2014) RBR E3 ubiquitin ligases: new structures, new insights, new questions. Biochem J 458: 421–437.
61. Jacobson MP, Friesner RA, Xiang Z, Honig B, (2002) On the role of the crystal environment in determining protein side-chain conformations. J Mol Biol 320: 597–608.
62. Altschul SF, Koonin EV, (1998) Iterated profile searches with PSI-BLAST–a tool for discovery in protein databases. Trends Biochem Sci 23: 444–447.
63. Krieger E, Dunbrack RL, JrHooft RW, Krieger B, (2012) Assignment of protonation states in proteins and ligands: combining pKa prediction with hydrogen bonding network optimization. Methods Mol Biol 819: 405–421.
64. Hooft RW, Sander C, Scharf M, Vriend G, (1996) The PDBFINDER database: a summary of PDB, DSSP and HSSP information with added value. Comput Appl Biosci 12: 525–529.
65. Hooft RW, Vriend G, Sander C, Abola EE, (1996) Errors in protein structures. Nature 381: 272.
66. Qiu J, Elber R, (2006) SSALN: an alignment algorithm using structure-dependent substitution matrices and gap penalties learned from structurally aligned protein pairs. Proteins 62: 881–891.
67. King RD, Sternberg MJ, (1996) Identification and application of the concepts important for accurate and reliable protein secondary structure prediction. Protein Sci 5: 2298–2310.
68. Zhou H, Pandit SB, Lee SY, Borreguero J, Chen H, et al. (2007) Analysis of TASSER-based CASP7 protein structure prediction results. Proteins 69 Suppl 8: 90–97.
69. Zhou H, Pandit SB, Skolnick J, (2009) Performance of the Pro-sp3-TASSER server in CASP8. Proteins 77 Suppl 9: 123–127.
70. Zhou H, Skolnick J, (2007) Ab initio protein structure prediction using chunk-TASSER. Biophys J 93: 1510–1518.
71. Zhou H, Skolnick J, (2009) Protein structure prediction by pro-Sp3-TASSER. Biophys J 96: 2119–2127.
72. Zhou H, Skolnick J, (2010) Improving threading algorithms for remote homology modeling by combining fragment and template comparisons. Proteins 78: 2041–2048.
73. Zhou H, Skolnick J, (2011) Template-based protein structure modeling using TASSER(VMT). Proteins
74. Dolan MA, Keil M, Baker DS, (2008) Comparison of Composer and ORCHESTRAR. Proteins 72: 1243–1258.
75. Muckstein U, Hofacker IL, Stadler PF, (2002) Stochastic pairwise alignments. Bioinformatics 18 Suppl 2: S153–160.
76. Canutescu AA, Shelenkov AA, Dunbrack RL, Jr (2003) A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci 12: 2001–2014.
77. Laskowski RA, MacArthur MW, Moss DS, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26: 283–291.
78. Joosten RP, Salzemann J, Bloch V, Stockinger H, Berglund AC, et al. (2009) PDB_REDO: automated re-refinement of X-ray structure models in the PDB. J Appl Crystallogr 42: 376–384.
79. Vriend G, (1990) WHAT IF: a molecular modeling and drug design program. J Mol Graph 8: 52–56.
80. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33–38.
81. Caulfield T, Medina-Franco JL, (2011) Molecular dynamics simulations of human DNA methyltransferase 3B with selective inhibitor nanaomycin A. J Struct Biol 176: 185–191.
82. Caulfield TR, (2011) Inter-ring rotation of apolipoprotein A-I protein monomers for the double-belt model using biased molecular dynamics. J Mol Graph Model 29: 1006–1014.
83. Sanchez IE, Beltrao P, Stricher F, Schymkowitz J, Ferkinghoff-Borg J, et al. (2008) Genome-wide prediction of SH2 domain targets using structural information and the FoldX algorithm. PLoS Comput Biol 4: e1000052.
84. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML, (1983) Comparison of simple potential functions for simulating liquid water. Journal of Chemical Physics 79: 926–935.
85. Reblova K, Lankas F, Razga F, Krasovska MV, Koca J, et al. (2006) Structure, dynamics, and elasticity of free 16s rRNA helix 44 studied by molecular dynamics simulations. Biopolymers 82: 504–520.
86. Reblova K, Fadrna E, Sarzynska J, Kulinski T, Kulhanek P, et al. (2007) Conformations of flanking bases in HIV-1 RNA DIS kissing complexes studied by molecular dynamics. Biophys J 93: 3932–3949.
87. T.E. Cheatham IaMAY (2001) Molecular dynamics simulation of nucleic acids: Successes, limitations and promise. Biopolymers 56: 232–256.
88. Polak E, Ribiere G, (1969) Note sur la convergence de méthodes de directions conjuguées.
89. Maestro-9.1 (2010) Maestro 9.1. In: 9.1 M, editor. New York, NY: Schrödinger, LLC.
90. Flores S, Sherman M, Bruns C, Eastman P, Altman R, (2010) Fast flexible modeling of macromolecular structure using internal coordinates. IEEE Transactions in Computational Biology and Bioinformatics 8: 1247–1257.
91. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA, (2004) Development and testing of a general amber force field. J Comput Chem 25: 1157–1174.
92. Flores SC, Altman RB, (2010) Turning limited experimental information into 3D models of RNA. RNA 16: 1769–1778.
93. Flores SC, Wan Y, Russell R, Altman RB, (2010) Predicting RNA structure by multiple template homology modeling. Pac Symp Biocomput 216–227.
94. Flores SC, Zemora G, Waldsich C, (2013) Insights into diseases of human telomerase from dynamical modeling. Pac Symp Biocomput 200–211.
95. Flores SC, (2014) Fast fitting to low resolution density maps: elucidating large-scale motions of the ribosome. Nucleic Acids Res 42: e9.
96. Moretti R, Fleishman SJ, Agius R, Torchala M, Bates PA, et al. (2013) Community-wide evaluation of methods for predicting the effect of mutations on protein-protein interactions. Proteins 81: 1980–1987.
97. Chatrchyan S, Khachatryan V, Sirunyan AM, Tumasyan A, Adam W, et al. (2013) Measurement of associated production of vector bosons and top quark-antiquark pairs in pp collisions at sqrt[s] = 7 TeV. Phys Rev Lett 110: 172002.
98. Charles D, Schweiters GMC, (2001) Internal Coordinates for Molecular Dynamics and Minimization in Structure determination and Refinement. Journal of Magnetic Resonance 152: 288–302.
99. Guerois R, Nielsen JE, Serrano L, (2002) Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J Mol Biol 320: 369–387.
100. Brandsdal BO, Aqvist J, Smalas AO, (2001) Computational analysis of binding of P1 variants to trypsin. Protein Sci 10: 1584–1595.