Activation mechanism of PINK1.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
02 2022
Historique:
received: 22 08 2021
accepted: 13 12 2021
pubmed: 22 12 2021
medline: 19 4 2022
entrez: 21 12 2021
Statut: ppublish

Résumé

Mutations in the protein kinase PINK1 lead to defects in mitophagy and cause autosomal recessive early onset Parkinson's disease

Identifiants

pubmed: 34933320
doi: 10.1038/s41586-021-04340-2
pii: 10.1038/s41586-021-04340-2
pmc: PMC8828467
doi:

Substances chimiques

Insect Proteins 0
Ubiquitin 0
Protein Kinases EC 2.7.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

328-335

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2021. The Author(s).

Références

Valente, E. M. et al. Hereditary early-onset Parkinson’s disease caused by mutations in PINK1. Science 304, 1158–1160 (2004).
pubmed: 15087508 doi: 10.1126/science.1096284
Pickrell, A. M. & Youle, R. J. The roles of PINK1, Parkin, and mitochondrial fidelity in Parkinson’s disease. Neuron 85, 257–273 (2015).
pubmed: 25611507 pmcid: 4764997 doi: 10.1016/j.neuron.2014.12.007
Kondapalli, C. et al. PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating serine 65. Open Biol. 2, 120080 (2012).
pubmed: 22724072 pmcid: 3376738 doi: 10.1098/rsob.120080
Kazlauskaite, A. et al. Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem. J. 460, 127–139 (2014).
pubmed: 24660806 doi: 10.1042/BJ20140334
Koyano, F. et al. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 510, 162–166 (2014).
pubmed: 24784582 doi: 10.1038/nature13392
Kane, L. A. et al. PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J. Cell Biol. 205, 143–153 (2014).
pubmed: 24751536 pmcid: 4003245 doi: 10.1083/jcb.201402104
Ordureau, A. et al. Quantitative proteomics reveal a feedforward mechanism for mitochondrial PARKIN translocation and ubiquitin chain synthesis. Mol. Cell 56, 360–375 (2014).
pubmed: 25284222 pmcid: 4254048 doi: 10.1016/j.molcel.2014.09.007
Wauer, T. et al. Ubiquitin Ser65 phosphorylation affects ubiquitin structure, chain assembly and hydrolysis. EMBO J. 34, 307–325 (2015).
pubmed: 25527291 doi: 10.15252/embj.201489847
Gladkova, C. et al. An invisible ubiquitin conformation is required for efficient phosphorylation by PINK1. EMBO J. 36, 3555–3572 (2017).
pubmed: 29133469 pmcid: 5730886 doi: 10.15252/embj.201797876
Schubert, A. F. et al. Structure of PINK1 in complex with its substrate ubiquitin. Nature 552, 51–56 (2017).
pubmed: 29160309 pmcid: 6020998 doi: 10.1038/nature24645
Kumar, A. et al. Structure of PINK1 and mechanisms of Parkinson’s disease-associated mutations. eLife 6, e29985 (2017).
pubmed: 28980524 pmcid: 5679756 doi: 10.7554/eLife.29985
Okatsu, K. et al. Structural insights into ubiquitin phosphorylation by PINK1. Sci. Rep. 8, 10382 (2018).
pubmed: 29991771 pmcid: 6039469 doi: 10.1038/s41598-018-28656-8
Hoehn, M. M. & Yahr, M. D. Parkinsonism: onset, progression and mortality. Neurology 17, 427–442 (1967).
pubmed: 6067254 doi: 10.1212/WNL.17.5.427
Corti, O., Lesage, S. & Brice, A. What genetics tells us about the causes and mechanisms of Parkinson’s disease. Physiol. Rev. 91, 1161–1218 (2011).
pubmed: 22013209 doi: 10.1152/physrev.00022.2010
Nguyen, T. N., Padman, B. S. & Lazarou, M. Deciphering the molecular signals of PINK1/Parkin mitophagy. Trends Cell Biol. 26, 733–744 (2016).
pubmed: 27291334 doi: 10.1016/j.tcb.2016.05.008
Harper, J. W., Ordureau, A. & Heo, J.-M. Building and decoding ubiquitin chains for mitophagy. Nat. Rev. Mol. Cell Biol. 19, 93–108 (2018).
pubmed: 29358684 doi: 10.1038/nrm.2017.129
Lazarou, M., Jin, S. M., Kane, L. A. & Youle, R. J. 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 (2012).
pubmed: 22280891 pmcid: 3288275 doi: 10.1016/j.devcel.2011.12.014
Okatsu, K. et al. A dimeric PINK1-containing complex on depolarized mitochondria stimulates Parkin recruitment. J. Biol. Chem. 288, 36372–36384 (2013).
pubmed: 24189060 pmcid: 3868751 doi: 10.1074/jbc.M113.509653
Wauer, T., Simicek, M., Schubert, A. F. & Komander, D. Mechanism of phospho-ubiquitin-induced PARKIN activation. Nature 524, 370–374 (2015).
pubmed: 26161729 pmcid: 4984986 doi: 10.1038/nature14879
Kumar, A. et al. Parkin–phosphoubiquitin complex reveals cryptic ubiquitin-binding site required for RBR ligase activity. Nat. Struct. Mol. Biol. 24, 475–483 (2017).
pubmed: 28414322 pmcid: 5420311 doi: 10.1038/nsmb.3400
Gladkova, C., Maslen, S. L., Skehel, J. M. & Komander, D. Mechanism of parkin activation by PINK1. Nature 559, 410–414 (2018).
pubmed: 29995846 pmcid: 6071873 doi: 10.1038/s41586-018-0224-x
Sauvé, V. et al. Mechanism of parkin activation by phosphorylation. Nat. Struct. Mol. Biol. 25, 623–630 (2018).
pubmed: 29967542 doi: 10.1038/s41594-018-0088-7
Woodroof, H. I. et al. Discovery of catalytically active orthologues of the Parkinson’s disease kinase PINK1: analysis of substrate specificity and impact of mutations. Open Biol. 1, 110012 (2011).
pubmed: 22645651 pmcid: 3352081 doi: 10.1098/rsob.110012
Taylor, S. S. & Kornev, A. P. Protein kinases: evolution of dynamic regulatory proteins. Trends Biochem. Sci 36, 65–77 (2011).
pubmed: 20971646 doi: 10.1016/j.tibs.2010.09.006
Patel, O. et al. Structure of SgK223 pseudokinase reveals novel mechanisms of homotypic and heterotypic association. Nat. Commun. 8, 1157 (2017).
pubmed: 29079850 pmcid: 5660093 doi: 10.1038/s41467-017-01279-9
Ha, B. H. & Boggon, T. J. The crystal structure of pseudokinase PEAK1 (Sugen kinase 269) reveals an unusual catalytic cleft and a novel mode of kinase fold dimerization. J. Biol. Chem. 293, 1642–1650 (2018).
pubmed: 29212708 doi: 10.1074/jbc.RA117.000751
Sekine, S. et al. Reciprocal roles of Tom7 and OMA1 during mitochondrial import and activation of PINK1. Mol. Cell 73, 1028–1043 (2019).
pubmed: 30733118 doi: 10.1016/j.molcel.2019.01.002
Hasson, S. A. et al. High-content genome-wide RNAi screens identify regulators of parkin upstream of mitophagy. Nature 504, 291–295 (2013).
pubmed: 24270810 pmcid: 5841086 doi: 10.1038/nature12748
Rasool, S. et al. Mechanism of PINK1 activation by autophosphorylation and insights into assembly on the TOM complex. Mol. Cell 82, 44–59 (2022).
Rasool, S. et al. PINK1 autophosphorylation is required for ubiquitin recognition. EMBO Rep. 19, e44981 (2018).
pubmed: 29475881 pmcid: 5891426 doi: 10.15252/embr.201744981
Aerts, L., Craessaerts, K., Strooper, B. D. & Morais, V. A. PINK1 kinase catalytic activity is regulated by phosphorylation on serines 228 and 402. J. Biol. Chem. 290, 2798–2811 (2015).
pubmed: 25527497 doi: 10.1074/jbc.M114.620906
Aerts, L., Craessaerts, K., Strooper, B. D. & Morais, V. A. In vitro comparison of the activity requirements and substrate specificity of human and triboleum castaneum PINK1 orthologues. PLoS ONE 11, e0146083 (2016).
pubmed: 26784449 pmcid: 4718624 doi: 10.1371/journal.pone.0146083
Okatsu, K. et al. PINK1 autophosphorylation upon membrane potential dissipation is essential for Parkin recruitment to damaged mitochondria. Nat. Commun. 3, 1016 (2012).
pubmed: 22910362 doi: 10.1038/ncomms2016
Punjani, A. & Fleet, D. J. 3D variability analysis: resolving continuous flexibility and discrete heterogeneity from single particle cryo-EM. J. Struct. Biol. 213, 107702 (2021).
pubmed: 33582281 doi: 10.1016/j.jsb.2021.107702
Soylu, İ. & Marino, S. M. Cy‐preds: an algorithm and a web service for the analysis and prediction of cysteine reactivity. Proteins Struct. Funct. Bioinform. 84, 278–291 (2016).
doi: 10.1002/prot.24978
Shrestha, S. et al. A redox-active switch in fructosamine-3-kinases expands the regulatory repertoire of the protein kinase superfamily. Sci. Signal. 13, eaax6313 (2020).
pubmed: 32636308 pmcid: 8455029 doi: 10.1126/scisignal.aax6313
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
pubmed: 34265844 pmcid: 8371605 doi: 10.1038/s41586-021-03819-2
Tunyasuvunakool, K. et al. Highly accurate protein structure prediction for the human proteome. Nature 596, 590–596 (2021).
pubmed: 34293799 pmcid: 8387240 doi: 10.1038/s41586-021-03828-1
Ovchinnikov, S., Mirdita, M. & Steinegger, M. ColabFold—making protein folding accessible to all via Google Colab (v1.0-alpha). Zenodo https://doi.org/10.5281/zenodo.5123297 (2021).
Pollock, L., Jardine, J., Urbé, S. & Clague, M. J. The PINK1 repertoire: not just a one trick pony. Bioessays 43, 2100168 (2021).
doi: 10.1002/bies.202100168
Hertz, N. T. et al. A neo-substrate that amplifies catalytic activity of Parkinson’s-disease-related kinase PINK1. Cell 154, 737–747 (2013).
pubmed: 23953109 pmcid: 3950538 doi: 10.1016/j.cell.2013.07.030
Lowe, E. D. et al. The crystal structure of a phosphorylase kinase peptide substrate complex: kinase substrate recognition. EMBO J. 16, 6646–6658 (1997).
pubmed: 9362479 pmcid: 1170269 doi: 10.1093/emboj/16.22.6646
Berrow, N. S. et al. A versatile ligation-independent cloning method suitable for high-throughput expression screening applications. Nucleic Acids Res. 35, e45 (2007).
pubmed: 17317681 pmcid: 1874605 doi: 10.1093/nar/gkm047
Aragão, D. et al. MX2: a high-flux undulator microfocus beamline serving both the chemical and macromolecular crystallography communities at the Australian Synchrotron. J. Synchrotron Radiat. 25, 885–891 (2018).
pubmed: 29714201 pmcid: 5929359 doi: 10.1107/S1600577518003120
McPhillips, T. M. et al. Blu-Ice and the distributed control system: software for data acquisition and instrument control at macromolecular crystallography beamlines. J. Synchrotron Radiat. 9, 401–406 (2002).
pubmed: 12409628 doi: 10.1107/S0909049502015170
Evans, P. R. & Murshudov, G. N. How good are my data and what is the resolution? Acta Crystallogr. D 69, 1204–1214 (2013).
pubmed: 23793146 pmcid: 3689523 doi: 10.1107/S0907444913000061
Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235–242 (2011).
pubmed: 21460441 pmcid: 3069738 doi: 10.1107/S0907444910045749
McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
pubmed: 19461840 pmcid: 2483472 doi: 10.1107/S0021889807021206
Adams, P. D. et al. The Phenix software for automated determination of macromolecular structures. Methods 55, 94–106 (2011).
pubmed: 21821126 pmcid: 3193589 doi: 10.1016/j.ymeth.2011.07.005
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
pubmed: 20383002 pmcid: 2852313 doi: 10.1107/S0907444910007493
Zivanov, J. et al. New tools for automated high-resolution cryo-EM structure determination in RELION-3. eLife 7, e42166 (2018).
pubmed: 30412051 pmcid: 6250425 doi: 10.7554/eLife.42166
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
pubmed: 28165473 doi: 10.1038/nmeth.4169
Yang, Z. et al. UCSF Chimera, MODELLER, and IMP: an integrated modeling system. J. Struct. Biol. 179, 269–278 (2012).
pubmed: 21963794 doi: 10.1016/j.jsb.2011.09.006
Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38–46 (2007).
pubmed: 16859925 doi: 10.1016/j.jsb.2006.05.009
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010).
pubmed: 20057044 doi: 10.1107/S0907444909042073
Pettersen, E. F. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).
pubmed: 32881101 doi: 10.1002/pro.3943
MacLean, B. et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966–968 (2010).
pubmed: 20147306 pmcid: 2844992 doi: 10.1093/bioinformatics/btq054
Slater, M. et al. Achieve the protein expression level you need with the mammalian HaloTag 7 flexi vectors. Promega Notes 100, 16–18 (2008).
Yamano, K., Fogel, A. I., Wang, C., Bliek, A. M. V. D. & Youle, R. J. Mitochondrial Rab GAPs govern autophagosome biogenesis during mitophagy. eLife 3, e01612 (2014).
pubmed: 24569479 pmcid: 3930140 doi: 10.7554/eLife.01612
McArthur, K. et al. BAK/BAX macropores facilitate mitochondrial herniation and mtDNA efflux during apoptosis. Science 359, eaao6047 (2018).
pubmed: 29472455 doi: 10.1126/science.aao6047
Wang, W. et al. Atomic structure of human TOM core complex. Cell Discov. 6, 67 (2020).
pubmed: 33083003 pmcid: 7522991 doi: 10.1038/s41421-020-00198-2

Auteurs

Zhong Yan Gan (ZY)

Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia.

Sylvie Callegari (S)

Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia.

Simon A Cobbold (SA)

Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia.

Thomas R Cotton (TR)

Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia.

Michael J Mlodzianoski (MJ)

Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia.

Alexander F Schubert (AF)

Medical Research Council Laboratory of Molecular Biology, Cambridge, UK.

Niall D Geoghegan (ND)

Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia.

Kelly L Rogers (KL)

Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia.

Andrew Leis (A)

Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia.

Grant Dewson (G)

Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia.

Alisa Glukhova (A)

Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia.
Drug Discovery Biology, Monash Faculty of Pharmacy and Pharmaceutical Sciences, Monash University, Parkville, Victoria, Australia.
Department of Biochemistry and Pharmacology, University of Melbourne, Melbourne, Victoria, Australia.

David Komander (D)

Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia. dk@wehi.edu.au.
Department of Medical Biology, University of Melbourne, Melbourne, Victoria, Australia. dk@wehi.edu.au.

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