Versatility of Preprotein Transfer from the Cytosol to Mitochondria

Trends in Cell Biology - Tập 29 - Trang 534-548 - 2019
Thomas Becker1,2, Jiyao Song1, Nikolaus Pfanner1,2
1Institute of Biochemistry and Molecular Biology, Centre for Biochemistry and Molecular Cell Research (ZBMZ), Faculty of Medicine, University of Freiburg, 79104 Freiburg, Germany
2Centre for Integrative Biological Signaling Studies (CIBSS), University of Freiburg, 79104 Freiburg, Germany

Tài liệu tham khảo

Wickner, 2005, Protein translocation across biological membranes, Science, 310, 1452, 10.1126/science.1113752 Guna, 2018, Transmembrane domain recognition during membrane protein biogenesis and quality control, Curr. Biol., 28, R498, 10.1016/j.cub.2018.02.004 Pagliarini, 2008, A mitochondrial protein compendium elucidates complex I disease biology, Cell, 134, 112, 10.1016/j.cell.2008.06.016 Morgenstern, 2017, Definition of a high-confidence mitochondrial proteome at quantitative scale, Cell Rep., 19, 2836, 10.1016/j.celrep.2017.06.014 Vögtle, 2009, Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability, Cell, 139, 428, 10.1016/j.cell.2009.07.045 Neupert, 2007, Translocation of proteins into mitochondria, Annu. Rev. Biochem., 76, 723, 10.1146/annurev.biochem.76.052705.163409 Wiedemann, 2017, Mitochondrial machineries for import and assembly, Annu. Rev. Biochem., 20, 685, 10.1146/annurev-biochem-060815-014352 Shiota, 2015, Molecular architecture of the active mitochondrial protein gate, Science, 349, 1544, 10.1126/science.aac6428 Bausewein, 2017, Cryo-EM structure of the TOM core complex from Neurospora crassa, Cell, 170, 693, 10.1016/j.cell.2017.07.012 Makki, 2019, Triplet-pore structure of a highly divergent TOM complex of hydrogenosomes in Trichomonas vaginalis, PLoS Biol., 17, 10.1371/journal.pbio.3000098 Abe, 2000, Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20, Cell, 100, 551, 10.1016/S0092-8674(00)80691-1 Yamamoto, 2009, Roles of Tom70 in import of presequence-containing mitochondrial proteins, J. Biol. Chem., 284, 31635, 10.1074/jbc.M109.041756 Backes, 2018, Tom70 enhances mitochondrial preprotein import efficiency by binding to internal targeting sequences, J. Cell Biol., 217, 1369, 10.1083/jcb.201708044 Endo, 2009, Multiple pathways for mitochondrial protein traffic, Biol. Chem., 390, 723, 10.1515/BC.2009.087 Schleiff, 2011, Common ground for protein translocation: access control for mitochondria and chloroplasts, Nat. Rev. Mol. Cell Biol., 12, 48, 10.1038/nrm3027 Beddoe, 2002, Delivery of nascent polypeptides to the mitochondrial surface, Biochim. Biophys. Acta, 1592, 35, 10.1016/S0167-4889(02)00262-8 Young, 2003, Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70, Cell, 112, 41, 10.1016/S0092-8674(02)01250-3 Yano, 2003, AIP is a mitochondrial import mediator that binds to both import receptor Tom20 and preproteins, J. Cell Biol., 163, 45, 10.1083/jcb.200305051 Endo, 1996, Binding of mitochondrial presequences to yeast cytosolic heat shock protein 70 depends on the amphiphilicity of the presequence, J. Biol. Chem., 271, 4161, 10.1074/jbc.271.8.4161 Faou, 2012, Tom34: a cytosolic cochaperone of the Hsp90/Hsp70 protein complex involved in mitochondrial protein import, Biochim. Biophys. Acta, 1823, 348, 10.1016/j.bbamcr.2011.12.001 Hoseini, 2016, The cytosolic cochaperone Sti1 is relevant for mitochondrial biogenesis and morphology, FEBS J., 283, 3338, 10.1111/febs.13813 Jores, 2018, Cytosolic Hsp70 and Hsp40 chaperones enable the biogenesis of mitochondrial β-barrel proteins, J. Cell Biol., 217, 3091, 10.1083/jcb.201712029 Hachiya, 1994, MSF, a novel cytosplasmic chaperone which functions in precursor targeting to mitochondria, EMBO J., 13, 5146, 10.1002/j.1460-2075.1994.tb06844.x Hachiya, 1995, Reconstitution of the initial steps of mitochondrial protein import, Nature, 376, 705, 10.1038/376705a0 Murakami, 1990, Purified presequence binding factor (PBF) forms an import-competent complex with a purified mitochondrial precursor protein, EMBO J., 9, 3201, 10.1002/j.1460-2075.1990.tb07518.x Murakami, 1992, Presequence binding factor-dependent and -independent import of proteins into mitochondria, J. Biol. Chem., 267, 13119, 10.1016/S0021-9258(18)42177-1 Deshaies, 1988, A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides, Nature, 332, 800, 10.1038/332800a0 Murakami, 1988, 70-kD heat shock-related protein is one of at least two distinct cytosolic factors stimulating protein import into mitochondria, J. Cell Biol., 107, 2051, 10.1083/jcb.107.6.2051 Balchin, 2016, In vivo aspects of protein folding and quality control, Science, 353, 10.1126/science.aac4354 Craig, 2017, How do J-proteins get Hsp70 to do so many different things?, Trends Biochem. Sci., 42, 355, 10.1016/j.tibs.2017.02.007 Kramer, 2019, Mechanisms of cotranslational maturation of newly synthesized proteins, Annu. Rev. Biochem., 10.1146/annurev-biochem-013118-111717 Gautschi, 2001, RAC, a stable ribosome-associated complex in yeast formed by the DnaK-DnaJ homologs Ssz1p and zuotin, Proc. Natl. Acad. Sci. U. S. A., 98, 3762, 10.1073/pnas.071057198 Sheffield, 1990, Mitochondrial precursor protein. Effects of 70-kilodalton heat shock protein on polypeptide folding, aggregation, and import competence, J. Biol. Chem., 265, 11069, 10.1016/S0021-9258(19)38558-8 Terada, 1995, Role of heat shock cognate 70 protein in import of ornithine transcarbamylase precursor into mammalian mitochondria, Mol. Cell. Biol., 15, 3708, 10.1128/MCB.15.7.3708 Schmidt, 2011, Regulation of mitochondrial protein import by cytosolic kinases, Cell, 144, 227, 10.1016/j.cell.2010.12.015 Fan, 2006, Hsp90 functions in the targeting and outer membrane translocation steps of Tom70-mediated mitochondrial protein import, J. Biol. Chem., 281, 33313, 10.1074/jbc.M605250200 Opaliński, 2018, Recruitment of cytosolic J-proteins by TOM receptor promotes mitochondrial protein biogenesis, Cell Rep., 25, 2036, 10.1016/j.celrep.2018.10.083 Sahi, 2013, Sequential duplications of an ancient member of the DnaJ-family expanded the functional chaperone network in the eukaryotic cytosol, Mol. Biol. Evol., 30, 985, 10.1093/molbev/mst008 Papić, 2013, The role of Djp1 in import of the mitochondrial protein Mim1 demonstrates specificity between a cochaperone and its substrate protein, Mol. Cell. Biol., 33, 4083, 10.1128/MCB.00227-13 Hansen, 2018, An ER surface retrieval pathway safeguards the import of mitochondrial membrane proteins in yeast, Science, 361, 1118, 10.1126/science.aar8174 Caplan, 1992, Ydj1 facilitates polypeptide translocation across different intracellular membranes by conserved mechanism, Cell, 71, 1143, 10.1016/S0092-8674(05)80063-7 Jores, 2016, Characterization of the targeting signal in mitochondrial β-barrel proteins, Nat. Commun., 7, 12036, 10.1038/ncomms12036 Becker, 2011, The mitochondrial import protein Mim1 promotes biogenesis of multispanning outer membrane proteins, J. Cell Biol., 194, 387, 10.1083/jcb.201102044 Papić, 2011, Multispan mitochondrial outer membrane protein Ugo1 follows a unique Mim1-dependent import pathway, J. Cell Biol., 194, 397, 10.1083/jcb.201102041 Hettema, 1998, The cytosolic DnaJ-like protein Djp1 is involved specifically in peroxisomal protein import, J. Cell Biol., 142, 421, 10.1083/jcb.142.2.421 Yogev, 2007, Translation-coupled translocation of yeast fumarase into mitochondria in vivo, J. Biol. Chem., 282, 29222, 10.1074/jbc.M704201200 Williams, 2014, Targeting and plasticity of mitochondrial proteins revealed by proximity-specific ribosome profiling, Science, 346, 748, 10.1126/science.1257522 Gehrke, 2015, PINK1 and Parkin control localized translation of respiratory chain component mRNAs on mitochondria outer membrane, Cell Metab., 21, 95, 10.1016/j.cmet.2014.12.007 Gold, 2017, Visualization of cytosolic ribosomes on the surface of mitochondria by electron cryotomography, EMBO Rep., 18, 1786, 10.15252/embr.201744261 Lapointe, 2018, Multi-omics reveal specific targets of the RNA-binding protein Puf3p and its orchestration of mitochondrial biogenesis, Cell Syst., 6, 125, 10.1016/j.cels.2017.11.012 Marc, 2002, Genome-wide analysis of mRNAs targeted to yeast mitochondria, EMBO Rep., 3, 159, 10.1093/embo-reports/kvf025 Zahedi, 2006, Proteomic analysis of the yeast mitochondrial outer membrane reveals accumulation of a subclass of preproteins, Mol. Biol. Cell, 17, 1436, 10.1091/mbc.e05-08-0740 Eliyahu, 2010, Tom20 mediates localization of mRNAs to mitochondria in a translation-dependent manner, Mol. Cell. Biol., 30, 284, 10.1128/MCB.00651-09 Garcia, 2010, Mitochondrial presequence and open reading frame mediate asymmetric localization of messenger RNA, EMBO Rep., 11, 285, 10.1038/embor.2010.17 Fünfschilling, 1999, Nascent polypeptide-associated complex stimulates protein import into yeast mitochondria, Mol. Biol. Cell, 10, 3289, 10.1091/mbc.10.10.3289 Lesnik, 2014, OM14 is a mitochondrial receptor for cytosolic ribosomes that supports co-translational import into mitochondria, Nat. Commun., 5, 5711, 10.1038/ncomms6711 Lahiri, 2014, A conserved endoplasmic reticulum membrane protein complex (EMC) facilitates phospholipids transfer from the ER to mitochondria, PLoS Biol., 12, 10.1371/journal.pbio.1001969 Murley, 2015, Ltc1 is an ER-localized sterol transporter and a component of ER-mitochondria and ER-vacuole contacts, J. Cell Biol., 209, 539, 10.1083/jcb.201502033 Eisenberg-Bord, 2016, A tether is a tether is a tether: tethering at membrane contact sites, Dev. Cell, 39, 395, 10.1016/j.devcel.2016.10.022 Murley, 2016, The emerging network of mitochondria-organelle contacts, Mol. Cell, 61, 648, 10.1016/j.molcel.2016.01.031 Ellenrieder, 2016, Separating mitochondrial protein assembly and endoplasmic reticulum tethering by selective coupling of Mdm10, Nat. Commun., 7, 10.1038/ncomms13021 Ellenrieder, 2017, Connection of protein transport and organelle contact sites in mitochondria, J. Mol. Biol., 429, 2148, 10.1016/j.jmb.2017.05.023 González Montoro, 2018, Vps39 interacts with Tom40 to establish one of two functionally distinct vacuole-mitochondria contact sites, Dev. Cell, 45, 621, 10.1016/j.devcel.2018.05.011 Yogev, 2011, Dual targeting of mitochondrial proteins: mechanism, regulation and function, Biochim. Biophys. Acta, 1808, 1012, 10.1016/j.bbamem.2010.07.004 Friedman, 2018, Lipid homeostasis is maintained by dual targeting of the mitochondrial PE biosynthesis enzyme to the ER, Dev. Cell, 44, 261, 10.1016/j.devcel.2017.11.023 Schuldiner, 2008, The GET complex mediates insertion of tail-anchored proteins into the ER membrane, Cell, 134, 634, 10.1016/j.cell.2008.06.025 Okreglak, 2014, The conserved AAA ATPase Msp1 confers organelle specificity to tail-anchored proteins, Proc. Natl. Acad. Sci. U. S. A., 111, 8019, 10.1073/pnas.1405755111 Chen, 2014, Msp1/ATAD1 maintains mitochondrial function by facilitating the degradation of mislocalized tail-anchored proteins, EMBO J., 33, 1548, 10.15252/embj.201487943 Zabezhinsky, 2016, An essential role for COPI in mRNA localization to mitochondria and mitochondrial function, Cell Rep., 15, 540, 10.1016/j.celrep.2016.03.053 Vitali, 2018, The GET pathway can increase the risk of mitochondrial outer membrane proteins to be mistargeted to the ER, J. Cell Sci., 131, 10.1242/jcs.211110 Costa, 2018, Defining the physiological role of SRP in protein-targeting efficiency and specificity, Science, 359, 689, 10.1126/science.aar3607 Gamerdinger, 2015, The principle of antagonism ensures protein targeting specificity at the endoplasmic reticulum, Science, 348, 201, 10.1126/science.aaa5335 Sugiura, 2017, Newly born peroxisomes are a hybrid of mitochondrial and ER-derived pre-peroxisomes, Nature, 542, 251, 10.1038/nature21375 Denic, 2013, Endoplasmic reticulum targeting and insertion of tail-anchored membrane proteins by the GET pathway, Cold Spring Harb. Perspect. Biol., 5, 10.1101/cshperspect.a013334 Cho, 2018, Substrate relay in an Hsp70–cochaperone cascade safeguards tail-anchored membrane protein targeting, EMBO J., 37, 10.15252/embj.201899264 Wang, 2010, A chaperone cascade sorts proteins for posttranslational membrane insertion into the endoplasmic reticulum, Mol. Cell, 40, 159, 10.1016/j.molcel.2010.08.038 Aviram, 2016, The SND proteins constitute an alternative targeting route to the endoplasmic reticulum, Nature, 540, 134, 10.1038/nature20169 Guna, 2018, The ER membrane protein complex is a transmembrane domain insertase, Science, 359, 470, 10.1126/science.aao3099 Itakura, 2016, Ubiquilins chaperone and triage mitochondrial membrane proteins for degradation, Mol. Cell, 63, 21, 10.1016/j.molcel.2016.05.020 Cichocki, 2018, Pex19 is involved in importing dually targeted tail-anchored proteins to both mitochondria and peroxisomes, Traffic, 19, 770, 10.1111/tra.12604 Farré, 2019, Peroxisome biogenesis, membrane contact sites, and quality control, EMBO Rep., 20, 10.15252/embr.201846864 Horie, 2002, Characterization of signal that directs C-tail-anchored proteins to mammalian mitochondrial outer membrane, Mol. Biol. Cell, 13, 1615, 10.1091/mbc.01-12-0570 Beilharz, 2003, Bipartitite signals mediate subcellular targeting of tail-anchored membrane proteins in Saccharomyces cerevisiae, J. Biol. Chem., 278, 8219, 10.1074/jbc.M212725200 Wohlever, 2017, Msp1 is a membrane protein dislocase for tail-anchored proteins, Mol. Cell, 67, 194, 10.1016/j.molcel.2017.06.019 Harbauer, 2014, The protein import machinery of mitochondria – a regulatory hub in metabolism, stress and disease, Cell Metab., 4, 357, 10.1016/j.cmet.2014.01.010 Ben-Menachem, 2018, Yeast aconitase mitochondrial import is modulated by interactions of its C and N-terminal domains and Ssa1/2 (Hsp70), Sci. Rep., 8, 5903, 10.1038/s41598-018-24068-w Avadhani, 2011, Bimodal targeting of cytochrome P450s to endoplasmic reticulum and mitochondria: the concept of chimeric signals, FEBS J., 278, 4218, 10.1111/j.1742-4658.2011.08356.x Nargund, 2012, Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation, Science, 337, 587, 10.1126/science.1223560 Chatterjee, 2016, MOF acetyl transferase regulates transcription and respiration in mitochondria, Cell, 167, 722, 10.1016/j.cell.2016.09.052 Zemanovic, 2018, Dynamic phosphorylation of the C-terminus of Hsp70 regulates the mitochondrial import of SOD2 and redox balance, Cell Rep., 25, 2605, 10.1016/j.celrep.2018.11.015 Kellems, 1975, Cytosplasmic-type 80S ribosomes associated with yeast mitochondria. IV. Attachment of ribosomes to the outer membrane of isolated mitochondria, J. Cell Biol., 65, 1, 10.1083/jcb.65.1.1 Garcia-Rodriguez, 2007, Puf3p, a Pumilio family RNA binding protein, localizes to mitochondria and regulates mitochondrial biogenesis and motility in budding yeast, J. Cell Biol., 176, 197, 10.1083/jcb.200606054 Gerber, 2004, Extensive association of functionally and cytotopically related mRNAs with PUF family RNA-binding proteins in yeast, PLoS Biol., 2, E79, 10.1371/journal.pbio.0020079 Saint-Georges, 2008, Yeast mitochondrial biogenesis: a role of the PUF RNA-binding protein Puf3p in mRNA localization, PLoS One, 3, 10.1371/journal.pone.0002293 Lee, 2015, Glucose-regulated phosphorylation of the PUF protein Puf3 regulates the translational fate of its bound mRNAs and association with RNA granules, Cell Rep., 11, 1638, 10.1016/j.celrep.2015.05.014 Segev, 2018, Specialized ribosomes and specific ribosomal protein paralogs control translation of mitochondrial proteins, J. Cell Biol., 217, 117, 10.1083/jcb.201706059 Gold, 2014, Visualizing active membrane protein complexes by electron cytotomography, Nat. Commun., 5, 4129, 10.1038/ncomms5129 Zhang, 2017, Two chaperones locked in an embrace: structure and function of the ribosome-associated complex RAC, Nat. Struct. Mol. Biol., 24, 611, 10.1038/nsmb.3435 George, 1998, The yeast nascent polypeptide-associated complex initiates protein targeting to mitochondria in vivo, Proc. Natl. Acad. Sci. U. S. A., 95, 2296, 10.1073/pnas.95.5.2296 Ponce-Rojas, 2017, αβ′-NAC cooperates with Sam37 to mediate early stages of mitochondrial protein import, FEBS J., 284, 814, 10.1111/febs.14024 Klein, 2012, Characterization of the insertase for β-barrel proteins of the outer mitochondrial membrane, J. Cell Biol., 199, 599, 10.1083/jcb.201207161 Höhr, 2018, Membrane protein insertion through a mitochondrial β-barrel gate, Science, 359, 10.1126/science.aah6834 Qiu, 2013, Coupling of mitochondrial import and export translocases by receptor-mediated supercomplex formation, Cell, 154, 596, 10.1016/j.cell.2013.06.033 Wenz, 2015, Sam37 is crucial for formation of the mitochondrial TOM–SAM supercomplex, thereby promoting β-barrel biogenesis, J. Cell Biol., 210, 1047, 10.1083/jcb.201504119 Paasch, 2018, Failed mitochondrial import and impaired proteostasis trigger SUMOylation of mitochondria proteins, J. Biol. Chem., 293, 599, 10.1074/jbc.M117.817833 Wrobel, 2015, Mistargeted mitochondrial proteins activate a proteostatic response in the cytosol, Nature, 524, 485, 10.1038/nature14951 Wang, 2015, A cytosolic network suppressing mitochondria-mediated proteostatic stress and cell death, Nature, 524, 481, 10.1038/nature14859 Weidberg, 2018, MitoCPR – a surveillance pathway that protects mitochondria in response to protein import stress, Science, 360, 10.1126/science.aan4146 Izawa, 2012, Roles of Dom34:Hbs1 in nonstop protein clearance from translocators for normal organelle protein influx, Cell Rep., 2, 447, 10.1016/j.celrep.2012.08.010 Izawa, 2017, Cytosolic protein Vms1 links ribosome quality control to mitochondrial and cellular homeostasis, Cell, 171, 890, 10.1016/j.cell.2017.10.002 Kostova, 2017, CAT-tailing as a fail-safe mechanism for efficient degradation of stalled nascent polypeptides, Science, 357, 414, 10.1126/science.aam7787 Verma, 2018, Vms1 and ANKZF1 peptidyl-tRNA hydrolases release nascent chains from stalled ribosomes, Nature, 557, 446, 10.1038/s41586-018-0022-5 Zurita Rendón, 2018, Vms1p is a release factor for the ribosome-associated quality control complex, Nat. Commun., 9, 2197, 10.1038/s41467-018-04564-3 Bhangoo, 2007, Multiple 40-kDa heat shock protein chaperones function in Tom70-dependent mitochondrial import, Mol. Biol. Cell, 18, 3414, 10.1091/mbc.e07-01-0088 Kampinga, 2010, The HSP70 chaperone machinery: J proteins as drivers of functional specificity, Nat. Rev. Mol. Cell Biol., 11, 579, 10.1038/nrm2941 Chewawiwat, 1999, Characterization of the novel mitochondrial protein import component, Tom34, in mammalian cells, J. Biochem., 125, 721, 10.1093/oxfordjournals.jbchem.a022342