Erv1 Mediates the Mia40-dependent Protein Import Pathway and Provides a Functional Link to the Respiratory Chain by Shuttling Electrons to Cytochrome c
Abstract
Unlike matrix-targeted or inner membrane proteins, those that are targeted to the mitochondrial intermembrane space (IMS) do not require ATP or the inner membrane electrochemical potential. Their import is mediated primarily by the essential IMS protein Mia40/Tim40. Here, we show that the mitochondrial flavin adenine dinucleotide (FAD)-linked sulfhydryl oxidase Erv1 (essential for respiration and vegetative growth 1) plays a central role in the biogenesis of small, cysteine proteins of the IMS that are import substrates for Mia40. In a temperature-sensitive strain of Erv1, steady-state levels of small translocases of the inner membrane (Tims) are specifically affected when cells are grown at the non-permissive temperature. Furthermore, mitochondria isolated from the erv1-ts show a specific import and assembly defect for the small Tims but not in any other protein import pathway. Erv1 does not directly oxidise the small Tims, as thiol trapping assays show that the small Tims can still be oxidised in erv1-ts cells grown at the non-permissive temperature and in isolated mitochondria from this strain. Moreover, addition of pure Erv1 into erv1-ts mitochondria lacking the endogenous protein restores import and assembly of the small Tims only to an extent, arguing for a cascade of interactions with Erv1 rather than for a direct interaction of Erv1 with the small Tims. Cytochrome c (cyt c) is the in vivo oxidase for Erv1, as yeast cells mutated in cyt c cannot grow under anaerobic conditions. Therefore, Erv1 functionally links the Mia40-dependent import pathway to the Mia40-independent cyt c import pathway transferring electrons from the incoming precursors to cyt c as an acceptor. In this context, the protein import process is linked to the respiratory chain via the communication of Erv1 with cyt c.
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Erv1 shuttles electrons from Mia40 to cytochrome c of the ETC to maintain Mia40's oxidized state.
“Erv1 serves to shuttle electrons from Mia40 to cytochrome c of the ETC in order to maintain its oxidized state (10, 40, 105, 292).”
From Redox regulation of mitochondrial function (2012) · cites this paper as [10]
Cites
Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form
Schägger, H., & von JAGOW, G. (1991) · Analytical Biochemistry · doi:10.1016/0003-2697(91)90094-a · Cited by 2,237 · see citing works
A Disulfide Relay System in the Intermembrane Space of Mitochondria that Mediates Protein Import
Mesecke, N., Terziyska, N., Kozany, C., Baumann, F., Neupert, W., Hell, K., & Herrmann, J. M. (2005) · Cell · doi:10.1016/j.cell.2005.04.011 · Cited by 557 · see citing works
Protein Disulfide Bond Formation in Prokaryotes
Kadokura, H., Katzen, F., & Beckwith, J. (2003) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.72.121801.161459 · Cited by 541 · see citing works
Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins
Chacińska, A., Pfannschmidt, S., Wiedemann, N., Kozjak‐Pavlovic, V., Szklarz, L. K. S., Schulze‐Specking, A., Truscott, K. N., Guiard, B., Meisinger, C., & Pfanner, N. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600389 · Cited by 464 · see citing works
Oxidative Protein Folding Is Driven by the Electron Transport System
Bader, M. W., Muse, W. B., Ballou, D. P., Gassner, C., & Bardwell, J. C. A. (1999) · Cell · doi:10.1016/s0092-8674(00)81016-8 · Cited by 385 · see citing works
Oxygen‐induced maturation of SOD1: a key role for disulfide formation by the copper chaperone CCS
Furukawa, Y., Torres, A. S., & O’Halloran, T. V. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600276 · Cited by 369 · see citing works
Import of Mitochondrial Carriers Mediated by Essential Proteins of the Intermembrane Space
Koehler, C. M., Jarosch, E., Tokatlidis, K., Schmid, K., Schweyen, R. J., & Schatz, G. (1998) · Science · doi:10.1126/science.279.5349.369 · Cited by 326 · see citing works
Self-citationLange, H., Lisowsky, T., Gerber, J., Mühlenhoff, U., Kispál, G., & Lill, R. (2001) · EMBO Reports · doi:10.1093/embo-reports/kve161 · Cited by 269 · see citing works
Self-citationFactors Controlling the Uptake of Yeast Copper/Zinc Superoxide Dismutase into Mitochondria
Field, L. S., Furukawa, Y., O’Halloran, T. V., & Culotta, V. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304296200 · Cited by 230 · see citing works
The Tim9p–Tim10p complex binds to the transmembrane domains of the ADP/ATP carrier
Curran, S. P., Leuenberger, D., Oppliger, W., & Koehler, C. M. (2002) · The EMBO Journal · doi:10.1093/emboj/21.5.942 · Cited by 220 · see citing works
Identification of Tim40 That Mediates Protein Sorting to the Mitochondrial Intermembrane Space
Naoé, M., Ohwa, Y., Ishikawa, D., Ohshima, C., Nishikawa, S., Yamamoto, H., & Endo, T. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m410272200 · Cited by 207 · see citing works
Tim9p, an essential partner subunit of Tim10p for the import of mitochondrial carrier proteins
Koehler, C. M., Merchant, S., Oppliger, W., Schmid, K., Jarosch, E., Dolfini, L., Junne, T., Schatz, G., & Tokatlidis, K. (1998) · The EMBO Journal · doi:10.1093/emboj/17.22.6477 · Cited by 204 · see citing works
Self-citationComplete pathway for protein disulfide bond formation encoded by poxviruses
Senkevich, T. G., White, C. L., Koonin, E. V., & Moss, B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.062163799 · Cited by 182 · see citing works
A new FAD-binding fold and intersubunit disulfide shuttle in the thiol oxidase Erv2p
Gross, E., Sevier, C. S., Vala, A., Kaiser, C. A., & Fass, D. (2001) · Nature Structural Biology · doi:10.1038/nsb740 · Cited by 181 · see citing works
Terziyska, N., Lutz, T., Kozany, C., Mokranjac, D., Mesecke, N., Neupert, W., Herrmann, J. M., & Hell, K. (2004) · FEBS Letters · doi:10.1016/j.febslet.2004.11.072 · Cited by 173 · see citing works
Erv1p from Saccharomyces cerevisiae is a FAD‐linked sulfhydryl oxidase
Lee, J.-E., Hofhaus, G., & Lisowsky, T. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01767-1 · Cited by 167 · see citing works
Self-citationTim9, a new component of the TIM22·54 translocase in mitochondria
Adam, A. C., Endres, M., Sirrenberg, C., Lottspeich, F., Neupert, W., & Brunner, M. (1999) · The EMBO Journal · doi:10.1093/emboj/18.2.313 · Cited by 147 · see citing works
Curran, S. P., Leuenberger, D., Schmidt, E., & Koehler, C. M. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200205124 · Cited by 146 · see citing works
Farrell, S. R., & Thorpe, C. (2005) · Biochemistry · doi:10.1021/bi0479555 · Cited by 144 · see citing works
Folding Studies of Cox17 Reveal an Important Interplay of Cysteine Oxidation and Copper Binding
Arnesano, F., Balatri, E., Banci, L., Bertini, I., & Winge, D. R. (2005) · Structure · doi:10.1016/j.str.2005.02.015 · Cited by 143 · see citing works
Import of small Tim proteins into the mitochondrial intermembrane space
Lutz, T., Neupert, W., & Herrmann, J. M. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg421 · Cited by 128 · see citing works
Oxygen regulation of anaerobic and aerobic genes mediated by a common factor in yeast.
Lowry, C. V., & Zitomer, R. S. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.19.6129 · Cited by 121 · see citing works
Nóbrega, M. P., Bandeira, S. C. B., Beers, J., & Tzagoloff, A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m207348200 · Cited by 121 · see citing works
Functional TIM10 Chaperone Assembly Is Redox-regulated in Vivo
Lu, H., Allen, S. P., Wardleworth, L., Savory, P., & Tokatlidis, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313045200 · Cited by 120 · see citing works
Self-citationKurz, M., Martin, H., Rassow, J., Pfanner, N., & Ryan, M. T. (1999) · Molecular Biology of the Cell · doi:10.1091/mbc.10.7.2461 · Cited by 119 · see citing works
Kobayashi, T., & Ito, K. (1999) · The EMBO Journal · doi:10.1093/emboj/18.5.1192 · Cited by 111 · see citing works
The Role of Hot13p and Redox Chemistry in the Mitochondrial TIM22 Import Pathway
Curran, S. P., Leuenberger, D., Leverich, E. P., Hwang, D. K., Beverly, K. N., & Koehler, C. M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404878200 · Cited by 87 · see citing works
Allen, S. P., Lu, H., Thornton, D. J., & Tokatlidis, K. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306027200 · Cited by 85 · see citing works
Self-citationApocytochrome c requires the TOM complex for translocation across the mitochondrial outer membrane
Diekert, K., de Kroon, A. I. P. M., Ahting, U., Niggemeyer, B., Neupert, W., KRUIJFF, B. D., & Lill, R. (2001) · The EMBO Journal · doi:10.1093/emboj/20.20.5626 · Cited by 85 · see citing works
Assembly of Tim9 and Tim10 into a Functional Chaperone
Vial, S., Lu, H., Allen, S. P., Savory, P., Thornton, D. J., Sheehan, J. K., & Tokatlidis, K. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202310200 · Cited by 82 · see citing works
Self-citationJan, P., Esser, K., Pratje, E., & Michaelis, G. (2000) · Molecular and General Genetics MGG · doi:10.1007/s004380051192 · Cited by 78 · see citing works
Functional reconstitution of the import of the yeast ADP/ATP carrier mediated by the TIM10 complex
Luciano, P., Vial, S., Vergnolle, M., Dyall, S. D., Robinson, D. R., & Tokatlidis, K. (2001) · The EMBO Journal · doi:10.1093/emboj/20.15.4099 · Cited by 61 · see citing works
Self-citationThe Structural Basis of the TIM10 Chaperone Assembly
Lu, H., Golovanov, A. P., Alcock, F., Grossmann, J. G., Allen, S. P., Lian, L., & Tokatlidis, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313046200 · Cited by 61 · see citing works
Self-citationA Disulfide Relay System in Mitochondria
Tokatlidis, K. (2005) · Cell · doi:10.1016/j.cell.2005.06.019 · Cited by 58 · see citing works
Self-citationChapter 20 Protein Import into Isolated Yeast Mitochondria
Glick, B. S. (1991) · Methods in cell biology · doi:10.1016/s0091-679x(08)61693-3 · Cited by 51 · see citing works
Biogenesis of Yeast Mitochondrial Cytochrome c: A Unique Relationship to the TOM Machinery
Wiedemann, N., Kozjak‐Pavlovic, V., Prinz, T., Ryan, M. T., Meisinger, C., Pfanner, N., & Truscott, K. N. (2003) · Journal of Molecular Biology · doi:10.1016/s0022-2836(03)00118-9 · Cited by 38 · see citing works
Esser, K., Pratje, E., & Michaelis, G. (1996) · Molecular and General Genetics MGG · doi:10.1007/bf02173009 · Cited by 37 · see citing works
Vergnolle, M., Sawney, H., Junne, T., Dolfini, L., & Tokatlidis, K. (2004) · Biochemical Journal · doi:10.1042/bj20040650 · Cited by 14 · see citing works
Self-citationDeletion of six open reading frames from the left arm of chromosome IV of Saccharomyces cerevisiae
Tuller, G., Prein, B., Jandrositz, A., Daum, G., & Kohlwein, S. D. (1999) · Yeast · doi:10.1002/(sici)1097-0061(19990915)15:12 · Cited by 8 · see citing works
Self-citationCollet, J., & Bardwell, J. C. A. (2002) · Nature Structural Biology · doi:10.1038/nsb0102-2 · Cited by 6 · see citing works
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Neupert, W., & Herrmann, J. M. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.052705.163409 · Cited by 1,486 · see citing works
Mitochondrial protein import: from proteomics to functional mechanisms
Schmidt, O., Pfanner, N., & Meisinger, C. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2959 · Cited by 717 · see citing works
Robinson, N. J., & Winge, D. R. (2010) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-030409-143539 · Cited by 708 · see citing works
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Handy, D. E., & Loscalzo, J. (2012) · Antioxidants & Redox Signaling · doi:10.1089/ars.2011.4123 · Cited by 588 · see citing works
Maturation of Iron-Sulfur Proteins in Eukaryotes: Mechanisms, Connected Processes, and Diseases
Lill, R., & Mühlenhoff, U. (2008) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.052705.162653 · Cited by 595 · see citing works
Hüttemann, M., Pecina, P., Rainbolt, M., Sanderson, T. H., Kagan, V. E., Samavati, L., Doan, J. W., & Lee, I. (2011) · Mitochondrion · doi:10.1016/j.mito.2011.01.010 · Cited by 522 · see citing works
Iron-Sulfur Protein Biogenesis in Eukaryotes: Components and Mechanisms
Lill, R., & Mühlenhoff, U. (2006) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.22.010305.104538 · Cited by 365 · see citing works
Chemistry and Enzymology of Disulfide Cross-Linking in Proteins
Fass, D., & Thorpe, C. (2018) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00123 · Cited by 321 · see citing works
Multiple pathways for sorting mitochondrial precursor proteins
Bolender, N., Sickmann, A., Wagner, R., Meisinger, C., & Pfanner, N. (2008) · EMBO Reports · doi:10.1038/sj.embor.7401126 · Cited by 319 · see citing works
Mitochondrial copper metabolism and delivery to cytochrome <i>c</i> oxidase
Horn, D., & Barrientos, A. (2008) · IUBMB Life · doi:10.1002/iub.50 · Cited by 283 · see citing works
Hu, J., Dong, L., & Outten, C. E. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m803028200 · Cited by 273 · see citing works
Mitochondrial protein import: Common principles and physiological networks
Dudek, J., Rehling, P., & van der Laan, M. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.05.028 · Cited by 269 · see citing works
MIA40 is an oxidoreductase that catalyzes oxidative protein folding in mitochondria
Banci, L., Bertini, I., Cefaro, C., Ciofi‐Baffoni, S., Gallo, A., Martinelli, M., Sideris, D. P., Katrakili, N., & Tokatlidis, K. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1553 · Cited by 260 · see citing works
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Riemer, J., Bulleid, N. J., & Herrmann, J. M. (2009) · Science · doi:10.1126/science.1170653 · Cited by 250 · see citing works
Kalpage, H. A., Bazylianska, V., Recanati, M., Fite, A., Liu, J., Wan, J., Mantena, N., Malek, M. H., Podgorski, I., Heath, E., et al. (2018) · The FASEB Journal · doi:10.1096/fj.201801417r · Cited by 226 · see citing works
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Baker, M. J., Frazier, A. E., Gulbis, J. M., & Ryan, M. T. (2007) · Trends in Cell Biology · doi:10.1016/j.tcb.2007.07.010 · Cited by 213 · see citing works
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Hangen, E., Féraud, O., Lachkar, S., Mou, H., Doti, N., Fimia, G. M., Lam, N.-V., Zhu, C., Godin, I., Müller, K., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.04.020 · Cited by 203 · see citing works
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Bien, M., Longen, S., Wagener, N., Chwalla, I., Herrmann, J. M., & Riemer, J. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.01.017 · Cited by 179 · see citing works
Cellular copper distribution: a mechanistic systems biology approach
Banci, L., Bertini, I., Cantini, F., & Ciofi‐Baffoni, S. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0330-x · Cited by 173 · see citing works
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Le Moan, N., Clement, G., Le Maout, S., Tacnet, F., & Toledano, M. B. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m513346200 · Cited by 170 · see citing works
Intermembrane Space Proteome of Yeast Mitochondria
Vögtle, F. ‐., Burkhart, J. M., Rao, S., Gerbeth, C., Hinrichs, J., Martinou, J., Chacińska, A., Sickmann, A., Zahedi, R. P., & Meisinger, C. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m112.021105 · Cited by 163 · see citing works
Identification of the Signal Directing Tim9 and Tim10 into the Intermembrane Space of Mitochondria
Milenkovic, D., Ramming, T., Müller, J. M., Wenz, L.-S., Gebert, N., Schulze‐Specking, A., Stojanovski, D., Rospert, S., & Chacińska, A. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-11-1108 · Cited by 167 · see citing works
Novel Mitochondrial Intermembrane Space Proteins as Substrates of the MIA Import Pathway
Gabriel, K., Milenkovic, D., Chacińska, A., Müller, J., Guiard, B., Pfanner, N., & Meisinger, C. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.10.038 · Cited by 166 · see citing works
The Ubiquitin-Proteasome System Regulates Mitochondrial Intermembrane Space Proteins
Bragoszewski, P., Gornicka, A., Sztolsztener, M. E., & Chacinska, A. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01579-12 · Cited by 149 · see citing works
A role for cytochrome c and cytochrome c peroxidase in electron shuttling from Erv1
Dabir, D. V., Leverich, E. P., Kim, S., Tsai, F. D., Hirasawa, M., Knaff, D. B., & Koehler, C. M. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601909 · Cited by 162 · see citing works
The Intermembrane Space of Mitochondria
Herrmann, J. M., & Riemer, J. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.3063 · Cited by 146 · see citing works
Structural insight into the mitochondrial protein import system.
Endo, T., Yamano, K., & Kawano, S. (2011) · Biochimica et Biophysica Acta · doi:10.1016/j.bbamem.2010.07.018 · Cited by 142 · see citing works
Modjtahedi, N., Tokatlidis, K., Dessen, P., & Kroemer, G. (2016) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2015.12.004 · Cited by 122 · see citing works
Self-citationFischer, M., Horn, S., Belkacemi, A., Kojer, K., Petrungaro, C., Habich, M., Ali, M., Küttner, V., Bien, M., Kauff, F., et al. (2013) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-12-0862 · Cited by 124 · see citing works
Mitochondrial Disulfide Relay: Redox-regulated Protein Import into the Intermembrane Space
Herrmann, J. M., & Riemer, J. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.r111.270678 · Cited by 122 · see citing works
Thirty years of protein translocation into mitochondria: Unexpectedly complex and still puzzling
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Cytochrome c biogenesis in mitochondria
Giegé, P., Grienenberger, J. M., & Bonnard, G. (2007) · Mitochondrion · doi:10.1016/j.mito.2007.10.001 · Cited by 115 · see citing works
Mitochondrial protein import and human health and disease
MacKenzie, J. A., & Payne, R. M. (2006) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2006.12.002 · Cited by 112 · see citing works
The Erv1–Mia40 disulfide relay system in the intermembrane space of mitochondria
Hell, K. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2007.12.005 · Cited by 110 · see citing works
Mitochondrial protein transport in health and disease
Kang, Y., Fielden, L. F., & Stojanovski, D. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.07.028 · Cited by 109 · see citing works
Morse, P. T., Arroum, T., Wan, J., Pham, L., Vaishnav, A., Bell, J., Pavelich, L., Malek, M. H., Sanderson, T. H., Edwards, B. F. P., et al. (2024) · Cells · doi:10.3390/cells13060493 · Cited by 111 · see citing works
Iron–Sulfur Clusters: Biogenesis, Molecular Mechanisms, and Their Functional Significance
Xu, X. M., & Møller, S. G. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3259 · Cited by 102 · see citing works
Backes, S., & Herrmann, J. M. (2017) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2017.00083 · Cited by 102 · see citing works
Kawano, S., Yamano, K., Naoé, M., Momose, T., Terao, K., Nishikawa, S., Watanabe, N., & Endo, T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901793106 · Cited by 100 · see citing works
Cysteine-mediated redox signalling in the mitochondria
Bak, D. W., & Weerapana, E. (2014) · Molecular BioSystems · doi:10.1039/c4mb00571f · Cited by 100 · see citing works
Gandhi, C. R., Chaillet, J. R., Nalesnik, M. A., Kumar, S., Dangi, A., Demetris, A. J., Ferrell, R. E., Wu, T., Divanovic, S., Stankeiwicz, T., et al. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.10.008 · Cited by 99 · see citing works
Atp23 biogenesis reveals a chaperone‐like folding activity of Mia40 in the IMS of mitochondria
Weckbecker, D., Longen, S., Riemer, J., & Herrmann, J. M. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.263 · Cited by 97 · see citing works
Meisinger, C., Wiedemann, N., Rissler, M., Strub, A., Milenkovic, D., Schönfisch, B., Müller, H., Kozjak‐Pavlovic, V., & Pfanner, N. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602679200 · Cited by 97 · see citing works
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Import of Proteins into Mitochondria
Stojanovski, D., Pfanner, N., & Wiedemann, N. (2007) · Methods in cell biology · doi:10.1016/s0091-679x(06)80036-1 · Cited by 95 · see citing works
Catch me if you can! Oxidative protein trapping in the intermembrane space of mitochondria
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Mitochondrial Protein Quality Control Mechanisms
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Reddehase, S., Grumbt, B., Neupert, W., & Hell, K. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.10.088 · Cited by 92 · see citing works
Grumbt, B., Stroobant, V., Terziyska, N., Israel, L., & Hell, K. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m707439200 · Cited by 91 · see citing works
The MIA pathway: A tight bond between protein transport and oxidative folding in mitochondria
Stojanovski, D., Brągoszewski, P., & Chacińska, A. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.04.014 · Cited by 91 · see citing works
Protein trafficking at the crossroads to mitochondria
Wasilewski, M., Chojnacka, K., & Chacińska, A. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2016.10.019 · Cited by 89 · see citing works
Nuclear–mitochondrial interaction
Cannino, G., Liegro, C. M. D., & Rinaldi, A. M. (2007) · Mitochondrion · doi:10.1016/j.mito.2007.07.001 · Cited by 89 · see citing works
Cooperation of translocase complexes in mitochondrial protein import
Kutik, S., Guiard, B., Meyer, H. E., Wiedemann, N., & Pfanner, N. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200708199 · Cited by 88 · see citing works
Biogenesis of the Essential Tim9–Tim10 Chaperone Complex of Mitochondria
Milenkovic, D., Gabriel, K., Guiard, B., Schulze‐Specking, A., Pfanner, N., & Chacińska, A. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m703294200 · Cited by 85 · see citing works
Sideris, D. P., & Tokatlidis, K. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05880.x · Cited by 84 · see citing works
Self-citationStojanovski, D., Milenkovic, D., Müller, J. M., Gabriel, K., Schulze‐Specking, A., Baker, M. J., Ryan, M. T., Guiard, B., Pfanner, N., & Chacińska, A. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200804095 · Cited by 82 · see citing works
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Sideris, D. P., & Tokatlidis, K. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3157 · Cited by 81 · see citing works
Self-citationGenerating disulfides with the Quiescin-sulfhydryl oxidases
Heckler, E. J., Rancy, P. C., Kodali, V. K., & Thorpe, C. (2007) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2007.10.002 · Cited by 81 · see citing works
New moonlighting functions of mitochondrial cytochrome c in the cytoplasm and nucleus
González‐Arzola, K., Velázquez‐Cruz, A., Guerra‐Castellano, A., Casado‐Combreras, M. Á., Pérez‐Mejías, G., Dı́az-Quintana, A., Díaz‐Moreno, I., & la Rosa, M. Á. D. (2019) · FEBS Letters · doi:10.1002/1873-3468.13655 · Cited by 78 · see citing works
The zinc‐binding protein Hot13 promotes oxidation of the mitochondrial import receptor Mia40
Mesecke, N., Bihlmaier, K., Grumbt, B., Longen, S., Terziyska, N., Hell, K., & Herrmann, J. M. (2008) · EMBO Reports · doi:10.1038/embor.2008.173 · Cited by 79 · see citing works
Müller, J. M., Milenkovic, D., Guiard, B., Pfanner, N., & Chacińska, A. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-08-0814 · Cited by 79 · see citing works
Terziyska, N., Grumbt, B., Kozany, C., & Hell, K. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m805035200 · Cited by 78 · see citing works
Assembly of β-barrel proteins in the mitochondrial outer membrane
Höhr, A. I. C., Straub, S. P., Warscheid, B., Becker, T., & Wiedemann, N. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2014.10.006 · Cited by 78 · see citing works
Order within a mosaic distribution of mitochondrial c‐type cytochrome biogenesis systems?
Allen, J. W. A., Jackson, A., Rigden, D. J., Willis, A. C., Ferguson, S. J., & Ginger, M. (2008) · The FEBS Journal · doi:10.1111/j.1742-4658.2008.06380.x · Cited by 88 · see citing works
The mitochondrial protein import machinery has multiple connections to the respiratory chain
Kulawiak, B., Höpker, J., Gebert, M., Guiard, B., Wiedemann, N., & Gebert, N. (2012) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.12.004 · Cited by 77 · see citing works
Peleh, V., Cordat, E., & Herrmann, J. M. (2016) · eLife · doi:10.7554/elife.16177 · Cited by 77 · see citing works
Cellular Disulfide Bond Formation in Bioactive Peptides and Proteins
Patil, N. A., Tailhades, J., Hughes, R., Separovic, F., Wade, J. D., & Hossain, M. A. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms16011791 · Cited by 76 · see citing works
The MIA system for protein import into the mitochondrial intermembrane space
Stojanovski, D., Müller, J. M., Milenkovic, D., Guiard, B., Pfanner, N., & Chacińska, A. (2007) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2007.10.004 · Cited by 76 · see citing works
The Mysterious Multitude: Structural Perspective on the Accessory Subunits of Respiratory Complex I
Padavannil, A., Ayala-Hernandez, M. G., Castellanos-Silva, E. A., & Letts, J. A. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.798353 · Cited by 69 · see citing works
Longen, S., Woellhaf, M. W., Petrungaro, C., Riemer, J., & Herrmann, J. M. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.11.007 · Cited by 70 · see citing works
Balancing oxidative protein folding: The influences of reducing pathways on disulfide bond formation
Kojer, K., & Riemer, J. (2014) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2014.02.004 · Cited by 72 · see citing works
Baker, M. J., Webb, C. T., Stroud, D. A., Palmer, C. S., Frazier, A. E., Guiard, B., Chacińska, A., Gulbis, J. M., & Ryan, M. T. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-09-0903 · Cited by 70 · see citing works
Mitochondrial Biogenesis, Switching the Sorting Pathway of the Intermembrane Space Receptor Mia40
Chacińska, A., Guiard, B., Müller, J. M., Schulze‐Specking, A., Gabriel, K., Kutik, S., & Pfanner, N. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m805356200 · Cited by 69 · see citing works
The sulfhydryl oxidase Erv1 is a substrate of the Mia40‐dependent protein translocation pathway
Terziyska, N., Grumbt, B., Bien, M., Neupert, W., Herrmann, J. M., & Hell, K. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.02.014 · Cited by 69 · see citing works
Reconstitution of the Mia40-Erv1 Oxidative Folding Pathway for the Small Tim Proteins
Tienson, H. L., Dabir, D. V., Neal, S. E., Loo, R. O., Hasson, S. A., Boontheung, P., Kim, S., Loo, J. A., & Koehler, C. M. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-10-1062 · Cited by 69 · see citing works
Hewitt, V. L., Alcock, F., & Lithgow, T. J. (2010) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2010.07.019 · Cited by 66 · see citing works
The MIA Pathway: A Key Regulator of Mitochondrial Oxidative Protein Folding and Biogenesis
Mordas, A. V., & Tokatlidis, K. (2015) · Accounts of Chemical Research · doi:10.1021/acs.accounts.5b00150 · Cited by 67 · see citing works
Self-citationBode, M., Woellhaf, M. W., Bohnert, M., van der Laan, M., Sommer, F., Jung, M., Zimmermann, R., Schroda, M., & Herrmann, J. M. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-11-1526 · Cited by 67 · see citing works
Augmenter of liver regeneration
Gandhi, C. R. (2012) · Fibrogenesis & Tissue Repair · doi:10.1186/1755-1536-5-10 · Cited by 65 · see citing works
Daithankar, V. N., Farrell, S. R., & Thorpe, C. (2009) · Biochemistry · doi:10.1021/bi900347v · Cited by 63 · see citing works
Redox regulation of protein folding in the mitochondrial intermembrane space
Koehler, C. M., & Tienson, H. L. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2008.08.002 · Cited by 62 · see citing works
A disulfide bond in the TIM23 complex is crucial for voltage gating and mitochondrial protein import
Ramesh, A., Peleh, V., Martinez‐Caballero, S., Wollweber, F., Sommer, F., van der Laan, M., Schroda, M., Alexander, R. T., Campo, M. L., & Herrmann, J. M. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201602074 · Cited by 62 · see citing works
Mitochondrial preprotein translocases as dynamic molecular machines
van der Laan, M., Rissler, M., & Rehling, P. (2006) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2006.00134.x · Cited by 61 · see citing works
Thiol switches in mitochondria: operation and physiological relevance
Riemer, J., Schwarzländer, M., Conrad, M., & Herrmann, J. M. (2015) · Biological Chemistry · doi:10.1515/hsz-2014-0293 · Cited by 58 · see citing works
Gross, D., Burgard, C., Reddehase, S., Leitch, J. M., Culotta, V., & Hell, K. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-04-0296 · Cited by 59 · see citing works
Oxidation-driven protein import into mitochondria: Insights and blind spots
Riemer, J., Fischer, M., & Herrmann, J. M. (2011) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2010.06.003 · Cited by 58 · see citing works
Oxygen-dependent activation of Cu,Zn-superoxide dismutase-1
Fetherolf, M. M., Boyd, S. D., Winkler, D. D., & Winge, D. R. (2017) · Metallomics · doi:10.1039/c6mt00298f · Cited by 58 · see citing works
AIF meets the CHCHD4/Mia40-dependent mitochondrial import pathway
Reinhardt, C., Arena, G., Nedara, K., Edwards, R., Brenner, C., Tokatlidis, K., & Modjtahedi, N. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2020.165746 · Cited by 58 · see citing works
Self-citationRole of membrane contact sites in protein import into mitochondria
Horvath, S. E., Rampelt, H., Oeljeklaus, S., Warscheid, B., van der Laan, M., & Pfanner, N. (2014) · Protein Science · doi:10.1002/pro.2625 · Cited by 57 · see citing works
Geldon, S., Fernández‐Vizarra, E., & Tokatlidis, K. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.720656 · Cited by 55 · see citing works
Self-citationAugmenter of liver regeneration: Essential for growth and beyond
Ibrahim, S., & Weiß, T. S. (2018) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2018.12.003 · Cited by 57 · see citing works
Pathways for Sensing and Responding to Hydrogen Peroxide at the Endoplasmic Reticulum
Roscoe, J. M., & Sevier, C. S. (2020) · Cells · doi:10.3390/cells9102314 · Cited by 55 · see citing works
Allen, J. W. A., Ferguson, S. J., & Ginger, M. L. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.07.015 · Cited by 55 · see citing works
Herrmann, J. M., Kauff, F., & Neuhaus, H. E. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2008.05.001 · Cited by 54 · see citing works
Disulphide Bond Formation in the Intermembrane Space of Mitochondria
Deponte, M., & Hell, K. (2009) · The Journal of Biochemistry · doi:10.1093/jb/mvp133 · Cited by 52 · see citing works
Disulfide Bond Formation: Sulfhydryl Oxidase ALR Controls Mitochondrial Biogenesis of Human MIA40
Sztolsztener, M. E., Brewinska, A., Guiard, B., & Chacińska, A. (2012) · Traffic · doi:10.1111/tra.12030 · Cited by 52 · see citing works
Daithankar, V. N., Schaefer, S., Dong, M., Bahnson, B. J., & Thorpe, C. (2010) · Biochemistry · doi:10.1021/bi100912m · Cited by 51 · see citing works
- Authors
- Allen, S., Balabanidou, V., Sideris, D. P., Lisowsky, T., & Tokatlidis, K.
- Affiliations
- University of Manchester (GB)
- University of Crete (GR)
- Corresponding author
- Tokatlidis, Kostas
- Venue
- Journal of Molecular Biology
- Publisher
- Elsevier BV
- Published
- 2005-11
- Volume
- 353
- Issue
- 5
- Pages
- 937-944
- ISSN
- 0022-2836 (ISSN-L)
- OpenAlex
- W2019250081
- Cited by
- 235
- References
- 40
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 7 · 2023: 2 · 2022: 4 · 2021: 13 · 2020: 7 · 2019: 7 · 2018: 2 · 2017: 15 · 2016: 11 · 2015: 11 · 2014: 12 · 2013: 9 · 2012: 18
- FWCI
- 7.28
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Journal of Molecular Biology (publishedVersion)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion)
- Funders
- University of Crete
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- Erv1, Mia40, Tim23, Tim17, electron transfer, mitochondrial protein biogenesis, temperature-sensitive mutants, yeast mitochondria, electron transport chain
- MeSH terms
- Mitochondrial Precursor Protein Import Complex Proteins, Electron Transport, Fungal Proteins, Membrane Proteins, Mitochondria, Temperature, Protein Transport, Mitochondrial Proteins, Saccharomyces cerevisiae Proteins, Mitochondrial Membrane Transport Proteins, Cytochromes c, Oxidoreductases Acting on Sulfur Group Donors, Mitochondrial Membranes
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