Mitochondrial Disulfide Bond Formation Is Driven by Intersubunit Electron Transfer in Erv1 and Proofread by Glutathione
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The disulfide relay system in the intermembrane space of mitochondria is of crucial importance for mitochondrial biogenesis. Major players in this pathway are the oxidoreductase Mia40 that oxidizes substrates and the sulfhydryl oxidase Erv1 that reoxidizes Mia40. To analyze in detail the mechanism of this oxidative pathway and the interplay of its components, we reconstituted the complete process in vitro using purified cytochrome c, Erv1, Mia40, and Cox19. Here, we demonstrate that Erv1 dimerizes noncovalently and that the subunits of this homodimer cooperate in intersubunit electron exchange. Moreover, we show that Mia40 promotes complete oxidation of the substrate Cox19. The efficient formation of disulfide bonds is hampered by the formation of long-lived, partially oxidized intermediates. The generation of these side products is efficiently counteracted by reduced glutathione. Thus, our findings suggest a role for a glutathione-dependent proofreading during oxidative protein folding by the mitochondrial disulfide relay.
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GSH prevents overoxidation of redox-active thiols during disulfide bond formation within the mitochondrial intermembrane space.
“GSH plays an important role in this process by preventing the overoxidation of redox-active thiols during disulfide bond formation within the intermembrane space (40, 292).”
From Redox regulation of mitochondrial function (2012) · cites this paper as [40]
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 [40]
The FAD-containing sulfhydryl oxidase Erv1 maintains the intermembrane protein Mia40 in an oxidized form.
“A crucial component of this system is the FAD-containing sulfhydryl oxidase Erv1, which maintains the intermembrane protein Mia40 in an oxidized form (40, 391).”
From Redox regulation of mitochondrial function (2012) · cites this paper as [40]
Cites
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
Self-citationEssential 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
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
Disulfide Formation in the ER and Mitochondria: Two Solutions to a Common Process
Riemer, J., Bulleid, N. J., & Herrmann, J. M. (2009) · Science · doi:10.1126/science.1170653 · Cited by 250 · see citing works
Self-citationAllen, S., Balabanidou, V., Sideris, D. P., Lisowsky, T., & Tokatlidis, K. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.08.049 · Cited by 235 · see citing works
The disulfide relay system of mitochondria is connected to the respiratory chain
Bihlmaier, K., Mesecke, N., Terziyska, N., Bien, M., Hell, K., & Herrmann, J. M. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200707123 · Cited by 207 · see citing works
Self-citationA 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
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
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
Farrell, S. R., & Thorpe, C. (2005) · Biochemistry · doi:10.1021/bi0479555 · Cited by 144 · see citing works
Wu, C., Dailey, T. A., Dailey, H. A., Wang, B., & Rose, J. P. (2003) · Protein Science · doi:10.1110/ps.0238103 · Cited by 111 · 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
The Erv family of sulfhydryl oxidases
Fass, D. (2007) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2007.11.009 · Cited by 104 · see citing works
Multidomain Flavin-Dependent Sulfhydryl Oxidases
Coppock, D. L., & Thorpe, C. (2006) · Antioxidants and Redox Signaling · doi:10.1089/ars.2006.8.300 · Cited by 99 · 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
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
Stojanovski, 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
Hofhaus, G., Lee, J., Tews, I., Rosenberg, B., & Lisowsky, T. (2003) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2003.03519.x · Cited by 80 · 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
Self-citationMüller, 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
Gain of Function in an ERV/ALR Sulfhydryl Oxidase by Molecular Engineering of the Shuttle Disulfide
Vitu, E., Bentzur, M., Lisowsky, T., Kaiser, C. A., & Fass, D. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.06.070 · 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
Characterization of the Cytochrome c Oxidase Assembly Factor Cox19 of Saccharomyces cerevisiae
Rigby, K. M., Zhang, L., Cobine, P. A., George, G. N., & Winge, D. R. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m610082200 · 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
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
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
Structural Determinants of Substrate Access to the Disulfide Oxidase Erv2p
Vala, A., Sevier, C. S., & Kaiser, C. A. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.09.076 · Cited by 35 · see citing works
[31] Sulfhydryl oxidases as factors for mitochondrial biogenesis
Hofhaus, G., & Lisowsky, T. (2002) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(02)48650-8 · Cited by 6 · see citing works
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Mitochondrial Machineries for Protein Import and Assembly
Wiedemann, N., & Pfanner, N. (2017) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060815-014352 · Cited by 894 · 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
Redox regulation of mitochondrial function
Handy, D. E., & Loscalzo, J. (2012) · Antioxidants & Redox Signaling · doi:10.1089/ars.2011.4123 · Cited by 588 · see citing works
The role of thiols in antioxidant systems
Ulrich, K., & Jakob, U. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.05.035 · Cited by 561 · see citing works
Nagy, P. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4973 · Cited by 488 · see citing works
Tumor‐Microenvironment‐Responsive Nanomedicine for Enhanced Cancer Immunotherapy
Peng, S., Xiao, F., Chen, M., & Gao, H. (2021) · Advanced Science · doi:10.1002/advs.202103836 · Cited by 446 · see citing works
Dual Role of Mitofilin in Mitochondrial Membrane Organization and Protein Biogenesis
von der Malsburg, K., Müller, J. M., Bohnert, M., Oeljeklaus, S., Kwiatkowska, P., Becker, T., Łoniewska-Lwowska, A., Wiese, S., Rao, S., Milenkovic, D., et al. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.08.026 · Cited by 412 · see citing works
The Protein Import Machinery of Mitochondria—A Regulatory Hub in Metabolism, Stress, and Disease
Harbauer, A. B., Zahedi, R. P., Sickmann, A., Pfanner, N., & Meisinger, C. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.01.010 · Cited by 377 · 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
Egea, J., Fabregat, I., Frapart, Y., Ghezzi, P., Görlach, A., Kietzmann, T., Kubaichuk, K. I., Knaus, U. G., López, M. G., González, G. O., et al. (2017) · Redox Biology · doi:10.1016/j.redox.2017.05.007 · Cited by 311 · 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
Structure of the mitochondrial import gate reveals distinct preprotein paths
Araiso, Y., Tsutsumi, A., Qiu, J., Imai, K., Shiota, T., Song, J., Lindau, C., Wenz, L.-S., Sakaue, H., Yunoki, K., et al. (2019) · Nature · doi:10.1038/s41586-019-1680-7 · Cited by 246 · see citing works
From structure to redox: The diverse functional roles of disulfides and implications in disease
Bechtel, T. J., & Weerapana, E. (2017) · PROTEOMICS · doi:10.1002/pmic.201600391 · Cited by 210 · see citing works
Petrungaro, C., Zimmermann, K. M., Küttner, V., Fischer, M., Dengjel, J., Bogeski, I., & Riemer, J. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.08.019 · Cited by 200 · see citing works
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Depuydt, M., Messens, J., & Collet, J. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3575 · Cited by 188 · see citing works
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Kojer, K., Bien, M., Gangel, H., Morgan, B., Dick, T. P., & Riemer, J. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.165 · Cited by 179 · see citing works
Self-citationThe Ubiquitin-Proteasome System Regulates Mitochondrial Intermembrane Space Proteins
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Mitochondrial protein import: from transport pathways to an integrated network
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The Incomplete Glutathione Puzzle: Just Guessing at Numbers and Figures?
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The Intermembrane Space of Mitochondria
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Self-citationBanci, L., Bertini, I., Cefaro, C., Cenacchi, L., Ciofi‐Baffoni, S., Felli, I. C., Gallo, A., Gonnelli, L., Luchinat, E., Sideris, D. P., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010095107 · Cited by 132 · see citing works
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Ayer, A., Gourlay, C. W., & Dawes, I. W. (2014) · FEMS Yeast Research · doi:10.1111/1567-1364.12114 · Cited by 125 · see citing works
Fischer, 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
Self-citationBohnert, M., Wenz, L.-S., Zerbes, R. M., Horvath, S. E., Stroud, D. A., von der Malsburg, K., Müller, J. M., Oeljeklaus, S., Perschil, I., Warscheid, B., et al. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-04-0295 · Cited by 123 · see citing works
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Neupert, W. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.02.001 · Cited by 121 · see citing works
Banci, L., Bertini, I., Calderone, V., Cefaro, C., Ciofi‐Baffoni, S., Gallo, A., Kallergi, E., Lionaki, E., Pozidis, C., & Tokatlidis, K. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1014542108 · Cited by 104 · 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
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Self-citationYang, J., Staples, O. D., Thomas, L. W., Briston, T., Robson, M. P., Poon, E., Simões, M. L., El‐Emir, E., Buffa, F. M., Ahmed, A., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58780 · Cited by 95 · see citing works
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Dabir, D. V., Hasson, S. A., Setoguchi, K., Johnson, M. E., Wongkongkathep, P., Douglas, C. J., Zimmerman, J., Damoiseaux, R. D., Teitell, M. A., & Koehler, C. M. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.03.006 · Cited by 92 · see citing works
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Wróbel, L., Trojanowska, A., Sztolsztener, M. E., & Chacińska, A. (2013) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-09-0649 · Cited by 87 · see citing works
Zhou, Y., Huang, W., & He, Y. (2018) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2018.05.025 · Cited by 86 · see citing works
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Peleh, V., Cordat, E., & Herrmann, J. M. (2016) · eLife · doi:10.7554/elife.16177 · Cited by 77 · see citing works
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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
Friederich, M. W., Erdogan, A. J., Coughlin, C. R., Elos, M. T., Jiang, H. L., O’Rourke, C. P., Lovell, M. A., Wartchow, E. P., Gowan, K., Chatfield, K. C., et al. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw431 · Cited by 74 · see citing works
Self-citationKojer, K., Peleh, V., Calabrese, G., Herrmann, J. M., & Riemer, J. (2014) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-10-1422 · Cited by 73 · see citing works
Self-citationLongen, 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
Self-citationBalancing oxidative protein folding: The influences of reducing pathways on disulfide bond formation
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Self-citationThe MIA Pathway: A Key Regulator of Mitochondrial Oxidative Protein Folding and Biogenesis
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Bode, 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
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Koch, J. R., & Schmid, F. X. (2014) · Nature Communications · doi:10.1038/ncomms4041 · Cited by 63 · see citing works
Klöppel, C., Suzuki, Y., Kojer, K., Petrungaro, C., Longen, S., Fiedler, S., Keller, S., & Riemer, J. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-04-0293 · Cited by 63 · see citing works
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Sayyed, U. M. H., & Mahalakshmi, R. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.101870 · Cited by 47 · see citing works
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Basu, S., Leonard, J. C., Desai, N., Mavridou, D. A. I., Tang, K. H., Goddard, A. D., Ginger, M. L., Lukeš, J., & Allen, J. W. A. (2012) · Eukaryotic Cell · doi:10.1128/ec.00304-12 · Cited by 45 · see citing works
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Needs, H. I., Protasoni, M., Henley, J. M., Prudent, J., Collinson, I. R., & Pereira, G. C. (2021) · Life · doi:10.3390/life11050432 · Cited by 30 · see citing works
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Herrmann, J. M., & Riemer, J. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.5841 · Cited by 33 · see citing works
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Cooperation of protein machineries in mitochondrial protein sorting.
Wenz, L.-S., Opaliński, Ł., Wiedemann, N., & Becker, T. (2015) · Biochimica et Biophysica Acta · doi:10.1016/j.bbamcr.2015.01.012 · Cited by 32 · see citing works
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Erdogan, A. J., & Riemer, J. (2016) · Cell and Tissue Research · doi:10.1007/s00441-016-2481-z · Cited by 28 · see citing works
Self-citationBourens, M., Dabir, D. V., Tienson, H. L., Sorokina, I., Koehler, C. M., & Barrientos, A. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.383562 · Cited by 27 · see citing works
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Koch, J. R., & Schmid, F. X. (2014) · ACS Chemical Biology · doi:10.1021/cb500408n · Cited by 26 · see citing works
Son, M., & Elliott, J. L. (2013) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2013.11.004 · Cited by 26 · see citing works
Banci, L., Bertini, I., Cefaro, C., Ciofi‐Baffoni, S., & Gallo, A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.246223 · Cited by 25 · see citing works
Guo, P., Ma, J.-D., Jiang, Y., Wang, S., Bao, Z. Z., Yu, X., Chen, Y., & Zhou, C. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.394759 · Cited by 25 · see citing works
Thiriveedi, V., Mattam, U., Pattabhi, P., Bisoyi, V., Talari, N. K., Krishnamoorthy, T., & Sepuri, N. B. V. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101725 · Cited by 24 · see citing works
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- Authors
- Bien, M., Longen, S., Wagener, N., Chwalla, I., Herrmann, J. M., & Riemer, J.
- Affiliations
- University of Kaiserslautern (DE)
- Ludwig-Maximilians-Universität München (DE)
- Corresponding author
- Herrmann, Johannes M.
- Riemer, Jan
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2010-02
- Volume
- 37
- Issue
- 4
- Pages
- 516-528
- ISSN
- 1097-2765 (ISSN-L)
- OpenAlex
- W2076363488
- Cited by
- 179
- References
- 30
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 7 · 2023: 9 · 2022: 7 · 2021: 14 · 2020: 5 · 2019: 8 · 2018: 10 · 2017: 13 · 2016: 5 · 2015: 13 · 2014: 16 · 2013: 16 · 2012: 27
- FWCI
- 7.94
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Keywords
- Erv1, Mia40, cytochrome c, protein dimerization, oxidative protein folding, glutathione, proofreading, mitochondrial biogenesis, in vitro reconstitution
- MeSH terms
- Mitochondrial Precursor Protein Import Complex Proteins, Amino Acid Sequence, Disulfides, Electron Transport, Glutathione, Mitochondria, Molecular Sequence Data, Oxidation-Reduction, Protein Binding, Saccharomyces cerevisiae, Sequence Alignment, Conserved Sequence, Protein Folding, Molecular Chaperones, Protein Subunits, Mitochondrial Proteins, Saccharomyces cerevisiae Proteins, Mitochondrial Membrane Transport Proteins, Oxidoreductases Acting on Sulfur Group Donors, Protein Multimerization
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