A disulfide bond in the TIM23 complex is crucial for voltage gating and mitochondrial protein import

Journal of Cell Biology

Volumn 214, Issue 4, 2016, Pages 417-431

  Ramesh, Ajay ^a   Peleh, Valentina ^a   Martinez Caballero, Sonia ^b   Wollweber, Florian ^c,d   Sommer, Frederik ^a   van der Laan, Martin ^c   Schroda, Michael ^a   Alexander, R Todd ^e   Campo, María Luisa ^b   Herrmann, Johannes M ^a  

^a University of Koblenz Landau   (Germany)

^b UNIVERSITY OF EXTREMADURA   (Spain)

^c SAARLAND UNIVERSITY   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; MITOCHONDRIAL PROTEIN; MUTANT PROTEIN; OXIDOREDUCTASE; PROTEIN ERV1; PROTEIN MIA40; PROTEIN TIM17; PROTEIN TIM23; THIOL OXIDASE; UNCLASSIFIED DRUG; DISULFIDE; MULTIPROTEIN COMPLEX; PROTEIN BINDING; PROTEIN PRECURSOR; SACCHAROMYCES CEREVISIAE PROTEIN; TIM23 PROTEIN, S CEREVISIAE;

ARTICLE; CHANNEL GATING; CONTROLLED STUDY; DISULFIDE BOND; ELECTRIC POTENTIAL; ENZYME ACTIVITY; INNER MEMBRANE; MITOCHONDRIAL MEMBRANE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; TEMPERATURE SENSITIVE MUTANT; CHEMISTRY; CONSERVED SEQUENCE; METABOLISM; OXIDATION REDUCTION REACTION; STRUCTURE ACTIVITY RELATION; TEMPERATURE;

CONSERVED SEQUENCE; DISULFIDES; ION CHANNEL GATING; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; MULTIPROTEIN COMPLEXES; MUTANT PROTEINS; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN PRECURSORS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPERATURE;

EID: 84983315619     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201602074     Document Type: Article

References (56)

1. Alder, N.N., R.E. Jensen, and A.E. Johnson. 2008. Fluorescence mapping of mitochondrial TIM23 complex reveals a water-facing, substrateinteracting helix surface. Cell. 134:439-450. http ://dx.doi.org /10.1016 /j .cell.2008.06.007
2. Allen, S., V. Balabanidou, D.P. Sideris, T. Lisowsky, and K. Tokatlidis. 2005. Erv1 mediates the Mia40-dependent protein import pathway and provides a functional link to the respiratory chain by shuttling electrons to cytochrome c. J. Mol. Biol. 353:937-944. http ://dx.doi.org /10.1016 /j .jmb.2005.08.049
3. Banci, L., I. Bertini, C. Cefaro, S. Ciofi-Baffoni, A. Gallo, M. Martinelli, D.P. Sideris, N. Katrakili, and K. Tokatlidis. 2009. MIA40 is an oxidoreductase that catalyzes oxidative protein folding in mitochondria. Nat. Struct. Mol. Biol. 16:198-206. http ://dx.doi.org /10.1038 /nsmb.1553
4. Bode, M., M.W. Woellhaf, M. Bohnert, M. van der Laan, F. Sommer, M. Jung, R. Zimmermann, M. Schroda, and J.M. Herrmann. 2015. Redox-regulated dynamic interplay between Cox19 and the copper-binding protein Cox11 in the intermembrane space of mitochondria facilitates biogenesis of cytochrome c oxidase. Mol. Biol. Cell. 26:2385-2401. http ://dx.doi.org /10.1091 /mbc.E14 -11 -1526
5. Chacinska, A., S. Pfannschmidt, N. Wiedemann, V. Kozjak, L.K. Sanjuán Szklarz, A. Schulze-Specking, K.N. Truscott, B. Guiard, C. Meisinger, and N. Pfanner. 2004. Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins. EMBO J. 23:3735-3746. http ://dx.doi.org /10.1038 /sj.emboj.7600389
6. Chacinska, A., M. Lind, A.E. Frazier, J. Dudek, C. Meisinger, A. Geissler, A. Sickmann, H.E. Meyer, K.N. Truscott, B. Guiard, et al. 2005. Mitochondrial presequence translocase: switching between TOM tethering and motor recruitment involves Tim21 and Tim17. Cell. 120:817-829. http ://dx.doi.org /10.1016 /j.cell.2005.01.011
7. Chacinska, A., C.M. Koehler, D. Milenkovic, T. Lithgow, and N. Pfanner. 2009. Importing mitochondrial proteins: machineries and mechanisms. Cell. 138:628-644. http ://dx.doi.org /10.1016 /j.cell.2009.08.005
8. Cox, J., and M. Mann. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26:1367-1372. http ://dx.doi.org /10.1038 /nbt.1511
9. Curran, S.P., D. Leuenberger, W. Oppliger, and C.M. Koehler. 2002. The Tim9p- Tim10p complex binds to the transmembrane domains of the ADP/ATP carrier. EMBO J. 21:942-953. http ://dx.doi.org /10.1093 /emboj /21.5.942
10. Dabir, D.V., E.P. Leverich, S.K. Kim, F.D. Tsai, M. Hirasawa, D.B. Knaff, and C.M. Koehler. 2007. A role for cytochrome c and cytochrome c peroxidase in electron shuttling from Erv1. EMBO J. 26:4801-4811. http ://dx.doi.org /10.1038 /sj.emboj.7601909
11. Davis, A.J., N.N. Alder, R.E. Jensen, and A.E. Johnson. 2007. The Tim9p/10p and Tim8p/13p complexes bind to specific sites on Tim23p during mitochondrial protein import. Mol. Biol. Cell. 18:475-486. http ://dx.doi .org /10.1091 /mbc.E06 -06 -0546
12. Dekker, P.J.T., P. Keil, J. Rassow, A.C. Maarse, N. Pfanner, and M. Meijer. 1993. Identification of MIM23, a putative component of the protein import machinery of the mitochondrial inner membrane. FEBS Lett. 330:66-70. http ://dx.doi.org /10.1016 /0014 -5793(93)80921 -G
13. Demishtein-Zohary, K., M. Marom, W. Neupert, D. Mokranjac, and A. Azem. 2015. GxxxG motifs hold the TIM23 complex together. FEBS J. 282:2178-2186. http ://dx.doi.org /10.1111 /febs.13266
14. Endo, T., K. Yamano, and S. Kawano. 2011. Structural insight into the mitochondrial protein import system. Biochim. Biophys. Acta. 1808:955-970. http ://dx.doi.org /10.1016 /j.bbamem.2010.07.018
15. Grigoriev, S.M., C. Muro, L.M. Dejean, M.L. Campo, S. Martinez-Caballero, and K.W. Kinnally. 2004. Electrophysiological approaches to the study of protein translocation in mitochondria. Int. Rev. Cytol. 238:227-274. http ://dx.doi.org /10.1016 /S0074 -7696(04)38005 -8
16. Hamill, O.P., A. Marty, E. Neher, B. Sakmann, and F.J. Sigworth. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391:85-100. http ://dx.doi .org /10.1007 /BF00656997
17. Harbauer, A.B., R.P. Zahedi, A. Sickmann, N. Pfanner, and C. Meisinger. 2014. The protein import machinery of mitochondria-a regulatory hub in metabolism, stress, and disease. Cell Metab. 19:357-372. http ://dx.doi .org /10.1016 /j.cmet.2014.01.010
18. Hasson, S.A., R. Damoiseaux, J.D. Glavin, D.V. Dabir, S.S. Walker, and C.M. Koehler. 2010. Substrate specificity of the TIM22 mitochondrial import pathway revealed with small molecule inhibitor of protein translocation. Proc. Natl. Acad. Sci. USA. 107:9578-9583. http ://dx.doi .org /10.1073 /pnas.0914387107
19. Káldi, K., M.F. Bauer, C. Sirrenberg, W. Neupert, and M. Brunner. 1998. Biogenesis of Tim23 and Tim17, integral components of the TIM machinery for matrix-targeted preproteins. EMBO J. 17:1569-1576. http ://dx.doi.org /10.1093 /emboj /17.6.1569
20. Kawano, S., K. Yamano, M. Naoé, T. Momose, K. Terao, S. Nishikawa, N. Watanabe, and T. Endo. 2009. Structural basis of yeast Tim40/Mia40 as an oxidative translocator in the mitochondrial intermembrane space. Proc. Natl. Acad. Sci. USA. 106:14403-14407. (published erratum appears in Proc. Natl. Acad. Sci. USA. 2009. 106:20133) http ://dx.doi.org /10.1073 /pnas.0901793106
21. Koch, J.R., and F.X. Schmid. 2014. Mia40 targets cysteines in a hydrophobic environment to direct oxidative protein folding in the mitochondria. Nat. Commun. 5:3041. http ://dx.doi.org /10.1038 /ncomms4041
22. Koehler, C.M., E. Jarosch, K. Tokatlidis, K. Schmid, R.J. Schweyen, and G. Schatz. 1998. Import of mitochondrial carriers mediated by essential proteins of the intermembrane space. Science. 279:369-373. http ://dx.doi .org /10.1126 /science.279.5349.369
23. Koll, H., B. Guiard, J. Rassow, J. Ostermann, A.L. Horwich, W. Neupert, and F.-U. Hartl. 1992. Antifolding activity of hsp60 couples protein import into the mitochondrial matrix with export to the intermembrane space. Cell. 68:1163-1175. http ://dx.doi.org /10.1016 /0092 -8674(92)90086 -R
24. Lobstein, J., C.A. Emrich, C. Jeans, M. Faulkner, P. Riggs, and M. Berkmen. 2012. SHuffle, a novel Escherichia coli protein expression strain capable of correctly folding disulfide bonded proteins in its cytoplasm. Microb. Cell Fact. 11:56. http ://dx.doi.org /10.1186 /1475 -2859 -11 -56
25. Lohret, T.A., R.E. Jensen, and K.W. Kinnally. 1997. Tim23, a protein import component of the mitochondrial inner membrane, is required for normal activity of the multiple conductance channel, MCC. J. Cell Biol. 137:377-386. http ://dx.doi.org /10.1083 /jcb.137.2.377
26. Lutz, T., W. Neupert, and J.M. Herrmann. 2003. Import of small Tim proteins into the mitochondrial intermembrane space. EMBO J. 22:4400-4408. http ://dx.doi.org /10.1093 /emboj /cdg421
27. Maarse, A.C., J. Blom, P. Keil, N. Pfanner, and M. Meijer. 1994. Identification of the essential yeast protein MIM17, an integral mitochondrial inner membrane protein involved in protein import. FEBS Lett. 349:215-221. http ://dx.doi.org /10.1016 /0014 -5793(94)00669 -5
28. Malhotra, K., M. Sathappa, J.S. Landin, A.E. Johnson, and N.N. Alder. 2013. Structural changes in the mitochondrial Tim23 channel are coupled to the proton-motive force. Nat. Struct. Mol. Biol. 20:965-972. http ://dx.doi.org /10.1038 /nsmb.2613
29. Mannella, C.A. 1982. Structure of the outer mitochondrial membrane: ordered arrays of porelike subunits in outer-membrane fractions from Neurospora crassa mitochondria. J. Cell Biol. 94:680-687. http ://dx.doi.org /10.1083 /jcb.94.3.680
30. Martinez-Caballero, S., S.M. Grigoriev, J.M. Herrmann, M.L. Campo, and K.W. Kinnally. 2007. Tim17p regulates the twin pore structure and voltage gating of the mitochondrial protein import complex TIM23. J. Biol. Chem. 282:3584-3593. http ://dx.doi.org /10.1074 /jbc.M607551200
31. Meier, S., W. Neupert, and J.M. Herrmann. 2005. Conserved N-terminal negative charges in the Tim17 subunit of the TIM23 translocase play a critical role in the import of preproteins into mitochondria. J. Biol. Chem. 280:7777-7785. http ://dx.doi.org /10.1074 /jbc.M412158200
32. Meinecke, M., R. Wagner, P. Kovermann, B. Guiard, D.U. Mick, D.P. Hutu, W. Voos, K.N. Truscott, A. Chacinska, N. Pfanner, and P. Rehling. 2006. Tim50 maintains the permeability barrier of the mitochondrial inner membrane. Science. 312:1523-1526. http ://dx.doi.org /10.1126 /science .1127628
33. Mesecke, N., N. Terziyska, C. Kozany, F. Baumann, W. Neupert, K. Hell, and J.M. Herrmann. 2005. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell. 121:1059-1069. http ://dx.doi.org /10.1016 /j.cell.2005.04.011
34. Milenkovic, D., K. Gabriel, B. Guiard, A. Schulze-Specking, N. Pfanner, and A. Chacinska. 2007. Biogenesis of the essential Tim9-Tim10 chaperone complex of mitochondria: site-specific recognition of cysteine residues by the intermembrane space receptor Mia40. J. Biol. Chem. 282:22472-22480. http ://dx.doi.org /10.1074 /jbc.M703294200
35. Milenkovic, D., T. Ramming, J.M. Müller, L.S. Wenz, N. Gebert, A. Schulze- Specking, D. Stojanovski, S. Rospert, and A. Chacinska. 2009. Identification of the signal directing Tim9 and Tim10 into the intermembrane space of mitochondria. Mol. Biol. Cell. 20:2530-2539. http ://dx.doi.org /10.1091 /mbc.E08 -11 -1108
36. Mühlhaus, T., J. Weiss, D. Hemme, F. Sommer, and M. Schroda. 2011. Quantitative shotgun proteomics using a uniform 15N-labeled standard to monitor proteome dynamics in time course experiments reveals new insights into the heat stress response of Chlamydomonas reinhardtii. Mol. Cell. Proteomics. 10:M110.004739. http ://dx.doi.org /10.1074 /mcp.M110 .004739
37. Muro, C., S.M. Grigoriev, D. Pietkiewicz, K.W. Kinnally, and M.L. Campo. 2003. Comparison of the TIM and TOM channel activities of the mitochondrial protein import complexes. Biophys. J. 84:2981-2989. http ://dx.doi.org /10.1016 /S0006 -3495(03)70024 -1
38. Naoé, M., Y. Ohwa, D. Ishikawa, C. Ohshima, S. Nishikawa, H. Yamamoto, and T. Endo. 2004. Identification of Tim40 that mediates protein sorting to the mitochondrial intermembrane space. J. Biol. Chem. 279:47815-47821. http ://dx.doi.org /10.1074 /jbc.M410272200
39. Neupert, W., and J.M. Herrmann. 2007. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76:723-749. http ://dx.doi.org /10 .1146 /annurev.biochem.76.052705.163409
40. Ohba, M., and G. Schatz. 1987. Disruption of the outer membrane restores protein import to trypsin-treated yeast mitochondria. EMBO J. 6:2117-2122.
41. Okamoto, H., A. Miyagawa, T. Shiota, Y. Tamura, and T. Endo. 2014. Intramolecular disulfide bond of Tim22 protein maintains integrity of the TIM22 complex in the mitochondrial inner membrane. J. Biol. Chem. 289:4827-4838. http ://dx.doi.org /10.1074 /jbc.M113.543264
42. Paschen, S.A., U. Rothbauer, K. Káldi, M.F. Bauer, W. Neupert, and M. Brunner. 2000. The role of the TIM8-13 complex in the import of Tim23 into mitochondria. EMBO J. 19:6392-6400. http ://dx.doi.org /10.1093 /emboj /19.23.6392
43. Peixoto, P.M., F. Graña, T.J. Roy, C.D. Dunn, M. Flores, R.E. Jensen, and M.L. Campo. 2007. Awaking TIM22, a dynamic ligand-gated channel for protein insertion in the mitochondrial inner membrane. J. Biol. Chem. 282:18694-18701. http ://dx.doi.org /10.1074 /jbc.M700775200
44. Peleh, V., A. Ramesh, and J.M. Herrmann. 2015. Import of proteins into isolated yeast mitochondria. Methods Mol. Biol. 1270:37-50. http ://dx.doi.org /10 .1007 /978 -1 -4939 -2309 -0 3
45. Peleh, V., E. Cordat, and J.M. Herrmann. 2016. Mia40 is a trans-site receptor that drives protein import into the mitochondrial intermembrane space by hydrophobic substrate binding. eLife. 5:e16177. http ://dx.doi.org /10 .7554 /eLife.16177
46. Rehling, P., K. Brandner, and N. Pfanner. 2004. Mitochondrial import and the twin-pore translocase. Nat. Rev. Mol. Cell Biol. 5:519-530. http ://dx.doi .org /10.1038 /nrm1426
47. Ryan, K.R., R.S. Leung, and R.E. Jensen. 1998. Characterization of the mitochondrial inner membrane translocase complex: the Tim23p hydrophobic domain interacts with Tim17p but not with other Tim23p molecules. Mol. Cell. Biol. 18:178-187. http ://dx.doi.org /10.1128 /MCB.18.1.178
48. Schulz, C., A. Schendzielorz, and P. Rehling. 2015. Unlocking the presequence import pathway. Trends Cell Biol. 25:265-275. http ://dx.doi.org /10.1016 /j.tcb.2014.12.001
49. Sideris, D.P., and K. Tokatlidis. 2007. Oxidative folding of small Tims is mediated by site-specific docking onto Mia40 in the mitochondrial intermembrane space. Mol. Microbiol. 65:1360-1373. http ://dx.doi.org /10.1111 /j.1365 -2958.2007.05880.x
50. Sideris, D.P., N. Petrakis, N. Katrakili, D. Mikropoulou, A. Gallo, S. Ciofi- Baffoni, L. Banci, I. Bertini, and K. Tokatlidis. 2009. A novel intermembrane space-targeting signal docks cysteines onto Mia40 during mitochondrial oxidative folding. J. Cell Biol. 187:1007-1022. http ://dx .doi.org /10.1083 /jcb.200905134
51. Sirrenberg, C., M. Endres, H. Fölsch, R.A. Stuart, W. Neupert, and M. Brunner. 1998. Carrier protein import into mitochondria mediated by the intermembrane proteins Tim10/Mrs11 and Tim12/Mrs5. Nature. 391:912-915. http ://dx.doi.org /10.1038 /36136
52. Truscott, K.N., P. Kovermann, A. Geissler, A. Merlin, M. Meijer, A.J. Driessen, J. Rassow, N. Pfanner, and R. Wagner. 2001. A presequence- and voltage-sensitive channel of the mitochondrial preprotein translocase formed by Tim23. Nat. Struct. Biol. 8:1074-1082. http ://dx.doi.org /10 .1038 /nsb726
53. van der Laan, M., M. Meinecke, J. Dudek, D.P. Hutu, M. Lind, I. Perschil, B. Guiard, R. Wagner, N. Pfanner, and P. Rehling. 2007. Motor-free mitochondrial presequence translocase drives membrane integration of preproteins. Nat. Cell Biol. 9:1152-1159. http ://dx.doi.org /10.1038 / ncb1635
54. Weckbecker, D., S. Longen, J. Riemer, and J.M. Herrmann. 2012. Atp23 biogenesis reveals a chaperone-like folding activity of Mia40 in the IMS of mitochondria. EMBO J. 31:4348-4358. http ://dx.doi.org /10.1038 / emboj.2012.263
55. Wrobel, L., A. Trojanowska, M.E. Sztolsztener, and A. Chacinska. 2013. Mitochondrial protein import: Mia40 facilitates Tim22 translocation into the inner membrane of mitochondria. Mol. Biol. Cell. 24:543-554. http :// dx.doi.org /10.1091 /mbc.E12 -09 -0649
56. Wrobel, L., A.M. Sokol, M. Chojnacka, and A. Chacinska. 2016. The presence of disulfide bonds reveals an evolutionarily conserved mechanism involved in mitochondrial protein translocase assembly. Sci. Rep. 6:27484. http :// dx.doi.org /10.1038 /srep27484