Protein Import by the Mitochondrial Presequence Translocase in the Absence of a Membrane Potential

Journal of Molecular Biology

Volumn 428, Issue 6, 2016, Pages 1041-1052

  Turakhiya, Uma ^a,b   Von Der Malsburg, Karina ^a,h   Gold, Vicki A M ^c   Guiard, Bernard ^d   Chacinska, Agnieszka ^e   Van Der Laan, Martin ^a,b,f   Ieva, Raffaele ^a,g  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^d CNRS   (France)

^e INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^f SAARLAND UNIVERSITY   (Germany)

^g UMR   (France)

^h CAMBRIDGE UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

ATP synthase; membrane potential; mitochondrial biogenesis; protein import; TIM23 complex

Indexed keywords

ADENOSINE TRIPHOSPHATE; CARRIER PROTEIN; MEMBRANE PROTEIN; PROTEIN PRECURSOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SACCHAROMYCES CEREVISIAE PROTEIN; TIM11 PROTEIN, S CEREVISIAE; TIM23 PROTEIN, S CEREVISIAE;

AMINO TERMINAL SEQUENCE; ARTICLE; CYTOSOL; ELECTROCHEMISTRY; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN TRANSPORT; DNA MUTATIONAL ANALYSIS; GENETICS; METABOLISM; MITOCHONDRION; PHYSIOLOGY;

DNA MUTATIONAL ANALYSIS; MEMBRANE POTENTIALS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84958581221     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2016.01.020     Document Type: Article

References (76)

1. O. Stehling, C. Wilbrecht, and R. Lill Mitochondrial iron-sulfur protein biogenesis and human disease Biochimie 100 2014 61 77
2. N. Gebert, M.T. Ryan, N. Pfanner, N. Wiedemann, and D. Stojanovski Mitochondrial protein import machineries and lipids: A functional connection Biochim. Biophys. Acta 1808 2011 1002 1011
3. A.M. Sokol, M.E. Sztolsztener, M. Wasilewski, E. Heinz, and A. Chacinska Mitochondrial protein translocases for survival and wellbeing FEBS Lett. 588 2014 2484 2495
4. S.E. Horvath, and G. Daum Lipids of mitochondria Prog. Lipid Res. 52 2013 590 614
5. F. Palmieri Diseases caused by defects of mitochondrial carriers: A review Biochim. Biophys. Acta 1777 2008 564 578
6. R. Rizzuto, D. De Stefani, A. Raffaello, and C. Mammucari Mitochondria as sensors and regulators of calcium signalling Nat. Rev. Mol. Cell Biol. 13 2012 566 578
7. M. Mimaki, X. Wang, M. McKenzie, D.R. Thorburn, and M.T. Ryan Understanding mitochondrial complex I assembly in health and disease Biochim. Biophys. Acta 1817 2012 851 862
8. S. Dennerlein, and P. Rehling Human mitochondrial COX1 assembly into cytochrome c oxidase at a glance J. Cell Sci. 128 2015 833 837
9. M. van der Laan, M. Bohnert, N. Wiedemann, and N. Pfanner Role of MINOS in mitochondrial membrane architecture and biogenesis Trends Cell Biol. 22 2012 185 192
10. K. Hell, W. Neupert, and R.A. Stuart Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA EMBO J. 20 2001 1281 1288
11. M. Ott, and J.M. Herrmann Co-translational membrane insertion of mitochondrially encoded proteins Biochim. Biophys. Acta 1803 2010 767 775
12. V. Krüger, M. Deckers, M. Hildenbeutel, M. van der Laan, M. Hellmers, C. Dreker, M. Preuss, J.M. Herrmann, P. Rehling, R. Wagner, and M. Meinecke The mitochondrial oxidase assembly protein1 (Oxa1) insertase forms a membrane pore in lipid bilayers J. Biol. Chem. 287 2012 33314 33326
13. A. Chacinska, C.M. Koehler, D. Milenkovic, T. Lithgow, and N. Pfanner Importing mitochondrial proteins: Machineries and mechanisms Cell 138 2009 628 644
14. C. Schulz, A. Schendzielorz, and P. Rehling Unlocking the presequence import pathway Trends Cell Biol. 25 2015 265 275
15. M. Bohnert, N. Pfanner, and M. van der Laan Mitochondrial machineries for insertion of membrane proteins Curr. Opin. Struct. Biol. 33 2015 92 102
16. C. de Marcos-Lousa, D.P. Sideris, and K. Tokatlidis Translocation of mitochondrial inner-membrane proteins: Conformation matters Trends Biochem. Sci. 31 2006 259 267
17. W. Neupert, and J.M. Herrmann Translocation of proteins into mitochondria Annu. Rev. Biochem. 76 2007 723 749
18. N. Wiedemann, N. Pfanner, and M.T. Ryan The three modules of ADP/ATP carrier cooperate in receptor recruitment and translocation into mitochondria EMBO J. 20 2001 951 960
19. S.P. Curran, D. Leuenberger, W. Oppliger, and C.M. Koehler The Tim9p-Tim10p complex binds to the transmembrane domains of the ADP/ATP carrier EMBO J. 21 2002 942 953
20. N. Gebert, A. Chacinska, K. Wagner, B. Guiard, C.M. Koehler, P. Rehling, N. Pfanner, and N. Wiedemann Assembly of the three small Tim proteins precedes docking to the mitochondrial carrier translocase EMBO Rep. 9 2008 548 554
21. P. Kovermann, K.N. Truscott, B. Guiard, P. Rehling, N.B. Sepuri, H. Müller, R.E. Jensen, R. Wagner, and N. Pfanner Tim22, the essential core of the mitochondrial protein insertion complex, forms a voltage-activated and signal-gated channel Mol. Cell 9 2002 363 373
22. P. Rehling, K. Model, K. Brandner, P. Kovermann, A. Sickmann, H.E. Meyer, W. Kühlbrandt, R. Wagner, K.N. Truscott, and N. Pfanner Protein insertion into the mitochondrial inner membrane by a twin-pore translocase Science 299 2003 1747 1751
23. M.F. Bauer, C. Sirrenberg, W. Neupert, and M. Brunner Role of Tim23 as voltage sensor and presequence receptor in protein import into mitochondria Cell 87 1996 33 41
24. K.N. Truscott, P. Kovermann, A. Geissler, A. Merlin, M. Meijer, A.J. Driessen, J. Rassow, N. Pfanner, and R. Wagner A presequence- and voltage-sensitive channel of the mitochondrial preprotein translocase formed by Tim23 Nat. Struct. Biol. 8 2001 1074 1082
25. M. Meinecke, R. Wagner, P. Kovermann, B. Guiard, D.U. Mick, D.P. Hutu, W. Voos, K.N. Truscott, A. Chacinska, N. Pfanner, and P. Rehling Tim50 maintains the permeability barrier of the mitochondrial inner membrane Science 312 2006 1523 1526
26. S. Martinez-Caballero, S.M. Grigoriev, J.M. Herrmann, M.L. Campo, and K.W. Kinnally Tim17p regulates the twin pore structure and voltage gating of the mitochondrial protein import complex TIM23 J. Biol. Chem. 282 2007 3584 3593
27. N.N. Alder, J. Sutherland, A.I. Buhring, R.E. Jensen, and A.E. Johnson Quaternary structure of the mitochondrial TIM23 complex reveals dynamic association between Tim23p and other subunits Mol. Biol. Cell 19 2008 159 170
28. K. Malhotra, M. Sathappa, J.S. Landin, A.E. Johnson, and N.N. Alder Structural changes in the mitochondrial Tim23 channel are coupled to the proton-motive force Nat. Struct. Mol. Biol. 20 2013 965 972
29. D. Roise, S.J. Horvath, J.M. Tomich, J.H. Richards, and G. Schatz A chemically synthesized pre-sequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers EMBO J. 5 1986 1327 1334
30. G. von Heijne Mitochondrial targeting sequences may form amphiphilic helices EMBO J. 5 1986 1335 1342
31. J. Martin, K. Mahlke, and N. Pfanner Role of an energized inner membrane in mitochondrial protein import. Δε drives the movement of presequences J. Biol. Chem. 266 1991 18051 18057
32. D. Roise Interaction of a synthetic mitochondrial presequence with isolated yeast mitochondria: Mechanism of binding and kinetics of import Proc. Natl. Acad. Sci. U. S. A. 89 1992 608 612
33. 2 modulates the Δε-dependence of translocation of the matrix-targeting sequence Mol. Biol. Cell 11 2000 3977 3991
34. M. van der Laan, N. Wiedemann, D.U. Mick, B. Guiard, P. Rehling, and N. Pfanner A role for Tim21 in membrane-potential-dependent preprotein sorting in mitochondria Curr. Biol. 16 2006 2271 2276
35. M. van der Laan, M. Meinecke, J. Dudek, D.P. Hutu, M. Lind, I. Perschil, B. Guiard, R. Wagner, N. Pfanner, and P. Rehling Motor-free mitochondrial presequence translocase drives membrane integration of preproteins Nat. Cell Biol. 9 2007 1152 1159
36. N. Pfanner, and W. Neupert Distinct steps in the import of ADP/ATP carrier into mitochondria J. Biol. Chem. 262 1987 7528 7536
37. J. Hirst, J. Carroll, I.M. Fearnley, R.J. Shannon, and J.E. Walker The nuclear encoded subunits of complex I from bovine heart mitochondria Biochim. Biophys. Acta 1604 2003 135 150
38. U. Brandt, A. Abdrakhmanova, V. Zickermann, A. Galkin, S. Dröse, K. Zwicker, and S. Kerscher Structure-function relationships in mitochondrial complex I of the strictly aerobic yeast Yarrowia lipolytica Biochem. Soc. Trans. 33 2005 840 844
39. V. Zickermann, H. Angerer, M.G. Ding, E. Nübel, and U. Brandt Small single transmembrane domain (STMD) proteins organize the hydrophobic subunits of large membrane protein complexes FEBS Lett. 584 2010 2516 2525
40. G.I. Belogrudov, J.M. Tomich, and Y. Hatefi Membrane topography and near-neighbor relationships of the mitochondrial ATP synthase subunits e, f, and g J. Biol. Chem. 271 1996 20340 20345
41. o-ATP synthase exists as a dimer: Identification of three dimer-specific subunits EMBO J. 17 1998 7170 7178
42. R. Rabl, V. Soubannier, R. Scholz, F. Vogel, N. Mendl, A. Vasiljev-Neumeyer, C. Körner, R. Jagasia, T. Keil, W. Baumeister, M. Cyrklaff, W. Neupert, and A.S. Reichert Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g J. Cell Biol. 185 2009 1047 1063
43. o-ATP synthase dimer and its role in shaping the mitochondrial cristae Proc. Natl. Acad. Sci. U. S. A. 109 2012 13602 13607
44. P. Paumard, J. Vaillier, B. Coulary, J. Schaeffer, V. Soubannier, D.M. Mueller, D. Brèthes, J.P. di Rago, and J. Velours The ATP synthase is involved in generating mitochondrial cristae morphology EMBO J. 21 2002 221 230
45. o-ATP synthase supracomplexes J. Biol. Chem. 281 2006 13990 13998
46. G. Arselin, M.F. Giraud, A. Dautant, J. Vaillier, D. Brèthes, B. Coulary-Salin, J. Schaeffer, and J. Velours The GxxxG motif of the transmembrane domain of subunit e is involved in the dimerization/oligomerization of the yeast ATP synthase complex in the mitochondrial membrane Eur. J. Biochem. 270 2003 1875 1884
47. G. Arselin, J. Vaillier, B. Salin, J. Schaeffer, M.F. Giraud, A. Dautant, D. Brèthes, and J. Velours The modulation in subunits e and g amounts of yeast ATP synthase modifies mitochondrial cristae morphology J. Biol. Chem. 279 2004 40392 40399
48. N.V. Dudkina, J. Heinemeyer, W. Keegstra, E.J. Boekema, and H.P. Braun Structure of dimeric ATP synthase from mitochondria: An angular association of monomers induces the strong curvature of the inner membrane FEBS Lett. 579 2005 5769 5772
49. o ATP synthase monomers bend the lipid bilayer in 2D membrane crystals Elife 4 2015 e06119
50. P. Paumard, G. Arselin, J. Vaillier, S. Chaignepain, K. Bathany, J.M. Schmitter, D. Brèthes, and J. Velours Two ATP synthases can be linked through subunits i in the inner mitochondrial membrane of Saccharomyces cerevisiae Biochemistry 41 2002 10390 10396
51. I. Wittig, J. Velours, R. Stuart, and H. Schägger Characterization of domain interfaces in monomeric and dimeric ATP synthase Mol. Cell. Proteomics 7 2008 995 1004
52. o-ATP synthase: The small subunits e and g associate with monomeric complexes to trigger dimerization J. Mol. Biol. 392 2009 855 861
53. o subunits k and i Mol. Biol. Cell 21 2010 1494 1504
54. o-ATP synthase of the yeast Saccharomyces cerevisiae: Importance of the N-terminal membrane anchor region Eukaryot. Cell. 4 2005 346 355
55. H. Fölsch, B. Guiard, W. Neupert, and R.A. Stuart Internal targeting signal of the BCS1 protein: A novel mechanism of import into mitochondria EMBO J. 15 1996 479 487
56. P.J. Dekker, F. Martin, A.C. Maarse, U. Bömer, H. Müller, B. Guiard, M. Meijer, J. Rassow, and N. Pfanner The Tim core complex defines the number of mitochondrial translocation contact sites and can hold arrested preproteins in the absence of matrix Hsp70-Tim44 EMBO J. 16 1997 5408 5419
57. A. Chacinska, M. van der Laan, C.S. Mehnert, B. Guiard, D.U. Mick, D.P. Hutu, K.N. Truscott, N. Wiedemann, C. Meisinger, N. Pfanner, and P. Rehling Distinct forms of mitochondrial TOM-TIM supercomplexes define signal-dependent states of preprotein sorting Mol. Cell. Biol. 30 2010 307 318
58. M. Gebert, S.G. Schrempp, C.S. Mehnert, A.K. Heißwolf, S. Oeljeklaus, R. Ieva, M. Bohnert, K. von der Malsburg, S. Wiese, T. Kleinschroth, C. Hunte, H.E. Meyer, I. Haferkamp, B. Guiard, B. Warscheid, N. Pfanner, and M. van der Laan Mgr2 promotes coupling of the mitochondrial presequence translocase to partner complexes J. Cell Biol. 197 2012 595 604
59. V.A. Gold, R. Ieva, A. Walter, N. Pfanner, M. van der Laan, and W. Kühlbrandt Visualizing active membrane protein complexes by electron cryotomography Nat. Commun. 5 2014 4129
60. R. Ieva, S.G. Schrempp, L. Opaliński, F. Wollweber, P. Höß, A.K. Heißwolf, M. Gebert, Y. Zhang, B. Guiard, S. Rospert, T. Becker, A. Chacinska, N. Pfanner, and M. van der Laan Mgr2 functions as lateral gatekeeper for preprotein sorting in the mitochondrial inner membrane Mol. Cell 56 2014 641 652
61. C. Sirrenberg, M. Endres, K. Becker, M.F. Bauer, E. Walther, W. Neupert, and M. Brunner Functional cooperation and stoichiometry of protein translocases of the outer and inner membranes of mitochondria J. Biol. Chem. 272 1997 29963 29966
62. L.S. Wenz, L. Opaliński, M.H. Schuler, L. Ellenrieder, R. Ieva, L. Böttinger, J. Qiu, M. van der Laan, N. Wiedemann, B. Guiard, N. Pfanner, and T. Becker The presequence pathway is involved in protein sorting to the mitochondrial outer membrane EMBO Rep. 15 2014 678 685
63. M. Bohnert, P. Rehling, B. Guiard, J.M. Herrmann, N. Pfanner, and M. van der Laan Cooperation of stop-transfer and conservative sorting mechanisms in mitochondrial protein transport Curr. Biol. 20 2010 1227 1232
64. L. Käll, A. Krogh, and E.L. Sonnhammer Advantages of combined transmembrane topology and signal peptide prediction - The Phobius Web server Nucleic Acids Res. 35 2007 W429 W432
65. T. Hessa, N.M. Meindl-Beinker, A. Bernsel, H. Kim, Y. Sato, M. Lerch-Bader, I. Nilsson, S.H. White, and G. von Heijne Molecular code for transmembrane-helix recognition by the Sec61 translocon Nature 450 2007 1026 1030
66. S.C. Botelho, M. Osterberg, A.S. Reichert, K. Yamano, P. Björkholm, T. Endo, G. von Heijne, and H. Kim TIM23-mediated insertion of transmembrane α-helices into the mitochondrial inner membrane EMBO J. 30 2011 1003 1011
67. 2 to the mitochondrial intermembrane space contains three distinct functional regions EMBO J. 12 1993 2303 2311
68. 2 into the mitochondrial intermembrane space: Specific recognition of the sorting signal EMBO J. 12 1993 2295 2302
69. M. Osterberg, S. Calado Botelho, G. von Heijne, and H. Kim Charged flanking residues control the efficiency of membrane insertion of the first transmembrane segment in yeast mitochondrial Mgm1p FEBS Lett. 585 2011 1238 1242
70. +-ATP synthase Biochemistry 31 1992 12451 12454
71. F.N. Vögtle, S. Wortelkamp, R.P. Zahedi, D. Becker, C. Leidhold, K. Gevaert, J. Kellermann, W. Voos, A. Sickmann, N. Pfanner, and C. Meisinger Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability Cell 139 2009 428 439
72. 1 complex J. Biol. Chem. 269 1994 12947 12953
73. 1 complex Science 281 1998 64 71
74. C. Meisinger, N. Pfanner, and K.N. Truscott Isolation of yeast mitochondria Methods Mol. Biol. 313 2006 33 39
75. H. Koll, B. Guiard, J. Rassow, J. Ostermann, A.L. Horwich, W. Neupert, and F.U. Hartl Antifolding activity of hsp60 couples protein import into the mitochondrial matrix with export to the intermembrane space Cell 68 1992 1163 1175
76. M. Preuss, K. Leonhard, K. Hell, R.A. Stuart, W. Neupert, and J. Herrmann Mba1, a novel component of the mitochondrial protein export machinery of the yeast Saccharomyces cerevisiae J. Cell Biol. 153 2001 1085 1096