XCoupling of mitochondrial import and export translocases by receptor-mediated supercomplex formation

Cell

Volumn 154, Issue 3, 2013, Pages

  Qiu, Jian ^a   Wenz, Lena Sophie ^a   Zerbes, Ralf M ^a   Oeljeklaus, Silke ^a   Bohnert, Maria ^a   Stroud, David A ^a,d   Wirth, Christophe ^a   Ellenrieder, Lars ^a   Thornton, Nicolas ^a   Kutik, Stephan ^a   Wiese, Sebastian ^a   Schulze Specking, Agnes ^a   Zufall, Nicole ^a   Chacinska, Agnieszka ^b   Guiard, Bernard ^c   Hunte, Carola ^a   Warscheid, Bettina ^a   Van Der Laan, Martin ^a   Pfanner, Nikolaus ^a   Wiedemann, Nils ^a   Becker, Thomas ^a   more..

^a UNIVERSITY OF FREIBURG   (Germany)

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

^c CNRS   (France)

^d LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; MITOCHONDRIAL PROTEIN; MUTANT PROTEIN; PORIN; PROTEIN PRECURSOR; RECEPTOR PROTEIN; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE 20;

ARTICLE; CELL ORGANELLE; COMPLEX FORMATION; CONTROLLED STUDY; IN VIVO STUDY; MITOCHONDRIAL MEMBRANE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT;

EID: 84881141249     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.06.033     Document Type: Article

References (55)

1. T. Becker, M. Gebert, N. Pfanner, and M. van der Laan Biogenesis of mitochondrial membrane proteins Curr. Opin. Cell Biol. 21 2009 484 493
2. T. Becker, B. Guiard, N. Thornton, N. Zufall, D.A. Stroud, N. Wiedemann, and N. Pfanner Assembly of the mitochondrial protein import channel: role of Tom5 in two-stage interaction of Tom40 with the SAM complex Mol. Biol. Cell 21 2010 3106 3113
3. M. Bohnert, L.S. Wenz, R.M. Zerbes, S.E. Horvath, D.A. Stroud, K. von der Malsburg, J.M. Müller, S. Oeljeklaus, I. Perschil, and B. Warscheid Role of mitochondrial inner membrane organizing system in protein biogenesis of the mitochondrial outer membrane Mol. Biol. Cell 23 2012 3948 3956
4. A. Chacinska, P. Rehling, B. Guiard, A.E. Frazier, A. Schulze-Specking, N. Pfanner, W. Voos, and C. Meisinger Mitochondrial translocation contact sites: separation of dynamic and stabilizing elements in formation of a TOM-TIM-preprotein supercomplex EMBO J. 22 2003 5370 5381
5. P. Dolezal, V. Likic, J. Tachezy, and T. Lithgow Evolution of the molecular machines for protein import into mitochondria Science 313 2006 314 318
6. J. Dukanovic, and D. Rapaport Multiple pathways in the integration of proteins into the mitochondrial outer membrane Biochim. Biophys. Acta 1808 2011 971 980
7. T. Endo, and K. Yamano Transport of proteins across or into the mitochondrial outer membrane Biochim. Biophys. Acta 1803 2010 706 714
8. S. Ghaemmaghami, W.K. Huh, K. Bower, R.W. Howson, A. Belle, N. Dephoure, E.K. O'Shea, and J.S. Weissman Global analysis of protein expression in yeast Nature 425 2003 737 741
9. S.J. Habib, T. Waizenegger, A. Niewienda, S.A. Paschen, W. Neupert, and D. Rapaport The N-terminal domain of Tob55 has a receptor-like function in the biogenesis of mitochondrial β-barrel proteins J. Cell Biol. 176 2007 77 88
10. C.L. Hagan, T.J. Silhavy, and D. Kahne β-Barrel membrane protein assembly by the Bam complex Annu. Rev. Biochem. 80 2011 189 210
11. M. Harner, C. Körner, D. Walther, D. Mokranjac, J. Kaesmacher, U. Welsch, J. Griffith, M. Mann, F. Reggiori, and W. Neupert The mitochondrial contact site complex, a determinant of mitochondrial architecture EMBO J. 30 2011 4356 4370
12. V. Hewitt, F. Alcock, and T. Lithgow Minor modifications and major adaptations: the evolution of molecular machines driving mitochondrial protein import Biochim. Biophys. Acta 1808 2011 947 954
13. S.C. Hoppins, and F.E. Nargang The Tim8-Tim13 complex of Neurospora crassa functions in the assembly of proteins into both mitochondrial membranes J. Biol. Chem. 279 2004 12396 12405
14. D. Ishikawa, H. Yamamoto, Y. Tamura, K. Moritoh, and T. Endo Two novel proteins in the mitochondrial outer membrane mediate β-barrel protein assembly J. Cell Biol. 166 2004 621 627
15. A. Klein, L. Israel, S.W.K. Lackey, F.E. Nargang, A. Imhof, W. Baumeister, W. Neupert, and D.R. Thomas Characterization of the insertase for β-barrel proteins of the outer mitochondrial membrane J. Cell Biol. 199 2012 599 611
16. T. Krimmer, D. Rapaport, M.T. Ryan, C. Meisinger, C.K. Kassenbrock, E. Blachly-Dyson, M. Forte, M.G. Douglas, W. Neupert, F.E. Nargang, and N. Pfanner Biogenesis of porin of the outer mitochondrial membrane involves an import pathway via receptors and the general import pore of the TOM complex J. Cell Biol. 152 2001 289 300
17. S. Kutik, D. Stojanovski, L. Becker, T. Becker, M. Meinecke, V. Krüger, C. Prinz, C. Meisinger, B. Guiard, and R. Wagner Dissecting membrane insertion of mitochondrial β-barrel proteins Cell 132 2008 1011 1024
18. C. Meisinger, M.T. Ryan, K. Hill, K. Model, J.H. Lim, A. Sickmann, H. Müller, H.E. Meyer, R. Wagner, and N. Pfanner Protein import channel of the outer mitochondrial membrane: a highly stable Tom40-Tom22 core structure differentially interacts with preproteins, small tom proteins, and import receptors Mol. Cell. Biol. 21 2001 2337 2348
19. K. Model, C. Meisinger, T. Prinz, N. Wiedemann, K.N. Truscott, N. Pfanner, and M.T. Ryan Multistep assembly of the protein import channel of the mitochondrial outer membrane Nat. Struct. Biol. 8 2001 361 370
20. W. Neupert, and J.M. Herrmann Translocation of proteins into mitochondria Annu. Rev. Biochem. 76 2007 723 749
21. S.A. Paschen, T. Waizenegger, T. Stan, M. Preuss, M. Cyrklaff, K. Hell, D. Rapaport, and W. Neupert Evolutionary conservation of biogenesis of β-barrel membrane proteins Nature 426 2003 862 866
22. D. Rapaport, and W. Neupert Biogenesis of Tom40, core component of the TOM complex of mitochondria J. Cell Biol. 146 1999 321 331
23. O. Schmidt, N. Pfanner, and C. Meisinger Mitochondrial protein import: from proteomics to functional mechanisms Nat. Rev. Mol. Cell Biol. 11 2010 655 667
24. T. Shiota, M. Maruyama, M. Miura, Y. Tamura, K. Yamano, M. Esaki, and T. Endo The Tom40 assembly process probed using the attachment of different intramitochondrial sorting signals Mol. Biol. Cell 23 2012 3936 3947
25. D. Stojanovski, N. Pfanner, and N. Wiedemann Import of proteins into mitochondria Methods Cell Biol. 80 2007 783 806
26. D.A. Stroud, T. Becker, J. Qiu, D. Stojanovski, S. Pfannschmidt, C. Wirth, C. Hunte, B. Guiard, C. Meisinger, N. Pfanner, and N. Wiedemann Biogenesis of mitochondrial β-barrel proteins: the POTRA domain is involved in precursor release from the SAM complex Mol. Biol. Cell 22 2011 2823 2833
27. N. Thornton, D.A. Stroud, D. Milenkovic, B. Guiard, N. Pfanner, and T. Becker Two modular forms of the mitochondrial sorting and assembly machinery are involved in biogenesis of α-helical outer membrane proteins J. Mol. Biol. 396 2010 540 549
28. J. Tommassen Assembly of outer-membrane proteins in bacteria and mitochondria Microbiology 156 2010 2587 2596
29. S. van Wilpe, M.T. Ryan, K. Hill, A.C. Maarse, C. Meisinger, J. Brix, P.J.T. Dekker, M. Moczko, R. Wagner, and M. Meijer Tom22 is a multifunctional organizer of the mitochondrial preprotein translocase Nature 401 1999 485 489
30. D.M. Walther, D. Rapaport, and J. Tommassen Biogenesis of β-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence Cell. Mol. Life Sci. 66 2009 2789 2804
31. N. Wiedemann, V. Kozjak, A. Chacinska, B. Schönfisch, S. Rospert, M.T. Ryan, N. Pfanner, and C. Meisinger Machinery for protein sorting and assembly in the mitochondrial outer membrane Nature 424 2003 565 571
32. N. Wiedemann, K.N. Truscott, S. Pfannschmidt, B. Guiard, C. Meisinger, and N. Pfanner Biogenesis of the protein import channel Tom40 of the mitochondrial outer membrane: intermembrane space components are involved in an early stage of the assembly pathway J. Biol. Chem. 279 2004 18188 18194
33. K. Yamano, Y. Yatsukawa, M. Esaki, A.E. Hobbs, R.E. Jensen, and T. Endo Tom20 and Tom22 share the common signal recognition pathway in mitochondrial protein import J. Biol. Chem. 283 2008 3799 3807
34. D.C. Bay, M. Hafez, M.J. Young, and D.A. Court Phylogenetic and coevolutionary analysis of the β-barrel protein family comprised of mitochondrial porin (VDAC) and Tom40 Biochim. Biophys. Acta 1818 2012 1502 1519
35. M. Bayrhuber, T. Meins, M. Habeck, S. Becker, K. Giller, S. Villinger, C. Vonrhein, C. Griesinger, M. Zweckstetter, and K. Zeth Structure of the human voltage-dependent anion channel Proc. Natl. Acad. Sci. USA 105 2008 15370 15375
36. T. Becker, L.S. Wenz, V. Krüger, W. Lehmann, J.M. Müller, L. Goroncy, N. Zufall, T. Lithgow, B. Guiard, and A. Chacinska The mitochondrial import protein Mim1 promotes biogenesis of multispanning outer membrane proteins J. Cell Biol. 194 2011 387 395
37. E. Blachly-Dyson, J. Song, W.J. Wolfgang, M. Colombini, and M. Forte Multicopy suppressors of phenotypes resulting from the absence of yeast VDAC encode a VDAC-like protein Mol. Cell. Biol. 17 1997 5727 5738
38. J. Brix, K. Dietmeier, and N. Pfanner Differential recognition of preproteins by the purified cytosolic domains of the mitochondrial import receptors Tom20, Tom22, and Tom70 J. Biol. Chem. 272 1997 20730 20735
39. J. Cox, and M. Mann MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 26 2008 1367 1372
40. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
41. M. Forte, H.R. Guy, and C.A. Mannella Molecular genetics of the VDAC ion channel: structural model and sequence analysis J. Bioenerg. Biomembr. 19 1987 341 350
42. M. Gebert, S.G. Schrempp, C.S. Mehnert, A.K. Heißwolf, S. Oeljeklaus, R. Ieva, M. Bohnert, K. von der Malsburg, S. Wiese, and T. Kleinschroth Mgr2 promotes coupling of the mitochondrial presequence translocase to partner complexes J. Cell Biol. 197 2012 595 604
43. D. Gessmann, N. Flinner, J. Pfannstiel, A. Schlösinger, E. Schleiff, S. Nussberger, and O. Mirus Structural elements of the mitochondrial preprotein-conducting channel Tom40 dissolved by bioinformatics and mass spectrometry Biochim. Biophys. Acta 1807 2011 1647 1657
44. S. Hiller, R.G. Garces, T.J. Malia, V.Y. Orekhov, M. Colombini, and G. Wagner Solution structure of the integral human membrane protein VDAC-1 in detergent micelles Science 321 2008 1206 1210
45. V. Kozjak, N. Wiedemann, D. Milenkovic, C. Lohaus, H.E. Meyer, B. Guiard, C. Meisinger, and N. Pfanner An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane J. Biol. Chem. 278 2003 48520 48523
46. C. Meisinger, N. Pfanner, and K.N. Truscott Isolation of yeast mitochondria Methods Mol. Biol. 313 2006 33 39
47. M. Moczko, U. Bömer, M. Kübrich, N. Zufall, A. Hönlinger, and N. Pfanner The intermembrane space domain of mitochondrial Tom22 functions as a trans binding site for preproteins with N-terminal targeting sequences Mol. Cell. Biol. 17 1997 6574 6584
48. S.E. Ong, B. Blagoev, I. Kratchmarova, D.B. Kristensen, H. Steen, A. Pandey, and M. Mann Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol. Cell. Proteomics 1 2002 376 386
49. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815
50. O. Schmidt, A.B. Harbauer, S. Rao, B. Eyrich, R.P. Zahedi, D. Stojanovski, B. Schönfisch, B. Guiard, A. Sickmann, N. Pfanner, and C. Meisinger Regulation of mitochondrial protein import by cytosolic kinases Cell 144 2011 227 239
51. J. Söding, A. Biegert, and A.N. Lupas The HHpred interactive server for protein homology detection and structure prediction Nucleic Acids Res. 33 Web Server issue 2005 W244 W248
52. D. Stojanovski, D. Milenkovic, J.M. Müller, K. Gabriel, A. Schulze-Specking, M.J. Baker, M.T. Ryan, B. Guiard, N. Pfanner, and A. Chacinska Mitochondrial protein import: precursor oxidation in a ternary complex with disulfide carrier and sulfhydryl oxidase J. Cell Biol. 183 2008 195 202
53. D.A. Stroud, S. Oeljeklaus, S. Wiese, M. Bohnert, U. Lewandrowski, A. Sickmann, B. Guiard, M. van der Laan, B. Warscheid, and N. Wiedemann Composition and topology of the endoplasmic reticulum-mitochondria encounter structure J. Mol. Biol. 413 2011 743 750
54. R. Ujwal, D. Cascio, J.P. Colletier, S. Faham, J. Zhang, L. Toro, P. Ping, and J. Abramson The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating Proc. Natl. Acad. Sci. USA 105 2008 17742 17747
55. K. Zeth Structure and evolution of mitochondrial outer membrane proteins of β-barrel topology Biochim. Biophys. Acta 1797 2010 1292 1299