Remodelling of the active presequence translocase drives motor-dependent mitochondrial protein translocation

Nature Communications

Volumn 5, Issue , 2014, Pages

  Schulz, Christian ^a   Rehling, Peter ^a,b  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CARRIER PROTEIN; HEAT SHOCK PROTEIN 70; MATRIX PROTEIN; MITOCHONDRIAL PROTEIN; PAM18 PROTEIN; PROTEIN; TIM23 PROTEIN; TRANSLOCON; UNCLASSIFIED DRUG; CHAPERONE; MOLECULAR MOTOR; PAM18 J PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TIM23 PROTEIN, S CEREVISIAE; TOM TRANSLOCASE;

BIOCHEMISTRY; ENZYME ACTIVITY; FUNCTIONAL ROLE; MITOCHONDRION; PEPTIDE; PHYSIOLOGY; PROTEIN; TRANSLOCATION;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; MITOCHONDRION; MOLECULAR DYNAMICS; MOTOR UNIT; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATASES; CARRIER PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MOLECULAR CHAPERONES; MOLECULAR MOTOR PROTEINS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84904191032     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5349     Document Type: Article

References (38)

1. Wickner, W. & Schekman, R. Protein translocation across biological membranes. Science 310, 1452-1456 (2005).
2. Flores-Pérez, U. & Jarvis, P. Molecular chaperone involvement in chloroplast protein import. Biochim. Biophys. Acta. 1833, 332-340 (2013).
3. Rapoport, T. A. Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450, 663-669 (2007).
4. Schleiff, E. & Becker, T. Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat. Rev. Mol. Cell. Biol. 12, 48-59 (2010).
5. Chacinska, A., Koehler, C. M., Milenkovic, D., Lithgow, T. & Pfanner, N. Importing mitochondrial proteins: machineries and mechanisms. Cell 138, 628-644 (2009).
6. Neupert, W. & Herrmann, J. M. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723-749 (2007).
7. van der Laan, M., Hutu, D. P. & Rehling, P. On the mechanism of preprotein import by the mitochondrial presequence translocase. Biochim. Biophys. Acta. 1803, 732-739 (2010).
8. Dolezal, P. Evolution of the Molecular Machines for Protein Import into Mitochondria. Science 313, 314-318 (2006).
9. Hartl, F. U. Molecular chaperones in cellular protein folding. Nature 381, 571-579 (1996).
10. Bukau, B. & Horwich, A. The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366 (1998).
11. Kozany, C., Mokranjac, D., Sichting, M., Neupert, W. & Hell, K. The J domainrelated cochaperone Tim16 is a constituent of the mitochondrial TIM23 preprotein translocase. Nat. Struct. Mol. Biol. 11, 234-241 (2004).
12. Li, Y. et al. The presequence translocase-associated protein import motor of mitochondria. Pam16 functions in an antagonistic manner to Pam18. J. Biol. Chem. 279, 38047-38054 (2004).
13. Truscott, K. N. et al. A J-protein is an essential subunit of the presequence translocase-associated protein import motor of mitochondria. J. Cell Biol. 163, 707-713 (2003).
14. D'Silva, P., Schilke, B., Walter, W., Andrew, A. & Craig, E. A. J protein cochaperone of the mitochondrial inner membrane required for protein import into the mitochondrial matrix. Proc. Natl Acad. Sci. USA 100, 13839-13844 (2003).
15. Mokranjac, D., Sichting, M., Neupert, W. & Hell, K. Tim14, a novel key component of the import motor of the TIM23 protein translocase of mitochondria. EMBO J. 22, 4945-4956 (2003).
16. Mokranjac, D., Bourenkov, G., Hell, K., Neupert, W. & Groll, M. Structure and function of Tim14 and Tim16, the J and J-like components of the mitochondrial protein import motor. EMBO J. 25, 4675-4685 (2006).
17. Mokranjac, D. et al. The import motor of the yeast mitochondrial TIM23 preprotein translocase contains two different J proteins, Tim14 and Mdj2. J. Biol. Chem. 280, 31608-31614 (2005).
18. D'Silva, P. R., Schilke, B., Walter, W. & Craig, E. A. Role of Pam16's degenerate J domain in protein import across the mitochondrial inner membrane. Proc. Natl Acad. Sci. USA 102, 12419-12424 (2005).
19. Liu, Q., D'Silva, P., Walter, W., Marszalek, J. & Craig, E. A. Regulated cycling of mitochondrial Hsp70 at the protein import channel. Science 300, 139-141 (2003).
20. Mayer, M. Timing the catch. Nat. Struct. Mol. Biol. 11, 6-8 (2004).
21. Endo, T., Yamano, K. & Kawano, S. Structural insight into the mitochondrial protein import system. Biochim. Biophys. Acta. 1808, 955-970 (2011).
22. Chacinska, A. et al. Mitochondrial translocation contact sites: separation of dynamic and stabilizing elements in formation of a TOM-TIM-preprotein supercomplex. EMBO J. 22, 5370-5381 (2003).
23. Gambill, B. D. et al. A dual role for mitochondrial heat shock protein 70 in membrane translocation of preproteins. J. Cell Biol. 123, 109-117 (1993).
24. Voisine, C. et al. The protein import motor of mitochondria: unfolding and trapping of preproteins are distinct and separable functions of matrix Hsp70. Cell 97, 565-574 (1999).
25. Dekker, P. J. et al. 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, 5408-5419 (1997).
26. Frazier, A. E. et al. Pam16 has an essential role in the mitochondrial protein import motor. Nat. Struct. Mol. Biol. 11, 226-233 (2004).
27. Chacinska, A. et al. Mitochondrial presequence translocase: switching between TOM tethering and motor recruitment involves Tim21 and Tim17. Cell 120, 817-829 (2005).
28. van der Laan, M. et al. Pam17 is required for architecture and translocation activity of the mitochondrial protein import motor. Mol. Cell. Biol. 25, 7449-7458 (2005).
29. Popov-Celeketić, D., Mapa, K., Neupert, W. & Mokranjac, D. Active remodelling of the TIM23 complex during translocation of preproteins into mitochondria. EMBO J. 27, 1469-1480 (2008).
30. Chacinska, A. et al. Distinct forms of mitochondrial TOM-TIM supercomplexes define signal-dependent states of preprotein sorting. Mol. Cell. Biol. 30, 307-318 (2010).
31. D'Silva, P., Schilke, B., Hayashi, M. & Craig, E. A. Interaction of the J-protein heterodimer Pam18/Pam16 of the mitochondrial import motor with the translocon of the inner membrane. Mol. Biol. Cell. 19, 424-432 (2008).
32. Gebert, M. et al. Mgr2 promotes coupling of the mitochondrial presequence translocase to partner complexes. J. Cell Biol. 197, 595-604 (2012).
33. Schiller, D. Pam17 and Tim44 act sequentially in protein import into the mitochondrial matrix. Int. J. Biochem. Cell. Biol. 41, 2343-2349 (2009).
34. van der Laan, M. et al. Motor-free mitochondrial presequence translocase drives membrane integration of preproteins. Nat. Cell. Biol. 9, 1152-1159 (2007).
35. Wiedemann, N., van der Laan, M., Hutu, D. P., Rehling, P. & Pfanner, N. Sorting switch of mitochondrial presequence translocase involves coupling of motor module to respiratory chain. J. Cell Biol. 179, 1115-1122 (2007).
36. van der Laan, M. et al. A role for Tim21 in membrane-potential-dependent preprotein sorting in mitochondria. Curr. Biol. 16, 2271-2276 (2006).
37. Berthold, J. et al. The MIM complex mediates preprotein translocation across the mitochondrial inner membrane and couples it to the mt-Hsp70/ATP driving system. Cell 81, 1085-1093 (1995).
38. Wagner, K. et al. The assembly pathway of the mitochondrial carrier translocase involves four preprotein translocases. Mol. Cell. Biol. 28, 4251-4260 (2008).