Mitochondrial translocation contact sites: Separation of dynamic and stabilizing elements in formation of a TOM-TIM-preprotein supercomplex

EMBO Journal

Volumn 22, Issue 20, 2003, Pages 5370-5381

  Chacinska, Agnieszka ^a   Rehling, Peter ^a   Guiard, Bernard ^b   Frazier, Ann E ^a   Schulze Specking, Agnes ^a   Pfanner, Nikolaus ^a   Voos, Wolfgang ^a   Meisinger, Chris ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

Author keywords

Contact sites; Mitochondria; Protein translocation; Saccharomyces cerevisiae

Indexed keywords

CARRIER PROTEIN; MEMBRANE PROTEIN; PROTEIN PRECURSOR;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; COMPLEX FORMATION; ENZYME SUBUNIT; MITOCHONDRION; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TRANSPORT;

CARRIER PROTEINS; MACROMOLECULAR SUBSTANCES; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; PROTEIN CONFORMATION; PROTEIN PRECURSORS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TETRAHYDROFOLATE DEHYDROGENASE;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0142105410     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg532     Document Type: Article

References (41)

1. Abe, Y., Shodai, T., Muto, T., Mihara, K., Torii, H., Nishikawa, S., Endo, T. and Kohda, D. (2000) Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell, 100, 551-560.
2. 0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J., 17, 7170-7178.
3. Bauer, M.F., Sirrenberg, C., Neupert, W. and Brunner, M. (1996) Role of Tim23 as voltage sensor and presequence receptor in protein import into mitochondria. Cell, 87, 33-41.
4. Bauer, M.F., Hofmann, S., Neupert, W. and Brunner, M. (2000) Protein translocation into mitochondria: the role of TIM complexes. Trends Cell Biol., 10, 25-31.
5. Bolliger, L., Junne, T., Schatz, G. and Lithgow, T. (1995) Acidic receptor domains on both sides of the outer membrane mediate translocation of precursor proteins into yeast mitochondria. EMBO J., 14, 6318-6326.
6. Bömer, U., Meijer, M., Maarse, A.C., Hönlinger, A., Dekker, P.J.T., Pfanner, N. and Rassow, J. (1997) Multiple interactions of components mediating preprotein translocation across the inner membrane. EMBO J., 16, 2205-2216.
7. Brix, J., Dietmeier, K. and Pfanner, N. (1997) Differential recognition of preproteins by the purified cytosolic domains of the mitochondrial import receptors Tom20, Tom22 and Tom70. J. Biol. Chem., 272, 20730-20735.
8. Court, D.A., Nargang, F.E., Steiner, H., Hodger, R.S., Neupert, W. and Lill, R. (1996) Role of the intermembrane-space domain of the preprotein receptor Tom22 in protein import into mitochondria. Mol. Cell Biol., 16, 4035-4042.
9. Dekker, P.J., Martin, F., Maarse, A.C., Bömer, U., Müller, H., Guiard, B., Meijer, M., Rassow, J. and Pfanner, N. (1997) 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.
10. Donzeau, M., Kaldi, K., Adam, A., Paschen, S., Wanner, G., Guiard, B., Bauer, M.F., Neupert, W. and Brunner, M. (2000) Tim23 links the inner and outer mitochondrial membranes. Cell, 101, 401-412.
11. Endo, T. and Kohda, D. (2002) Functions of outer membrane receptors in mitochondrial protein import. Biochim. Biophys Acta, 1592, 3-14.
12. Gambill, B.D., Voos, W., Kang, P.J., Miao, B., Langer, T., Craig, E.A. and Pfanner, N. (1993) A dual role for mitochondrial heat shock protein 70 in membrane translocation of preproteins. J. Cell Biol., 123, 109-117.
13. Geissler, A. et al. (2002) The mitochondrial presequence translocase: an essential role of Tim50 in directing preproteins to the import channel. Cell, 111, 507-518.
14. Hill, K., Model, K., Ryan, M.T., Dietmeier, K., Martin, F., Wagner, R. and Pfanner, N. (1998) Tom 40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature, 395, 516-521.
15. Horst, M., Hilfiker-Rothenfluh, S., Oppliger, W. and Schatz, G. (1995) Dynamic interaction of the protein translocation systems in the inner and outer membranes of yeast mitochondria. EMBO J., 14, 2293-2297.
16. Jascur, T., Goldenberg, D.P., Vestweber, D. and Schatz, G. (1992) Sequential translocation of an artificial precursor protein across the two mitochondrial membranes. J. Biol. Chem., 267, 13636-13641.
17. Jensen, R.E. and Johnson, A.E. (2001) Opening the door to mitochondrial protein import. Nat. Struct. Biol. 8, 1008-1010.
18. Kanamori, T., Nishikawa, S., Shin, I., Schultz, P.G. and Endo, T. (1997) Probing the environment along the protein import pathways in yeast mitochondria by site-specific photocrosslinking. Proc. Natl Acad. Sci. USA, 94, 485-490.
19. Kanamori, T., Nishikawa, S., Nakai, M., Shin, I., Schultz, P.G. and Endo, T. (1999) Uncoupling of transfer of the presequence and unfolding of the mature domain in precursor translocation across the mitochondrial outer membrane. Proc. Natl Acad. Sci. USA, 96, 3634-3639.
20. Koehler, C.M., Merchant, S. and Schatz, G. (1999) How membrane proteins travel across the mitochondrial intermembrane space. Trends Biochem. Sci., 24, 428-432.
21. Koll, H., Guiard, B., Rassow, J., Ostermann, J., Horwich, A.L., Neupert, W. and Hartl, F.U. (1992) Antifolding activity of hsp60 couples protein import into the mitochondrial matrix with export to the intermembrane space. Cell, 68, 1163-1175.
22. Komiya, T., Rospert, S., Koehler, C., Looser, R., Schatz, G. and Mihara, K. (1998) Interaction of mitochondrial targeting signals with acidic receptor domains along the protein import pathway: evidence for the 'acid chain' hypothesis. EMBO J., 17, 3886-3898.
23. Künkele, K.P. et al. (1998) The preprotein translocation channel of the outer membrane of mitochondria. Cell, 93, 1009-1019.
24. Meisinger, C. et al. (2001) 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, 2337-2348.
25. Moczko, M., Bömer, U., Kübrich, M., Zufall, N., Hönlinger, A. and Pfanner, N. (1997) The intermembrane space domain of mitochondrial Tom22 functions as a trans binding site for preproteins with N-terminal targeting sequences. Mol. Cell. Biol., 17, 6574-6584.
26. Mokranjac, D., Paschen, S.A., Kozany, C., Prokisch, H., Hoppins, S.C., Nargang, F.E., Neupert, W. and Hell, K. (2003) Tim50, a novel component of the TIM23 preprotein translocase of mitochondria. EMBO J., 22, 816-825.
27. Pfanner, N. and Chacinska, A. (2002) The mitochondrial import machinery: preprotein-conducting channels with binding sites for presequences. Biochim. Biophys Acta, 1592, 15-24.
28. Rassow, J., Guiard, B., Wienhues, U., Herzog, V., Hartl, F.U. and Neupert, W. (1989) Translocation arrest by reversible folding of a precursor protein imported into mitochondria: a means to quantitate translocation contact sites. J. Cell Biol., 109, 1421-1428.
29. Rassow, J., Hartl, F.U., Guiard, B., Pfanner, N. and Neupert, W. (1990) Polypeptides traverse the mitochondrial envelope in an extended state. FEBS Lett., 275, 190-194.
30. Ryan, K.R., Leung, R.S. and Jensen, R.E. (1998) Characterization of the mitochondrial inner membrane translocase complex: the Tim23p hydrophobic domain interacts with Tim 17p but not with other Tim23p molecules. Mol. Cell. Biol., 18, 178-187.
31. Ryan, M.T., Voos, W. and Pfanner, N. (2001) Assaying protein import into mitochondria. Methods Cell Biol., 65, 189-215.
32. Schägger, H. and von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem., 199, 223-231.
33. Schleyer, M. and Neupert, W. (1985) Transport of proteins into mitochondria: translocational intermediates spanning contact sites between outer and inner membranes. Cell, 43, 339-350.
34. Schülke, N., Sepuri, N.B. and Pain, D. (1997) In vivo zippering of inner and outer mitochondrial membranes by a stable translocation intermediate. Proc. Natl Acad. Sci. USA, 94, 7314-7319.
35. Schülke, N., Sepuri, N.B., Gordon, D.M., Saxena, S., Dancis, A. and Pain, D. (1999) A multisubunit complex of outer and inner mitochondrial membrane protein translocases stabilized in vivo by translocation intermediates. J. Biol. Chem., 274, 22847-22854.
36. Sikorski, R.S. and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics, 122, 19-27.
37. Sirrenberg, C., Endres, M., Becker, K., Bauer, M.F., Walther, E., Neupert, W. and Brunner, M. (1997) Functional cooperation and stoichiometry of protein translocases of the outer and inner membranes of mitochondria. J. Biol. Chem., 272, 29963-29966.
38. Truscott, K.N., Kovermann, P., Geissler, A., Merlin, A., Meijer, M., Driessen, A.J., Rassow, J., Pfanner, N. and Wagner, R. (2001) A presequence- and voltage-sensitive channel of the mitochondrial preprotein translocase formed by Tim23. Nat. Struct. Biol., 8, 1074-1082.
39. van Wilpe, S. et al. (1999) Tom22 is a multifunctional organizer of the mitochondrial preprotein translocase. Nature, 401, 485-489.
40. Wienhues, U., Becker, K., Schleyer, M., Guiard, B., Tropschug, M., Horwich, A.L., Pfanner, N. and Neupert, W. (1991) Protein folding causes an arrest of preprotein translocation into mitochondria in vivo, J. Cell Biol., 115, 1601-1609.
41. Yamamoto, H., Esaki, M., Kanamori, T., Tamura, Y., Nishikawa, S. and Endo, T. (2002) Tim50 is a subunit of the TIM23 complex that links protein translocation across the outer and inner mitochondrial membranes. Cell, 111, 519-528.