Quaternary structure of the mitochondrial TIM23 complex reveals dynamic association between Tim23p and other subunits

Molecular Biology of the Cell

Volumn 19, Issue 1, 2008, Pages 159-170

  Alder, Nathan N ^a   Sutherland, Jennifer ^a   Buhring, Ashley I ^a   Jensen, Robert E ^b   Johnson, Arthur E ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN TIM23P; PROTEIN TIM50P; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CROSS LINKING; HYDROPHILICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN STRUCTURE;

CROSS-LINKING REAGENTS; IMMUNOPRECIPITATION; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; MODELS, BIOLOGICAL; MUTANT PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY;

EID: 38749103444     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-07-0669     Document Type: Article

References (43)

1. 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.
2. Bohnert, M., Pfanner, N., and van der Laan, M. (2007). A dynamic machinery for import of mitochondrial precursor proteins. FEBS Lett. 581, 2802-2810.
3. 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 mitochondrial membrane. EMBO J. 16, 2205-2216.
4. Chacinska, A. et al. (2005). Mitochondrial presequence translocase: switching between TOM tethering and motor recruitment involves Tim21 and Tim17. Cell 120, 817-829.
5. Chacinska, A., Rehling, P., Guiard, B., Frazier, A. E., Schulze-Specking, A., Pfanner, N., Voos, W., and Meisinger, C. (2003). Mitochondrial translocation contact sites: separation of dynamic and stabilizing elements in formation of a TOM-TIM-preprotein supercomplex. EMBO J. 22, 5370-5381.
6. Daum, G., Böhni, P. C., and Schatz, G. (1982). Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J. Biol. Chem. 257, 13028-13033.
7. Davis, A. J., Alder, N. N., Jensen, R. E., and Johnson, A. E. (2007). The Tim9p/10p and Tim8p/13p complexes bind to specific sites on Tim23p during mitochdondrial protein import. Mol. Biol. Cell 18, 475-486.
8. Davis, A. J., Ryan, K. R., and Jensen, R. E. (1998). Tim23p contains separate and distinct signals for targeting to mitochondria and insertion into the inner membrane. Mol. Biol. Cell 9, 2577-2593.
9. Davis, A. J., Sepuri, N. B., Holder, J., Johnson, A. E., and Jensen, R. E. (2000). Two intermembrane space TIM complexes interact with different domains of Tim23p during its import into mitochondria. J. Cell Biol. 150, 1271-1282.
10. Dekker, P.J.T., 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.
11. Donzeau, M., Káldi, 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.
12. Eilers, M., and Schatz, G. (1986). Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature 322, 228-232.
13. Flanagan, J. J., Chen, J.-C., Miao, Y., Shao, Y., Lin, J., Bock, P. E., and Johnson, A. E. (2003). Signal recognition particle binds to ribosome-bound signal sequences with fluorescence-detected subnanomolar affinity that does not diminish as the nascent chain lengthens. J. Biol. Chem. 278, 18628-18637.
14. Frazier, A. E., Chacinska, A., Truscott, K. N., Guiard, B., Pfanner, N., and Rehling, P. (2003). Mitochondria use different mechanisms for transport of multispanning membrane proteins through the intermembrane space. Mol. Cell. Biol. 23, 7818-7828.
15. Geissler, A., Chacinska, A., Truscott, K. N., Wiedemann, N., Brandner, K., Sickmann, A., Meyer, H. E., Meisinger, C., Pfanner, N., and Rehling, P. (2002). The mitochondrial presequence translocase: an essential role of Tim50 in directing preproteins to the import channel. Cell 111, 507-518.
16. Kanamori, T., Nishikawa, S.-I., 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.
17. Krishnasastry, M., Walker, B., Braha, O., and Bayley, H. (1994). Surface labeling of key residues during assembly of the transmembrane pore formed by staphylococcal α-hemolysin. FEBS Lett. 356, 66-71.
18. Lohret, T. A., Jensen, R. E., and Kinnally, K. W. (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.
19. Martinez-Caballero, S., Grigoriev, S. M., Herrmann, J. M., Campo, M. L., and Kinnally, K. W. (2007). Tim17p regulates the twin pore structure and voltage gating of the mitochondrial protein import complex TIM23. J. Biol. Chem. 282, 3584-3593.
20. McCormick, P. J., Miao, Y., Shao, Y., Lin, J., and Johnson, A. E. (2003). Cotranslational protein integration into the ER membrane is mediated by the binding of nascent chains to translocon proteins. Mol. Cell 12, 329-341.
21. Meier, S., Neupert, W., and Herrmann, J. M. (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.
22. Meinecke, M. et al. (2006). Tim50 maintains the permeability barrier of the mitochondrial inner membrane. Science 312, 1523-1526.
23. 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.
24. Mokranjac, D., Popov-Čeleketić, D., Hell, K., and Neupert, W. (2005). Role of Tim21 in mitochondrial contact sites. J. Biol. Chem. 280, 23437-23440.
25. Moro, F., Sirrenberg, C., Schneider, H.-C., Neupert, W., and Brunner, M. (1999). The TIM17·23 preprotein translocase of mitochondria: composition and function in protein transport into the matrix. EMBO J. 18, 3667-3675.
26. Neupert, W., and Brunner, M. (2002). The protein import motor of mitochondria. Nat. Rev. Mol. Cell Biol. 3, 555-565.
27. Neupert, W., and Herrmann, J. M. (2007). Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723-749.
28. Nicholls, D. G., and Ferguson, S. J. (1992). Bioenergetics 2. London: Academic Press.
29. Plath, K., Mothes, W., Wilkinson, B. M., Stirling, C. J., and Rapoport, T. A. (1998). Signal sequence recognition in posttranslational protein transport across the yeast ER membrane. Cell 94, 795-807.
30. Rapaport, D., Künkele, K.-P., Dembowski, M., Ahting, U., Nargang, F. E., Neupert, W., and Lill, R. (1998). Dynamics of the TOM complex of mitochondria during binding and translocation of preproteins. Mol. Cell. Biol. 18, 5256-5262.
31. Rehling, P., Brandner, K., and Pfanner, N. (2004). Mitochondrial import and the twin-pore translocase. Nat. Rev. Mol. Cell Biol. 5, 519-530.
32. 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 Tim17p but not with other Tim23p molecules. Mol. Cell. Biol. 18, 178-187.
33. Ryan, M. T., Müller, H., and Pfanner, N. (1999). Functional staging of ADP/ATP carrier translocation across the outer mitochondrial membrane. J. Biol. Chem. 274, 20619-20627.
34. Saksena, S., Shao, Y., Braunagel, S. C., Summers, M. D., and Johnson, A. E. (2004). Cotranslational integration and initial sorting at the endoplasmic reticulum translocon of proteins destined for the inner nuclear membrane. Proc. Natl. Acad. Sci. USA 101, 12537-12542.
35. Smyth, D. G., Blumenfeld, O. O., and Konigsberg, W. (1964). Reactions of N-ethylmaleimide with peptides and amino acids. Biochem. J. 91, 589-595.
36. Stan, T., Ahting, U., Dembowski, M., Künkele, K.-P., Nussberger, S., Neupert, W., and Rapaport, D. (2000). Recognition of preproteins by the isolated TOM complex of mitochondria. EMBO J. 19, 4895-4902.
37. Tombola, F., Pathak, M. M., and Isacoff, E. Y. (2005). How far will you go to sense voltage? Neuron 48, 719-725.
38. Truscott, K. N., Kovermann, P., Geissler, A., Merlin, A., Meijer, M., Driessen, A.J.M., 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. Tzung, S.-P., Kim, K. M., Basañez, G., Giedt, C. D., Simon, J., Zimmerberg, J., Zhang, K.Y.J., and Hockenbery, D. M. (2001). Antimycin A mimics a cell-death-inducing Bcl-2 homology domain 3. Nat. Cell Biol. 3, 183-191.
40. van der Laan, M., Chacinska, A., Lind, M., Perschil, I., Sickmann, A., Meyer, H. E., Guiard, B., Meisinger, C., Pfanner, N., and Rehling, P. (2005). Pam17 is required for architecture and translocation activity of the mitochondrial protein import motor. Mol. Cell. Biol. 25, 7449-7458.
41. van der Laan, M., Wiedemann, N., Mick, D. U., Guiard, B., Rehling, P., and Pfanner, N. (2006). A role for Tim21 in membrane-potential-dependent preprotein sorting in mitochondria. Curr. Biol. 16, 2271-2276.
42. Yaffe, M. P. (1991). Analysis of mitochondrial function and assembly. Methods Enzymol. 194, 627-643.
43. Yamamoto, H., Esaki, M., Kanamori, T., Tamura, Y., Nishikawa, S.-i., 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.