The protein import motor of mitochondria: Unfolding and trapping of preproteins are distinct and separable functions of matrix Hsp70

Cell

Volumn 97, Issue 5, 1999, Pages 565-574

  Voisine, Cindy ^a   Craig, Elizabeth A ^a   Zufall, Nicole ^b   Von Ahsen, Oliver ^b   Pfanner, Nikolaus ^b   Voos, Wolfgang ^b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; HEAT SHOCK PROTEIN 70;

AMINO ACID SUBSTITUTION; ARTICLE; ENZYME ACTIVITY; GENE MUTATION; MEMBRANE MODEL; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN TRANSPORT; YEAST;

EID: 0033612301     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80768-0     Document Type: Article

References (41)

1. 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.
2. Bömer, U., Maarse, A.C., Martin, F., Geissler, A., Merlin, A., Schönfisch, B., Meijer, M., Pfanner, N., and Rassow, J. (1998). Separation of structural and dynamic functions of the mitochondrial translocase: Tim44 is crucial for the inner membrane import sites in translocation of tightly folded domains, but not of loosely folded preproteins. EMBO J. 17, 4226-4237.
3. Brodsky, J.L. (1996). Post-translational protein translocation: not all hsc70s are created equal. Trends Biochem. Sci. 21, 122-126.
4. Chauwin, J.F., Oster, G., and Glick, B.S. (1998). Strong precursorpore interactions constrain models for mitochondrial protein import. Biophys. J. 74, 1732-1743.
5. 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.
6. Duong, F., Eichler, J., Price, A., Leonard, M.R., and Wickner, W. (1997). Biogenesis of the gram-negative bacterial envelope. Cell 91, 567-573.
7. Eilers, M., and Schatz, G. (1986). Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature 322, 228-232.
8. 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.
9. 2 promotes early divergence from the general mitochondrial import pathway and restricts the unfoldase activity of matrix Hsp70. EMBO J. 14, 6043-6057.
10. Gaume, B., Klaus, C., Ungermann, C., Guiard, B., Neupert, W., and Brunner, M. (1998). Unfolding of preproteins upon import into mitochondria. EMBO J. 17, 6497-6507.
11. Glick, B.S. (1995). Can Hsp70 proteins act as force-generating motors? Cell 80, 11-14.
12. 2 to the mitochondrial intermembrane space: the tightly folded heme-binding domain makes import dependent upon matrix ATP. Protein Sci. 2, 1901-1917.
13. Hamman, B.D., Hendershot, L.M., and Johnson, A.E. (1998). BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell 92, 747-758.
14. Horst, M., Oppliger, W., Feifel, B., Schatz, G., and Glick, B.S. (1996). The mitochondrial protein import motor: dissociation of mitochondrial hsp70 from its membrane anchor requires ATP binding rather than ATP hydrolysis. Protein Sci. 5, 759-767.
15. Kang, P.J., Ostermann, J., Shilling, J., Neupert, W., Craig, E.A., and Pfanner, N. (1990). Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature 348, 137-143.
16. Kronidou, N.G., Oppliger, W., Bolliger, L., Hannavy, K., Glick, B.S., Schatz, G., and Horst, M. (1994). Dynamic interaction between Isp45 and mitochondrial hsp70 in the protein import system of the yeast mitochondrial inner membrane. Proc. Natl. Acad. Sci. USA 91, 12818-12822.
17. Lyman, S.K., and Schekman, R. (1997). Binding of secretory precursor polypeptides to a translocon subcomplex is regulated by BiP. Cell 88, 85-96.
18. Matouschek, A., Azem, A., Ratliff, K., Glick, B.S., Schmid, K., and Schatz, G. (1997). Active unfolding of precursor proteins during mitochondrial protein import. EMBO J. 16, 6727-6736.
19. Neupert, W. (1997). Protein import into mitochondria. Annu. Rev. Biochem. 66, 863-917.
20. Orr-Weaver, T.L., Nicolas, A., and Szostak, J.W. (1988). Gene conversion adjacent to regions of double-strand break repair. Mol. Cell. Biol. 8, 5292-5298.
21. Ostermann, J., Horwich, A.L., Neupert, W., and Hartl, F.U. (1989). Protein folding in mitochondria requires complex formation with hsp60 and ATP hydrolysis. Nature 341, 125-130.
22. Panzner, S., Dreier, L., Hartmann, E., Kostka, S., and Rapoport, T.A. (1995). Posttranslational protein transport in yeast reconstituted with a purified complex of Sec proteins and Kar2p. Cell 81, 561-570.
23. Peitsch, M.C. (1996). ProMod and Swiss-Model: Internet-based tools for automated comparative protein modelling. Biochem. Soc. Trans. 24, 274-279.
24. Pfanner, N., and Meijer, M. (1995). Protein sorting: pulling in the proteins. Curr. Biol. 5, 132-135.
25. Pfanner, N., Craig, E.A., and Hönlinger, A. (1997). Mitochondrial preprotein translocase. Annu. Rev. Cell. Dev. Biol. 13, 25-51.
26. 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.
27. Rassow, J., Maarse, A.C., Krainer, E., Kübrich, M., Müller, H., Meijer, M., Craig, E.A., and Pfanner, N. (1994). Mitochondrial protein import: biochemical and genetic evidence for interaction of matrix hsp70 and the inner membrane protein MIM44. J. Cell Biol. 127, 1547-1556.
28. Ryan, K.R., and Jensen, R.E. (1995). Protein translocation across mitochondrial membranes: what a long, strange trip it is. Cell 83, 517-519.
29. Schatz, G., and Dobberstein, B. (1996). Common principles of protein translocation across membranes. Science 271, 1519-1526.
30. Schneider, H.-C., Berthold, J., Bauer, M.F., Dietmeier, K., Guiard, B., Brunner, M., and Neupert, W. (1994). Mitochondrial Hsp70/MIM44 complex facilitates protein import. Nature 371, 768-774.
31. Schneider, H.-C., Westermann, B., Neupert, W., and Brunner, M. (1996). The nucleotide exchange factor MGE exerts a key function in the ATP-dependent cycle of mt-Hsp70-Tim44 interaction driving mitochondrial protein import. EMBO J. 15, 5796-5803.
32. 2 into the mitochondrial intermembrane space: specific recognition of the sorting signal. EMBO J. 12, 2295-2302.
33. Simon, M.S., Peskin, C.S., and Oster, G.F. (1992). What drives the translocation of proteins? Proc. Natl. Acad. Sci. USA 89, 3770-3774.
34. Söllner, T., Rassow, J., and Pfanner, N. (1991). Analysis of mitochondrial protein import using translocation intermediates and specific antibodies. Methods Cell Biol. 34, 345-358.
35. Stuart, R.A., Gruhler, A., van der Klei, I., Guiard, B., Koll, H., and Neupert, W. (1994). The requirement of matrix ATP for the import of precursor proteins into the mitochondrial matrix and intermembrane space. Eur. J. Biochem. 220, 9-18.
36. Ungermann, C., Neupert, W., and Cyr, D.M. (1994). The role of hsp70 in conferring unidirectionality on protein translocation. Science 266, 1250-1253.
37. Ungermann, C., Guiard, B., Neupert, W., and Cyr, D.M. (1996). The Δψ-and Hsp70/MIM44-dependent reaction cycle driving early steps of protein import into mitochondria. EMBO J. 15, 735-744.
38. von Ahsen, O., Voos, W., Henninger, H., and Pfanner, N. (1995). The mitochondrial protein import machinery. Role of ATP in dissociation of the Hsp70-Mim44 complex. J. Biol. Chem. 270, 29848-29853.
39. Voos, W., Gambill, B.D., Guiard, B., Pfanner, N., and Craig, E.A. (1993). Presequence and mature part of preproteins strongly influence the dependence of mitochondrial protein import on heat shock protein 70 in the matrix. J. Cell Biol. 123, 119-126.
40. Voos, W., von Ahsen, O., Müller, H., Guiard, B., Rassow, J., and Pfanner, N. (1996). Differential requirement for the mitochondrial Hsp70-Tim44 complex in unfolding and translocation of preproteins. EMBO J. 15, 2668-2677.
41. Zhu, X., Zhao, X., Burkholder, W.F., Gragerov, A., Ogata, C.M., Gottesman, M.E., and Hendrickson, W.A. (1996). Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272, 1606-1614.