Active unfolding of precursor proteins during mitochondrial protein import

EMBO Journal

Volumn 16, Issue 22, 1997, Pages 6727-6736

  Matouschek, Andreas ^d   Azem, Abdussalam ^b   Ratliff, Kevin ^a   Glick, Benjamin S ^c   Schmid, Karl ^b   Schatz, Gottfried ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF CHICAGO   (United States)

^d NONE

Author keywords

Heat shock protein 70; Hsp70; Import; Motor proteins; Protein translocation

Indexed keywords

ADENOSINE TRIPHOSPHATE; DIHYDROFOLATE REDUCTASE; PROTEIN PRECURSOR;

ARTICLE; CELL MEMBRANE TRANSPORT; CYTOPLASM; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS);

EID: 0030781431     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.22.6727     Document Type: Article

References (62)

1. Arretz,M., Schneider.H., Guiard,B., Brunner,M. and Neupert,W. (1994) Characterization of the mitochondrial processing peplidase of Neurospora crassa. J. Biol. Chem., 269, 4959-4967.
2. Bai,Y., Sosnick,T.R., Mayne,L. and Englander,S.W. (1995) Protein folding intermediates: Native-state hydrogen exchange. Science. 269. 192-197.
3. 2 to the mitochondrial intermembrane space contains three distinct functional regions. EMBO J., 12, 2303-2311.
4. Bolliger,L., Deloche,O., Glick,B.S., Georgopoulos,C., Jenö, R., Kronidou, N., Morst, M., Morishima.N, and Schatz,G. (1994) A mitochondrial homolog of bacterial GrpE interacts with mitochondrial hsp70 and is essential for viability. EMBO J., 3, 1998-2006.
5. Bujard,H., Gentz,R., Lanzer,M., Stueber,D.M., Mueller,M., Ibrahimi,I., Hacuptle,M.T. and Dobherstein,B. (1987) A T5 promoter-based transcription-translation system for the analysis of proteins in vitro and in vivo. Methods Enzymol., 155, 416-433.
6. Chang,A.C.Y. and Cohn,S.N. (1978) Phenotypic expression in Ecoli of a UNA sequence coding for mouse dihydrofolale reductase. J. Bacteriol., 134, 1141-1156.
7. Chen,W.J. and Douglas,M.G. (1987) Phosphodiester bond cleavage outside mitochondria is required for the completion of protein import into the mitochondrial matrix. Cell. 49, 651-658.
8. Creighton,T.E. (1993) Proteins: Structure and Molecular Properties. W.H.Freeman and Company, New York.
9. Cyr,D.M., Stuart,R.A. and Neuperl,W. (1993) A matrix ATP requirement for for presequence translocation across the inner membrane of mitochondria. J. Biol. Chem., 268, 23751-23754.
10. Deshaies,R.J., Koch,B.D., Werner-Washburne,M., Craig,H.A. and Schekman,R. (1988) A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature. 332, 800-805.
11. Eilers,M. and Schatz,G. (1986) Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature, 322. 228-232.
12. Eilers,M., Hwang,S. and Schatz,G. (1988) Unfolding and refolding of a purified precursor protein during import into isolated mitochondria. EMBO J., 7. 1139-1145.
13. Endo,T. and Schatz,G. (1988) Latent membrane perturbation activity of a mitochondrial precursor protein is exposed by unfolding. EMBO J., 7, 1153-1158.
14. 2 promotes early divergence from the general mitochondrial import pathway and restricts the unfoldase activity of matrix Hsp70. EMBO J., 14, 6043-6057.
15. 2 and cytochrome cl are processed in two steps. Proc. Natl Acad. Sci. USA. 79, 267-271.
16. Glick,B.S. (1995) Can hsp70 proteins act as force generating motors? Cell. 80, 11-14.
17. Glick,B.S. and Pon,L.A. (1995) Isolation of highly purified mitochondria from Saccharomyces cerevisiae cerevisiae. Methods Enzymol., 213-223.
18. 2 to the mitochondrial intermembrane space: The tightly folded heme-binding domain makes import dependent upon matrix ATP. Protein Sci., 2, 1901-1917.
19. 2). EMBO J., 4, 3265-3272.
20. Gray,T.H. and Fersht,A.R. (1993) Refolding of barnase in the presence of GroE. J. Mol. Biol., 232. 1197-1207.
21. Hachiya,N., Alam,R., Sakasegawa,Y., Sakaguchi,M., Mihara,K. and Omura,T. (1993) A Mitochondrial import factor purified from rat liver cytosol is an ATP-dependent conformational modulator for precursor proteins. EMBO J., 12, 1579-1586.
22. Hartley,R.W. (1989) Barnase and Barstar: Two small proteins to fold and fit together. Trends Biochem. Sci., 14. 450-454.
23. Hase,T., Muller,U., Riezman,H. and Schatz,G. (1984) A 70-kd protein of the yeast mitochondrial outer membrane is targeted and anchored via its extreme amino terminus. EMBO J., 3, 3157-3164.
24. Haucke,V. Lithgow,T., Rospert,S., Hahne.K. and Schatz, G. (1995) The yeast mitochondriai protein import receptor Mas20p binds precursor proteins through electrostatic interaction with the positively charged presequcnce. J. Biol. Chtm., 270, 5565-5570.
25. Hines,V. and Schatz,G. (1993) Precursor binding to yeast mitochondria. A general role for the outer membrane protein Mas70p. J. Biol. Chem., 268, 449-454.
26. Hurt,E.C. Pesold-Hurt,B. and Schatz,G. (1984) The amino-terminal region of an imported mitochondrial precursor polypeptide can direct cytoplasmic dihydrofolate reductase into the mitochondrial matrix. EMBO J., 3, 3149-3156.
27. Hwang,S., Jascur,T., Vestweber,D., Pon,L. and Schatz,G. (1989) Disrupted yeast mitochondria can import precursor proteins directly through their inner membrane. J. Cell Biol., 109. 487-493.
28. Hwang,S.T., Wachter,C. and Schatz,G. (1991) Protein import into the yeast mitochondrial matrix. A new translocation intermediate between the two mitochondrial membranes. J. Biol. Chem., 266, 21083-21089.
29. Jascur,T. (1991) Import of precursor proteins into yeast submitochondrial particles. Methods Cell Biol., 34, 359-368.
30. Kang,P.-L., 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.
31. Kraut, J. and Matthews,D.A. (1987) In Jumak,F.A. and McPherson,A. (eds). Dihydrofolate Reductase, John Wiley & Sons. New York. Vol. 111, pp. 1-72.
32. Kronidou,N., 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.
33. Laloraya,S., Gambill,B.D. and Craig,E.A. (1994) A role for a eukaryotic GrpE-related protein. Mge1p. in protein translocation. Proc. Natl Acad. Sci. USA. 91, 6481-6485.
34. Liberek, K., Showyre,D., Zuylicz,M., Johnson.C. and Georgopoulos,C., (1991) The Escherichia coli DnaK chaperone. the 70-kDa heat shock protein cukaryotic equivalent, changes conformation upon ATP hydrolysis, thus triggering its dissociation from a bound target protein. J. Biol. Chem., 266, 14491-14496.
35. Madox,J. (1994) More models of muscle movement. Nature. 368, 287.
36. Manning-Krieg,U., Scherer,P.F. and Schatz,G. (1991) Sequential action of mitochondrial chaperones in protein import into the matrix. EMBO J., 10. 3273-3280.
37. Matouschek,A., Matthews,J.M., Johnson,C.M. and Fersht,A.R. (1994a) Extrapoloation to water of kinetic and equilibrium data for the unfolding of barnase in urea solutions. Protein Engng. 7, 1089-1095.
38. Matouschek,A., Serrano,I., and Fersht,A.R. (1994b) Analysis of protein folding by protein engineering. In Pain,R.H. (ed.). Mechanisms of Protein Folding. IRL Press. Oxford, UK, pp. 137-159.
39. Matouschek,A., Otzen,D.E., Itdiaki,L.S., Jackson,S.E, and Fersht. A.R. (1995) Movement of the position of the transition state in protein folding. Biochemistry, 34, 13656-13662.
40. Mayer,A., Neupert.W. and Lill,R. (1995) Mitochondrial protein import: Reversible binding of the presequcnce at the trans side of the outer membrane drives partial translocalion and unfolding. Cell. 80. 127-137.
41. Mayo,S.L. and Baldwin,R.L. (1993) Guanidinium chloride induction of partial unfolding in amide proton exchange in RNasc A. Science. 262, 873-876.
42. Ostennann,J., Voos,W., Kang,P.J., Craig,E.A., Neupert,W. and Pfanner,N. (1990) Precursor proteins in transit through mitochondrial transit sites interact with hsp70 in the matrix. FEBS Lett., 277, 281-284.
43. Paddon,C.J. and Hartley,R.W. (1987) Expression of Bacillus amyloliquefacins extracellular ribonuclease (Bamase) in Escherichia coli following an inactivating mutation. Gene. 53, 11-19.
44. Pelham,H.R. (1986) Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell. 46, 959-961.
45. Pfanner,N. and Meijer,M. (1995) Pulling in the proteins. Curr. Biol., 5. 132-135.
46. Rassow,J., Hartl,F.-U., Guiard,B., Pfanner.N. and Neupert.N. (1990) Polypeptides traverse the mitochondrial envelope in an extended state. FEBS Lett., 275, 190-194.
47. 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.
48. Rospert,S., Looser,R., Dubaquié.Y. Matouschek,A., Glick,B.S. and Schatz,G. (1996) Hsp60-independent protein folding in the matrix of yeast mitochondria. EMBO J., 15. 764-774.
49. Schcrer,P.K., Krieg,U.C., Hwang,S.T., Vestweber,D. and Schatz,G. (1990) A precursor protein partly translocated into yeast mitochondria is bound to a 70 kDa mitochondrial stress stress. EMBO J., 9. 4315-4322.
50. Schmid,D., Jaussi,R, and Christen, P. (1992) Precursor of mitochondrial aspartate aminotransferase synlhesized in Escherichia coli is complexed with heat-shock protein DnaK. Eur. J. Biochem., 208. 699-704.
51. Schneider,J.-C., Benhold, J., Bauer,M.K., Dietmeier.K., Guiard,B., Brunner,M. and Neupert,W. (1994) Mitochondrial Hsp70/MIM44 complex facilitates protein import. Nature. 371, 768-774.
52. Shi,L., Kataoka,M. and Fink,A.L. (1996) Conformational characterisation of DnaK and its complexes by small-angle X-ray scattering. Biochemistry. 35, 3297-3108.
53. Simon,S.M., Peskin.C.S. and Oster,G.F. (1992) What drives, the translocation of proteins? Proc. Natl Acad. Sci. USA. 89, 3770-3774.
54. Smilh,B.J. and Yaffe,M.P. (1991) A mutation in the yeast heat-shock factor gene causes temperature- sensitive defects in both mitochondrial protein import and the cell cycle. Mol. Cell. Biol., 11, 2647-2655.
55. Stuart,R.A., Cyr,D.M., Craig,E.A. and Neupert,W. (1994) Mitochondrial molecular chaperones: their role in protein translocation. Trends Biochem. Sci., 19, 87-92.
56. Stueber,D., Ibrahimi,I., Cutler,D., Dobherstein,B. and Bujard,H. (1984) A novel in vitro transcription-translation system: accurate and efticient synthesis of single proteins from cloned DNA sequences. EMBO J., 3,3143-3148.
57. Ungermann,C., Ncupert,W. and Cyr.D.M. (1994) The role of hsp70 in conferring unidirectionality on protein translocation into mitochondria. Science. 266, 1250-1253.
58. Vestweber,D. and Schatz,G. (1988) Point mutations destabilizing a precursor protein enhance its post-translational import into mitochondria. EMBO J., 7. 1147-1151.
59. Viitanen,P.V., Donaldson,G.K., Lorimer,G.H., Luben.T.H. and Gatenby,A.A. (1991) Complex interactions between the chaperonin 60 molecular chaperone and dihydrofolate reductase. Biochemistry. 30, 9716-9723.
60. Voos. W., Gambill, B.D., Guiard,B., Pfanner,N. and Craig,E.A. (1993) Presequence and mature pan of preproteins strongly influence the dependence of mitochondrial protein import on heat shock protein 70 in the matrix. J.Cell Biol., 123, 119 126.
61. Voos,W., Gambill,B.D., Laloraya,S., Ang,D., Craig,E.A. and Pfanner,N. (1994) Mitochondrial GrpE is present in a complex with hsp70 and preprotcins in transit across membranes. Mol. Cell. Biol., 14, 6627-6634.
62. Wilbanks,S.M., Chen,L., Tsuruta,H., Hodgson,K.O. and McKay,D.B. (199S) Solution small-angle X-ray scattering study of the molecular chaperone Hsc70 and its subfragments. Biochemistry. 34. 12095-12106.