Regulated interactions of mtHsp70 with Tim44 at the translocon in the mitochondrial inner membrane

Nature Structural and Molecular Biology

Volumn 11, Issue 11, 2004, Pages 1084-1091

  D'Silva, Patrick ^a   Liu, Qinglian ^a,b   Walter, William ^a   Craig, Elizabeth A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; HEAT SHOCK PROTEIN 70; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; POLYPEPTIDE; PROTEIN TIM44; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; CYTOSOL; ENZYME SUBSTRATE COMPLEX; MITOCHONDRIAL MEMBRANE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RIBOSOME; YEAST;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANISOTROPY; BIOLOGICAL TRANSPORT; DOSE-RESPONSE RELATIONSHIP, DRUG; ESCHERICHIA COLI; GENE LIBRARY; HSP70 HEAT-SHOCK PROTEINS; HYDROLYSIS; IMMUNOPRECIPITATION; INTRACELLULAR MEMBRANES; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MUTATION; PEPTIDES; PLASMIDS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPECTROMETRY, FLUORESCENCE; TIME FACTORS;

EID: 7544224771     PISSN: 15459993     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsmb846     Document Type: Article

References (47)

1. Neupert, W. & Brunner, M. The protein import motor of mitochondria. Nat. Rev. Mol. Cell Biol. 8, 555-565 (2002).
2. Wiedemann, N., Frazier, A.E. & Pfanner, N. The protein import machinery of mitochondria. J. Biol. Chem. 279, 14473-14476 (2004).
3. Jensen, R.E. & Johnson, A.E. Opening the door to mitochondrial protein import. Nat. Struct. Biol. 8, 1008-1010 (2001).
4. Bauer, M.F., Sirrenberg, C., Neupert, W. & Brunner, M. Role of Tim23 as voltage sensor and presequence receptor in protein import into mitochondria. Cell 87, 33-41 (1996).
5. Truscott, K. et al. A presequence- and voltage-sensitive channel of the mitochondrial preprotein translocase formed by Tim23. Nat. Struct. Biol. 8, 1074-1082 (2001).
6. Huang, S., Ratliff, K.S. & Matouschek, A. Protein unfolding by the mitochondrial membrane potential. Nat. Struct. Biol. 9, 301-307 (2002).
7. Kang, P.J. et al. Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature 348, 137-143 (1990).
8. Scherer, P., Krieg, U., Hwang, S., Vestweber, D. & Schatz, G. A precursor protein partially translocated into yeast mitochondria is bound to a 70kd mitochondrial stress protein. EMBO J. 9, 4315-4322 (1990).
9. 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).
10. Pilon, M. & Schekman, R. Protein translocation: how Hsp70 pulls it off. Cell 97, 679-682 (1999).
11. Schneider, H.-C. et al. Mitochondrial Hsp70/MIM44 complex facilitates protein import. Nature 371, 768-774 (1994).
12. 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).
13. 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).
14. Maarse, A.C., Blom, J., Grivell, L.A. & Meijer, M. MPI, an essential gene encoding a mitochondrial membrane protein, is possibly involved in protein import into yeast mitochondria. EMBO J. 11, 3619-3628 (1992).
15. Scherer, P.E., Manning-Krieg, U.C., Jeno, P., Schatz, G. & Horst, M. Identification of a 45-kDa protein at the import site of the yeast mitochondrial inner membrane. Proc. Natl. Acad. Sci. USA 89, 11930-11934 (1992).
16. 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).
17. 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).
18. D'Silva, P.D., 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).
19. Kozany, C., Mokranjac, D., Sichting, M., Neupert, W. & Hell, K. The J domain-related cochaperone Tim16 is a constituent of the mitochondrial TIM23 preprotein translocase. Nat. Struct. Mol. Biol. 11, 234-241 (2004).
20. Frazier, A.E. et al. Pam16 has an essential role in the mitochondrial protein import motor. Nat. Struct. Mol. Biol. 11, 226-233 (2004).
21. Liu, Q., Krzewska, J., Liberek, K. & Craig, E.A. Mitochondrial Hsp70 Ssc1:role in protein folding. J. Biol. Chem. 276, 6112-6118 (2001).
22. Bukau, B. & Norwich, A.L. The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366 (1998).
23. Hartl, F. & Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852-1858 (2002).
24. Rudiger, S., Buchberger, A. & Bukau, B. Interaction of Hsp70 chaperones with substrates. Nat. Struct. Biol. 4, 342-349 (1997).
25. Mayer, M.P. et al. Multistep mechanism of substrate binding determines chaperone activity of Hsp70. Nat. Struct. Biol. 7, 586-593 (2000).
26. Buchberger, A., Reinstein, J. & Bukau, B. The DnaK chaperone system: mechanism and comparison with other Hsp70 systems. In Molecular Chaperones and Folding Catalysts: Regulation, Cellular Function and Mechanisms (ed. Bukau, B.) 609-635 (Harwood Academic, 1999).
27. Laufen, T. et al. Mechanism of regulation of Hsp70 chaperones by DnaJ co-chaperones. Proc. Natl. Acad. Sci. USA 96, 5452-5457 (1999).
28. Krimmer, T., Rassow, J., Kunau, W.H., Voos, W. & Pfanner, N. Mitochondrial protein import motor: the ATPase domain of matrix Hsp70 is crucial for binding to Tim44, while the peptide binding domain and the carboxy-terminal segment play a stimulatory role. Mol. Cell. Biol. 20, 5879-5887 (2000).
29. Moro, F., Okamoto, K., Donzeau, M., Neupert, W. & Brunner, M. Mitochondrial protein import: molecular basis of the ATP-dependent interaction of MtHsp70 with Tim44. J. Biol. Chem. 277, 6874-6880 (2002).
30. Strub, A., Rottgers, K. & Voos, W. The Hsp70 peptide-binding domain determines the interaction of the ATPase domain with Tim44 in mitochondria. EMBO J. 21, 2626-2635 (2002).
31. Craig, E.A. & Marszalek, J. A specialized mitochondrial molecular chaperone system: a role in formation of Fe/S centers. Cell Mol. Life Sci. 59, 1658-1665 (2002).
32. Zhu, X. et al. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272, 1606-1614 (1996).
33. Voos, W. et al. Differential requirement for the mitochondrial Hsp70-Tim44 complex in unfolding and translocation of preproteins. EMBO J. 15, 2668-2677 (1996).
34. Merlin, A. et al. The J-related segment of Tim44 is essential for cell Viability: A mutant Tim44 remains in the mitochondrial import site, but inefficiently recruits mtHSP70 and impairs protein translocation. J. Cell Biol. 145, 961-972 (1999).
35. Lim, J.H., Martin, F., Guiard, B., Pfanner, N. & Voos, W. The mitochondrial Hsp70-dependent import system actively unfolds preproteins and shortens the lag phase of translocation. EMBO J. 20, 941-950 (2001).
36. Geissler, A., Rassow, J., Pfanner, N. & Voos, W. Mitochondrial import driving forces: enhanced trapping by matrix Hsp70 stimulates the translocation and reduces the membrane potential dependence of loosely folded preproteins. Mol. Cell. Biol. 21, 7097-7104 (2001).
37. Rassow, J. et al. Mitochondrial protein import: biochemical and genetic evidence for interaction of matrix Hsp70 and the inner membrane protein Mim44. J. Cell Biol. 127, 1547-1556 (1994).
38. Strub, A., Zufall, N. & Voos, W. The putative helical lid of the Hsp70 peptide-binding domain is required for efficient preprotein translocation into mitochondria. J. Mol. Biol. 334, 1087-1099 (2003).
39. Jordan, R. & McMacken, R. Modulation of the ATPase activity of the molecular chaperone DnaK by peptides and the DnaJ and GrpE heat shock proteins, J. Biol. Chem. 270, 4563-4569 (1995).
40. O'Brien, M. & McKay, D. Threonine 204 of the chaperone protein hsc70 influences the structure of the active site but is not essential for ATP hydrolysis. J. Biol. Chem. 268, 24323-24329 (1993).
41. Lopez-Buesca, P., Pfund, C. & Craig, E.A. The biochemical properties of the ATPase activity of a 70-kDa heat shock protein (Hsp70) are governed by the C-terminal domains. Proc. Natl. Acad. Sci. USA 95, 15253-15258 (1998).
42. Slepenkov, S.V. & Witt, S.N. Peptide-induced conformational changes in the molecular chaperone DnaK. Biochemistry 37, 16749-16756 (1998).
43. Slepenkov, S. & Witt, S. Detection of a concerted conformational change in the ATPase domain of DnaK triggered by peptide binding. FEBS Lett. 539, 100-104 (2003).
44. Miao, B., Davis, J.E. & Craig, E.A. Mge1 functions as a nucleotide release factor for Sscl, a mitochondrial Hsp70 of Saccharomyces cerevisiae. J. Mol. Biol. 265, 541-552 (1997).
45. Miroux, B. & Walker, J.E. Over-production of proteins in Escherichia coli: Mutant hosts that allow synthesis of some membrane proteins and Globular proteins at high levels. J. Mol. Biol. 260, 289-298 (1996).
46. Horst, M. et al. Sequential action of two hsp70 complexes during protein import into mitochondria. EMBO J. 16, 1842-1849 (1997).
47. Dutkiewicz, R. et al. Ssq1, a mitochondrial Hsp70 involved in iron-sulfur (Fe/S) center biogenesis: Similarities to and differences from its bacterial counterparts. J. Biol. Chem. 278, 29719-29727 (2003).