Mitochondrial ATP-independent chaperones

IUBMB Life

Volumn 61, Issue 9, 2009, Pages 909-914

  Petrakis, Nikos ^a,b   Alcock, Felicity ^a,c   Tokatlidis, Kostas ^a,b  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

^c MONASH UNIVERSITY   (Australia)

Author keywords

ATP; Chaperones; Membranes; Mitochondria; Small tims; Yeast

Indexed keywords

CHAPERONE; PROTEIN TIM; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; MEMBRANE PROTEIN;

HUMAN; MEMBRANE TRANSPORT; MITOCHONDRIAL MEMBRANE; NONHUMAN; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; ANIMAL; BIOSYNTHESIS; CHEMISTRY; MITOCHONDRION; PHYSIOLOGY; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE;

EUKARYOTA;

ADENOSINE TRIPHOSPHATE; ANIMALS; HUMANS; MEMBRANE PROTEINS; MITOCHONDRIA; MOLECULAR CHAPERONES; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE;

EID: 70350784082     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.235     Document Type: Review

References (65)

1. Anfinsen, C. B. (1972) The formation and stabilization of protein structure. Biochem. J. 128, 737-749.
2. van den Berg, B., Wain, R., Dobson, C. M., and Ellis, R. J. (2000) Macromolecular crowding perturbs protein refolding kinetics: implications for folding inside the cell. EMBO J. 19, 3870-3875. (Pubitemid 30608527)
3. Dobson, C. M. (2003) Protein folding and misfolding. Nature 426, 884-890.
4. Kopito, R. R. (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10, 524-530.
5. Bukau, B., Weissman, J., and Horwich, A. (2006) Molecular chaperones and protein quality control. Cell 125, 443-451.
6. Lee, S. and Tsai, F. T. (2005) Molecular chaperones in protein quality control. J. Biochem. Mol. Biol. 38, 259-265.
7. Dierks, T., Klappa, P., Wiech, H., and Zimmermann, R. (1993) The role of molecular chaperones in protein transport into the endoplasmic reticulum. Philos. Trans. R. Soc. Lond. B Biol. Sci. 339, 335-341.
8. Slepenkov, S. V. and Witt, S. N. (2002) The unfolding story of the Escherichia coli Hsp70 DnaK: is DnaK a holdase or an unfoldase? Mol. Microbiol. 45, 1197-1206.
9. Driessen, A. J., Fekkes, P., and van der Wolk, J. P. (1998) The Sec system. Curr. Opin. Microbiol. 1, 216-222.
10. Wiedemann, N., Pfanner, N., and Chacinska, A. (2006) Chaperoning through the mitochondrial intermembrane space. Mol. Cell 21, 145-148. (Pubitemid 43102582)
11. Gothel, S. F. and Marahiel, M. A. (1999) Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell. Mol. Life Sci. 55, 423-436.
12. Berndt, C., Lillig, C. H., and Holmgren, A. (2008) Thioredoxins and glutaredoxins as facilitators of protein folding. Biochim. Biophys. Acta 1783, 641-650.
13. Morano, K. A., Liu, P. C., and Thiele, D. J. (1998) Protein chaperones and the heat shock response in Saccharomyces cerevisiae. Curr. Opin. Microbiol. 1, 197-203.
14. Arsene, F., Tomoyasu, T., and Bukau, B. (2000) The heat shock response of Escherichia coli. Int. J. Food Microbiol. 55, 3-9.
15. Neupert, W. and Herrmann, J. M. (2007) Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723-749.
16. Webb, C. T., Gorman, M. A., Lazarou, M., Ryan, M. T., and Gulbis, J. M. (2006) Crystal structure of the mitochondrial chaperone TIM9.10 reveals a six-bladed alpha-propeller. Mol. Cell 21, 123-133. (Pubitemid 43017854)
17. Koehler, C. M., Merchant, S., Oppliger, W., Schmid, K., Jarosch, E., Dolfini, L., Junne, T., Schatz, G., and Tokatlidis, K. (1998) Tim9p, an essential partner subunit of Tim10p for the import of mitochondrial carrier proteins. EMBO J. 17, 6477-6486.
18. Sirrenberg, C., Endres, M., Folsch, H., Stuart, R. A., Neupert, W., and Brunner, M. (1998) Carrier protein import into mitochondria mediated by the intermembrane proteins Tim10/Mrs11 and Tim12/Mrs5. Nature 391, 912-915.
19. Gentle, I. E., Perry, A. J., Alcock, F. H., Likic, V. A., Dolezal, P., Ng, E. T., Purcell, A. W., McConnville, M., Naderer, T., Chanez, A. L., Charriere, F., Aschinger, C., Schneider, A., Tokatlidis, K., and Lithgow, T. (2007) Conserved motifs reveal details of ancestry and structure in the small TIM chaperones of the mitochondrial intermembrane space. Mol. Biol. Evol. 24, 1149-1160.
20. Hofmann, S., Rothbauer, U., Muhlenbein, N., Neupert, W., Gerbitz, K. D., Brunner, M., and Bauer, M. F. (2002) The C66W mutation in the deafness dystonia peptide 1 (DDP1) affects the formation of functional DDP1.TIM13 complexes in the mitochondrial intermembrane space. J. Biol. Chem. 277, 23287-23293.
21. Rothbauer, U., Hofmann, S., Muhlenbein, N., Paschen, S. A., Gerbitz, K. D., Neupert, W., Brunner, M., and Bauer, M. F. (2001) Role of the deafness dystonia peptide 1 (DDP1) in import of human Tim23 into the inner membrane of mitochondria. J. Biol. Chem. 276, 37327-37334.
22. Roesch, K., Curran, S. P., Tranebjaerg, L., and Koehler, C. M. (2002) Human deafness dystonia syndrome is caused by a defect in assembly of the DDP1/TIMM8a-TIMM13 complex. Hum. Mol. Genet. 11, 477-486.
23. Koehler, C. M. (2004) The small Tim proteins and the twin Cx3C motif. Trends Biochem. Sci. 29, 1-4.
24. Curran, S. P., Leuenberger, D., Oppliger, W., and Koehler, C. M. (2002) The Tim9p-Tim10p complex binds to the transmembrane domains of the ADP/ATP carrier. EMBO J. 21, 942-953.
25. Allen, S., Lu, H., Thornton, D., and Tokatlidis, K. (2003) Juxtaposition of the two distal CX3C motifs via intrachain disulfide bonding is essential for the folding of Tim10. J. Biol. Chem. 278, 38505-38513.
26. Lu, H., Golovanov, A. P., Alcock, F., Grossmann, J. G., Allen, S., Lian, L. Y., and Tokatlidis, K. (2004) The structural basis of the TIM10 chaperone assembly. J. Biol. Chem. 279, 18959-18966.
27. Baker, M. J., Webb, C. T., Stroud, D. A., Palmer, C. S., Frazier, A. E., Guiard, B., Chacinska, A., Gulbis, J. M., and Ryan, M. T. (2009) Structural and functional requirements for activity of the Tim9-Tim10 complex in mitochondrial protein import. Mol. Biol. Cell 20, 769-779.
28. Beverly, K. N., Sawaya, M. R., Schmid, E., and Koehler, C. M. (2008) The Tim8-Tim13 complex has multiple substrate binding sites and binds cooperatively to Tim23. J. Mol. Biol. 382, 1144-1156.
29. Vial, S., Lu, H., Allen, S., Savory, P., Thornton, D., Sheehan, J., and Tokatlidis, K. (2002) Assembly of Tim9 and Tim10 into a functional chaperone. J. Biol. Chem. 277, 36100-36108.
30. Lu, H., Allen, S., Wardleworth, L., Savory, P., and Tokatlidis, K. (2004) Functional TIM10 chaperone assembly is redox-regulated in vivo. J. Biol. Chem. 279, 18952-18958.
31. Alcock, F. H., Grossmann, J. G., Gentle, I. E., Likic, V. A., Lithgow, T., and Tokatlidis, K. (2008) Conserved substrate binding by chaperones in the bacterial periplasm and the mitochondrial intermembrane space. Biochem. J. 409, 377-387.
32. Korndorfer, I. P., Dommel, M. K., and Skerra, A. (2004) Structure of the periplasmic chaperone Skp suggests functional similarity with cytosolic chaperones despite differing architecture. Nat. Struct. Mol. Biol. 11, 1015-1020.
33. Walton, T. A. and Sousa, M. C. (2004) Crystal structure of Skp, a prefoldin-like chaperone that protects soluble and membrane proteins from aggregation. Mol. Cell 15, 367-374.
34. Siegert, R., Leroux, M. R., Scheufler, C., Hartl, F. U., and Moarefi, I. (2000) Structure of the molecular chaperone prefoldin: unique interaction of multiple coiled coil tentacles with unfolded proteins. Cell 103, 621-632.
35. Stirling, P. C., Bakhoum, S. F., Feigl, A. B., and Leroux, M. R. (2006) Convergent evolution of clamp-like binding sites in diverse chaperones. Nat. Struct. Mol. Biol. 13, 865-870.
36. Leroux, M. R., Fandrich, M., Klunker, D., Siegers, K., Lupas, A. N., Brown, J. R., Schiebel, E., Dobson, C. M., and Hartl, F. U. (1999) MtGimC, a novel archaeal chaperone related to the eukaryotic chaperonin cofactor GimC/prefoldin. EMBO J. 18, 6730-6743.
37. Vainberg, I. E., Lewis, S. A., Rommelaere, H., Ampe, C., Vandekerckhove, J., Klein, H. L., and Cowan, N. J. (1998) Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93, 863-873.
38. Lundin, V. F., Stirling, P. C., Gomez-Reino, J., Mwenifumbo, J. C., Obst, J. M., Valpuesta, J. M., and Leroux, M. R. (2004) Molecular clamp mechanism of substrate binding by hydrophobic coiled-coil residues of the archaeal chaperone prefoldin. Proc. Natl. Acad. Sci. USA 101, 4367-4372.
39. Martin-Benito, J., Boskovic, J., Gomez-Puertas, P., Carrascosa, J. L., Simons, C. T., Lewis, S. A., Bartolini, F., Cowan, N. J., and Valpuesta, J. M. (2002) Structure of eukaryotic prefoldin and of its complexes with unfolded actin and the cytosolic chaperonin CCT. EMBO J. 21, 6377-6386.
40. Schafer, U., Beck, K., and Muller, M. (1999) Skp, a molecular chaperone of gram-negative bacteria, is required for the formation of soluble periplasmic intermediates of outer membrane proteins. J. Biol. Chem. 274, 24567-24574.
41. Chen, R. and Henning, U. (1996) A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins. Mol. Microbiol. 19, 1287-1294.
42. De Cock, H., Schafer, U., Potgeter, M., Demel, R., Muller, M., and Tommassen, J. (1999) Affinity of the periplasmic chaperone Skp of Escherichia coli for phospholipids, lipopolysaccharides and non-native outer membrane proteins. Role of Skp in the biogenesis of outer membrane protein. Eur. J. Biochem. 259, 96-103.
43. Qu, J., Mayer, C., Behrens, S., Holst, O., and Kleinschmidt, J. H. (2007) The trimeric periplasmic chaperone Skp of Escherichia coli forms 1:1 complexes with outer membrane proteins via hydrophobic and electrostatic interactions. J. Mol. Biol. 374, 91-105.
44. Walton, T. A., Sandoval, C. M., Fowler, C. A., Pardi, A., and Sousa, M. C. (2009) The cavity-chaperone Skp protects its substrate from aggregation but allows independent folding of substrate domains. Proc. Natl. Acad. Sci. USA 106, 1772-1777.
45. Vergnolle, M. A., Baud, C., Golovanov, A. P., Alcock, F., Luciano, P., Lian, L. Y., and Tokatlidis, K. (2005) Distinct domains of small Tims involved in subunit interaction and substrate recognition. J. Mol. Biol. 351, 839-849.
46. Adam, A., Endres, M., Sirrenberg, C., Lottspeich, F., Neupert, W., and Brunner, M. (1999) Tim9, a new component of the TIM22.54 translocase in mitochondria. EMBO J. 18, 313-319.
47. Truscott, K. N., Wiedemann, N., Rehling, P., Muller, H., Meisinger, C., Pfanner, N., and Guiard, B. (2002) Mitochondrial import of the ADP/ATP carrier: the essential TIM complex of the intermembrane space is required for precursor release from the TOM complex. Mol. Cell Biol. 22, 7780-7789.
48. Vasiljev, A., Ahting, U., Nargang, F. E., Go, N. E., Habib, S. J., Kozany, C., Panneels, V., Sinning, I., Prokisch, H., Neupert, W., Nussberger, S., and Rapaport, D. (2004) Reconstituted TOM core complex and Tim9/Tim10 complex of mitochondria are sufficient for translocation of the ADP/ATP carrier across membranes. Mol. Biol. Cell 15, 1445-1458.
49. Endres, M., Neupert, W., and Brunner, M. (1999) Transport of the ADP/ATP carrier of mitochondria from the TOM complex to the TIM22.54 complex. EMBO J. 18, 3214-3221.
50. Lionaki, E., de Marcos Lousa, C., Baud, C., Vougioukalaki, M., Panayotou, G., and Tokatlidis, K. (2008) The essential function of Tim12 in vivo is ensured by the assembly interactions of its C-terminal domain. J. Biol. Chem. 283, 15747-15753.
51. Leuenberger, D., Bally, N. A., Schatz, G., and Koehler, C. M. (1999) Different import pathways through the mitochondrial intermembrane space for inner membrane proteins. EMBO J. 18, 4816-4822.
52. Paschen, S. A., Rothbauer, U., Kaldi, K., Bauer, M. F., Neupert, W., and Brunner, M. (2000) The role of the TIM8-13 complex in the import of Tim23 into mitochondria. EMBO J. 19, 6392-6400.
53. 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 mitochondrial protein import. Mol. Biol. Cell 18, 475-486.
54. 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.
55. Gentle, I., Gabriel, K., Beech, P., Waller, R., and Lithgow, T. (2004) The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J. Cell Biol. 164, 19-24.
56. Voulhoux, R., Bos, M. P., Geurtsen, J., Mols, M., and Tommassen, J. (2003) Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299, 262-265.
57. Wu, T., Malinverni, J., Ruiz, N., Kim, S., Silhavy, T. J., and Kahne, D. (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121, 235-245.
58. Habib, S. J., Waizenegger, T., Lech, M., Neupert, W., and Rapaport, D. (2005) Assembly of the TOB complex of mitochondria. J. Biol. Chem. 280, 6434-6440.
59. Wiedemann, N., Truscott, K. N., Pfannschmidt, S., Guiard, B., Meisinger, C., and Pfanner, N. (2004) Biogenesis of the protein import channel Tom40 of the mitochondrial outer membrane: intermembrane space components are involved in an early stage of the assembly pathway. J. Biol. Chem. 279, 18188-18194.
60. Tatsuta, T., Model, K., and Langer, T. (2005) Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol. Biol. Cell 16, 248-259.
61. Burri, L., Vascotto, K., Gentle, I. E., Chan, N. C., Beilharz, T., Stapleton, D. I., Ramage, L., and Lithgow, T. (2006) Integral membrane proteins in the mitochondrial outer membrane of Saccharomyces cerevisiae. FEBS J. 273, 1507-1515.
62. Allen, S., Balabanidou, V., Sideris, D. P., Lisowsky, T., and Tokatlidis, K. (2005) Erv1 mediates the Mia40-dependent protein import pathway and provides a functional link to the respiratory chain by shuttling electrons to cytochrome c. J. Mol. Biol. 353, 937-944.
63. Chacinska, A., Pfannschmidt, S., Wiedemann, N., Kozjak, V., Sanjuan Szklarz, L. K., Schulze-Specking, A., Truscott, K. N., Guiard, B., Meisinger, C., and Pfanner, N. (2004) Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins. EMBO J. 23, 3735-3746.
64. Mesecke, N., Terziyska, N., Kozany, C., Baumann, F., Neupert, W., Hell, K., and Herrmann, J. M. (2005) A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121, 1059-1069.
65. Milenkovic, D., Ramming, T., Muller, J. M., Wenz, L. S., Gebert, N., Schulze-Specking, A., Stojanovski, D., Rospert, S., and Chacinska, A. Identification of the signal directing Tim9 and Tim10 into the intermembrane space of mitochondria. Mol. Biol. Cell 20, 2530-2539.