Insertion of hydrophobic membrane proteins into the inner mitochondrial membrane - A guided tour

Journal of Molecular Biology

Volumn 326, Issue 3, 2003, Pages 639-657

  Rehling, Peter ^a   Pfanner, Nikolaus ^a   Meisinger, Christof ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Carrier proteins; Mitochondria; TIM; TOM; Translocation

Indexed keywords

MEMBRANE PROTEIN;

CELL ORGANELLE; CYTOSOL; GENETIC CODE; GENOME; HUMAN; HYDROPHOBICITY; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW;

INSERTION SEQUENCES;

EID: 0037459118     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01440-7     Document Type: Review

References (128)

1. Lightowlers R.N., Lill R. High-level mitochondriology at high altitude: workshop on mitochondrial (dys-)function. EMBO Rep. 2:2001;1074-1077.
2. Nakai K., Horton P. PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 24:1999;34-36.
3. Taylor A.B., Smith B.S., Kitada S., Kojima K., Miyaura H., Otwinowski Z., et al. Crystal structures of mitochondrial processing peptidase reveal the mode for specific cleavage of import signal sequences. Structure. 9:2001;615-625.
4. vonHeijne G. Mitochondrial targeting sequences may form amphipathic helices. EMBO J. 5:1989;1335-1342.
5. Roise D., Theiler F., Horvath S.J., Tomich J.M., Richards J.H., Allison D.S., Schatz G. Amphiphilicity is essential for mitochondrial pre-sequence function. EMBO J. 7:1988;649-653.
6. Lemire B.D., Fankhauser C., Baker A., Schatz G. The mitochondrial targeting function of randomly generated peptide sequences correlates with predicted helical amphiphilicity. J. Biol. Chem. 264:1989;20206-20215.
7. Abe Y., Shodai T., Muto T., Mihara K., Torii H., Nishikawa S., et al. Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell. 100:2000;551-560.
8. Neupert W. Protein import into mitochondria. Annu. Rev. Biochem. 66:1997;863-917.
9. Pfanner N., Geissler A. Versatility of the mitochondrial protein import machinery. Nature Rev. Mol. Cell. Biol. 2:2001;339-349.
10. 2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism. Cell. 69:1992;809-822.
11. 5 reductase to two different submitochondrial compartments. Cell. 79:1994;829-839.
12. 2 promotes early divergence from the general mitochondrial import pathway and restricts the unfoldase activity of matrix Hsp70. EMBO J. 14:1995;6043-6057.
13. Nunnari J., Fox T.D., Walter P. A mitochondrial protease with two catalytic subunits of non-overlapping specificities. Science. 262:1993;1997-2004.
14. Smagula C., Douglas M.G. Mitochondrial import of the ADP/ATP carrier protein in Saccharomyces cerevisiae. Sequences required for receptor binding and membrane translocation. J. Biol. Chem. 263:1988;6783-6790.
15. Pfanner N., Hoeben P., Tropschug M., Neupert W. The carboxyl-terminal two-thirds of the ADP/ATP carrier polypeptide contains sufficient information to direct translocation into mitochondria. J. Biol. Chem. 262:1987;14851-14854.
16. Nelson D.R., Felix C.M., Swanson J.M. Highly conserved charge-pair networks in the mitochondrial carrier family. J. Mol. Biol. 277:1998;285-308.
17. Brix J., Rüdiger S., Bukau B., Schneider-Mergener J., Pfanner N. Distribution of binding sequences for the mitochondrial import receptors Tom20, Tom22, and Tom70 in a pre-sequence-carrying pre-protein and a non-cleavable pre-protein. J. Biol. Chem. 274:1999;16522-16530.
18. Brix J., Ziegler G.A., Dietmeier K., Schneider-Mergener J., Schulz G.E., Pfanner N. The mitochondrial import receptor Tom70: identification of a 25 kDa core domain with a specific binding site for pre-proteins. J. Mol. Biol. 303:2000;479-488.
19. Wiedemann N., Pfanner N., Ryan M.T. The three modules of ADP/ATP carrier cooperate in receptor recruitment and translocation into mitochondria. EMBO J. 20:2001;951-960.
20. Söllner T., Griffiths G., Pfaller R., Pfanner N., Neupert W. MOM19, an import receptor for mitochondrial precursor proteins. Cell. 59:1989;1061-1070.
21. Ramage L., Junne T., Hahne K., Lithgow T., Schatz G. Functional cooperation of mitochondrial protein import receptors in yeast. EMBO J. 12:1993;4115-4123.
22. Moczko M., Gärtner F., Pfanner N. The protein import receptor MOM19 of yeast mitochondria. FEBS Letters. 326:1993;251-254.
23. Kiebler M., Keil P., Schneider H., van der Klei I.J., Pfanner N., Neupert W. The mitochondrial receptor complex: a central role of MOM22 in mediating pre-protein transfer from receptors to the general insertion pore. Cell. 74:1993;483-492.
24. Lithgow T., Junne T., Suda K., Gratzer S., Schatz G. The mitochondrial outer membrane protein Mas22p is essential for protein import and viability of yeast. Proc. Natl Acad. Sci. USA. 91:1994;11973-11977.
25. Nakai M., Endo T. Identification of yeast MAS17 encoding the functional counterpart of the mitochondrial receptor complex protein MOM22 of Neurospora crassa. FEBS Letters. 357:1995;202-206.
26. Hönlinger A., Kübrich M., Moczko M., Gärtner F., Mallet L., Bussereau F., et al. The mitochondrial receptor complex: Mom22 is essential for cell viability and directly interacts with pre-proteins. Mol. Cell. Biol. 15:1995;3382-3389.
27. van Wilpe S., Ryan M.T., Hill K., Maarse A.C., Meisinger C., Brix J., et al. Tom22 is a multifunctional organizer of the mitochondrial pre-protein translocase. Nature. 401:1999;485-489.
28. Hase T., Müller U., Riezman H., Schatz G. A 70-kd protein of the yeast mitochondrial outer membrane is targeted and anchored via its extreme amino terminus. EMBO J. 3:1984;3157-3164.
29. Hase T., Riezman H., Suda K., Schatz G. Import of proteins into mitochondria: nucleotide sequence of the gene for a 70-kd protein of the yeast mitochondrial outer membrane. EMBO J. 2:1983;2169-2172.
30. 1 precursor reveals an unusually complex amino-terminal pre-sequence. EMBO J. 3:1984;2137-2143.
31. Söllner T., Pfaller R., Griffiths G., Pfanner N., Neupert W. A mitochondrial import receptor for the ADP/ATP carrier. Cell. 62:1990;107-115.
32. Steger H.F., Söllner T., Kiebler M., Dietmeier K.A., Pfaller R., Trulzsch K.S., et al. Import of ADP/ATP carrier into mitochondria: two receptors act in parallel. J. Cell Biol. 111:1990;2353-2363.
33. Hines V., Brandt A., Griffiths G., Horstmann H., Brutsch H., Schatz G. Protein import into yeast mitochondria is accelerated by the outer membrane protein MAS70. EMBO J. 9:1990;3191-3200.
34. Brix J., Dietmeier K., Pfanner N. Differential recognition of pre-proteins by the purified cytosolic domains of the mitochondrial import receptors Tom20, Tom22, and Tom70. J. Biol. Chem. 272:1997;20730-20735.
35. Hill K., Model K., Ryan M.T., Dietmeier K., Martin F., Wagner R., Pfanner N. Tom40 forms the hydrophilic channel of the mitochondrial import pore for pre-proteins. Nature. 395:1998;516-521.
36. Ahting U., Thieffry M., Engelhardt H., Hegerl R., Neupert W., Nussberger S. Tom40, the pore-forming component of the protein-conducting TOM channel in the outer membrane of mitochondria. J. Cell Biol. 153:2001;1151-1160.
37. Dietmeier K., Hönlinger A., Bömer U., Dekker P.J., Eckerskorn C., Lottspeich F., et al. Tom5 functionally links mitochondrial pre-protein receptors to the general import pore. Nature. 388:1997;195-200.
38. Alconada A., Kübrich M., Moczko M., Hönlinger A., Pfanner N. The mitochondrial receptor complex: the small subunit Mom8b/Isp6 supports association of receptors with the general insertion pore and transfer of pre-proteins. Mol. Cell. Biol. 15:1995;6196-6205.
39. Kassenbrock C.K., Cao W., Douglas M.G. Genetic and biochemical characterization of ISP6, a small mitochondrial outer membrane protein associated with the protein translocation complex. EMBO J. 12:1993;3023-3034.
40. Hönlinger A., Bömer U., Alconada A., Eckerskorn C., Lottspeich F., Dietmeier K., Pfanner N. Tom7 modulates the dynamics of the mitochondrial outer membrane translocase and plays a pathway-related role in protein import. EMBO J. 15:1996;2125-2137.
41. Dekker P.J., Ryan M.T., Brix J., Müller H., Hönlinger A., Pfanner N. Pre-protein translocase of the outer mitochondrial membrane: molecular dissection and assembly of the general import pore complex. Mol. Cell. Biol. 18:1998;6515-6524.
42. Künkele K.P., Heins S., Dembowski M., Nargang F.E., Benz R., Thieffry M., et al. The pre-protein translocation channel of the outer membrane of mitochondria. Cell. 93:1998;1009-1019.
43. Meisinger C., Ryan M.T., Hill K., Model K., Lim J.H., Sickmann A., et al. Protein import channel of the outer mitochondrial membrane: a highly stable Tom40-Tom22 core structure differentially interacts with pre-proteins, small tom proteins, and import receptors. Mol. Cell. Biol. 21:2001;2337-2348.
44. Ahting U., Thun C., Hegerl R., Typke D., Nargang F.E., Neupert W., Nussberger S. The TOM core complex: the general protein import pore of the outer membrane of mitochondria. J. Cell Biol. 147:1999;959-968.
45. Baker K.P., Schaniel A., Vestweber D., Schatz G. A yeast mitochondrial outer membrane protein essential for protein import and cell viability. Nature. 348:1990;605-609.
46. Pfaller R., Pfanner N., Neupert W. Mitochondrial protein import. Bypass of proteinaceous surface receptors can occur with low specificity and efficiency. J. Biol. Chem. 264:1989;34-39.
47. Model K., Prinz T., Ruiz T., Radermacher M., Krimmer T., Kühlbrandt W., et al. Protein translocase of the outer mitochondrial membrane: role of import receptors in the structural organization of the TOM complex. J. Mol. Biol. 316:2002;657-666.
48. Eilers M., Schatz G. Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature. 322:1986;228-232.
49. Rassow J., Hartl F.U., Guiard B., Pfanner N., Neupert W. Polypeptides traverse the mitochondrial envelope in an extended state. FEBS Letters. 275:1990;190-194.
50. Künkele K.P., Juin P., Pompa C., Nargang F.E., Henry J.P., Neupert W., et al. The isolated complex of the translocase of the outer membrane of mitochondria. Characterization of the cation-selective and voltage-gated pre-protein-conducting pore. J. Biol. Chem. 273:1998;31032-31039.
51. Rehling P., Wiedemann N., Pfanner N., Truscott K.N. The mitochondrial import machinery for pre-proteins. Crit. Rev. Biochem. Mol. Biol. 36:2001;291-336.
52. Herrmann J.M., Neupert W. Protein transport into mitochondria. Curr. Opin. Microbiol. 3:2000;210-214.
53. Koehler C.M. Protein translocation pathways of the mitochondrion. FEBS Letters. 476:2000;27-31.
54. Chacinska A., Panner N., Meisinger C. How mitochondria import hydrophilic and hydrophobic proteins. Trends Cell Biol. 12:2002;299-303.
55. Komiya T., Rospert S., Koehler C., Looser R., Schatz G., Mihara K. Interaction of mitochondrial targeting signals with acidic receptor domains along the protein import pathway: evidence for the 'acid chain' hypothesis. EMBO J. 17:1998;3886-3898.
56. Mayer A., Neupert W., Lill R. Mitochondrial protein import: reversible binding of the pre-sequence at the trans side of the outer membrane drives partial translocation and unfolding. Cell. 80:1995;127-137.
57. Bolliger L., Junne T., Schatz G., Lithgow T. Acidic receptor domains on both sides of the outer membrane mediate translocation of precursor proteins into yeast mitochondria. EMBO J. 14:1995;6318-6326.
58. Moczko M., Bömer U., Kübrich M., Zufall N., Hönlinger A., Pfanner N. The intermembrane space domain of mitochondrial Tom22 functions as a trans binding site for pre-proteins with N-terminal targeting sequences. Mol. Cell. Biol. 17:1997;6574-6584.
59. Bauer M.F., Sirrenberg C., Neupert W., Brunner M. Role of Tim23 as voltage sensor and pre-sequence receptor in protein import into mitochondria. Cell. 87:1996;33-41.
60. Dekker P.J., Martin F., Maarse A.C., Bömer U., Müller H., Guiard B., et al. The Tim core complex defines the number of mitochondrial translocation contact sites and can hold arrested pre-proteins in the absence of matrix Hsp70-Tim44. EMBO J. 16:1997;5408-5419.
61. Rassow J., Dekker P.J.T., van Wilpe S., Meijer M., Soll J. The pre-protein translocase of the mitochondrial inner membrane: function and evolution. J. Mol. Biol. 286:1999;105-120.
62. Truscott K.N., Kovermann P., Geissler A., Merlin A., Meijer M., Driessen A.J., et al. A pre-sequence- and voltage-sensitive channel of the mitochondrial pre-protein translocase formed by Tim23. Nature Struct. Biol. 8:2001;1074-1082.
63. Gärtner F., Voos W., Querol A., Miller B.R., Craig E.A., Cumsky M.G., Pfanner N. Mitochondrial import of subunit Va of cytochrome c oxidase characterized with yeast mutants. J. Biol. Chem. 270:1995;3788-3795.
64. Stuart R. Insertion of proteins into the inner membrane of mitochondria: the role of the Oxa1 complex. Biochim. Biophys. Acta. 1592:2002;79-87.
65. Chen M., Xie K., Jiang F., Yi L., Dalbey R.E. YidC, a newly defined evolutionarily conserved protein, mediates membrane protein assembly in bacteria. Biol. Chem. 383:2002;1565-1572.
66. Hell K., Neupert W., Stuart R.A. Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA. EMBO J. 20:2001;1281-1288.
67. Pfanner N., Neupert W. Transport of proteins into mitochondria: a potassium diffusion potential is able to drive the import of ADP/ATP carrier. EMBO J. 4:1985;2819-2825.
68. Schleyer M., Schmidt B., Neupert W. Requirement of a membrane potential for the posttranslational transfer of proteins into mitochondria. Eur. J. Biochem. 125:1982;109-116.
69. Gasser S.M., Daum G., Schatz G. Import of proteins into mitochondria. Energy-dependent uptake of precursors by isolated mitochondria. J. Biol. Chem. 257:1982;13034-13041.
70. Martin J., Mahlke K., Pfanner N. Role of an energized inner membrane in mitochondrial protein import. Delta psi drives the movement of pre-sequences. J. Biol. Chem. 266:1991;18051-18057.
71. Huang S., Ratliff K.S., Matouschek A. Protein unfolding by the mitochondrial membrane potential. Nature Struct. Biol. 9:2002;301-307.
72. Herrmann J.M., Neupert W. What fuels polypeptide translocation? An energetical view on mitochondrial protein sorting. Biochim. Biophys. Acta. 1459:2000;331-338.
73. Voos W., Martin H., Krimmer T., Pfanner N. Mechanisms of protein translocation into mitochondria. Biochim. Biophys. Acta. 1422:1999;235-254.
74. Neupert W., Brunner M. The protein import motor of mitochondria. Nature Rev. Mol. Cell. Biol. 3:2002;555-565.
75. Schneider H.C., Berthold J., Bauer M.F., Dietmeier K., Guiard B., Brunner M., Neupert W. Mitochondrial Hsp70/MIM44 complex facilitates protein import. Nature. 371:1994;768-774.
76. Kronidou N.G., Oppliger W., Bolliger L., Hannavy K., Glick B.S., Schatz G., Horst M. Dynamic interaction between Isp45 and mitochondrial hsp70 in the protein import system of the yeast mitochondrial inner membrane. Proc. Natl Acad. Sci. USA. 91:1994;12818-12822.
77. Rassow J., Maarse A.C., Krainer E., Kübrich M., Müller H., Meijer M., et al. Mitochondrial protein import: biochemical and genetic evidence for interaction of matrix hsp70 and the inner membrane protein MIM44. J. Cell Biol. 127:1994;1547-1556.
78. Horst M., Jeno P., Kronidou N.G., Bolliger L., Oppliger W., Scherer P., et al. Protein import into yeast mitochondria: the inner membrane import site protein ISP45 is the MPI1 gene product. EMBO J. 12:1993;3035-3041.
79. Blom J., Kübrich M., Rassow J., Voos W., Dekker P.J., Maarse A.C., et al. The essential yeast protein MIM44 (encoded by MPI1) is involved in an early step of pre-protein translocation across the mitochondrial inner membrane. Mol. Cell. Biol. 13:1993;7364-7371.
80. Scherer P.E., Krieg U.C., Hwang S.T., Vestweber D., Schatz G. A precursor protein partly translocated into yeast mitochondria is bound to a 70 kd mitochondrial stress protein. EMBO J. 9:1990;4315-4322.
81. Kang P.J., Ostermann J., Shilling J., Neupert W., Craig E.A., Pfanner N. Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature. 348:1990;137-143.
82. Glick B.S. Can Hsp70 proteins act as force-generating motors? Cell. 80:1995;11-14.
83. Ungermann C., Neupert W., Cyr D.M. The role of Hsp70 in conferring unidirectionality on protein translocation into mitochondria. Science. 266:1994;1250-1253.
84. Gaume B., Klaus C., Ungermann C., Guiard B., Neupert W., Brunner M. Unfolding of pre-proteins upon import into mitochondria. EMBO J. 17:1998;6497-6507.
85. Okamoto K., Brinker A., Paschen S.A., Moarefi I., Hayer-Hartl M., Neupert W., Brunner M. The protein import motor of mitochondria: a targeted molecular ratchet driving unfolding and translocation. EMBO J. 21:2002;3659-3671.
86. Horst M., Oppliger W., Feifel B., Schatz G., Glick B.S. The mitochondrial protein import motor: dissociation of mitochondrial hsp70 from its membrane anchor requires ATP binding rather than ATP hydrolysis. Protein Sci. 5:1996;759-767.
87. von Ahsen O., Voos W., Henninger H., Pfanner N. The mitochondrial protein import machinery. Role of ATP in dissociation of the Hsp70.Mim44 complex. J. Biol. Chem. 270:1995;29848-29853.
88. Voisine C., Craig E.A., Zufall N., von Ahsen O., Pfanner N., Voos W. The protein import motor of mitochondria: unfolding and trapping of pre-proteins are distinct and separable functions of matrix Hsp70. Cell. 97:1999;565-574.
89. Voos W., von Ahsen O., Muller H., Guiard B., Rassow J., Pfanner N. Differential requirement for the mitochondrial Hsp70-Tim44 complex in unfolding and translocation of pre-proteins. EMBO J. 15:1996;2668-2677.
90. Geissler A., Rassow J., Pfanner N., Voos W. Mitochondrial import driving forces: enhanced trapping by matrix Hsp70 stimulates translocation and reduces the membrane potential dependence of loosely folded pre-proteins. Mol. Cell. Biol. 21:2001;7097-7104.
91. Zimmermann R., Neupert W. Transport of proteins into mitochondria. Posttranslational transfer of ADP/ATP carrier into mitochondria in vitro. Eur. J. Biochem. 109:1980;217-229.
92. Dekker P.J., Müller H., Rassow J., Pfanner N. Characterization of the pre-protein translocase of the outer mitochondrial membrane by blue native electrophoresis. Biol. Chem. 377:1996;535-538.
93. Hachiya N., Mihara K., Suda K., Horst M., Schatz G., Lithgow T. Reconstitution of the initial steps of mitochondrial protein import. Nature. 376:1995;705-709.
94. Hachiya N., Alam R., Sakasegawa Y., Sakaguchi M., Mihara K., Omura T. A mitochondrial import factor purified from rat liver cytosol is an ATP-dependent conformational modulator for precursor proteins. EMBO J. 12:1993;1579-1586.
95. Komiya T., Rospert S., Schatz G., Mihara K. Binding of mitochondrial precursor proteins to the cytoplasmic domains of the import receptors Tom70 and Tom20 is determined by cytoplasmic chaperones. EMBO J. 16:1997;4267-4275.
96. Pfanner N., Neupert W. Distinct steps in the import of ADP/ATP carrier into mitochondria. J. Biol. Chem. 262:1987;7528-7536.
97. Pfanner N., Tropschug M., Neupert W. Mitochondrial protein import: nucleoside triphosphates are involved in conferring import-competence to precursors. Cell. 49:1987;815-823.
98. Pfaller R., Steger H.F., Rassow J., Pfanner N., Neupert W. Import pathways of precursor proteins into mitochondria: multiple receptor sites are followed by a common membrane insertion site. J. Cell. Biol. 107:1988;2483-2490.
99. Rassow J., Pfanner N. Mitochondrial pre-proteins en route from the outer membrane to the inner membrane are exposed to the intermembrane space. FEBS Letters. 293:1991;85-88.
100. Söllner T., Rassow J., Wiedmann M., Schlossmann J., Keil P., Neupert W., Pfanner N. Mapping of the protein import machinery in the mitochondrial outer membrane by crosslinking of translocation intermediates. Nature. 355:1992;84-87.
101. Schlossmann J., Dietmeier K., Pfanner N., Neupert W. Specific recognition of mitochondrial pre-proteins by the cytosolic domain of the import receptor MOM72. J. Biol. Chem. 269:1994;11893-11901.
102. Ryan M.T., Müller H., Pfanner N. Functional staging of ADP/ATP carrier translocation across the outer mitochondrial membrane. J. Biol. Chem. 274:1999;20619-20627.
103. Koehler C.M., Jarosch E., Tokatlidis K., Schmid K., Schweyen R.J., Schatz G. Import of mitochondrial carriers mediated by essential proteins of the intermembrane space. Science. 279:1998;369-373.
104. Koehler C.M., Merchant S., Oppliger W., Schmid K., Jarosch E., Dolfini L., et al. Tim9p, an essential partner subunit of Tim10p for the import of mitochondrial carrier proteins. EMBO J. 17:1998;6477-6486.
105. Adam A., Endres M., Sirrenberg C., Lottspeich F., Neupert W., Brunner M. Tim9, a new component of the TIM22.54 translocase in mitochondria. EMBO J. 18:1999;313-319.
106. Sirrenberg C., Endres M., Folsch H., Stuart R.A., Neupert W., Brunner M. Carrier protein import into mitochondria mediated by the intermembrane proteins Tim10/Mrs11 and Tim12/Mrs5. Nature. 391:1998;912-915.
107. Sirrenberg C., Bauer M.F., Guiard B., Neupert W., Brunner M. Import of carrier proteins into the mitochondrial inner membrane mediated by Tim22. Nature. 384:1996;582-585.
108. Curran S.P., Leuenberger D., Oppliger W., Koehler C.M. The Tim9p-Tim10p complex binds to the transmembrane domains of the ADP/ATP carrier. EMBO J. 21:2002;942-953.
109. Endres M., Neupert W., Brunner M. Transport of the ADP/ATP carrier of mitochondria from the TOM complex to the TIM22.54 complex. EMBO J. 18:1999;3214-3221.
110. Truscott K.N., Wiedemann N., Rehling P., Müller H., Meisinger C., Panner N., Guiard B. 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. 22:2002;7780-7789.
111. Murphy M.P., Leuenberger D., Curran S.P., Oppliger W., Koehler C.M. The essential function of the small Tim proteins in the TIM22 import pathway does not depend on formation of the soluble 70-kilodalton complex. Mol. Cell. Biol. 21:2001;6132-6138.
112. Kovermann P., Truscott K.N., Guiard B., Rehling P., Sepuri N.B., Muller H., et al. Tim22, the essential core of the mitochondrial protein insertion complex, forms a voltage-activated and signal-gated channel. Mol. Cell. 9:2002;363-373.
113. Koehler C.M., Murphy M.P., Bally N.A., Leuenberger D., Oppliger W., Dolfini L., et al. Tim18p, a new subunit of the TIM22 complex that mediates insertion of imported proteins into the yeast mitochondrial inner membrane. Mol. Cell. Biol. 20:2000;1187-1193.
114. Kerscher O., Sepuri N.B., Jensen R.E. Tim18p is a new component of the Tim54p-Tim22p translocon in the mitochondrial inner membrane. Mol. Biol. Cell. 11:2000;103-116.
115. Kerscher O., Holder J., Srinivasan M., Leung R.S., Jensen R.E. The Tim54p-Tim22p complex mediates insertion of proteins into the mitochondrial inner membrane. J. Cell Biol. 139:1997;1663-1675.
116. Rapoport T.A., Jungnickel B., Kutay U. Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu. Rev. Biochem. 65:1996;271-303.
117. Driessen A.J., Fekkes P., van der Wolk J.P. The Sec system. Curr. Opin. Microbiol. 1:1998;216-222.
118. Bauer M.F., Hofmann S., Neupert W., Brunner M. Protein translocation into mitochondria: the role of TIM complexes. Trends Cell Biol. 10:2000;25-31.
119. Jarvis P., Soll J. Toc, Tic, and chloroplast protein import. Biochim. Biophys. Acta. 1541:2001;64-79.
120. Wachter C., Schatz G., Glick B.S. Role of ATP in the intramitochondrial sorting of cytochrome c1 and the adenine nucleotide translocator. EMBO J. 11:1992;4787-4794.
121. el Moualij B., Duyckaerts C., Lamotte-Brasseur J., Sluse F.E. Phylogenetic classification of the mitochondrial carrier family of Saccharomyces cerevisiae. Yeast. 13:1997;573-581.
122. Kurz M., Martin H., Rassow J., Pfanner N., Ryan M.T. Biogenesis of Tim proteins of the mitochondrial carrier import pathway: differential targeting mechanisms and crossing over with the main import pathway. Mol. Biol. Cell. 10:1999;2461-2474.
123. Kaldi K., Bauer M.F., Sirrenberg C., Neupert W., Brunner M. Biogenesis of Tim23 and Tim17, integral components of the TIM machinery for matrix-targeted pre-proteins. EMBO J. 17:1998;1569-1576.
124. Leuenberger D., Bally N.A., Schatz G., Koehler C.M. Different import pathways through the mitochondrial intermembrane space for inner membrane proteins. EMBO J. 18:1999;4816-4822.
125. Koehler C.M., Leuenberger D., Merchant S., Renold A., Junne T., Schatz G. Human deafness dystonia syndrome is a mitochondrial disease. Proc. Natl Acad. Sci. USA. 96:1999;2141-2146.
126. Paschen S.A., Rothbauer U., Kaldi K., Bauer M.F., Neupert W., Brunner M. The role of the TIM8-13 complex in the import of tim23 into mitochondria. EMBO J. 19:2000;6392-6400.
127. Roesch K., Curran S.P., Tranebjaerg L., Koehler C.M. Human deafness dystonia syndrome is caused by a defect in assembly of the DDP1/TIMM8a-TIMM13 complex. Hum. Mol. Genet. 11:2002;477-486.
128. Rothbauer U., Hofmann S., Muhlenbein N., Paschen S.A., Gerbitz K.D., Neupert W., et al. Role of the deafness dystonia peptide 1 (DDP1) in import of human Tim23 into the inner membrane of mitochondria. J. Biol. Chem. 276:2001;37327-37334.