The protein import and assembly machinery of the mitochondrial outer membrane

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1658, Issue 1-2, 2004, Pages 37-43

  Taylor, Rebecca D ^a   Pfanner, Nikolaus ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Mitochondria; Porin; Protein assembly; Protein sorting; SAM complex; TOM complex

Indexed keywords

MITOCHONDRIAL PROTEIN; OUTER MEMBRANE PROTEIN; PORIN;

BETA SHEET; BIOGENESIS; CELL STRUCTURE; CONSERVATION BIOLOGY; EUKARYOTE; MEMBRANE TRANSPORT; MITOCHONDRIAL MEMBRANE; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROKARYOTE; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW;

EVOLUTION, MOLECULAR; INTRACELLULAR MEMBRANES; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; PROTEIN PRECURSORS; RECEPTORS, CELL SURFACE;

EUKARYOTA; PROKARYOTA;

EID: 3543038880     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2004.04.017     Document Type: Review

References (66)

1. Schatz G., Dobberstein B. Common principles of protein translocation across membranes. Science. 271:1996;1519-1526
2. Attardi G., Schatz G. Biogenesis of mitochondria. Annu. Rev. Cell Biol. 4:1988;289-333
3. Neupert W. Protein import into mitochondria. Ann. Rev. Biochem. 66:1997;863-917
4. Pfanner N., Geissler A. Versatility of the mitochondrial protein import machinery. Nat. Rev., Mol. Cell Biol. 2:2001;339-349
5. Eaton S., Bartlett K., Pourfarzam M. Mammalian mitochondrial beta-oxidation. Biochem. J. 320(Pt. 2):1996;345-357
6. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev., Mol. Cell Biol. 1:2000;11-21
7. Lill R., Kispal G. Maturation of cellular Fe-S proteins: an essential function of mitochondria. Trends Biochem. Sci. 25:2000;352-356
8. 2+ release: an intimate connection. Trends Biochem. Sci. 25:2000;215-221
9. Bootman M.D., Lipp P., Berridge M.J. The organisation and functions of local Ca(2+) signals. J. Cell. Sci. 114:2001;2213-2222
10. Morgan-Hughes J.A., Hanna M.G. Mitochondrial encephalomyopathies: the enigma of genotype versus phenotype. Biochim. Biophys. Acta. 1410:1999;125-145
11. Schapira A.H., Cock H.R. Mitochondrial myopathies and encephalomyopathies. Eur. J. Clin. Investig. 29:1999;886-898
12. Schapira A.H. Mitochondrial disorders. Biochim. Biophys. Acta. 1410:1999;99-102
13. Tatton W.G., Olanow C.W. Apoptosis in neurodegenerative diseases: the role of mitochondria. Biochim. Biophys. Acta. 1410:1999;195-213
14. Wallace D.C., Murdock D.G. Mitochondria and dystonia: the movement disorder connection? Proc. Natl. Acad. Sci. U. S. A. 96:1999;1817-1819
15. Wallace D.C. Mitochondrial diseases in man and mouse. Science. 283:1999;1482-1488
16. Schon E.A., Kim S.H., Ferreira J.C., Magalhaes P., Grace M., Warburton D., Gross S.J. Chromosomal non-disjunction in human oocytes: is there a mitochondrial connection? Hum. Reprod. 15(Suppl. 2):2000;160-172
17. Shoubridge E.A. Nuclear genetic defects of oxidative phosphorylation. Hum. Mol. Genet. 10:2001;2277-2284
18. Pfanner N., Craig E.A., Hönlinger A. Mitochondrial preprotein translocase. Annu. Rev. Cell Dev. Biol. 13:1997;25-51
19. Emanuelsson O., von Heijne G. Prediction of organellar targeting signals. Biochim. Biophys. Acta. 1541:2001;114-119
20. Hurt E.C., Müller U., Schatz G. The first twelve amino acids of a yeast mitochondrial outer membrane protein can direct a nuclear-encoded cytochrome oxidase subunit to the mitochondrial inner membrane. EMBO J. 4:1985;3509-3518
21. McBride H.M., Millar D.G., Li J.M., Shore G.C. A signal-anchor sequence selective for the mitochondrial outer membrane. J. Cell Biol. 119:1992;1451-1457
22. Rodriguez-Cousino N., Nargang F.E., Baardman R., Neupert W., Lill R., Court D.A. An import signal in the cytosolic domain of the Neurospora mitochondrial outer membrane protein TOM22. J. Biol. Chem. 273:1998;11527-11532
23. Kaufmann T., Schlipf S., Sanz J., Neubert K., Stein R., Borner C. Characterization of the signal that directs Bcl-x(L), but not Bcl-2, to the mitochondrial outer membrane. J. Cell Biol. 160:2003;53-64
24. Nguyen M., Millar D.G., Yong V.W., Korsmeyer S.J., Shore G.C. Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence. J. Biol. Chem. 268:1993;25265-25268
25. Shore G.C., McBride H.M., Millar D.G., Steenaart N.A., Nguyen M. Import and insertion of proteins into the mitochondrial outer membrane. Eur. J. Biochem. 227:1995;9-18
26. Rapaport D., Neupert W. Biogenesis of Tom40, core component of the TOM complex of mitochondria. J. Cell Biol. 146:1999;321-331
27. 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
28. 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
29. 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
30. 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
31. Diekert K., Kispal G., Guiard B., Lill R. An internal targeting signal directing proteins into the mitochondrial intermembrane space. Proc. Natl. Acad. Sci. U. S. A. 96:1999;11752-11757
32. Künkele K.P., Heins S., Dembowski M., Nargang F.E., Benz R., Thieffry M., Walz J., Lill R., Nussberger S., Neupert W. The preprotein translocation channel of the outer membrane of mitochondria. Cell. 93:1998;1009-1019
33. Abe Y., Shodai T., Muto T., Mihara K., Torii H., Nishikawa S., Endo T., Kohda D. Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell. 100:2000;551-560
34. 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 presequence-carrying preprotein and a non-cleavable preprotein. J. Biol. Chem. 274:1999;16522-16530
35. Hines V., Brandt A., Griffiths G., Horstmann H., Brütsch H., Schatz G. Protein import into yeast mitochondria is accelerated by the outer membrane protein MAS70. EMBO J. 9:1990;3191-3200
36. Söllner T., Pfaller R., Griffiths G., Pfanner N., Neupert W. A mitochondrial import receptor for the ADP/ATP carrier. Cell. 62:1990;107-115
37. 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
38. 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 preprotein transfer from receptors to the general insertion pore. Cell. 74:1993;483-492
39. Mayer A., Nargang F.E., Neupert W., Lill R. MOM22 is a receptor for mitochondrial targeting sequences and cooperates with MOM19. EMBO J. 14:1995;4204-4211
40. van Wilpe S., Ryan M.T., Hill K., Maarse A.C., Meisinger C., Brix J., Dekker P.J., Moczko M., Wagner R., Meijer M., Guiard B., Hönlinger A., Pfanner N. Tom22 is a multifunctional organizer of the mitochondrial preprotein translocase. Nature. 401:1999;485-489
41. Dietmeier K., Hönlinger A., Bömer U., Dekker P.J., Eckerskorn C., Lottspeich F., Kubrich M., Pfanner N. Tom5 functionally links mitochondrial preprotein receptors to the general import pore. Nature. 388:1997;195-200
42. 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
43. 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 preproteins. Nature. 395:1998;516-521
44. Mannella C.A., Neuwald A.F., Lawrence C.E. Detection of likely transmembrane beta strand regions in sequences of mitochondrial pore proteins using the Gibbs sampler. J. Bioenerg. Biomembranes. 28:1996;163-169
45. 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
46. Model K., Meisinger C., Prinz T., Wiedemann N., Truscott K.N., Pfanner N., Ryan M.T. Multistep assembly of the protein import channel of the mitochondrial outer membrane. Nat. Struct. Biol. 8:2001;361-370
47. Keil P., Weinzierl A., Kiebler M., Dietmeier K., Söllner T., Pfanner N. Biogenesis of the mitochondrial receptor complex. Two receptors are required for binding of MOM38 to the outer membrane surface. J. Biol. Chem. 268:1993;19177-19180
48. Taylor R.D., McHale B.J., Nargang F.E. Characterization of Neurospora crassa Tom40-deficient mutants and effect of specific mutations on Tom40 assembly. J. Biol. Chem. 278:2003;765-775
49. Wiedemann N., Kozjak V., Chacinska A., Schonfisch B., Rospert S., Ryan M.T., Pfanner N., Meisinger C. Machinery for protein sorting and assembly in the mitochondrial outer membrane. Nature. 424:2003;565-571
50. Rapaport D., Taylor R.D., Kaser M., Langer T., Neupert W., Nargang F.E. Structural requirements of Tom40 for assembly into preexisting TOM complexes of mitochondria. Mol. Biol. Cell. 12:2001;1189-1198
51. Gratzer S., Lithgow T., Bauer R.E., Lamping E., Paltauf F., Kohlwein S.D., Haucke V., Junne T., Schatz G., Horst M. Mas37p, a novel receptor subunit for protein import into mitochondria. J. Cell Biol. 129:1995;25-34
52. Kozjak V., Wiedemann N., Milenkovic D., Lohaus C., Meyer H.E., Guiard B., Meisinger C., Pfanner N. An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J. Biol. Chem. 248:2003;48520-48523
53. Paschen S.A., Waizenegger T., Stan T., Preuss M., Cyrklaff M., Hell K., Rapaport D., Neupert W. Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature. 426:2003;862-866
54. Gentle I., Gabriel K., Beech P., Waller R., Lithgow T. The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J. Cell Biol. 164:2004;19-24
55. Sogo L.F., Yaffe M.P. Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane. J. Cell Biol. 126:1994;1361-1373
56. Hoppins S.C., Nargang F.E. The Tim8-Tim13 complex of Neurospora crassa functions in the assembly of proteins into both mitochondrial membranes. J. Biol. Chem. 279:2004;12396-12405
57. Wiedemann N., Truscott K.N., Pfannschmidt S., Guiard B., Meisinger C., Pfanner N. 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. 279:2004;18188-18194
58. Bulieris P.V., Behrens S., Holst O., Kleinschmidt J.H. Folding and insertion of the outer membrane protein OmpA is assisted by the chaperone Skp and by lipopolysaccharide. J. Biol. Chem. 278:2003;9092-9099
59. Werner J., Augustus A.M., Misra R. Assembly of TolC, a structurally unique and multifunctional outer membrane protein of Escherichia coli K-12. J. Bacteriol. 185:2003;6540-6547
60. Genevrois S., Steeghs L., Roholl P., Letesson J.J., van der Ley P. The Omp85 protein of Neisseria meningitidis is required for lipid export to the outer membrane. EMBO J. 22:2003;1780-1789
61. Voulhoux R., Bos M.P., Geurtsen J., Mols M., Tommassen J. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science. 299:2003;262-265
62. Grad L.I., Descheneau A.T., Neupert W., Lill R., Nargang F.E. Inactivation of the Neurospora crassa mitochondrial outer membrane protein TOM70 by repeat-induced point mutation (RIP) causes defects in mitochondrial protein import and morphology. Curr. Genet. 36:1999;137-146
63. Nargang F.E., Künkele K.P., Mayer A., Ritzel R.G., Neupert W., Lill R. 'Sheltered disruption' of Neurospora crassa MOM22, an essential component of the mitochondrial protein import complex. EMBO J. 14:1995;1099-1108
64. Harkness T.A., Nargang F.E., van der Klei I., Neupert W., Lill R. A crucial role of the mitochondrial protein import receptor MOM19 for the biogenesis of mitochondria. J. Cell Biol. 124:1994;637-648
65. Dimmer K.S., Fritz S., Fuchs F., Messerschmitt M., Weinbach N., Neupert W., Westermann B. Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol. Biol. Cell. 13:2002;847-853
66. Hoppins S.C., Taylor R.D., Nargang F.E. Import of proteins into mitochondria. Brambl R., Marzluf G.A. The Mycota III. 2nd ed. Biochemistry and Molecular Biology. 2004;33-51 Springer-Verlag, Berlin-Heidelberg