Functions of the small proteins in the TOM complex of Neurospora crasssa

Molecular Biology of the Cell

Volumn 16, Issue 9, 2005, Pages 4172-4182

  Sherman, E Laura ^a   Go, Nancy E ^a   Nargang, Frank E ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; MITOCHONDRIAL PROTEIN; MUTANT PROTEIN; PROTEIN PRECURSOR; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE PROTEIN; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE PROTEIN 5; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE PROTEIN 6; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE PROTEIN 7; UNCLASSIFIED DRUG;

ARTICLE; CELL ORGANELLE; COMPLEX FORMATION; CONTROLLED STUDY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NEUROSPORA CRASSA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN ISOLATION; PROTEIN STABILITY; PROTEIN TARGETING; PROTEIN TRANSPORT;

FUNGAL PROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; NEUROSPORA CRASSA; ORGANISMS, GENETICALLY MODIFIED; PROTEIN PRECURSORS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE PROTEINS;

NEUROSPORA; NEUROSPORA CRASSA;

EID: 24344508557     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-03-0187     Document Type: Article

References (60)

1. Ahting, U., Thieffry, M., Engelhardt, H., Hegerl, R., Neupert, W., and Nussberger, S. (2001). Tom40, the pore-forming component of the protein-conducting TOM channel in the outer membrane of mitochondria. J. Cell Biol. 153, 1151-1160.
2. Ahting, U., Thun, C, Hegerl, R., Typke, D., Nargang, F. E., Neupert, W., and Nussberger, S. (1999). The TOM core complex: the general protein import pore of the outer membrane of mitochondria. J. Cell Biol. 147, 959-968.
3. Alconada, A., Kübrich, M., Moczko, M., Hönlinger, A., and Pfanner, N. (1995). The mitochondrial receptor complex: the small subunit Mom8b/Isp6 supports association of receptors with the general insertion pore and transfer of preproteins. Mol. Cell. Biol. 15, 6196-6205.
4. Ausubel, R. A., Brent, R., Kingston, R. E., Moore, D. D., and Seidman, J. G. (1992). Current Protocols in Molecular Biology, New York: Greene and Wiley Interscience.
5. Baker, K. P., Schaniel, A., Vestweber, D., and Schatz, G. (1990). A yeast mitochondrial outer membrane protein is essential for protein import and cell viability. Nature 348, 605-609.
6. Court, D. A., Nargang, F. E., Steiner, H., Hodges, R. S., Neupert, W., and Lill, R. (1996). Role of the intermembrane space domain of the preprotein receptor Tom22 in protein import into mitochondria. Mol. Cell. Biol. 16, 4035-4042.
7. Davis, R. H., and De Serres, F. J. (1970). Genetic and microbiological research techniques for Neurospora crassa. Methods Enzymol. 17, 79-143.
8. Dekker, P.J.T., Ryan, M. T., Brix, J., Müller, H., Hönlinger, A., and Pfanner, N. (1998). Preprotein translocase of the outer mitochondrial membrane: molecular dissection and assembly of the general import pore complex. Mol. Cell. Biol. 18, 6515-6524.
9. Dembowski, M., Künkele, K.-P., Nargang, F., Neupert, W., and Rapaport, D. (2001). Assembly of Tom6 and Tom7 into the TOM core complex of Neurospora crassa. J. Biol. Chem. 276, 17679-17685.
10. Descheneau, A. T., Cleary, I. A., and Nargang, F. E. (2005). Genetic evidence for a regulatory pathway controlling alternative oxidase production in Neurospora crassa. Genetics 169, 123-135.
11. Dietmeier, K., Hönlinger, A., Bömer, U., Dekker, P.J.T., Eckerskorn, C., Lottspeich, F., Kübrich, M., and Pfanner, N. (1997). Tom5 functionally links mitochondrial preprotein receptors to the general import pore. Nature 388, 195-200.
12. Endo, T., Yamamoto, H., and Esaki, M. (2003). Functional cooperation and separation of translocators in protein import into mitochondria, the double-membrane bounded organelles. J. Cell Sci. 116, 3259-3267.
13. Esaki, M., Shimizu, H., Ono, T., Yamamoto, H., Kanamori, T., Nishikawa, S., and Endo, T. (2004). Mitochondrial protein import. Requirement of presequence elements and Tom components for precursor binding of the TOM complex. J. Biol. Chem. 279, 45701-45707.
14. Galagan, J. E. et al. (2003). The genome sequence of the filamentous fungus Neurospora crassa. Nature 422, 859-868.
15. 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.
16. Good, A. G., and Crosby, W. L. (1989). Anaerobic induction of alanine aminotransferase in barley root tissue. Plant Physiol. 90, 1305-1309.
17. Habib, S. J., Vasiljev, A., Neupert, W., and Rapaport, D. (2003). Multiple functions of tail-anchor domains of mitochondrial outer membrane proteins. FEBS Lett. 555, 511-515.
18. Harkness, T.A.A., Nargang, F. E., Van der Klei, I., Neupert, W., and Lill, R. (1994). A crucial role of the mitochondrial protein import receptor MOM19 for the biogenesis of mitochondria. J. Cell Biol. 124, 637-648.
19. Hill, K., Modell, K., Ryan, M., Dietmeier, K., Martin, F., Wagner, R., and Pfanner, N. (1998). Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature 395, 516-521.
20. Hönlinger, A., Bömer, U., Alconada, A., Eckerskorn, C., Lottspeich, F., Dietmeier, K., and Pfanner, N. (1996). Tom7 modulates the dynamics of the mitochondrial outer membrane translocase and plays a pathway-related role in protein import. EMBO J. 15, 2125-2137.
21. Hoppins, S. C., Taylor, R. D., and Nargang, F. E. (2004). Import of proteins into mitochondria. In: The Mycota III. Biochemistry and Molecular Biology, eds. R. Brambl and G. A. Marzluf, Heidelberg: Springer-Verlag, 33-51.
22. Horie, C., Suzuki, H., Sakaguchi, M., and Mihara, K. (2003). Targeting and assembly of mitochondrial tail-anchored protein Tom5 to the TOM complex depend on a signal distinct from that of tail-anchored proteins dispersed in the membrane. J. Biol. Chem. 278, 41462-41471.
23. Humphries, A. D., Streimann, I. C., Stojanovski, D., Johnston, A. J., Yano, M., Hoogenraad, N. J., and Ryan, M. T. (2005). Dissection of the mitochondrial import and assembly pathway for human Tom40. J. Biol. Chem. 280, 11535-11543.
24. Ishikawa, D., Yamamoto, H., Tamura, Y., Moritoh, K., and Endo, T. (2004). Two novel proteins in the mitochondrial outer membrane mediate β-barrel protein assembly. J. Cell Biol. 166, 621-627.
25. Kanamori, T., Nishikawa, S., Nakai, M., Shin, I., Schultz, P. G., and Endo, T. (1999). Uncoupling of transfer of the presequence and unfolding of the mature domain in precursor translocation across the mitochondrial outer membrane. Proc. Natl. Acad. Sci. USA 96, 3634-3639.
26. Kassenbrock, C. K., Cao, W., and Douglas, M. G. (1993). Generic and biochemical characterization of ISP6, a small mitochondrial outer membrane protein associated with the protein translocation complex. EMBO J. 12, 3023-3034.
27. Kiebler, M., Keil, P., Schneider, H., van der Klei, I., Pfanner, N., and Neupert, W. (1993). The mitochondrial receptor complex: a central role of MOM22 in mediating transfer of preproteins from receptors to the general insertion pore. Cell 74, 483-492.
28. Koehler, C. M. (2004). New developments in mitochondrial assembly. Annu. Rev. Cell Dev. Biol. 20, 309-335.
29. Kozjak, V., Wiedemann, N., Milenkovic, D., Lohaus, C., Meyer, H. E., Guiard, B., Meisinger, C., and Pfanner, N. (2003). An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J. Biol. Chem. 278, 48520-48523.
30. Kurz, M., Martin, H., Rassow, J., Pfanner, N., and Ryan, M. T. (1999). 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, 2461-2474.
31. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
32. Mayer, A., Lill, R., and Neupert, W. (1993). Translocation and insertion of precursor proteins into isolated outer membranes of mitochondria. J. Cell Biol. 121, 1233-1243.
33. Mayer, A., Nargang, F. E., Neupert, W., and Lill, R. (1995). MOM22 is a receptor for mitochondrial targeting sequences and cooperates with MOM19. EMBO J. 14, 4204-4211.
34. Meisinger, C. et al. (2004). The mitochondrial morphology protein Mdm10 functions in assembly of the preprotein translocase of the outer membrane. Dev. Cell 7, 61-71.
35. Meisinger, C., Ryan, M. T., Hill, K., Model, K., Lim, J. H., Sickmann, A., Müller, H., Meyer, H. E., Wagner, R., and Pfanner, N. (2001). Protein import channel of the outer mitochondrial membrane: a highly stable Tom40-Tom22 core structure differentially interacts with preproteins, small tom proteins, and import receptors. Mol. Cell. Biol. 21, 2337-2348.
36. Milenkovic, D., Kozjak, V., Wiedemann, N., Lohaus, C., Meyer, H. E., Guiard, B., Pfanner, N., and Meisinger, C. (2004). Sam35 of the mitochondrial protein sorting and assembly machinery is a peripheral outer membrane protein essential for cell viability. J. Biol. Chem. 279, 22781-22785.
37. Moczko, M., Bömer, U., Kübrich, M., Zufall, N., Hönlinger, A., and Pfanner, N. (1997). The intermembrane space domain of mitochondrial Tom22 functions as a trans binding site for preproteins with N-terminal targeting sequences. Mol. Cell. Biol. 17, 6574-6584.
38. Model, K., Meisinger, C., Prinz, T., Wiedemann, N., Truscott, K. N., Pfanner, N., and Ryan, M. T. (2001). Multistep assembly of the protein import channel of the mitochondrial outer membrane. Nat. Struct. Biol. 8, 361-370.
39. Nakai, M., Kinoshita, K., and Endo, T. (1995). Mitochondrial receptor complex protein. The intermembrane space domain of yeast Masl7 is not essential for its targeting or function. J. Biol. Chem. 270, 30571-30575.
40. Nargang, F. E., Künkele, K.-P., Mayer, A., Ritzel, R. G., Neupert, W., and Lill, R. (1995). "Sheltered disruption" of Neurospora crassa MOM22, an essential component of the mitochondrial protein import complex. EMBO J. 14, 1099-1108.
41. Paschen, S., and Neupert, W. (2001). Protein import into mitochondria. Life 52, 101-112.
42. Paschen, S. A., Waizenegger, T., Stan, T., Preuss, M., Cyrklaff, M., Hell, K., Rapaport, D., and Neupert, W. (2003). Evolutionary conservation of biogenesis of β-barrel membrane proteins. Nature 426, 862-866.
43. Pfanner, N., and Wiedemann, N. (2002). Mitochondrial protein import: two membranes, three translocases. Curr. Opin. Cell Biol. 14, 400-411.
44. Rapaport, D. (2002). Biogenesis of the mitochondrial TOM complex. Trends Biochem. Sci. 27, 191-197.
45. Rapaport, D., Kunkele, K. P., Dembowski, M., Ahring, U., Nargang, F. E., Neupert, W., and Lill, R. (1998a). Dynamics of the TOM complex of mitochondria during binding and translocation of preproteins. Mol. Cell. Biol. 18, 5256-5262.
46. Rapaport, D., Mayer, A., Neupert, W., and Lill, R. (1998b). Cis and trans sites of the TOM complex of mitochondria in unfolding and initial translocation of preproteins. J. Biol. Chem. 273, 8806-8813.
47. Rapaport, D., Neupert, W., and Lill, R. (1997). Mitochondrial protein import: Tom40 plays a major role in targeting and translocarion of preproteins by forming a specific binding site for the presequence. J. Biol. Chem. 272, 18725-18731.
48. Sambrook, J., and Rusell, D. W. (2001). Molecular Cloning. A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
49. Schägger, H., Cramer, W. A., and von Jagow, G. (1994). Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal. Biochem. 217, 220-230.
50. Schägger, H., and von Jagow, G. (1991). Blue native electrophoresis for isolation of membrane complexes in enzymatically active form. Anal. Biochem. 199, 223-231.
51. Schmitt, S., Ahring, U., Eichacker, L., Granvogl, B., Go, N. E., Nargang, F. E., Neupert, W., and Nussberger, S. (2005). Role of Tom5 in maintaining the structural stability of the TOM complex of mitochondria. J. Biol. Chem. 280, 14499-14506.
52. Selker, E. U. (1990). Premeiotic instability of repeated sequences in Neurospora crassa. Annu. Rev. Genet. 24, 579-613.
53. Staben, C., Jensen, B., Singer, M., Pollock, J., and Schechtman, M. (1989). Use of bacterial hygromycin B resistance gene as a dominant selectable marker in Neurospora crassa transformation. Fungal Genet. Newsl. 36, 79-81.
54. Tanton, L. L., Nargang, C. E., Kessler, K. E., Li, Q., and Nargang, F. E. (2003). Alternative oxidase expression in Neurospora crassa. Fungal Genet. Biol. 39, 176-190.
55. Taylor, R., McHale, B., and Nargang, F. E. (2003). Characterization of Neurospora crassa Tom40-deficient mutants and effect of specific mutations on Tom40 assembly. J. Biol. Chem. 278, 765-775.
56. van Wilpe, S. et al. (1999). Tom22 is a multifunctional organizer of the mitochondrial preprotein translocase. Nature 401, 485-489.
57. Waizenegger, T., Habib, S. J., Lech, M., Mokranjac, D., Paschen, S. A., Hell, K., Neupert, W., and Rapaport, D. (2004). Tob38, a novel essential component in the biogenesis of β-barrel proteins of mitochondria. EMBO Rep. 5, 704-709.
58. Waizenegger, T., Schmitt, S., Zivkovic, J., Neupert, W., and Rapaport, D. (2005). Mim1, a protein required for the assembly of the TOM complex of mitochondria. EMBO Rep. 6, 57-62.
59. Wendland, J., Lengeler, K., and Kothe, E. (1996). An instant preparation method for nucleic acids of filamentous fungi. Fungal Genet. Newslett. 43, 54-55.
60. Wiedemann, N., Kozjak, V., Chacinska, A., Schönfisch, B., Rospert, S., Ryan, M. T., Pfanner, N., and Meisinger, C. (2003). Machinery for protein sorting and assembly in the mitochondrial outer membrane. Nature 424, 565-571.