Nascent polypeptide-associated complex stimulates protein import into yeast mitochondria

Molecular Biology of the Cell

Volumn 10, Issue 10, 1999, Pages 3289-3299

  Fünfschilling, Ursula ^a,b   Rospert, Sabine ^a,b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b MAX PLANCK RESEARCH UNIT FOR ENZYMOLOGY OF PROTEIN FOLDING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TRANSPORT; YEAST;

EID: 0343330935     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.10.3289     Document Type: Article

References (62)

1. Ades, I.Z., and Butow, R.A. (1980). The products of mitochondria-bound cytoplasmic polysomes in yeast. J. Biol. Chem. 255, 9918-9924.
2. Bolliger, L., Junne, T., Schatz, G., and Lithgow, T. (1995). Acidic receptor domains on both sides of the outer membrane mediate translocation of precursor proteins into yeast mitochondria. EMBO J. 14, 6318-6326.
3. Branda, S.S., and Isaya, G. (1995). Prediction and identification of new natural substrates of the yeast mitochondrial intermediate peptidase. J. Biol. Chem. 270, 27366-27373.
4. Brix, J., Rüdiger, S., Bukau, B., Schneider-Mergener, J., and Pfanner, N. (1999). Distribution of binding sequences for the mitochondrial import receptors Tom20, Tom22, and Tom70 in a presequence-carrying preprotein and a noncleavable preprotein. J. Biol. Chem. 274, 16522-16530.
5. Caplan, A.J., Cyr, D.M., and Douglas, M.G. (1992). YDJ1p facilitates polypeptide translocation across different intracellular membranes by a conserved mechanism. Cell 71, 1143-1155.
6. Cartwright, P., Beilharz, T., Hansen, P., Garrett, J., and Lithgow, T. (1997). Mft52, an acid-bristle protein in the cytosol that delivers precursor proteins to yeast mitochondria. J. Biol. Chem. 272, 5320-5325.
7. 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.
8. Deshaies, R.J., Koch, B.D., Werner-Washburne, M., Craig, E.A., and Schekman, R. (1988). A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature 332, 800-805.
9. Dietmeier, K., Hönlinger, A., Bömer, U., Dekker, P.J., Eckerskorn, C., Lottspeich, F., Kubrich, M., and Pfanner, N. (1997). Tom5 functionally links mitochondrial preprotein receptors to the general import pore [see comments]. Nature 388, 195-200.
10. Dubaquié, Y., Looser, R., Fünfschilling, U., Jenö, P., and Rospert, S. (1998). Identification of in vivo substrates of the yeast mitochondrial chaperonins reveals overlapping but nonidentical requirement for hsp60 and hsp10. EMBO J. 17, 5868-5876.
11. Fujiki, M., and Verner, K. (1993). Coupling of cytosolic protein synthesis and mitochondrial protein import in yeast. Evidence for cotranslational import in vivo. J. Biol. Chem. 268, 1914-1920.
12. Garcia, P.D., Hansen, W., and Walter, P. (1991). In vitro protein translocation across microsomal membranes of Saccharomyces cerevisiae. Methods Enzymol. 194, 675-682.
13. George, R., Beddoe, T., Landl, K., and Lithgow, T. (1998). The yeast nascent polypeptide-associated complex initiates protein targeting to mitochondria in vivo. Proc. Natl. Acad. Sci. USA 95, 2296-2301.
14. Gilmore, R., Collins, P., Johnson, J., Kellaris, K., and Rapiejko, P. (1991). Transcription of full-length and truncated mRNA transcripts to study protein translocation across the endoplasmic reticulum. Methods Cell Biol. 34, 223-239.
15. Glick, B.S., and Pon, L.A. (1995). Isolation of highly purified mitochondria from Saccharomyces cerevisiae. Methods Enzymol. 260, 213-223.
16. Haucke, V., Lithgow, T., Rospert, S., Hahne, K., and Schatz, G. (1995). The yeast mitochondrial protein import receptor Mas20p binds precursor proteins through electrostatic interaction with the positively charged presequence. J. Biol. Chem. 270, 5565-5570.
17. Heinemeyer, W., Kleinschmidt, J.A., Saidowsky, J., Escher, C., and Wolf, D.H. (1991). Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J. 10, 555-562.
18. Hill, K., Model, K., Ryan, M.T., 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.
19. Hines, V., and Schatz, G. (1993). Precursor binding to yeast mitochondria. A general role for the outer membrane protein Mas70p. J. Biol. Chem. 268, 449-454.
20. Kanamori, T., Nishikawa, S., Shin, I., Schultz, P.G., and Endo, T. (1997). Probing the environment along the protein import pathways in yeast mitochondria by site-specific photocrosslinking. Proc. Natl. Acad. Sci. USA 94, 485-490.
21. Kellems, R.E., Allison, V.F., and Butow, R.A. (1974). Cytoplasmic type 80 S ribosomes associated with yeast mitochondria. II. Evidence for the association of cytoplasmic ribosomes with the outer mitochondrial membrane in situ. J. Biol. Chem. 249, 3297-3303.
22. Kellems, R.E., Allison, V.F., and Butow, R.A. (1975). Cytoplasmic type 80S ribosomes associated with yeast mitochondria. IV. Attachment of ribosomes to the outer membrane of isolated mitochondria. J. Cell Biol. 65, 1-14.
23. Komiya, T., Rospert, S., Koehler, C., Looser, R., Schatz, G., and Mihara, K. (1998). Interaction of mitochondrial targeting signals with acidic receptor domains along the protein import pathway: evidence for the "acid chain" hypothesis. EMBO J. 17, 3886-3898.
24. Komiya, T., Sakaguchi, M., and Mihara, K. (1996). Cytoplasmic chaperones determine the targeting pathway of precursor proteins to mitochondria. EMBO J. 15, 399-407.
25. Künkele, K.P., Heins, S., Dembowski, M., Nargang, F.E., Benz, R., Thieffry, M., Walz, J., Lill, R., Nussberger, S., and Neupert, W. (1998). The preprotein translocation channel of the outer membrane of mitochondria. Cell 93, 1009-1019.
26. Lauring, B., Kreibich, G., and Weidmann, M. (1995a). The intrinsic ability of ribosomes to bind to endoplasmic reticulum membranes is regulated by signal recognition particle and nascent-polypeptide-associated complex [see comments]. Proc. Natl Acad. Sci. USA 92, 9435-9439.
27. Lauring, B., Sakai, H., Kreibich, G., and Wiedmann, M. (1995b). Nascent polypeptide-associated complex protein prevents mistar-geting of nascent chains to the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 92, 5411-5415 (erratum 92, 8088).
28. Lill, R., and Neupert, W. (1996). Mechanisms of protein import across the mitochondrial outer membrane. Trends Cell Biol. 6, 56-61.
29. Lithgow, T., Glick, B.S., and Schatz, G. (1995). The protein import receptor of mitochondria. Trends Biochem. Sci. 20, 98-101.
30. Lithgow, T., Junne, T., Suda, K., Gratzer, S., and Schatz, G. (1994a). The mitochondrial outer membrane protein Mas22p is essential for protein import and viability of yeast. Proc. Natl. Acad. Sci. USA 91, 11973-11981.
31. Lithgow, T., Junne, T., Wachter, C., and Schatz, G. (1994b). Yeast mitochondria lacking the two import receptors Mas20p and Mas70p can efficiently and specifically import precursor proteins. J. Biol. Chem. 269, 15325-15330.
32. Luciano, P., Tokatlidis, K., Chambre, I., Germanique, J.C., and Geli, V. (1998). The mitochondrial processing peptidase behaves as a zinc-metallopeptidase. J. Mol. Biol. 280, 193-199.
33. Moczko, M., Ehmann, B., Gartner, F., Honlinger, A., Schafer, E., and Pfanner, N. (1994). Deletion of the receptor MOM19 strongly impairs import of cleavable preproteins into Saccharomyces cerevisiae mitochondria. J. Biol. Chem. 269, 9045-9051.
34. Möller, I., Jung, M., Beatrix, B., Levy, R., Kreibich, G., Zimmermann, R., Wiedmann, M., and Lauring, B. (1998). A general mechanism for regulation of access to the translocon: competition for a membrane attachment site on ribosomes. Proc. Natl. Acad. Sci. USA 95, 13425-13430.
35. Moreau, A., Yotov, W.V., Glorieux, F.H., and St-Arnaud, R. (1998). Bone-specific expression of the alpha chain of the nascent polypeptide-associated complex, a coactivator potentiating c-Jun-mediated transcription. Mol. Cell. Biol. 18, 1312-1321.
36. Mueckler, M., and Lodish, H.F. (1986). The human glucose transporter can insert posttranslationally into microsomes. Cell 44, 629-637.
37. Murakami, K., and Mori, M. (1990). Purified presequence binding factor (PBF) forms an import-competent complex with a purified mitochondrial precursor protein. EMBO J. 9, 3201-3208.
38. Neuhof, A., Rolls, M.M., Jungnickel, B., Kalies, K.U., and Rapoport, T.A. (1998). Binding of signal recognition particle gives ribosome/ nascent chain complexes a competitive advantage in endoplasmic reticulum membrane interaction. Mol. Biol. Cell 9, 103-115.
39. Nobumoto, M., Yamada, M., Song, S., Inouye, S., and Nakazawa, A. (1998). Mechanism of mitochondrial import of adenylate kinase isozymes. J. Biochem. 123, 128-135.
40. Ono, H., and Tuboi, S. (1990). Purification and identification of a cytosolic factor required for import of precursors of mitochondrial proteins into mitochondria. Arch. Biochem. Biophys. 280, 299-304.
41. Parthun, M.R., Mangus, D.A., and Jaehning, J.A. (1992). The EGD1 product, a yeast homolog of human BTF3, may be involved in GAL4 DNA binding. Mol. Cell. Biol. 12, 5683-5689.
42. Pfanner, N., Craig, E.A., and Hönlinger, A. (1997). Mitochondrial preprotein translocase. Annu. Rev. Cell. Dev. Biol. 13, 25-51.
43. Powers, T., and Walter, P. (1996). The nascent polypeptide-associated complex modulates interactions between the signal recognition particle and the ribosome. Curr. Biol. 6, 331-338.
44. Raden, D., and Gilmore, R. (1998). Signal recognition particle-dependent targeting of ribosomes to the rough endoplasmic reticulum in the absence and presence of the nascent polypeptide-associated complex. Mol. Biol. Cell 9, 117-130.
45. Rapaport, D., Neupert, W., and Lill, R. (1997). Mitochondrial protein import. Tom40 plays a major role in targeting and translocation of preproteins by forming a specific binding site for the presequence. J. Biol. Chem. 272, 18725-18731.
46. Reid, G.A., and Schatz, G. (1982). Import of proteins into mitochondria. Yeast cells grown in the presence of carbonyl cyanide m-chlorophenylhydrazone accumulate massive amounts of some mitochondrial precursor polypeptides. J. Biol. Chem. 257, 13056-13061.
47. Reimann, B., Bradsher, J., Franke, J., Hartmann, E., Wiedmann, M., Prehn, S., and Wiedmann, B. (1999). Initial characterization of the nascent polypeptide-associated complex in yeast. Yeast 15, 397-407.
48. Roise, D., Horvath, S.J., Tomich, J.M., Richards, J.H., and Schatz, G. (1986). A chemically synthesized presequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers. EMBO J. 5, 1327-1334.
49. Rospert, S., and Schatz, G. (1998). Protein translocation into mitochondria. In: Cell Biology, a Laboratory Handbook, vol. 2, ed. J.E. Celis, San Diego: Academic Press, 277-285.
50. Schatz, G. (1997). Just follow the acid chain [news; comment]. Nature 388, 121-122.
51. Schneider, E., Lochmann, E.R., and Lother, H. (1976). Distribution of membrane-bound and free ribosomes in growing yeast. Biochim. Biophys. Acta 432, 92-97.
52. Schulke, N., Sepuri, N.B., and Pain, D. (1997). In vivo zippering of inner and outer mitochondrial membranes by a stable translocation intermediate. Proc. Natl. Acad. Sci. USA 94, 7314-7319.
53. Shi, X., Parthun, M.R., and Jaehning, J.A. (1995). The yeast EGD2 gene encodes a homologue of the alpha NAC subunit of the human nascent-polypeptide-associated complex. Gene 165, 199-202.
54. Shimokata, K., Nishio, T., Song, M.C., Kitada, S., Ogishima, T., and Ito, A. (1997). Substrate recognition by mitochondrial processing peptidase toward the malate dehydrogenase precursor. J. Biochem. 122, 1019-1023.
55. Stein, I., Peleg, Y., Even-Ram, S., and Pines, O. (1994). The single translation product of the FUM1 gene (fumarase) is processed in mitochondria before being distributed between the cytosol and mitochondria in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 4770-4778.
56. von Heijne, G. (1986). Mitochondrial targeting sequences may form amphiphilic helices. EMBO J. 5, 1335-1342.
57. Wachter, C., Schatz, G., and Glick, B.S. (1994). Protein import into mitochondria: the requirement for external ATP is precursor-specific whereas intramitochondrial ATP is universally needed for translocation into the matrix. Mol. Biol. Cell 5, 465-474.
58. Wang, S., Sakai, H., and Wiedmann, M. (1995). NAC covers ribosome-associated nascent chains thereby forming a protective environment for regions of nascent chains just emerging from the peptidyl transferase center. J. Cell Biol. 130, 519-528.
59. Wiedmann, B., Sakai, H., Davis, T.A., and Wiedmann, M. (1994). A protein complex required for signal-sequence-specific sorting and translocation. Nature 370, 434-440.
60. Wienhues, U., Becker, K., Schleyer, M., Guiard, B., Tropschug, M., Horwich, A.L., Pfanner, N., and Neupert, W. (1991). Protein folding causes an arrest of preprotein translocation into mitochondria in vivo. J. Cell Biol. 115, 1601-1609.
61. Yotov, W.V., Moreau, A., and St-Arnaud, R. (1998). The alpha chain of the nascent polypeptide-associated complex functions as a transcriptional coactivator. Mol. Cell. Biol. 18, 1303-1311.
62. Zheng, X.M., Black, D., Chambon, P., and Egly, J.M. (1990). Sequencing and expression of complementary DNA for the general transcription factor BTF3. Nature 344, 556-559.