Proteomic analysis of the yeast mitochondrial outer membrane reveals accumulation of a subclass of preproteins

Molecular Biology of the Cell

Volumn 17, Issue 3, 2006, Pages 1436-1450

  Zahedi, Rene P ^a   Sickmann, Albert ^a   Boehm, Andreas M ^a   Winkler, Christiane ^a   Zufall, Nicole ^b   Schönfisch, Birgit ^b   Guiard, Bernard ^c   Pfanner, Nikolaus ^b   Meisinger, Chris ^b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MESSENGER RNA; PROTEIN HFD1; PROTEIN PRECURSOR; PROTEIN YMR110C; PROTEOME; SCLEROPROTEIN; UNCLASSIFIED DRUG;

ARTICLE; EUKARYOTE; GENE TARGETING; GENOME ANALYSIS; MITOCHONDRIAL MEMBRANE; MODEL; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SJOEGREN LARSSON SYNDROME; YEAST;

EUKARYOTA; PROKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 33644912080     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-08-0740     Document Type: Article

References (87)

1. Alconada, A., Gärtner, F., Hönlinger, A., Kübrich, M., and Pfanner, N. (1995). Mitochondrial receptor complex from Neurospora crassa and Saccharomyces cerevisiae. Methods Enzymol. 260, 263-286.
2. Alto, N. M., Soderling, J., and Scott, J. D. (2002). Rab32 is an A-kinase anchoring protein and participates in mitochondrial dynamics. J. Cell Biol. 158, 659-668.
3. Athenstaedt, K., Zweytick, D., Jandrositz, A., Kohlwein, S. D., and Daum, G. (1999). Identification and characterization of major lipid particle proteins of the yeast Saccharomyces cerevisiae. J. Bacteriol. 181, 6441-6448.
4. Chacinska, A., Pfannschmidt, S., Wiedemańn, N., Kozjak, V., Sanjuán 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.
5. Cherry, J. M., et al. (1997). Genetic and physical maps of Saccharomyces cerevisiae. Nature 387, 67-73.
6. Da Cruz, S., Xenarios, I., Langridge, J., Vilbois, F., Parone, P. A., and Martinou, J. C. (2003). Proteomic analysis of the mouse liver mitochondrial inner membrane. J. Biol. Chem. 278, 41566-41571.
7. 2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J. Biol. Chem. 257, 13028-13033.
8. De Laurenzi, V., Rogers, G. R., Hamrock, D. J., Marekov, L. N., Steinert, P. M., Compton, J. G., Markova, N., and Rizzo, W. B. (1996). Sjögren-Larsson syndrome is caused by mutations in the fatty aldehyde dehydrogenase gene. Nat. Genet. 12, 52-57.
9. Dekker, P. J., Martin, F., Maarse, A. C., Bömer, U., Müller, H., Guiard, B., Meijer, M., Rassow, J., and Pfanner, N. (1997). The Tim core complex defines the number of mitochondrial contact sites and can hold arrested preproteins in the absence of matrix Hsp70-Tim44. EMBO J. 16, 5408-5419.
10. 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.
11. Frederick, R. L., McCaffery, J. M., Cunningham, K. W., Okamoto, K., and Shaw, J. M. (2004). Yeast Miro GTPase, Gem1, regulates mitochondrial morphology via a novel pathway. J. Cell Biol. 167, 87-98.
12. Fünfschilling, U., and Rospert, S. (1999). Nascent polypeptide-associated complex stimulates protein import into yeast mitochondria. Mol. Biol. Cell 10, 3289-3299.
13. 2 promotes early divergence from the general mitochondrial import pathway and restricts the unfoldase activity of matrix Hsp70. EMBO J. 14, 6043-6057.
14. George, R., Walsh, P., Beddoe, T., and Lithgow, T. (2002). The nascent polypeptide-associated complex (NAC) promotes interaction of ribosomes with the mitochondrial surface in vivo. FEBS Lett. 526, 213-216.
15. Ghaemmaghami, S., Huh, W. K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K., and Weissman, J. S. (2003). Global analysis of protein expression in yeast. Nature 425, 737-741.
16. 2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism. Cell 69, 809-822.
17. Green, D. R., and Kroemer, G. (2004). The pathophysiology of mitochondrial cell death. Science 305, 626-629.
18. Guda, C., Guda, P., Fahy, E., and Subramaniam, S. (2004). MITOPRED: a Web server for the prediction of mitochondrial proteins. Nucleic Acids Res. 32, W372-W374.
19. 5 reductase to two different submitochondrial compartments. Cell 79, 829-839.
20. Hartl, F. U., Ostermann, J., Guiard, B., and Neupert, W. (1987). Successive translocation into and out of the mitochondrial matrix: targeting of proteins to the intermembrane space by a bipartite signal peptide. Cell 51, 1027-1037.
21. 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.
22. Hodges, P. E., Carrico, P. M., Hogan, J. D., O'Neil, K. E., Owen, J. J., Mangan, M., Davis, B. P., Brooks, J. E., and Garrels, J. L. (2002). Annotating the human proteome: the human proteome survey database (humanPSD) and an indepth target database for G-protein-coupled receptors (GPCR-PD) from Incyte Genomics. Nucleic Acids Res. 30, 137-141.
23. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S., and O'Shea, E. K. (2003). Global analysis of protein localization in budding yeast. Nature 425, 686-691.
24. Jan, Y., Matter, M., Pai, J., Chen, Y., Pilch, J., Komatsu, M., Ong, E., Fukuda, M., and Ruoshlari, E. (2004). A mitochondrial protein, Bit1, mediates apoptosis regulated by integrins and Groucho/TLE corepressors. Cell 116, 751-762.
25. Jensen, R. E., and Dunn, C. D. (2002). Protein import into and across the mitochondrial inner membrane: role of the TIM23 and TIM22 translocons. Biochim. Biophys. Acta 2592, 25-34.
26. Jensen, R. E., Dunn, C. D., Youngman, M. J., and Sesaki, H. (2004). Mitochondrial building blocks. Trends Cell Biol. 14, 215-218.
27. Jeffery, C. J. (2005). Mass spectrometry and the search for moonlighting proteins. Mass Spectrom. Rev. 24, 772-782.
28. Karlberg, E. O., and Andersson, S. G. (2003). Mitochondrial gene history and mRNA localization: is there a correlation? Nat. Rev. Genet. 4, 391-397.
29. Karlberg, O., Canback, B., Kurland, C. G., and Andersson, S. G. (2000). The dual origin of the yeast mitochondrial proteome. Yeast 17, 170-187.
30. Karniely, S., and Pines, O. (2005). Single translation -dual destination: mechanisms of dual protein targeting in eukaryotes. EMBO Rep. 6, 420-425.
31. 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.
32. Kelson, T. L., Secor McVoy, J. R., and Rizzo, W. B. (1997). Human liver fatty aldehyde dehydrogenase: microsomal localization, purification, and biochemical characterization. Biochim. Biophys. Acta 1335, 99-110.
33. Kinner, A., and Kölling, R. (2003). The yeast deubiquinating enzyme Ubpl6 is anchored to the outer mitochondrial membrane. FEBS Lett. 549, 135-140.
34. Knox, C., Sass, E., Neupert, W., and Pines, O. (1998). Import into mitochondria, folding and retrograde movement of fumarase in yeast. J. Biol. Chem. 273, 25587-25593.
35. Koehler, C. M. (2004). New developments in mitochondrial assembly. Annu. Rev. Cell Dev. Biol. 20, 309-335.
36. Kumar, A., et al. (2002). Subcellular localization of the yeast proteome. Genes Dev. 16, 707-719.
37. Leber, R., Landl, K., Zinser, E., Ahorn, H., Spok, A., Kohlwein, S. D., Turnowsky, F., and Daum, G. (1998). Dual localization of squalene epoxidase, Erg1p, in yeast reflects a relationship between the endoplasmic reticulum and lipid particles. Mol. Biol. Cell 9, 375-386.
38. Lill, R., and Mühlenhoff, U. (2005). Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem. Sci. 30, 133-141.
39. Marcotte, E. M., Xenarios, I., van Der Bliek, A. M., and Eisenberg, D. (2000). Localizing proteins in the cell from their phylogenetic profiles. Proc. Natl. Acad. Sci. USA 97, 12115-12120.
40. Marc, P., Margeot, A., Devaux, F., Blugeon, C., Corral-Debrinski, M., and Jacq, C. (2002). Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Rep. 3, 159-164.
41. Margeot, A., Blugeon, C., Sylvestre, J., Vialette, S., Jacq, C., and Corral-Debrinski, M. (2002). In Saccharomyces cerevisiae, ATP2 mRNA sorting to the vicinity of mitochondria is essential for respiratory function. EMBO J. 21, 6893-6904.
42. Margeot, A., Garcia, M., Wang, W., Tetaud, E., di Rago, J. P., and Jacq, C. (2005). Why are so many mRNAs translated to the vicinity of mitochondria: a role in protein complex assembly? Gene 354, 64-71.
43. McCammon, M. T., Hartmann, M. A., Bottema, C. D., and Parks, L. W. (1984). Sterol methylation in Saccharomyces cerevisiae. J. Bacteriol. 157, 475-483.
44. 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.
45. Meisinger, C., Sommer, T., and Pfanner, N. (2000). Purification of Saccharomyces cerevisiae mitochondria devoid of microsomal and cytosolic contaminations. Anal. Biochem. 287, 339-342.
46. Mihara, K. (2003). Cell biology: moving inside membranes. Nature 424, 505-506.
47. Mitulovic, G., et al. (2003). An improved method for tracking and reducing the void volume in nano HPLC-MS with micro trapping columns. Anal. Bioanal. Chem. 376, 946-951.
48. Mitulovic, G., et al. (2004). Automated, on-line two-dimensional nano liquid chromatography tandem mass spectrometry for rapid analysis of complex protein digests. Proteomics 4, 2545-2557.
49. Miyauchi, K., Yamamoto, A., Masaki, R., Fujiki, Y., and Tashiro, Y. (1993). Microsomal aldehyde dehydrogenase or its cross-reacting protein exists in outer mitochondrial membranes and peroxisomal membranes in rat liver. Cell Struct. Funct. 18, 427-436.
50. Mootha, V. K., et al. (2003). Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115, 629-640.
51. Mueller, J. C., Andreoli, C., Prokisch, H., and Meitinger, T. (2004). Mechanisms for multiple intracellular localization of human mitochondrial proteins. Mitochondrion 3, 315-325.
52. Nakai, K., and Horton, P. (1999). PSORT: a program for detecting the sorting signals of proteins and predicting their subcellular localization Trends Biochem. Sci. 24, 34-35.
53. Naoé, M., Ohwa, Y., Ishikawa, D., Ohshima, C., Nishikawa, S., Yamamoto, H., and Endo, T. (2004). Identification of Tim40 that mediates protein sorting to the mitochondrial intermembrane space. J. Biol. Chem. 279, 47815-47821.
54. Neupert, W. (1997). Protein import into mitochondria. Annu. Rev. Biochem. 66, 863-917.
55. Newmeyer, D. D., and Ferguson-Miller, S. (2003). Mitochondria: releasing power for life and unleashing the machine of death. Cell 212, 481-490.
56. Ohlmeier, S., Kastaniotis, A. J., Hiltunen, J. K., and Bergmann, U. (2004). The yeast mitochondrial proteome, a study of fermentative and respiratory growth. J. Biol. Chem. 279, 3956-3979.
57. Pauli, D., Tonka, C. H., and Ayme-Southgate, A. (1988). An unusual split Drosophila heat shock gene expressed during embryogenesis, pupation and in testis. J. Mol. Biol. 200, 47-53.
58. Pfanner, N., Wiedemann, N., Meisinger, C., and Lithgow, T. (2004). Assembling the mitochondrial outer membrane. Nat. Struct. Mol. Biol. 11, 1044-1048.
59. Prokisch, H., et al. (2004). Integrative analysis of the mitochondrial proteome in yeast. PLoS Biol. 2, e160
60. Reichert, A. S., and Neupert, W. (2004). Mitochondriomics or what makes us breathe. Trends Genet. 20, 555-562.
61. Rizzo, W. B., Lin, Z., and Camey, G. (2001). Fatty aldehyde dehydrogenase: genomic structure, expression and mutation analysis in Sjögren-Larsson syndrome. Chem. Biol. Interact. 130-132, 297-307.
62. Schapira, A. H. (2000). Mitochondrial disorders. Curr. Opin. Neurol. 13, 527-532.
63. Scheffler, I. E. (1999). Mitochondria, New York: Wiley.
64. Schon, E. A. (2000). Mitochondrial genetics and disease. Trends Biochem. Sci. 25, 555-560.
65. 2 into the mitochondrial intermembrane space: specific recognition of the sorting signal. EMBO J. 12, 2295-2302.
66. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
67. Sickmann, A., et al. (2003). The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. USA 100, 13207-13212.
68. Sikorski, R. S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
69. Skoog, B., and Wichmann, A. (1986). Calculation of the isoelectric points of poly-peptides from the amino acid composition. Trends Analyt. Chem. 5, 82-83.
70. Small, I., Peeters, N., Legeai, F., and Lurin, C. (2004). Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4, 1581-1590.
71. Steinmetz, L. M., et al. (2002). Systematic screen for human disease genes in yeast. Nat. Genet. 31, 400-404.
72. Sylvestre, J., Margeot, A., Jacq, C., Dujardin, G., and Corral-Debrinski, M. (2003). The role of the 3′ untranslated region in mRNA sorting to the vicinity of mitochondria is conserved from yeast to human cells. Mol. Biol. Cell 14, 3848-3856.
73. Takano, A., Endo, T., and Yoshihisa, T. (2005). tRNA actively shuttles between the nucleus and cytosol in yeast. Science 309, 140-142.
74. Taylor, S. W., et al. (2003). Characterization of the human heart mitochondrial proteome. Nat. Biotechnol. 21, 281-286.
75. Terziyska, N., Lutz, T., Kozany, C., Mokranjac, D., Mesecke, N., Neupert, W., Herrmann, J. M., and Hell, K. (2005). Mia40, a novel factor for protein import into the intermembrane space of mitochondria is able to bind metal ions. FEBS Lett. 579, 179-184.
76. Truscott, K. N., Brandner, K., and Pfanner, N. (2003). Mechanisms of protein import into mitochondria. Curr. Biol. 13, R326-R337.
77. Tusnady, G. E., and Simon, I. (2001). The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849-850.
78. van Wilpe, S., et al. (1999). Tom22 is a multifunctional organizer of the mitochondrial preprotein translocase. Nature 401, 485-489.
79. Verner, K. (1993). Co-translational protein import into mitochondria: an alternative view. Trends Biochem. Sci. 18, 366-371.
80. Wagner, Y., Sickmann, A., Meyer, H. E., and Daum, G. (2003). Multidimensional nano-HPLC for analysis of protein complexes. J. Am. Soc. Mass. Spectrom. 14, 1003-1011.
81. Wallace, D. C. (2005). A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 39, 359-407.
82. Washburn, M. P., Wolters, D., and Yates, J. R. (2001). Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19, 242-247.
83. 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.
84. Wiedemann, N., Pfanner, N., and Rehling, P. (2005). Import of precursor proteins into isolated yeast mitochondria. Methods Mol. Biol. 313, 373-383.
85. Wu, M., Xu, L.G., Li, X., Zhai, Z., and Shu, H. B. (2002). AMID, an apoptosis-indudng factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis. J. Biol. Chem. 277, 25617-25623.
86. Yoshihisa, T., Yunoki-Esaki, K., Ohshima, C., Tanaka, N., and Endo, T. (2003). Possibility of cytoplasmic pre-tRNA splicing: the yeast tRNA splicing endonuclease mainly localizes on the mitochondria. Mol. Biol. Cell 14, 3266-3279.
87. Zahedi, R. P., Meisinger, C., and Sickmann, A. (2005). Two-dimensional benzyldimethyl-n-hexadecylammonium chloride/SDS-PAGE for membrane proteomics. Proteomics 5, 3581-3588.