Mitochondrial outer membrane proteome of trypanosoma brucei reveals novel factors required to maintain mitochondrial morphology

Molecular and Cellular Proteomics

Volumn 12, Issue 2, 2013, Pages 515-528

  Niemann, Moritz ^a   Wiese, Sebastian ^b   Mani, Jan ^a   Chanfon, Astrid ^a   Jackson, Christopher ^a   Meisinger, Chris ^a,b   Warscheid, Bettina ^b   Schneider, Andre ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; HEAT SHOCK PROTEIN 70; LONG CHAIN FATTY ACID COENZYME A LIGASE; OUTER MEMBRANE PROTEIN; PROTEIN; PROTEINASE; PROTEOME; UBIQUITIN THIOLESTERASE;

ARTICLE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; TANDEM MASS SPECTROMETRY; TRYPANOSOMA BRUCEI; YEAST;

ANIMALS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; LIFE CYCLE STAGES; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; ORGANELLE SHAPE; PROTEOME; PROTOZOAN PROTEINS; RNA, SMALL INTERFERING; SACCHAROMYCES CEREVISIAE; TANDEM MASS SPECTROMETRY; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84874054463     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.023093     Document Type: Article

References (58)

1. Lüscher, A., Koning, H. P. d., and Maser, P. (2007) Chemotherapeutic strategies against Trypanosoma brucei: drug targets vs. drug targeting. Curr. Pharm. Des. 13, 555-567
2. Cavalier-Smith, T. (2010) Kingdoms Protozoa and Chromista and the eo- zoan root of the eukaryotic tree. Biol. Lett. 6, 342-345
3. Lukes, J., Hashimi, H., and Zíkova, A. (2005) Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr. Genet. 48, 277-299
4. Stuart, K. D., Schnaufer, A., Ernst, N. L, and Panigrahi, A. K. (2005) Complex management: RNA editing in trypanosomes. Trends Biochem. Sci. 30, 97-105
5. Schneider, A. (2011) Mitochondrial tRNA import and its consequences for mitochondrial translation. Ann. Rev. Biochem. 80, 1033-1053
6. Pusnik, M., Schmidt, O., Perry, A. J., Oeljeklaus, S., Niemann, M., Warsc- heid, B., Lithgow, T., Meisinger, C, and Schneider, A. (2011) Mitochondrial preprotein translocase of trypanosomatids has a bacterial origin. Curr. Biol. 21, 1738-1743
7. Zarsky, V., Tachezy, J., and Dolezal, P. (2012) Tom40 is likely common to all mitochondria. Curr. Biol. 22, R479-R481
8. Pusnik, M., Schmidt, O., Perry, A. J., Oeljeklaus, S., Niemann, M., Warsc- heid, B., Meisinger, C, Lithgow, T., and Schneider, A. (2012) Response to Zarsky et al. Curr. Biol. 22, R481-R482
9. Harsman, A., Niemann, M., Pusnik, M., Schmidt, O., Burmann, B. M., Hiller, S., Meisinger, C., Schneider, A., and Wagner, R. (2012) Bacterial origin of a mitochondrial outer membrane protein translocase: new perspectives from comparative single channel electrophysiology. J. Biol. Chem. 287, 31437-31445
10. Simpson, L., and Kretzer, F. (1997) The mitochondrion in dividing Leishma- nia tarentolae cells is symmetric and circular and becomes a single asymmetric tubule in non-dividing cells due to division of the kinetoplast portion. Mol. Biochem. Parasitol. 87, 71-78
11. Tyler, K. M., Matthews, K. R., and Gull, K. (1997) The bloodstream differ- entiation-division of Tryranosoma brucei studied using mitochondrial markers. Proc. R. Soc. Lond. 264, 1481-1490
12. Matthews, K. R. (2005) The developmental cell biology of Trypanosoma brucei. J. Cell Sci. 118, 283-290
13. Priest, J. W., and Hajduk, S. L. (1994) Developmental regulation of mito- chondrial biogenesis in Trypanosoma brucei. J. Bioenerget. Biomemb. 26, 179-191
14. Schneider, A. (2001) Unique aspects of mitochondrial biogenesis in trypanosomatids. Int. J. Parasitol. 31, 1403-1415
15. Besteiro, S., Barrett, M. P., Riviere, L., and Bringaud, F. (2005) Energy generation in insect stages of Trypanosoma brucei: metabolism in flux. Trends Parasitol. 21, 185-191
16. Panigrahi, A. K., Ogata, Y., Zíková, A., Anupama, A., Dalley, R. A., Acestor, N., Myler, P. J., and Stuart, K. D. (2009) A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics 9, 434-450
17. Acestor, N., Panigrahi, A. K., Ogata, Y., Anupama, A., and Stuart, K. D. (2009) Protein composition of Trypanosoma brucei mitochondrial membranes. Proteomics 9, 5497-5508
18. Acestor, N., Zíková, A., Dalley, R. A., Anupama, A., Panigrahi, A. K., and Stuart, K. D. (2011) Trypanosoma brucei mitochondrial respiratome: composition and organization in procyclic form. Mol. Cell. Proteomics 10, M110.006908
19. Zíková, A., Panigrahi, A. K., Dalley, R. A., Acestor, N., Anupama, A., Ogata, Y., Myler, P. J., and Stuart, K. (2008) Trypanosoma brucei mitochondrial ribosomes: affinity purification and component identification by mass spectrometry. Mol. Cell. Proteomics 7, 1286-1296
20. Schneider, A., Charrière, F., Pusnik, M., and Horn, E. K. (2007) Isolation of mitochondria from procyclic Trypanosoma brucei. Methods Mol. Biol. 372, 67-80
21. Pusnik, M., Charrière, F., Mä ser, P., Waller, R. F., Dagley, M. J., Lithgow, T., and Schneider, A. (2009) The single mitochondrial porin of Trypanosoma brucei is the main metabolite transporter in the outer mitochondrial membrane. Mol. Biol. Evol. 26, 671-680
22. Sharma, S., Singha, U. K., and Chaudhuri, M. (2010) Role of Tob55 on mitochondrial protein biogenesis in Trypanosoma brucei. Mol. Biochem. Parasitol. 174, 89-100
23. Pusnik, M., Mani, J., Schmid, O., Niemann, M., Oeljeklaus, S., Schnarwiler, F., Warscheid, B., Lithgow, T., Meisinger, C., and Schneider, A. (2012) An essential novel component of the non-canonical mitochondrial outer membrane protein import system of trypanosomatids. Mol. Biol. Cell 23, 3420-3428
24. Zahedi, R. P., Sickmann, A., Boehm, A. M., Winkler, C., Zufall, N., Schön- fisch, B., Guiard, B., Pfanner, N., and Meisinger, C. (2006) Proteomic analysis of the yeast mitochondrial outer membrane reveals accumulation of a subclass of preproteins. Mol. Biol. Cell 17, 1436-1450
25. Schmitt, S., Prokisch, H., Schlunck, T., Camp, D. G., Ahting, U., Waizeneg- ger, T., Scharfe, C., Meitinger, T., Imhof, A., Neupert, W., Oefner, P. J., and Rapaport, D. (2006) Proteome analysis of mitochondrial outer membrane from Neurospora crassa. Proteomics 6, 72-80
26. Duncan, O., Taylor, N. L., Carrie, C., Eubel, H., Kubiszewski-Jakubiak, S., Zhang, B., Narsai, R., Millar, A. H., and Whelan, J. (2011) Multiple lines of evidence localize signaling, morphology, and lipid biosynthesis machinery to the mitochondrial outer membrane of Arabidopsis. Plant Physiol. 157, 1093-1113
27. Alsford, S., Turner, D. J., Obado, S. O., Sanchez-Flores, A., Glover, L., Berriman, M., Hertz-Fowler, C., and Horn, D. (2011) High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res. 21, 915-924
28. Hauser, R., Pypaert, M., Hä usler, T., Horn, E. K., and Schneider, A. (1996) In vitro import of proteins into mitochondria of Trypanosoma brucei and Leishmania tarentolae. J. Cell Sci. 109, 517-523
29. Alconada, A., Gä rtner, F., Hönlinger, A., Kübrich, M., and Pfanner, N. (1995) Mitochondrial receptor complex from Neurospora crassa and Saccharomyces cerevisiae. Methods Enzymol. 260, 263-286
30. Mayer, A., Driessen, A., Neupert, W., and Lill, R. (1995) Purified and protein- loaded mitochondrial outer membrane vesicles for functional analysis of preprotein transport. Methods Enzymol. 260, 252-263
31. Wessel, D., and Fugge, U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143
32. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
33. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., and Mann, M. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805
34. Oberholzer, M., Morand, S., Kunz, S., and Seebeck, T. (2005) A vector series for rapid PCR-mediated C-terminal in situ tagging of Trypanosoma brucei genes. Mol. Biochem. Parasitol. 145, 117-120
35. Wirtz, E., Leal, S., Ochatt, C, and Cross, G. A. (1999) A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99, 89-101
36. Bochud-Allemann, N., and Schneider, A. (2002) Mitochondrial substrate level phosphorylation is essential for growth of procyclic Trypanosoma brucei. J. Biol. Chem. 277, 32849-32854
37. Sherwin, T., Schneider, A., Sasse, R., Seebeck, T., and Gull, K. (1987) Distinct localization and cell cycle dependence of COOH terminally tyrosinolated a-tubulin in the microtubules of Trypanosoma brucei brucei. J. Cell Biol. 104, 439-445
38. Smith, T. K., and Butikofer, P. (2010) Lipid metabolism in Trypanosoma brucei. Mol. Biochem. Parasitol. 172, 66-79
39. Parsons, D. F., Williams, G. R., and Chance, B. (1966) Characteristics of isolated and purified preparations of the outer and inner membranes of mitochondria. Ann. N.Y. Acad. Sci. 137, 643-666
40. Michel, A. H., and Kornmann, B. (2012) The ERMES complex and ER- mitochondria connections. Biochem. Soc. Trans. 40, 445-450
41. Andersen, J. S., Christopher, J., Wilkinson, J., Mayor, T., Mortensen, P., Nigg, E. A., and Mann, M. (2003) Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426, 570-574
42. Foster, L. J., Hoog, C. L. d., Zhang, Y., Zhang, Y., Xie, X., Moohta, V. K., and Mann, M. (2006) A mammalian organelle map by protein correlation profiling. Cell 125, 187-199
43. Wiese, S., Gronemeyer, T., Ofman, R., Kunze, M., Grou, C. P., Almeida, J. A., Eisenacher, M., Stephan, C, Hayen, H., Schollenberger, L., Korosec, T., Waterham, H. R., Schliebs, W., Erdmann, R., Berger, J., Meyer, H. E., Just, W., Azevedo, J. E., Wanders, R. J. A., and Warscheid, B. (2007) Proteomics characterization of mouse kidney peroxisomes by tandem mass spectrometry and protein correlation profiling. Mol. Cell. Proteomics 6, 2045-2057
44. Perocchi, F., Gohil, V. M., Girgis, H. S., Bao, X. R., McCombs, J. E., Palmer, A. E., and Mootha, V. K. (2010) MICU1 encodes a mitochondrial EF hand protein required for Ca2+ uptake. Nature 467, 291-296
45. Stefani, D. D., Raffaello, A., Teardo, E., Szabo, I., and Rizzuto, R. (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476, 336-340
46. Baughman, J. M., Perocchi, F., Girgis, H. S., Plovanich, M., Belcher-Timme, C. A., Sancak, Y., Bao, X. R., Strittmatter, L., Goldberger, O., Bogorad, R. L., Koteliansky, V., and Mootha, V. K. (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476, 341-345
47. Colasante, C, Diaz, P. P., Clayton, C, and Voncken, F. (2009) Mitochon- drial carrier family inventory of Trypanosoma brucei brucei: Identification, expression and subcellular localisation. Mol. Biochem. Parasitol. 167, 104-117
48. Dacks, J. B., Walker, G., and Field, M. C. (2008) Implications of the new eukaryotic systematics for parasitologists. Parasitol. Int. 57, 97-104
49. Flinner, N., Schleiff, E., and Mirus, O. (2012) Identification of two voltage- dependent anion channel-like protein sequences conserved in Kinetoplastida. Biol. Lett. 8, 446-449
50. Schmidt, O., Pfanner, N., and Meisinger, C. (2010) Mitochondrial protein import: from proteomics to functional mechanisms. Nat. Rev. Mol. Cell Biol. 11, 655-667
51. Westermann, B. (2010) Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol. 11, 872-884
52. Crausaz-Esseiva, A., Chanez, A.-L., Bochud-Allemann, N., Martinou, J. C, Hemphill, A., and Schneider, A. (2004) Temporal dissection of Baxinduced events leading to fission of the single mitochondrion in Trypanosoma brucei. EMBO Rep. 5, 268-273
53. Chanez, A.-L., Hehl, A., Engstler, M., and Schneider, A. (2006) Ablation of the single dynamin of T brucei blocks mitochondrial fission and endocytosis and leads to a precise cytokinesis arrest. J. Cell Sci. 119, 2968-2974
54. Morgan, G. W., Goulding, D., and Field, M. C. (2004) The single dynamin- like protein of Trypanosoma brucei regulates mitochondrial division and is not required for endocytosis. J. Biol. Chem. 279, 10692-10701
55. Vassella, E., Straesser, K., and Boshart, M. (1997) A mitochondrion-specific dye for multicolour fluorescent imaging of Trypanosoma brucei. Mol. Biochem. Parasitol. 90, 381-385
56. Cristodero, M., Seebeck, T., and Schneider, A. (2010) Mitochondrial trans- lation is essential in bloodstream forms of Trypanosoma brucei. Mol. Microbiol. 78, 757-769
57. Tschopp, F., Charriere, F., and Schneider, A. (2011) In vivo study in Tryp- anosoma brucei links mitochondrial transfer RNA import to mitochondrial protein import. EMBO Rep. 12, 825-832
58. Seidman, D., Johnson, D., Gerbasi, V., Golden, D., Orlando, R., and Hajduk, S. (2012) Mitochondrial membrane complex that contains proteins necessary for tRNA import in Trypanosoma brucei. J. Biol. Chem. 287, 8892-8903