Landscape of submitochondrial protein distribution

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Vögtle, F Nora ^a   Burkhart, Julia M ^b   Gonczarowska Jorge, Humberto ^b   Kücükköse, Cansu ^a,c   Taskin, Asli Aras ^a   Kopczynski, Dominik ^b   Ahrends, Robert ^b   Mossmann, Dirk ^a   Sickmann, Albert ^b,d,e   Zahedi, René P ^b   Meisinger, Chris ^a,c  

^a UNIVERSITY OF FREIBURG   (Germany)

^b LEIBNIZ INSTITUT FÜR ANALYTISCHE WISSENSCHAFTEN ISAS E V   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITY OF ABERDEEN   (United Kingdom)

^e RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; PROTEOME; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO ACID SEQUENCE; HUMAN; IMMUNOBLOTTING; INTRACELLULAR MEMBRANE; METABOLISM; PROCEDURES; PROTEOMICS; TANDEM MASS SPECTROMETRY;

AMINO ACID SEQUENCE; HUMANS; IMMUNOBLOTTING; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MITOCHONDRIAL PROTEINS; PROTEOME; PROTEOMICS; SACCHAROMYCES CEREVISIAE PROTEINS; TANDEM MASS SPECTROMETRY;

EID: 85027857002     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00359-0     Document Type: Article

References (58)

1. Pagliarini, D. J. et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123 (2008).
2. Taylor, S. W. et al. Characterization of the human heart mitochondrial proteome. Nat. Biotechnol. 21, 281-286 (2003).
3. Meisinger, C., Sickmann, A. & Pfanner, N. The mitochondrial proteome: from inventory to function. Cell 134, 22-24 (2008).
4. Calvo, S. E. & Mootha, V. K. The mitochondrial proteome and human disease. Annu. Rev. Genomics Hum. Genet. 11, 25-44 (2010).
5. Schmidt, O., Pfanner, N. & Meisinger, C. Mitochondrial protein import: from proteomics to functional mechanisms. Nat. Rev. Mol. Cell Biol. 11, 655-667 (2010).
6. Sickmann, A. et al. The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl Acad. Sci. USA 100, 13207-13212 (2003).
7. Reinders, J., Zahedi, R. P., Pfanner, N., Meisinger, C. & Sickmann, A. Towards the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics. J. Proteome Res. 5, 1543-1554 (2006).
8. Cherry, J. M. et al. Saccharomyces genome database: the genomics resourse of budding yeast. Nucleic Acids Res. 40, D700-D705 (2012).
9. The UniProt Consortium. UniProt: a hub for protein information. Nucleic Acids Res. 43, D204-D212 (2015).
10. Kumar, A. et al. Subcellular localization of the yeast proteome. Genes Dev. 16, 707-719 (2002).
11. De Hertogh, B. et al. Phylogenetic classification of tranporters and other membrane proteins from Saccharomyces cerevisiae. Funct. Integr. Genomics 2, 154-170 (2002).
12. Wasilewski, M., Chojnacka, K. & Chacinska, A. Protein trafficking at the crossroads to mitochondria. Biochim. Biophys. Acta 1864, 125-137 (2017).
13. Mick, D. U., Fox, T. D. & Rehling, P. Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation. Nat. Rev. Mol. Cell Biol. 12, 14-20 (2011).
14. Rhee, H. W. et al. Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging. Science 339, 1328-1331 (2013).
15. Hung, V. et al. Proteomic mapping of the human mitochondrial intermembrane space in live cells via ratiometric APEX tagging. Mol. Cell 55, 332-341 (2014).
16. Meisinger, C., Pfanner, C. & Truscott, K. N. Isolation of yeast mitochondria. Methods Mol. Biol. 313, 33-39 (2006).
17. Vögtle, F. N. et al. Intermembrane space proteome of yeast mitochondria. Mol. Cell. Proteomics 11, 1840-1852 (2012).
18. Ong, S. E. & Mann, M. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat. Protoc. 1, 2650-2660 (2006).
19. Fujiki, Y., Hubbard, A. L., Fowler, S. & Lazarow, P. B. Isolation of intracellular membranes by means of sodium carbonate treatment: application to Endoplasmic reticulum. J. Cell Biol. 93, 97-102 (1982).
20. Meineke, B. et al. The outer membrane form of the mitochondrial protein Mcr1 follows a TOM-independent membrane insertion pathway. FEBS Lett. 582, 855-860 (2008).
21. Pfeffer, S., Woellhaf, M. W., Herrmann, J. M. & Förster, F. Organization of the mitochondrial translation machinery studied in situ by cryoelectron tomography. Nat. Commun. 6, 6019 (2015).
22. Brandina, I. et al. Enolase takes part in a macromolecular complex associated to mitochondria in yeast. Biochim. Biophys. Acta 1757, 1217-1228 (2006).
23. Tieu, Q. & Nunnari, J. Mdv1p is a WD repeat protein that interacts with the dynamin-related GTPase, Dnm1p, to trigger mitochondrial fivision. J. Cell Biol. 151, 353-366 (2000).
24. Przybyla-Zawislak, B., Gadde, D. M., Ducharme, K. & McCammon, M. T. Genetic and biochemical interactions involving tricarboxylic acid cycle (TCA) function using a collection of mutants defective in all TCA cycle genes. Genetics 152, 153-166 (1999).
25. Heublein, M. et al. The novel component Kgd4 recruits the E3 subunit to the mitochondrial α-ketoglutarate dehydrogenase. Mol. Biol. Cell 25, 3342-3349 (2014).
26. Acosta, M. J. et al. Coenzyme Q biosynthesis in health and disease. Biochim. Biophys. Acta 1857, 1079-1085 (2016).
27. Glerum, D. M. & Tzagoloff, A. Submitochondrial distributions and stabilities of subunits 4, 5, and 6 of yeast cytochrome oxidase in assembly defective mutants. FEBS Lett. 412, 410-414 (1997).
28. Yuga, M., Gomi, K., Klionsky, D. J. & Shintani, T. Aspartyl aminopeptidase is imported from the cytoplasm to the vacuole by selective autophagy in Saccharomyces cerevisiae. J. Biol. Chem. 286, 13704-13713 (2011).
29. Vögtle, F. N. et al. Global analysis of the mitochondrial N-Proteome identifies a processing peptidase critical for protein stability. Cell 139, 428-439 (2009).
30. Steinmetz, L. M. et al. Systematic screen for human disease genes in yeast. Nat. Genet. 31, 400-404 (2002).
31. Zahedi, R. P. et al. Proteomic analysis of the yeast mitochondrial outer membrane reveals accumulation of a subclass of preproteins. Mol. Biol. Cell 17, 1436-1450 (2006).
32. Duncan, O., van der Merwe, M. J., Daley, D. O. & Whelan, J. The outer mitochondrial membrane in higher plants. Trends Plant Sci. 18, 207-217 (2013).
33. Niemann, M. et al. Mitochondrial outer membrane proteome of Trypanosoma brucei reveals novel factors required to maintain mitochondrial morphology. Mol. Cell. Proteomics 12, 515-528 (2013).
34. Schmitt, S. et al. Proteome analysis of mitochondrial outer membrane from neurospora crassa. Proteomics 6, 72-80 (2006).
35. Khalimonchuk, O. et al. Pet191 is a cytochrome c oxidase assembly factor in saccharomyces cerevisiae. Eukaryot. Cell. 7, 1427-1431 (2008).
36. Alikhani, N. et al. Targeting capacity and conservation of PreP homologues localization in mitochondria of different species. J. Mol. Biol. 410, 400-410 (2011).
37. Inadome, H., Noda, Y., Adachi, H. & Yoda, K. A novel protein, Mpm1, of the mitochondria of the yeast Saccharomyces cerevisiae. Biosci. Biotechnol. Biochem. 65, 2577-2580 (2001).
38. Büchler, M., Tisljar, U. & Wolf, D. H. Proteinase yscD (ologopeptidase yscD): structure, function and relationship of the yeast enzyme with mammalian thimet oligopeptidase. Eur. J. Biochem. 219, 627-639 (1994).
39. Kambacheld, M., Augustin, S., Tatsuta, T., Müller, S. & Langer, T. Role of the novel metallopaptidase Mop112 and saccharolysin for the complete degradation of proteins residing in different subcompartments of mitochondria. J. Biol. Chem. 280, 20132-20139 (2005).
40. Mossmann, D. et al. Amyloid beta peptide induces mitochondrial dysfunction by inhibition of preprotein maturation. Cell Metab. 20, 662-669 (2014).
41. Maarten Altelaar, A. F., Munoz, J. & Heck, A. J. R. Next-generation proteomics: towards an integrative view of proteome dynamics. Nat. Rev. Genet. 14, 35-48 (2013).
42. Aebersold, R. & Mann, M. Mass-spectrometric exploration of proteome structure and function. Nature 537, 347-355 (2016).
43. Christoforou, A. et al. A draft map of the mouse pluripotent stem cell spacial proteome. Nat. Commun. 7, 8992 (2016).
44. Stefely, J. A. et al. Mitochondrial functions elucidated by multi-omic mass spectrometry profiling. Nat. Biotechnol. 34, 1191-1197 (2016).
45. Hartwell, L. H. Saccharomyces cerevisiae cell cycle. Bacteriol. Rev. 38, 164-198 (1974).
46. Tsukada, M. & Ohsumi, Y. Isolation and characterization of autophagydefective mutants of Saccharomyces cerevisiae. FEBS Lett. 333, 169-174 (1993).
47. Rutter, J. & Hughes, A. L. Power(2): the power of yeast genetics applied to the powerhouse of the cell. Trends Endocrinol. Metab. 26, 59-68 (2015).
48. Neupert, W. & Herrmann, J. M. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723-749 (2007).
49. Pfanner, N. et al. Uniform nomenclature for the mitochondrial contact site and cristae organizing system. J. Cell Biol. 204, 1083-1086 (2014).
50. Feng, Y. et al. Global analysis of protein structural changes in complex proteomes. Nat. Biotechnol. 32, 1036-1044 (2014).
51. Sikorski, R. S. & Hieter, P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27 (1989).
52. Meisinger, C., Sommer, T. & Pfanner, N. Purification of Saccharomyces cerevisiae mitochondria devoid of microsomal and cytosolic contaminations. Anal. Biochem. 287, 339-342 (2000).
53. Burkhart, J. M., Schumbrutzki, C., Wortelkamp, S., Sickmann, A. & Zahedi, R. P. Systematic and quantitative comparison of digest efficiency and specificity reveals the impact of trypsin quality on MS-based proteomics. J. Proteomics 75, 1454-1462 (2012).
54. Vaudel, M., Barsnes, H., Berven, F. S., Sickmann, A. & Martens, L. Search GUI: An open-source graphical user interface for simultaneous OMSSA and X! Tandem searches. Proteomics 11, 996-999 (2011).
55. Vaudel, M. et al. PeptideShaker enables reanalysis of MS-derived proteomics data sets. Nat. Biotechnol. 33, 22-24 (2015).
56. Zybailov, B. et al. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J. Proteome Res. 5, 2339-2347 (2006).
57. Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372 (2008).
58. Vizcaino, J. A. et al. 2016 update of the PRIDE database and related tools. Nucleic Acids Res. 44, D447-D456 (2016).