Membrane integration of a mitochondrial signal-anchored protein does not require additional proteinaceous factors

Biochemical Journal

Volumn 442, Issue 2, 2012, Pages 381-389

  Merklinger, Elisa ^a   Gofman, Yana ^b   Kedrov, Alexej ^c   Driessen, Arnold J M ^c   Ben Tal, Nir ^d   Shai, Yechiel ^e   Rapaport, Doron ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b INSTITUTE OF MATERIALS RESEARCH   (Germany)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d TEL AVIV UNIVERSITY   (Israel)

^e WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Ergosterol; Mitochondrion; Outer membrane; Signal anchored protein (SA protein)

Indexed keywords

ERGOSTEROL; OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN OM45; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; ARTIFICIAL MEMBRANE; BIOGENESIS; ENDOPLASMIC RETICULUM; ENERGY; INFRARED SPECTROSCOPY; LIPID BILAYER; LIPID COMPOSITION; LIPID VESICLE; MITOCHONDRION; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; THERMOSTABILITY;

ENDOPLASMIC RETICULUM; MEMBRANE LIPIDS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; PROTEIN BINDING; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; THERMODYNAMICS; UNILAMELLAR LIPOSOMES;

EID: 84856839337     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111363     Document Type: Article

References (40)

1. Pfanner, N., Wiedemann, N., Meisinger, C. and Lithgow, T. (2004) Assembling the mitochondrial outer membrane. Nat. Struct. Mol. Biol. 11, 1044-1048 (Pubitemid 39453331)
2. Endo, T. and Yamano, K. (2009) Multiple pathways for mitochondrial protein traffic. Biol. Chem. 390, 723-730
3. Walther, D. M. and Rapaport, D. (2009) Biogenesis of mitochondrial outer membrane proteins. Biochim. Biophys. Acta 1793, 42-51
4. Shore, G. C., McBride, H. M., Millar, D. G., Steenaart, N. A. E. and Nguyen, M. (1995) Import and insertion of proteins into the mitochondrial outer membrane. Eur. J. Biochem. 227, 9-18
5. Borgese, N., Colombo, S. and Pedrazzini, E. (2003) The tale of tail-anchored proteins: coming from the cytosol and looking for a membrane. J. Cell Biol. 161, 1013-1019 (Pubitemid 36870163)
6. Isenmann, S., Khew-Goodall, Y., Gamble, J., Vadas, M. and Wattenberg, B. W. (1998) A splice-isoform of vesicle-associated membrane protein-1 (VAMP-1) contains a mitochondrial targeting signal. Mol. Biol. Cell 9, 1649-1660 (Pubitemid 28337513)
7. Lan, L., Isenmann, S. and Wattenberg, B. W. (2000) Targeting and insertion of C-terminally anchored proteins to the mitochondrial outer membrane is specific and saturable but does not strictly require ATP or molecular chaperones. Biochem. J. 349, 611-621 (Pubitemid 30465797)
8. Horie, C., Suzuki, H., Sakaguchi, M. and Mihara, K. (2002) Characterization of signal that directs C-tail-anchored proteins to mammalian mitochondrial outer membrane. Mol. Biol. Cell 13, 1615-1625 (Pubitemid 34522643)
9. Kemper, C., Habib, S. J., Engl, G., Heckmeyer, P., Dimmer, K. S. and Rapaport, D. (2008) Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components. J. Cell Sci. 121, 1990-1998 (Pubitemid 352015196)
10. Schneider, H., Sollner, T., Dietmeier, K., Eckerskorn, C., Lottspeich, F., Trulzsch, B., Neupert, W. and Pfanner, N. (1991) Targeting of the master receptor MOM19 to mitochondria. Science 254, 1659-1662 (Pubitemid 21917513)
11. Schlossmann, J. and Neupert, W. (1995) Assembly of the preprotein receptor MOM72/MAS70 into the protein import complex of the outer membrane of mitochondria. J. Biol. Chem. 270, 27116-27121
12. Ahting, U., Waizenegger, T., Neupert, W. and Rapaport, D. (2005) Signal-anchored proteins follow a unique insertion pathway into the outer membrane of mitochondria. J. Biol. Chem. 280, 48-53 (Pubitemid 40164963)
13. Meineke, B., Engl, G., Kemper, C., Vasiljev-Neumeyer, A., Paulitschke, H. and Rapaport, D. (2008) The outer membrane form of the mitochondrial protein Mcr1 follows a TOM-independent membrane insertion pathway. FEBS Lett. 582, 855-860
14. Becker, T., Pfannschmidt, S., Guiard, B., Stojanovski, D., Milenkovic, D., Kutik, S., Pfanner, N., Meisinger, C. and Wiedemann, N. (2008) Biogenesis of the mitochondrial TOM complex: Mim1 promotes insertion and assembly of signal-anchored receptors. J. Biol. Chem. 283, 120-127
15. Hulett, J. M., Lueder, F., Chan, N. C., Perry, A. J., Wolynec, P., Likic, V. A., Gooley, P. R. and Lithgow, T. (2008) The transmembrane segment of Tom20 is recognized by Mim1 for docking to the mitochondrial TOM complex. J. Mol. Biol. 376, 694-704
16. Popov-Celeketic, J., Waizenegger, T. and Rapaport, D. (2008) Mim1 functions in an oligomeric form to facilitate the integration of Tom20 into the mitochondrial outer membrane. J. Mol. Biol. 376, 671-680
17. Dukanovic, J. and Rapaport, D. (2011) Multiple pathways in the integration of proteins into the mitochondrial outer membrane. Biochim. Biophys. Acta 1808, 971-980
18. Waizenegger, T., Stan, T., Neupert, W. and Rapaport, D. (2003) Signal-anchor domains of proteins of the outer membrane of mitochondria: structural and functional characteristics. J. Biol. Chem. 278, 42064-42071 (Pubitemid 37310472)
19. De Kroon, A. I. P. M., Koorengevel, M. C., Goerdayal, S. S., Mulders, P. C., Janssen, M. J. and De Kruijff, B. (1999) Isolation and characterization of highly purified mitochondrial outer membranes of the yeast Saccharomyces cerevisiae. Mol. Membr. Biol. 16, 205-211 (Pubitemid 29308821)
20. Ishiguro, R., Matsumoto, M. and Takahashi, S. (1996) Interaction of fusogenic synthetic peptide with phospholipid bilayers: orientation of the peptide alpha-helix and binding isotherm. Biochemistry 35, 4976-4983 (Pubitemid 26126714)
21. Sharon, M., Oren, Z., Shai, Y. and Anglister, J. (1999) 2D-NMR and ATR-FTIR study of the structure of a cell-selective diastereomer of melittin and its orientation in phospholipids. Biochemistry 38, 15305-15316 (Pubitemid 129520364)
22. Tamm, L. K. and Tatulian, S. A. (1997) Infrared spectroscopy of proteins and peptides in lipid bilayers. Q. Rev. Biophys. 30, 365-429 (Pubitemid 28260614)
23. Ghosh, J. K., Peisajovich, S. G. and Shai, Y. (2000) Sendai virus internal fusion peptide: structural and functional characterization and a plausible mode of viral entry inhibition. Biochemistry 39, 11581-11592
24. Rosenfeld, Y., Barra, D., Simmaco, M., Shai, Y. and Mangoni, M. L. (2006) A synergism between temporins toward Gram-negative bacteria overcomes resistance imposed by the lipopolysaccharide protective layer. J. Biol. Chem. 281, 28565-28574 (Pubitemid 44506999)
25. Tang, J., Signarvic, R. S., DeGrado, W. F. and Gai, F. (2007) Role of helix nucleation in the kinetics of binding of mastoparan X to phospholipid bilayers. Biochemistry 46, 13856-13863 (Pubitemid 350223913)
26. Colombo, S. F., Longhi, R. and Borgese, N. (2009) The role of cytosolic proteins in the insertion of tail-anchored proteins into phospholipid bilayers. J. Cell Sci. 122, 2383-2392
27. Huang, H. W. (2000) Action of antimicrobial peptides: two-state model. Biochemistry 39, 8347-8352
28. White, S. H., Ladokhin, A. S., Jayasinghe, S. and Hristova, K. (2001) How membranes shape protein structure. J. Biol. Chem. 276, 32395-32398
29. Shai, Y. (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers 66, 236-248
30. Andreev, O. A., Karabadzhak, A. G., Weerakkody, D., Andreev, G. O., Engelman, D. M. and Reshetnyak, Y. K. (2010) pH (low) insertion peptide (pHLIP) inserts across a lipid bilayer as a helix and exits by a different path. Proc. Natl. Acad. Sci. U.S.A. 107, 4081-4086
31. van Klompenburg, W., Nilsson, I., von Heijne, G. and de Kruijff, B. (1997) Anionic phospholipids are determinants of membrane protein topology. EMBO J. 16, 4261-4266 (Pubitemid 27298178)
32. Shahidullah, K. and London, E. (2008) Effect of lipid composition on the topography of membrane-associated hydrophobic helices: stabilization of transmembrane topography by anionic lipids. J. Mol. Biol. 379, 704-718
33. Brambillasca, S., Yabal, M., Makarow, M. and Borgese, N. (2006) Unassisted translocation of large polypeptide domains across phospholipid bilayers. J. Cell Biol. 175, 767-777 (Pubitemid 44878509)
34. Dimmer, S. K. and Rapaport, D. (2009) The enigmatic role of Mim1 in mitochondrial biogenesis. Eur. J. Cell Biol. 89, 212-215
35. Gebert, N., Joshi, A. S., Kutik, S., Becker, T., McKenzie, M., Guan, X. L., Mooga, V. P., Stroud, D. A., Kulkarni, G., Wenk, M. R. et al. (2009) Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: implications for Barth syndrome. Curr. Biol. 19, 2133-2139
36. Kim, T. H., Zhao, Y., Ding, W. X., Shin, J. N., He, X., Seo, Y. W., Chen, J., Rabinowich, H., Amoscato, A. A. and Yin, X. M. (2004) Bid-cardiolipin interaction at mitochondrial contact site contributes to mitochondrial cristae reorganization and cytochrome C release. Mol. Biol. Cell 15, 3061-3072 (Pubitemid 38850104)
37. Gonzalvez, F., Schug, Z. T., Houtkooper, R. H., MacKenzie, E. D., Brooks, D. G., Wanders, R. J., Petit, P. X., Vaz, F. M. and Gottlieb, E. (2008) Cardiolipin provides an essential activating platform for caspase-8 on mitochondria. J. Cell Biol. 183, 681-696
38. Zinser, E., Sperka-Gottlieb, C. D., Fasch, E. V., Kohlwein, S. D., Paltauf, F. and Daum, G. (1991) Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae. J. Bacteriol. 173, 2026-2034
39. Schneiter, R., Brugger, B., Sandhoff, R., Zellnig, G., Leber, A., Lampl, M., Athenstaedt, K., Hrastnik, C., Eder, S., Daum, G. et al. (1999) Electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis of the lipid molecular species composition of yeast subcellular membranes reveals acyl chain-based sorting/remodeling of distinct molecular species en route to the plasma membrane. J. Cell Biol. 146, 741-754 (Pubitemid 29408901)
40. Egashira, M., Gorbenko, G., Tanaka, M., Saito, H., Molotkovsky, J., Nakano, M. and Handa, T. (2002) Cholesterol modulates interaction between an amphipathic class A peptide, Ac-18A-NH2, and phosphatidylcholine bilayers. Biochemistry 41, 4165-4172 (Pubitemid 34251056)