Role for two conserved intermembrane space proteins, Ups1p and Up2p, in intra-mitochondrial phospholipid trafficking

Journal of Biological Chemistry

Volumn 287, Issue 19, 2012, Pages 15205-15218

  Tamura, Yasushi ^a   Onguka, Ouma ^a   Aiken Hobbs, Alyson E ^a   Jensen, Robert E ^a   Iijima, Miho ^a   Claypool, Steven M ^a   Sesaki, Hiromi ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLIPINS; ENDOPLASMIC RETICULUM; INNER MEMBRANES; INNER MITOCHONDRIAL MEMBRANES; INTERMEMBRANE SPACE; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL MORPHOLOGY; OUTER MEMBRANE; OVER-EXPRESSION; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHOLIPID TRANSPORT; YEAST SACCHAROMYCES CEREVISIAE;

AMINO ACIDS; BIOCHEMISTRY; CELL MEMBRANES; DEFECTS; METABOLISM; MITOCHONDRIA; PHOSPHOLIPIDS; PHYSIOLOGY; YEAST;

PROTEINS;

MEMBRANE PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHOLIPID; PROTEIN MDM31P; PROTEIN UP2P; PROTEIN UPS1P; UNCLASSIFIED DRUG;

ARTICLE; CELL GROWTH; CELL STRUCTURE; CONTROLLED STUDY; GROWTH INHIBITION; LIPID COMPOSITION; LIPID METABOLISM; MITOCHONDRIAL MEMBRANE; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; ENDOPLASMIC RETICULUM; HYDROGEN-ION CONCENTRATION; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; MUTATION; PHOSPHATIDYLETHANOLAMINES; PHOSPHATIDYLSERINES; PHOSPHOLIPIDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SERINE;

SACCHAROMYCES CEREVISIAE;

EID: 84860859573     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.338665     Document Type: Article

References (55)

1. Claypool, S. M. (2009) Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function. Biochim. Biophys. Acta 1788, 2059-2068
2. Joshi, A. S., Zhou, J., Gohil, V. M., Chen, S., and Greenberg, M. L. (2009) Cellular functions of cardiolipin in yeast. Biochim. Biophys. Acta 1793, 212-218
3. Jiang, F., Ryan, M. T., Schlame, M., Zhao, M., Gu, Z., Klingenberg, M., Pfanner, N., and Greenberg, M. L. (2000) Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J. Biol. Chem. 275, 22387-22394 (Pubitemid 30621825)
4. van der Laan, M., Meinecke, M., Dudek, J., Hutu, D. P., Lind, M., Perschil, I., Guiard, B., Wagner, R., Pfanner, N., and Rehling, P. (2007) Motor-free mitochondrial presequence translocase drives membrane integration of preproteins. Nat. Cell Biol. 9, 1152-1159 (Pubitemid 47500491)
5. Kutik, S., Rissler, M., Guan, X. L., Guiard, B., Shui, G., Gebert, N., Heacock, P. N., Rehling, P., Dowhan, W., Wenk, M. R., Pfanner, N., and Wiedemann, N. (2008) The translocator maintenance protein Tam41 is required for mitochondrial cardiolipin biosynthesis. J. Cell Biol. 183, 1213-1221
6. 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., Rehling, P., Meisinger, C., Ryan, M. T., Wiedemann, N., Greenberg, M. L., and Pfanner, N. (2009) Mitochondrial cardiolipin involved in outer-membrane protein biogenesis. Implications for Barth syndrome. Curr. Biol. 19, 2133-2139
7. Tamura, Y., Endo, T., Iijima, M., and Sesaki, H. (2009) Ups1p and Ups2p antagonistically regulate cardiolipin metabolism in mitochondria. J. Cell Biol. 185, 1029-1045
8. Harada, Y., Tamura, Y., and Endo, T. (2010) Identification of yeast Art5 as a multicopy suppressor for the mitochondrial translocator maintenance protein Tam41. Biochem. Biophys. Res. Commun. 392, 228-233
9. Choi, S. Y., Huang, P., Jenkins, G. M., Chan, D. C., Schiller, J., and Frohman, M. A. (2006) A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nat. Cell Biol. 8, 1255-1262 (Pubitemid 44660590)
10. DeVay, R. M., Dominguez-Ramirez, L., Lackner, L. L., Hoppins, S., Stahlberg, H., and Nunnari, J. (2009) Coassembly of Mgm1 isoforms requires cardiolipin and mediates mitochondrial inner membrane fusion. J. Cell Biol. 186, 793-803
11. Rujiviphat, J., Meglei, G., Rubinstein, J. L., and McQuibban, G. A. (2009) Phospholipid association is essential for dynamin-related protein Mgm1 to function in mitochondrial membrane fusion. J. Biol. Chem. 284, 28682-28686
12. Huang, H., Gao, Q., Peng, X., Choi, S. Y., Sarma, K., Ren, H., Morris, A. J., and Frohman, M. A. (2011) piRNA-associated germ line nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial surface lipid signaling. Dev. Cell 20, 376-387
13. Lutter, M., Fang, M., Luo, X., Nishijima, M., Xie, X., and Wang, X. (2000) Cardiolipin provides specificity for targeting of tBid to mitochondria. Nat. Cell Biol. 2, 754-761
14. Lucken-Ardjomande, S., Montessuit, S., and Martinou, J. C. (2008) Contributions to Bax insertion and oligomerization of lipids of the mitochondrial outer membrane. Cell Death Differ. 15, 929-937 (Pubitemid 351524434)
15. Sani, M. A., Dufourc, E. J., and Gröbner, G. (2009) How does the Bax-α1 targeting sequence interact with mitochondrial membranes? The role of cardiolipin. Biochim. Biophys. Acta 1788, 623-631
16. Zaltsman, Y., Shachnai, L., Yivgi-Ohana, N., Schwarz, M., Maryanovich, M., Houtkooper, R. H., Vaz, F. M., De Leonardis, F., Fiermonte, G., Palmieri, F., Gillissen, B., Daniel, P. T., Jimenez, E., Walsh, S., Koehler, C. M., Roy, S. S., Walter, L., Hajnóczky, G., and Gross, A. (2010) MTCH2/MIMP is a major facilitator of tBID recruitment to mitochondria. Nat. Cell Biol. 12, 553-562
17. Voelker, D. R. (1989) Reconstitution of phosphatidylserine import into rat liver mitochondria. J. Biol. Chem. 264, 8019-8025
18. Simbeni, R., Tangemann, K., Schmidt, M., Ceolotto, C., Paltauf, F., and Daum, G. (1993) Import of phosphatidylserine into isolated yeast mitochondria. Biochim. Biophys. Acta 1145, 1-7 (Pubitemid 23026346)
19. Trotter, P. J., Pedretti, J., and Voelker, D. R. (1993) Phosphatidylserine decarboxylase from Saccharomyces cerevisiae. Isolation of mutants, cloning of the gene, and creation of a null allele. J. Biol. Chem. 268, 21416-21424 (Pubitemid 23292337)
20. Kodaki, T., and Yamashita, S. (1987) Yeast phosphatidylethanolamine methylation pathway. Cloning and characterization of two distinct methyltransferase genes. J. Biol. Chem. 262, 15428-15435
21. Chang, S. C., Heacock, P. N., Clancey, C. J., and Dowhan, W. (1998) The PEL1 gene (renamed PGS1) encodes the phosphatidylglycerophosphate synthase of Saccharomyces cerevisiae. J. Biol. Chem. 273, 9829-9836 (Pubitemid 28183078)
22. Osman, C., Haag, M., Wieland, F. T., Brügger, B., and Langer, T. (2010) A mitochondrial phosphatase required for cardiolipin biosynthesis: the PGP phosphatase Gep4. EMBO J. 29, 1976-1987
23. Chang, S. C., Heacock, P. N., Mileykovskaya, E., Voelker, D. R., and Dowhan, W. (1998) Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharomyces cerevisiae. J. Biol. Chem. 273, 14933-14941 (Pubitemid 28272784)
24. Kornmann, B., Currie, E., Collins, S. R., Schuldiner, M., Nunnari, J., Weissman, J. S., and Walter, P. (2009) An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477-481
25. Kornmann, B., Osman, C., and Walter, P. (2011) The conserved GTPase Gem1 regulates endoplasmic reticulum-mitochondria connections. Proc. Natl. Acad. Sci. U.S.A. 108, 14151-14156
26. Stroud, D. A., Oeljeklaus, S., Wiese, S., Bohnert, M., Lewandrowski, U., Sickmann, A., Guiard, B., van der Laan, M., Warscheid, B., and Wiedemann, N. (2011) Composition and topology of the endoplasmic reticulum-mitochondria encounter structure. J. Mol. Biol. 413, 743-750
27. Kopec, K. O., Alva, V., and Lupas, A. N. (2010) Homology of SMP domains to the TULIP superfamily of lipid-binding proteins provides a structural basis for lipid exchange between ER and mitochondria. Bioinformatics 26, 1927-1931
28. Burgess, S. M., Delannoy, M., and Jensen, R. E. (1994) MMM1 encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria. J. Cell Biol. 126, 1375-1391 (Pubitemid 24284604)
29. Sogo, L. F., and Yaffe, M. P. (1994) Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane. J. Cell Biol. 126, 1361-1373 (Pubitemid 24284603)
30. Berger, K. H., Sogo, L. F., and Yaffe, M. P. (1997) Mdm12p, a component required for mitochondrial inheritance that is conserved between budding and fission yeast. J. Cell Biol. 136, 545-553 (Pubitemid 27083757)
31. Dimmer, K. S., Fritz, S., Fuchs, F., Messerschmitt, M., Weinbach, N., Neupert, W., and Westermann, B. (2002) Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 847-853 (Pubitemid 34250350)
32. Frederick, R. L., Okamoto, K., and Shaw, J. M. (2008) Multiple pathways influence mitochondrial inheritance in budding yeast. Genetics 178, 825-837 (Pubitemid 351398796)
33. Youngman, M. J., Hobbs, A. E., Burgess, S. M., Srinivasan, M., and Jensen, R. E. (2004) Mmm2p, a mitochondrial outer membrane protein required for yeast mitochondrial shape and maintenance of mtDNA nucleoids. J. Cell Biol. 164, 677-688 (Pubitemid 38282952)
34. Sesaki, H., Dunn, C. D., Iijima, M., Shepard, K. A., Yaffe, M. P., Machamer, C. E., and Jensen, R. E. (2006) Ups1p, a conserved intermembrane space protein, regulates mitochondrial shape and alternative topogenesis of Mgm1p. J. Cell Biol. 173, 651-658 (Pubitemid 46165573)
35. Osman, C., Haag, M., Potting, C., Rodenfels, J., Dip, P. V., Wieland, F. T., Brügger, B., Westermann, B., and Langer, T. (2009) The genetic interactome of prohibitins. Coordinated control of cardiolipin and phosphatidylethanolamine by conserved regulators in mitochondria. J. Cell Biol. 184, 583-596
36. Dimmer, K. S., Jakobs, S., Vogel, F., Altmann, K., and Westermann, B. (2005) Mdm31 and Mdm32 are inner membrane proteins required for maintenance of mitochondrial shape and stability of mitochondrial DNA nucleoids in yeast. J. Cell Biol. 168, 103-115 (Pubitemid 40111061)
37. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P., and Boeke, J. D. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C. A useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132 (Pubitemid 28062863)
38. Winston, F., Dollard, C., and Ricupero-Hovasse, S. L. (1995) Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11, 53-55
39. Sesaki, H., and Jensen, R. E. (1999) Division versus fusion. Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 147, 699-706
40. Jensen, R. E., Schmidt, S., and Mark, R. J. (1992) Mutations in a 19-amino acid hydrophobic region of the yeast cytochrome c1 presequence prevent sorting to the mitochondrial intermembrane space. Mol. Cell. Biol. 12, 4677-4686
41. Adams, A., Gottschling, D., Kaiser, C., and Stearns, T. (1997) Methods in Yeast Genetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
42. Vaden, D. L., Gohil, V. M., Gu, Z., and Greenberg, M. L. (2005) Separation of yeast phospholipids using one-dimensional thin layer chromatography. Anal. Biochem. 338, 162-164 (Pubitemid 40228910)
43. Claypool, S. M., McCaffery, J. M., and Koehler, C. M. (2006) Mitochondrial mislocalization and altered assembly of a cluster of Barth syndrome mutant tafazzins. J. Cell Biol. 174, 379-390 (Pubitemid 44156768)
44. Tamura, Y., Iijima, M., and Sesaki, H. (2010) Mdm35p imports Ups proteins into the mitochondrial intermembrane space by functional complex formation. EMBO J. 29, 2875-2887
45. Pon, L., Moll, T., Vestweber, D., Marshallsay, B., and Schatz, G. (1989) Protein import into mitochondria. ATP-dependent protein translocation activity in a submitochondrial fraction enriched in membrane contact sites and specific proteins. J. Cell Biol. 109, 2603-2616 (Pubitemid 20011889)
46. Tamura, Y., Harada, Y., Shiota, T., Yamano, K., Watanabe, K., Yokota, M., Yamamoto, H., Sesaki, H., and Endo, T. (2009) Tim23-Tim50 pair coordinates functions of translocators and motor proteins in mitochondrial protein import. J. Cell Biol. 184, 129-141
47. Shiota, T., Mabuchi, H., Tanaka-Yamano, S., Yamano, K., and Endo, T. (2011) In vivo protein-interaction mapping of a mitochondrial translocator protein Tom22 at work. Proc. Natl. Acad. Sci. U.S.A. 108, 15179-15183
48. Chacinska, A., Lind, M., Frazier, A. E., Dudek, J., Meisinger, C., Geissler, A., Sickmann, A., Meyer, H. E., Truscott, K. N., Guiard, B., Pfanner, N., and Rehling, P. (2005) Mitochondrial presequence translocase: switching between TOM tethering and motor recruitment involves Tim21 and Tim17. Cell 120, 817-829 (Pubitemid 40568799)
49. Mokranjac, D., Popov-Celeketić, D., Hell, K., and Neupert, W. (2005) Role of Tim21 in mitochondrial translocation contact sites. J. Biol. Chem. 280, 23437-23440 (Pubitemid 40884819)
50. Hoppins, S., Collins, S. R., Cassidy-Stone, A., Hummel, E., Devay, R. M., Lackner, L. L., Westermann, B., Schuldiner, M., Weissman, J. S., and Nunnari, J. (2011) A mitochondrial focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J. Cell Biol. 195, 323-340
51. von der Malsburg, K., Müller, J. M., Bohnert, M., Oeljeklaus, S., Kwiatkowska, P., Becker, T., Loniewska-Lwowska, A., Wiese, S., Rao, S., Milenkovic, D., Hutu, D. P., Zerbes, R. M., Schulze-Specking, A., Meyer, H. E., Martinou, J. C., Rospert, S., Rehling, P., Meisinger, C., Veenhuis, M., Warscheid, B., van der Klei, I. J., Pfanner, N., Chacinska, A., and van der Laan, M. (2011) Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev. Cell 21, 694-707
52. Harner, M., Körner, C., Walther, D., Mokranjac, D., Kaesmacher, J., Welsch, U., Griffith, J., Mann, M., Reggiori, F., and Neupert, W. (2011) The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J. 30, 4356-4370
53. de Brito, O. M., and Scorrano, L. (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605-610
54. Fujimoto, M., and Hayashi, T. (2011) New insights into the role of mitochondria- associated endoplasmic reticulum membrane. Int. Rev. Cell Mol. Biol. 292, 73-117
55. 2/M transition. J. Biol. Chem. 285, 10397-10407