Unresolved mysteries in the biogenesis of mitochondrial membrane proteins

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 4, 2012, Pages 1085-1090

  Dimmer, Kai Stefan ^a   Rapaport, Doron ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Membrane protein; Mitochondrial import; Mitochondrial translocase; Protein insertion into mitochondrial membrane

Indexed keywords

CELL MEMBRANE PROTEIN; LIPID; MESSENGER RNA; MITOCHONDRIAL PROTEIN; PROTEIN OXA; PROTEIN TIM23; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELL MEMBRANE TRANSPORT; CELL ORGANELLE; LIPID MEMBRANE; MEMBRANE BIOLOGY; MEMBRANE STRUCTURE; MITOCHONDRIAL MEMBRANE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; THERMODYNAMICS;

ANIMALS; HUMANS; LIPID METABOLISM; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; PROTEIN TRANSPORT; RNA TRANSPORT; RNA, MESSENGER;

EUKARYOTA;

EID: 84857643393     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.08.027     Document Type: Review

References (89)

1. J. Reinders, R.P. Zahedi, N. Pfanner, C. Meisinger, and A. Sickmann Toward the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics J. Proteome Res. 5 2006 1543 1554
2. S.W. Taylor, E. Fahy, B. Zhang, G.M. Glenn, D.E. Warnock, S. Wiley, A.N. Murphy, S.P. Gaucher, R.A. Capaldi, B.W. Gibson, and S.S. Ghosh Characterization of the human heart mitochondrial proteome Nat. Biotechnol. 21 2003 281 286
3. V.K. Mootha, J. Bunkenborg, J.V. Olsen, M. Hjerrild, J.R. Wisniewski, E. Stahl, M.S. Bolouri, H.N. Ray, S. Sihag, M. Kamal, N. Patterson, E.S. Lander, and M. Mann Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria Cell 115 2003 629 640
4. O. Schmidt, N. Pfanner, and C. Meisinger Mitochondrial protein import: from proteomics to functional mechanisms Nat. Rev. Mol. Cell Biol. 11 2010 655 667
5. D.M. Walther, and D. Rapaport Biogenesis of mitochondrial outer membrane proteins Biochim. Biophys. Acta 1793 2009 42 51
6. T. Becker, M. Gebert, N. Pfanner, and M. van der Laan Biogenesis of mitochondrial membrane proteins Curr. Opin. Cell Biol. 21 2009 484 493
7. C. Kemper, S.J. Habib, G. Engl, P. Heckmeyer, K.S. Dimmer, and D. Rapaport Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components J. Cell Sci. 121 2008 1990 1998
8. B. Meineke, G. Engl, C. Kemper, A. Vasiljev-Neumeyer, H. Paulitschke, and D. Rapaport The outer membrane form of the mitochondrial protein Mcr1 follows a TOM-independent membrane insertion pathway FEBS Lett. 582 2008 855 860
9. K. Setoguchi, H. Otera, and K. Mihara Cytosolic factor- and TOM-independent import of C-tail-anchored mitochondrial outer membrane proteins EMBO J. 25 2006 5635 5647
10. J. Schlossmann, and W. Neupert Assembly of the preprotein receptor MOM72/MAS70 into the protein import complex of the outer membrane of mitochondria J. Biol. Chem. 270 1995 27116 27121
11. H. Schneider, T. Sollner, K. Dietmeier, C. Eckerskorn, F. Lottspeich, B. Trulzsch, W. Neupert, and N. Pfanner Targeting of the master receptor MOM19 to mitochondria Science 254 1991 1659 1662
12. U. Ahting, T. Waizenegger, W. Neupert, and D. Rapaport Signal-anchored proteins follow a unique insertion pathway into the outer membrane of mitochondria J. Biol. Chem. 280 2005 48 53
13. H. Otera, Y. Taira, C. Horie, Y. Suzuki, H. Suzuki, K. Setoguchi, H. Kato, T. Oka, and K. Mihara A novel insertion pathway of mitochondrial outer membrane proteins with multiple transmembrane segments J. Cell Biol. 179 2007 1355 1363
14. D. Stojanovski, B. Guiard, V. Kozjak-Pavlovic, N. Pfanner, and C. Meisinger Alternative function for the mitochondrial SAM complex in biogenesis of alpha-helical TOM proteins J. Cell Biol. 179 2007 881 893
15. C. Horie, H. Suzuki, M. Sakaguchi, and K. Mihara Targeting and assembly of mitochondrial tail-anchored protein Tom5 to the TOM complex depend on a signal distinct from that of tail-anchored proteins dispersed in the membrane J. Biol. Chem. 278 2003 41462 41471
16. M. Dembowski, K.P. Kunkele, F.E. Nargang, W. Neupert, and D. Rapaport Assembly of Tom6 and Tom7 into the TOM core complex of Neurospora crassa J. Biol. Chem. 276 2001 17679 17685
17. K.S. Dimmer, and D. Rapaport The enigmatic role of Mim1 in mitochondrial biogenesis Eur. J. Cell Biol. 89 2010 212 215
18. S. Mnaimneh, A.P. Davierwala, J. Haynes, J. Moffat, W.T. Peng, W. Zhang, X. Yang, J. Pootoolal, G. Chua, A. Lopez, M. Trochesset, D. Morse, N.J. Krogan, S.L. Hiley, Z. Li, Q. Morris, J. Grigull, N. Mitsakakis, C.J. Roberts, J.F. Greenblatt, C. Boone, C.A. Kaiser, B.J. Andrews, and T.R. Hughes Exploration of essential gene functions via titratable promoter alleles Cell 118 2004 31 44
19. J. Popov-Celeketic, T. Waizenegger, and D. Rapaport Mim1 functions in an oligomeric form to facilitate the integration of Tom20 into the mitochondrial outer membrane J. Mol. Biol. 376 2008 671 680
20. T. Waizenegger, S. Schmitt, J. Zivkovic, W. Neupert, and D. Rapaport Mim1, a protein required for the assembly of the TOM complex of mitochondria EMBO Rep. 6 2005 57 62
21. D. Ishikawa, H. Yamamoto, Y. Tamura, K. Moritoh, and T. Endo Two novel proteins in the mitochondrial outer membrane mediate beta-barrel protein assembly J. Cell Biol. 166 2004 621 627
22. T. Becker, S. Pfannschmidt, B. Guiard, D. Stojanovski, D. Milenkovic, S. Kutik, N. Pfanner, C. Meisinger, and N. Wiedemann Biogenesis of the mitochondrial TOM complex: Mim1 promotes insertion and assembly of signal-anchored receptors J. Biol. Chem. 283 2008 120 127
23. J.M. Hulett, F. Lueder, N.C. Chan, A.J. Perry, P. Wolynec, V.A. Likic, P.R. Gooley, and T. Lithgow The transmembrane segment of Tom20 is recognized by Mim1 for docking to the mitochondrial TOM complex J. Mol. Biol. 376 2008 694 704
24. D. Papic, K. Krumpe, J. Dukanovic, K.S. Dimmer, and D. Rapaport Multispan mitochondrial outer membrane protein Ugo1 follows a unique Mim1-dependent import pathway J. Cell Biol. 194 2011 397 405
25. T. Becker, L.S. Wenz, V. Kruger, W. Lehmann, J.M. Muller, L. Goroncy, N. Zufall, T. Lithgow, B. Guiard, A. Chacinska, R. Wagner, C. Meisinger, and N. Pfanner The mitochondrial import protein Mim1 promotes biogenesis of multispanning outer membrane proteins J. Cell Biol. 194 2011 387 395
26. K. Wagner, P. Rehling, L.K. Sanjuan Szklarz, R.D. Taylor, N. Pfanner, and M. van der Laan Mitochondrial F1Fo-ATP synthase: the small subunits e and g associate with monomeric complexes to trigger dimerization J. Mol. Biol. 392 2009 855 861
27. N. Altamura, N. Capitanio, N. Bonnefoy, S. Papa, and G. Dujardin The Saccharomyces cerevisiae OXA1 gene is required for the correct assembly of cytochrome c oxidase and oligomycin-sensitive ATP synthase FEBS Lett. 382 1996 111 115
28. L. Jia, M.K. Dienhart, and R.A. Stuart Oxa1 directly interacts with Atp9 and mediates its assembly into the mitochondrial F1Fo-ATP synthase complex Mol. Biol. Cell 18 2007 1897 1908
29. C. Lemaire, P. Hamel, J. Velours, and G. Dujardin Absence of the mitochondrial AAA protease Yme1p restores F0-ATPase subunit accumulation in an oxa1 deletion mutant of Saccharomyces cerevisiae J. Biol. Chem. 275 2000 23471 23475
30. P. Hamel, C. Lemaire, N. Bonnefoy, P. Brivet-Chevillotte, and G. Dujardin Mutations in the membrane anchor of yeast cytochrome c1 compensate for the absence of Oxa1p and generate carbonate-extractable forms of cytochrome c1 Genetics 150 1998 601 611
31. T. Endo, K. Yamano, and S. Kawano Structural insight into the mitochondrial protein import system Biochim. Biophys. Acta 1808 2011 955 970
32. J.C. Young, N.J. Hoogenraad, and F.U. Hartl Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70 Cell 112 2003 41 50
33. N. Pfanner, N. Wiedemann, C. Meisinger, and T. Lithgow Assembling the mitochondrial outer membrane Nat. Struct. Mol. Biol. 11 2004 1044 1048
34. V. Kozjak, N. Wiedemann, D. Milenkovic, C. Lohaus, H.E. Meyer, B. Guiard, C. Meisinger, and N. Pfanner An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane J. Biol. Chem. 278 2003 48520 48523
35. S.A. Paschen, T. Waizenegger, T. Stan, M. Preuss, M. Cyrklaff, K. Hell, D. Rapaport, and W. Neupert Evolutionary conservation of biogenesis of beta-barrel membrane proteins Nature 426 2003 862 866
36. I. Gentle, K. Gabriel, P. Beech, R. Waller, and T. Lithgow The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria J. Cell Biol. 164 2004 19 24
37. A. Chacinska, M. Lind, A.E. Frazier, J. Dudek, C. Meisinger, A. Geissler, A. Sickmann, H.E. Meyer, K.N. Truscott, B. Guiard, N. Pfanner, and P. Rehling Mitochondrial presequence translocase: switching between TOM tethering and motor recruitment involves Tim21 and Tim17 Cell 120 2005 817 829
38. M. van der Laan, N. Wiedemann, D.U. Mick, B. Guiard, P. Rehling, and N. Pfanner A role for Tim21 in membrane-potential-dependent preprotein sorting in mitochondria Curr. Biol. 16 2006 2271 2276
39. A. Chacinska, M. van der Laan, C.S. Mehnert, B. Guiard, D.U. Mick, D.P. Hutu, K.N. Truscott, N. Wiedemann, C. Meisinger, N. Pfanner, and P. Rehling Distinct forms of mitochondrial TOM-TIM supercomplexes define signal-dependent states of preprotein sorting Mol. Cell. Biol. 30 2010 307 318
40. D. Popov-Celeketic, K. Mapa, W. Neupert, and D. Mokranjac Active remodelling of the TIM23 complex during translocation of preproteins into mitochondria EMBO J. 27 2008 1469 1480
41. D. Mokranjac, and W. Neupert The many faces of the mitochondrial TIM23 complex Biochim. Biophys. Acta 1797 2010 1045 1054
42. A. Chacinska, C.M. Koehler, D. Milenkovic, T. Lithgow, and N. Pfanner Importing mitochondrial proteins: machineries and mechanisms Cell 138 2009 628 644
43. D. Popov-Celeketic, K. Waegemann, K. Mapa, W. Neupert, and D. Mokranjac Role of the import motor in insertion of transmembrane segments by the mitochondrial TIM23 complex EMBO Rep. 12 2011 542 548
44. S. Meier, W. Neupert, and J.M. Herrmann Proline residues of transmembrane domains determine the sorting of inner membrane proteins in mitochondria J. Cell Biol. 170 2005 881 888
45. K. Kaldi, M.F. Bauer, C. Sirrenberg, W. Neupert, and M. Brunner Biogenesis of Tim23 and Tim17, integral components of the TIM machinery for matrix-targeted preproteins EMBO J. 17 1998 1569 1576
46. C. Sirrenberg, M. Endres, H. Folsch, R.A. Stuart, W. Neupert, and M. Brunner Carrier protein import into mitochondria mediated by the intermembrane proteins Tim10/Mrs11 and Tim12/Mrs5 Nature 391 1998 912 915
47. C. Sirrenberg, M.F. Bauer, B. Guiard, W. Neupert, and M. Brunner Import of carrier proteins into the mitochondrial inner membrane mediated by Tim22 Nature 384 1996 582 585
48. C.M. Koehler The small Tim proteins and the twin Cx3C motif Trends Biochem. Sci. 29 2004 1 4
49. P. Rehling, K. Model, K. Brandner, P. Kovermann, A. Sickmann, H.E. Meyer, W. Kuhlbrandt, R. Wagner, K.N. Truscott, and N. Pfanner Protein insertion into the mitochondrial inner membrane by a twin-pore translocase Science 299 2003 1747 1751
50. J. Luirink, T. Samuelsson, and J.W. de Gier YidC/Oxa1p/Alb3: evolutionarily conserved mediators of membrane protein assembly FEBS Lett. 501 2001 1 5
51. L. Jia, M. Dienhart, M. Schramp, M. McCauley, K. Hell, and R.A. Stuart Yeast Oxa1 interacts with mitochondrial ribosomes: the importance of the C-terminal region of Oxa1 EMBO J. 22 2003 6438 6447
52. G. Szyrach, M. Ott, N. Bonnefoy, W. Neupert, and J.M. Herrmann Ribosome binding to the Oxa1 complex facilitates co-translational protein insertion in mitochondria EMBO J. 22 2003 6448 6457
53. K. Hell, W. Neupert, and R.A. Stuart Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA EMBO J. 20 2001 1281 1288
54. K. Hell, J. Herrmann, E. Pratje, W. Neupert, and R.A. Stuart Oxa1p mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space FEBS Lett. 418 1997 367 370
55. S.A. Saracco, and T.D. Fox Cox18p is required for export of the mitochondrially encoded Saccharomyces cerevisiae Cox2p C-tail and interacts with Pnt1p and Mss2p in the inner membrane Mol. Biol. Cell 13 2002 1122 1131
56. U. Wienhues, K. Becker, M. Schleyer, B. Guiard, M. Tropschug, A.L. Horwich, N. Pfanner, and W. Neupert Protein folding causes an arrest of preprotein translocation into mitochondria in vivo J. Cell Biol. 115 1991 1601 1609
57. P.J. Dekker, F. Martin, A.C. Maarse, U. Bomer, H. Muller, B. Guiard, M. Meijer, J. Rassow, and N. Pfanner The Tim core complex defines the number of mitochondrial translocation contact sites and can hold arrested preproteins in the absence of matrix Hsp70-Tim44 EMBO J. 16 1997 5408 5419
58. H. Yamamoto, M. Esaki, T. Kanamori, Y. Tamura, S. Nishikawa, and T. Endo Tim50 is a subunit of the TIM23 complex that links protein translocation across the outer and inner mitochondrial membranes Cell 111 2002 519 528
59. A. Chacinska, P. Rehling, B. Guiard, A.E. Frazier, A. Schulze-Specking, N. Pfanner, W. Voos, and C. Meisinger Mitochondrial translocation contact sites: separation of dynamic and stabilizing elements in formation of a TOM-TIM-preprotein supercomplex EMBO J. 22 2003 5370 5381
60. D. Mokranjac, D. Popov-Celeketic, K. Hell, and W. Neupert Role of Tim21 in mitochondrial translocation contact sites J. Biol. Chem. 280 2005 23437 23440
61. R. Albrecht, P. Rehling, A. Chacinska, J. Brix, S.A. Cadamuro, R. Volkmer, B. Guiard, N. Pfanner, and K. Zeth The Tim21 binding domain connects the preprotein translocases of both mitochondrial membranes EMBO Rep. 7 2006 1233 1238
62. Y. Tamura, Y. Harada, T. Shiota, K. Yamano, K. Watanabe, M. Yokota, H. Yamamoto, H. Sesaki, and T. Endo Tim23-Tim50 pair coordinates functions of translocators and motor proteins in mitochondrial protein import J. Cell Biol. 184 2009 129 141
63. M. Bohnert, P. Rehling, B. Guiard, J.M. Herrmann, N. Pfanner, and M. van der Laan Cooperation of stop-transfer and conservative sorting mechanisms in mitochondrial protein transport Curr. Biol. 20 2010 1227 1232
64. J. Dukanovic, K.S. Dimmer, N. Bonnefoy, K. Krumpe, and D. Rapaport Genetic and functional interactions between the mitochondrial outer membrane proteins Tom6 and Sam37 Mol. Cell. Biol. 29 2009 5975 5988
65. T. Becker, B. Guiard, N. Thornton, N. Zufall, D.A. Stroud, N. Wiedemann, and N. Pfanner Assembly of the mitochondrial protein import channel: role of Tom5 in two-stage interaction of Tom40 with the SAM complex Mol. Biol. Cell 21 2010 3106 3113
66. C. Meisinger, N. Wiedemann, M. Rissler, A. Strub, D. Milenkovic, B. Schonfisch, H. Muller, V. Kozjak, and N. Pfanner Mitochondrial protein sorting: differentiation of beta-barrel assembly by Tom7-mediated segregation of Mdm10 J. Biol. Chem. 281 2006 22819 22826
67. K. Yamano, S. Tanaka-Yamano, and T. Endo Mdm10 as a dynamic constituent of the TOB/SAM complex directs coordinated assembly of Tom40 EMBO Rep. 11 2010 187 193
68. I.R. Boldogh, D.W. Nowakowski, H.C. Yang, H. Chung, S. Karmon, P. Royes, and L.A. Pon A protein complex containing Mdm10p, Mdm12p, and Mmm1p links mitochondrial membranes and DNA to the cytoskeleton-based segregation machinery Mol. Biol. Cell 14 2003 4618 4627
69. M.J. Youngman, A.E. Hobbs, S.M. Burgess, M. Srinivasan, and R.E. Jensen Mmm2p, a mitochondrial outer membrane protein required for yeast mitochondrial shape and maintenance of mtDNA nucleoids J. Cell Biol. 164 2004 677 688
70. B. Kornmann, E. Currie, S.R. Collins, M. Schuldiner, J. Nunnari, J.S. Weissman, and P. Walter An ER-mitochondria tethering complex revealed by a synthetic biology screen Science 325 2009 477 481
71. K. Beyer, and B. Nuscher Specific cardiolipin binding interferes with labeling of sulfhydryl residues in the adenosine diphosphate/adenosine triphosphate carrier protein from beef heart mitochondria Biochemistry 35 1996 15784 15790
72. K. Beyer, and M. Klingenberg ADP/ATP carrier protein from beef heart mitochondria has high amounts of tightly bound cardiolipin, as revealed by 31P nuclear magnetic resonance Biochemistry 24 1985 3821 3826
73. M. Zhang, E. Mileykovskaya, and W. Dowhan Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria J. Biol. Chem. 280 2005 29403 29408
74. M. Rytomaa, and P.K. Kinnunen Evidence for two distinct acidic phospholipid-binding sites in cytochrome c J. Biol. Chem. 269 1994 1770 1774
75. S. Kutik, M. Rissler, X.L. Guan, B. Guiard, G. Shui, N. Gebert, P.N. Heacock, P. Rehling, W. Dowhan, M.R. Wenk, N. Pfanner, and N. Wiedemann The translocator maintenance protein Tam41 is required for mitochondrial cardiolipin biosynthesis J. Cell Biol. 183 2008 1213 1221
76. N. Gebert, A.S. Joshi, S. Kutik, T. Becker, M. McKenzie, X.L. Guan, V.P. Mooga, D.A. Stroud, G. Kulkarni, M.R. Wenk, P. Rehling, C. Meisinger, M.T. Ryan, N. Wiedemann, M.L. Greenberg, and N. Pfanner Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: implications for Barth syndrome Curr. Biol. 19 2009 2133 2139
77. Y. Tamura, T. Endo, M. Iijima, and H. Sesaki Ups1p and Ups2p antagonistically regulate cardiolipin metabolism in mitochondria J. Cell Biol. 185 2009 1029 1045
78. Y. Tamura, Y. Harada, K. Yamano, K. Watanabe, D. Ishikawa, C. Ohshima, S. Nishikawa, H. Yamamoto, and T. Endo Identification of Tam41 maintaining integrity of the TIM23 protein translocator complex in mitochondria J. Cell Biol. 174 2006 631 637
79. E. Zinser, C.D. Sperka-Gottlieb, E.V. Fasch, S.D. Kohlwein, F. Paltauf, and G. Daum Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae J. Bacteriol. 173 1991 2026 2034
80. R. Schneiter, B. Brugger, R. Sandhoff, G. Zellnig, A. Leber, M. Lampl, K. Athenstaedt, C. Hrastnik, S. Eder, G. Daum, F. Paltauf, F.T. Wieland, and S.D. Kohlwein 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 1999 741 754
81. R.E. Kellems, V.F. Allison, and R.A. Butow Cytoplasmic type 80S ribosomes associated with yeast mitochondria. IV. Attachment of ribosomes to the outer membrane of isolated mitochondria J. Cell Biol. 65 1975 1 14
82. R.E. Kellems, V.F. Allison, and R.A. Butow Cytoplasmic type 80 S ribosomes associated with yeast mitochondria. II. Evidence for the association of cytoplasmic ribosomes with the outer mitochondrial membrane in situ J. Biol. Chem. 249 1974 3297 3303
83. R. George, P. Walsh, T. Beddoe, and T. Lithgow The nascent polypeptide-associated complex (NAC) promotes interaction of ribosomes with the mitochondrial surface in vivo FEBS Lett. 516 2002 213 216
84. M. Garcia, X. Darzacq, T. Delaveau, L. Jourdren, R.H. Singer, and C. Jacq Mitochondria-associated yeast mRNAs and the biogenesis of molecular complexes Mol. Biol. Cell 18 2007 362 368
85. P. Marc, A. Margeot, F. Devaux, C. Blugeon, M. Corral-Debrinski, and C. Jacq Genome-wide analysis of mRNAs targeted to yeast mitochondria EMBO Rep. 3 2002 159 164
86. E. Eliyahu, L. Pnueli, D. Melamed, T. Scherrer, A.P. Gerber, O. Pines, D. Rapaport, and Y. Arava Tom20 mediates localization of mRNAs to mitochondria in a translation-dependent manner Mol. Cell. Biol. 30 2010 284 294
87. T. Quenault, T. Lithgow, and A. Traven PUF proteins: repression, activation and mRNA localization Trends Cell Biol. 21 2011 104 112
88. L.J. Garcia-Rodriguez, A.C. Gay, and L.A. Pon Puf3p, a Pumilio family RNA binding protein, localizes to mitochondria and regulates mitochondrial biogenesis and motility in budding yeast J. Cell Biol. 176 2007 197 207
89. I. Stein, Y. Peleg, S. Even-Ram, and O. Pines The single translation product of the FUM1 gene (fumarase) is processed in mitochondria before being distributed between the cytosol and mitochondria in Saccharomyces cerevisiae Mol. Cell. Biol. 14 1994 4770 4778