Coupling of mitochondrial translation with the formation of respiratory complexes in yeast mitochondria

Acta Biochimica Polonica

Volumn 47, Issue 4, 2000, Pages 973-991

  Chacińska, Agnieszka ^a   Boguta, Magdalena ^a  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

Mitochondrial inner membrane; Mitochondrial ribosomes; Mitochondrial translation; Saccharomyces cerevisiae; Translational activators

Indexed keywords

BIOLOGICAL MODEL; ELECTRON TRANSPORT; METABOLISM; MITOCHONDRION; PHYSIOLOGY; PROTEIN SYNTHESIS; REVIEW; SACCHAROMYCES CEREVISIAE;

ELECTRON TRANSPORT; MITOCHONDRIA; MODELS, BIOLOGICAL; PROTEIN BIOSYNTHESIS; SACCHAROMYCES CEREVISIAE;

EID: 0347574101     PISSN: 0001527X     EISSN: None     Source Type: Journal    
DOI: 10.18388/abp.2000_3952     Document Type: Article

References (125)

1. Ackerman, S.H. & Tzagoloff, A. (1990) ATP 10, a yeast nuclear gene required for the assembly of the mitochondrial F1-F0 complex. J. Biol. Chem. 265, 9952-9959.
2. Ackerman, S.H., Martin, J. & Tzagoloff, A. (1992) Characterization of ATP11 and detection of the encoded protein in mitochondria of Saccharomyces cerevisiae. J. Biol. Chem. 267, 7386-7394.
3. Altamura, N., Capitanio, N., Bonnefoy, N., Papa, S. & Dujardin, G. (1996) The Saccharomyces cerevisiae OXA1 gene is required for the correct assembly of cytochrome c oxidase and oligomycin-sensitive ATP synthase. FEBS Lett. 382, 111-115.
4. Arnold, I., Pfeiffer, K., Neupert, W., Stuart, R.A. & Schägger, H. (1999) ATP synthase of yeast mitochondria. Isolation of subunit j and disruption of the ATP18 gene. J. Biol. Chem. 274, 36-40.
5. Arlt, H., Tauer, R., Feldmann, H., Neupert, W. & Langer, T. (1996) The YTA10-12 complex, an AAA protease with chaperone-like activity in the inner membrane of mitochondria. Cell 85, 875-885.
6. Arlt, H., Steglich, G., Perryman, R., Guiard, B., Neupert, W. & Langer, T. (1998) The formation of respiratory chain complexes in mitochondria is under the proteolytic control of the m-AAA protease. EMBO J. 17, 4837-4847.
7. Bauer, M., Behrens, M., Esser, K., Michaelis, G. & Pratje, E. (1994) PET1402, a nuclear gene required for proteolytic processing of cytochrome oxidase subunit 2 in yeast. Mol. Gen. Genet. 245, 272-278.
8. Bauerfeind, M., Esser, K. & Michaelis, G. (1998) The Saccharomyces cerevisiae SOM1 gene: Heterologous complementation studies, homologues in other organisms, and association of the gene product with the inner mitochondrial membrane. Mol. Gen. Genet. 257, 635-640.
9. Behrens, M., Michaelis, G. & Pratje, E. (1991) Mitochondrial inner membrane protease 1 of Saccharomyces cerevisiae shows sequence similarity to the Escherichia coli leader peptidase. Mol. Gen. Genet. 228, 167-176.
10. Biswas, T.K. & Getz, G.S. (1999) The single amino acid changes in the yeast mitochondrial S4 ribosomal protein cause temperature-sensitive defect in the accumulation of mitochondrial 15S rRNA. Biochemistry 38, 13042-13054.
11. Boguta, M., Dmochowska, A., Borsuk, P., Wrobel, K., Gargouri, A., Lazowska, J., Slonimski, P.P., Szczesniak, B. & Kruszewska, A. (1992) NAM9 nuclear suppressor of mitochondrial ochre mutations in Saccharomyces cerevisiae codes for a protein homologous to S4 ribosomal proteins from chloroplasts, bacteria, and eucaryotes. Mol. Cell. Biol. 12, 402-412.
12. Boguta, M., Chacinska, A., Murawski, M. & Szczesniak, B. (1997) Expression of the yeast NAM9 gene coding for mitochondrial ribosomal protein. Acta Biochim. Polon. 44, 251-258.
13. Bonnefoy, N. & Fox, T.D. (2000) In vivo analysis of mutated initiation codons in the mitochondrial COX2 gene of Saccharomyces cerevisiae fused to the reporter gene ARG8m reveals lack of downstream reinitiation. Mol. Gen. Genet. 262, 1036-1046.
14. Bonnefoy, N., Kermorgant, M., Groudinsky, O., Minet, M., Slonimski, P.P. & Dujardin, G. (1994a) Cloning of a human gene involved in cytochrome oxidase assembly by functional complementation of an oxa1-mutation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 91, 11978-11982.
15. Bonnefoy, N., Chalvet, F., Hamel, P., Slonimski, P.P. & Dujardin, G. (1994b) OXA1, a Saccharomyces cerevisiae nuclear gene whose sequence is conserved from prokaryotes to eukaryotes controls cytochrome oxidase biogenesis. J. Mol. Biol. 239, 201-212.
16. Borst, P. & Grivell, L.A. (1971) Mitochondrial ribosomes. FEBS Lett. 13, 73-88.
17. Bousquet, I., Dujardin, G. & Slonimski, P.P. (1991) ABC1, a novel yeast nuclear gene has a dual function in mitochondria: It suppresses a cytochrome b mRNA translation defect and is essential for the electron transfer in the bc 1 complex. EMBO J. 10, 2023-2031.
18. Bowman, S., Ackerman, S.H., Griffiths, D.E. & Tzagoloff, A. (1991) Characterization of ATP12, a yeast nuclear gene required for the assembly of the mitochondrial F1-ATPase. J. Biol. Chem. 266, 7517-7523.
19. 1 complex and the neighbouring complexes II and IV in the mitochondrial respiratory chain. Eur. J. Biochem. 246, 103-111.
20. Brown, N.G., Costanzo, M.C. & Fox, T.D. (1994) Interactions among three proteins that specifically activate translation of the mitochondrial COX3 mRNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 1045-1053.
21. Bunn, C.L., Mitchell, C.H., Lukins, H.B. & Linnane, A.W. (1970) A new class of cytoplasmically determined antibiotic resistant mutants in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 67, 1233-1240.
22. Chacinska, A., Boguta, M., Krzewska, J. & Rospert, S. (2000) Prion dependent switching between respiratory competence and deficiency in the yeast nam9-1 mutant. Mol. Cell. Biol. 20, 7220-7229.
23. Church, C., Chapon, C. & Poyton, R.O. (1996) Cloning and characterization of PET100, a gene required for the assembly of yeast cytochrome c oxidase. J. Biol. Chem. 271, 18499-18450.
24. Colby, G., Wu, M. & Tzagoloff, A. (1998) MTO1 codes for a mitochondrial protein required for respiration in paromomycin-resistant mutants of Saccharomyces cerevisiae. J. Biol. Chem. 273, 27945-27952.
25. Costanzo, M.C. & Fox, T.D. (1988) Specific translational activation by nuclear gene products occurs in the 5′ untranslated leader of a yeast mitochondrial mRNA. Proc. Natl. Acad. Sci. U.S.A. 85, 2677-2681.
26. Costanzo, M.C. & Fox, T.D. (1990) Control of mitochondrial gene expression in Saccharomyces cerevisiae. Annu. Rev. Genet. 24, 91-113.
27. Costanzo, M.C. & Fox, T.D. (1993) Suppression of a defect in the 5′ untranslated leader of mitochondrial COX3 mRNA by a mutation affecting an mRNA-specific translational activator protein. Mol. Cell. Biol. 13, 4806-4813.
28. Crivellone, M.D. (1994) Characterization of CBP4, a new gene essential for the expression of ubiquinol-cytochrome c reductase in Saccharomyces cerevisiae. J. Biol. Chem. 269, 21284-21292.
29. Decoster, E., Simon, M., Hatat, D. & Faye, G. (1990) The MSS51 gene product is required for the translation of the COX1 mRNA in yeast mitochondria. Mol. Gen. Genet. 224, 111-118.
30. Decoster, E., Vassal, A. & Faye, G. (1993) MSS1, a nuclear-encoded mitochondrial GTPase involved in the expression of COX1 subunit of cytochrome c oxidase. J. Mol. Biol. 232, 79-88.
31. Dieckmann, C.L. & Staples, R.R. (1994) Regulation of mitochondrial gene expression in Saccharomyces cerevisiae. Mol. Cell. Biol. 7, 177-184.
32. Dieckmann, C.L. & Tzagoloff, A. (1985) Assembly of the mitochondrial membrane system. CBP6, a yeast nuclear gene necessary for synthesis of cytochrome b. J. Biol. Chem. 260, 1513-1520.
33. Dmochowska, A., Konopinska, A., Krzymowska, M., Szczesniak, B. & Boguta, M. (1995) The NAM9-1 suppressor mutation in a nuclear gene encoding ribosomal mitochondrial protein of Saccharomyces cerevisiae. Gene 162, 81-85.
34. Dunstan, H.M., Green-Willms, N.S. & Fox, T.D. (1997) In vivo analysis of Saccharomyces cerevisiae COX2 mRNA 5′-untranslated leader functions in mitochondrial translation initiation and translational activation. Genetics 147, 87-100.
35. Esser, K., Pratje, E. & Michaelis, G. (1996) SOM1, a small new gene required for mitochondrial inner membrane peptidase function in Saccharomyces cerevisiae. Mol. Gen. Genet. 252, 437-445.
36. Folley, L.S. & Fox, T.D. (1994) Reduced dosage of genes encoding ribosomal protein S18 suppresses a mitochondrial initiation codon mutation in Saccharomyces cerevisiae. Genetics 137, 369-379.
37. Fox, T.D. (1996a) Genetics of mitochondrial translation; in Translational Control, pp. 733-758, Cold Spring Harbor Laboratory Press.
38. Fox, T.D. (1996b) Translational control of endogenous and recoded nuclear genes in yeast mitochondria: Regulation and membrane targeting. Experientia 52, 1130-1135.
39. Fox, T.D. & Weiss-Brummer, B. (1980) Leaky +1 and -1 frameshift mutations at the same site in a yeast mitochondrial gene. Nature 288, 60-63.
40. Glerum, D.M. & Tzagoloff, A. (1994) Isolation of a human cDNA for heme A:farnesyltransferase by functional complementation of a yeast cox10 mutant. Proc. Natl. Acad. Sci. U.S.A. 91, 8452-8456.
41. Glerum, D.M., Koerner, T.J. & Tzagoloff, A. (1995) Cloning and characterization of COX14, whose product is required for assembly of yeast cytochrome oxidase J. Biol. Chem. 270, 15585-15590.
42. Glerum, D.M., Shtanko, A. & Tzagoloff, A. (1996a) SCO1 and SCO2 act as high copy suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae. J. Biol. Chem. 271, 20531-20535.
43. Glerum, D.M., Shtanko, A. & Tzagoloff, A. (1996b) Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J. Biol. Chem. 271, 14504-14509.
44. Glerum, D.M., Muroff, I., Jin, C. & Tzagoloff, A. (1997) COX15 codes for a mitochondrial protein essential for the assembly of yeast cytochrome oxidase. J. Biol. Chem. 272, 19088-19094.
45. Graack, H.R. & Wittmann-Liebold, B. (1998) Mitochondrial ribosomal proteins (MRPs) of yeast. Biochem. J. 329, 433-448.
46. Green-Willms, N.S., Fox, T.D. & Costanzo, M.C. (1998) Functional interactions between yeast mitochondrial ribosomes and mRNA 5′ untranslated leaders. Mol. Cell. Biol. 18, 1826-1834.
47. Grivell, L.A. (1995) Nucleo-mitochondrial interactions in mitochondrial gene expression. Crit. Rev. Biochem. Mol. Biol. 30, 121-164.
48. Grivell, L.A., Artal-Sanz, M., Hakkaart, G., de Jong, L., Nijtmans, L.G., van Oosterum, K., Siep, M. & van der Spek, H. (1999) Mitochondrial assembly in yeast. FEBS Lett. 452, 57-60.
49. Guzelin, E., Rep, M. & Grivell, L.A. (1996) Afg3p, a mitochondrial ATP-dependent metalloprotease, is involved in degradation of mitochondrially-encoded Cox1, Cox3, Cob, Su6, Su8 and Su9 subunits of the inner membrane complexes III, IV and V. FEBS Lett. 381, 42-46.
50. Haffter, P., McMullin, T.W. & Fox, T.D. (1990) A genetic link between an mRNA-specific translational activator and the translation system in yeast mitochondria. Genetics 125, 495-503.
51. Haffter, P., McMullin, T.W. & Fox, T.D. (1991) Functional interactions among two yeast mitochondrial ribosomal proteins and an mRNA-specific translational activator. Genetics 127, 319-326.
52. Haffter, P. & Fox, T.D. (1992) Suppression of carboxy-terminal truncations of the yeast mitochondrial mRNA-specific translational activator PET122 by mutations in two new genes, MRP17 and PET127. Mol. Gen. Genet. 235, 64-73.
53. 5 reductase to two different submitochondrial compartments. Cell 79, 829-839.
54. 1. Genetics 150, 601-611.
55. He, S. & Fox, T.D. (1997) Membrane translocation of mitochondrially coded Cox2p: Distinct requirements for export of N and C termini and dependence on the conserved protein Oxa1p. Mol. Biol. Cell 8, 1449-1460.
56. He, S. & Fox, T.D. (1999) Mutations affecting a yeast mitochondrial inner membrane protein, pntlp, block export of a mitochondrially synthesized fusion protein from the matrix. Mol. Cell. Biol. 19, 6598-6607.
57. Hell, K., Herrmann, J., Pratje, E., Neupert, W. & Stuart, R.A. (1997) Oxa1p mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space. FEBS Lett. 418, 367-370.
58. Hell, K., Herrmann, J.M., Pratje, E., Neupert, W. & Stuart, R.A. (1998) Oxa1p, an essential component of the N-tail protein export machinery in mitochondria. Proc. Natl. Acad. Sci. U.S.A. 95, 2250-2255.
59. Hell, K., Tzagoloff, A., Neupert, W. & Stuart, R.A. (2000) Identification of Cox20p, a novel protein involved in the maturation and assembly of cytochrome oxidase subunit 2. J. Biol. Chem. 275, 4571-4578.
60. Herrmann, J.M., Neupert, W. & Stuart, R.A. (1997) Insertion into the mitochondrial inner membrane of a polytopic protein, the nuclear-encoded Oxa1p. EMBO J. 16, 2217-2226.
61. Hiser, L., Di Valentin, M., Hamer, A.G. & Hosler, J.P. (2000) Cox11p is required for stable formation of the Cu(B) and magnesium centers of cytochrome c oxidase. J. Biol. Chem. 275, 619-623.
62. Hudspeth, M.E., Ainley, W.M., Shumard, D.S., Butow, R.A. & Grossman, L.I. (1982) Location and structure of the var1 gene on yeast mitochondrial DNA: Nucleotide sequence of the 40.0 allele. Cell 30, 617-626.
63. Kermorgant, M., Bonnefoy, N. & Dujardin, G. (1997) Oxa1p, which is required for cytochrome c oxidase and ATP synthase complex formation, is embedded in the mitochondrial inner membrane. Curr. Genet. 31, 302-307.
64. Leonhard, K., Herrmann, J.M., Stuart, R.A., Mannhaupt, G., Neupert, W. & Langer, T. (1996) AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO J. 15, 4218-4229.
65. Mason, T.L.., Pan, C., Sanchirico, M.E. & Sirum-Connolly, K. (1996) Molecular genetics of the peptidyl transferase center and the unusual Var1 protein in yeast mitochondrial ribosomes. Experientia 121, 1148-1156.
66. Manthey, G.M. & McEwen, J.E. (1995) The product of the nuclear gene PET309 is required for translation of mature mRNA and stability or production of intron-containing RNAs derived from the mitochondrial COX1 locus of Saccharomyces cerevisiae. EMBO J. 14, 4031-4043.
67. Manthey, G.M., Przybyla-Zawislak, B.D. & McEwen, J.E. (1998) The Saccharomyces cerevisiae Pet309 protein is embedded in the mitochondrial inner membrane. Eur. J. Biochem. 155, 156-161.
68. Marzuki, S. & Hibbs, A.R. (1986) Are all mitochondrial translation products synthesized on membrane-bound ribosomes? Biochim. Biophys. Acta 866, 120-124.
69. McEwen, J.E., Hong, K.H., Park, S. & Preciado, G.T. (1993) Sequence and chromosomal localization of two PET genes required for cytochrome c oxidase assembly in Saccharomyces cerevisiae. Curr. Genet. 23, 9-14.
70. McKee, E.E. & Poyton, R.O. (1984) Mitochondrial gene expression in Saccharomyces cerevisiae. I. Optimal conditions for protein synthesis in isolated mitochondria. J. Biol. Chem. 259, 9320-9331.
71. McMullin, T.W. & Fox, T.D. (1993) COX3 mRNA-specific translational activator proteins are associated with the inner mitochondrial membrane in Saccharomyces cerevisiae. J. Biol. Chem. 268, 11737-11741.
72. McMullin, T.W., Haffter, P. & Fox, T.D. (1990) A novel small-subunit ribosomal protein of yeast mitochondria that interacts functionally with an mRNA-specific translational activator. Mol. Cell. Biol. 10, 4590-4595.
73. Meyer, W., Bomer, U. & Pratje, E. (1997) Mitochondrial inner membrane bound Pet1402 protein is rapidly imported into mitochondria and affects the integrity of the cytochrome oxidase and ubiquinol-cytochrome c oxidoreductase complexes. Biol. Chem. 378, 1373-1379.
74. Michaelis, U. & Rodel, G. (1990) Identification of CBS2 as a mitochondrial protein in Saccharomyces cerevisiae. Mol. Gen. Genet. 223, 394-400.
75. Michaelis, U., Korte, A. & Rodel, G. (1991) Association of cytochrome b translational activator proteins with the mitochondrial membrane: Implications for cytochrome b expression in yeast. Mol. Gen. Genet. 230, 177-185.
76. Mittelmeier, T.M. & Dieckmann, C.L. (1995) In vivo analysis of sequences required for translation of cytochrome b transcripts in yeast mitochondria. Mol. Cell. Biol. 15, 780-789.
77. Mulero, J.J. & Fox, T.D. (1993a) PET111 acts in the 5′-leader of the Saccharomyces cerevisiae mitochondrial COX2 mRNA to promote its translation. Genetics 133, 509-516.
78. Mulero, J.J. & Fox, T.D. (1993b) Alteration of the Saccharomyces cerevisiae COX2 mRNA 5′-untranslated leader by mitochondrial gene replacement and functional interaction with the ftranslational activator protein PET111. Mol. Biol. Cell, 4, 1327-1335.
79. Mulero, J.J. & Fox, T.D. (1994) Reduced but accurate translation from a mutant AUA initiation codon in the mitochondrial COX2 mRNA of Saccharomyces cerevisiae. Mol. Gen. Genet. 242, 383-390.
80. Mulero, J.J., Rosenthal, J.K. & Fox, T.D. (1994) PET112, a Saccharomyces cerevisiae nuclear gene required to maintain rho+ mitochondrial DNA. Curr. Genet. 25, 299-304.
81. Myers, A.M., Pape, L.K. & Tzagoloff, A. (1985) Mitochondrial protein synthesis is required for maintenance of intact mitochondrial genomes in Saccharomyces cerevisiae. EMBO J. 4, 2087-2092.
82. Nagata, S., Tsunetsungu-Yokota, Y., Naito, A. & Kaziro, Y. (1983) Molecular cloning and sequence determination of the nuclear gene coding for mitochondrial elongation factor Tu of S. cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 80, 6192-6196.
83. Nakai, T., Yasuhara, T., Fujiki, Y. & Ohashi, A. (1995) Multiple genes, including a member of the AAA family, are essential for degradation of unassembled subunit 2 of cytochrome c oxidase in yeast mitochondria. Mol. Cell. Biol. 15, 4441-4452.
84. Nijtmans, L.G., de Jong, L., Artal Sanz, M., Coates, P.J., Berden, J.A., Back, J.W., Muijsers, A.O., van der Spek, H. & Grivell, L.A. (2000) Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J. 19, 2444-2451.
85. Nobrega, M.P., Nobrega, F.G. & Tzagoloff, A. (1990) COX10 codes for a protein homologous to the ORF1 product of Paracoccus denitrificans and is required for the synthesis of yeast cytochrome oxidase. J. Biol. Chem. 265, 14220-14226.
86. Nobrega, F.G., Nobrega, M.P. & Tzagoloff, A. (1992) BCS1, a novel gene required for the expression of functional Rieske iron-sulfur protein in Saccharomyces cerevisiae. EMBO J. 11, 3821-3829.
87. Nunnari, J., Fox, T.D. & Walter, P. (1993) A mitochondrial protease with two catalytic subunits of nonoverlapping specificities. Science 262, 1997-2004.
88. Pajic, A., Tauer, R., Feldmann, H., Neupert, W. & Langer, T. (1994) Yta10p is required for the ATP-dependent degradation of polypeptides in the inner membrane of mitochondria. FEBS Lett. 353, 201-206.
89. Paul, M.F. & Tzagoloff, A. (1995) Mutations in RCA1 and AFG3 inhibit F1-ATPase assembly in Saccharomyces cerevisiae. FEBS Lett. 373, 66-70.
90. Pel, H.J. & Grivell, L.A. (1994) Protein synthesis in mitochondria. Mol. Biol. Rep. 19, 183-194.
91. Pel, H.J., Tzagoloff, A. & Grivell, L.A. (1992a) The identification of 18 nuclear genes required for the expression of the yeast mitochondrial gene encoding cytochrome c oxidase subunit 1. Curr. Genet. 21, 139-146.
92. Pel, H.J., Maat, C., Rep, M. & Grivell, L.A. (1992b) The yeast nuclear gene MRF1 encodes a mitochondrial peptide chain release factor and cures several mitochondrial RNA splicing defects. Nucleic Acids Res. 20, 6339-6346.
93. Pel, H.J., Rep, M., Dubbink, H.J. & Grivell, L.A. (1993) Single point mutations in domain II of the yeast mitochondrial release factor mRF-1 affect ribosome binding. Nucleic Acids Res. 21, 5308-5315.
94. Poyton, R.O., Duhl, D.M.J. & Clarkson, G.H.D. (1992) Protein export from the mitochondrial matrix. Trends Cell. Biol. 2, 369-375.
95. Poyton, R.O., Goehring, B., Droste, M., Sevarino, K.A., Allen, L.A. & Zhao, X.J. (1995) Cytochrome-c oxidase from Saccharomyces cerevisiae. Methods Enzymol. 260, 97-116.
96. Pratje, E. & Guiard, B. (1986) One nuclear gene controls the removal of transient pre-sequences from two yeast proteins: One encoded by the nuclear the other by the mitochondrial genome. EMBO J. 5, 1313-1317.
97. Rentzsch, A., Krummeck-Weiss, G., Hofer, A., Bartuschka, A., Ostermann, K. & Rodel, G. (1999) Mitochondrial copper metabolism in yeast: Mutational analysis of Sco1p involved in the biogenesis of cytochrome c oxidase. Curr. Genet. 35, 103-108.
98. Rep, M. & Grivell, L.A. (1996) MBA1 encodes a mitochondrial membrane-associated protein required for biogenesis of the respiratory chain. FEBS Lett. 388, 185-188.
99. Rep, M., Nooy, J., Guelin, E. & Grivell, L.A. (1996) Three genes for mitochondrial proteins suppress null-mutations in both Afg3 and Rca1 when over-expressed. Curr. Genet. 30, 206-211.
100. Rodel, G. (1986) Two yeast nuclear genes, CBS1 and CBS2, are required for translation of mitochondrial transcripts bearing the 5′-untranslated COB leader. Curr. Genet. 11, 41-45.
101. Rodel, G. (1997) Translational activator proteins required for cytochrome b synthesis in Saccharomyces cerevisiae. Curr. Genet. 31, 375-379.
102. Rodel, G. & Fox, T.D. (1987) The yeast nuclear gene CBS1 is required for translation of mitochondrial mRNAs bearing the cob 5′ untranslated leader. Mol. Gen. Genet. 206, 45-50.
103. Rojo, E.E., Guiard, B., Neupert, W. & Stuart, R.A. (1999) N-terminal tail export from the mitochondrial matrix. Adherence to the prokaryotic "positive-inside" rule of membrane protein topology. J. Biol. Chem. 274, 19617-19622.
104. Rosenthal, L.P. & Bodley, J.W. (1987) Purification and characterization of Saccharomyces cerevisiae mitochondrial elongation factor Tu. J. Biol. Chem. 262, 10955-10959.
105. Sanchirico, M.E., Fox, T.D. & Mason, T.L. (1998) Accumulation of mitochondrially synthesized Saccharomyces cerevisiae Cox2p and Cox3p depends on targeting information in untranslated portions of their mRNAs. EMBO J. 17, 5796-5804.
106. Schneider, A., Behrens, M., Scherer, P., Pratje, E., Michaelis, G. & Schatz, G. (1991) Inner membrane protease I, an enzyme mediating intramitochondrial protein sorting in yeast. EMBO J. 10, 247-254.
107. Sevarino, K.A. & Poyton, R.O. (1980) Mitochondrial membrane biogenesis: Identification of a precursor to yeast cytochrome c oxidase subunit II, an integral polypeptide. Proc. Natl. Acad. Sci. U.S.A. 77, 142-146.
108. Snyers, L., Umlauf, E. & Prohaska, R. (1998) Oligomeric nature of the integral membrane protein stomatin. J. Biol. Chem. 273, 17221-17226.
109. Spithill, T.W., Trembath, M.K., Lukins, H.B. & Linnane, A.W. (1978) Mutations of the mitochondrial DNA of Saccharomyces cerevisiae which affect the interaction between mitochondrial ribosomes and the inner mitochondrial membrane. Mol. Gen. Genet. 164, 155-162.
110. Steele, D.F., Butler, C.A. & Fox, T.D. (1996) Expression of a recoded nuclear gene inserted into yeast mitochondrial DNA is limited by mRNA-specific translational activation. Proc. Natl. Acad. Sci. U.S.A. 93, 5253-5257.
111. Steglich, G., Neupert, W. & Langer, T. (1999) Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol. Cell. Biol. 19, 3435-3442.
112. Suzuki, C.K., Rep, M., van Dijl, J.M., Suda, K., Grivell, L.A. & Schatz, G. (1997) ATP-dependent proteases that also chaperone protein biogenesis. Trends Biochem. Sci. 22, 118-123.
113. Thorsness, P.E., White, K.H. & Fox, T.D. (1993) Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae. Mol. Cell. Biol. 13, 5418-5426.
114. Tokatlidis, K. & Schatz, G. (1999) Biogenesis of mitochondrial inner membrane proteins. J. Biol. Chem. 274, 35285-35288.
115. Torello, A.T., Overholtzer, M.H., Cameron, V.L., Bonnefoy, N. & Fox, T.D. (1997) Deletion of the leader peptide of the mitochondrially encoded precursor of Saccharomyces cerevisiae cytochrome c oxidase subunit II. Genetics 145, 903-910.
116. Tzagoloff, A., Nobrega, M., Gorman, N. & Sinclair, P. (1993) On the functions of the yeast COX10 and COX11 gene products. Biochem. Mol. Biol. Int. 31, 593-598.
117. Vambutas, A., Ackerman, S.H. & Tzagoloff, A. (1991) Mitochondrial translational-initiation and elongation factors in Saccharomyces cereuisiae. Eur. J. Biochem. 201, 643-652.
118. Wang, Z.G. & Ackerman, S.H. (1998) Mutational studies with Atp12p, a protein required for assembly of the mitochondrial F1-ATPase in [yeast. Identification of domains important for atp12p function and oligomerization. J. Biol. Chem. 273, 2993-3002.
119. Wang, Z.G. & Ackerman, S.H. (2000) The assembly factor Atp11p binds to the beta-subunit of the mitochondrial F(1)-ATPase. J. Biol. Chem. 275, 5767-5772.
120. Wȩgierski, T., Dmochowska, A., Jablonowska, A., Dziembowski, A., Bartnik, E. & Stȩpien, P.P. (1998) Yeast nuclear PET127 gene can suppress deletions of the SUV3 or DSS1 genes: An indication of a functional interaction between 3′ and 5′ ends of mitochondrial mRNAs. Acta Biochim. Polon. 45, 935-940.
121. Wiesenberger, G. & Fox, T.D. (1997) Pet127, a membrane-associated protein involved in stability and processing of Saccharomyces cerevisiae mitochondrial RNAs. Mol. Cell. Biol. 17, 2816-2824.
122. Wiesenberger, G., Costanzo, M.C. & Fox, T.D. (1995) Analysis of the Saccharomyces cerevisiae mitochondrial COX3 mRNA 5′ untranslated leader: Translational activation and mRNA processing. Mol. Cell. Biol. 15, 3291-3300.
123. Weiss-Brummer, B. & Huttenhofer, A. (1989) The paromomycin resistance mutation (parr-454) in the 15 S rRNA gene of the yeast Saccharomyces cerevisiae is involved in ribosomal frameshifting. Mol. Gen. Genet. 217, 362-369.
124. Weiss, R.B., Murphy, J.P. & Gallant, J.A. (1984) Genetic screen for cloned release factor genes. J. Bacteriol. 158, 362-364.
125. Wu, M. & Tzagoloff, A. (1989) Identification and characterization of a new gene (CBP3) required for the expression of yeast coenzyme QH2-cytochrome c reductase. J. Biol. Chem. 264, 11122-11130.