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

• Authors: Agnieszka Chacińska , Magdalena Boguta
• Languages of publication: EN

Abstracts

EN

In contrast to most other eukaryotic organisms, yeast can survive without respiration. This ability has been exploited to investigate nuclear genes required for expression of mitochondrial DNA. Availability of complete Saccharomyces cerevisiae genomic sequence has provided additional help in detailed molecular analysis. Seven of the eight major products encoded by mitochondrial DNA are hydrophobic subunits of respiratory complexes in the inner membrane. Localization of the translation process in the same cellular compartment ensures synthesis of mitochondrially encoded proteins near sites of their assembly into multimeric respiratory complexes. Association of mitochondrial ribosomes with the membrane is mediated by mRNA-specific translational activators, that are involved in the recognition of initation codon. The newly synthesized mitochondrial proteins are transferred to membrane by a specific export system. This review discusses the role of membrane-localized factors responsible for quality control and turnover of mitochondrially synthesized subunits as well as for assembly of respiratory complexes.

Keywords

EN

mitochondrial inner membrane; mitochondrial ribosomes; translational activators; mitochondrial translation; Saccharomyces cerevisiae

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2000
• Volume: 47
• Issue: 4
• Pages: 973-991

Dates

published

2000

received

2000-08-28

revised

2000-10-31

accepted

2000-11-2

Contributors

author

Agnieszka Chacińska

• Institute of Biochemistry and Biophysics, Polish Academy of Sciences, A. Pawińskiego 5A, 02-106 Warszawa, Poland

author

Magdalena Boguta

• Institute of Biochemistry and Biophysics, Polish Academy of Sciences, A. Pawińskiego 5A, 02-106 Warszawa, Poland

References

• 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.
• 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.
• 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.
• Arnold, I., Pfeiffer, K., Neupert, W., Stuart, R.A. &Schaegger, H. (1999) ATP synthase of yeast mitochondria. Isolation of subunit j and disruption of the ATP18 gene. J. Biol. Chem. 274, 36-40.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• Borst, P. &Grivell, L.A. (1971) Mitochondrial ribosomes. FEBS Lett. 13, 73-88.
• 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.
• 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.
• Brasseur, G., Tron, G., Dujardin, G., Slonimski, P.P. &Brivet-Chevillotte, P. (1997) The nuclear ABC1 gene is essential for the correct conformation and functioning of the cytochrome bc1 complex and the neighbouring complexes II and IV in the mitochondrial respiratory chain. Eur. J. Biochem. 246, 103-111.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• Costanzo, M.C. &Fox, T.D. (1990) Control of mitochondrial gene expression in Saccharomyces cerevisiae. Annu. Rev. Genet. 24, 91-113.
• 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.
• 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.
• 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.
• 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.
• Dieckmann, C.L. &Staples, R.R. (1994) Regulation of mitochondrial gene expression in Saccharomyces cerevisiae. Mol. Cell. Biol. 7, 177-184.
• 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.
• 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.
• 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.
• 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.
• 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.
• Fox, T.D. (1996a) Genetics of mitochondrial translation; in Translational Control, pp. 733-758, Cold Spring Harbor Laboratory Press.
• Fox, T.D. (1996b) Translational control of endogenous and recoded nuclear genes in yeast mitochondria: Regulation and membrane targeting. Experientia 52, 1130-1135.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• Graack, H.R. &Wittmann-Liebold, B. (1998) Mitochondrial ribosomal proteins (MRPs) of yeast. Biochem. J. 329, 433-448.
• 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.
• Grivell, L.A. (1995) Nucleo-mitochondrial interactions in mitochondrial gene expression. Crit. Rev. Biochem. Mol. Biol. 30, 121-164.
• 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.
• 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.
• 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.
• 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.
• 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.
• Hahne, K., Haucke, V., Ramage, L. &Schatz, G. (1994) Incomplete arrest in the outer membrane sorts NADH-cytochrome b5 reductase to two different submitochondrial compartments. Cell 79, 829-839.
• Hamel, P., Lemaire, C., Bonnefoy, N., Brivet- Chevillotte, P. &Dujardin, G. (1998) 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, 601-611.
• 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.
• He, S. &Fox, T.D. (1999) Mutations affecting a yeast mitochondrial inner membrane protein, pnt1p, block export of a mitochondrially synthesized fusion protein from the matrix. Mol. Cell. Biol. 19, 6598-6607.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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 52, 1148-1156.
• 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.
• 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. 255, 156-161.
• Marzuki, S. &Hibbs, A.R. (1986) Are all mitochondrial translation products synthesized on membrane-bound ribosomes? Biochim. Biophys. Acta 866, 120-124.
• 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.
• 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.
• 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.
• 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.
• 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.
• Michaelis, U. &Rodel, G. (1990) Identification of CBS2 as a mitochondrial protein in Saccharomyces cerevisiae. Mol. Gen. Genet. 223, 394-400.
• 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.
• 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.
• 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.
• 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 translational activator protein PET111. Mol. Biol. Cell, 4, 1327-1335.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• Nunnari, J., Fox, T.D. &Walter, P. (1993) A mitochondrial protease with two catalytic subunits of nonoverlapping specificities. Science 262, 1997-2004.
• 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.
• Paul, M.F. &Tzagoloff, A. (1995) Mutations in RCA1 and AFG3 inhibit F1-ATPase assembly in Saccharomyces cerevisiae. FEBS Lett. 373, 66-70.
• Pel, H.J. &Grivell, L.A. (1994) Protein synthesis in mitochondria. Mol. Biol. Rep. 19, 183-194.
• 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.
• 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.
• 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.
• Poyton, R.O., Duhl, D.M.J. &Clarkson, G.H.D. (1992) Protein export from the mitochondrial matrix. Trends Cell. Biol. 2, 369-375.
• 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.
• 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.
• 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.
• 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.
• 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.
• 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.
• Rodel, G. (1997) Translational activator proteins required for cytochrome b synthesis in Saccharomyces cerevisiae. Curr. Genet. 31, 375-379.
• 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.
• 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.
• Rosenthal, L.P. &Bodley, J.W. (1987) Purification and characterization of Saccharomyces cerevisiae mitochondrial elongation factor Tu. J. Biol. Chem. 262, 10955-10959.
• 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.
• 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.
• 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.
• Snyers, L., Umlauf, E. &Prohaska, R. (1998) Oligomeric nature of the integral membrane protein stomatin. J. Biol. Chem. 273, 17221- 17226.
• 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.
• 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.
• 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.
• 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.
• 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.
• Tokatlidis, K. &Schatz, G. (1999) Biogenesis of mitochondrial inner membrane proteins. J. Biol. Chem. 274, 35285-35288.
• 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.
• 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.
• Vambutas, A., Ackerman, S.H. &Tzagoloff, A. (1991) Mitochondrial translational-initiation and elongation factors in Saccharomyces cerevisiae. Eur. J. Biochem. 201, 643-652.
• 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.
• 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.
• Węgierski, T., Dmochowska, A., Jabłonowska, A., Dziembowski, A., Bartnik, E. &Stępien, 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.
• 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.
• 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.
• 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.
• Weiss, R.B., Murphy, J.P. &Gallant, J.A. (1984) Genetic screen for cloned release factor genes. J. Bacteriol. 158, 362-364.
• 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.