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Accumulation of the cytochrome c oxidase subunits I and II in yeast requires a mitochondrial membrane-associated protein, encoded by the nuclear SCO1 gene

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Summary

The yeast nuclear SCO1 gene is required for accumulation of the mitochondrially synthesized cytochrome c oxidase subunits I and II (COXI and COXII). We cloned and characterized the SCO1 gene. It codes for a 0.9 kb transcript. DNA sequence analysis predicts a 33 kDa protein. As shown by in vitro transcription and translation experiments in combination with import studies on isolated mitochodria, this protein is matured into a 30 kDa polypeptide which is tightly associated with a mitochondrial membrane. The possible function of the SCO1 gene product in the assembly of cytochrome c oxidase is discussed.

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References

  • Bennetzen JL, Hall BD (1982) Codon selection in yeast. J Biol Chem 257:3026–3031

    Google Scholar 

  • Bonitz GS, Coruzzi G, Thalenfeld BE, Tzagoloff A, Macino G (1980) Assembly of the mitochondrial membrane system: structure and nucleotide sequence of the gene coding for subunit 1 of yeast cytochrome oxidase. J Biol Chem 255:11927–11941

    Google Scholar 

  • Capaldi RA, Malatesta F, Darley-Usmar VM (1983) Structure of cytochrome c oxidase. Biochim Biophys Acta 726:135–148

    Google Scholar 

  • Corruzi G and Tzagoloff A (1979) Assembly of the mitochondrial membrane system: DNA sequence of subunit 2 of yeast cytochrome oxidase. J Biol Chem 254:9324–9330

    Google Scholar 

  • Costanzo MC, Fox TD (1986) Product of Saccharomyces cerevisiae nuclear gene PET494 activates translation of specific mitochondrial mRNA. Mol Cell Biol 6:3694–3703

    Google Scholar 

  • Costanzo MC, Fox TD (1988) Specific translational activation by nuclear gene products occurs in the 5′ untranslated leader of a yeast mitochondrial mRNA. Proc Natl Acad Sci USA 85:2677–2681

    Google Scholar 

  • Costanzo MC, Seaver EC, Fox TD (1986) At least two nuclear gene products are specifically required for translation of a single yeast mitochondrial mRNA. EMBO J 5:3637–3641

    Google Scholar 

  • Daum G, Böhni PC, Schatz G (1982) Import of proteins into mitochondria: cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J Biol Chem 257:13028–13033

    Google Scholar 

  • Dieckmann CL, 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

    Google Scholar 

  • Douglas MG, McCammon MT, Vassarotti A (1986) Targeting proteins into mitochondria. Microbiol Rev 50:166–178

    Google Scholar 

  • Dowhan W, Bibus RC, Schatz G (1985) The cytoplasmically-made subunit IV is necessary for assembly of cytochrome c oxidase in yeast. EMBO J 4:179–184

    Google Scholar 

  • Fox TD (1979) Five TGA “stop” codons occur within the translated sequence of the yeast mitochondrial gene for cytochome c oxidase subunit II. Proc Natl Acad Sci USA 76:6534–6538

    Google Scholar 

  • Fujiki Y, Hubbard AL, Fowlern S, Lazarow PB (1982) Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J Cell Biol 93:97–102

    Google Scholar 

  • Groot GSP, Poyton RO (1975) Oxygen control of cytochrome c oxidase synthesis in isolated mitochondria from Saccharomyces cerevisiae. Nature 255:238–240

    Google Scholar 

  • Hartl F-U, Schmidt B, Wachter E, Weiss H, Neupert W (1986) Transport into mitochondria and intramitochondrial sorting of the Fe/S protein of ubiquinol-cytochrome c reductase. Cell 47:939–951

    Google Scholar 

  • Hartl F-U, Ostermann J, Guiard B, Neupert W (1987) Successive translocation into and out of the mitochondrial matrix: targeting of proteins to the intermembrane space by a bipartite signal peptide. Cell 51:1027–1037

    Google Scholar 

  • Hurt EC, van Loon APGM (1986) How proteins find mitochondria and intramitochondrial compartments. Trends Biochem Sci 11:204–207

    Google Scholar 

  • Hurt EC, Pesold-Hurt B, Suda K, Oppliger W, Schatz G (1985) The first twelve amino acids (less than half of the pre-sequence) of an imported mitochondrial protein can direct mouse cytosolic dihydrofolate reductase into the yeast mitochondrial matrix. EMBO J 4:2061–2068

    Google Scholar 

  • Kloeckener-Gruissem B, McEwen JE, Poyton RO (1987) Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae: multiple trans-acting nuclear genes exert specific effects on expression of each of the cytochrome c oxidase subunits encoded on mitochondrial DNA. Curr Genet 12:311–322

    Google Scholar 

  • Koerner TJ, Hill J, Tzagoloff A (1985) Cloning and characterization of the yeast nuclear gene for subunit 5 of cytochrome oxidase. J Biol Chem 260:9513–9515

    Google Scholar 

  • Kramer W, Drutsa V, Jansen HW, Kramer B, Pflugfelder M, Fritz HJ (1984) The gapped duplex DNA approach to oligonucleotide-directed mutation construction. Nucleic Acids Res 12:9441–9456

    Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Google Scholar 

  • Maarse AC, Van Loon APGM, Riezman H, Gregor I, Schatz G, Grivell LA (1984) Subunit IV of yeast cytochrome c oxidase: cloning and nucleotide sequencing of the gene and partial amino acid sequencing of the mature protein. EMBO J 3:2831–2837

    Google Scholar 

  • Mahler HR, Bastos RN, Feldman F, Flury U, Lin CC, Perlman PS, Phan SH (1975) Biogenetic autonomy of mitochondrial and its limits. In: Tzagoloff A (ed) Membrane biogenesis. Plenum Press, New York, pp 15–61

    Google Scholar 

  • McEwen JE, Ko C, Kloeckner-Gruissem B, Poyton RO (1986) Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae. J Biol Chem 261:11872–11879

    Google Scholar 

  • Patterson TE, Poyton RO (1986) COX8, the structural gene for yeast cytochrome c oxidase subunit VIII. J Biol Chem 261:17192–17197

    Google Scholar 

  • Poutre CG, Fox TD (1987) PET111, a Saccharomyces cerevisiae nuclear gene required for translation of the mitochondrial mRNA encoding oxidase subunit II. Genetics 115:637–647

    Google Scholar 

  • Power SD, Lochrie MA, Sevario KA, Patterson TE, Poyton RO (1984) The nuclear-coded subunits of yeast cytochrome c oxidase: I. Fractionation of the holoenzyme into chemically pure polypeptides and the identification of two new subunits using solvent extraction and reversed phase high performance liquid chromatography. J Biol Chem 259:6564–6570

    Google Scholar 

  • Rao JKM, Argos P (1986) A conformational preference parameter to predict helices in integral membrane proteins. Biochim Biophys Acta 869:197–214

    Google Scholar 

  • Rechsteiner M, Rogers S, Rote K (1987) Protein structure and intracellular stability. Trends Biochem Sci 12:390–394

    Google Scholar 

  • Riezmann H, Hay R, Witte C, Nelson N, Schatz G (1983) Yeast mitochondrial outer membrane specifically binds cytoplasmically synthesized precursors of mitochondrial proteins. EMBO J 2:1113–1118

    Google Scholar 

  • Rödel G (1986) Two nuclear genes, CBS1 and CBS2, are required for translation of mitochondrial transcripts bearing the 5′ untranslated COB leader. Curr Genet 11:41–45

    Google Scholar 

  • Rödel G, Fox TD (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

    Google Scholar 

  • Rödel G, Körte A, Kaudewitz F (1985) Mitochondrial suppression of a yeast nuclear mutation which affects the translation of the mitochondrial apocytochrome b transcript. Curr Genet 9:641–648

    Google Scholar 

  • Saltzgaber-Müller J, Schatz G (1978) Heme is necessary for accumulation and assembly of cytochrome c oxidase subunits in Saccharomyces cerevisiae. J Biol Chem 253:305–310

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Google Scholar 

  • Schatz G (1987) Signals guiding proteins to their correct locations in mitochondria. Eur J Biochem 165:1–6

    Google Scholar 

  • Schatz G, Mason TL (1974) The biosynthesis of mitochondrial proteins. Annu Rev Biochem 43:51–87

    Google Scholar 

  • Schulze M, Rödel G (1988) SCO1, a yeast nuclear gene essential for accumulation of mitochondrial cytochrome c oxidase subunit II. Mol Gen Genet 211:492–498

    Google Scholar 

  • Séraphin B, Simon M, Faye G (1985) Primary structure of a gene for subunit V of the cytochrome c oxidase from Saccharomyces cerevisiae. Curr Genet 9:435–439

    Google Scholar 

  • Sherman F, Fink GR, Lawrence CW (1986) In: Methods in Yeast Genetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Thalenfeld BE, Tzagoloff A (1980) Assembly of the mitochondrial membrane system: sequence of the oxi2 gene of yeast mitochondrial DNA. J Biol Chem 255:6173–6180

    Google Scholar 

  • Van Heijne G (1986) Mitochondrial targeting sequences may form amphiphilic helices. EMBO J 5:1335–1342

    Google Scholar 

  • Weiss-Brummer B, Guba R, Haid A, Schweyen RJ (1979) Fine structure of OXI1, the mitochondrial gene coding for subunit II of yeast cytochrome c oxidase. Curr Genet 1:75–83

    Google Scholar 

  • Woodrow G, Schatz G (1979) The role of oxygen in the biosynthesis of cytochrome c oxidase of yeast mitochondria. J Biol Chem 254:6088–6093

    Google Scholar 

  • Wright RM, Ko C, Cumsky MG, Poyton RO (1984) Isolation and sequence of the structural gene for cytochrome c oxidase subunit VI from Saccharomyces cerevisiae. J Biol Chem 259:15401–15407

    Google Scholar 

  • Wright RM, Dircks LK, Poyton RO (1986) Characterization of COX9, the nuclear gene encoding the yeast mitochondrial protein cytochrome c oxidase subunit VIIa. J Biol Chem 261:17183–17191

    Google Scholar 

  • Zwizinski C, Schleyer M, Neupert W (1984) Proteinaceous receptors for the import of mitochondrial precursor proteins. J Biol Chem 259:7850–7856

    Google Scholar 

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Author notes

  1. Gerhard Rödel

    Present address: Labor für Molekulare Biologie und Allgemeine Pathologie, Institut für Pathologie und Rechtsmedizin der Universität Ulm, Neuherbergstrasse 11, D-8000, München 45, Germany

Authors and Affiliations

  1. Institut für Genetik und Mikrobiologie der Universität München, Maria-Ward-Strasse 1a, D-8000, München 19, Germany

    Marion Schulze & Gerhard Rödel

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  1. Marion Schulze
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  2. Gerhard Rödel
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Communicated by W. Gajewski

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Schulze, M., Rödel, G. Accumulation of the cytochrome c oxidase subunits I and II in yeast requires a mitochondrial membrane-associated protein, encoded by the nuclear SCO1 gene. Mol Gen Genet 216, 37–43 (1989). https://doi.org/10.1007/BF00332228

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  • DOI: https://doi.org/10.1007/BF00332228

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