Modular assembly of yeast mitochondrial ATP synthase and cytochrome oxidase

Leticia Veloso Ribeiro Franco 1 , 2 , Chen Hsien Su 1  and Alexander Tzagoloffhttp://orcid.org/https://orcid.org/0000-0002-1439-0885 1
  • 1 Department of Biological Sciences, Columbia University, NY 10027, New York City, USA
  • 2 Instituto de Ciências Biomédicas, Universidade de São Paulo, 05508-000, São Paulo, Brasil
Leticia Veloso Ribeiro Franco
  • Department of Biological Sciences, Columbia University, New York City, NY 10027, USA
  • Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, 05508-000, Brasil
  • Search for other articles:
  • degruyter.comGoogle Scholar
, Chen Hsien Su
  • Department of Biological Sciences, Columbia University, New York City, NY 10027, USA
  • Search for other articles:
  • degruyter.comGoogle Scholar
and Alexander TzagoloffORCID iD: https://orcid.org/0000-0002-1439-0885

Abstract

The respiratory pathway of mitochondria is composed of four electron transfer complexes and the ATP synthase. In this article, we review evidence from studies of Saccharomyces cerevisiae that both ATP synthase and cytochrome oxidase (COX) are assembled from independent modules that correspond to structurally and functionally identifiable components of each complex. Biogenesis of the respiratory chain requires a coordinate and balanced expression of gene products that become partner subunits of the same complex, but are encoded in the two physically separated genomes. Current evidence indicates that synthesis of two key mitochondrial encoded subunits of ATP synthase is regulated by the F1 module. Expression of COX1 that codes for a subunit of the COX catalytic core is also regulated by a mechanism that restricts synthesis of this subunit to the availability of a nuclear-encoded translational activator. The respiratory chain must maintain a fixed stoichiometry of the component enzyme complexes during cell growth. We propose that high-molecular-weight complexes composed of Cox6, a subunit of COX, and of the Atp9 subunit of ATP synthase play a key role in establishing the ratio of the two complexes during their assembly.

  • Abrahams, J.P., Leslie, A.G., Lutter, R., and Walker, J.E. (1994). Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370, 621–628.

    • Crossref
    • PubMed
    • Export Citation
  • Ackerman, S.H. and Tzagoloff, A. (1990a). Identification of two nuclear genes (ATP11, ATP12) required for assembly of the yeast F1–ATPase. Proc. Natl. Acad. Sci. U.S.A. 87, 4986–4990.

    • Crossref
    • Export Citation
  • Ackerman, S.H. and Tzagoloff, A. (1990b). ATP10, a yeast nuclear gene required for the assembly of the mitochondrial F1–F0 complex. J. Biol. Chem. 265, 9952–9969.

  • Aich, A., Wang, C., Chowdhury, A., Ronsör, C., Pacheu-Grau, D., Richter-Dennerlein, R., Dennerlein, S., and Rehling, P. (2018). COX16 promotes COX2 metallation and assembly during respiratory complex IV biogenesis. eLife 7, e32572.

    • Crossref
    • PubMed
    • Export Citation
  • Arechaga, I., Butler, P.J., and Walker, J.E. (2002). Self-assembly of ATP synthase subunit c rings. FEBS Lett. 515, 189–193.

    • Crossref
    • PubMed
    • Export Citation
  • Arnold, I., Pfeiffer, K., Neupert, W., and Stuart, R.A. (1998). Yeast mitochondrial F1F0–ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J. 17, 7170–7178.

    • Crossref
    • PubMed
    • Export Citation
  • Arnold, I., Pfeiffer, K., Neupert, W., Stuart, R.A., and Schägger, H. (1999). ATP synthase of yeast mitochondria. Isolation of subunit j and disruption of the ATP18 gene. J. Biol. Chem. 274, 36–40.

    • Crossref
    • Export Citation
  • Arselin, G., Giraud, M.F., Dautant, A., Vaillier, J., Brèthes, D., Coulary-Salin, B., Schaeffer, J., and Velours, J. (2003). The GxxxG motif of the transmembrane domain of subunit e is involved in the dimerization/oligomerization of the yeast ATP synthase complex in the mitochondrial membrane. Eur. J. Biochem. 270, 1875–1884.

    • Crossref
    • Export Citation
  • Ballhausen, B., Altendorf, K., and Deckers-Hebestreit, G. (2009). Constant c10 ring stoichiometry in the Escherichia coli ATP synthase analyzed by cross-linking. J. Bacteriol. 191, 2400–2404.

    • Crossref
    • PubMed
    • Export Citation
  • Barrientos, A., Pierre, D., Lee, J., and Tzagoloff, A. (2003). Cytochrome oxidase assembly does not require catalytically active cytochrome C. J. Biol. Chem. 278, 8881–8887.

    • Crossref
    • PubMed
    • Export Citation
  • Barrientos, A., Zambrano, A., and Tzagoloff, A. (2004). Mss51p and Cox14p jointly regulate mitochondrial Cox1p expression in Saccharomyces cerevisiae. EMBO J. 23, 3472–3482.

    • Crossref
    • PubMed
    • Export Citation
  • Barros, M.H. and Tzagoloff, A. (2002). Regulation of the heme A biosynthetic pathway in Saccharomyces cerevisiae. FEBS Lett. 516, 119–123.

    • Crossref
    • PubMed
    • Export Citation
  • Barros, M.H. and Tzagoloff, A. (2017). Aep3p-dependent translation of yeast mitochondrial ATP8. Mol. Biol. Cell 28, 1426–1434.

    • Crossref
    • PubMed
    • Export Citation
  • Barros, M.H. and McStay, G.P. (2020). Modular biogenesis of mitochondrial respiratory complexes. Mitochondrion 50, 94–114.

    • Crossref
    • PubMed
    • Export Citation
  • Barros, M.H., Carlson, C.G., Glerum, D.M., and Tzagoloff, A. (2002). Involvement of mitochondrial ferredoxin and Cox15p in hydroxylation of heme O. FEBS Lett. 492, 133–138.

  • Barros, M.H., Myers, A.M., Van Driesche, S., and Tzagoloff, A. (2006). COX24 codes for a mitochondrial protein required for processing of the COX1 transcript. J. Biol. Chem. 281, 3743–3751.

    • Crossref
    • PubMed
    • Export Citation
  • Behrens, M., Michaelis, G., and 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.

    • Crossref
    • PubMed
    • Export Citation
  • Bestwick, M., Khalimonchuk, O., Pierrel, F., and Winge, D.R. (2010). The role of Coa2 in hemylation of yeast Cox1 revealed by its genetic interaction with Cox10. Mol. Cell. Biol. 30, 172–185.

    • Crossref
    • PubMed
    • Export Citation
  • Blum, T.B., Hahn, A., Meier, T., Davies, K.M., and Kühlbrandt, W. (2019). Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows. Proc. Natl. Acad. Sci. U.S.A. 116, 4250–4255.

    • Crossref
    • PubMed
    • Export Citation
  • Bonitz, S.G., Coruzzi, G., Thalenfeld, B.E., Tzagoloff, A., and 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.

    • PubMed
    • Export Citation
  • Bourens, M. and Barrientos, A. (2017). Human mitochondrial cytochrome c oxidase assembly factor COX18 acts transiently as a membrane insertase within the subunit 2 maturation module. J. Biol. Chem. 292, 7774–7783.

    • Crossref
    • PubMed
    • Export Citation
  • Bourens, M., Dabir, D.V., Tienson, H.L., Sorokina, I., Koehler, C.M., and Barrientos, A. (2012). Role of twin Cys-Xaa9-Cys motif cysteines in mitochondrial import of the cytochrome c oxidase biogenesis factor Cmc1. J. Biol. Chem. 287, 31258–31269.

    • Crossref
    • PubMed
    • Export Citation
  • Bourens, M., Boulet, A., Leary, S.C., and Barrientos, A. (2014). Human COX20 cooperates with SCO1 and SCO2 to mature COX2 and promote the assembly of cytochrome c oxidase. Hum. Mol. Genet. 23, 2901–2913.

    • Crossref
    • PubMed
    • Export Citation
  • Bousquet, I., Dujardin, G., Poyton, R.O., and Slonimski, P.P. (1990). Two group I mitochondrial introns in the cob-box and coxI genes require the same MRS1/PET157 nuclear gene product for splicing. Curr. Genet. 18, 117–124.

    • Crossref
    • Export Citation
  • Bowman, S., Ackerman, S.H., Griffiths, D.E., and 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.

    • PubMed
    • Export Citation
  • Boyer, P.D. (1997). The ATP synthase—a splendid molecular machine. Annu. Rev. Biochem. 66, 717–749.

    • Crossref
    • PubMed
    • Export Citation
  • Camougrand, N., Pélissier, P., Velours, G., and Guérin, M. (1995). NCA2, a second nuclear gene required for the control of mitochondrial synthesis of subunits 6 and 8 of ATP synthase in Saccharomyces cerevisiae. J. Mol. Biol. 247, 588–596.

    • Crossref
    • PubMed
    • Export Citation
  • Carlson, C.G., Barrientos, A., Tzagoloff, A., and Glerum, D.M. (2003). COX16 encodes a novel protein required for the assembly of cytochrome oxidase in Saccharomyces cerevisiae. J. Biol. Chem 278, 3770–3775.

    • Crossref
    • PubMed
    • Export Citation
  • Chance, B. and Williams, G.R. (1955). Respiratory enzymes in oxidative phosphorylation. IV. The respiratory chain. J. Biol. Chem. 217, 429–438.

    • PubMed
    • Export Citation
  • Cheng, M.Y., Hartl, F.U., Martin, J., Pollock, R.A., Kalousek, F., Neupert, W., Hallberg, E.M., Hallberg, R.L., and Horwich, A.L. (1989). Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337, 620–625.

    • Crossref
    • PubMed
    • Export Citation
  • Christianson, T. and Rabinowitz, M. (1983). Identification of multiple transcriptional initiation sites on the yeast mitochondrial genome by in vitro capping with guanylyltransferase. J. Biol. Chem. 258, 14025–14033.

    • PubMed
    • Export Citation
  • Church, G.M., Slonimski, P.P., and Gilbert, W. (1979). Pleiotropic mutations within two yeast mitochondrial cytochrome genes block mRNA processing. Cell 18, 1209–1215.

    • Crossref
    • PubMed
    • Export Citation
  • Cross, R.L. and Müller, V. (2004). The evolution of A-, F-, and V-type ATP synthases and ATPases: reversals in function and changes in the H+/ATP coupling ratio. FEBS Lett. 576, 1–4.

    • Crossref
    • Export Citation
  • Cruciat, C.M., Brunner, S., Baumann, F., Neupert, W., and Stuart, R.A. (2000). The cytochrome bc1 and cytochrome c oxidase complexes associate to form a single supracomplex in yeast mitochondria. J. Biol. Chem. 275, 18093–18098.

    • Crossref
    • Export Citation
  • Dawitz, H., Schäfer, J., Schaart, J.M., Magits, W., Brzezinski, P., and Ott, M. (2020). Rcf1 modulates cytochrome c oxidase activity especially under energy-demanding conditions. Front. Physiol. 10, 1555.

    • Crossref
    • PubMed
    • Export Citation
  • Davies, K.M., Strauss, M., Daum, B., Kief, J.H., Osiewacz, H.D., Rycovska, A., Zickermann, V., and Kühlbrandt, W. (2011). Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc. Natl. Acad. Sci. U.S.A. 108, 14121–14126.

    • Crossref
    • PubMed
    • Export Citation
  • Dennerlein, S., Oeljeklaus, S., Jans, D., Hellwig, C., Bareth, B., Jakobs, S., Deckers, M., Warscheid, B., and Rehling, P. (2015). MITRAC7 acts as a COX1-specific chaperone and reveals a checkpoint during cytochrome c oxidase assembly. Cell Rep. 12, 1644–1655.

    • Crossref
    • PubMed
    • Export Citation
  • Dewey, R.E., Schuster, A.M., Levings, C.S., and Timothy, D.H. (1985). Nucleotide sequence of FO–ATPase proteolipid (subunit 9) gene of maize mitochondria. Proc. Natl. Acad. Sci. U.S.A. 82, 1015–1019.

    • Crossref
    • Export Citation
  • Dautant, A., Velours, J., and Giraud, M.F. (2010). Crystal structure of the Mg·ADP-inhibited state of the yeast F1c10–ATP synthase. J. Biol. Chem. 285, 29502–29510.

    • Crossref
    • PubMed
    • Export Citation
  • Decoster, E., Simon, M., Hatat, D., and 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.

    • Crossref
    • PubMed
    • Export Citation
  • Elliott, L.E., Saracco, S.A., and Fox, T.D. (2012). Multiple roles of the Cox20 chaperone in assembly of Saccharomyces cerevisiae cytochrome c oxidase. Genetics 190, 559–567.

    • Crossref
    • PubMed
    • Export Citation
  • Ellis, T.P., Lukins, H.B., Nagley, P., and Corner, B.E. (1999). Suppression of a nuclear aep2 mutation in Saccharomyces cerevisiae by a base substitution in the 5′-untranslated region of the mitochondrial oli1 gene encoding subunit 9 of ATP synthase. Genetics 151, 1353–1363.

    • PubMed
    • Export Citation
  • Ellis, T.P., Helfenbein, K.G., Tzagoloff, A., and Dieckmann, C.L. (2004). Aep3p stabilizes the mitochondrial bicistronic mRNA encoding subunits 6 and 8 of the H+-translocating ATP synthase of Saccharomyces cerevisiae. J. Biol. Chem. 279, 15728–15733.

    • Crossref
    • PubMed
    • Export Citation
  • Finnegan, P.M., Ellis, T.P., Nagley, P., and Lukins, H.B. (1995). The mature AEP2 gene product of Saccharomyces cerevisiae, required for the expression of subunit 9 of ATP synthase, is a 58 kDa mitochondrial protein. FEBS Lett. 368, 505–508.

    • Crossref
    • PubMed
    • Export Citation
  • Ferguson-Miller, S. and Babcock, G.T. (1996). Heme/copper terminal oxidases. Chem. Rev. 96, 2889–2908.

    • Crossref
    • PubMed
    • Export Citation
  • Fillingame, R.H. and Dmitriev, O.Y. (2002). Structural model of the transmembrane F0 rotary sector of H+-transporting ATP synthase derived by solution NMR and intersubunit cross-linking in situ. Biochim. Biophys. Acta 1565, 232–245.

    • Crossref
    • Export Citation
  • Fontanesi, F., Soto, I.C., Horn, D., and Barrientos, A. (2010). Mss51 and Ssc1 facilitate translational regulation of cytochrome c oxidase biogenesis. Mol. Cell. Biol. 30, 245–259.

    • Crossref
    • PubMed
    • Export Citation
  • Fontanesi, F., Clemente, P., and Barrientos, A. (2011). Cox25 teams up with Mss51, Ssc1, and Cox14 to regulate mitochondrial cytochrome c oxidase subunit 1 expression and assembly in Saccharomyces cerevisiae. J. Biol. Chem. 286, 555–566.

    • Crossref
    • PubMed
    • Export Citation
  • Foury, F., Roganti, T., Lecrenier, N., and Purnelle, B. (1998). The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett. 440, 325–331.

    • Crossref
    • PubMed
    • Export Citation
  • Franco, L.V.R., Su, C.H., McStay, G.P., Yu, G.J., and Tzagoloff, A. (2018). Cox2p of yeast cytochrome oxidase assembles as a stand-alone subunit with the Cox1p and Cox3p modules. J. Biol. Chem. 293, 16899–16911.

    • Crossref
    • PubMed
    • Export Citation
  • Fujikawa, M., Sugawara, K., Tanabe, T., and Yoshida, M. (2015). Assembly of human mitochondrial ATP synthase through two separate intermediates, F1-c-ring and b-e-g complex. FEBS Lett. 589, 2707–2712.

    • Crossref
    • PubMed
    • Export Citation
  • García-Villegas, R., Camacho-Villasana, Y., Shingú-Vázquez, M.Á., Cabrera-Orefice, A., Uribe-Carvajal, S., Fox, T.D., and Pérez-Martínez, X. (2017). The Cox1 C-terminal domain is a central regulator of cytochrome c oxidase biogenesis in yeast mitochondria. J. Biol. Chem. 292, 10912–10925.

    • Crossref
    • PubMed
    • Export Citation
  • Genova, M.L. and Lenaz, G. (2014). Functional role of mitochondrial respiratory supercomplexes. Biochim. Biophys. Acta 837, 427–443.

  • Ghosh, A., Trivedi, P.P., Timbalia, S.A., Griffin, A.T., Rahn, J.J., Chan, S.S., and Gohil, V.M. (2014). Copper supplementation restores cytochrome c oxidase assembly defect in a mitochondrial disease model of COA6 deficiency. Hum. Mol. Genet. 23, 3596–3606.

    • Crossref
    • Export Citation
  • Glerum, D.M., Shtanko, A., and Tzagoloff, A. (1996). SCO1 and SCO2 act as high copy suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae. J. Biol. Chem. 271, 20531–20535.

    • Crossref
    • PubMed
    • Export Citation
  • Golik, P., Szczepanek, T., Bartnik, E., Stepien, P.P., and Lazowska, J. (1995). The S. cerevisiae nuclear gene SUV3 encoding a putative RNA helicase is necessary for the stability of mitochondrial transcripts containing multiple introns. Curr. Genet. 28, 217–224.

    • Crossref
    • Export Citation
  • Gomis-Rüth, F.X., Moncalián, G., Pérez-Luque, R., González, A., Cabezón, E., de la Cruz, F., and Coll, M. (2001). The bacterial conjugation protein TrwB resembles ring helicases and F1–ATPase. Nature 409, 637–641.

    • Crossref
    • PubMed
    • Export Citation
  • Green, D.E., Allmann, D.W., Bachmann, E., Baum, H., Kopaczyk, K., Korman, E.F., Lipton, S., MacLennan, D.H., McConnell, D.G., Perdue, J.P., et al. (1967). Formation of membranes by repeating units. Arch. Biochem. Biophys. 119, 312–335.

    • Crossref
    • PubMed
    • Export Citation
  • Green-Willms, N.S., Butler, C.A., Dunstan, H.M., and Fox, T.D. (2001). Pet111p, an inner membrane-bound translational activator that limits expression of the Saccharomyces cerevisiae mitochondrial gene COX2. J. Biol. Chem. 276, 6392–6397.

    • Crossref
    • PubMed
    • Export Citation
  • Guo, H., Suzuki, T., and Rubinstein, J.L. (2019). Structure of a bacterial ATP synthase. Elife 8.

    • PubMed
    • Export Citation
  • Hadikusumo, R.G., Meltzer, S., Choo, W.M., Jean-Francois, M.J, Linnane, A.W., and Marzuki, S. (1988). The definition of mitochondrial H+ ATPase assembly defects in mit-mutants of Saccharomyces cerevisiae with a monoclonal antibody to the enzyme complex as an assembly probe. Biochim. Biophys. Acta 933, 212–222.

    • Crossref
    • PubMed
    • Export Citation
  • Hartley, A.M., Lukoyanova, N., Zhang, Y., Cabrera-Orefice, A., Arnold, S., Meunier, B., Pinotsis, N., and Maréchal, A. (2019). Structure of yeast cytochrome c oxidase in a supercomplex with cytochrome bc1. Nat. Struct. Mol. Biol. 26, 78–83.

    • Crossref
    • Export Citation
  • Hatefi, Y., Haavik, A.G., and Griffiths, D.E. (1962a). Studies on the electron transfer system. XL. Preparation and properties of mitochondrial DPNH-coenzyme Q reductase. J. Biol. Chem. 237, 1676–1680.

  • Hatefi, Y., Haavik, A.G., and Griffiths, D.E. (1962b). Studies on the electron transfer system. XLI. Reduced coenzyme Q (QH2)–cytochrome c reductase. J. Biol. Chem. 237, 1681–1685.

  • Hatefi, Y., Haavik, A.G., Fowler, L.R., and Griffiths, D.E. (1962c). Studies on the electron transfer system. XLII. Reconstitution of the electron transfer system. J. Biol. Chem. 237, 2661–2669.

  • Hell, K., Herrmann, J.M., Pratje, E., Neupert, W., and Stuart, R.A. (1997). Oxalp mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space. FEBS Lett. 418, 367–370.

    • Crossref
    • Export Citation
  • Hell, K., Herrmann, J.M., Pratje, E., Neupert, W., and 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.

    • Crossref
    • PubMed
    • Export Citation
  • Hell, K., Tzagoloff, A., Neupert, W., and 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.

    • Crossref
    • PubMed
    • Export Citation
  • Herbert, C.J., Labouesse, M., Dujardin, G., and Slonimski, P.P. (1988). The NAM2 proteins from S. cerevisiae and S. douglasii are mitochondrial leucyl-tRNA synthetases, and are involved in mRNA splicing. EMBO J. 7, 473–483.

    • Crossref
    • Export Citation
  • Herrmann, J.M., Stuart, R.A., Craig, E.A., and Neupert, W. (1994). Mitochondrial heat shock protein 70, a molecular chaperone for proteins encoded by mitochondrial DNA. J. Cell Biol. 127, 893–902.

    • Crossref
    • PubMed
    • Export Citation
  • Hilbers, F., Eggers, R., Pradela, K., Friedrich, K., Herkenhoff-Hesselmann, B., Becker, E., and Deckers-Hebestreit, G. (2013). Subunit δ is the key player for assembly of the H+-translocating unit of Escherichia coli FOF1 ATP Synthase. J. Biol. Chem. 288, 25880–25894.

    • Crossref
    • Export Citation
  • Iwata, S., Ostermeier, C., Ludwig, B., and Michel, H. (1995). Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376, 660–669.

    • Crossref
    • PubMed
    • Export Citation
  • Jan, P.S., Esser, E., Pratje, E., and Michaelis, G. (2000). Som1, a third component of the yeast mitochondrial inner membrane peptidase complex that contains Imp1 and Imp2. Mol. Gen. Genet. 263, 483–491.

    • Crossref
    • PubMed
    • Export Citation
  • Jia, L., Dienhart, M.K., and Stuart, R.A. (2007). Oxa1 directly interacts with Atp9 and mediates its assembly into the mitochondrial F1Fo–ATP synthase complex. Mol. Biol. Cell 18, 1897–1908.

    • Crossref
    • PubMed
    • Export Citation
  • Jones, J.L., Hofmann, K.B., Cowan, A.T., Temiakov, D., Cramer, P., and Anikin, M. (2019). Yeast mitochondrial protein Pet111p binds directly to two distinct targets in COX2 mRNA, suggesting a mechanism of translational activation. J. Biol. Chem. 294, 7528–7536.

    • Crossref
    • PubMed
    • Export Citation
  • Kagawa, Y. and Racker, E. (1966). Partial resolution of the enzymes catalyzing oxidative phosphorylation. 8. Properties of a factor conferring oligomycin sensitivity on mitochondrial adenosine triphosphatase. J. Biol. Chem. 241, 2461–246.

  • Karen, M.D., Anselmi, C., Wittig, I., Faraldo-Gómez, J.D., and Kuhlbrandt, W. (2012). Structure of the yeast F1Fo–ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc. Natl. Acad. Sci. U.S.A. 109, 13602–13607.

    • Crossref
    • PubMed
    • Export Citation
  • Keil, M., Bareth, B., Woellhaf, M.W., Peleh, V., Prestele, M., Rehling, P., and Herrmann, J.M. (2012). Oxa1–ribosome complexes coordinate the assembly of cytochrome c oxidase in mitochondria. J. Biol. Chem. 287, 34484–34493.

    • Crossref
    • PubMed
    • Export Citation
  • Kennell, J.C., Moran, J.V., Perlman, P.S., Butow, R.A., and Lambowitz, A.M. (1993). Reverse transcriptase activity associated with maturase-encoding group II introns in yeast mitochondria. Cell 73, 133–146.

    • Crossref
    • PubMed
    • Export Citation
  • Kermorgant, M., Bonnefoy, N., and 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.

    • Crossref
    • PubMed
    • Export Citation
  • Khalimonchuk, O., Bestwick, M., Meunier, B., Watts, T.C., and Winge, D.R. (2010). Formation of the redox cofactor centers during Cox1 maturation in yeast cytochrome oxidase. Mol. Cell Biol. 30, 1004–1017.

    • Crossref
    • PubMed
    • Export Citation
  • LaMarche, A.E., Abate, M.I., Chan, S.H., and Trumpower, B.L. (1992). Isolation and characterization of COX12, the nuclear gene for a previously unrecognized subunit of Saccharomyces cerevisiae cytochrome c oxidase. J. Biol. Chem. 267, 22473–22480.

    • PubMed
    • Export Citation
  • Lazowska, J., Jacq, C., and Slonimski, P.P. (1980). Sequence of introns and flanking exons in wild-type and box3 mutants of cytochrome b reveals an interlaced splicing protein coded by an intron. Cell 22, 333–348.

    • Crossref
    • PubMed
    • Export Citation
  • Lefebvre-Legendre, L., Vaillier, J., Benabdelhak, H., Velours, J., Slonimski, P.P., and di Rago, J.P. (2001). Identification of a nuclear gene (FMC1) required for the assembly/stability of yeast mitochondrial F1–ATPase in heat stress conditions. J. Biol. Chem. 276, 6789–6796.

    • Crossref
    • PubMed
    • Export Citation
  • Lefebvre-Legendre, L., Salin, B., Schaëffer, J., Brèthes, D., Dautant, A., Ackerman, S.H., and di Rago, J.P. (2005). Failure to assemble the alpha 3 beta 3 subcomplex of the ATP synthase leads to accumulation of the alpha and beta subunits within inclusion bodies and the loss of mitochondrial cristae in Saccharomyces cerevisiae. J. Biol. Chem. 280, 18386–18392.

    • Crossref
    • PubMed
    • Export Citation
  • Levchenko, M., Wuttke, J.M., Römpler, K., Schmidt, B., Neifer, K., Juris, L., Wissel, M., Rehling, P., and Deckers, M. (2016). Cox26 is a novel stoichiometric subunit of the yeast cytochrome c oxidase. Biochim. Biophys. Acta 1863, 1624–1632.

    • Crossref
    • PubMed
    • Export Citation
  • Lorenzi, I., Oeljeklaus, S., Ronsör, C., Bareth, B., Warscheid, B., Rehling, P., and Dennerlein, S. (2016). Ribosome-associated Mba1 escorts Cox2 from insertion machinery to maturing assembly intermediates. Mol. Cell. Biol. 36, 2782–2793.

    • Crossref
    • PubMed
    • Export Citation
  • Luck, D.J. (1963). Genesis of mitochondria in Neurospora crassa. Proc. Natl. Acad. Sci. U.S.A. 49, 233–240.

    • Crossref
    • PubMed
    • Export Citation
  • Ludlam, A., Brunzelle, J., Pribyl, T., Xu, X., Gatti, D.L., and Ackerman, S.H. (2009). Chaperones of F1–ATPase. J. Biol. Chem. 284, 17138–17146.

    • Crossref
    • PubMed
    • Export Citation
  • Luttik, M.A., Overkamp, K.M., Kötter, P., de Vries, S., van Dijken, J.P., and Pronk, J.T. (1998). The Saccharomyces cerevisiae NDE1 and NDE2 genes encode separate mitochondrial NADH dehydrogenases catalyzing the oxidation of cytosolic NADH. J. Biol. Chem. 273, 24529–24534.

    • Crossref
    • PubMed
    • Export Citation
  • Lytovchenko, O., Naumenko, N., Oeljeklaus, S., Schmidt, B., von der Malsburg, K., Deckers, M., Warscheid, B., van der Laan, M., and Rehling, P. (2014). The INA complex facilitates assembly of the peripheral stalk of the mitochondrial F1Fo–ATP synthase. EMBO J. 33, 1624–1638.

    • Crossref
    • PubMed
    • Export Citation
  • Macreadie, I.G., Novitski, C.E., Maxwell, R.J., John, U., Ooi, B.G., McMullen, G.L., Lukins, H.B., Linnane, A.W., and Nagley, P. (1983). Biogenesis of mitochondria: the mitochondrial gene (aap1) coding for mitochondrial ATPase subunit 8 in Saccharomyces cerevisiae. Nucleic Acids Res. 11, 4435–4451.

    • Crossref
    • PubMed
    • Export Citation
  • Manthey, G.M. and 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.

    • Crossref
    • PubMed
    • Export Citation
  • Mayorga, J.P., Camacho-Villasana, Y., Shingú-Vázquez, M., García-Villegas, R., Zamudio-Ochoa, A., García-Guerrero, A.E., Hernández, G., and Pérez-Martínez, X. (2016). A novel function of Pet54 in regulation of cox1 synthesis in Saccharomyces cerevisiae mitochondria. J. Biol. Chem. 291, 9343–9355.

    • Crossref
    • PubMed
    • Export Citation
  • McEwen, J.E., Ko, C., Kloeckner-Gruissem, B., and Poyton, R. (1986). Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae. Characterization of mutants in 34 complementation groups. J. Biol. Chem. 261, 11872–11879.

    • PubMed
    • Export Citation
  • McStay, G.P., Su, C.H., and Tzagoloff, A. (2013a). Modular assembly of yeast cytochrome oxidase. Mol. Biol. Cell. 24, 440–452.

    • Crossref
    • Export Citation
  • McStay, G.P., Su, C.H., Thomas, S.M., Xu, J.T., and Tzagoloff, A. (2013b). Characterization of assembly intermediates containing subunit 1 of yeast cytochrome oxidase. J. Biol. Chem. 288, 26546–26556.

    • Crossref
    • Export Citation
  • McStay, G.P., Su, C.H., and Tzagoloff, A. (2013c). Stabilization of Cox1p intermediates by the Cox14p–Coa3p complex. FEBS Lett. 587, 943–949.

    • Crossref
    • Export Citation
  • Mick, D.U., Vukotic, M., Piechura, H., Meyer, H.E., Warscheid, B., Deckers, M., and Rehling, P. (2010). Coa3 and Cox14 are essential for negative feedback regulation of COX1 translation in mitochondria. J. Cell Biol. 191, 141–154.

    • Crossref
    • PubMed
    • Export Citation
  • Mick, D.U., Fox, T.D., and Rehling, P. (2011). Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation. Nat. Rev. Mol. Cell Biol. 12, 14–20.

    • Crossref
    • PubMed
    • Export Citation
  • Mick, D.U., Dennerlein, S., Wiese, H., Reinhold, R., Pacheu-Grau, D., Lorenzi, I., Sasarman, F., Weraarpachai, W., Shoubridge, E.A., Warscheid, B., et al. (2012). MITRAC links mitochondrial protein translocation to respiratory-chain assembly and translational regulation. Cell 151, 1528–1541.

    • Crossref
    • PubMed
    • Export Citation
  • Mileykovskaya, E., Penczek, P.A., Fang, J., Mallampalli, V.K., Sparagna, G.C., and Dowhan, W. (2012). Arrangement of the respiratory chain complexes in Saccharomyces cerevisiae supercomplex III2IV2 revealed by single particle cryo-electron microscopy. J. Biol. Chem. 287, 23095–23103.

    • Crossref
    • PubMed
    • Export Citation
  • Möller-Hergt, B.V., Carlström, A., Stephan, K., Imhof, A., and Ott, M. (2018). The ribosome receptors Mrx15 and Mba1 jointly organize cotranslational insertion and protein biogenesis in mitochondria. Mol. Biol. Cell 29, 2386–2396.

    • Crossref
    • PubMed
    • Export Citation
  • Moreno, J.I., Buie, K.S., Price, R.E., and Piva, M.A. (2009). Ccm1p/Ygr150cp, a pentatricopeptide repeat protein, is essential to remove the fourth intron of both COB and COX1 pre-mRNAs in Saccharomyces cerevisiae. Curr. Genet. 55, 475–484.

    • Crossref
    • PubMed
    • Export Citation
  • Mulkidjanian, A.Y., Makarova, K.S., Galperin, M.Y., and Koonin, E.V. (2007). Inventing the dynamo machine: the evolution of the F-type and V-type ATPases. Nat. Rev. Microbiol. 5, 892–899.

    • Crossref
    • PubMed
    • Export Citation
  • Naumenko, N., Morgenstern, M., Rucktäschel, R., Warscheid, B., and Rehling, P. (2017). INA complex lyases the F1Fo–ATP synthase membrane motor modules. Nat. Commun. 8, 1237.

    • Crossref
    • Export Citation
  • Neupert, W. and Herrmann, J.M. (2007). Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723–749.

    • Crossref
    • PubMed
    • Export Citation
  • Ndi, M., Marin-Buera, L., Salvatori, R., Singh, A.P., and Ott, M. (2018). Biogenesis of the bc1 complex of the mitochondrial respiratory chain. J. Mol. Biol. 430, 3892–3905.

    • Crossref
    • PubMed
    • Export Citation
  • Osman, C., Wilmes, C., Tatsuta, T., and Langer, T. (2007). Prohibitins interact genetically with Atp23, a novel processing peptidase and chaperone for the F1Fo–ATP synthase. Mol. Biol. Cell 18, 627–635.

    • Crossref
    • PubMed
    • Export Citation
  • Ott, M., Prestele, M., Bauerschmitt, H., Funes, S., Bonnefoy, N., andHerrmann, J.M. (2006). Mba1, a membrane-associated ribosome receptor in mitochondria. EMBO J. 25, 1603–1610.

    • Crossref
    • PubMed
    • Export Citation
  • Ozaki, Y., Suzuki, T., Kuruma, Y., Ueda, T., and Yoshida, M. (2008). UncI protein can mediate ring-assembly of c-subunits of FoF1–ATP synthase in vitro. Biochem. Biophys. Res. Commun. 367, 663–666.

    • Crossref
    • PubMed
    • Export Citation
  • Payne, M.J., Finnegan, P.M., Smooker, P.M., and Lukins, H.B. (1993). Characterization of a second nuclear gene, AEP1, required for expression of the mitochondrial OLI1 gene in Saccharomyces cerevisiae. Curr. Genet. 24, 126–135.

    • Crossref
    • PubMed
    • Export Citation
  • Pélissier, P., Camougrand, N., Velours, G., and Guérin, M. (1995). NCA3, a nuclear gene involved in the mitochondrial expression of subunits 6 and 8 of the Fo-F1 ATP synthase of S. cerevisiae. Curr. Genet. 27, 409–416.

    • Crossref
    • PubMed
    • Export Citation
  • Perez-Martinez, X., Broadley, S.A., and Fox, T.D. (2003). Mss51p promotes mitochondrial Cox1p synthesis and interacts with newly synthesized Cox1p. EMBO J. 22, 5951–5961.

    • Crossref
    • PubMed
    • Export Citation
  • Perez-Martinez, X., Butler, C.A., Shingu-Vazquez, M., and Fox, T.D. (2009). Dual functions of Mss51 couple synthesis of Cox1 to assembly of cytochrome c oxidase in Saccharomyces cerevisiae mitochondria. Mol. Biol. Cell 20, 4371–4380.

    • Crossref
    • PubMed
    • Export Citation
  • Pierrel, F., Bestwick, M.L., Cobine, P.A., Khalimonchuk, O., Cricco, J.A., and Winge, D.R. (2007). Coa1 links the Mss51 post-translational function. to Cox1 cofactor insertion in cytochrome c oxidase assembly. EMBO J. 26, 4335–4346.

    • Crossref
    • PubMed
    • Export Citation
  • Preuss, M., Leonhard, K., Hell, K., Stuart, R.A., Neupert, W., and Herrmann, J.M. (2001). Mba1, a novel component of the mitochondrial protein export machinery of the yeast Saccharomyces cerevisiae. J. Cell Biol. 153, 1085–1096.

    • Crossref
    • PubMed
    • Export Citation
  • Rak, M. and Tzagoloff, A. (2009). F1-dependent translation of mitochondrially encoded Atp6p and Atp8p subunits of yeast ATP synthase. Proc. Natl. Acad. Sci. U.S.A. 106, 18509–18514.

    • Crossref
    • PubMed
    • Export Citation
  • Rak, M., Tetaud, E., Godard, F., Sagot, I., Salin, B., Duvezin-Caubet, S., Slonimski, P.P., Rytka, J., and di Rago, J.P. (2007). Yeast cells lacking the mitochondrial gene encoding the ATP synthase subunit 6 exhibit a selective loss of complex IV and unusual mitochondrial morphology. J. Biol. Chem. 282, 10853–10864.

    • Crossref
    • PubMed
    • Export Citation
  • Rak, M., Gokova, S., and Tzagoloff, A. (2011). Modular assembly of yeast mitochondrial ATP synthase. EMBO J. 30, 920–930.

    • Crossref
    • PubMed
    • Export Citation
  • Rak, M., Su, C.H., Xu, J.T., Azpiroz, R., Singh, A.M., and Tzagoloff, A. (2016). Regulation of mitochondrial translation of the ATP8/ATP6 mRNA by Smt1p. Mol. Biol. Cell 27, 919–929.

    • Crossref
    • PubMed
    • Export Citation
  • Rathore, S., Berndtsson, J., Marin-Buera, L., Conrad, J., Carroni, M., Brzezinski, P., and Ott, M. (2019). Cryo-EM structure of the yeast respiratory supercomplex. Nat. Struct. Mol. Biol. 26, 50–57.

    • Crossref
    • PubMed
    • Export Citation
  • Reinders, J., Wagner, K., Zahedi, R.P., Stojanovski, D., Eyrich, B., van der Laan, M., Rehling, P., Sickmann, A., Pfanner, N., and Meisinger, C. (2007). Profiling phosphoproteins of yeast mitochondria reveals a role of phosphorylation in assembly of the ATP synthase. Mol. Cell. Proteomics 6, 1896–1906.

    • Crossref
    • PubMed
    • Export Citation
  • Rigby, K., Cobine, P.A., Khalimonchuk, O., and Winge, D.R. (2008). Mapping the functional interaction of Sco1 and Cox2 in cytochrome oxidase biogenesis. J. Biol. Chem. 283, 15015–15022.

    • Crossref
    • PubMed
    • Export Citation
  • Saddar, S., Dienhart, M.K., and Stuart, R.A. (2008). The F1F0–ATP synthase complex influences the assembly state of the cytochrome bc 1-cytochrome oxidase supercomplex and its association with the TIM23 machinery. J. Biol. Chem. 283, 6677–6686.

    • Crossref
    • PubMed
    • Export Citation
  • Sánchez-Caballero, L., Guerrero-Castillo, S., and Nijtmans, L. (2016). Unraveling the complexity of mitochondrial complex I assembly: a dynamic process. Biochim. Biophys. Acta 1857, 980–990.

    • Crossref
    • PubMed
    • Export Citation
  • Saracco, S.A. and Fox, T.D. (2002). 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, 1122–1131

    • Crossref
    • PubMed
    • Export Citation
  • Saraste, M. (1990). Structural features of cytochrome oxidase. Q. Rev. Biophys. 23, 331–366.

    • Crossref
    • PubMed
    • Export Citation
  • Saraste, M. and Castresana, J. (1994). Cytochrome oxidase evolved by tinkering with denitrification enzymes. FEBS Lett. 341, 1–4.

    • Crossref
    • PubMed
    • Export Citation
  • Schägger, H. and Pfeiffer, K. (2000). Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 19, 1777–1783.

    • Crossref
    • PubMed
    • Export Citation
  • Schatz, G. (1968). Impaired binding of mitochondrial adenosine triphosphatase in the cytoplasmic “petite” mutant of Saccharomyces cerevisiae. J. Biol. Chem. 243, 2192–2199.

    • PubMed
    • Export Citation
  • Séraphin, B., Simon, M., and Faye, G. (1988). MSS18, a yeast nuclear gene involved in the splicing of intron aI5 beta of the mitochondrial cox1 transcript. EMBO J. 7, 1455–1464.

    • Crossref
    • PubMed
    • Export Citation
  • Seraphin, B., Simon, M., Boulet, A., and Faye, G. (1989). Mitochondrial splicing requires a protein from a novel helicase family. Nature 337, 84–87.

    • Crossref
    • PubMed
    • Export Citation
  • Sharma, V., Ala-Vannesluoma, P., Vattulainen, I., Wikström, M., and Róg, T. (2015). Role of subunit III and its lipids in the molecular mechanism of cytochrome c oxidase. Biochim. Biophys. Acta 1847, 690–697.

    • Crossref
    • PubMed
    • Export Citation
  • Simon, M. and Faye, G. (1984). Organization and processing of the mitochondrial oxi3/oli2 multigenic transcript in yeast. Mol. Gen. Genet. 196, 266–274.

    • Crossref
    • PubMed
    • Export Citation
  • Smith, D., Gray, J., Mitchell, L., Antholine, W.E., and Hosler, J.P. (2005). Assembly of cytochrome c oxidase in the absence of the assembly protein Surf1p leads to loss of the active site heme. J. Biol. Chem. 280, 17652–17656.

    • Crossref
    • PubMed
    • Export Citation
  • Soma, S., Morgada, M.N., Naik, M.T., Boulet, A., Roesler, A., Dziuba, N., Ghosh, A., Yu, Q., Lindahl, P.A., Ames, J.B., et al. (2019). COA6 Is structurally tuned to function as a thiol-disulfide oxidoreductase in copper delivery to mitochondrial cytochrome c oxidase. Cell Rep. 29, 4114–4126.

    • Crossref
    • PubMed
    • Export Citation
  • Soto, I.C., Fontanesi, F., Myers, R.S., Hamel, P., and Barrientos, A. (2012). A heme-sensing mechanism in the translational regulation of mitochondrial cytochrome c oxidase biogenesis. Cell Metab. 16, 801–813.

    • Crossref
    • PubMed
    • Export Citation
  • Spannagel, C., Vaillier, J., Arselin, G., Graves, P.V., and Velours, J. (1997). The subunit f of mitochondrial yeast ATP synthase—characterization of the protein and disruption of the structural gene ATP17. Eur. J. Biochem. 247, 1111–1117.

    • Crossref
    • PubMed
    • Export Citation
  • Srivastava, A.P., Luo, M., Zhou, W., Symersky, J., Bai, D., Chambers, M.G., Faraldo-Gómez, J.D., Liao, M., and Mueller, D.M. (2018). High-resolution cryo-EM analysis of the yeast ATP synthase in a lipid membrane. Science 11, 360.

  • Stock, D., Leslie, A.G., and Walker, J.E. (1999). Molecular architecture of the rotary motor in ATP synthase. Science 286, 1700–1705.

    • Crossref
    • PubMed
    • Export Citation
  • Stock, D., Gibbons, C., Arechaga, I., Leslie, A.G., and Walker, J.E. (2000). The rotary mechanism of ATP synthase. Curr. Opin. Struct. Biol. 10, 672–679.

    • Crossref
    • PubMed
    • Export Citation
  • Strogolova, V., Hoang, N.H., Hosler, J., and Stuart, R.A. (2019). The yeast mitochondrial proteins Rcf1 and Rcf2 support the enzymology of the cytochrome c oxidase complex and generation of the proton motive force. J. Biol. Chem. 294, 4867–4877.

    • Crossref
    • PubMed
    • Export Citation
  • Strogolova, V., Furness, A., Robb-McGrath, M., Garlich, J., and Stuart, R.A. (2012). Rcf1 and Rcf2, members of the hypoxia-induced gene 1 protein family, are critical components of the mitochondrial cytochrome bc1–cytochrome c oxidase supercomplex. Mol. Cell Biol. 32, 1363–1373.

    • Crossref
    • PubMed
    • Export Citation
  • Stroh, A., Anderka, O., Pfeiffer, K., Yagi, T., Finel, M., Ludwig, B., and Schägger, H. (2004). Assembly of respiratory complexes I, III, and IV into NADH oxidase supercomplex stabilizes complex I in Paracoccus denitrificans. J. Biol. Chem. 279, 5000–5007.

    • Crossref
    • PubMed
    • Export Citation
  • Su, C.H. and Tzagoloff, A. (2017). Cox16 protein is physically associated with Cox1p assembly intermediates and with cytochrome oxidase. J. Biol. Chem. 292, 16277–16283.

    • Crossref
    • PubMed
    • Export Citation
  • Su, C.H., McStay, G.P., and Tzagoloff, A. (2014). The Cox3p assembly module of yeast cytochrome oxidase. Mol. Biol. Cell. 25, 965–976.

    • Crossref
    • PubMed
    • Export Citation
  • Suzuki, T., Ozaki, Y., Sone, N., Feniouk, B.A., and Yoshida, M. (2007). The product of uncI gene in F1Fo–ATP synthase operon plays a chaperone-like role to assist c-ring assembly. Proc. Natl. Acad. Sci. U.S.A. 104, 20776–20781.

    • Crossref
    • Export Citation
  • Suzuki, T., Iida, N., Suzuki, J., Watanabe, Y., Endo, T., Hisabori, T., and Yoshida, M. (2016). Expression of mammalian mitochondrial F1–ATPase in Escherichia coli depends on two chaperone factors, AF1 and AF2. FEBS Open Bio. 6, 1267–1272.

    • Crossref
    • PubMed
    • Export Citation
  • Symersky, J., Pagadala, V., Osowski, D., Krah, A., Meier, T., Faraldo-Gómez, J.D., and Mueller, D.M. (2012). Structure of the c10 ring of the yeast mitochondrial ATP synthase in the open conformation. Nat. Struct. Mol. Biol. 19, 485–491.

    • Crossref
    • Export Citation
  • Szklarczyk, R., Wanschers, B.F., Cuypers, T.D., Esseling, J.J., Riemersma, M., van den Brand, M.A., Gloerich, J., Lasonder, E., van den Heuvel, L.P., Nijtmans, L.G., et al. (2012). Iterative orthology prediction uncovers new mitochondrial proteins and identifies C12orf62 as the human ortholog of COX14, a protein involved in the assembly of cytochrome c oxidase. Genome Biol. 13, R12.

    • Crossref
    • PubMed
    • Export Citation
  • Taylor, N.G., Swenson, S., Harris, N.J., Germany, E.M., Fox, J.L., and Khalimonchuk, O. (2017). The assembly factor Pet117 couples heme a synthase activity to cytochrome oxidase assembly. J. Biol. Chem. 292, 1815–1825.

    • Crossref
    • PubMed
    • Export Citation
  • Trueblood, C.E. and Poyton, R.O. (1987). Differential effectiveness of yeast cytochrome c oxidase subunit genes results from differences in expression not function. Mol. Cell. Biol. 7, 3520–3526.

    • Crossref
    • PubMed
    • Export Citation
  • Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., and Yoshikawa, S. (1996). The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272, 1136–1144.

    • Crossref
    • PubMed
    • Export Citation
  • Turk, E.M. and Caprara, M.G. (2010). Splicing of yeast aI5beta group I intron requires SUV3 to recycle MRS1 via mitochondrial degradosome-promoted decay of excised intron ribonucleoprotein (RNP). J. Biol. Chem. 285, 8585–8594.

    • Crossref
    • Export Citation
  • Tzagoloff, A. (1969). Assembly of the mitochondrial membrane system. II. Synthesis of the mitochondrial adenosine triphosphatase F1. J. Biol. Chem. 244, 5027–5033.

    • PubMed
    • Export Citation
  • Tzagoloff, A. and Akai, A. (1972). Assembly of the mitochondrial membrane system. 8. Properties of the products of mitochondrial protein synthesis in yeast. J. Biol. Chem. 247, 6517–6523.

    • PubMed
    • Export Citation
  • Tzagoloff, A. and Dieckmann, C.L. (1990). PET genes of Saccharomyces cerevisiae. Microbiol. Rev. 54, 211–225.

    • Crossref
    • PubMed
    • Export Citation
  • Tzagoloff, A., MacLennan, D.H., McConnell, D.G., and Green, D.E. (1967). Studies on the electron transfer system. Formation of membranes as the basis of the reconstitution of the mitochondrial electron transfer system. J. Biol. Chem. 242, 2051–2061.

    • PubMed
    • Export Citation
  • Tzagoloff, A., Nobrega, M., Gorman, N., and Sinclair, P. (1993). On the functions of the yeast COX10 and COX11 gene products. Biochem. Mol. Biol. Int. 31, 593–598.

    • PubMed
    • Export Citation
  • Tzagoloff, A., Barrientos, A., Neupert, W., and Herrmann, J.M. (2004). Atp10p assists assembly of Atp6p into the F0 unit of the yeast mitochondrial ATPase. J. Biol. Chem. 279, 19775–19780.

    • Crossref
    • PubMed
    • Export Citation
  • Valencik, M.L., Kloeckener-Gruissem, B., Poyton, R.O., and McEwen, J.E. (1989). Disruption of the yeast nuclear PET54 gene blocks excision of mitochondrial intron aI5 beta from pre-mRNA for cytochrome c oxidase subunit I. EMBO J. 8, 3899–3904.

    • Crossref
    • PubMed
    • Export Citation
  • Walker, J.E. (1998). ATP synthesis by rotary catalysis. (Nobel Lecture). Angew. Chem. Int. Ed. Engl. 37, 2308–2319.

    • Crossref
    • PubMed
    • Export Citation
  • Walker, J.E. and Dickson, V.K. (2006). The peripheral stalk of the mitochondrial ATP synthase. Biochim. Biophys. Acta 1757, 286–296.

    • Crossref
    • PubMed
    • Export Citation
  • Wang, Z.G. and Ackerman, S.H. (2000). The assembly factor Atp11p binds to the β-subunit of the mitochondrial F1–ATPase. J. Biol. Chem. 275, 5767–5772.

    • Crossref
    • PubMed
    • Export Citation
  • Wang, Z.G., White, P.S., and Ackerman, S.H. (2001). Atp11p and Atp12p are assembly factors for the F1–ATPase in human mitochondria. J. Biol. Chem. 276, 30773–30778.

    • Crossref
    • PubMed
    • Export Citation
  • Watt, I.N., Montgomery, M.G., Runswick, M.J., Leslie, A.G.W., Walker, J.E. (2010). Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proc. Natl. Acad. Sci. U.S.A. 107, 16823–16827.

    • Crossref
    • PubMed
    • Export Citation
  • Watts, T., Khalimonchuk, O., Wolf, R.Z., Turk, E.M., Mohr, G., and Winge, D.R. (2011). Mne1 is a novel component of the mitochondrial splicing apparatus responsible for processing of a COX1 group I intron in yeast. J. Biol. Chem. 286, 10137–10146.

    • Crossref
    • Export Citation
  • Wiesenberger, G., Costanzo, M.C., and 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.

    • Crossref
    • PubMed
    • Export Citation
  • Wikstrom, M. (1989). Identification of the electron transfers in cytochrome oxidase that are coupled to proton-pumping. Nature 338, 776–778.

    • Crossref
    • PubMed
    • Export Citation
  • Wu, M., Gu, J., Guo, R., Huang, Y., and Yang, M. (2016). Structure of mammalian respiratory supercomplex I1, III2, IV1. Cell 167, 1598–1609.

    • Crossref
    • Export Citation
  • Zamudio-Ochoa, A., Camacho-Villasana, Y., García-Guerrero, A.E., and Pérez-Martínez, X. (2014). The Pet309 pentatricopeptide repeat motifs mediate efficient binding to the mitochondrial COX1 transcript in yeast. RNA Biol. 11, 953–967.

    • Crossref
    • PubMed
    • Export Citation
  • Zeng, X., Kucharczyk, R., di Rago, J.P., and Tzagoloff, A. (2007a). The leader peptide of yeast Atp6p is required for efficient interaction with the Atp9p ring of the mitochondrial ATPase. J. Biol. Chem. 282, 36167–36176.

    • Crossref
    • Export Citation
  • Zeng, X., Neupert, W., and Tzagoloff, A. (2007b). The metalloprotease encoded by ATP23 has a dual function in processing and assembly of subunit 6 of mitochondrial ATPase. Mol. Biol. Cell 18, 617–626.

    • Crossref
    • Export Citation
  • Zeng, X., Barros, M.H., Shulman, T., and Tzagoloff, A. (2008). ATP25, a new nuclear gene of Saccharomyces cerevisiae required for expression and assembly of the Atp9p subunit of mitochondrial ATPase. Mol. Biol. Cell 19, 1366–1377.

    • Crossref
    • PubMed
    • Export Citation
  • Ziaja, K., Michaelis, G., and Lisowsky, T. (1993). Nuclear control of the messenger RNA expression for mitochondrial ATPase subunit 9 in a new yeast mutant. J. Mol. Biol. 229, 909–916.

    • Crossref
    • Export Citation
Purchase article
Get instant unlimited access to the article.
$42.00
Log in
Already have access? Please log in.


or
Log in with your institution

Journal + Issues

Biological Chemistry keeps you up-to-date with the latest advances in the molecular life sciences. The journal publishes Research Articles, Short Communications, Reviews and Minireviews. Areas include: general biochemistry/pathobiochemistry, structural biology, molecular and cellular biology, genetics and epigenetics, virology, molecular medicine, plant molecular biology/biochemistry and novel experimental methodologies.

Search