Startseite Modular assembly of yeast mitochondrial ATP synthase and cytochrome oxidase
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Modular assembly of yeast mitochondrial ATP synthase and cytochrome oxidase

  • Leticia Veloso Ribeiro Franco , Chen Hsien Su und Alexander Tzagoloff ORCID logo EMAIL logo
Veröffentlicht/Copyright: 6. Mai 2020

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.

Acknowledgments

This research was supported by a National Institutes of Health Grant Funder Id: http://dx.doi.org/10.13039/100000057, 5R01GM111864 to A.T. and a FAPESP postdoctoral fellowship Funder Id: http://dx.doi.org/10.13039/501100001807, 2019/16015-3 to L.V.R.F.

References

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, 621–628.10.1038/370621a0Suche in Google Scholar

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, 4986–4990.10.1073/pnas.87.13.4986Suche in Google Scholar

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, 9952–9969.10.1016/S0021-9258(19)38763-0Suche in Google Scholar

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, e32572.10.7554/eLife.32572Suche in Google Scholar

Arechaga, I., Butler, P.J., and Walker, J.E. (2002). Self-assembly of ATP synthase subunit c rings. FEBS Lett. 515, 189–193.10.1016/S0014-5793(02)02447-XSuche in Google Scholar

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, 7170–7178.10.1093/emboj/17.24.7170Suche in Google Scholar PubMed PubMed Central

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, 36–40.10.1074/jbc.274.1.36Suche in Google Scholar PubMed

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, 1875–1884.10.1046/j.1432-1033.2003.03557.xSuche in Google Scholar PubMed

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, 2400–2404.10.1128/JB.01390-08Suche in Google Scholar PubMed PubMed Central

Barrientos, A., Pierre, D., Lee, J., and Tzagoloff, A. (2003). Cytochrome oxidase assembly does not require catalytically active cytochrome C. J. Biol. Chem. 278, 8881–8887.10.1074/jbc.M212427200Suche in Google Scholar PubMed

Barrientos, A., Zambrano, A., and Tzagoloff, A. (2004). Mss51p and Cox14p jointly regulate mitochondrial Cox1p expression in Saccharomyces cerevisiae. EMBO J. 23, 3472–3482.10.1038/sj.emboj.7600358Suche in Google Scholar

Barros, M.H. and Tzagoloff, A. (2002). Regulation of the heme A biosynthetic pathway in Saccharomyces cerevisiae. FEBS Lett. 516, 119–123.10.1016/S0014-5793(02)02514-0Suche in Google Scholar

Barros, M.H. and Tzagoloff, A. (2017). Aep3p-dependent translation of yeast mitochondrial ATP8. Mol. Biol. Cell 28, 1426–1434.10.1091/mbc.e16-11-0775Suche in Google Scholar

Barros, M.H. and McStay, G.P. (2020). Modular biogenesis of mitochondrial respiratory complexes. Mitochondrion 50, 94–114.10.1016/j.mito.2019.10.008Suche in Google Scholar

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, 133–138.10.1016/S0014-5793(01)02249-9Suche in Google Scholar

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, 3743–3751.10.1074/jbc.M510778200Suche in Google Scholar

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, 167–176.10.1007/BF00282462Suche in Google Scholar

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, 172–185.10.1128/MCB.00869-09Suche in Google Scholar

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, 4250–4255.10.1073/pnas.1816556116Suche in Google Scholar

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, 11927–11941.10.1016/S0021-9258(19)70224-5Suche in Google Scholar

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, 7774–7783.10.1074/jbc.M117.778514Suche in Google Scholar

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, 31258–31269.10.1074/jbc.M112.383562Suche in Google Scholar

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, 2901–2913.10.1093/hmg/ddu003Suche in Google Scholar

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, 117–124.10.1007/BF00312599Suche in Google Scholar

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, 7517–7523.10.1016/S0021-9258(20)89477-0Suche in Google Scholar

Boyer, P.D. (1997). The ATP synthase—a splendid molecular machine. Annu. Rev. Biochem. 66, 717–749.10.1146/annurev.biochem.66.1.717Suche in Google Scholar

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, 588–596.10.1016/S0022-2836(05)80140-8Suche in Google Scholar

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, 3770–3775.10.1074/jbc.M209893200Suche in Google Scholar

Chance, B. and Williams, G.R. (1955). Respiratory enzymes in oxidative phosphorylation. IV. The respiratory chain. J. Biol. Chem. 217, 429–438.10.1016/S0021-9258(19)57192-7Suche in Google Scholar

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, 620–625.10.1038/337620a0Suche in Google Scholar PubMed

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, 14025–14033.10.1016/S0021-9258(17)44019-1Suche in Google Scholar

Church, G.M., Slonimski, P.P., and Gilbert, W. (1979). Pleiotropic mutations within two yeast mitochondrial cytochrome genes block mRNA processing. Cell 18, 1209–1215.10.1016/0092-8674(79)90233-2Suche in Google Scholar

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, 1–4.10.1016/j.febslet.2004.08.065Suche in Google Scholar PubMed

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, 18093–18098.10.1074/jbc.M001901200Suche in Google Scholar PubMed

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, 1555.10.3389/fphys.2019.01555Suche in Google Scholar PubMed PubMed Central

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, 14121–14126.10.1073/pnas.1103621108Suche in Google Scholar PubMed PubMed Central

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, 1644–1655.10.1016/j.celrep.2015.08.009Suche in Google Scholar PubMed

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, 1015–1019.10.1073/pnas.82.4.1015Suche in Google Scholar PubMed PubMed Central

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, 29502–29510.10.1074/jbc.M110.124529Suche in Google Scholar PubMed PubMed Central

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, 111–118.10.1007/BF00259457Suche in Google Scholar PubMed

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, 559–567.10.1534/genetics.111.135665Suche in Google Scholar

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, 1353–1363.10.1093/genetics/151.4.1353Suche in Google Scholar

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, 15728–15733.10.1074/jbc.M314162200Suche in Google Scholar

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, 505–508.10.1016/0014-5793(95)00727-QSuche in Google Scholar

Ferguson-Miller, S. and Babcock, G.T. (1996). Heme/copper terminal oxidases. Chem. Rev. 96, 2889–2908.10.1021/cr950051sSuche in Google Scholar

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, 232–245.10.1016/S0005-2736(02)00572-2Suche in Google Scholar

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, 245–259.10.1128/MCB.00983-09Suche in Google Scholar

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, 555–566.10.1074/jbc.M110.188805Suche in Google Scholar

Foury, F., Roganti, T., Lecrenier, N., and Purnelle, B. (1998). The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett. 440, 325–331.10.1016/S0014-5793(98)01467-7Suche in Google Scholar

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, 16899–16911.10.1074/jbc.RA118.004138Suche in Google Scholar PubMed PubMed Central

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, 2707–2712.10.1016/j.febslet.2015.08.006Suche in Google Scholar

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, 10912–10925.10.1074/jbc.M116.773077Suche in Google Scholar

Genova, M.L. and Lenaz, G. (2014). Functional role of mitochondrial respiratory supercomplexes. Biochim. Biophys. Acta 837, 427–443.10.1016/j.bbabio.2013.11.002Suche in Google Scholar

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, 3596–3606.10.1093/hmg/ddu069Suche in Google Scholar

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, 20531–20535.10.1074/jbc.271.34.20531Suche in Google Scholar

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, 217–224.10.1007/BF00309780Suche in Google Scholar

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, 637–641.10.1038/35054586Suche in Google Scholar

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, 312–335.10.1016/0003-9861(67)90461-4Suche in Google Scholar

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, 6392–6397.10.1074/jbc.M009856200Suche in Google Scholar PubMed

Guo, H., Suzuki, T., and Rubinstein, J.L. (2019). Structure of a bacterial ATP synthase. Elife 8.10.7554/eLife.43128Suche in Google Scholar PubMed PubMed Central

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, 212–222.10.1016/0005-2728(88)90072-2Suche in Google Scholar

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, 78–83.10.1038/s41594-018-0172-zSuche in Google Scholar

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, 1676–1680.10.1016/S0021-9258(19)83761-4Suche in Google Scholar

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, 1681–1685.10.1016/S0021-9258(19)83762-6Suche in Google Scholar

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, 2661–2669.10.1016/S0021-9258(19)73804-6Suche in Google Scholar

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, 367–370.10.1016/S0014-5793(97)01412-9Suche in Google Scholar

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, 2250–2255.10.1073/pnas.95.5.2250Suche in Google Scholar PubMed PubMed Central

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, 4571–4578.10.1074/jbc.275.7.4571Suche in Google Scholar PubMed

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, 473–483.10.1002/j.1460-2075.1988.tb02835.xSuche in Google Scholar PubMed PubMed Central

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, 893–902.10.1083/jcb.127.4.893Suche in Google Scholar PubMed PubMed Central

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, 25880–25894.10.1074/jbc.M113.484675Suche in Google Scholar

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, 660–669.10.1038/376660a0Suche in Google Scholar

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, 483–491.10.1007/s004380051192Suche in Google Scholar

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, 1897–1908.10.1091/mbc.e06-10-0925Suche in Google Scholar

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, 7528–7536.10.1074/jbc.RA118.005355Suche in Google Scholar

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, 2461–246.10.1016/S0021-9258(18)96640-8Suche in Google Scholar

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, 13602–13607.10.1073/pnas.1204593109Suche in Google Scholar

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, 34484–34493.10.1074/jbc.M112.382630Suche in Google Scholar

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, 133–146.10.1016/0092-8674(93)90166-NSuche in Google Scholar

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, 302–307.10.1007/s002940050209Suche in Google Scholar PubMed

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, 1004–1017.10.1128/MCB.00640-09Suche in Google Scholar

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, 22473–22480.10.1016/S0021-9258(18)41696-1Suche in Google Scholar

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, 333–348.10.1016/0092-8674(80)90344-XSuche in Google Scholar

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, 6789–6796.10.1074/jbc.M009557200Suche in Google Scholar PubMed

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, 18386–18392.10.1074/jbc.M410789200Suche in Google Scholar PubMed

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, 1624–1632.10.1016/j.bbamcr.2016.04.007Suche in Google Scholar PubMed

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, 2782–2793.10.1128/MCB.00361-16Suche in Google Scholar PubMed PubMed Central

Luck, D.J. (1963). Genesis of mitochondria in Neurospora crassa. Proc. Natl. Acad. Sci. U.S.A. 49, 233–240.10.1073/pnas.49.2.233Suche in Google Scholar PubMed PubMed Central

Ludlam, A., Brunzelle, J., Pribyl, T., Xu, X., Gatti, D.L., and Ackerman, S.H. (2009). Chaperones of F1–ATPase. J. Biol. Chem. 284, 17138–17146.10.1074/jbc.M109.002568Suche in Google Scholar PubMed PubMed Central

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, 24529–24534.10.1074/jbc.273.38.24529Suche in Google Scholar PubMed

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, 1624–1638.10.15252/embj.201488076Suche in Google Scholar

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, 4435–4451.10.1093/nar/11.13.4435Suche in Google Scholar

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, 4031–4043.10.1002/j.1460-2075.1995.tb00074.xSuche in Google Scholar

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, 9343–9355.10.1074/jbc.M116.721985Suche in Google Scholar

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, 11872–11879.10.1016/S0021-9258(18)67323-5Suche in Google Scholar

McStay, G.P., Su, C.H., and Tzagoloff, A. (2013a). Modular assembly of yeast cytochrome oxidase. Mol. Biol. Cell. 24, 440–452.10.1091/mbc.e12-10-0749Suche in Google Scholar

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, 26546–26556.10.1074/jbc.M113.498592Suche in Google Scholar PubMed PubMed Central

McStay, G.P., Su, C.H., and Tzagoloff, A. (2013c). Stabilization of Cox1p intermediates by the Cox14p–Coa3p complex. FEBS Lett. 587, 943–949.10.1016/j.febslet.2013.02.022Suche in Google Scholar PubMed PubMed Central

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, 141–154.10.1083/jcb.201007026Suche in Google Scholar PubMed PubMed Central

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, 14–20.10.1038/nrm3029Suche in Google Scholar PubMed PubMed Central

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, 1528–1541.10.1016/j.cell.2012.11.053Suche in Google Scholar PubMed

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, 23095–23103.10.1074/jbc.M112.367888Suche in Google Scholar PubMed PubMed Central

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, 2386–2396.10.1091/mbc.E18-04-0227Suche in Google Scholar PubMed PubMed Central

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, 475–484.10.1007/s00294-009-0260-zSuche in Google Scholar PubMed PubMed Central

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, 892–899.10.1038/nrmicro1767Suche in Google Scholar PubMed

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, 1237.10.1038/s41467-017-01437-zSuche in Google Scholar PubMed PubMed Central

Neupert, W. and Herrmann, J.M. (2007). Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723–749.10.1146/annurev.biochem.76.052705.163409Suche in Google Scholar PubMed

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, 3892–3905.10.1016/j.jmb.2018.04.036Suche in Google Scholar PubMed

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, 627–635.10.1091/mbc.e06-09-0839Suche in Google Scholar PubMed PubMed Central

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, 1603–1610.10.1038/sj.emboj.7601070Suche in Google Scholar PubMed PubMed Central

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, 663–666.10.1016/j.bbrc.2007.12.170Suche in Google Scholar PubMed

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, 126–135.10.1007/BF00324676Suche in Google Scholar PubMed

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, 409–416.10.1007/BF00311209Suche in Google Scholar PubMed

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, 5951–5961.10.1093/emboj/cdg566Suche in Google Scholar PubMed PubMed Central

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, 4371–4380.10.1091/mbc.e09-06-0522Suche in Google Scholar PubMed PubMed Central

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, 4335–4346.10.1038/sj.emboj.7601861Suche in Google Scholar PubMed PubMed Central

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, 1085–1096.10.1083/jcb.153.5.1085Suche in Google Scholar PubMed PubMed Central

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, 18509–18514.10.1073/pnas.0910351106Suche in Google Scholar PubMed PubMed Central

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, 10853–10864.10.1074/jbc.M608692200Suche in Google Scholar PubMed

Rak, M., Gokova, S., and Tzagoloff, A. (2011). Modular assembly of yeast mitochondrial ATP synthase. EMBO J. 30, 920–930.10.1038/emboj.2010.364Suche in Google Scholar PubMed PubMed Central

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, 919–929.10.1091/mbc.E15-09-0642Suche in Google Scholar

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, 50–57.10.1038/s41594-018-0169-7Suche in Google Scholar

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, 1896–1906.10.1074/mcp.M700098-MCP200Suche in Google Scholar

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, 15015–15022.10.1074/jbc.M710072200Suche in Google Scholar

Saddar, S., Dienhart, M.K., and Stuart, R.A. (2008). The F1F0–ATP synthase complex influences the assembly state of the cytochrome bc1-cytochrome oxidase supercomplex and its association with the TIM23 machinery. J. Biol. Chem. 283, 6677–6686.10.1074/jbc.M708440200Suche in Google Scholar

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, 980–990.10.1016/j.bbabio.2016.03.031Suche in Google Scholar

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, 1122–113110.1091/mbc.01-12-0580Suche in Google Scholar

Saraste, M. (1990). Structural features of cytochrome oxidase. Q. Rev. Biophys. 23, 331–366.10.1017/S0033583500005588Suche in Google Scholar

Saraste, M. and Castresana, J. (1994). Cytochrome oxidase evolved by tinkering with denitrification enzymes. FEBS Lett. 341, 1–4.10.1016/0014-5793(94)80228-9Suche in Google Scholar

Schägger, H. and Pfeiffer, K. (2000). Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 19, 1777–1783.10.1093/emboj/19.8.1777Suche in Google Scholar PubMed PubMed Central

Schatz, G. (1968). Impaired binding of mitochondrial adenosine triphosphatase in the cytoplasmic “petite” mutant of Saccharomyces cerevisiae. J. Biol. Chem. 243, 2192–2199.10.1016/S0021-9258(18)93462-9Suche in Google Scholar

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, 1455–1464.10.1002/j.1460-2075.1988.tb02963.xSuche in Google Scholar PubMed PubMed Central

Seraphin, B., Simon, M., Boulet, A., and Faye, G. (1989). Mitochondrial splicing requires a protein from a novel helicase family. Nature 337, 84–87.10.1038/337084a0Suche in Google Scholar PubMed

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, 690–697.10.1016/j.bbabio.2015.04.007Suche in Google Scholar PubMed

Simon, M. and Faye, G. (1984). Organization and processing of the mitochondrial oxi3/oli2 multigenic transcript in yeast. Mol. Gen. Genet. 196, 266–274.10.1007/BF00328059Suche in Google Scholar PubMed

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, 17652–17656.10.1074/jbc.C500061200Suche in Google Scholar PubMed

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, 4114–4126.10.1016/j.celrep.2019.11.054Suche in Google Scholar PubMed PubMed Central

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, 801–813.10.1016/j.cmet.2012.10.018Suche in Google Scholar PubMed PubMed Central

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, 1111–1117.10.1111/j.1432-1033.1997.01111.xSuche in Google Scholar PubMed

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, 360.10.1126/science.aas9699Suche in Google Scholar PubMed PubMed Central

Stock, D., Leslie, A.G., and Walker, J.E. (1999). Molecular architecture of the rotary motor in ATP synthase. Science 286, 1700–1705.10.1126/science.286.5445.1700Suche in Google Scholar

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, 672–679.10.1016/S0959-440X(00)00147-0Suche in Google Scholar

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, 4867–4877.10.1074/jbc.RA118.006888Suche in Google Scholar PubMed PubMed Central

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, 1363–1373.10.1128/MCB.06369-11Suche in Google Scholar PubMed PubMed Central

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, 5000–5007.10.1074/jbc.M309505200Suche in Google Scholar PubMed

Su, C.H. and Tzagoloff, A. (2017). Cox16 protein is physically associated with Cox1p assembly intermediates and with cytochrome oxidase. J. Biol. Chem. 292, 16277–16283.10.1074/jbc.M117.801811Suche in Google Scholar PubMed PubMed Central

Su, C.H., McStay, G.P., and Tzagoloff, A. (2014). The Cox3p assembly module of yeast cytochrome oxidase. Mol. Biol. Cell. 25, 965–976.10.1091/mbc.e13-10-0575Suche in Google Scholar

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, 20776–20781.10.1073/pnas.0708075105Suche in Google Scholar PubMed PubMed Central

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, 1267–1272.10.1002/2211-5463.12143Suche in Google Scholar PubMed PubMed Central

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, 485–491.10.1038/nsmb.2284Suche in Google Scholar PubMed PubMed Central

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, R12.10.1186/gb-2012-13-2-r12Suche in Google Scholar

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, 1815–1825.10.1074/jbc.M116.766980Suche in Google Scholar

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, 3520–3526.10.1128/MCB.7.10.3520Suche in Google Scholar

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, 1136–1144.10.1126/science.272.5265.1136Suche in Google Scholar

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, 8585–8594.10.1074/jbc.M109.090761Suche in Google Scholar

Tzagoloff, A. (1969). Assembly of the mitochondrial membrane system. II. Synthesis of the mitochondrial adenosine triphosphatase F1. J. Biol. Chem. 244, 5027–5033.10.1016/S0021-9258(18)94305-XSuche in Google Scholar

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, 6517–6523.10.1016/S0021-9258(19)44723-6Suche in Google Scholar

Tzagoloff, A. and Dieckmann, C.L. (1990). PET genes of Saccharomyces cerevisiae. Microbiol. Rev. 54, 211–225.10.1128/mr.54.3.211-225.1990Suche in Google Scholar

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, 2051–2061.10.1016/S0021-9258(18)96015-1Suche in Google Scholar

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.Suche in Google Scholar

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, 19775–19780.10.1074/jbc.M401506200Suche in Google Scholar PubMed

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, 3899–3904.10.1002/j.1460-2075.1989.tb08569.xSuche in Google Scholar PubMed PubMed Central

Walker, J.E. (1998). ATP synthesis by rotary catalysis. (Nobel Lecture). Angew. Chem. Int. Ed. Engl. 37, 2308–2319.10.1002/(SICI)1521-3773(19980918)37:17<2308::AID-ANIE2308>3.0.CO;2-WSuche in Google Scholar

Walker, J.E. and Dickson, V.K. (2006). The peripheral stalk of the mitochondrial ATP synthase. Biochim. Biophys. Acta 1757, 286–296.10.1016/j.bbabio.2006.01.001Suche in Google Scholar

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, 5767–5772.10.1074/jbc.275.8.5767Suche in Google Scholar

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, 30773–30778.10.1074/jbc.M104133200Suche in Google Scholar

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, 16823–16827.10.1073/pnas.1011099107Suche in Google Scholar

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, 10137–10146.10.1074/jbc.M110.205625Suche in Google Scholar

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, 3291–3300.10.1128/MCB.15.6.3291Suche in Google Scholar

Wikstrom, M. (1989). Identification of the electron transfers in cytochrome oxidase that are coupled to proton-pumping. Nature 338, 776–778.10.1038/338776a0Suche in Google Scholar

Wu, M., Gu, J., Guo, R., Huang, Y., and Yang, M. (2016). Structure of mammalian respiratory supercomplex I1, III2, IV1. Cell 167, 1598–1609.10.1016/j.cell.2016.11.012Suche in Google Scholar

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, 953–967.10.4161/rna.29780Suche in Google Scholar

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, 36167–36176.10.1074/jbc.M705436200Suche in Google Scholar PubMed

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, 617–626.10.1091/mbc.e06-09-0801Suche in Google Scholar PubMed PubMed Central

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, 1366–1377.10.1091/mbc.e07-08-0746Suche in Google Scholar PubMed PubMed Central

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, 909–916.10.1006/jmbi.1993.1095Suche in Google Scholar PubMed

Received: 2020-01-13
Accepted: 2020-02-24
Published Online: 2020-05-06
Published in Print: 2020-05-26

©2020 Walter de Gruyter GmbH, Berlin/Boston

Artikel in diesem Heft

  1. Frontmatter
  2. Highlight: In Honor of Walter Neupert: Mitochondria
  3. Editorial
  4. Mitochondria and friends – a special issue in honor of Walter Neupert (1939–2019)
  5. Early steps in mitochondrial protein translocation
  6. From cytosol to mitochondria: the beginning of a protein journey
  7. Evolution of mitochondrial protein import – lessons from trypanosomes
  8. Protein import: crossing the outer membrane
  9. Biogenesis pathways of α-helical mitochondrial outer membrane proteins
  10. The structure of the TOM core complex in the mitochondrial outer membrane
  11. Porins as helpers in mitochondrial protein translocation
  12. Protein translocation beyond the outer membrane
  13. From TOM to the TIM23 complex – handing over of a precursor
  14. How to get to the other side of the mitochondrial inner membrane – the protein import motor
  15. The biogenesis of mitochondrial intermembrane space proteins
  16. Protein import by the mitochondrial disulfide relay in higher eukaryotes
  17. Mitochondrial ultrastructure and dynamics
  18. The MICOS complex, a structural element of mitochondria with versatile functions
  19. Asymmetric inheritance of mitochondria in yeast
  20. Lipid transport and mitochondrial contact sites
  21. New horizons in mitochondrial contact site research
  22. The endoplasmic reticulum-mitochondria encounter structure: coordinating lipid metabolism across membranes
  23. Lipid homeostasis in mitochondria
  24. The biogenesis of enzymes
  25. Modular assembly of yeast mitochondrial ATP synthase and cytochrome oxidase
  26. From the discovery to molecular understanding of cellular iron-sulfur protein biogenesis
  27. Mitochondrial quality control
  28. Regulation of mitochondrial plasticity by the i-AAA protease YME1L
  29. PINK1 and Parkin: team players in stress-induced mitophagy
Heruntergeladen am 9.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/hsz-2020-0112/html
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