DOI: 10.1093/genetics/150.2.601. Mutations in the Membrane Anchor of Yeast Cytochrome c1 Compensate for the Absence of Oxa1p and Generate Carbonate-Extractable Forms of Cytochrome c1

Mutations in the Membrane Anchor of Yeast Cytochrome c1 Compensate for the Absence of Oxa1p and Generate Carbonate-Extractable Forms of Cytochrome c1

10.1093/genetics/150.2.601

Crossref journal-article

Oxford University Press (OUP)

Genetics (286)

Abstract

Abstract Oxa1p is a mitochondrial inner membrane protein that is mainly required for the insertion/assembly of complex IV and ATP synthase and is functionally conserved in yeasts, humans, and plants. We have isolated several independent suppressors that compensate for the absence of Oxa1p. Molecular cloning and sequencing reveal that the suppressor mutations (CYT1-1 to -6) correspond to amino acid substitutions that are all located in the membrane anchor of cytochrome c1 and decrease the hydrophobicity of this anchor. Cytochrome c1 is a catalytic subunit of complex III, but the CYT1-1 mutation does not seem to affect the electron transfer activity. The double-mutant cyt1-1,164, which has a drastically reduced electron transfer activity, still retains the suppressor activity. Altogether, these results suggest that the suppressor function of cytochrome c1 is independent of its electron transfer activity. In addition to the membranebound cytochrome c1, carbonate-extractable forms accumulate in all the suppressor strains. We propose that these carbonate-extractable forms of cytochrome c1 are responsible for the suppressor function by preventing the degradation of the respiratory complex subunits that occur in the absence of Oxa1p.

Bibliography

Hamel, P., Lemaire, C., Bonnefoy, N., Brivet-Chevillotte, P., & Dujardin, G. (1998). Mutations in the Membrane Anchor of Yeast Cytochrome c1 Compensate for the Absence of Oxa1p and Generate Carbonate-Extractable Forms of Cytochrome c1. Genetics, 150(2), 601â611.

Authors 5

Patrice Hamel (first)
Claire Lemaire (additional)
Nathalie Bonnefoy (additional)
Paule Brivet-Chevillotte (additional)
Geneviève Dujardin (additional)

References 39 Referenced 33

10.1016/0014-5793(96)00165-2 / FEBS lett. / The Saccharomyces cerevisiae OXA1 gene is required for the correct assembly of cytochrome c oxidase and oligomycinsensitive ATP synthase by Altamura (1996)
10.1016/S0092-8674(00)81271-4 / Cell / The YTA10-12 complex, an AAA protease with chaperon-like activity in the inner membrane of mitochondria by Artl (1996)
10.1007/BF00290106 / Mol. Gen. Genet. / PET1402, a nuclear gene required for proteolytic processing of cytochrome oxidase subunit 2 in yeast by Bauer (1994)
10.1006/jmbi.1994.1363 / J. Mol. Biol. / OXA1 a Saccharomyces cerevisiae nuclear gene, whose sequence is conserved in prokaryotes and eukaryotes, controls cytochrome c oxidase biogenesis by Bonnefoy (1994)
10.1073/pnas.91.25.11978 / Proc. Natl. Acad. Sci. USA / Cloning of a novel human gene involved in cytochrome oxidase assembly by functional complementation of an oxa1- mutation in Saccharomyces cerevisiae by Bonnefoy (1994)
10.1074/jbc.270.49.29356 / J. Biol. Chem. / Structure-function relationships of the mitochondrial bc1 complex in temperature-sensitive mutants of the cytochrome b gene, impaired in the catalytic center N by Brasseur (1995)
10.1007/BF02150679 / J. Bioenerg. Biomembr. / Subunit 8 of the Saccharomyces cerevisiae cytochrome bc1 complex interacts with succinate-ubiquinone reductase complex by Bruel (1996)
10.1007/BF00271736 / Mol. Gen. Genet. / Long range control circuits whithin mitochondria and between nucleus and mitochondria. I. Methodology and phenomenology of suppressors by Dujardin (1980)
10.1016/0003-2697(90)90018-5 / Anal. Biochem. / Detection of hemoprotein peroxidase activity on polyvinylidene difluoride membrane by Dutta (1990)
10.3109/10409239509085141 / Crit. Rev. Biochem. Mol. Biol. / Nucleo-mitochondrial interactions in mitochondrial gene expression by Grivell (1995)
10.1046/j.1365-313x.1997.12061319.x / Plant J. / Functional complementation of an oxa1- yeast mutation identifies an Arabidopsis thaliana cDNA involved in the assembly of respiratory complexes by Hamel (1997)
10.1093/oxfordjournals.jbchem.a122067 / J. Biochem. / Expression of modified cytochrome c1 genes and restoration of the respiratory function in a yeast mutant lacking the nuclear cytochrome c1 gene by Hase (1987)
10.1093/oxfordjournals.jbchem.a122068 / J. Biochem. / A carboxyl-terminal hydrophobic region of yeast cytochrome c1 is necessary for functionnal assembly into complex III of the respiratory chain by Hase (1987)
10.1091/mbc.8.8.1449 / Mol. Biol. Cell / Membrane translocation of mitochondrially coded Cox2p: distinct requirements for export of N and C termini and dependence on the conserved protein Oxa1p by He (1997)
10.1016/S0014-5793(97)01412-9 / FEBS Lett. / Oxa1p mediates the export of the N- and Ctermini of pCoxII from the mitochondrial matrix to the intermembrane space by Hell (1997)
10.1073/pnas.95.5.2250 / Proc. Natl. Acad. Sci. USA / Oxa1p, an essential component of the N-tail export machinery in mitochondria by Hell (1998)
10.1093/emboj/16.9.2217 / EMBO J. / Insertion into the mitochondrial inner membrane of a polytopic protein, the nuclear-encoded Oxa1p by Herrmann (1997)
10.1007/s002940050209 / Curr. Genet. / Oxa1p, which is required for cytochrome c oxidase and ATP synthase complex formation, is embedded in the mitochondrial inner membrane by Kermorgant (1997)
10.1016/S0021-9258(18)98678-3 / J. Biol. Chem. / Preparation and characterization of the water-soluble hemebinding domain of cytochrome c1 from Rhodobacter sphaeroides bc1 complex by Konishi (1991)
10.1111/j.1432-1033.1981.tb05319.x / Eur. J. Biochem. / Membrane-bound and watersoluble cytochrome c1 from Neurospora crassa by Li (1981)
10.1007/s002940050222 / Curr. Genet. / A mutation in cytochrome oxidase subunit 2 restores respiration of the mutant pet ts1402 by Meyer (1997)
10.1515/bchm.1997.378.11.1373 / Biol. Chem. / Mitochondrial inner membrane bound PET1402 protein is rapidly imported into mitochondria and affects the integrity of the cytochrome oxidase and ubiquinol-cytochrome c oxidoreductase complexes by Meyer (1997)
10.1093/oxfordjournals.jbchem.a123283 / J. Biochem. / Replacement of putative axial ligands of heme iron in yeast cytochrome c1 by site-directed mutagenesis by Nakai (1990)
{'key': '2022010310535438000_R24', 'first-page': '443', 'article-title': 'Regulation of cytochrome oxidase formation by mutations in a mitochondrial gene for cytochrome b', 'volume-title': 'Genetics and Biogenesis of Chloroplasts and Mitochondria.', 'author': 'Pajot', 'year': '1976'} / Genetics and Biogenesis of Chloroplasts and Mitochondria. / Regulation of cytochrome oxidase formation by mutations in a mitochondrial gene for cytochrome b by Pajot (1976)
10.1073/pnas.92.9.3735 / Proc. Natl. Acad. Sci. USA / Diminished degradation of yeast cytochrome c by interactions with its physiological partners by Pearce (1995)
10.1074/jbc.270.36.20879 / J. Biol. Chem. / Degradation of cytochrome oxidase subunits in mutants of yeast lacking cytochrome c and suppression of the degradation by mutation of yme1 by Pearce (1995)
10.1016/S0021-9258(20)81361-1 / J. Biol. Chem. / Partial resolution of the enzyme catalyzing oxidative phosphorylation. I. Purification and properties of soluble, dinitrophenol-stimulated adenosine triphosphatase by Pullman (1960)
10.1021/bi00127a036 / Biochemistry / Spin-label electron paramagnetic resonance and differential scanning calorimetry studies of the interactions between mitochondrial cytochrome c oxidase and adenosine triphosphate synthase complex by Qiu (1992)
10.1007/s002940050122 / Curr. Genet. / Three genes for mitochondrial proteins suppress null-mutations in both Afg3 and Rca1 when over-expressed by Rep (1996)
10.1007/s002940050145 / Curr. Genet. / The role of protein degradation in mitochondrial function and biogenesis by Rep (1996)
10.1002/j.1460-2075.1984.tb02103.x / EMBO J. / Sequencing of the nuclear gene for the yeast cytochrome c1 precursor reveals an unusually complex amino terminal sequence by Sadler (1984)
10.1016/S0968-0004(97)01020-7 / Trends Biochem. Sci. / ATP-dependent proteases that also chaperone protein biogenesis by Suzuki (1997)
{'key': '2022010310535438000_R33', 'first-page': '5418', 'article-title': 'Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae', 'volume': '13', 'author': 'Thorness', 'year': '1993', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae by Thorness (1993)
10.1128/mr.54.2.101-129.1990 / Microbiol. Rev. / Cytochrome bc1 complexes of microorganisms by Trumpower (1990)
10.1016/S0021-9258(18)47170-0 / J. Biol. Chem. / A new member of a family of ATPase is essential for assembly of mitochondrial respiratory chain and ATP synthetase complexes in Saccharomyces cerevisiae by Tzagoloff (1994)
10.1006/abio.1993.1127 / Anal. Biochem. / Detection of c-type cytochromes using enhanced chemiluminescence by Vargas (1993)
10.1016/0378-1119(91)90032-7 / Gene / New vectors in fission yeast: application for cloning the his2 gene by Weilguny (1991)
10.1126/science.277.5322.60 / Science / Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria by Xia (1997)
10.1038/33612 / Nature / Electron transfer by domain movement in cytochrome bc1 by Zhang (1998)

Dates

Type	When
Created	4 years, 4 months ago (April 27, 2021, 10:34 p.m.)
Deposited	3 years, 7 months ago (Jan. 3, 2022, 6:36 a.m.)
Indexed	1 year, 10 months ago (Oct. 29, 2023, 12:20 p.m.)
Issued	26 years, 10 months ago (Oct. 1, 1998)
Published	26 years, 10 months ago (Oct. 1, 1998)
Published Online	26 years, 10 months ago (Oct. 1, 1998)
Published Print	26 years, 10 months ago (Oct. 1, 1998)

Funders 0

None

BibTeX

@article{Hamel_1998, title={Mutations in the Membrane Anchor of Yeast Cytochrome c1 Compensate for the Absence of Oxa1p and Generate Carbonate-Extractable Forms of Cytochrome c1}, volume={150}, ISSN={1943-2631}, url={http://dx.doi.org/10.1093/genetics/150.2.601}, DOI={10.1093/genetics/150.2.601}, number={2}, journal={Genetics}, publisher={Oxford University Press (OUP)}, author={Hamel, Patrice and Lemaire, Claire and Bonnefoy, Nathalie and Brivet-Chevillotte, Paule and Dujardin, Geneviève}, year={1998}, month=oct, pages={601–611} }

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      "article-title": "The Saccharomyces cerevisiae OXA1 gene is required for the correct assembly of cytochrome c oxidase and oligomycinsensitive ATP synthase",
      "volume": "382",
      "author": "Altamura",
      "year": "1996",
      "journal-title": "FEBS lett."
    },
    {
      "key": "2022010310535438000_R2",
      "doi-asserted-by": "crossref",
      "first-page": "875",
      "DOI": "10.1016/S0092-8674(00)81271-4",
      "article-title": "The YTA10-12 complex, an AAA protease with chaperon-like activity in the inner membrane of mitochondria",
      "volume": "85",
      "author": "Artl",
      "year": "1996",
      "journal-title": "Cell"
    },
    {
      "key": "2022010310535438000_R3",
      "doi-asserted-by": "crossref",
      "first-page": "272",
      "DOI": "10.1007/BF00290106",
      "article-title": "PET1402, a nuclear gene required for proteolytic processing of cytochrome oxidase subunit 2 in yeast",
      "volume": "245",
      "author": "Bauer",
      "year": "1994",
      "journal-title": "Mol. Gen. Genet."
    },
    {
      "key": "2022010310535438000_R4",
      "doi-asserted-by": "crossref",
      "first-page": "201",
      "DOI": "10.1006/jmbi.1994.1363",
      "article-title": "OXA1 a Saccharomyces cerevisiae nuclear gene, whose sequence is conserved in prokaryotes and eukaryotes, controls cytochrome c oxidase biogenesis",
      "volume": "239",
      "author": "Bonnefoy",
      "year": "1994",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "2022010310535438000_R5",
      "doi-asserted-by": "crossref",
      "first-page": "11978",
      "DOI": "10.1073/pnas.91.25.11978",
      "article-title": "Cloning of a novel human gene involved in cytochrome oxidase assembly by functional complementation of an oxa1- mutation in Saccharomyces cerevisiae",
      "volume": "91",
      "author": "Bonnefoy",
      "year": "1994",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2022010310535438000_R6",
      "doi-asserted-by": "crossref",
      "first-page": "29356",
      "DOI": "10.1074/jbc.270.49.29356",
      "article-title": "Structure-function relationships of the mitochondrial bc1 complex in temperature-sensitive mutants of the cytochrome b gene, impaired in the catalytic center N",
      "volume": "270",
      "author": "Brasseur",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2022010310535438000_R7",
      "doi-asserted-by": "crossref",
      "first-page": "59",
      "DOI": "10.1007/BF02150679",
      "article-title": "Subunit 8 of the Saccharomyces cerevisiae cytochrome bc1 complex interacts with succinate-ubiquinone reductase complex",
      "volume": "28",
      "author": "Bruel",
      "year": "1996",
      "journal-title": "J. Bioenerg. Biomembr."
    },
    {
      "key": "2022010310535438000_R8",
      "doi-asserted-by": "crossref",
      "first-page": "469",
      "DOI": "10.1007/BF00271736",
      "article-title": "Long range control circuits whithin mitochondria and between nucleus and mitochondria. I. Methodology and phenomenology of suppressors",
      "volume": "179",
      "author": "Dujardin",
      "year": "1980",
      "journal-title": "Mol. Gen. Genet."
    },
    {
      "key": "2022010310535438000_R9",
      "doi-asserted-by": "crossref",
      "first-page": "96",
      "DOI": "10.1016/0003-2697(90)90018-5",
      "article-title": "Detection of hemoprotein peroxidase activity on polyvinylidene difluoride membrane",
      "volume": "184",
      "author": "Dutta",
      "year": "1990",
      "journal-title": "Anal. Biochem."
    },
    {
      "key": "2022010310535438000_R10",
      "doi-asserted-by": "crossref",
      "first-page": "121",
      "DOI": "10.3109/10409239509085141",
      "article-title": "Nucleo-mitochondrial interactions in mitochondrial gene expression",
      "volume": "30",
      "author": "Grivell",
      "year": "1995",
      "journal-title": "Crit. Rev. Biochem. Mol. Biol."
    },
    {
      "key": "2022010310535438000_R11",
      "doi-asserted-by": "crossref",
      "first-page": "101",
      "DOI": "10.1046/j.1365-313x.1997.12061319.x",
      "article-title": "Functional complementation of an oxa1- yeast mutation identifies an Arabidopsis thaliana cDNA involved in the assembly of respiratory complexes",
      "volume": "12",
      "author": "Hamel",
      "year": "1997",
      "journal-title": "Plant J."
    },
    {
      "key": "2022010310535438000_R12",
      "doi-asserted-by": "crossref",
      "first-page": "401",
      "DOI": "10.1093/oxfordjournals.jbchem.a122067",
      "article-title": "Expression of modified cytochrome c1 genes and restoration of the respiratory function in a yeast mutant lacking the nuclear cytochrome c1 gene",
      "volume": "102",
      "author": "Hase",
      "year": "1987",
      "journal-title": "J. Biochem."
    },
    {
      "key": "2022010310535438000_R13",
      "doi-asserted-by": "crossref",
      "first-page": "411",
      "DOI": "10.1093/oxfordjournals.jbchem.a122068",
      "article-title": "A carboxyl-terminal hydrophobic region of yeast cytochrome c1 is necessary for functionnal assembly into complex III of the respiratory chain",
      "volume": "102",
      "author": "Hase",
      "year": "1987",
      "journal-title": "J. Biochem."
    },
    {
      "key": "2022010310535438000_R14",
      "doi-asserted-by": "crossref",
      "first-page": "1449",
      "DOI": "10.1091/mbc.8.8.1449",
      "article-title": "Membrane translocation of mitochondrially coded Cox2p: distinct requirements for export of N and C termini and dependence on the conserved protein Oxa1p",
      "volume": "8",
      "author": "He",
      "year": "1997",
      "journal-title": "Mol. Biol. Cell"
    },
    {
      "key": "2022010310535438000_R15",
      "doi-asserted-by": "crossref",
      "first-page": "367",
      "DOI": "10.1016/S0014-5793(97)01412-9",
      "article-title": "Oxa1p mediates the export of the N- and Ctermini of pCoxII from the mitochondrial matrix to the intermembrane space",
      "volume": "418",
      "author": "Hell",
      "year": "1997",
      "journal-title": "FEBS Lett."
    },
    {
      "key": "2022010310535438000_R16",
      "doi-asserted-by": "crossref",
      "first-page": "2250",
      "DOI": "10.1073/pnas.95.5.2250",
      "article-title": "Oxa1p, an essential component of the N-tail export machinery in mitochondria",
      "volume": "95",
      "author": "Hell",
      "year": "1998",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2022010310535438000_R17",
      "doi-asserted-by": "crossref",
      "first-page": "2217",
      "DOI": "10.1093/emboj/16.9.2217",
      "article-title": "Insertion into the mitochondrial inner membrane of a polytopic protein, the nuclear-encoded Oxa1p",
      "volume": "16",
      "author": "Herrmann",
      "year": "1997",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022010310535438000_R18",
      "doi-asserted-by": "crossref",
      "first-page": "302",
      "DOI": "10.1007/s002940050209",
      "article-title": "Oxa1p, which is required for cytochrome c oxidase and ATP synthase complex formation, is embedded in the mitochondrial inner membrane",
      "volume": "31",
      "author": "Kermorgant",
      "year": "1997",
      "journal-title": "Curr. Genet."
    },
    {
      "key": "2022010310535438000_R19",
      "doi-asserted-by": "crossref",
      "first-page": "14270",
      "DOI": "10.1016/S0021-9258(18)98678-3",
      "article-title": "Preparation and characterization of the water-soluble hemebinding domain of cytochrome c1 from Rhodobacter sphaeroides bc1 complex",
      "volume": "266",
      "author": "Konishi",
      "year": "1991",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2022010310535438000_R20",
      "doi-asserted-by": "crossref",
      "first-page": "199",
      "DOI": "10.1111/j.1432-1033.1981.tb05319.x",
      "article-title": "Membrane-bound and watersoluble cytochrome c1 from Neurospora crassa",
      "volume": "116",
      "author": "Li",
      "year": "1981",
      "journal-title": "Eur. J. Biochem."
    },
    {
      "key": "2022010310535438000_R21",
      "doi-asserted-by": "crossref",
      "first-page": "401",
      "DOI": "10.1007/s002940050222",
      "article-title": "A mutation in cytochrome oxidase subunit 2 restores respiration of the mutant pet ts1402",
      "volume": "31",
      "author": "Meyer",
      "year": "1997",
      "journal-title": "Curr. Genet."
    },
    {
      "key": "2022010310535438000_R22",
      "doi-asserted-by": "crossref",
      "first-page": "1373",
      "DOI": "10.1515/bchm.1997.378.11.1373",
      "article-title": "Mitochondrial inner membrane bound PET1402 protein is rapidly imported into mitochondria and affects the integrity of the cytochrome oxidase and ubiquinol-cytochrome c oxidoreductase complexes",
      "volume": "378",
      "author": "Meyer",
      "year": "1997",
      "journal-title": "Biol. Chem."
    },
    {
      "key": "2022010310535438000_R23",
      "doi-asserted-by": "crossref",
      "first-page": "798",
      "DOI": "10.1093/oxfordjournals.jbchem.a123283",
      "article-title": "Replacement of putative axial ligands of heme iron in yeast cytochrome c1 by site-directed mutagenesis",
      "volume": "108",
      "author": "Nakai",
      "year": "1990",
      "journal-title": "J. Biochem."
    },
    {
      "key": "2022010310535438000_R24",
      "first-page": "443",
      "article-title": "Regulation of cytochrome oxidase formation by mutations in a mitochondrial gene for cytochrome b",
      "volume-title": "Genetics and Biogenesis of Chloroplasts and Mitochondria.",
      "author": "Pajot",
      "year": "1976"
    },
    {
      "key": "2022010310535438000_R25",
      "doi-asserted-by": "crossref",
      "first-page": "3735",
      "DOI": "10.1073/pnas.92.9.3735",
      "article-title": "Diminished degradation of yeast cytochrome c by interactions with its physiological partners",
      "volume": "92",
      "author": "Pearce",
      "year": "1995",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2022010310535438000_R26",
      "doi-asserted-by": "crossref",
      "first-page": "20879",
      "DOI": "10.1074/jbc.270.36.20879",
      "article-title": "Degradation of cytochrome oxidase subunits in mutants of yeast lacking cytochrome c and suppression of the degradation by mutation of yme1",
      "volume": "270",
      "author": "Pearce",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2022010310535438000_R27",
      "doi-asserted-by": "crossref",
      "first-page": "3322",
      "DOI": "10.1016/S0021-9258(20)81361-1",
      "article-title": "Partial resolution of the enzyme catalyzing oxidative phosphorylation. I. Purification and properties of soluble, dinitrophenol-stimulated adenosine triphosphatase",
      "volume": "235",
      "author": "Pullman",
      "year": "1960",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2022010310535438000_R28",
      "doi-asserted-by": "crossref",
      "first-page": "3297",
      "DOI": "10.1021/bi00127a036",
      "article-title": "Spin-label electron paramagnetic resonance and differential scanning calorimetry studies of the interactions between mitochondrial cytochrome c oxidase and adenosine triphosphate synthase complex",
      "volume": "31",
      "author": "Qiu",
      "year": "1992",
      "journal-title": "Biochemistry"
    },
    {
      "key": "2022010310535438000_R29",
      "doi-asserted-by": "crossref",
      "first-page": "206",
      "DOI": "10.1007/s002940050122",
      "article-title": "Three genes for mitochondrial proteins suppress null-mutations in both Afg3 and Rca1 when over-expressed",
      "volume": "30",
      "author": "Rep",
      "year": "1996",
      "journal-title": "Curr. Genet."
    },
    {
      "key": "2022010310535438000_R30",
      "doi-asserted-by": "crossref",
      "first-page": "367",
      "DOI": "10.1007/s002940050145",
      "article-title": "The role of protein degradation in mitochondrial function and biogenesis",
      "volume": "30",
      "author": "Rep",
      "year": "1996",
      "journal-title": "Curr. Genet."
    },
    {
      "key": "2022010310535438000_R31",
      "doi-asserted-by": "crossref",
      "first-page": "2137",
      "DOI": "10.1002/j.1460-2075.1984.tb02103.x",
      "article-title": "Sequencing of the nuclear gene for the yeast cytochrome c1 precursor reveals an unusually complex amino terminal sequence",
      "volume": "3",
      "author": "Sadler",
      "year": "1984",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022010310535438000_R32",
      "doi-asserted-by": "crossref",
      "first-page": "118",
      "DOI": "10.1016/S0968-0004(97)01020-7",
      "article-title": "ATP-dependent proteases that also chaperone protein biogenesis",
      "volume": "22",
      "author": "Suzuki",
      "year": "1997",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "2022010310535438000_R33",
      "first-page": "5418",
      "article-title": "Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae",
      "volume": "13",
      "author": "Thorness",
      "year": "1993",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2022010310535438000_R34",
      "doi-asserted-by": "crossref",
      "first-page": "101",
      "DOI": "10.1128/mr.54.2.101-129.1990",
      "article-title": "Cytochrome bc1 complexes of microorganisms",
      "volume": "54",
      "author": "Trumpower",
      "year": "1990",
      "journal-title": "Microbiol. Rev."
    },
    {
      "key": "2022010310535438000_R35",
      "doi-asserted-by": "crossref",
      "first-page": "26144",
      "DOI": "10.1016/S0021-9258(18)47170-0",
      "article-title": "A new member of a family of ATPase is essential for assembly of mitochondrial respiratory chain and ATP synthetase complexes in Saccharomyces cerevisiae",
      "volume": "269",
      "author": "Tzagoloff",
      "year": "1994",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2022010310535438000_R36",
      "doi-asserted-by": "crossref",
      "first-page": "323",
      "DOI": "10.1006/abio.1993.1127",
      "article-title": "Detection of c-type cytochromes using enhanced chemiluminescence",
      "volume": "209",
      "author": "Vargas",
      "year": "1993",
      "journal-title": "Anal. Biochem."
    },
    {
      "key": "2022010310535438000_R37",
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      "first-page": "47",
      "DOI": "10.1016/0378-1119(91)90032-7",
      "article-title": "New vectors in fission yeast: application for cloning the his2 gene",
      "volume": "99",
      "author": "Weilguny",
      "year": "1991",
      "journal-title": "Gene"
    },
    {
      "key": "2022010310535438000_R38",
      "doi-asserted-by": "crossref",
      "first-page": "60",
      "DOI": "10.1126/science.277.5322.60",
      "article-title": "Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria",
      "volume": "277",
      "author": "Xia",
      "year": "1997",
      "journal-title": "Science"
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      "key": "2022010310535438000_R39",
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      "first-page": "677",
      "DOI": "10.1038/33612",
      "article-title": "Electron transfer by domain movement in cytochrome bc1",
      "volume": "392",
      "author": "Zhang",
      "year": "1998",
      "journal-title": "Nature"
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