{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T07:32:20Z","timestamp":1790839940622,"version":"4.1.0"},"reference-count":70,"publisher":"Oxford University Press (OUP)","issue":"8","license":[{"start":{"date-parts":[[2022,11,26]],"date-time":"2022-11-26T00:00:00Z","timestamp":1669420800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100013465","name":"Association Fran\u00e7aise contre les Myopathies","doi-asserted-by":"publisher","award":["AFM #22382"],"award-info":[{"award-number":["AFM #22382"]}],"id":[{"id":"10.13039\/100013465","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100011224","name":"University City Science Center","doi-asserted-by":"publisher","award":["2016\/23\/B\/NZ3\/02098"],"award-info":[{"award-number":["2016\/23\/B\/NZ3\/02098"]}],"id":[{"id":"10.13039\/100011224","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,4,6]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The mitochondrial DNA mutation m.9032T&amp;gt;C was previously identified in patients presenting with NARP (Neuropathy Ataxia Retinitis Pigmentosa). Their clinical features had a maternal transmission and patient\u2019s cells showed a reduced oxidative phosphorylation capacity, elevated reactive oxygen species (ROS) production and hyperpolarization of the mitochondrial inner membrane, providing evidence that m.9032T&amp;gt;C is truly pathogenic. This mutation leads to replacement of a highly conserved leucine residue with proline at position 169 of ATP synthase subunit a (L169P). This protein and a ring of identical c-subunits (c-ring) move protons through the mitochondrial inner membrane coupled to ATP synthesis. We herein investigated the consequences of m.9032T&amp;gt;C on ATP synthase in a strain of Saccharomyces cerevisiae with an equivalent mutation (L186P). The mutant enzyme assembled correctly but was mostly inactive as evidenced by a \u2009&amp;gt;\u200995% drop in the rate of mitochondrial ATP synthesis and absence of significant ATP-driven proton pumping across the mitochondrial membrane. Intragenic suppressors selected from L186P yeast restoring ATP synthase function to varying degrees (30\u201370%) were identified at the original mutation site (L186S) or in another position of the subunit a (H114Q, I118T). In light of atomic structures of yeast ATP synthase recently described, we conclude from these results that m.9032T&amp;gt;C disrupts proton conduction between the external side of the membrane and the c-ring, and that H114Q and I118T enable protons to access the c-ring through a modified pathway.<\/jats:p>","DOI":"10.1093\/hmg\/ddac292","type":"journal-article","created":{"date-parts":[[2022,11,27]],"date-time":"2022-11-27T01:16:33Z","timestamp":1669511793000},"page":"1313-1323","source":"Crossref","is-referenced-by-count":3,"title":["Molecular basis of diseases induced by the mitochondrial DNA mutation m.9032T&amp;gt;C"],"prefix":"10.1093","volume":"32","author":[{"given":"Emilia","family":"Baranowska","sequence":"first","affiliation":[{"name":"Polish Academy of Sciences Institute of Biochemistry and Biophysics, , 02-206 Warsaw , Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katarzyna","family":"Niedzwiecka","sequence":"additional","affiliation":[{"name":"Polish Academy of Sciences Institute of Biochemistry and Biophysics, , 02-206 Warsaw , Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiranjit","family":"Panja","sequence":"additional","affiliation":[{"name":"Polish Academy of Sciences Institute of Biochemistry and Biophysics, , 02-206 Warsaw , Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Camille","family":"Charles","sequence":"additional","affiliation":[{"name":"Univ. Bordeaux, CNRS, IBGC, UMR 5095 , F-33000 Bordeaux , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alain","family":"Dautant","sequence":"additional","affiliation":[{"name":"Univ. Bordeaux, CNRS, IBGC, UMR 5095 , F-33000 Bordeaux , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean-Paul","family":"di Rago","sequence":"additional","affiliation":[{"name":"Univ. Bordeaux, CNRS, IBGC, UMR 5095 , F-33000 Bordeaux , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2290-5375","authenticated-orcid":false,"given":"D\u00e9borah","family":"Tribouillard-Tanvier","sequence":"additional","affiliation":[{"name":"Univ. 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Acta Bioenerg."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.bbabio.2018.11.005","article-title":"Functional investigation of an universally conserved leucine residue in subunit a of ATP synthase targeted by the pathogenic m.9176T&gt;G mutation","volume":"1860","author":"Kucharczyk","year":"2019","journal-title":"Biochim. Biophys. Acta Bioenerg."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1016\/j.bbabio.2019.06.002","article-title":"The pathogenic MT-ATP6 m.8851T&gt;C mutation prevents proton movements within the n-side hydrophilic cleft of the membrane domain of ATP synthase.","volume":"1860","author":"Kucharczyk","year":"2019","journal-title":"Biochim. Biophys. 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Genet."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1016\/0014-5793(94)80310-2","article-title":"Level of ATP synthase activity required for yeast Saccharomyces cerevisiae to grow on glycerol media","volume":"343","author":"Mukhopadhyay","year":"1994","journal-title":"FEBS Lett."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.1016\/j.bbabio.2009.12.022","article-title":"Consequences of the pathogenic T9176C mutation of human mitochondrial DNA on yeast mitochondrial ATP synthase","volume":"1797","author":"Kucharczyk","year":"2010","journal-title":"Biochim. Biophys. Acta"},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/S0079-6603(05)80003-0","article-title":"Function, structure, and biogenesis of mitochondrial ATP synthase","volume":"80","author":"Ackerman","year":"2005","journal-title":"Prog. Nucleic Acid Res. Mol. Biol."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"19775","DOI":"10.1074\/jbc.M401506200","article-title":"Atp10p assists assembly of Atp6p into the F0 unit of the yeast mitochondrial ATPase","volume":"279","author":"Tzagoloff","year":"2004","journal-title":"J. Biol. Chem."},{"key":"2023040610565287300_","first-page":"13235","volume-title":"Proc. Natl. Acad. Sci. U.S.A.","author":"Duvezin-Caubet","year":"2003"},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"16305","DOI":"10.1074\/jbc.M513805200","article-title":"A ``petite obligate'' mutant of Saccharomyces cerevisiae: functional mtDNA is lethal in cells lacking the delta subunit of mitochondrial F1-ATPase","volume":"281","author":"Duvezin-Caubet","year":"2006","journal-title":"J. Biol. Chem."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1091\/mbc.e13-02-0112","article-title":"The depletion of F(1) subunit epsilon in yeast leads to an uncoupled respiratory phenotype that is rescued by mutations in the proton-translocating subunits of F(0)","volume":"25","author":"Tetaud","year":"2014","journal-title":"Mol. Biol. Cell"},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"3792","DOI":"10.1093\/hmg\/ddz160","article-title":"Deregulating mitochondrial metabolite and ion transport has beneficial effects in yeast and human cellular models for NARP syndrome","volume":"28","author":"Su","year":"2019","journal-title":"Hum. Mol. Genet."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1515\/hsz-2020-0112","article-title":"Modular assembly of yeast mitochondrial ATP synthase and cytochrome oxidase","volume":"401","author":"Franco","year":"2020","journal-title":"Biol. Chem."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"7626","DOI":"10.1021\/bi034394t","article-title":"Investigation of the role and mechanism of IF1 and STF1 proteins, twin inhibitory peptides which interact with the yeast mitochondrial ATP synthase","volume":"42","author":"Venard","year":"2003","journal-title":"Biochemistry"},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"5379","DOI":"10.1016\/S0021-9258(19)43611-9","article-title":"Mitochondrial assembly in respiration-deficient mutants of Saccharomyces cerevisiae. 3. A nuclear mutant lacking mitochondrial adenosine triphosphatase","volume":"248","author":"Ebner","year":"1973","journal-title":"J. Biol. Chem."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"2889","DOI":"10.1093\/hmg\/ddp226","article-title":"Introducing the human Leigh syndrome mutation T9176G into Saccharomyces cerevisiae mitochondrial DNA leads to severe defects in the incorporation of Atp6p into the ATP synthase and in the mitochondrial morphology","volume":"18","author":"Kucharczyk","year":"2009","journal-title":"Hum. Mol. Genet."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1111\/j.1432-1033.1997.00813.x","article-title":"The absence of the mitochondrial ATP synthase delta subunit promotes a slow growth phenotype of rho- yeast cells by a lack of assembly of the catalytic sector F1","volume":"245","author":"Giraud","year":"1997","journal-title":"Eur. J. Biochem."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"1366","DOI":"10.1091\/mbc.e07-08-0746","article-title":"ATP25, a new nuclear gene of Saccharomyces cerevisiae required for expression and assembly of the Atp9p subunit of mitochondrial ATPase","volume":"19","author":"Zeng","year":"2008","journal-title":"Mol. Biol. Cell"},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1534\/genetics.106.065821","article-title":"The Saccharomyces cerevisiae ATP22 gene codes for the mitochondrial ATPase subunit 6-specific translation factor","volume":"175","author":"Zeng","year":"2007","journal-title":"Genetics"},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"6606","DOI":"10.1016\/S0021-9258(18)68684-3","article-title":"Interaction between Glu-219 and His-245 within the a subunit of F1F0-ATPase in Escherichia coli","volume":"263","author":"Cain","year":"1988","journal-title":"J. Biol. Chem."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/0005-2728(88)90031-X","article-title":"The proton pore in the Escherichia coli F0F1-ATPase: substitution of glutamate by glutamine at position 219 of the alpha-subunit prevents F0-mediated proton permeability","volume":"933","author":"Lightowlers","year":"1988","journal-title":"Biochim. Biophys. Acta"},{"issue":"1","key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"2615","DOI":"10.1038\/s41467-020-16387-2","article-title":"Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch","volume":"11","author":"Sobti","year":"2020","journal-title":"Nat. Commun."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/j.str.2003.12.001","article-title":"Structural and functional characterization of pi bulges and other short intrahelical deformations","volume":"12","author":"Cartailler","year":"2004","journal-title":"Structure"},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1093\/protein\/15.5.353","article-title":"Occurrence, conformational features and amino acid propensities for the pi-helix","volume":"15","author":"Fodje","year":"2002","journal-title":"Protein Eng."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/j.molcel.2016.05.037","article-title":"Structure of a complete ATP synthase dimer reveals the molecular basis of inner mitochondrial membrane morphology","volume":"63","author":"Hahn","year":"2016","journal-title":"Mol. 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A."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"1036","DOI":"10.1007\/PL00008646","article-title":"In vivo analysis of mutated initiation codons in the mitochondrial COX2 gene of Saccharomyces cerevisiae fused to the reporter gene ARG8m reveals lack of downstream reinitiation","volume":"262","author":"Bonnefoy","year":"2000","journal-title":"Mol. Gen. Genet."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"34039","DOI":"10.1074\/jbc.M703053200","article-title":"A yeast model of the neurogenic ataxia retinitis pigmentosa (NARP) T8993G mutation in the mitochondrial ATP synthase-6 gene","volume":"282","author":"Rak","year":"2007","journal-title":"J. Biol. Chem."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"36167","DOI":"10.1074\/jbc.M705436200","article-title":"The leader peptide of yeast Atp6p is required for efficient interaction with the Atp9p ring of the mitochondrial ATPase","volume":"282","author":"Zeng","year":"2007","journal-title":"J. Biol. Chem."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1002\/yea.320020304","article-title":"Yeast\/E. coli shuttle vectors with multiple unique restriction sites","volume":"2","author":"Hill","year":"1986","journal-title":"Yeast"},{"key":"2023040610565287300_","first-page":"3651","volume-title":"Proceedings of the National Academy of Sciences of the United States of America","author":"Conde","year":"1976"},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/0076-6879(79)55021-6","article-title":"Preparation of yeast mitochondria (Saccharomyces cerevisiae) with good P\/O and respiratory control ratios","volume":"55","author":"Guerin","year":"1979","journal-title":"Methods Enzymol."},{"key":"2023040610565287300_","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/S0021-9258(19)52451-6","article-title":"Protein measurement with the Folin phenol reagent","volume":"193","author":"Lowry","year":"1951","journal-title":"J. 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