On the role of ubiquinone in the proton translocation mechanism of respiratory complex I.


Journal

FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157

Informations de publication

Date de publication:
Jan 2023
Historique:
revised: 23 09 2022
received: 08 08 2022
accepted: 23 09 2022
pubmed: 2 10 2022
medline: 26 1 2023
entrez: 1 10 2022
Statut: ppublish

Résumé

Complex I converts oxidoreduction energy into a proton electrochemical gradient across the inner mitochondrial or bacterial cell membrane. This gradient is the primary source of energy for aerobic synthesis of ATP. Oxidation of reduced nicotinamide adenine dinucleotide (NADH) by ubiquinone (Q) yields NAD

Identifiants

pubmed: 36180980
doi: 10.1002/1873-3468.14506
doi:

Substances chimiques

Ubiquinone 1339-63-5
Electron Transport Complex I EC 7.1.1.2
Protons 0
NAD 0U46U6E8UK

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

224-236

Subventions

Organisme : Academy of Finland
Organisme : Helsingin Yliopisto
Organisme : Jane ja Aatos Erkon Säätiö
Organisme : Magnus Ehrnroothin Säätiö
Organisme : Sigrid Juséliuksen Säätiö

Informations de copyright

© 2022 The Authors. FEBS Letters published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.

Références

Wikström M. Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett. 1984;169:300-4.
Galkin A, Grivennikova V, Vinogradov A. → H+/2e stoichiometry in NADH-quinone reductase reactions catalyzed by bovine heart submitochondrial particles. FEBS Lett. 1999;451:157-61.
Galkin A, Dröse S, Brandt U. The proton pumping stoichiometry of purified mitochondrial complex I reconstituted into proteoliposomes. Biochim Biophys Acta Bioenerg. 2006;1757:1575-81.
Baradaran R, Berrisford JM, Minhas GS, Sazanov LA. Crystal structure of the entire respiratory complex I. Nature. 2013;494:443-8.
Zickermann V, Wirth C, Nasiri H, Siegmund K, Schwalbe H, Hunte C, et al. Mechanistic insight from the crystal structure of mitochondrial complex I. Science. 2015;347:44-9.
Zhu J, Vinothkumar KR, Hirst J. Structure of mammalian respiratory complex I. Nature. 2016;536:354-8.
Parey K, Haapanen O, Sharma V, Köfeler H, Züllig T, Prinz S, et al. High-resolution cryo-EM structures of respiratory complex I: mechanism, assembly, and disease. Sci Adv. 2019;5:eaax9484.
Kolata P, Efremov RG. Structure of Escherichia coli respiratory complex I reconstituted into lipid nanodiscs reveals an uncoupled conformation. Elife. 2021;10:e68710.
Michel J, DeLeon-Rangel J, Zhu S, Van Ree K, Vik SB. Mutagenesis of the L, M, and N subunits of complex I from Escherichia coli indicates a common role in function. PLoS ONE. 2011;6:e17420.
Nakamaru-Ogiso E, Kao M-C, Chen H, Sinha SC, Yagi T, Ohnishi T. The membrane subunit NuoL (ND5) is involved in the indirect proton pumping mechanism of Escherichia coli complex I. J Biol Chem. 2010;285:39070-8.
Euro L, Belevich G, Verkhovsky MI, Wikström M, Verkhovskaya M. Conserved lysine residues of the membrane subunit NuoM are involved in energy conversion by the proton-pumping NADH: ubiquinone oxidoreductase (complex I). Biochim Biophys Acta Bioenerg. 2008;1777:1166-72.
Burbaev DS, Moroz I, Kotlyar A, Sled V, Vinogradov A. Ubisemiquinone in the NADH-ubiquinone reductase region of the mitochondrial respiratory chain. FEBS Lett. 1989;254:47-51.
Vinogradov A, Sled V, Burbaev DS, Grivennikova V, Moroz I, Ohnishi T. Energy-dependent complex I-associated ubisemiquinones in submitochondrial particles. FEBS Lett. 1995;370:83-7.
Kerscher S, Kashani-Poor N, Zwicker K, Zickermann V, Brandt U. Exploring the catalytic core of complex I by Yarrowia lipolytica yeast genetics. J Bioenerg Biomembr. 2001;33:187-96.
Tocilescu MA, Fendel U, Zwicker K, Kerscher S, Brandt U. Exploring the ubiquinone binding cavity of respiratory complex I. J Biol Chem. 2007;282:29514-20.
Shinzawa-Itoh K, Seiyama J, Terada H, Nakatsubo R, Naoki K, Nakashima Y, et al. Bovine heart NADH− ubiquinone oxidoreductase contains one molecule of ubiquinone with ten isoprene units as one of the cofactors. Biochemistry. 2009;49:487-92.
Verkhovsky M, Bloch DA, Verkhovskaya M. Tightly-bound ubiquinone in the Escherichia coli respiratory complex I. Biochim Biophys Acta Bioenerg. 2012;1817:1550-6.
Dröse S, Zwicker K, Brandt U. Full recovery of the NADH: ubiquinone activity of complex I (NADH: ubiquinone oxidoreductase) from Yarrowia lipolytica by the addition of phospholipids. Biochim Biophys Acta Bioenerg. 2002;1556:65-72.
Parey K, Brandt U, Xie H, Mills DJ, Siegmund K, Vonck J, et al. Cryo-EM structure of respiratory complex I at work. Elife. 2018;7:e39213.
Gutiérrez-Fernández J, Kaszuba K, Minhas GS, Baradaran R, Tambalo M, Gallagher DT, et al. Key role of quinone in the mechanism of respiratory complex I. Nat Commun. 2020;11:1-17.
Kampjut D, Sazanov LA. The coupling mechanism of mammalian respiratory complex I. Science. 2020;370:eabc4209.
Gu J, Liu T, Guo R, Zhang L, Yang M. The coupling mechanism of mammalian mitochondrial complex I. Nat Struct Mol Biol. 2022;29:172-82.
Chung I, Wright JJ, Bridges HR, Ivanov BS, Biner O, Pereira CS, et al. Cryo-EM structures define ubiquinone-10 binding to mitochondrial complex I and conformational transitions accompanying Q-site occupancy. Nat Commun. 2022;13:1-13.
Uno S, Masuya T, Zdorevskyi O, Ikunishi R, Shinzawa-Itoh K, Lasham J, et al. Diverse reaction behaviors of artificial ubiquinones in mitochondrial respiratory complex I. J Biol Chem. 2022;298:102075.
Murai M, Mashimo Y, Hirst J, Miyoshi H. Exploring interactions between the 49 kDa and ND1 subunits in mitochondrial NADH-ubiquinone oxidoreductase (complex I) by photoaffinity labeling. Biochemistry. 2011;50:6901-8.
Nakanishi S, Abe M, Yamamoto S, Murai M, Miyoshi H. Bis-THF motif of acetogenin binds to the third matrix-side loop of ND1 subunit in mitochondrial NADH-ubiquinone oxidoreductase. Biochim Biophys Acta Bioenerg. 2011;1807:1170-6.
Wikström M, Sharma V, Kaila VR, Hosler JP, Hummer G. New perspectives on proton pumping in cellular respiration. Chem Rev. 2015;115:2196-221.
Haapanen O, Sharma V. Role of water and protein dynamics in proton pumping by respiratory complex I. Sci Rep. 2017;7:1-12.
Haapanen O, Sharma V. A modeling and simulation perspective on the mechanism and function of respiratory complex I. Biochim Biophys Acta Bioenerg. 2018;1859:510-23.
Warnau J, Sharma V, Gamiz-Hernandez AP, Di Luca A, Haapanen O, Vattulainen I, et al. Redox-coupled quinone dynamics in the respiratory complex I. Proc Natl Acad Sci USA. 2018;115:E8413-20.
Teixeira MH, Arantes GM. Balanced internal hydration discriminates substrate binding to respiratory complex I. Biochim Biophys Acta Bioenerg. 2019;1860:541-8.
Haapanen O, Djurabekova A, Sharma V. Role of second quinone binding site in proton pumping by respiratory complex I. Front Chem. 2019;7:221.
Haapanen O, Sharma V. Redox-and protonation-state driven substrate-protein dynamics in respiratory complex I. Curr Opin Electrochem. 2021;29:100741.
Moser CC, Farid TA, Chobot SE, Dutton PL. Electron tunneling chains of mitochondria. Biochim Biophys Acta Bioenerg. 2006;1757:1096-109.
Djurabekova A, Galemou Yoga E, Nyman A, Pirttikoski A, Zickermann V, Haapanen O, et al. Docking and molecular simulations reveal a quinone-binding site on the surface of respiratory complex I. FEBS Lett. 2022;596:1133-46.
Verkhovskaya ML, Belevich N, Euro L, Wikström M, Verkhovsky MI. Real-time electron transfer in respiratory complex I. Proc Natl Acad Sci USA. 2008;105:3763-7.
de Vries S, Dörner K, Strampraad MJ, Friedrich T. Electron tunneling rates in respiratory complex I are tuned for efficient energy conversion. Angew Chem Int Ed. 2015;54:2844-8.
Belevich N, Belevich G, Verkhovskaya M. Real-time optical studies of respiratory complex I turnover. Biochim Biophys Acta Bioenerg. 2014;1837:1973-80.
Rich P, Maréchal A. 8.5 electron transfer chains: structures, mechanisms and energy coupling. In: Egelman EH, editor. Comprehensive biophysics. Amsterdam: Elsevier; 2012. p. 72-93.
Verkhovskaya M, Wikström M. Oxidoreduction properties of bound ubiquinone in complex I from Escherichia coli. Biochim Biophys Acta Bioenerg. 2014;1837:246-50.
Brandt U. Proton-translocation by membrane-bound NADH: ubiquinone-oxidoreductase (complex I) through redox-gated ligand conduction. Biochim Biophys Acta Bioenerg. 1997;1318:79-91.
Brandt U. Energy converting NADH: quinone oxidoreductase (complex I). Annu Rev Biochem. 2006;75:69-92.
Treberg JR, Brand MD. A model of the proton translocation mechanism of complex I. J Biol Chem. 2011;286:17579-84.
Brandt U. A two-state stabilization-change mechanism for proton-pumping complex I. Biochim Biophys Acta Bioenerg. 2011;1807:1364-9.
Kaila VR. Resolving chemical dynamics in biological energy conversion: long-range proton-coupled electron transfer in respiratory complex I. Acc Chem Res. 2021;54:4462-73.
Wright JJ, Fedor JG, Hirst J, Roessler MM. Using a chimeric respiratory chain and EPR spectroscopy to determine the origin of semiquinone species previously assigned to mitochondrial complex I. BMC Biol. 2020;18:1-13.
Land E, Simic M, Swallow A. Optical absorption spectrum of half-reduced ubiquinone. Biochim Biophys Acta Bioenerg. 1971;226:239-40.
Gupta C, Khaniya U, Chan CK, Dehez F, Shekhar M, Gunner MR, et al. Charge transfer and chemo-mechanical coupling in respiratory complex I. J Am Chem Soc. 2020;142:9220-30.
Sharma V, Belevich G, Gamiz-Hernandez AP, Róg T, Vattulainen I, Verkhovskaya ML, et al. Redox-induced activation of the proton pump in the respiratory complex I. Proc Natl Acad Sci USA. 2015;112:11571-6.
Gamiz-Hernandez AP, Jussupow A, Johansson MP, Kaila VR. Terminal electron-proton transfer dynamics in the quinone reduction of respiratory complex I. J Am Chem Soc. 2017;139:16282-8.
Kaila VR. Long-range proton-coupled electron transfer in biological energy conversion: towards mechanistic understanding of respiratory complex I. J R Soc Interface. 2018;15:20170916.
Hummer G, Wikström M. Molecular simulation and modeling of complex I. Biochim Biophys Acta Bioenerg. 2016;1857:915-21.
Hirst J, Roessler MM. Energy conversion, redox catalysis and generation of reactive oxygen species by respiratory complex I. Biochim Biophys Acta Bioenerg. 2016;1857:872-83.
Yoga EG, Haapanen O, Wittig I, Siegmund K, Sharma V, Zickermann V. Mutations in a conserved loop in the PSST subunit of respiratory complex I affect ubiquinone binding and dynamics. Biochim Biophys Acta Bioenerg. 2019;1860:573-81.
Haapanen O, Reidelbach M, Sharma V. Coupling of quinone dynamics to proton pumping in respiratory complex I. Biochim Biophys Acta Bioenerg. 2020;1861:148287.
Parey K, Lasham J, Mills DJ, Djurabekova A, Haapanen O, Yoga EG, et al. High-resolution structure and dynamics of mitochondrial complex I-insights into the proton pumping mechanism. Sci Adv. 2021;7:eabj3221.
Sarewicz M, Pintscher S, Pietras R, Borek A, Bujnowicz Ł, Hanke G, et al. Catalytic reactions and energy conservation in the cytochrome bc 1 and b 6 f complexes of energy-transducing membranes. Chem Rev. 2021;121:2020-108.
Devault D. Energy transduction in electron transport. Biochim Biophys Acta Bioenerg. 1971;226:193-9.
Rich PR. Electron transfer reactions between quinols and quinones in aqueous and aprotic media. Biochim Biophys Acta Bioenerg. 1981;637:28-33.
Wraight CA, Gunner MR. The acceptor quinones of purple photosynthetic bacteria-structure and spectroscopy. The purple phototrophic bacteria. Berlin: Springer; 2009. p. 379-405.
Nuber F, Mérono L, Oppermann S, Schimpf J, Wohlwend D, Friedrich T. A quinol anion as catalytic intermediate coupling proton translocation with electron transfer in E. coli respiratory complex I. Front Chem. 2021;9:672969.
Uno S, Masuya T, Shinzawa-Itoh K, Lasham J, Haapanen O, Shiba T, et al. Oversized ubiquinones as molecular probes for structural dynamics of the ubiquinone reaction site in mitochondrial respiratory complex I. J Biol Chem. 2020;295:2449-63.
Wikström M, Springett R. Thermodynamic efficiency, reversibility, and degree of coupling in energy conservation by the mitochondrial respiratory chain. Commun Biol. 2020;3:1-9.
Astumian RD. Kinetic asymmetry allows macromolecular catalysts to drive an information ratchet. Nat Commun. 2019;10:1-14.
Lasham J, Haapanen O, Zickermann V, Sharma V. Tunnel dynamics of quinone derivatives and its coupling to protein conformational rearrangements in respiratory complex I. bioRxiv. 2022. https://doi.org/10.1101/2022.06.21.497056
Kampjut D, Sazanov LA. Structure of respiratory complex I-an emerging blueprint for the mechanism. Curr Opin Struct Biol. 2022;74:102350.
Kravchuk V, Petrova O, Kampjut D, Wojciechowska-Bason A, Breese Z, Sazanov L. A universal coupling mechanism of respiratory complex I. Nature. 2022;609:808-14.
Hameedi MA, Grba DN, Richardson KH, Jones AJ, Song W, Roessler MM, et al. A conserved arginine residue is critical for stabilizing the N2 FeS cluster in mitochondrial complex I. J Biol Chem. 2021;296:100474.
Mühlbauer ME, Saura P, Nuber F, Di Luca A, Friedrich T, Kaila VR. Water-gated proton transfer dynamics in respiratory complex I. J Am Chem Soc. 2020;142:13718-28.
Wikström M, Sharma V. Proton pumping by cytochrome c oxidase-a 40 year anniversary. Biochim Biophys Acta Bioenerg. 2018;1859:692-8.
Rich PR. Mitochondrial cytochrome c oxidase: catalysis, coupling and controversies. Biochem Soc Trans. 2017;45:813-29.
Yoga EG, Parey K, Djurabekova A, Haapanen O, Siegmund K, Zwicker K, et al. Essential role of accessory subunit LYRM6 in the mechanism of mitochondrial complex I. Nat Commun. 2020;11:1-8.
Di Luca A, Gamiz-Hernandez AP, Kaila VR. Symmetry-related proton transfer pathways in respiratory complex I. Proc Natl Acad Sci USA. 2017;114:E6314-21.
Schrodinger L. The PyMOL molecular graphics system. 2010, Version 1, r1; 2019.
Chovancova E, Pavelka A, Benes P, Strnad O, Brezovsky J, Kozlikova B, et al. (2012) CAVER 3.0: a tool for the analysis of transport pathways in dynamic protein structures.

Auteurs

Mårten Wikström (M)

HiLIFE Institute of Biotechnology, University of Helsinki, Finland.

Amina Djurabekova (A)

Department of Physics, University of Helsinki, Finland.

Vivek Sharma (V)

HiLIFE Institute of Biotechnology, University of Helsinki, Finland.
Department of Physics, University of Helsinki, Finland.

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