Xuejun C. Zhang, Bin Li. Towards understanding the mechanisms of proton pumps in Complex-I of the respiratory chain[J]. Biophysics Reports, 2019, 5(5-6): 219-234. doi: 10.1007/s41048-019-00094-7
Citation: Xuejun C. Zhang, Bin Li. Towards understanding the mechanisms of proton pumps in Complex-I of the respiratory chain[J]. Biophysics Reports, 2019, 5(5-6): 219-234. doi: 10.1007/s41048-019-00094-7

Towards understanding the mechanisms of proton pumps in Complex-I of the respiratory chain

doi: 10.1007/s41048-019-00094-7
Funds:  Xuejun C. Zhang
  • Received Date: 15 April 2019
  • Publish Date: 31 December 2019
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  • Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301(5633):610-615
    Amarneh B, Vik SB (2003) Mutagenesis of subunit N of the Escherichia coli complex I. Identification of the initiation codon and the sensitivity of mutants to decylubiquinone. Biochemistry 42(17):4800-4808
    Babot M, Labarbuta P, Birch A, Kee S, Fuszard M, Botting CH, Wittig I, Heide H, Galkin A (2014) ND3, ND1 and 39 kDa subunits are more exposed in the de-active form of bovine mitochondrial complex I. Biochim Biophys Acta 1837(6):929-939
    Baradaran R, Berrisford JM, Minhas GS, Sazanov LA (2013) Crystal structure of the entire respiratory complex I. Nature 494(7438):443-448
    Belevich G, Knuuti J, Verkhovsky MI, Wikstrom M, Verkhovskaya M (2011) Probing the mechanistic role of the long alpha-helix in subunit L of respiratory Complex I from Escherichia coli by site-directed mutagenesis. Mol Microbiol 82(5):1086-1095
    Brandt U (2011) A two-state stabilization-change mechanism for proton-pumping complex I. Biochim Biophys Acta 1807(10):1364-1369
    Cabrera-Orefice A, Yoga EG, Wirth C, Siegmund K, Zwicker K, Guerrero-Castillo S, Zickermann V, Hunte C, Brandt U (2018)Locking loop movement in the ubiquinone pocket of complex I disengages the proton pumps. Nat Commun 9(1):4500
    Carroll J, Fearnley IM, Skehel JM, Shannon RJ, Hirst J, Walker JE (2006) Bovine complex I is a complex of 45 different subunits. J Biol Chem 281(43):32724-32727
    Cooley RB, Arp DJ, Karplus PA (2010) Evolutionary origin of a secondary structure:pi-helices as cryptic but widespread insertional variations of alpha-helices that enhance protein functionality. J Mol Biol 404(2):232-246
    Dang S, Sun L, Huang Y, Lu F, Liu Y, Gong H, Wang J, Yan N (2010)Structure of a fucose transporter in an outward-open conformation. Nature 467(7316):734-738
    Di Luca A, Gamiz-Hernandez AP, Kaila VRI (2017) Symmetryrelated proton transfer pathways in respiratory complex I.Proc Natl Acad Sci USA 114(31):E6314-E6321
    Drose S, Krack S, Sokolova L, Zwicker K, Barth HD, Morgner N, Heide H, Steger M, Nubel E, Zickermann V, Kerscher S, Brutschy B, Radermacher M, Brandt U (2011) Functional dissection of the proton pumping modules of mitochondrial complex I. PLoS Biol 9(8):e1001128
    Dudkina NV, Kudryashev M, Stahlberg H, Boekema EJ (2011)Interaction of complexes I, III, and IV within the bovine respirasome by single particle cryoelectron tomography. Proc Natl Acad Sci USA 108(37):15196-15200
    Efremov RG, Sazanov LA (2011) Structure of the membrane domain of respiratory complex I. Nature 476(7361):414-420
    Efremov RG, Sazanov LA (2012) The coupling mechanism of respiratory complex I-a structural and evolutionary perspective. Biochim Biophys Acta 1817 10:1785-1795
    Efremov RG, Baradaran R, Sazanov LA (2010) The architecture of respiratory complex I. Nature 465(7297):441-445
    Euro L, Belevich G, Verkhovsky MI, Wikstrom M, Verkhovskaya M (2008) Conserved lysine residues of the membrane subunit NuoM are involved in energy conversion by the protonpumping NADH:ubiquinone oxidoreductase (Complex I).Biochim Biophys Acta 1777(9):1166-1172
    Fearnley IM, Walker JE (1992) Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins. Biochim Biophys Acta 1140(2):105-134
    Formosa LE, Dibley MG, Stroud DA, Ryan MT (2018) Building a complex complex:assembly of mitochondrial respiratory chain complex I. Semin Cell Dev Biol 76:154-162
    Friedrich T, Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett 479(1-2):1-5
    Friedrich T, Steinmuller K, Weiss H (1995) The proton-pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts. FEBS Lett 367(2):107-111
    Galkin A, Meyer B, Wittig I, Karas M, Schagger H, Vinogradov A, Brandt U (2008) Identification of the mitochondrial ND3 subunit as a structural component involved in the active/deactive enzyme transition of respiratory complex I. J Biol Chem 283(30):20907-20913
    Guenebaut V, Schlitt A, Weiss H, Leonard K, Friedrich T (1998)Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Mol Biol 276(1):105-112
    Hamamoto T, Hashimoto M, Hino M, Kitada M, Seto Y, Kudo T, Horikoshi K (1994) Characterization of a gene responsible for the Na+/H+ antiporter system of alkalophilic Bacillus species strain C-125. Mol Microbiol 14(5):939-946
    Heng J, Zhao Y, Liu M, Liu Y, Fan J, Wang X, Zhang XC (2015)Substrate-bound structure of the E. coli multidrug resistance transporter MdfA. Cell Res 25(9):1060-1073
    Hill TL (1989) Free energy transduction and biochemical cycle kineticsedn. Springer-Verlag, New York Hirst J (2013) Mitochondrial complex I. Annu Rev Biochem 82:551-575
    Huang Y, Lemieux MJ, Song J, Auer M, Wang DN (2003) Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301(5633):616-620
    Jardetzky O (1966) Simple allosteric model for membrane pumps.Nature 211(5052):969-970
    Jones AJ, Blaza JN, Varghese F, Hirst J (2017) Respiratory Complex I in Bos taurus and Paracoccus denitrificans pumps four protons across the membrane for every NADH oxidized. J Biol Chem 292(12):4987-4995
    Kaila VRI (2018) Long-range proton-coupled electron transfer in biological energy conversion:towards mechanistic understanding of respiratory complex I. J R Soc Interface. https://doi.org/10.1098/rsif.2017.0916
    Kaila VR, Wikstrom M, Hummer G (2014) Electrostatics, hydration, and proton transfer dynamics in the membrane domain of respiratory complex I. Proc Natl Acad Sci USA 111(19):6988-6993
    Kotlyar AB, Sled VD, Vinogradov AD (1992) Effect of Ca2+ ions on the slow active/inactive transition of the mitochondrial NADH-ubiquinone reductase. Biochim Biophys Acta 1098(2):144-150
    Morino M, Ogoda S, Krulwich TA, Ito M (2017) Differences in the phenotypic effects of mutations in homologous MrpA and MrpD subunits of the multi-subunit Mrp-type Na(+)/H(+)antiporter. Extremophiles 21(1):51-64
    Murai M, Murakami S, Ito T, Miyoshi H (2015) Amilorides bind to the quinone binding pocket of bovine mitochondrial complex I. Biochemistry 54(17):2739-2746
    Nakamaru-Ogiso E, Sakamoto K, Matsuno-Yagi A, Miyoshi H, Yagi T (2003) The ND5 subunit was labeled by a photoaffinity analogue of fenpyroximate in bovine mitochondrial complex I. Biochemistry 42(3):746-754
    Nakamaru-Ogiso E, Kao MC, Chen H, Sinha SC, Yagi T, Ohnishi T (2010) The membrane subunit NuoL (ND5) is involved in the indirect proton pumping mechanism of Escherichia coli complex I. J Biol Chem 285(50):39070-39078
    Ohnishi T, Ohnishi ST, Salerno JC (2018) Five decades of research on mitochondrial NADH-quinone oxidoreductase (complex I).Biol Chem 399(11):1249-1264
    Parey K, Brandt U, Xie H, Mills DJ, Siegmund K, Vonck J, Kuhlbrandt W, Zickermann V (2018) Cryo-EM structure of respiratory complex I at work. Elife. https://doi.org/10.7554/eLife.39213
    Pornillos O, Chang G (2006) Inverted repeat domains in membrane proteins. FEBS Lett 580(2):358-362
    Roberts PG, Hirst J (2012) The deactive form of respiratory complex I from mammalian mitochondria is a Na+/H+ antiporter. J Biol Chem 287(41):34743-34751
    Sazanov LA (2015) A giant molecular proton pump:structure and mechanism of respiratory complex I. Nat Rev Mol Cell Biol 16(6):375-388
    Sazanov LA, Peak-Chew SY, Fearnley IM, Walker JE (2000)Resolution of the membrane domain of bovine complex I into subcomplexes:implications for the structural organization of the enzyme. Biochemistry 39(24):7229-7235
    Schuller JM, Birrell JA, Tanaka H, Konuma T, Wulfhorst H, Cox N, Schuller SK, Thiemann J, Lubitz W, Setif P, Ikegami T, Engel BD, Kurisu G, Nowaczyk MM (2019) Structural adaptations of photosynthetic complex I enable ferredoxin-dependent electron transfer. Science 363(6424):257-260
    Screpanti E, Hunte C (2007) Discontinuous membrane helices in transport proteins and their correlation with function.J Struct Biol 159(2):261-267
    Shi Y (2013) Common folds and transport mechanisms of secondary active transporters. Annu Rev Biophys 42:51-72
    Sperling E, Gorecki K, Drakenberg T, Hagerhall C (2016) Functional Differentiation of antiporter-like polypeptides in Complex I; a Site-directed mutagenesis study of residues conserved in MrpA and NuoL but not in MrpD, NuoM, and NuoN. PLoS One 11(7):e0158972
    Steimle S, Schnick C, Burger EM, Nuber F, Kramer D, Dawitz H, Brander S, Matlosz B, Schafer J, Maurer K, Glessner U, Friedrich T (2015) Cysteine scanning reveals minor local rearrangements of the horizontal helix of respiratory complex I. Mol Microbiol 98(1):151-161
    Steuber J (2003) The C-terminally truncated NuoL subunit (ND5 homologue) of the Na+-dependent complex I from Escherichia coli transports Na+. J Biol Chem 278(29):26817-26822
    Torres-Bacete J, Nakamaru-Ogiso E, Matsuno-Yagi A, Yagi T (2007)Characterization of the NuoM (ND4) subunit in Escherichia coli NDH-1:conserved charged residues essential for energycoupled activities. J Biol Chem 282(51):36914-36922
    Torres-Bacete J, Sinha PK, Matsuno-Yagi A, Yagi T (2011) Structural contribution of C-terminal segments of NuoL (ND5) and NuoM (ND4) subunits of complex I from Escherichia coli.J Biol Chem 286(39):34007-34014
    Verkhovskaya M, Bloch DA (2013) Energy-converting respiratory Complex I:on the way to the molecular mechanism of the proton pump. Int J Biochem Cell Biol 45(2):491-511
    Verkhovskaya ML, Belevich N, Euro L, Wikstrom M, Verkhovsky MI (2008) Real-time electron transfer in respiratory complex I.Proc Natl Acad Sci USA 105(10):3763-3767
    Vinogradov AD (1998) Catalytic properties of the mitochondrial NADH-ubiquinone oxidoreductase (complex I) and the pseudo-reversible active/inactive enzyme transition. Biochim Biophys Acta 1364(2):169-185
    Walker JE (1992) The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains. Q Rev Biophys 25(3):253-324
    Weinert T, Skopintsev P, James D, Dworkowski F, Panepucci E, Kekilli D, Furrer A, Brunle S, Mous S, Ozerov D, Nogly P, Wang M, Standfuss J (2019) Proton uptake mechanism in bacteriorhodopsin captured by serial synchrotron crystallography.Science 365(6448):61-65
    Wickstrand C, Dods R, Royant A, Neutze R (2015) Bacteriorhodopsin:would the real structural intermediates please stand up? Biochim Biophys Acta 1850 3:536-553
    Wraight CA (2006) Chance and design-proton transfer in water, channels and bioenergetic proteins. Biochim Biophys Acta 1757(8):886-912
    Yu H, Wu CH, Schut GJ, Haja DK, Zhao G, Peters JW, Adams MWW, Li H (2018) Structure of an ancient respiratory system. Cell 173(7):1636-1649
    Zhang XC, Li H (2019) Interplay between the electrostatic membrane potential and conformational changes in membrane proteins. Protein Sci. https://doi.org/10.1002/pro.3563
    Zhang XC, Zhao Y, Heng J, Jiang D (2015) Energy coupling mechanisms of MFS transporters. Protein Sci 24(10):1560-1579
    Zhang XC, Liu M, Lu G, Heng J (2018a) Thermodynamic secrets of multidrug resistance:a new take on transport mechanisms of secondary active antiporters. Protein Sci 27(3):595-613
    Zhang XC, Yang H, Liu Z, Sun F (2018b) Thermodynamics of voltage-gated ion channels. Biophys Rep 4(6):300-319
    Zhu J, Vinothkumar KR, Hirst J (2016) Structure of mammalian respiratory complex I. Nature 536(7616):354-358
    Zhu S, Vik SB (2015) Constraining the lateral helix of respiratory Complex I by cross-linking does not impair enzyme activity or proton translocation. J Biol Chem 290(34):20761-20773
    Zickermann V, Wirth C, Nasiri H, Siegmund K, Schwalbe H, Hunte C, Brandt U (2015) Structural biology. Mechanistic insight from the crystal structure of mitochondrial complex I. Science 347(6217):44-49
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