A New Hypothesis on the Simultaneous Direct and Indirect Proton Pump Mechanisms in NADH-quinone Oxidoreductase (complex I)

Overview

Journal FEBS Lett

Specialty Biochemistry

Date 2010 Sep 7

PMID 20816962

Citations 14

Authors

Tomoko Ohnishi

Eiko Nakamaru-Ogiso

S Tsuyoshi Ohnishi

Affiliations

Soon will be listed here.

Abstract

Recently, Sazanov's group reported the X-ray structure of whole complex I [Nature, 465, 441 (2010)], which presented a strong clue for a "piston-like" structure as a key element in an "indirect" proton pump. We have studied the NuoL subunit which has a high sequence similarity to Na(+)/H(+) antiporters, as do the NuoM and N subunits. We constructed 27 site-directed NuoL mutants. Our data suggest that the H(+)/e(-) stoichiometry seems to have decreased from (4H(+)/2e(-)) in the wild-type to approximately (3H(+)/2e(-)) in NuoL mutants. We propose a revised hypothesis that each of the "direct" and the "indirect" proton pumps transports 2H(+) per 2e(-).

Citing Articles

Molecular Dynamics Simulation of T10609C and C10676G Mutations of Mitochondrial Gene Associated With Proton Translocation in Type 2 Diabetes Mellitus and Cataract Patients.

Destiarani W, Mulyani R, Yusuf M, Maksum I Bioinform Biol Insights. 2021; 14:1177932220978672.

PMID: 33402819 PMC: 7747115. DOI: 10.1177/1177932220978672.

Long-range proton-coupled electron transfer in biological energy conversion: towards mechanistic understanding of respiratory complex I.

Kaila V J R Soc Interface. 2018; 15(141).

PMID: 29643224 PMC: 5938582. DOI: 10.1098/rsif.2017.0916.

Mrp Antiporters Have Important Roles in Diverse Bacteria and Archaea.

Ito M, Morino M, Krulwich T Front Microbiol. 2017; 8:2325.

PMID: 29218041 PMC: 5703873. DOI: 10.3389/fmicb.2017.02325.

Di Luca A, Gamiz-Hernandez A, Kaila V Proc Natl Acad Sci U S A. 2017; 114(31):E6314-E6321.

PMID: 28716925 PMC: 5547640. DOI: 10.1073/pnas.1706278114.

A giant molecular proton pump: structure and mechanism of respiratory complex I.

Sazanov L Nat Rev Mol Cell Biol. 2015; 16(6):375-88.

PMID: 25991374 DOI: 10.1038/nrm3997.

References

Yagi T, Matsuno-Yagi A . The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry. 2003; 42(8):2266-74. DOI: 10.1021/bi027158b. View

Efremov R, Baradaran R, Sazanov L . The architecture of respiratory complex I. Nature. 2010; 465(7297):441-5. DOI: 10.1038/nature09066. View

Ohnishi T . Structural biology: Piston drives a proton pump. Nature. 2010; 465(7297):428-9. DOI: 10.1038/465428a. View

Wikstrom M . Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett. 1984; 169(2):300-4. DOI: 10.1016/0014-5793(84)80338-5. View

Galkin A, Grivennikova V, Vinogradov A . -->H+/2e- stoichiometry in NADH-quinone reductase reactions catalyzed by bovine heart submitochondrial particles. FEBS Lett. 1999; 451(2):157-61. DOI: 10.1016/s0014-5793(99)00575-x. View

Yano T, Dunham W, Ohnishi T . Characterization of the delta muH+-sensitive ubisemiquinone species (SQ(Nf)) and the interaction with cluster N2: new insight into the energy-coupled electron transfer in complex I. Biochemistry. 2005; 44(5):1744-54. DOI: 10.1021/bi048132i. View

Friedrich T, Weiss H . Modular evolution of the respiratory NADH:ubiquinone oxidoreductase and the origin of its modules. J Theor Biol. 1997; 187(4):529-40. DOI: 10.1006/jtbi.1996.0387. View

Ohnishi S, Salerno J, Ohnishi T . Possible roles of two quinone molecules in direct and indirect proton pumps of bovine heart NADH-quinone oxidoreductase (complex I). Biochim Biophys Acta. 2010; 1797(12):1891-3. PMC: 2997716. DOI: 10.1016/j.bbabio.2010.06.010. View

Baranova E, Holt P, Sazanov L . Projection structure of the membrane domain of Escherichia coli respiratory complex I at 8 A resolution. J Mol Biol. 2006; 366(1):140-54. DOI: 10.1016/j.jmb.2006.11.026. View

10.

Nakamaru-Ogiso E, Han H, Matsuno-Yagi A, Keinan E, Sinha S, Yagi T . The ND2 subunit is labeled by a photoaffinity analogue of asimicin, a potent complex I inhibitor. FEBS Lett. 2010; 584(5):883-8. PMC: 2836797. DOI: 10.1016/j.febslet.2010.01.004. View

11.

Torres-Bacete J, Nakamaru-Ogiso E, Matsuno-Yagi A, Yagi T . Characterization of the NuoM (ND4) subunit in Escherichia coli NDH-1: conserved charged residues essential for energy-coupled activities. J Biol Chem. 2007; 282(51):36914-22. DOI: 10.1074/jbc.M707855200. View

12.

Guenebaut V, Schlitt A, Weiss H, Leonard K, Friedrich T . Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Mol Biol. 1998; 276(1):105-12. DOI: 10.1006/jmbi.1997.1518. View

13.

Nakamaru-Ogiso E, Seo B, Yagi T, Matsuno-Yagi A . Amiloride inhibition of the proton-translocating NADH-quinone oxidoreductase of mammals and bacteria. FEBS Lett. 2003; 549(1-3):43-6. DOI: 10.1016/s0014-5793(03)00766-x. View

14.

Baranova E, Morgan D, Sazanov L . Single particle analysis confirms distal location of subunits NuoL and NuoM in Escherichia coli complex I. J Struct Biol. 2007; 159(2):238-42. DOI: 10.1016/j.jsb.2007.01.009. View

15.

Nakamaru-Ogiso E, Sakamoto K, Matsuno-Yagi A, Miyoshi H, Yagi T . The ND5 subunit was labeled by a photoaffinity analogue of fenpyroximate in bovine mitochondrial complex I. Biochemistry. 2003; 42(3):746-54. DOI: 10.1021/bi0269660. View

16.

Mitchell P . Keilin's respiratory chain concept and its chemiosmotic consequences. Science. 1979; 206(4423):1148-59. DOI: 10.1126/science.388618. View

17.

Amarneh B, Vik S . Mutagenesis of subunit N of the Escherichia coli complex I. Identification of the initiation codon and the sensitivity of mutants to decylubiquinone. Biochemistry. 2003; 42(17):4800-8. DOI: 10.1021/bi0340346. View

18.

Ohnishi T . Iron-sulfur clusters/semiquinones in complex I. Biochim Biophys Acta. 1998; 1364(2):186-206. DOI: 10.1016/s0005-2728(98)00027-9. View

19.

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

20.

Hunte C, Screpanti E, Venturi M, Rimon A, Padan E, Michel H . Structure of a Na+/H+ antiporter and insights into mechanism of action and regulation by pH. Nature. 2005; 435(7046):1197-202. DOI: 10.1038/nature03692. View