Energy-converting respiratory Complex I: On the way to the molecular mechanism of the proton pump

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 2, 2013, Pages 491-511

  Verkhovskaya, Marina ^a   Bloch, Dmitry A ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Bioenergetics; Electron transfer; NADH:ubiquinone oxidoreductase; Proton translocation; Proton pump

Indexed keywords

FERROUS SULFATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINONE;

BINDING SITE; CATALYSIS; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ENERGY CONVERSION; ENERGY METABOLISM; ENZYME STRUCTURE; MOLECULAR MECHANICS; OXIDATIVE PHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN STRUCTURE; PROTON TRANSPORT; RESPIRATORY CHAIN; REVIEW; THERMODYNAMICS;

ANIMALS; BACTERIA; BINDING SITES; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX I; HUMANS; HYDROGEN-ION CONCENTRATION; IRON-SULFUR PROTEINS; MITOCHONDRIA; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; UBIQUINONE;

EID: 84872332798     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2012.08.024     Document Type: Review

References (181)

1. P.M. Ahlers, K. Zwicker, S. Kerscher, and U. Brandt Function of conserved acidic residues in the PSST homologue of complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica J Biol Chem 275 2000 23577 23582
2. R.A. Alberty Calculation of standard transformed formation properties of biochemical reactants and standard apparent reduction potentials of half reactions Arch Biochem Biophys 358 1998 25 39
3. S.P. Albracht Nickel hydrogenases: in search of the active site Biochim Biophys Acta 1188 1994 167 204
4. S.P. Albracht, G. Dooijewaard, F.J. Leeuwerik, and B.V. Swol EPR signals of NADH:Q oxidoreductase. Shape and intensity Biochim Biophys Acta 459 1977 300 317
5. B. Amarneh, and S.B. Vik Mutagenesis of subunit N of the Escherichia coli complex I. Identification of the initiation codon and the sensitivity of mutants to decylubiquinone Biochemistry 42 2003 4800 4808
6. H. Angerer, H.R. Nasiri, V. Niedergesäß, S. Kerscher, H. Schwalbe, and U. Brandt Tracing the tail of ubiquinone in mitochondrial complex I Biochim Biophys Acta 1817 2012 1776 1784
7. J. Basran, R.J. Harris, M.J. Sutcliffe, and N.S. Scrutton H-tunneling in the multiple H-transfers of the catalytic cycle of morphinone reductase and in the reductive half-reaction of the homologous pentaerythritol tetranitrate reductase J Biol Chem 278 2003 43973 43982
8. H. Beinert, G. Palmer, T. Cremona, and T.P. Singer Correlation of enzymatic activity and the appearance of the EPR signal at g = 1.94 in NADH dehydrogenase and its thermal breakdown products Biochem Biophys Res Commun 12 1963 432 438
9. G. Belevich, L. Euro, M. Wikström, and M. Verkhovskaya Role of the conserved arginine 274 and histidine 224 and 228 residues in the NuoCD subunit of complex I from Escherichia coli Biochemistry 46 2007 526 533
10. G. Belevich, J. Knuuti, M.I. Verkhovsky, M. Wikström, and M. Verkhovskaya 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 2011 1086 1095
11. I. Belevich, and M.I. Verkhovsky Molecular mechanism of proton translocation by cytochrome c oxidase Antioxid Redox Signal 10 2008 1 29
12. N.P. Belevich, M.L. Verkhovskaya, and M.I. Verkhovsky Chapter 4. Electron transfer in respiratory complexes resolved by an ultra-fast freeze-quench approach Methods Enzymol 456 2009 75 93
13. J.M. Berrisford, and L.A. Sazanov Structural basis for the mechanism of respiratory complex I J Biol Chem 284 2009 29773 29783
14. - stoichiometry for NADH dehydrogenase I and dimethyl sulfoxide reductase in anaerobically grown Escherichia coli cells J Bacteriol 178 1996 6233 6237
15. U. Brandt Energy converting NADH:quinone oxidoreductase (complex I) Annu Rev Biochem 75 2006 69 92
16. U. Brandt A two-state stabilization-change mechanism for proton-pumping complex I Biochim Biophys Acta 1807 2011 1364 1369
17. H.R. Bridges, E. Bill, and J. Hirst Mössbauer spectroscopy on respiratory complex I: the iron-sulfur cluster ensemble in the NADH-reduced enzyme is partially oxidized Biochemistry 51 2012 149 158
18. H.J. Bright, and M. Appleby The pH dependence of the individual steps in the glucose oxidase reaction J Biol Chem 244 1969 3625 3634
19. M.E. Call, K.W. Wucherpfennig, and J.J. Chou The structural basis for intramembrane assembly of an activating immunoreceptor complex Nat Immunol 11 2010 1023 1029
20. J. Carroll, R.J. Shannon, I.M. Fearnley, J.E. Walker, and J. Hirst Definition of the nuclear encoded protein composition of bovine heart mitochondrial complex I. Identification of two new subunits J Biol Chem 277 2002 50311 50317
21. S.K. Chamorovsky, D.A. Cherepanov, C.S. Chamorovsky, and A.Y. Semenov Correlation of electron transfer rate in photosynthetic reaction centers with intraprotein dielectric properties Biochim Biophys Acta 1767 2007 441 448
22. V.A. Couch, E.S. Medvedev, and A.A. Stuchebrukhov Electrostatics of the FeS clusters in respiratory complex I Biochim Biophys Acta 1787 2009 1266 1271
23. 1 complex account for the function of a dimeric complex Biochim Biophys Acta 1777 2008 1001 1019
24. S. DiMauro Lessons from mitochondrial DNA mutations Semin Cell Dev Biol 12 2001 397 405
25. R. Djafarzadeh, S. Kerscher, K. Zwicker, M. Radermacher, M. Lindahl, and H. Schägger Biophysical and structural characterization of proton-translocating NADH-dehydrogenase (complex I) from the strictly aerobic yeast Yarrowia lipolytica Biochim Biophys Acta 1459 2000 230 238
26. S. Dröse, S. Krack, L. Sokolova, K. Zwicker, H.D. Barth, and N. Morgner Functional dissection of the proton pumping modules of mitochondrial complex I PLoS Biol 9 2011 e1001128
27. S. Dröse, K. Zwicker, and U. Brandt Full recovery of the NADH:ubiquinone activity of complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica by the addition of phospholipids Biochim Biophys Acta 1556 2002 65 72
28. P.L. Dutton, C.C. Moser, V.D. Sled, F. Daldal, and T. Ohnishi A reductant-induced oxidation mechanism for Complex I Biochim Biophys Acta 1364 1998 245 257
29. R.G. Efremov, R. Baradaran, and L.A. Sazanov The architecture of respiratory complex I Nature 465 2010 441 445
30. R.G. Efremov, and L.A. Sazanov Respiratory complex I: 'steam engine' of the cell Curr Opin Struct Biol 21 2011 532 540
31. R.G. Efremov, and L.A. Sazanov Structure of the membrane domain of respiratory complex I Nature 476 2011 414 420
32. R.G. Efremov, and L.A. Sazanov The coupling mechanism of respiratory complex I-a structural and evolutionary perspective Biochim Biophys Acta 2012
33. L. Euro, G. Belevich, D.A. Bloch, M.I. Verkhovsky, M. Wikström, and M. Verkhovskaya The role of the invariant glutamate 95 in the catalytic site of complex I from Escherichia coli Biochim Biophys Acta 1787 2009 68 73
34. L. Euro, G. Belevich, M.I. Verkhovsky, M. Wikström, and M. Verkhovskaya 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 1777 2008 1166 1172
35. L. Euro, G. Belevich, M. Wikström, and M. Verkhovskaya High affinity cation-binding sites in complex I from Escherichia coli Biochim Biophys Acta 1787 2009 1024 1028
36. L. Euro, D.A. Bloch, M. Wikström, M.I. Verkhovsky, and M. Verkhovskaya Electrostatic interactions between FeS clusters in NADH:ubiquinone oxidoreductase (complex I) from Escherichia coli Biochemistry 47 2008 3185 3193
37. A.S. Fernandes, F.L. Sousa, M. Teixeira, and M.M. Pereira Electron paramagnetic resonance studies of the iron-sulfur centers from complex I of Rhodothermus marinus Biochemistry 45 2006 1002 1008
38. D. Flemming, P. Hellwig, and T. Friedrich Involvement of tyrosines 114 and 139 of subunit NuoB in the proton pathway around cluster N2 in Escherichia coli NADH:ubiquinone oxidoreductase J Biol Chem 278 2003 3055 3062
39. D. Flemming, P. Hellwig, S. Lepper, D.P. Kloer, and T. Friedrich Catalytic importance of acidic amino acids on subunit NuoB of the Escherichia coli NADH:ubiquinone oxidoreductase (complex I) J Biol Chem 281 2006 24781 24789
40. D. Flemming, A. Schlitt, V. Spehr, T. Bischof, and T. Friedrich Iron-sulfur cluster N2 of the Escherichia coli NADH:ubiquinone oxidoreductase (complex I) is located on subunit NuoB J Biol Chem 278 2003 47602 47609
41. T. Friedrich, and H. Weiss Modular evolution of the respiratory NADH:ubiquinone oxidoreductase and the origin of its modules J Theor Biol 187 1997 529 540
42. A. Galkin, S. Dröse, and U. Brandt The proton pumping stoichiometry of purified mitochondrial complex I reconstituted into proteoliposomes Biochim Biophys Acta 1757 2006 1575 1581
43. - stoichiometry in NADH-quinone reductase reactions catalyzed by bovine heart submitochondrial particles FEBS Lett 451 1999 157 161
44. X. Gong, T. Xie, L. Yu, M. Hesterberg, D. Scheide, and T. Friedrich The ubiquinone-binding site in NADH:ubiquinone oxidoreductase from Escherichia coli J Biol Chem 278 2003 25731 25737
45. V.G. Grivennikova, A.B. Kotlyar, J.S. Karliner, G. Cecchini, and A.D. Vinogradov Redox-dependent change of nucleotide affinity to the active site of the mammalian complex I Biochemistry 46 2007 10971 10978
46. V.G. Grivennikova, R. Roth, N.V. Zakharova, C. Hägerhäll, and A.D. Vinogradov The mitochondrial and prokaryotic proton-translocating NADH:ubiquinone oxidoreductases: similarities and dissimilarities of the quinone-junction sites Biochim Biophys Acta 1607 2003 79 90
47. V.G. Grivennikova, and A.D. Vinogradov Generation of superoxide by the mitochondrial complex I Biochim Biophys Acta 1757 2006 553 561
48. + antiporter system of alkalophilic Bacillus species strain C-125 Mol Microbiol 14 1994 939 946
49. Y. Hatefi, A.G. Haavik, and D.E. Griffiths Studies on the electron transfer system. XL. Preparation and properties of mitochondrial DPNH-coenzyme Q reductase J Biol Chem 237 1962 1676 1680
50. R. Hedderich Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I J Bioenerg Biomembr 36 2004 65 75
51. T.L. Hill Cooperativity theory in biochemistry. Steady-state and equilibrium systems 1985 Springer-Verlag NY
52. P.C. Hinkle P/O ratios of mitochondrial oxidative phosphorylation Biochim Biophys Acta 1706 2005 1 11
53. P.C. Hinkle, M.A. Kumar, A. Resetar, and D.L. Harris Mechanistic stoichiometry of mitochondrial oxidative phosphorylation Biochemistry 30 1991 3576 3582
54. J. Hirst Energy transduction by respiratory complex I-an evaluation of current knowledge Biochem Soc Trans 33 2005 525 529
55. J. Hirst Towards the molecular mechanism of respiratory complex I Biochem J 425 2010 327 339
56. J. Hirst, M.S. King, and K.R. Pryde The production of reactive oxygen species by complex I Biochem Soc Trans 36 2008 976 980
57. C. Hunte, V. Zickermann, and U. Brandt Functional modules and structural basis of conformational coupling in mitochondrial complex I Science 329 2010 448 451
58. W.J. Ingledew, and T. Ohnishi An analysis of some thermodynamic properties of iron-sulphur centres in site I of mitochondria Biochem J 186 1980 111 117
59. M. Jastroch, A.S. Divakaruni, S. Mookerjee, J.R. Treberg, and M.D. Brand Mitochondrial proton and electron leaks Essays Biochem 47 2010 53 67
60. W. Junge Protons, proteins and ATP Photosynth Res 80 2004 197 221
61. V.R.I. Kaila, M.I. Verkhovsky, and M. Wikström Proton-coupled electron transfer in cytochrome oxidase Chem Rev 110 2010 7062 7081
62. N. Kakutani, M. Murai, N. Sakiyama, and H. Miyoshi Exploring the binding site of delta(lac)-acetogenin in bovine heart mitochondrial NADH-ubiquinone oxidoreductase Biochemistry 49 2010 4794 4803
63. M.C. Kao, S. Di Bernardo, E. Nakamaru-Ogiso, H. Miyoshi, A. Matsuno-Yagi, and T. Yagi Characterization of the membrane domain subunit NuoJ (ND6) of the NADH-quinone oxidoreductase from Escherichia coli by chromosomal DNA manipulation Biochemistry 44 2005 3562 3571
64. M.C. Kao, S. Di Bernardo, M. Perego, E. Nakamaru-Ogiso, A. Matsuno-Yagi, and T. Yagi Functional roles of four conserved charged residues in the membrane domain subunit NuoA of the proton-translocating NADH-quinone oxidoreductase from Escherichia coli J Biol Chem 279 2004 32360 32366
65. +-translocating NADH-quinone oxidoreductase probed by zero-length cross-linking Biochemistry 43 2004 3750 3755
66. M.C. Kao, E. Nakamaru-Ogiso, A. Matsuno-Yagi, and T. Yagi Characterization of the membrane domain subunit NuoK (ND4L) of the NADH-quinone oxidoreductase from Escherichia coli Biochemistry 44 2005 9545 9554
67. N. Kashani-Poor, K. Zwicker, S. Kerscher, and U. Brandt A central functional role for the 49-kDa subunit within the catalytic core of mitochondrial complex I J Biol Chem 276 2001 24082 24087
68. S. Kerscher, S. Drose, V. Zickermann, and U. Brandt The three families of respiratory NADH dehydrogenases Results Probl Cell Differ 45 2008 185 222
69. Y.C. Kim, M. Wikström, and G. Hummer Kinetic gating of the proton pump in cytochrome c oxidase Proc Natl Acad Sci U S A 106 2009 13707 13712
70. A. Kohen, and J.P. Klinman Hydrogen tunneling in biology Chem Biol 6 1999 R191 R198
71. + reduction catalysed by tightly coupled inside-out vesicles from Paracoccus denitrificans Eur J Biochem 269 2002 4020 4024
72. A.B. Kotlyar, J.S. Karliner, and G. Cecchini A novel strong competitive inhibitor of complex I FEBS Lett 579 2005 4861 4866
73. K. Krab, and M. Wikström Principles of coupling between electron transfer and proton translocation with special reference to proton translocation mechanisms in cytochrome-oxidase Biochim Biophys Acta 895 1987 25 39
74. G. Krishnamoorthy, and P.C. Hinkle Studies on the electron transfer pathway, topography of iron-sulfur centers, and site of coupling in NADH-Q oxidoreductase J Biol Chem 263 1988 17566 17575
75. K. Kumari, B.A. Baggenstoss, A.L. Parker, and P.H. Weigel Mutation of two intramembrane polar residues conserved within the hyaluronan synthase family alters hyaluronan product size J Biol Chem 281 2006 11755 11760
76. A.J. Lambert, and M.D. Brand Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I) J Biol Chem 279 2004 39414 39420
77. A.J. Lambert, and M.D. Brand Superoxide production by NADH:ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane Biochem J 382 2004 511 517
78. C.R.D. Lancaster Quinone-binding sites in membrane proteins: what can we learn from the Rhodopseudomonas viridis reaction centre Biochem Soc Trans 27 1999 591 596
79. C.R.D. Lancaster, and A. Kröger Succinate:quinone oxidoreductases: new insights from X-ray crystal structures Biochim Biophys Acta 1459 2000 422 431
80. +-driven ATP synthase Nature 481 2012 214 219
81. H. Leif, V.D. Sled, T. Ohnishi, H. Weiss, and T. Friedrich Isolation and characterization of the proton translocating NADH ubiquinone oxidoreductase from Escherichia coli Eur J Biochem 230 1995 538 548
82. V. Leskovac, S. Trivic, G. Wohlfahrt, J. Kandrac, and D. Pericin Glucose oxidase from Aspergillus niger: the mechanism of action with molecular oxygen, quinones, and one-electron acceptors Int J Biochem Cell Biol 37 2005 731 750
83. X.Y. Liu, and L.H. Matherly Functional interactions between arginine-133 and aspartate-88 in the human reduced folate carrier: evidence for a charge-pair association Biochem J 358 2001 511 516
84. K. Mandery, H. Sticht, K. Bujok, I. Schmidt, C. Fahrmayr, and B. Balk Functional and structural relevance of conserved positively charged lysine residues in organic anion transporting polypeptide 1B3 Mol Pharmacol 80 2011 400 406
85. P. Maróti, D.K. Hanson, M. Schiffer, and P. Sebban Long-range electrostatic interaction in the bacterial photosynthetic reaction centre Nat Struct Biol 2 1995 1057 1059
86. D. Marshall, N. Fisher, L. Grigic, V. Zickermann, U. Brandt, and R.J. Shannon ATR-FTIR redox difference spectroscopy of Yarrowia lipolytica and bovine complex I Biochemistry 45 2006 5458 5467
87. C. Mathiesen, and C. Hägerhäll Transmembrane topology of the NuoL, M and N subunits of NADH:quinone oxidoreductase and their homologues among membrane-bound hydrogenases and bona fide antiporters Biochim Biophys Acta 1556 2002 121 132
88. S.G. Mayhew The effects of pH and semiquinone formation on the oxidation-reduction potentials of flavin mononucleotide. A reappraisal Eur J Biochem 265 1999 698 702
89. E.S. Medvedev, V.A. Couch, and A.A. Stuchebrukhov Determination of the intrinsic redox potentials of FeS centers of respiratory complex I from experimental titration curves Biochim Biophys Acta 1797 2010 1665 1671
90. R. Meijers, and E. Cedergren-Zeppezauer A variety of electrostatic interactions and adducts can activate NAD(P) cofactors for hydride transfer Chem Biol Interact 178 2009 24 28
91. S.W. Meinhardt, T. Kula, T. Yagi, T. Lillich, and T. Ohnishi Electron paramagnetic resonance characterization of the iron-sulfur clusters in the NADH-ubiquinone oxidoreductase segment of the respiratory chain in Paracoccus denitrificans J Biol Chem 262 1987 9147 9153
92. S.W. Meinhardt, T. Kula, T. Yagi, T. Lillich, and T. Ohnishi EPR characterization of the iron-sulfur clusters in the NADH:ubiquinone oxidoreductase segment of the respiratory chain in Paracoccus denitrificans J Biol Chem 262 1987 9147 9153
93. J. Michel, J. DeLeon-Rangel, S. Zhu, K. Van Ree, and S.B. Vik Mutagenesis of the L, M, and N subunits of complex I from Escherichia coli indicates a common role in function PLoS One 6 2011 e17420
94. V.K. Moparthi, and C. Hägerhäll The evolution of respiratory chain complex I from a smaller last common ancestor consisting of 11 protein subunits J Mol Evol 72 2011 484 497
95. + antiport activity, sodium exclusion, individual Mrp protein levels, or Mrp complex formation J Biol Chem 285 2010 30942 30950
96. C.C. Moser, T.A. Farid, S.E. Chobot, and P.L. Dutton Electron tunneling chains of mitochondria Biochim Biophys Acta 1757 2006 1096 1109
97. M. Murai, Y. Mashimo, J. Hirst, and H. Miyoshi Exploring interactions between the 49 kDa and ND1 subunits in mitochondrial NADH-ubiquinone oxidoreductase (complex I) by photoaffinity labeling Biochemistry 50 2011 6901 6908
98. M. Murai, K. Sekiguchi, T. Nishioka, and H. Miyoshi Characterization of the inhibitor binding site in mitochondrial NADH-ubiquinone oxidoreductase by photoaffinity labeling using a quinazoline-type inhibitor Biochemistry 48 2009 688 698
99. S. Muraoka, and E.C. Slater The redox states of respiratory-chain components in rat-liver mitochondria. I. Effect of varying substrate concentration and of azide Biochim Biophys Acta 180 1969 221 226
100. M.P. Murphy How mitochondria produce reactive oxygen species Biochem J 417 2009 1 13
101. E. Nakamaru-Ogiso, H. Han, A. Matsuno-Yagi, E. Keinan, S.C. Sinha, and T. Yagi The ND2 subunit is labeled by a photoaffinity analogue of asimicin, a potent complex I inhibitor FEBS Lett 584 2010 883 888
102. E. Nakamaru-Ogiso, M.C. Kao, H. Chen, S.C. Sinha, T. Yagi, and T. Ohnishi The membrane subunit NuoL(ND5) is involved in the indirect proton pumping mechanism of Escherichia coli complex I J Biol Chem 285 2010 39070 39078
103. E. Nakamaru-Ogiso, K. Sakamoto, A. Matsuno-Yagi, H. Miyoshi, and T. Yagi The ND5 subunit was labeled by a photoaffinity analogue of fenpyroximate in bovine mitochondrial complex I Biochemistry 42 2003 746 754
104. S. Nakanishi, M. Abe, S. Yamamoto, M. Murai, and H. Miyoshi Bis-THF motif of acetogenin binds to the third matrix-side loop of ND1 subunit in mitochondrial NADH-ubiquinone oxidoreductase Biochim Biophys Acta 1807 2011 1170 1176
105. D.G. Nicholls Mitochondrial ion circuits Essays Biochem 47 2010 25 35
106. S.T. Ohnishi, J.C. Salerno, and T. Ohnishi Possible roles of two quinone molecules in direct and indirect proton pumps of bovine heart NADH-quinone oxidoreductase (complex I) Biochim Biophys Acta 1797 2010 1891 1893
107. T. Ohnishi Iron-sulfur clusters/semiquinones in complex I Biochim Biophys Acta 1364 1998 186 206
108. T. Ohnishi Structural biology: piston drives a proton pump Nature 465 2010 428 429
109. T. Ohnishi, and E. Nakamaru-Ogiso Were there any misassignments among iron-sulfur clusters N4, N5 and N6b in NADH-quinone oxidoreductase (complex I) Biochim Biophys Acta 1777 2008 703 710
110. T. Ohnishi, E. Nakamaru-Ogiso, and S.T. Ohnishi A new hypothesis on the simultaneous direct and indirect proton pump mechanisms in NADH-quinone oxidoreductase (complex I) FEBS Lett 584 2010 4131 4137
111. T. Ohnishi, V.D. Sled, T. Yano, T. Yagi, D.S. Burbaev, and A.D. Vinogradov Structure-function studies of iron-sulfur clusters and semiquinones in the NADH-Q oxidoreductase segment of the respiratory chain Biochim Biophys Acta 1365 1998 301 308
112. N.R. Orme-Johnson, W.H. Orme-Johnson, R.E. Hansen, H. Beinert, and Y. Hatefi EPR detectable electron acceptors in submitochondrial particles from beef heart with special reference to the iron-sulfur components of DPNH-ubiquinone reductase Biochem Biophys Res Commun 44 1971 446 452
113. A. Osyczka, C.C. Moser, F. Daldal, and P.L. Dutton Reversible redox energy coupling in electron transfer chains Nature 427 2004 607 612
114. C.C. Page, C.C. Moser, X.X. Chen, and P.L. Dutton Natural engineering principles of electron tunnelling in biological oxidation-reduction Nature 402 1999 47 52
115. V. Petruzzella, A.M. Sardanelli, S. Scacco, D. Panelli, F. Papa, and R. Trentadue Dysfunction of mitochondrial respiratory chain complex I in neurological disorders: genetics and pathogenetic mechanisms Adv Exp Med Biol 942 2012 371 384
116. S.J. Pilkington, J.M. Skehel, R.B. Gennis, and J.E. Walker Relationship between mitochondrial NADH-ubiquinone reductase and a bacterial NAD-reducing hydrogenase Biochemistry 30 1991 2166 2175
117. T. Pohl, T. Bauer, K. Dörner, S. Stolpe, P. Sell, and G. Zocher Iron-sulfur cluster N7 of the NADH:ubiquinone oxidoreductase (complex I) is essential for stability but not involved in electron transfer Biochemistry 46 2007 6588 6596
118. M.F. Powell, and T.C. Bruice Hydride vs electron-transfer in the reduction of flavin and flavin radical by 1,4-dihydropyridines J Am Chem Soc 105 1983 1014 1021
119. - transport J Biol Chem 254 1979 10200 10205
120. K.R. Pryde, and J. Hirst Superoxide is produced by the reduced flavin in mitochondrial complex I: a single, unified mechanism that applies during both forward and reverse electron transfer J Biol Chem 286 2011 18056 18065
121. J. Pätsi, M. Kervinen, M. Finel, and I.E. Hassinen Leber hereditary optic neuropathy mutations in the ND6 subunit of mitochondrial complex I affect ubiquinone reduction kinetics in a bacterial model of the enzyme Biochem J 409 2008 129 137
122. T. Rasmussen, D. Scheide, B. Brors, L. Kintscher, H. Weiss, and T. Friedrich Identification of two tetranuclear FeS clusters on the ferredoxin-type subunit of NADH:ubiquinone oxidoreductase (complex I) Biochemistry 40 2001 6124 6131
123. T. Reda, C.D. Barker, and J. Hirst Reduction of the iron-sulfur clusters in mitochondrial NADH:ubiquinone oxidoreductase (complex I) by EuII-DTPA, a very low potential reductant Biochemistry 47 2008 8885 8893
124. +/site stoichiometry of mitochondrial electron transport J Biol Chem 253 1978 6331 6334
125. P.R. Rich Electron and proton transfers through quinones and cytochrome bc complexes Biochim Biophys Acta 768 1984 53 79
126. P.R. Rich, and A. Maréchal The mitochondrial respiratory chain Essays Biochem 47 2010 1 23
127. M.M. Roessler, M.S. King, A.J. Robinson, F.A. Armstrong, J. Harmer, and J. Hirst Direct assignment of EPR spectra to structurally defined iron-sulfur clusters in complex I by double electron-electron resonance Proc Natl Acad Sci U S A 107 2010 1930 1935
128. M. Sahin-Toth, R.L. Dunten, A. Gonzalez, and H.R. Kaback Functional interactions between putative intramembrane charged residues in the lactose permease of Escherichia coli Proc Natl Acad Sci U S A 89 1992 10547 10551
129. L.A. Sazanov, J. Carroll, P. Holt, L. Toime, and I.M. Fearnley A role for native lipids in the stabilization and two-dimensional crystallization of the Escherichia coli NADH-ubiquinone oxidoreductase (complex I) J Biol Chem 278 2003 19483 19491
130. L.A. Sazanov, and P. Hinchliffe Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus Science 311 2006 1430 1436
131. D. Scheide, R. Huber, and T. Friedrich The proton-pumping NADH:ubiquinone oxidoreductase (complex I) of Aquifex aeolicus FEBS Lett 512 2002 80 84
132. U. Schulte, V. Haupt, A. Abelmann, W. Fecke, B. Brors, and T. Rasmussen A reductase/isomerase subunit of mitochondrial NADH:ubiquinone oxidoreductase (complex I) carries an NADPH and is involved in the biogenesis of the complex J Mol Biol 292 1999 569 580
133. P. Sebban, P. Maroti, M. Schiffer, and D.K. Hanson Electrostatic dominoes: long distance propagation of mutational effects in photosynthetic reaction centers of Rhodobacter capsulatus Biochemistry 34 1995 8390 8397
134. K. Sekiguchi, M. Murai, and H. Miyoshi Exploring the binding site of acetogenin in the ND1 subunit of bovine mitochondrial complex I Biochim Biophys Acta 1787 2009 1106 1111
135. K. Shinzawa-Itoh, J. Seiyama, H. Terada, R. Nakatsubo, K. Naoki, and Y. Nakashima Bovine heart NADH-ubiquinone oxidoreductase contains one molecule of ubiquinone with ten isoprene units as one of the cofactors Biochemistry 49 2010 487 492
136. Y. Shiraishi, M. Murai, N. Sakiyama, K. Ifuku, and H. Miyoshi Fenpyroximate binds to the interface between PSST and 49 kDa subunits in mitochondrial NADH-ubiquinone oxidoreductase Biochemistry 51 2012 1953 1963
137. T.A. Scholes, and P.C. Hinkle Energetics of ATP-driven reverse electron transfer from cytochrome c to fumarate and from succinate to NAD in submitochondrial particles Biochemistry 23 1984 3341 3345
138. L. Sinegina, M. Wikström, M.I. Verkhovsky, and M.L. Verkhovskaya Activation of isolated NADH:ubiquinone reductase I (complex I) from Escherichia coli by detergent and phospholipids. Recovery of ubiquinone reductase activity and changes in EPR signals of iron-sulfur clusters Biochemistry 44 2005 8500 8506
139. P.K. Sinha, J. Torres-Bacete, E. Nakamaru-Ogiso, N. Castro-Guerrero, A. Matsuno-Yagi, and T. Yagi Critical roles of subunit NuoH (ND1) in the assembly of peripheral subunits with the membrane domain of Escherichia coli NDH-1 J Biol Chem 284 2009 9814 9823
140. V.D. Sled, N.I. Rudnitzky, Y. Hatefi, and T. Ohnishi Thermodynamic analysis of flavin in mitochondrial NADH ubiquinone oxidoreductase (complex-I) Biochemistry 33 1994 10069 10075
141. V.D. Sled, and A.D. Vinogradov Kinetics of the mitochondrial NADH-ubiquinone oxidoreductase interaction with hexammineruthenium(III) Biochim Biophys Acta 1141 1993 262 268
142. +-ATP synthases from chloroplasts and Escherichia coli Proc Natl Acad Sci U S A 105 2008 3745 3750
143. S. Steimle, C. Bajzath, K. Dorner, M. Schulte, V. Bothe, and T. Friedrich Role of subunit NuoL for proton translocation by respiratory complex I Biochemistry 50 2011 3386 3393
144. J.S. Sumner, and R.G. Matthews Stereochemistry and mechanism of hydrogen transfer between NADPH and methylenetetrahydrofolate in the reaction catalyzed by methylenetetrahydrofolate reductase from pig liver J Am Chem Soc 114 1992 6949 6956
145. K.I. Takamiya, and P.L. Dutton Ubiquinone in Rhodopseudomonas sphaeroidea. Some thermodynamic properties Biochim Biophys Acta 546 1979 1 16
146. M.A. Tocilescu, U. Fendel, K. Zwicker, S. Dröse, S. Kerscher, and U. Brandt The role of a conserved tyrosine in the 49-kDa subunit of complex I for ubiquinone binding and reduction Biochim Biophys Acta 1797 2010 625 632
147. M.A. Tocilescu, U. Fendel, K. Zwicker, S. Kerscher, and U. Brandt Exploring the ubiquinone binding cavity of respiratory complex I J Biol Chem 282 2007 29514 29520
148. M.A. Tocilescu, V. Zickermann, K. Zwicker, and U. Brandt Quinone binding and reduction by respiratory complex I Biochim Biophys Acta 1797 2010 1883 1890
149. J. Torres-Bacete, E. Nakamaru-Ogiso, A. Matsuno-Yagi, and T. Yagi Characterization of the NuoM (ND4) subunit in Escherichia coli NDH-1: conserved charged residues essential for energy-coupled activities J Biol Chem 282 2007 36914 36922
150. J. Torres-Bacete, P.K. Sinha, A. Matsuno-Yagi, and T. Yagi Structural contribution of C-terminal segments of NuoL (ND5) and NuoM (ND4) subunits of complex I from Escherichia coli J Biol Chem 286 2011 34007 34014
151. J.R. Treberg, and M.D. Brand A model of the proton translocation mechanism of complex I J Biol Chem 286 2011 17579 17584
152. J.R. Treberg, C.L. Quinlan, and M.D. Brand Evidence for two sites of superoxide production by mitochondrial NADH-ubiquinone oxidoreductase (complex I) J Biol Chem 286 2011 27103 27110
153. E.E. Trimmer, D.P. Ballou, L.J. Galloway, S.A. Scannell, D.R. Brinker, and K.R. Casas Aspartate 120 of Escherichia coli methylenetetrahydrofolate reductase: evidence for major roles in folate binding and catalysis and a minor role in flavin reactivity Biochemistry 44 2005 6809 6822
154. 3 J Phys Chem B 104 2000 6293 6301
155. R. van Belzen, A.B. Kotlyar, N. Moon, W.R. Dunham, and S.P. Albracht The iron-sulfur clusters 2 and ubisemiquinone radicals of NADH:ubiquinone oxidoreductase are involved in energy coupling in submitochondrial particles Biochemistry 36 1997 886 893
156. I. Velazquez, E. Nakamaru-Ogiso, T. Yano, T. Ohnishi, and T. Yagi Amino acid residues associated with cluster N3 in the NuoF subunit of the proton-translocating NADH-quinone oxidoreductase from Escherichia coli FEBS Lett 579 2005 3164 3168
157. 2 to the photosynthetic reaction center of the purple bacterium Rhodobacter sphaeroides Biophys J 74 1998 3226 3240
158. 2+ in structure and function of complex I from Escherichia coli Biochim Biophys Acta 1807 2011 36 41
159. M.L. Verkhovskaya, N. Belevich, L. Euro, M. Wikström, and M.I. Verkhovsky Real-time electron transfer in respiratory complex I Proc Natl Acad Sci U S A 105 2008 3763 3767
160. M. Verkhovsky, D.A. Bloch, and M. Verkhovskaya Tightly-bound ubiquinone in the Escherichia coli respiratory complex I Biochim Biophys Acta 1817 2012 1550 1556
161. M.I. Verkhovsky, and A.V. Bogachev Sodium-translocating NADH:quinone oxidoreductase as a redox-driven ion pump Biochem Biophys Acta 1797 2010 738 746
162. M.I. Verkhovsky, A.V. Bogachev, A.V. Pivtsov, Y.V. Bertsova, M.V. Fedin, D.A. Bloch, and L.V. Kulik Sodium-dependent movement of covalently bound FMN residue(s) in Na+-translocating NADH:quinone oxidoreductase Biochemistry 1817 2012 1550 1556
163. A.D. Vinogradov, and V.G. Grivennikova Generation of superoxide-radical by the NADH:ubiquinone oxidoreductase of heart mitochondria Biochemistry (Moscow) 70 2005 120 127
164. H. Wang, S. Lin, E. Katilius, C. Laser, J.P. Allen, and J.C. Williams Unusual temperature dependence of photosynthetic electron transfer due to protein dynamics J Phys Chem B 113 2009 818 824
165. I.N. Watt, M.G. Montgomery, M.J. Runswick, A.G.W. Leslie, and J.E. Walker Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria Proc Natl Acad Sci USA 107 2010 16823 16827
166. M. Wikström Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone FEBS Lett 169 1984 300 304
167. M. Wikström, and G. Hummer Stoichiometry of proton translocation by respiratory complex I and its mechanistic implications Proc Natl Acad Sci U S A 109 2012 4431 4436
168. M. Wikström, and M.I. Verkhovsky Mechanism and energetics of proton translocation by the respiratory heme-copper oxidases Biochim Biophys Acta 1767 2007 1200 1214
169. G. Yakovlev, T. Reda, and J. Hirst Reevaluating the relationship between EPR spectra and enzyme structure for the iron sulfur clusters in NADH:quinone oxidoreductase Proc Natl Acad Sci U S A 104 2007 12720 12725
170. Nf) and the interaction with cluster N2: new insight into the energy-coupled electron transfer in complex I Biochemistry 44 2005 1744 1754
171. T. Yano, S. Magnitsky, and T. Ohnishi Characterization of the complex I-associated ubisemiquinone species: toward the understanding of their functional roles in the electron/proton transfer reaction Biochim Biophys Acta 1459 2000 299 304
172. T. Yano, S. Magnitsky, V.D. Sled, T. Ohnishi, and T. Yagi Characterization of the putative 2x[4Fe-4S]-binding NQO9 subunit of the proton-translocating NADH-quinone oxidoreductase (NDH-1) of Paracoccus denitrificans. Expression, reconstitution, and EPR characterization J Biol Chem 274 1999 28598 28605
173. T. Yano, J. Sklar, E. Nakamaru-Ogiso, Y. Takahashi, T. Yagi, and T. Ohnishi Characterization of cluster N5 as a fast-relaxing [4Fe-4S] cluster in the Nqo3 subunit of the proton-translocating NADH-ubiquinone oxidoreductase from Paracoccus denitrificans J Biol Chem 278 2003 15514 15522
174. T. Yano, V.D. Sled, T. Ohnishi, and T. Yagi Expression and characterization of the flavoprotein subcomplex composed of 50-kDa (NQO1) and 25-kDa (NQO2) subunits of the proton-translocating NADH-quinone oxidoreductase of Paracoccus denitrificans J Biol Chem 271 1996 5907 5913
175. C.Y. Yip, M.E. Harbour, K. Jayawardena, I.M. Fearnley, and L.A. Sazanov Evolution of respiratory complex I: supernumerary subunits are present in the alpha-proteobacterial enzyme J Biol Chem 286 2011 5023 5033
176. C.A. Yu, X. Cen, H.W. Ma, Y. Yin, L. Yu, and L. Esser Domain conformational switch of the iron-sulfur protein in cytochrome bc1 complex is induced by the electron transfer from cytochrome bL to bH Biochim Biophys Acta 1777 2008 1038 1043
177. P. Zhang, N. Battchikova, V. Paakkarinen, H. Katoh, M. Iwai, and M. Ikeuchi Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1 Biochem J 390 2005 513 520
178. V. Zickermann, M. Bostina, C. Hunte, T. Ruiz, M. Radermacher, and U. Brandt Functional implications from an unexpected position of the 49-kDa subunit of NADH:ubiquinone oxidoreductase J Biol Chem 278 2003 29072 29078
179. V. Zickermann, S. Dröse, M.A. Tocilescu, K. Zwicker, S. Kerscher, and U. Brandt Challenges in elucidating structure and mechanism of proton pumping NADH:ubiquinone oxidoreductase (complex I) J Bioenerg Biomembr 40 2008 475 483
180. Y. Zu, S. Di Bernardo, T. Yagi, and J. Hirst Redox properties of the [2Fe-2S] center in the 24 kDa (NQO2) subunit of NADH:ubiquinone oxidoreductase (complex I) Biochemistry 41 2002 10056 10069
181. K. Zwicker, A. Galkin, S. Dröse, L. Grgic, S. Kerscher, and U. Brandt The Redox-Bohr group associated with iron-sulfur cluster N2 of complex I J Biol Chem 281 2006 23013 23017