The coupling mechanism of respiratory complex i - A structural and evolutionary perspective

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 10, 2012, Pages 1785-1795

  Efremov, Rouslan G ^a,b   Sazanov, Leonid A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

Author keywords

Coupling mechanism; Hydrogenase; Modular evolution; NADH:ubiquinone oxidoreductase; Proton translocation; Redox reaction

Indexed keywords

HYDROGENASE; QUINONE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

BACILLUS SUBTILIS; CONFERENCE PAPER; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ELECTRON; ESCHERICHIA COLI; METHANOSARCINA MAZEI; MOLECULAR EVOLUTION; MOLECULAR MECHANICS; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN TRANSPORT; THERMUS THERMOPHILUS;

BACTERIA; BACTERIAL PROTEINS; ELECTRON TRANSPORT COMPLEX I; EVOLUTION, MOLECULAR; ION TRANSPORT; PROTEIN STRUCTURE, QUATERNARY; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84864659415     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.02.015     Document Type: Conference Paper

References (75)

1. J.E. Walker The NADH-ubiquinone oxidoreductase (complex I) of respiratory chains Q. Rev. Biophys. 25 1992 253 324
2. T. Yagi, and A. Matsuno-Yagi The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked Biochemistry 42 2003 2266 2274
3. U. Brandt Energy converting NADH:quinone oxidoreductase (complex I) Annu. Rev. Biochem. 75 2006 69 92
4. T. Ohnishi Iron-sulfur clusters/semiquinones in complex I Biochim. Biophys. Acta 1364 1998 186 206
5. L.A. Sazanov Respiratory complex I: mechanistic and structural insights provided by the crystal structure of the hydrophilic domain Biochemistry 46 2007 2275 2288
6. J. Hirst Towards the molecular mechanism of respiratory complex I Biochem. J. 425 2010 327 339
7. - stoichiometry in NADH-quinone reductase reactions catalyzed by bovine heart submitochondrial particles FEBS Lett. 451 1999 157 161
8. A. Galkin, S. Drose, and U. Brandt The proton pumping stoichiometry of purified mitochondrial complex I reconstituted into proteoliposomes Biochim. Biophys. Acta 1757 2006 1575 1581
9. M. Wikstrom Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone FEBS Lett. 169 1984 300 304
10. S.J.F. David, and G. Nicholls Bioenergetics 2002 Academic Press
11. A.D. Vinogradov Catalytic properties of the mitochondrial NADH-ubiquinone oxidoreductase (complex I) and the pseudo-reversible active/inactive enzyme transition Biochim. Biophys. Acta 1364 1998 169 185
12. J. Carroll, I.M. Fearnley, J.M. Skehel, R.J. Shannon, J. Hirst, and J.E. Walker Bovine complex I is a complex of 45 different subunits J. Biol. Chem. 281 2006 32724 32727
13. T. Friedrich Complex I: a chimaera of a redox and conformation-driven proton pump? J. Bioenerg. Biomembr. 33 2001 169 177
14. L.A. Sazanov, and P. Hinchliffe Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus Science 311 2006 1430 1436
15. R.G. Efremov, R. Baradaran, and L.A. Sazanov The architecture of respiratory complex I Nature 465 2010 441 445
16. R.G. Efremov, and L.A. Sazanov Structure of the membrane domain of respiratory complex I Nature 476 2011 414 420
17. C. Hunte, V. Zickermann, and U. Brandt Functional modules and structural basis of conformational coupling in mitochondrial complex I Science 329 2010 448 451
18. 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
19. J.A. Birrell, M.S. King, and J. Hirst A ternary mechanism for NADH oxidation by positively charged electron acceptors, catalyzed at the flavin site in respiratory complex I FEBS Lett. 585 2011 2318 2322
20. T. Hayashi, and A.A. Stuchebrukhov Electron tunneling in respiratory complex I Proc. Natl. Acad. Sci. U. S. A. 107 2010 19157 19162
21. K.R. Vinothkumar, and R. Henderson Structures of membrane proteins Q. Rev. Biophys. 43 2010 65 158
22. V.K. Moparthi, and C. Hagerhall The evolution of respiratory chain complex I from a smaller last common ancestor consisting of 11 protein subunits J. Mol. Evol. 2011
23. R. Hedderich Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I J. Bioenerg. Biomembr. 36 2004 65 75
24. T. Friedrich, and D. Scheide The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases FEBS Lett. 479 2000 1 5
25. M. Finel Organization and evolution of structural elements within complex I Biochim. Biophys. Acta 1364 1998 112 121
26. 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
27. T.H. Swartz, S. Ikewada, O. Ishikawa, M. Ito, and T.A. Krulwich The Mrp system: a giant among monovalent cation/proton antiporters? Extremophiles 9 2005 345 354
28. P.M. Vignais, and B. Billoud Occurrence, classification, and biological function of hydrogenases: an overview Chem. Rev. 107 2007 4206 4272
29. P.J. Holt, D.J. Morgan, and L.A. Sazanov The location of NuoL and NuoM subunits in the membrane domain of the Escherichia coli complex I: implications for the mechanism of proton pumping J. Biol. Chem. 278 2003 43114 43120
30. 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
31. E.D. Levy, E. Boeri Erba, C.V. Robinson, and S.A. Teichmann Assembly reflects evolution of protein complexes Nature 453 2008 1262 1265
32. A. Tran-Betcke, U. Warnecke, C. Bocker, C. Zaborosch, and B. Friedrich Cloning and nucleotide sequences of the genes for the subunits of NAD-reducing hydrogenase of Alcaligenes eutrophus H16 J. Bacteriol. 172 1990 2920 2929
33. C. Mathiesen, and C. Hagerhall The 'antiporter module' of respiratory chain complex I includes the MrpC/NuoK subunit - a revision of the modular evolution scheme FEBS Lett. 549 2003 7 13
34. S. Baumer, T. Ide, C. Jacobi, A. Johann, G. Gottschalk, and U. Deppenmeier The F420H2 dehydrogenase from Methanosarcina mazei is a redox-driven proton pump closely related to NADH dehydrogenases J. Biol. Chem. 275 2000 17968 17973
35. K. Bagramyan, and A. Trchounian Structural and functional features of formate hydrogen lyase, an enzyme of mixed-acid fermentation from Escherichia coli Biochemistry (Mosc.) 68 2003 1159 1170
36. M. Hakobyan, H. Sargsyan, and K. Bagramyan Proton translocation coupled to formate oxidation in anaerobically grown fermenting Escherichia coli Biophys. Chem. 115 2005 55 61
37. Y.J. Kim, H.S. Lee, E.S. Kim, S.S. Bae, J.K. Lim, R. Matsumi, A.V. Lebedinsky, T.G. Sokolova, D.A. Kozhevnikova, S.S. Cha, S.J. Kim, K.K. Kwon, T. Imanaka, H. Atomi, E.A. Bonch-Osmolovskaya, J.H. Lee, and S.G. Kang Formate-driven growth coupled with H(2) production Nature 467 2010 352 355
38. J. Meuer, S. Bartoschek, J. Koch, A. Kunkel, and R. Hedderich Purification and catalytic properties of Ech hydrogenase from Methanosarcina barkeri Eur. J. Biochem. 265 1999 325 335
39. C. Welte, V. Kallnik, M. Grapp, G. Bender, S. Ragsdale, and U. Deppenmeier Function of Ech hydrogenase in ferredoxin-dependent, membrane-bound electron transport in Methanosarcina mazei J. Bacteriol. 192 2010 674 678
40. C. Welte, C. Kratzer, and U. Deppenmeier Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei FEBS J. 277 2010 3396 3403
41. R. Sapra, K. Bagramyan, and M.W. Adams A simple energy-conserving system: proton reduction coupled to proton translocation Proc. Natl. Acad. Sci. U. S. A. 100 2003 7545 7550
42. C.C. Page, C.C. Moser, X. Chen, and P.L. Dutton Natural engineering principles of electron tunnelling in biological oxidation-reduction Nature 402 1999 47 52
43. M.A. Smith, M. Finel, V. Korolik, and G.L. Mendz Characteristics of the aerobic respiratory chains of the microaerophiles Campylobacter jejuni and Helicobacter pylori Arch. Microbiol. 174 2000 1 10
44. G.H. Peng, U. Ermler, T. Clason, S. Bornemann, T. Hedderich, T. Ruiz, B. Meyer, M. Radermacher, M. Karas, and H. Michel The structure of complex I from the hyperthermophilic eubacterium Aquifex aeolicus Biochim. Biophys. Acta 1797 2010 22-22
45. J.C. Boyington, V.N. Gladyshev, S.V. Khangulov, T.C. Stadtman, and P.D. Sun Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster Science 275 1997 1305 1308
46. I.M. Fearnley, and J.E. Walker Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins Biochim. Biophys. Acta 1140 1992 105 134
47. 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
48. M.L. Verkhovskaya, N. Belevich, L. Euro, M. Wikstrom, and M.I. Verkhovsky Real-time electron transfer in respiratory complex I Proc. Natl. Acad. Sci. U. S. A. 105 2008 3763 3767
49. J.M. Berrisford, and L.A. Sazanov Structural basis for the mechanism of respiratory complex I J. Biol. Chem. 284 2009 29773 29783
50. 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
51. J. Fritsch, P. Scheerer, S. Frielingsdorf, S. Kroschinsky, B. Friedrich, O. Lenz, and C.M. Spahn The crystal structure of an oxygen-tolerant hydrogenase uncovers a novel iron-sulphur centre Nature 479 2011 249 252
52. Y. Shomura, K.S. Yoon, H. Nishihara, and Y. Higuchi Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase Nature 479 2011 253 256
53. T. Goris, A.F. Wait, M. Saggu, J. Fritsch, N. Heidary, M. Stein, I. Zebger, F. Lendzian, F.A. Armstrong, B. Friedrich, and O. Lenz A unique iron-sulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase Nat. Chem. Biol. 7 2011 310 318
54. J.C. Fontecilla-Camps, A. Volbeda, C. Cavazza, and Y. Nicolet Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases Chem. Rev. 107 2007 4273 4303
55. 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
56. H. Ogata, W. Lubitz, and Y. Higuchi [NiFe] hydrogenases: structural and spectroscopic studies of the reaction mechanism Dalton Trans. 2009 7577 7587
57. S. Magnitsky, L. Toulokhonova, T. Yano, V.D. Sled, C. Hagerhall, V.G. Grivennikova, D.S. Burbaev, A.D. Vinogradov, and T. Ohnishi EPR characterization of ubisemiquinones and iron-sulfur cluster N2, central components of the energy coupling in the NADH-ubiquinone oxidoreductase (complex I) in situ J. Bioenerg. Biomembr. 34 2002 193 208
58. P.E. Siegbahn, M.R. Blomberg, M. Wirstam nee Pavlov, and R.H. Crabtree The mechanism of the Ni-Fe hydrogenases: a quantum chemical perspective J. Biol. Inorg. Chem. 6 2001 460 466
59. Y. Higuchi, H. Ogata, K. Miki, N. Yasuoka, and T. Yagi Removal of the bridging ligand atom at the Ni-Fe active site of [NiFe] hydrogenase upon reduction with H2, as revealed by X-ray structure analysis at 1.4 A resolution Structure 7 1999 549 556
60. M.D. Collins, and D. Jones Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication Microbiol. Rev. 45 1981 316 354
61. Q.H. Tran, J. Bongaerts, D. Vlad, and G. Unden Requirement for the proton-pumping NADH dehydrogenase I of Escherichia coli in respiration of NADH to fumarate and its bioenergetic implications Eur. J. Biochem. 244 1997 155 160
62. R.C. Prince, P. Leslie Dutton, and J. Malcolm Bruce Electrochemistry of ubiquinones: menaquinones and plastoquinones in aprotic solvents FEBS Lett. 160 1983 273 276
63. P.R. Rich Electron and proton transfers through quinones and cytochrome bc complexes Biochim. Biophys. Acta 768 1984 53 79
64. P.R. Rich, and D.S. Bendall The kinetics and thermodynamics of the reduction of cytochrome c by substituted p-benzoquinols in solution Biochim. Biophys. Acta 592 1980 506 518
65. K. Zwicker, A. Galkin, S. Drose, 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
66. D.S. Burbaev, I.A. Moroz, A.B. Kotlyar, V.D. Sled, and A.D. Vinogradov Ubisemiquinone in the NADH-ubiquinone reductase region of the mitochondrial respiratory chain FEBS Lett. 254 1989 47 51
67. S. Kumar, and R. Nussinov Salt bridge stability in monomeric proteins J. Mol. Biol. 293 1999 1241 1255
68. P.W. Atkins, and J. De Paula Atkins' Physical Chemistry 7th ed. 2002 Oxford University Press Oxford
69. U. Brandt A two-state stabilization-change mechanism for proton-pumping complex I Biochim. Biophys. Acta 1807 2011 1364 1369
70. V.R. Kaila, M.I. Verkhovsky, and M. Wikstrom Proton-coupled electron transfer in cytochrome oxidase Chem. Rev. 110 2010 7062 7081
71. G. Belevich, L. Euro, M. Wikstrom, 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
72. L. Grgic, K. Zwicker, N. Kashani-Poor, S. Kerscher, and U. Brandt Functional significance of conserved histidines and arginines in the 49-kDa subunit of mitochondrial complex I J. Biol. Chem. 279 2004 21193 21199
73. 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
74. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, J.D. Thompson, T.J. Gibson, and D.G. Higgins Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948
75. U. Brandt Energy conservation by bifurcated electron-transfer in the cytochrome-bc1 complex Biochim. Biophys. Acta 1275 1996 41 46