Electron tunneling chains of mitochondria

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1757, Issue 9-10, 2006, Pages 1096-1109

  Moser, Christopher C ^a   Farid, Tammer A ^a   Chobot, Sarah E ^a   Dutton, P Leslie ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cytochrome c oxidase cytochrome bc1; Electron and nuclear tunneling; Mitochondria; NADH ubiquinone oxidoreductase; Oxidoreduction catalytic transformation Energy conversion; Succinate dehydrogenase

Indexed keywords

ARTICLE; CATALYSIS; ELECTRON TRANSPORT; ENERGY CONSERVATION; MITOCHONDRION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CATTLE; COENZYMES; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; SWINE;

EID: 33749184515     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2006.04.015     Document Type: Article

References (73)

1. Page C.C., Moser C.C., Chen X., and Dutton P.L. Natural engineering principles of electron tunneling in biological oxidation-reduction. Nature (London) 402 (1999) 47-52
2. Marcus R.A., and Sutin N. Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811 (1985) 265-322
3. Gunner M.R., and Dutton P.L. Temperature and -delta-G-degrees dependence of the electron- transfer from Bph.- to Qa in reaction center protein from Rhodobacter sphaeroides with different quinones as Qa. J. Am. Chem. Soc. 111 (1989) 3400-3412
4. Moser C.C., Keske J.M., Warncke K., Farid R.S., and Dutton P.L. Nature of biological electron transfer. Nature (London) 355 (1992) 796-802
5. Hopfield J.J. Electron transfer between biological molecules by thermally activated tunneling. Proc. Natl. Acad. Sci. U. S. A. 71 (1974) 3640-3644
6. Karpefors M., Adelroth P., Namslauer A., Zhen Y.J., and Brzezinski P. Formation of the "peroxy" intermediate in cytochrome c oxidase is associated with internal proton/hydrogen transfer. Biochemistry 39 (2000) 14664-14669
7. Adelroth P., Brzezinski P., and Malmstrom B.G. Internal electron transfer in cytochrome c oxidase from Rhodobacter sphaeroides. Biochemistry 34 (1995) 2844-2849
8. Babcock G.T., and Wikstrom M. Oxygen activation and the conservation of energy in cell respiration. Nature 356 (1992) 301-309
9. Wikstrom M., Verkhovsky M.I., and Hummer G. Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta, Bioenerg. 1604 (2003) 61-65
10. Osyczka A., Moser C.C., Daldal F., and Dutton P.L. Reversible redox energy coupling in electron transfer chains. Nature 427 (2004) 607-612
11. Oliveberg M., and Malmstrom B.G. Internal electron transfer in cytochrome c oxidase: evidence for a rapid equilibrium between cytochrome a and the bimetallic site. Biochemistry 39 (1991) 7053-7057
12. Verkhovsky M.I., Morgan J.E., and Wikstrom M. Intramolecular electron transfer in cytochrome c oxidase: a cascade of equilibria. Biochemistry 31 (1992) 11860-11863
13. Regan J.J., Ramirez B.E., Winkler J.R., Gray H.B., and Malmstrom B.G. Pathways for electron tunneling in cytochrome c oxidase. J. Bioenerg. Biomembr. 30 (1998) 35-39
14. Pilet E., Jasaitis A., Liebl U., and Vos M.H. Electron transfer between hemes in mammalian cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 16198-16203
15. Verkhovsky M.I., Jasaitis A., and Wikstrom M. Ultrafast haem-haem electron transfer in cytochrome c oxidase. Biochim. Biophys. Acta 1506 (2001) 143-146
16. Nicholls P., and Wrigglesworth J.M. Routes of cytochrome a3 reduction - the neoclassical model revisited. Ann. N. Y. Acad. Sci. 550 (1988) 59-67
17. Mitchell P. Protonmotive redox mechanism of the cytochrome b-c1 complex in the respiratory chain: protonmotive ubiquinone cycle. FEBS Lett. 56 (1975) 1-6
18. Crofts A.R., Meinhardt S.W., Jones K.R., and Snozzi M. The role of the quinone pool in the cyclic electron-transfer chain of Rhodopseudomonas sphaeroides: a modified q-cycle mechanism. Biochim. Biophys. Acta 723 (1983) 202-218
19. Chance B., Crofts A.R., Nishimura M., and Price B. Fast membrane H+ binding in the light-activated state of chromatium chromatophores. Eur. J. Biochem. 13 (1970) 364-374
20. Robertson D.E., Prince R.C., Bowyer J.R., Matsuura K., Dutton P.L., and Ohnishi T. Thermodynamic properties of the semiquinone and its binding site in the Ubiquinol-Cytochrome c (c2) oxidoreductase of respiratory and photosynthetic systems. J. Biol. Chem. 259 (1984) 1758-1763
21. Ohnishi T., and Trumpower B.L. Differential effects of antimycin on ubisemiquinone bound in different environments in isolated succinate-cytochrome c reductase complex. J. Biol. Chem. 255 (1980) 3278-3284
22. Junemann S., Heathcote P., and Rich P.R. On the mechanism of quinol oxidation in the bc1 complex. J. Biol. Chem. 273 (1998) 21603-21607
23. Rich P.R. Electron and proton transfers through quinones and cytochrome-bc complexes. Biochim. Biophys. Acta 768 (1984) 53-79
24. Ding H., Moser C.C., Robertson D.E., Tokito M.K., Daldal F., and Dutton P.L. Ubiquinone pair in the Qo site central to the primary energy conversion reactions of cytochrome bc1 complex. Biochemistry 34 (1995) 15979-15996
25. Takamiya K., and Dutton P.L. Ubiquinone in Rhodopseudomonas sphaeroides. Some thermodynamic properties. Biochim. Biopphys. Acta 546 (1979) 1-16
26. Takamiya K.-I., and Dutton P.L. Ubiquinone in Rhodopseudomonas sphaeroides some thermodynamic properties. Biochim. Biophys. Acta 546 (1979) 1-16
27. Mitchell P. Possible molecular mechanisms of the protonmotive function of cytochrome systems. J. Theor. Biol. 62 (1976) 327-367
28. Iwata S., Lee J.W., Okada K., Lee J.K., Iwata M., Rasmussen B., Link T.A., Ramaswamy S., and Jap B.K. Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science 281 (1998) 64-71
29. Kim H., Xia D., Yu C.A., Xia J.Z., Kachurin A.M., Zhang L., Yu L., and Deisenhofer J. Inhibitor binding changes domain mobility in the iron-sulfur protein of the mitochondrial bc1 complex from bovine heart. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 8026-8033
30. Zhang Z., Huang L., Shulmeister V.M., Chi Y.-I., Kim K.K., Hung L.-W., Crofts A.R., Berry E.A., and Kim S.H. Electron transfer by domain movement in cytochrome bc1. Nature 392 (1998) 677-684
31. Sadoski R.C., Engstrom G., Tian H., Zhang L., Yu C.A., Yu L., Durham B., and Millett F. Use of a photoactivated ruthenium dimer complex to measure electron transfer between the Rieske iron-sulfur protein and cytochrome c(1) in the cytochrome bc(1) complex. Biochemistry 39 (2000) 4231-4236
32. Rich P.R., Jeal A.E., Madgwick S.A., and Moody A.J. Inhibitor effects on Redox-linked protonations of the B-hemes of the mitochondrial-Bc1 complex. Biochim. Biophys. Acta 1018 (1990) 29-40
33. Siedow J.N., Power S., de la Rosa F.F., and Palmer G. The preparation and characterization of highly purified, enzymically active complex III from Baker's Yeast. J. Biol. Chem. 253 (1978) 2392-2399
34. de la Rosa F.F., and Palmer G. Reductive titration of CoQ-depleted complex III from Baker's Yeast: evidence for an exchange-coupled complex between QH. and Low-spin Ferricytochrome b. FEBS Lett. 163 (1983) 140-143
35. Osyczka A., Moser C.C., and Dutton P.L. Fixing the Q Cycle. Trends Biochem. Sci. 30 (2005) 176-182
36. Cecchini G., Schroder I., Gunsalus R.P., and Maklashina E. Succinate dehydrogenase and fumarate reductase from Escherichia coli. Biochim. Biophys. Acta, Bioenerg. 1553 (2002) 140-157
37. Sun F., Huo X., Zhai Y.J., Wang A.J., Xu J.X., Su D., Bartlam M., and Rao Z.H. Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121 (2005) 1043-1057
38. Anderson R.F., Hille R., Shinde S.S., and Cecchini G. Electron transfer within complex II - succinate: ubiquinone oxidoreductase of Escherichia coli. J. Biol. Chem. 280 (2005) 33331-33337
39. Iverson T.M., Luna-Chavez C., Cecchini G., and Rees D.C. Structure of the Escherichia coli fumarate reductase respiratory complex. Science 284 (1999) 1961-1966
40. Ingledew W.J., Salerno J.C., and Ohnishi T. Studies on electron-paramagnetic resonance-spectra manifested by a respiratory-chain hydrogen carrier. Arch. Biochem. Biophys. 177 (1976) 176-184
41. Hederstedt L., and Rutberg L. Biosynthesis and membrane-binding of succinate-dehydrogenase in Bacillus subtilis. J. Bacteriol. 144 (1980) 941-951
42. Hederstedt L. Succinate: quinone oxidoreductase in the bacteria Paracoccus denitrificans and Bacillus subtilis. Biochim. Biophys. Acta, Bioenerg. 1553 (2002) 74-83
43. Osyczka A., Moser C.C., and Dutton P.L. Novel cyanide inhibition at cytochrome c1 of Rhodobacter capsulatus cytochrome bc1. Biochim. Biophys. Acta 1655 (2004) 71-76
44. Peterson J., Vibat C., and Gennis R.B. Identification of the axial heme ligands of cytochrome B(556) in succinate-ubiquinone oxidoreductase from Escherichia coli. FEBS Lett. 355 (1994) 155-156
45. Borsook H., and Schott H. The role of the enzyme in the enzyme-fumarate equilibrium. J. Biol. Chem. 92 (1931) 535-557
46. Wikstrom M. 2 Protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett. 169 (1984) 300-304
47. Dutton P.L., Ohnishi T., Darrouzet E., Leonard M.D., Sharp R.E., Gibney B.R., and Daldal F. In: Quinn P., and Kagan V. (Eds). Coenzyme Q: From Molecular Mechanisms to Nutrition and Health (2000), CRC Press Publishers, Florida 65-82
48. Dutton P.L., Moser C.C., Sled V.D., Daldal F., and Ohnishi T. A reductant-induced oxidation mechanism for Complex I. Biochim. Biophys. Acta 1364 (1998) 245-257
49. Ohnishi T., and Salerno J.C. Conformation-driven and semiquinone-gated proton-pump mechanism in the NADH-ubiquinone oxidoreductase (complex I). FEBS Lett. 579 (2005) 4555-4561
50. Ohnishi T., and Salerno J.C. In: Spiro T.G. (Ed). Iron-Sulfur Proteins (1982), Wiley, New York 285-327
51. Hinchliffe P., and Sazanov L.A. Organization of iron-sulfur clusters in respiratory complex I. Science 309 (2005) 771-774
52. Sazanov L.A., and Hinchliffe P. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311 (2006) 1430-1436
53. Ohnishi T. In: Capaldi R.A. (Ed). Membrane Proteins in Energy Transduction (1979), Marcel Dekker Inc., New York 1-87
54. Horsefield R., Iwata S., and Byrne B. Complex II from a structural perspective. Curr. Prot. Peptide Sci. 5 (2004) 107-118
55. Ragan C.I., and Racker E. Resolution and reconstitution of mitochondrial electron-transport system.4. reconstitution of rotenone-sensitive reduced nicotinamide adenine dinucleotide-ubiquinone reductase from reduced nicotinamide adenine-dinucleotide dehydrogenase and phospholipids. J. Biol. Chem. 248 (1973) 6876-6884
56. Uhlmann M., and Friedrich T. EPR signals assigned to Fe/S cluster N1c of the Escherichia coli NADH: ubiquinone oxidoreductase (Complex I) derive from cluster N1a. Biochemistry 44 (2005) 1653-1658
57. Nakamaru-Ogiso E., Yano T., Yagi T., and Ohnishi T. Characterization of the iron-sulfur cluster N7 (N1c) in the subunit NuoG of the proton-translocating NADH-quinone oxidoreductase from Escherichia coli. J. Biol. Chem. 280 (2005) 301-307
58. Friedrich T., and Weiss H. Modular evolution of the respiratory NADH:ubiquinone oxidoreductase and the origin of its modules. J. Theor. Biol. 187 (1997) 529-540
59. Banci L., Bertnini I., Huber J.G., Spyroulias G.A., and Turano P. Solution structure of reduced horse heart cytochrome c. J. Biol. Inorg. Chem. 4 (1999) 21-31
60. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., ShinzawaItoh K., Nakashima R., Yaono R., and Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 angstrom. Science 272 (1996) 1136-1144
61. Yoshikawa S., Shinzawa-Itoh K., Nakashima R., Yaono R., Yamashita E., Inoue N., Yao M., Fei M.J., Libeu C.P., Mizushima T., Yamaguchi H., Tomizaki T., and Tsukihara T. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280 (1998) 1723-1729
62. Yano T., Dunham W.R., and Ohnishi T. Characterization of the Delta mu(H)+-sensitive ubisemiquinone species (SQ(Nf)) and the interaction with cluster N2: new insight into the energy-coupled electron transfer in complex I. Biochemistry 44 (2005) 1744-1754
63. Ohnishi T. Iron-sulfur clusters semiquinones in Complex I. Biochim. Biophys. Acta, Bioenerg. 1364 (1998) 186-206
64. Trumpower B.L. Function of the iron-sulfur protein of the cytochrome-b-c1 segment in electron-transfer and energy-conserving reactions of the mitochondrial respiratory-chain. Biochim. Biophys. Acta 639 (1981) 129-155
65. Moody A.J., and Rich P.R. The effect of pH on redox titrations of haem a in cyanide-liganded cytochrome c oxidase: experimental and modelling studies. Biochim. Biophys. Acta 1015 (1990) 205-215
66. Rasmussen T., Scheide D., Brors B., Kintscher L., Weiss H., and Friedrich T. Identification of two tetranuclear FeS clusters on the ferredoxin-type subunit of NADH: ubiquinone oxidoreductase (complex I). Biochemistry 40 (2001) 6124-6131
67. Tommos C., Skalicky J.J., Pilloud D.L., Moser C.C., Wand A.J., and Dutton P.L. De novo proteins designed to study properties of redox-active amino acids. J. Inorg. Biochem. 74 (1999) 316
68. Ohnishi T., Salerno J.C., Winter D.B., Lim J., Yu C.A., Yu L., and King T.E. Thermodynamic and Epr characteristics of 2 ferredoxin-type iron-sulfur centers in succinate ubiquinone reductase segment of respiratory-chain. J. Biol. Chem. 251 (1976) 2094-2104
69. Ohnishi T., Lim J., Winter D.B., and King T.E. Thermodynamic and Epr characteristics of a hipip-type iron-sulfur center in succinate-dehydrogenase of respiratory-chain. J. Biol. Chem. 251 (1976) 2105-2109
70. Yu L., Xu J.X., Haley P.E., and Yu C.A. Properties of bovine heart mitochondrial cytochrome-B560. J. Biol. Chem. 262 (1987) 1137-1143
71. Sled V.D., Rudnitzky N.I., Hatefi Y., and Ohnishi T. Thermodynamic analysis of flavin in mitochondrial NADH-Ubiquinone Oxidoreductase (Complex-I). Biochemistry 33 (1994) 10069-10075
72. Ohnishi T., King T.E., Salerno J.C., Blum H., Bowyer J.R., and Maida T. Thermodynamic and electron-paramagnetic resonance characterization of flavin in succinate-dehydrogenase. J. Biol. Chem. 256 (1981) 5577-5582
73. Ohnishi T.T., and B.L. Differential effects of antimycin on ubisemiquinone bound in different environments in isolated succinate-cytochrome c reductase complex. J. Biol. Chem. 255 (1985) 3278-3284