Activated Q-cycle as a common mechanism for cytochrome bc1 and cytochrome b6f complexes

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 12, 2010, Pages 1858-1868

  Mulkidjanian, Armen Y ^a,b  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Cytochrome b; Electron transfer; Photosynthesis; Plastoquinone; Proton transfer; Rhodobacter capsulatus; Rhodobacter sphaeroides; Ubiquinol:cytochrome c oxidoreductase; Ubiquinone

Indexed keywords

CYTOCHROME B6F; DIMER; MONOMER; QUINONE DERIVATIVE; SEMIQUINONE; UBIQUINOL CYTOCHROME C REDUCTASE;

CYANOBACTERIUM; ELECTRIC POTENTIAL; ENZYME ACTIVE SITE; ENZYME MECHANISM; MEMBRANE VESICLE; OXIDATION; OXIDATION REDUCTION REACTION; PLANT; PRIORITY JOURNAL; PROTON TRANSPORT; REVIEW; RHODOBACTER CAPSULATUS;

BACTERIAL PROTEINS; BENZOQUINONES; BINDING SITES; CYTOCHROME B6F COMPLEX; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX III; MODELS, CHEMICAL; OXIDATION-REDUCTION; PLANT PROTEINS; RHODOBACTER CAPSULATUS;

ANIMALIA; CYANOBACTERIA; RHODOBACTER CAPSULATUS; RHODOBACTER SPHAEROIDES; VIRIDIPLANTAE;

EID: 78149465155     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.07.008     Document Type: Review

References (140)

1. Berry E.A., Guergova-Kuras M., Huang L.S., Crofts A.R. Structure and function of cytochrome bc complexes. Ann. Rev. Biochem. 2000, 69:1005-1075.
2. Rich P.R. The quinone chemistry of bc complexes. Biochim. Biophys. Acta 2004, 1658:165-171.
3. 6f complex. Annu. Rev. Biochem. 2006, 75:769-790.
4. 1 and related bc complexes: the Rieske/Cytochrome b complex as the functional core of a central electron/proton transfer complex. The Purple Phototrophic Bacteria 2008, 451-473. Springer, Dordrecht. N. Hunter, F. Daldal, M. Thurnauer, J.T. Beatty (Eds.).
5. 1 complex. Results Probl. Cell Differ. 2008, 45:253-278.
6. 6f complex. Organellar and Metabolic Processes 2008, vol. 2:603-637. Elsevier, Oxford. Second Edition. D.B. Stern (Ed.).
7. 6f complex. Photochem. Photobiol. 2008, 84:1349-1358.
8. Cramer W.A., Knaff D.B. Energy transduction in biological membranes: a textbook of bioenergetics 1990, Springer-Verlag.
9. Jackson J.B., Crofts A.R. The kinetics of light induced carotenoid changes in Rhodopseudomonas spheroides and their relation to electrical field generation across the chromatophore membrane. Eur. J. Biochem. 1971, 18:120-130.
10. Cogdell R.J., Jackson J.B., Crofts A.R. The effect of redox potential on the coupling between rapid hydrogen-ion binding and electron transport in chromatophores from Rhodopseudomonas spheroides. J. Bioenerg. 1973, 4:211-227.
11. 6 and f in chloroplasts. Proc. Natl. Acad. Sci. U. S. A. 1979, 76:2765-2769.
12. Crofts A.R., Wraight C.A. The electrochemical domain of photosynthesis. Biochim. Biophys. Acta 1983, 726:149-185.
13. Crofts A.R., Meinhardt S.W., Jones K.R., Snozzi M. The role of the quinone pool in the cyclic electron transfer chain of Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 1983, 723:202-218.
14. Joliot P., Joliot A. Proton pumping and electron transfer in the cytochrome b/f complex of algae. Biochim. Biophys. Acta 1986, 849:211-222.
15. Rich P.R., Madgwick S.A., Brown S., vonJagow G., Brandt U. MOA-stilbene: A new tool for investigation of the reactions of the chloroplast cytochrome bf complex. Photosynth. Res. 1992, 34:465-477.
16. Hope A.B., Huilgol R.R., Panizza M., Thompson M., Matthews D.B. The flash-induced turnover of cytochrome b-563, cytochrome f and plastocyanin in chloroplasts. Models and estimation of kinetic-parameters. Biochim. Biophys. Acta 1992, 1100:15-26.
17. 1 and the voltage generation. Biochim. Biophys. Acta 2002, 1553:177-182.
18. 1 complexes of phototrophic bacteria: introducing the activated Q-cycle. Photochem. Photobiol. Sci. 2007, 6:19-34.
19. 1 complex from bovine heart mitochondria. Science 1997, 277:60-66.
20. 1. Nature 1998, 392:677-684.
21. 1 complex. Science 1998, 281:64-71.
22. 1 complex with its bound substrate cytochrome c. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:2800-2805.
23. 1: comparison with its mitochondrial and chloroplast counterparts. Photosynth. Res. 2004, 81:251-275.
24. Esser L., Elberry M., Zhou F., Yu C.A., Yu L., Xia D. Inhibitor-complexed structures of the cytochrome bc1 from the photosynthetic bacterium Rhodobacter sphaeroides. J. Biol. Chem. 2008, 283:2846-2857.
25. Berry E.A., Huang L.S. Observations concerning the quinol oxidation site of the cytochrome bc1 complex. FEBS Lett. 2003, 555:13-20.
26. Mitchell P. Protonmotive redox mechanism of the cytochrome b-c1 complex in the respiratory chain: protonmotive ubiquinone cycle. FEBS Lett. 1975, 56:1-6.
27. Mitchell P. The protonmotive Q cycle: a general formulation. FEBS Lett. 1975, 59:137-139.
28. Mitchell P. Possible molecular mechanisms of the protonmotive function of cytochrome systems. J. Theor. Biol. 1976, 62:327-367.
29. Wikstrom M.K., Berden J.A. Oxidoreduction of cytochrome b in the presence of antimycin. Biochim. Biophys. Acta 1972, 283:403-420.
30. Chance B., Wilson D.F., Dutton P.L., Erecinska M. Energy-coupling mechanisms in mitochondria: kinetic, spectroscopic, and thermodynamic properties of an energy-transducing form of cytochrome b. Proc. Natl. Acad. Sci. U. S. A. 1970, 66:1175-1182.
31. Lawford H.G., Garland P.B. Proton translocation coupled to quinol oxidation in ox heart mitochondria. Biochem. J. 1973, 136:711-720.
32. Hurt E.C., Gabellini N., Shahak Y., Lockau W., Hauska G. Extra proton translocation and membrane potential generation - universal properties of cytochrome bc1/b6f complexes reconstituted into liposomes. Arch. Biochem. Biophys. 1983, 225:879-885.
33. Garland P.B., Clegg R.A., Boxer D., Downie J.A., Haddock B.A. Proton-translocating nitrate reductase of Escherichia coli. Electron Transfer Chains and Oxidative Phosphorylation 1975, 351-358. North-Holland Publ. Co., Amsterdam. E. Quagliariello, S. Papa, F. Palmieri, E.C. Slater, N. Siliprandi (Eds.).
34. Crofts A.R. The Q-cycle - a personal perspective. Photosynth. Res. 2004, 80:223-243.
35. Slater E.C. The mechanism of action of the respiratory inhibitor, antimycin. Biochim. Biophys. Acta 1973, 301:129-154.
36. Wikstrom M.K. The different cytochrome b components in the respiratory chain of animal mitochondria and their role in electron transport and energy conservation. Biochim. Biophys. Acta 1973, 301:155-193.
37. Wikstrom M., Krab K., Saraste M. Proton-translocating cytochrome complexes. Ann. Rev. Biochem. 1981, 50:623-655.
38. 2: cytochrome c oxidoreductase. J. Bioenerg. Biomembr. 1986, 18:195-224.
39. Jackson J.B. Bacterial photosynthesis. Bacterial energy transduction 1988, 317-376. Academic Press, London. C. Anthony (Ed.).
40. Dutton P.L., Prince R.C. Reaction center driven cytochrome interactions in electron and proton translocation and energy conservation. The Photosynthetic Bacteria 1978, 525-570. Academic Press, New York. R.K. Clayton, W.R. Sistrom (Eds.).
41. 1-complex of Rhodobacter sphaeroides chromatophores. Biochim. Biophys. Acta 1989, 973:189-197.
42. 2 segment of Rhodopseudomonas sphaeroides chromatophores. Biochim. Biophys. Acta 1979, 546:17-42.
43. 1-complex is strongly electrogenic. FEBS Lett. 1994, 353:189-193.
44. 2 oxidoreductase complex of Rhodopseudomonas sphaeroides. FEBS Lett. 1984, 178:336-342.
45. 1 complex. FEBS Lett. 1984, 178:343-350.
46. Schultz B.E., Hansen K.C., Lin C.C., Chan S.I. Rapid photochemical generation of ubiquinol through a radical pathway: an avenue for probing submillisecond enzyme kinetics. J. Org. Chem. 2000, 65:3244-3247.
47. Schultz B.E., Chan S.I. Structures and proton-pumping strategies of mitochondrial respiratory enzymes. Annu. Rev. Biophys. Biomol. Struct. 2001, 30:23-65.
48. 1 complex. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:4864-4869.
49. 1 complex prevents center P inhibition by reverse reactions at center N. Biochim. Biophys. Acta 2008, 1777:1044-1052.
50. Andersson S.G.E., Zomorodipour A., Andersson J.O., Sicheritz-Ponten T., Alsmark U.C.M., Podowski R.M., Naslund A.K., Eriksson A.S., Winkler H.H., Kurland C.G. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 1998, 396:133-140.
51. Saraste M. Location of haem-binding sites in the mitochondrial cytochrome b. FEBS Lett. 1984, 166:367-372.
52. Widger W.R., Cramer W.A., Herman R.G., Trebst A. Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and the chloroplast b6-f complex: position of the cytochrome b hemes in the membrane. Proc. Natl. Acad. Sci. U. S. A. 1984, 81:674-678.
53. 1 complex. Biochim. Biophys. Acta 1996, 1275:47-53.
54. 2 oxidoreductase from Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 1981, 635:149-166.
55. Bowyer J.R., Crofts A.R. On the mechanism of photosynthetic electron transfer in Rhodopseudomonas capsulata and Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 1981, 636:218-233.
56. Matsuura K., O'Keefe D.P., Dutton P.L. A reevaluation of the events leading to the electrogenic reaction and proton translocation in the ubiquinol-cytochrome c oxidoreductase of Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 1983, 722:12-22.
57. 1-complex of Rhodobacter sphaeroides. The electron transfer between cytochrome b hemes can be non-electrogenic. FEBS Lett. 1991, 284:227-231.
58. 1 complex: reaction mechanism and prevention of short-circuiting. Biochim. Biophys. Acta 2005, 1709:5-34.
59. Mulkidjanian A.Y. Proton in the well and through the desolvation barrier. Biochim. Biophys. Acta 2006, 1757:415-427.
60. 1 complex of Rhodobacter capsulatus. Photosynthesis: from Light to Biosphere: Proceedings of the Xth International Photosynthesis Congress, Vol. II 1995, 547-550. Kluwer Academic Publishers, Dordrecht. P. Mathis (Ed.).
61. 1 complex of Rhodobacter capsulatus: ubiquinol oxidation in a dimeric Q-cycle?. FEBS Lett. 1998, 431:291-296.
62. Jones M.R., Jackson J.B. Proton efflux from right-side-out membrane vesicles of Rhodobacter sphaeroides after short flashes. Biochim. Biophys. Acta 1990, 1019:51-58.
63. Klishin S.S., Mulkidjanian A.Y. Proton transfer paths at the quinol oxidizing site of the Rb. capsulatus cytochrome bc complex. Photosynthesis: Fundamental aspects to global perspectives, Vol. 1, Montreal 2005, 260-262. A. van der Est, D. Bruce (Eds.).
64. 1 complex. Biochemistry 2001, 40:12584-12590.
65. Feniouk B.A., Kozlova M.A., Knorre D.A., Cherepanov D.A., Mulkidjanian A.Y., Junge W. The proton driven rotor of ATP synthase: Ohmic conductance (10 fS), and absence of voltage gating. Biophys. J. 2004, 86:665-680.
66. Cherepanov D.A., Krishtalik L.I., Mulkidjanian A.Y. Photosynthetic electron transfer controlled by protein relaxation: analysis by Langevin stochastic approach. Biophys. J. 2001, 80:1033-1049.
67. Madej M.G., Nasiri H.R., Hilgendorff N.S., Schwalbe H., Lancaster C.R. Evidence for transmembrane proton transfer in a dihaem-containing membrane protein complex. EMBO J. 2006, 25:4963-4970.
68. Skulachev V.P., Chistyakov V.V., Jasaitis A.A., Smirnova E.G. Inhibition of the respiratory chain by zinc ions. Biochem. Biophys. Res. Comm. 1967, 26:1-6.
69. 1 complex. Eur. J. Biochem. 1991, 197:555-561.
70. 1 complex by blocking a protonatable group. J. Biol. Chem. 1995, 270:25001-25006.
71. 1 complex. Biochim. Biophys. Acta 2000, 1459:440-448.
72. 1 complexes. Biophys. J. 2007, 93:2934-2951.
73. Wenz T., Hellwig P., MacMillan F., Meunier B., Hunte C. Probing the role of E272 in quinol oxidation of mitochondrial complex III. Biochemistry 2006, 45:9042-9052.
74. 1 complex. Biophys. J. 1999, 77:1753-1768.
75. 1 complex but not for single turnover Qo site catalysis. J. Biol. Chem. 2002, 277:3471-3476.
76. 1 complex. Biochemistry 2005, 44:10520-10532.
77. 1. Biochemistry 2009, 48:1888-1899.
78. 1 complex. J. Biol. Chem. 2006, 281:30925-30932.
79. 1 complex: evidence for anti-cooperative ubiquinol oxidation and communication between center P ubiquinol oxidation sites. J. Biol. Chem. 2007, 282:22289-22297.
80. 1 complex: the advantages of being a twin. Biochim. Biophys. Acta 2008, 1777:1079-1091.
81. Brandt U., von Jagow G. Analysis of inhibitor binding to the mitochondrial cytochrome c reductase by fluorescence quench titration. Evidence for a 'catalytic switch' at the Qo center. Eur. J. Biochem. 1991, 195:163-170.
82. P site of the cytochrome complex. The 'proton-gated affinity change' mechanism. FEBS Lett. 1997, 412:257-264.
83. Osyczka A., Moser C.C., Dutton P.L. Fixing the Q cycle. Trends Biochem. Sci. 2005, 30:176-182.
84. Cape J.L., Bowman M.K., Kramer D.M. Understanding the cytochrome bc complexes by what they don't do. The Q-cycle at 30. Trends Plant Sci. 2006, 11:46-55.
85. 1 complex. Photosynth. Res. 2007, 92:17-34.
86. Chobot S.E., Zhang H., Moser C.C., Dutton P.L. Breaking the Q-cycle: finding new ways to study Qo through thermodynamic manipulations. J. Bioenerg. Biomembr. 2008, 40:501-507.
87. 1 complex dimer is controlled by the energized state and by impaired electron transfer between low and high potential hemes. FEBS Lett. 2007, 581:1535-1541.
88. 2:cytochrome c oxidoreductase studied by pre-steady-state kinetics. Biochim. Biophys. Acta 1982, 681:41-53.
89. De Vries S., Albracht S.P., Berden J.A., Marres C.A., Slater E.C. The effect of pH, ubiquinone depletion and myxothiazol on the reduction kinetics of the prosthetic groups of ubiquinol:cytochrome c oxidoreductase. Biochim. Biophys. Acta 1983, 723:91-103.
90. Moser C.C., Keske J.M., Warncke K., Farid R.S., Dutton P.L. Nature of biological electron transfer. Nature 1992, 355:796-802.
91. Osyczka A., Moser C.C., Daldal F., Dutton P.L. Reversible redox energy coupling in electron transfer chains. Nature 2004, 427:607-612.
92. 1 complex. J. Biol. Chem. 2004, 279:15040-15049.
93. 1 complex dimer is reduced through center N. J. Biol. Chem. 2005, 280:22732-22740.
94. 1 complex: enzyme with one inactive monomer is fully active but unable to activate the second ubiquinol oxidation site in response to ligand binding at the ubiquinone reduction site. J. Biol. Chem. 2010, 285:502-510.
95. Mulkidjanian A.Y. Proton transfer by membrane proteins: whether there are rules?. Biochim. Biophys. Acta 2006, 1757(Supplement 1):92.
96. Siedow J.N., Power S., de la Rosa F.F., Palmer G. The preparation and characterization of highly purified, enzymically active complex III from baker's yeast. J. Biol. Chem. 1978, 253:2392-2399.
97. de la Rosa F.F., 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. 1983, 163:140-143.
98. 1 complex. Biochim. Biophys. Acta 1990, 1018:29-40.
99. 1 complex. Consequences for semiquinone stabilization. J. Biol. Chem. 2007, 282:24198-24208.
100. 2) oxidoreductase of respiratory and photosynthetic systems. J. Biol. Chem. 1984, 259:1758-1763.
101. 2 oxidoreductase complex of Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 1984, 766:322-333.
102. 2 reductase of Rhodobacter sphaeroides under the neutral and alkaline conditions. FEBS Lett. 1990, 277:127-130.
103. 6f complex. Nature 2003, 426:413-418.
104. 6f complex of oxygenic photosynthesis: tuning the cavity. Science 2003, 302:1009-1014.
105. 6f complex of oxygenic photosynthesis. Biochemistry 2004, 43:16329-16336.
106. 6f complex studied by EPR: a pair of strongly interacting hemes. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:519-524.
107. 6f complex. J. Biol. Chem. 1997, 272:21901-21908.
108. 6f complex of oxygenic photosynthesis protects against oxygen damage. J. Biol. Chem. 1999, 274:1581-1587.
109. 6f complex: unusual optical properties protect the complex against singlet oxygen. Biophys. J. 2005, 88:4178-4187.
110. Martinez S.E., Huang D., Szczepaniak A., Cramer W.A., Smith J.L. Crystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation. Structure 1994, 2:95-105.
111. 6 and cytochrome f redox changes in chloroplasts - evidence for a Q-cycle. FEBS Lett. 1982, 150:286-292.
112. O'Keefe D.P. Structure and function of the chloroplast cytochrome bf complex. Photosynth. Res. 1988, 17:189-216.
113. Hope A.B., Rich P.R. Proton uptake by the chloroplast cytochrome bf complex. Biochim. Biophys. Acta 1989, 975:96-103.
114. 6. Biochemistry 1998, 37:17199-17208.
115. 6f complex. Biochemistry 2000, 39:2692-2699.
116. 6f turnovers from the study of H/D substitution effects on the electrogenicity and electron transfer reactions. Biochemistry 2000, 39:3304-3310.
117. Jones R.W., Whitmarsh J. Origin of the electrogenic reaction in the chloroplast cytochrome b/f complex. Photobiochem. Photobiophys. 1985, 9:119-127.
118. Jones R.W., Whitmarsh J. Inhibition of electron transfer and the electrogenic reaction in the cytochrome b/f complex by 2-n-nonyl-4-hydroxyquinoline N-oxide(NQNO) and 2, 5-dibromo-3-methyl-6-isopropyl-p-benzoquinone (DBMIB). Biochim. Biophys. Acta 1988, 933:258-268.
119. Rich P.R., Madgwick S.A., Moss D.A. The interactions of duroquinol, DBMIB and NQNO with the chloroplast cytochrome bf complex. Biochim. Biophys. Acta 1991, 1058:312-328.
120. 6f complex: quinone analogue inhibitors as ligands of heme cn. J. Mol. Biol. 2007, 370:39-52.
121. 6f complex. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15860-15865.
122. Heimann S., Klughammer C., Schreiber U. Two distinct states of the thylakoid bf complex. FEBS Lett. 1998, 426:126-130.
123. 6f complex as a structural and functional dimer. Biochemistry 1994, 33:4401-4409.
124. 6 in situ. Biochemistry 1989, 28:8990-8998.
125. Joliot P., Joliot A. Cyclic electron flow in C3 plants. Biochim. Biophys. Acta 2006, 1757:362-368.
126. Breyton C., Nandha B., Johnson G.N., Joliot P., Finazzi G. Redox modulation of cyclic electron flow around photosystem I in C3 plants. Biochemistry 2006, 45:13465-13475.
127. Takamiya K.I., Dutton P.L. Ubiquinone in Rhodopseudomonas sphaeroides. Some thermodynamic properties. Biochim. Biophys. Acta 1979, 546:1-16.
128. Urban P.F., Klingenberg M. On the redox potentials of ubiquinone and cytochrome b in the respiratory chain. Eur. J. Biochem. 1969, 9:519-525.
129. Allen J.F. Botany. State transitions - a question of balance. Science 2003, 299:1530-1532.
130. Eberhard S., Finazzi G., Wollman F.A. The dynamics of photosynthesis. Annu. Rev. Genet. 2008, 42:463-515.
131. Vener A.V., van Kan P.J., Rich P.R., Ohad I.I., Andersson B. Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:1585-1590.
132. Humphrey W., Dalke A., Schulten K. VMD: visual molecular dynamics. J. Mol. Graph. 1996, 14:33-38.
133. 1 complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment. Struct. Fold. Des. 2000, 8:669-684.
134. 2 oxidoreductase of Rhodopseudomonas capsulata. Evidence from a mutant defective in ubiquinol oxidation. J. Biol. Chem. 1986, 261:584-591.
135. 1 complex from Rhodobacter sphaeroides site directed mutagenesis. Biochemistry 1991, 30:6747-6754.
136. 2 from Rhodopseudomonas sphaeroides. FEBS Lett. 1982, 149:223-227.
137. 2 oxidoreductase from Rhodobacter capsulatus: definition of a minimal, functional isolated preparation. Biochemistry 1993, 32:1310-1317.
138. 1 complex. Biochemistry 2002, 41:14372-14382.
139. 1 complex. J. Biol. Chem. 2002, 277:3464-3470.
140. Rich P.R., Heathcote P., Moss D.A. Kinetic studies of electron transfer in a hybrid system constructed from the cytochrome bf complex and photosystem I. Biochim. Biophys. Acta 1987, 892:138-151.