The inhibitor DBMIB provides insight into the functional architecture of the Qo site in the cytochrome b6f complex

Biochemistry

Volumn 43, Issue 24, 2004, Pages 7707-7716

  Roberts, A G ^a,b   Bowman, M K ^a,c   Kramer, D M ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BENZENE; CRYSTAL STRUCTURE; OXIDATION; PARAMAGNETIC RESONANCE; PROTEINS; SINGLE CRYSTALS;

MITOCHONDRIA;

BIOCHEMICAL ENGINEERING;

2,5 DIBROMO 6 ISOPROPYL 3 METHYLBENZOQUINONE; CYTOCHROME B; CYTOCHROME B6; CYTOCHROME C1; CYTOCHROME F; IRON SULFUR PROTEIN; MYXOTHIAZOL; OXIDOREDUCTASE; QUINOL OXIDASE; STIGMATELLIN; TRIDECYLSTIGMATELLIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CHICKEN; COMPLEX FORMATION; CRYSTAL STRUCTURE; CYANOBACTERIUM; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME STRUCTURE; EXCITATION; MASTIGOCLADUS LAMINOSUS; MITOCHONDRION; NONHUMAN; OXIDATION; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; REDUCTION; STOICHIOMETRY; THYLAKOID; X RAY CRYSTALLOGRAPHY;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CYTOCHROME B6F COMPLEX; DIBROMOTHYMOQUINONE; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME INHIBITORS; KINETICS; MODELS, MOLECULAR; OXIDATION-REDUCTION;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; GALLUS GALLUS; MASTIGOCLADUS LAMINOSUS; SPINACIA OLERACEA;

EID: 2942744706     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049521f     Document Type: Article

References (98)

1. Berry, E. A., Guergova-Kuras, M., Huang, L., and Crofts, A. R. (2000) Structure and function of cytochrome bc complexes, Annu. Rev. Biochem. 69, 1005-1075.
2. 6f complex; structure of the lumen-side domain of cytochromef, J. Bioenerg. Biomembr. 26, 31-47.
3. 6f complex: de plus ca change de ples c'est la meme chose, J. Bioenerg. Biomembr. 31, 201-213.
4. Hope, A. B. (2000) Electron transfers amongst cytochrome f, plastocyanin and photosystem I: kinetics and mechanisms, Biochim. Biophys. Acta 1456, 5-26.
5. Trumpower, B. L., and Gennis, R. B. (1994) Energy transduction by cytochrome complexes in mitochondrial and bacterial respiration: the enzymology of coupling electron-transfer reactions to transmembrane proton translocation, Annu. Rev. Biochem. 63, 675-716.
6. 1 of quinol-cytochrome c reductase, J. Biol. Chem. 271, 12457-12462.
7. Yu, J., and Le Brun, N. E. (1998) Studies of the cytochrome subunits of menaquinone:cytochrome c reductase (bc complex) of Bacillus subtilis. Evidence for the covalent attachment of heme to the cytochrome b subunit, J. Biol. Chem. 273, 8860-8866.
8. 6f complex-composition structure and function, in Oxygenic Photosynthesis: The Light Reactions (Ort, D. R., and Yocum, C. F., Eds.) pp 377-398, Kluwer Academic Publishers, Dordrecht, The Netherlands.
9. 6f complex, in The Molecular Biology of Cyanobacteria (Bryant, D. A., Ed.) pp 259-317, Kluwer Academic Publishers, Dordrecht, The Netherlands.
10. 6f complex at 8 Å resolution, J. Biol. Chem. 272, 20263-20268.
11. Mitchell, P. (1975) The protonmotive Q cycle: a general formulation, FEBS Lett. 59, 137-139.
12. 2 oxidoreductase? Photosynth. Res. 22, 69-87.
13. 1 complex, J. Biol. Chem. 265, 11409-11412.
14. Crofts, A. R. (1985) The mechanism of the ubiquinol: cytochrome c oxidoreductases of mitochondria and of Rhodopseudomonas sphaeroides, in The Enzymes of Biological Membranes (Martonosi, A. N., Ed.) pp 347-382, Plenum Publishing, New York.
15. Brandt, U., and Trumpower, B. (1994) The protonmotive Q cycle in mitochondria and bacteria, Crit. Rev. Biochem. Mol. Biol. 29, 165-197.
16. 1 complex by proton-gated charge transfer, FEBS Lett. 387, 1-6.
17. 1, Nature 392, 677-684.
18. Chain, R. K., and Malkin, R. (1979) On the interaction of 2,5-dibromo-3-methyl-6-isopropylbenzoquinone (DBMIB) with bound electron carriers in spinach chloroplasts, Arch. Biochem. Biophys. 197, 52-56.
19. Rich, P. R. (1984) Electron and proton transfers through quinones and cytochrome bc complexes, Biochim. Biophys. Acta 768, 53-79.
20. Kramer, D. M., and Crofts, A. R. (1993) The concerted reduction of the high- and low-potential chains of the bf complex by plastoquinol, Biochim. Biophys. Acta 1183, 72-84.
21. Sacksteder, C. A., Kanazawa, A., Jacoby, M. E., and Kramer, D. M. (2000) The proton to electron stoichiometry of steady-state photosynthesis in living plants: A proton-pumping Q cycle is continuously engaged, Proc. Natl. Acad. Sci. U.S.A. 97, 14283-14288.
22. 1 complex, Biochemistry 41, 7866-7874.
23. 1 complex reveal dynamic aspects of mechanism, in Photosynthesis: Mechanisms and Effects (Garab, G., Ed.) pp 1481-1486, Kluwer Academic Publishers, Dordrecht, The Netherlands.
24. 6f complex of oxygenic photosynthesis: tuning the cavity, Science 302, 1009-1014.
25. 1 complex from bovine heart mitochondria, Science 277, 60-66.
26. 1 complex, Biophys. J. 77, 1753-1768.
27. 1: a new device for electron transfer in proteins, Trends Biochem. Sci. 26, 445-451.
28. 1 complex, Science 281, 64-71.
29. 1 complex from the yeast Saccharomyces cerevisiae cocrystallized with an antibody Fv fragment, Struct. Folding Des. 8, 669-684.
30. 1 complex: role of the iron sulfur protein and its mobility, Biochemistry 38, 15791-15806.
31. 1 complex from mitochondria and photosynthetic bacteria, Biochemistry 38, 15827-15839.
32. Brugna, M., Rodgers, S., Schricker, A., Montoya, G., Kazmeier, M., Nitschke, W., and Sinning, I. (2000) A spectroscopic method for observing the domain movement of the Rieske iron-sulfur protein, Proc. Natl. Acad. Sci. U.S.A. 97, 2069-2074.
33. o-site inhibitor DBMIB favours the proximal position of the chloroplast Rieske protein and induces a pK-shift of the redox-linked proton, FEBS Lett. 450, 245-250.
34. Brugna, M., Nitschke, W., Asso, M., Guigliarelli, B., Lemesle-Meunier, D., and Schmidt, C. (1999) Redox components of cytochrome bc-type enzymes in acidophilic prokaryotes. II. The Rieske protein of phylogenetically distant acidophilic organisms, J. Biol. Chem. 274, 16766-16772.
35. Liebl, U., Pezennec, S., Riedel, A., Kellner, E., and Nitschke, W. (1992) The Rieske FeS center from the Gram-positive bacterium PS3 and its interaction with the menaquinone pool studied by EPR, J. Biol. Chem. 267, 14068-14072.
36. 6f complex induced by inhibitor binding, J. Biol. Chem. 275, 13195-13201.
37. 6f complex, Biochemistry 39, 2692-2699.
38. 1 complex by the formation of an intersubunit disulfide bond between cytochrome b and the iron-sulfur protein, J. Biol. Chem. 275, 38597-38604.
39. 1 and its implications for energy conversion, Proc. Natl. Acad. Sci. U.S.A. 97, 4567-4572.
40. 1 complex: domain movement, subunit interactions, and emerging rationale engineering attempts, J. Bioenerg. Biomembr. 31, 275-288.
41. 1 complex, Eur. J. Biochem. 267, 5777-5782.
42. 1 complex: effects of inhibitors and mutations, Biochemistry 39, 15484-15492.
43. o site catalysis, Biochemistry 39, 3285-3296.
44. 6f complex 'Rieske' iron-sulfur protein domain movements, Biochemistry 41, 4070-4079.
45. o site model, Biochemistry 31, 3144-3158.
46. 1 complex, Biochim. Biophys. Acta 1275, 41-46.
47. 1 complex, Biochemistry 34, 15979-15996.
48. o site, J. Bioenerg. Biomembr. 31, 225-233.
49. 1 complex, Biochemistry 38, 14973-14980.
50. 6f complex, Biochemistry 40, 13407-13412.
51. 1 complex, J. Biol. Chem. 276, 35231-35234.
52. Matsuura, K., Bowyer, J. R., Ohnishi, T., and Dutton, P. L. (1983) Inhibition of electron transfer by 3-alkyl-2-hydroxy-1,4-naphthoquinones in the ubiquinol-cytochrome c oxidoreductases of Rhodopseudomonas sphaeroides and mammalian mitochondria, J. Biol. Chem. 258, 1571-1579.
53. o site inhibitor, Biochemistry 38, 3440-3446.
54. Brandt, U., Schagger, H., and von Jagow, G. (1988) Characterisation of binding of the methoxyacrylate inhibitors to mitochondrial cytochrome c reductase, Eur. J. Biochem. 173, 499-506.
55. von Jagow, G., and Ohnishi, T. (1985) The chromone inhibitor stigmatellin-binding to the ubiquinol oxidation center at the c-side of the mitochondrial membrane, FEBS Lett. 185, 311-315.
56. o site inhibitor bound, J. Biol. Chem. 278, 31303-31311.
57. Ohnishi, T., Brandt, U., and von Jagow, G. (1988) Studies on the effect of stigmatellin derivatives on cytochrome b and the Rieske iron-sulfur cluster of cytochrome c reductase from bovine heart mitochondria, Eur. J. Biochem. 176, 385-389.
58. Bowyer, J. R., and Trumpower, B. L. (1980) Inhibition of the oxidant-induced reduction of cytochrome b by a synthetic analogue of ubiquinone, FEBS Lett. 115, 171-174.
59. Link, T. A., Haase, U., Brandt, U., and Jagow, G. v. (1993) What information do inhibitors provide about the structure of hydroquinone oxidation site of ubihydroquinone: cytochrome c oxidoreductase? J. Bioenerg. Biomembr. 25, 221-232.
60. Rich, P. R., Madgwick, S. A., Brown, S., von Jagow, G., and Brandt, U. (1992) MOA-stilbene: a new tool for investigation of the reactions of the chloroplast cytochrome bf complex, Photosynth. Res. 34, 465-477.
61. 1 complex probed by superoxide production, Biochemistry 42, 6493-6499.
62. Loschen, G., and Azzi, A. (1974) Dibromothymoquinone: a new inhibitor of mitochondrial electron transport at the level of ubiquinone, FEBS Lett. 41, 115-117.
63. Riedel, A., Rutherford, A. W., Hauska, G., Muller, A., and Nitschke, W. (1991) Chloroplast Rieske center. EPR study on its spectral characteristics, relaxation and orientation properties, J. Biol. Chem. 266, 17838-17844.
64. Malkin, R. (1981) Redox properties of the DBMIB-Rieske iron-sulfur complex in spinach chloroplast membranes, FEBS Lett. 131, 169-172.
65. Oettmeier, W., Godde, D., Kunze, B., and Hofle, G. (1985) Stigmatellin. A dual type inhibitor of photosynthetic electron transport, Biochim. Biophys. Acta 807, 216-219.
66. a matching on binding affinity and hydrogen bond length, Biochemistry 34, 15459-15466.
67. Prince, R. C., Linkletter, S. J. G., and Dutton, P. L. (1981) The thermodynamic properties of some commonly used oxidation-reduction mediators, inhibitors and dyes, as determined by polarography, Biochim. Biophys. Acta 635, 132-148.
68. Link, T. A. (1994) Two pK values of the oxidized 'Rieske' [2Fe-2S] cluster observed by CD spectroscopy, Biochim. Biophys. Acta 1185, 81-84.
69. Kuila, D., and Fee, J. A. (1986) Evidence for a redox-linked ionizable group associated with the [2Fe-2S] cluster of Thermus Rieske protein, J. Biol. Chem. 261, 2768-2771.
70. Prince, R. C., and Dutton, P. L. (1976) Furthur studies on the Rieske iron-sulfur center in mitochondrial and photosynthetic systems: A pK on the oxidized form, FEBS Lett. 65, 117-119.
71. 1-type Rieske [2Fe-2S] center of Thermus thermophilus, J. Am. Chem. Soc. 123, 9906-9907.
72. Malkin, R. (1981) Interaction of the quinone analogue, DBMIB, with the photosynthetic Rieske iron-sulfur center, Isr. J. Chem. 21, 301-305.
73. Oettmeier, W., Masson, K., and Dostatni, R. (1987) Halogenated 1,4-benzoquinones as irreversibly binding inhibitors of photosynthetic electron transport, Biochim. Biophys. Acta 890, 260-269.
74. Lozier, R. H., and Butler, W. L. (1972) The effects of dibromothymoquinone on fluorescence and electron transport of spinach chloroplasts, FEBS Lett. 26, 161-164.
75. 6 complex of five polypeptides with plastoquinol-plastocyanin-oxidoreductase activity from spinach chloroplasts, Eur. J. Biochem. 117, 591-599.
76. 1-type (Rhodopseudomonas sphaeroides), Methods Enzymol. 126, 271-285.
77. Rutherford, A. W., and Setif, P. (1990) Orientation of P700, the primary electron donor of photosystem I, Biochim. Biophys. Acta 1019, 128-132.
78. Blasie, J. K., Erecinska, M., Samuels, S., and Leigh, J. S. (1978) The structure of a cytochrome oxidase-lipid model membrane, Biochim. Biophys. Acta 501, 33-52.
79. More, C., Belle, V., Asso, M., Fournel, A., Roger, G., and Guigliarelli, B. (1999) EPR spectroscopy: a powerful technique for the structural and functional investigation of metalloproteins, Biospectroscopy 5, S3-S18.
80. Guigliarelli, B., Guillaussier, J., More, C., Setif, P., Bottin, H., and Bertrand, P. (1993) Structural organization of the iron-sulfur centers in Synechocystis 6803 photosystem I, J. Biol. Chem. 268, 900-908.
81. Metzger, S. U., Cramer, W. A., and Whitmarsh, J. (1997) Critical analysis of the extinction coefficient of chloroplast cytochromef, Biochim. Biophys. Acta 1319, 233-241.
82. Bergström, J., and Vanngard, T. (1982) EPR signals and orientation of cytochromes in the spinach chloroplast thylakoid membrane, Biochim. Biophys. Acta 682, 452-456.
83. Crowder, M. S., Prince, R. C., and Bearden, A. (1982) Orientation of membrane-bound cytochromes in chloroplasts, detected by low-temperature EPR spectroscopy, FEBS Lett. 144, 204-208.
84. 6f complex, Nature 426, 413-418.
85. Poole, C. P., Jr. (1983) Electron Spin Resonance: A Comprehensive Treatise on Experimental Techniques, 2nd ed., Dover Publications, Mineola, NY.
86. 1 and related) complexes, Methods Enzymol. 382, 21-45.
87. 1 in complex with famoxadone: the role of aromatic-aromatic interaction in inhibition, Biochemistry 41, 11692-11702.
88. 1 complex from bovine heart, Proc. Natl. Acad. Sci. U.S.A. 95, 8026-8033.
89. Kramer, D. M., and Sacksteder, C. A. (1998) A diffused-optics flash kinetic spectrophotometer (DOFS) for measurements of absorbance changes in intact plants in the steady-state, Photosynth. Res. 56, 103-112.
90. Cruz, J. A., Sacksteder, C. A., Kanazawa, A., and Kramer, D. M. (2001) Contribution of electric field (ΔΨ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo control of pmf parsing into ΔΨ and ΔpH by ionic strength, Biochemistry 40, 1226-1237.
91. Bertrand, P., Guigliarelli, B., Gayda, J.-P., Beardwood, P., and Gibson, J. F. (1985) A ligand-field model to describe a new class of 2Fe-2S clusters in proteins and their synthetic analogues, Biochim. Biophys. Acta 831, 261-266.
92. 1 complex, Biochemistry 43, 430-436.
93. 1 complexes of Rhodospirillum rubrum, Rhodobacter sphaeroides R-26, and bovine heart mitochondria, Biochemistry 30, 1892-1901.
94. o site occupants and the head domain position of the Fe-S protein subunit, Biochemistry 43, 2217-2227.
95. Jones, R. W., and Whitmarsh, J. (1988) 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 933, 258-268.
96. 1 complex, J. Biol. Chem. 277, 3464-3470.
97. 6f complex to structure changes in the hinge region of the Rieske iron-sulfur protein, J. Biol. Chem. 278, 20925-20933.
98. Muster, P., Binder, A., Schneider, K., and Bachofen, R. (1983) Influence of temperature and pH on the growth of the thermophilic cyanobacterium Mastigocladus laminosus in continuous culture, Plant Cell Physiol. 24, 273-280.