Summary
Cytochrome bo is a terminal quinol oxidase of the aerobic respiratory chain of Escherichia coli and catalyzes not only the scalar protolytic reactions but also redox-coupled proton pumping. Structure-function studies of the quinol oxidation site (QL) using systematically selected quinone analogues, 1,4-benzoquinones, substituted phenols, and ubiquinone-2 derivatives revealed the structural features of the quinol oxidation site. We found further that bacterial quinol oxidases share common features of the quinol oxidation site irrespective of their structural similarities. In addition, we identified the presence of a tightly bound ubiquinone-8 (QH) and examined the possible roles of the QH site in the two-electron oxidation of substrates at the QL site and in mediating sequential one-electron transfer from QL to the low-spin heme b. Based on these observations, we discuss molecular mechanism of the substrate oxidation by cytochrome bo.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Anraku Y, Gennis RB (1987) The aerobic respiratory chain of Escherichia coli. Trends Biochem Sci 12: 262–266
Saraste M (1990) Structural features of cytochrome oxidase. Q Rev Biophys 23: 331–336
Mogi T, Nakamura H, Anraku Y (1994) Molecular structure of a heme-copper redox center of the Escherichia coli ubiquinol oxidase: evidence and model. J Biochem (Tokyo) 116: 471–477
Garcia-Horsman JA, Barquera B, Rumbley J, et al. (1994) The superfamily of hemecopper respiratory oxidases. J Bacteriol 176: 5587–5600
Iwata S, Ostermeier C, Ludwig B, et al. (1995) Structure at 2.8Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376: 660–669
Tsukihara T, Aoyama H, Yamashita E, et al. (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272: 1136–1144
Wilmanns M, Lappalainen P, Kelly M, et al. (1995) Crystal structure of the membrane-exposed domain from a respiratory quinol oxidase complex with an engineered dinuclear copper center. Proc Natl Acad Sci USA 92: 11955–11959
Welter R, Gu LQ, Yu L, et al. (1994) Identification of the ubiquinol-binding site in the cytochrome boa-ubiquinol oxidase of Escherichia coli. J Biol Chem 269: 28834–28838
Castresana J, Lübben M, Saraste M, et al. (1994) Evolution of cytochrome oxidase, an enzyme older than atomospheric oxygen. EMBO J 13: 2516–2525
Kita K, Konishi K, Anraku Y (1984) Terminal oxidases of Escherichia coli aerobic respiratory chain. I. Purification and properties of cytochrome b562-o complex from cells in the early exponential phase of aerobic growth. J Biol Chem 259: 3368–3374
Matsushita K, Patel L, Kaback HR (1984) Cytochrome o type oxidase from Escherichia coli. Characterization of the enzyme and mechanism of electrochemical proton gradient generation. Biochemistry 23: 4703–4714
Meunier B, Madgwick SA, Reil E, et al. (1995) New inhibitors of the quinol oxidation sites of bacterial cytochromes bo and bd. Biochemistry 34: 1076–1083
Sato-Watanabe M, Mogi T, Miyoshi H, et al. (1994) Structure-function studies on the ubiquinol oxidation site of the cytochrome bo complex from Escherichia coli using pbenzoquinones and substituted phenols. J Biol Chem 269: 28899–28907
Hansch C, Leo A (1979) In: Substituent constants for correlation analysis in chemistry and biology. Wiley, New York
Bondi A (1964) van der Waals volumes and radii. J Phys Chem 68:441–451
Sakamoto K, Miyoshi H, Takegami K, et al. (1996) Probing substrate binding site of the Escherichia coli quinol oxidases using synthetic ubiquinol analogues. J Biol Chem 271: 29897–29902
Okamura MY, Feher G (1992) Proton transfer in reaction center from photosynthetic bacteria. Annu Rev Biochem 61: 861–896
Mitchell P (1976) Possible molecular mechanisms of the protonmotive function of cytochrome system. J Theor Biol 62: 327–367
Brandt U (1996) Energy conservation by bifurcated electron-transfer in the cytochrome-bc, complex. Biochim Biophys Acta 1275: 41–46
Orii Y, Mogi T, Sato-Watanabe M, et al. (1995) Facilitated intramolecular electron transfer in the Escherichia coli bo-type ubiquinol oxidase requires chloride. Biochemistry 34: 1127–1132
Wang J, Rumbley J, Ching YC, et al. (1995) Reaction of cytochrome bo, with oxygen: extra redox center(s) are present in the protein. Biochemistry 34: 15504–15511
Sato-Watanabe M, Mogi T, Ogura T, et al. (1994) Identification of a novel quinone-binding site in the cytochrome bo complex from Escherichia coli. J Biol Chem 269: 28908–28912
Svensson-Ek M, Thomas JW, Gennis RB, et al. (1996) Kinetics of electron and proton transfer during the reaction of wild type and helix VI mutants of cytochrome bo, with oxygen. Biochemistry 35: 13673–13680
Puustinen A, Verkhovsky MI, Morgan JE, et al. (1996) Reaction of the Escherichia coli quinol oxidase cytochrome bo with dioxygen: the role of a bound ubiquinone molecule. Proc Natl Acad Sci USA 93: 1545–1548
Zickermann I, Anemüller S, Richter OMH, et al. (1996) Biochemical and spectroscopic properties of the four-subunit quinol oxidase (cytochrome ba,) from Paracoccus denitrificans. Biochim Biophys Acta 1277: 93–102
Sato-Watanabe M, Itoh S, Mogi T, et al. (1995) Stabilization of a semiquinone radical at the high-affinity quinone-binding site (QH) of the Escherichia coli bo-type ubiquinol oxidase. FEBS Lett 374: 265–269
Ingledew WJ, Ohnishi T, Salerno JC (1995) Studies on a stabilization of ubisemiquinone by Escherichia coli quinol oxidase, cytochrome bo. Eur J Biochem 227: 903–908
Osborn JP, Musser SM, Scultz BE, et al. (1996) Rapid formation of a ubisemiquinone species upon oxidation of quinol by the cytochrome bo, from Escherichia coli. Keio J Med 45: S52
Sato-Watanabe M, Mogi T, Miyoshi H, et al. (1995) Characterization of the quinol oxidation site of the E. coli cytochrome bo complex. Biophys J 68: A318
Yang FD, Yu L, Yu CA, et al. (1986) Use of an azido-ubiquinone derivative to identify subunit I as the ubiquinol-binding site of the cytochrome d terminal oxidase complex of Escherichia coli. J Biol Chem 261: 14987–14990
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1998 Springer-Verlag Tokyo
About this paper
Cite this paper
Sato-Watanabe, M., Mogi, T., Miyoshi, H., Anraku, Y. (1998). Cooperation of Two Quinone-Binding Sites in the Oxidation of Substrates by Cytochrome bo . In: Ishimura, Y., Shimada, H., Suematsu, M. (eds) Oxygen Homeostasis and Its Dynamics. Keio University Symposia for Life Science and Medicine, vol 1. Springer, Tokyo. https://doi.org/10.1007/978-4-431-68476-3_3
Download citation
DOI: https://doi.org/10.1007/978-4-431-68476-3_3
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-68478-7
Online ISBN: 978-4-431-68476-3
eBook Packages: Springer Book Archive