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Science 24 May 1996:
Vol. 272. no. 5265, pp. 1136 - 1144
DOI: 10.1126/science.272.5265.1136
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Research Articles

The Whole Structure of the 13-Subunit Oxidized Cytochrome c Oxidase at 2.8 Å

Tomitake Tsukihara, Hiroshi Aoyama, Eiki Yamashita, Takashi Tomizaki, Hiroshi Yamaguchi, Kyoko Shinzawa-Itoh, Ryosuke Nakashima, Rieko Yaono, Shinya Yoshikawa *

The crystal structure of bovine heart cytochrome c oxidase at 2.8 Å resolution with an R value of 19.9 percent reveals 13 subunits, each different from the other, five phosphatidyl ethanolamines, three phosphatidyl glycerols and two cholates, two hemes A, and three copper, one magnesium, and one zinc. Of 3606 amino acid residues in the dimer, 3560 have been converged to a reasonable structure by refinement. A hydrogen-bonded system, including a propionate of a heme A (heme a), part of peptide backbone, and an imidazole ligand of CuA, could provide an electron transfer pathway between CuA and heme a. Two possible proton pathways for pumping, each spanning from the matrix to the cytosolic surfaces, were identified, including hydrogen bonds, internal cavities likely to contain water molecules, and structures that could form hydrogen bonds with small possible conformational change of amino acid side chains. Possible channels for chemical protons to produce H2O, for removing the produced water, and for O2, respectively, were identified.

T. Tsukihara, H. Aoyama, E. Yamashita, T. Tomizaki, H. Yamaguchi are at the Institute for Protein Research, Osaka University, 3-2 Yamada-oka, Suita 565, Japan.
K. Shinzawa-Itoh, R. Nakashima, R. Yaono, S. Yoshikawa are at the Department of Life Science, Himeji Institute of Technology, Kamigohri Akoh, Hyogo 678-12, Japan.
* To whom correspondence should be addressed.


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R. R. Hantgan, D. S. Lyles, T. C. Mallett, M. Rocco, C. Nagaswami, and J. W. Weisel (2003)
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S. Naithani, S. A. Saracco, C. A. Butler, and T. D. Fox (2003)
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PNAS 99, 12955-12958
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Molecular and Spectroscopic Analysis of the Cytochrome cbb3 Oxidase from Pseudomonas stutzeri.
R. S. Pitcher, M. R. Cheesman, and N. J. Watmough (2002)
J. Biol. Chem. 277, 31474-31483
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A. Camara-Artigas, D. Brune, and J. P. Allen (2002)
PNAS 99, 11055-11060
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Metabolic consequences of a novel missense mutation of the mtDNA CO I gene.
D. A. Varlamov, A. P. Kudin, S. Vielhaber, R. Schroder, R. Sassen, A. Becker, D. Kunz, K. Haug, J. Rebstock, A. Heils, et al. (2002)
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E. Leal-Pinto, B. E. Cohen, M. S. Lipkowitz, and R. G. Abramson (2002)
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Nitric Oxide Reacts with the Single-electron Reduced Active Site of Cytochrome c Oxidase.
A. Giuffre, M. C. Barone, M. Brunori, E. D'Itri, B. Ludwig, F. Malatesta, H.-W. Muller, and P. Sarti (2002)
J. Biol. Chem. 277, 22402-22406
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Membrane Potential-controlled Inhibition of Cytochrome c Oxidase by Zinc.
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   Abstract »    Full Text »    PDF »
Localization and topology of a urate transporter/channel, a galectin, in epithelium-derived cells.
J. Z. Rappoport, M. S. Lipkowitz, and R. G. Abramson (2001)
Am J Physiol Cell Physiol 281, C1926-C1939
   Abstract »    Full Text »    PDF »
Role of positively charged transmembrane segments in the insertion and assembly of mitochondrial inner-membrane proteins.
Y. Saint-Georges, P. Hamel, C. Lemaire, and G. Dujardin (2001)
PNAS 98, 13814-13819
   Abstract »    Full Text »    PDF »
Peripheral Mitochondrial Inner Membrane Protein, Mss2p, Required for Export of the Mitochondrially Coded Cox2p C Tail in Saccharomyces cerevisiae.
S. A. Broadley, C. M. Demlow, and T. D. Fox (2001)
Mol. Cell. Biol. 21, 7663-7672
   Abstract »    Full Text »    PDF »
Yeast Sco1, a Protein Essential for Cytochrome c Oxidase Function Is a Cu(I)-binding Protein.
T. Nittis, G. N. George, and D. R. Winge (2001)
J. Biol. Chem. 276, 42520-42526
   Abstract »    Full Text »    PDF »
Cytochrome c oxidase contains an extra charged amino acid cluster in a new type of respiratory chain in the amino-acid-producing Gram-positive bacterium Corynebacterium glutamicum.
J. Sakamoto, T. Shibata, T. Mine, R. Miyahara, T. Torigoe, S. Noguchi, K. Matsushita, and N. Sone (2001)
Microbiology 147, 2865-2871
   Abstract »    Full Text »    PDF »
On the role of the K-proton transfer pathway in cytochrome c oxidase.
M. Brändén, H. Sigurdson, A. Namslauer, R. B. Gennis, P. Ädelroth, and P. Brzezinski (2001)
PNAS
   Abstract »    Full Text »
Gene Cluster of Rhodothermus marinus High-Potential Iron-Sulfur Protein:Oxygen Oxidoreductase, a caa3-Type Oxidase Belonging to the Superfamily of Heme-Copper Oxidases.
M. Santana, M. M. Pereira, N. P. Elias, C. M. Soares, and M. Teixeira (2001)
J. Bacteriol. 183, 687-699
   Abstract »    Full Text »
A Functional-Phylogenetic Classification System for Transmembrane Solute Transporters.
M. H. Saier Jr. (2000)
Microbiol. Mol. Biol. Rev. 64, 354-411
   Abstract »    Full Text »    PDF »
Internal packing of helical membrane proteins.
M. Eilers, S. C. Shekar, T. Shieh, S. O. Smith, and P. J. Fleming (2000)
PNAS 97, 5796-5801
   Abstract »    Full Text »    PDF »
A Pathogenic 15-Base Pair Deletion in Mitochondrial DNA-encoded Cytochrome c Oxidase Subunit III Results in the Absence of Functional Cytochrome c Oxidase.
K. C. Hoffbuhr, E. Davidson, B. A. Filiano, M. Davidson, N. G. Kennaway, and M. P. King (2000)
J. Biol. Chem. 275, 13994-14003
   Abstract »    Full Text »    PDF »
Membrane Topology and Insertion of Membrane Proteins: Search for Topogenic Signals.
M. van Geest and J. S. Lolkema (2000)
Microbiol. Mol. Biol. Rev. 64, 13-33
   Abstract »    Full Text »    PDF »
Cytochrome oxidase immunohistochemistry: clues for genetic mechanisms.
S. Rahman, B. D. Lake, J.-W. Taanman, M. G. Hanna, J. M. Cooper, A. H. V. Schapira, and J. V. Leonard (2000)
Brain 123, 591-600
   Abstract »    Full Text »    PDF »
Phosphatidylglycerol Is Involved in the Dimerization of Photosystem II.
O. Kruse, B. Hankamer, C. Konczak, C. Gerle, E. Morris, A. Radunz, G. H. Schmid, and J. Barber (2000)
J. Biol. Chem. 275, 6509-6514
   Abstract »    Full Text »    PDF »
Time Dependence of the Catalytic Intermediates in Cytochrome c Oxidase.
S. Han, S. Takahashi, and D. L. Rousseau (2000)
J. Biol. Chem. 275, 1910-1919
   Abstract »    Full Text »    PDF »


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