PDBsum entry 1ar1

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protein ligands metals Protein-protein interface(s) links
Complex (oxidoreductase/antibody) PDB id
Protein chains
529 a.a. *
252 a.a. *
118 a.a. *
108 a.a. *
HEA ×2
LDA ×9
_CU ×3
Waters ×52
* Residue conservation analysis
PDB id:
Name: Complex (oxidoreductase/antibody)
Title: Structure at 2.7 angstrom resolution of the paracoccus denitrificans two-subunit cytochromE C oxidase complexed with an antibody fv fragment
Structure: CytochromE C oxidase. Chain: a. Synonym: cytochrome aa3, complex iv, ferrocytochromE C, oxidoreductase. Engineered: yes. CytochromE C oxidase. Chain: b. Synonym: cytochrome aa3, complex iv, ferrocytochromE C, oxidoreductase.
Source: Paracoccus denitrificans. Organism_taxid: 266. Atcc: 13543. Cellular_location: cytoplasmic membrane. Expressed in: escherichia coli. Expression_system_taxid: 562. Mus musculus. House mouse. Organism_taxid: 10090.
Biol. unit: Tetramer (from PQS)
2.70Å     R-factor:   0.207     R-free:   0.261
Authors: C.Ostermeier,A.Harrenga,U.Ermler,H.Michel
Key ref:
C.Ostermeier et al. (1997). Structure at 2.7 A resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment. Proc Natl Acad Sci U S A, 94, 10547-10553. PubMed id: 9380672 DOI: 10.1073/pnas.94.20.10547
08-Aug-97     Release date:   11-Feb-98    
Go to PROCHECK summary

Protein chain
Pfam   ArchSchema ?
P98002  (COX1B_PARDE) -  Cytochrome c oxidase subunit 1-beta
558 a.a.
529 a.a.
Protein chain
Pfam   ArchSchema ?
P08306  (COX2_PARDE) -  Cytochrome c oxidase subunit 2
298 a.a.
252 a.a.
Protein chain
Pfam   ArchSchema ?
P18525  (HVM54_MOUSE) -  Ig heavy chain V region 5-84
117 a.a.
118 a.a.*
Protein chain
Pfam   ArchSchema ?
P01636  (KV5A4_MOUSE) -  Ig kappa chain V-V region MOPC 149
108 a.a.
108 a.a.*
Key:    PfamA domain  Secondary structure  CATH domain
* PDB and UniProt seqs differ at 20 residue positions (black crosses)

 Enzyme reactions 
   Enzyme class: Chains A, B: E.C.  - Cytochrome-c oxidase.
[IntEnz]   [ExPASy]   [KEGG]   [BRENDA]
      Reaction: 4 ferrocytochrome c + O2 + 4 H+ = 4 ferricytochrome c + 2 H2O
4 × ferrocytochrome c
Bound ligand (Het Group name = HEA)
matches with 50.00% similarity
+ O(2)
+ 4 × H(+)
= 4 × ferricytochrome c
+ 2 × H(2)O
      Cofactor: Cu cation
Molecule diagrams generated from .mol files obtained from the KEGG ftp site
 Gene Ontology (GO) functional annotation 
  GO annot!
  Cellular component     membrane   4 terms 
  Biological process     oxidation-reduction process   8 terms 
  Biochemical function     electron carrier activity     8 terms  


DOI no: 10.1073/pnas.94.20.10547 Proc Natl Acad Sci U S A 94:10547-10553 (1997)
PubMed id: 9380672  
Structure at 2.7 A resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment.
C.Ostermeier, A.Harrenga, U.Ermler, H.Michel.
The aa3 type cytochrome c oxidase consisting of the core subunits I and II only was isolated from the soil bacterium Paracoccus denitrificans and crystallized as complex with a monoclonal antibody Fv fragment. Crystals could be grown in the presence of a number of different nonionic detergents. However, only undecyl-beta-D-maltoside and cyclohexyl-hexyl-beta-D-maltoside yielded well-ordered crystals suitable for high resolution x-ray crystallographic studies. The crystals belong to space group P212121 and diffract x-rays to at least 2.5 A (1 A = 0.1 nm) resolution using synchrotron radiation. The structure was determined to a resolution of 2.7 A using molecular replacement and refined to a crystallographic R-factor of 20.5% (Rfree = 25.9%). The refined model includes subunits I and II and the 2 chains of the Fv fragment, 2 heme A molecules, 3 copper atoms, and 1 Mg/Mn atom, a new metal (Ca) binding site, 52 tentatively identified water molecules, and 9 detergent molecules. Only four of the water molecules are located in the cytoplasmic half of cytochrome c oxidase. Most of them are near the interface of subunits I and II. Several waters form a hydrogen-bonded cluster, including the heme propionates and the Mg/Mn binding site. The Fv fragment binds to the periplasmic polar domain of subunit II and is critically involved in the formation of the crystal lattice. The crystallization procedure is well reproducible and will allow for the analysis of the structures of mechanistically interesting mutant cytochrome c oxidases.
  Selected figure(s)  
Figure 1.
Fig. 1. Ribbon representation of the structure of the two-subunit cytochrome c oxidase from P. denitrificans complexed with the antibody F[v] fragment 7E2. Subunit I, olive green; subunit II, dark red; F[v] fragment, blue; heme a, red; heme a[3], blue; copper atoms, dark blue spheres; water molecules, green spheres. The programs MOLSCRIPT (29) and RASTER 3D (30) were used to prepare the figure.
Figure 6.
Fig. 6. The hydrogen bonded network between the heme groups and Cu[A]. Residues of subunit I are shown in olive green, those of subunit II in dark red, copper atoms are dark blue spheres, iron atoms dark red spheres, the Mg/Mn atom is a blue sphere, water molecules are green spheres, heme a is red, and heme a[3] is blue. The figure^ was produced using the programs MOLSCRIPT (29) and RASTER 3D^ (30).
  Figures were selected by an automated process.  

Literature references that cite this PDB file's key reference

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Bovine cytochrome c oxidase structures enable O2 reduction with minimization of reactive oxygens and provide a proton-pumping gate.
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PDB codes: 3ag1 3ag2 3ag3 3ag4
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20576851 S.Buschmann, E.Warkentin, H.Xie, J.D.Langer, U.Ermler, and H.Michel (2010).
The structure of cbb3 cytochrome oxidase provides insights into proton pumping.
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PDB code: 3mk7
20396396 Y.Yoshioka, and M.Mitani (2010).
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A peroxide bridge between Fe and Cu ions in the O2 reduction site of fully oxidized cytochrome c oxidase could suppress the proton pump.
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PDB codes: 2zxw 3abl 3abm
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19348907 L.Geren, B.Durham, and F.Millett (2009).
Chapter 28 Use of ruthenium photoreduction techniques to study electron transfer in cytochrome oxidase.
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19623382 P.E.Siegbahn, and M.R.Blomberg (2009).
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18509049 A.V.Pisliakov, P.K.Sharma, Z.T.Chu, M.Haranczyk, and A.Warshel (2008).
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18459161 D.Horn, and A.Barrientos (2008).
Mitochondrial copper metabolism and delivery to cytochrome c oxidase.
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18953640 D.Xia, L.Esser, M.Elberry, F.Zhou, L.Yu, and C.A.Yu (2008).
The road to the crystal structure of the cytochrome bc (1) complex from the anoxigenic, photosynthetic bacterium Rhodobacter sphaeroides.
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18664577 E.A.Gorbikova, I.Belevich, M.Wikström, and M.I.Verkhovsky (2008).
The proton donor for O-O bond scission by cytochrome c oxidase.
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18752061 I.A.Smirnova, D.Zaslavsky, J.A.Fee, R.B.Gennis, and P.Brzezinski (2008).
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17949262 I.Belevich, and M.I.Verkhovsky (2008).
Molecular mechanism of proton translocation by cytochrome C oxidase.
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18956030 J.P.Collman, and R.A.Decréau (2008).
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17876762 M.P.Johansson, V.R.Kaila, and L.Laakkonen (2008).
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18294138 M.S.Muntyan, and D.A.Bloch (2008).
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18771294 M.S.Rogers, R.Hurtado-Guerrero, S.J.Firbank, M.A.Halcrow, D.M.Dooley, S.E.Phillips, P.F.Knowles, and M.J.McPherson (2008).
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PDB codes: 2vz1 2vz3
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18953727 S.Gupta, and S.Mazumdar (2008).
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18430799 V.R.Kaila, M.I.Verkhovsky, G.Hummer, and M.Wikström (2008).
Glutamic acid 242 is a valve in the proton pump of cytochrome c oxidase.
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  18084085 B.Liu, V.M.Luna, Y.Chen, C.D.Stout, and J.A.Fee (2007).
An unexpected outcome of surface engineering an integral membrane protein: improved crystallization of cytochrome ba(3) from Thermus thermophilus.
  Acta Crystallogr Sect F Struct Biol Cryst Commun, 63, 1029-1034.
PDB codes: 2qpd 2qpe
17514341 C.Dallacosta, W.A.Alves, A.M.da Costa Ferreira, E.Monzani, and L.Casella (2007).
A new dinuclear heme-copper complex derived from functionalized protoporphyrin IX.
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17895387 J.Treuffet, K.J.Kubarych, J.C.Lambry, E.Pilet, J.B.Masson, J.L.Martin, M.H.Vos, M.Joffre, and A.Alexandrou (2007).
Direct observation of ligand transfer and bond formation in cytochrome c oxidase by using mid-infrared chirped-pulse upconversion.
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17470809 K.Muramoto, K.Hirata, K.Shinzawa-Itoh, S.Yoko-o, E.Yamashita, H.Aoyama, T.Tsukihara, and S.Yoshikawa (2007).
A histidine residue acting as a controlling site for dioxygen reduction and proton pumping by cytochrome c oxidase.
  Proc Natl Acad Sci U S A, 104, 7881-7886.
PDB codes: 2eij 2eik 2eil 2eim 2ein
17668091 K.N.White, I.Sen, I.Szundi, Y.R.Landaverry, L.E.Bria, J.P.Konopelski, M.M.Olmstead, and O.Einarsdóttir (2007).
Synthesis and structural characterization of cross-linked histidine-phenol Cu(ii) complexes as cytochrome c oxidase active site models.
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17360500 K.Shimokata, Y.Katayama, H.Murayama, M.Suematsu, T.Tsukihara, K.Muramoto, H.Aoyama, S.Yoshikawa, and H.Shimada (2007).
The proton pumping pathway of bovine heart cytochrome c oxidase.
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Conserved lipid-binding sites in membrane proteins: a focus on cytochrome c oxidase.
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18240421 M.Hüttemann, I.Lee, L.Samavati, H.Yu, and J.W.Doan (2007).
Regulation of mitochondrial oxidative phosphorylation through cell signaling.
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17350588 M.H.Olsson, P.E.Siegbahn, M.R.Blomberg, and A.Warshel (2007).
Exploring pathways and barriers for coupled ET/PT in cytochrome c oxidase: a general framework for examining energetics and mechanistic alternatives.
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17565764 O.Schiemann, and T.F.Prisner (2007).
Long-range distance determinations in biomacromolecules by EPR spectroscopy.
  Q Rev Biophys, 40, 1.  
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Spectroscopic characterization of heme iron-nitrosyl species and their role in NO reductase mechanisms in diiron proteins.
  Nat Prod Rep, 24, 610-620.  
18021063 P.R.Rich, and M.Iwaki (2007).
A comparison of catalytic site intermediates of cytochrome c oxidase and peroxidases.
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17571060 T.G.Schmidt, and A.Skerra (2007).
The Strep-tag system for one-step purification and high-affinity detection or capturing of proteins.
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17997553 T.Hayashi, I.J.Lin, Y.Chen, J.A.Fee, and P.Moënne-Loccoz (2007).
Fourier transform infrared characterization of a CuB-nitrosyl complex in cytochrome ba3 from Thermus thermophilus: relevance to NO reductase activity in heme-copper terminal oxidases.
  J Am Chem Soc, 129, 14952-14958.  
16761090 D.M.Popovic, and A.A.Stuchebrukhov (2006).
Two conformational states of Glu242 and pKas in bovine cytochrome c oxidase.
  Photochem Photobiol Sci, 5, 611-620.  
16791638 I.Bento, M.A.Carrondo, and P.F.Lindley (2006).
Reduction of dioxygen by enzymes containing copper.
  J Biol Inorg Chem, 11, 539-547.  
17176062 J.Hemp, D.E.Robinson, K.B.Ganesan, T.J.Martinez, N.L.Kelleher, and R.B.Gennis (2006).
Evolutionary migration of a post-translationally modified active-site residue in the proton-pumping heme-copper oxygen reductases.
  Biochemistry, 45, 15405-15410.  
16756489 J.P.Hosler, S.Ferguson-Miller, and D.A.Mills (2006).
Energy transduction: proton transfer through the respiratory complexes.
  Annu Rev Biochem, 75, 165-187.  
17203431 L.Laakkonen, R.W.Jobson, and V.A.Albert (2006).
A new model for the evolution of carnivory in the bladderwort plant (utricularia): adaptive changes in cytochrome C oxidase (COX) provide respiratory power.
  Plant Biol (Stuttg), 8, 758-764.  
17050688 L.Qin, C.Hiser, A.Mulichak, R.M.Garavito, and S.Ferguson-Miller (2006).
Identification of conserved lipid/detergent-binding sites in a high-resolution structure of the membrane protein cytochrome c oxidase.
  Proc Natl Acad Sci U S A, 103, 16117-16122.
PDB code: 2gsm
16614069 M.H.Olsson, and A.Warshel (2006).
Monte Carlo simulations of proton pumps: on the working principles of the biological valve that controls proton pumping in cytochrome c oxidase.
  Proc Natl Acad Sci U S A, 103, 6500-6505.  
16387770 O.Farver, E.Grell, B.Ludwig, H.Michel, and I.Pecht (2006).
Rates and Equilibrium of CuA to heme a electron transfer in Paracoccus denitrificans cytochrome c oxidase.
  Biophys J, 90, 2131-2137.  
16842995 P.Brzezinski, and P.Adelroth (2006).
Design principles of proton-pumping haem-copper oxidases.
  Curr Opin Struct Biol, 16, 465-472.  
17001032 P.Haste Andersen, M.Nielsen, and O.Lund (2006).
Prediction of residues in discontinuous B-cell epitopes using protein 3D structures.
  Protein Sci, 15, 2558-2567.  
16820845 R.P.Pesavento, D.A.Pratt, J.Jeffers, and W.A.van der Donk (2006).
Model studies of the Cu(B) site of cytochrome c oxidase utilizing a Zn(II) complex containing an imidazole-phenol cross-linked ligand.
  Dalton Trans, (), 3326-3337.  
16060654 D.A.Mills, L.Geren, C.Hiser, B.Schmidt, B.Durham, F.Millett, and S.Ferguson-Miller (2005).
An arginine to lysine mutation in the vicinity of the heme propionates affects the redox potentials of the hemes and associated electron and proton transfer in cytochrome c oxidase.
  Biochemistry, 44, 10457-10465.  
16192282 E.Olkhova, V.Helms, and H.Michel (2005).
Titration behavior of residues at the entrance of the D-pathway of cytochrome c oxidase from paracoccus denitrificans investigated by continuum electrostatic calculations.
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16151864 I.Bertini, G.Cavallaro, and A.Rosato (2005).
A structural model for the adduct between cytochrome c and cytochrome c oxidase.
  J Biol Inorg Chem, 10, 613-624.
PDB code: 1zyy
15857953 J.Xu, and G.A.Voth (2005).
Computer simulation of explicit proton translocation in cytochrome c oxidase: the D-pathway.
  Proc Natl Acad Sci U S A, 102, 6795-6800.  
15735345 L.M.Hunsicker-Wang, R.L.Pacoma, Y.Chen, J.A.Fee, and C.D.Stout (2005).
A novel cryoprotection scheme for enhancing the diffraction of crystals of recombinant cytochrome ba3 oxidase from Thermus thermophilus.
  Acta Crystallogr D Biol Crystallogr, 61, 340-343.
PDB code: 1xme
15696544 M.D.Swain, and D.E.Benson (2005).
Geometric preferences of crosslinked protein-derived cofactors reveal a high propensity for near-sequence pairs.
  Proteins, 59, 64-71.  
16014708 M.Wikström, C.Ribacka, M.Molin, L.Laakkonen, M.Verkhovsky, and A.Puustinen (2005).
Gating of proton and water transfer in the respiratory enzyme cytochrome c oxidase.
  Proc Natl Acad Sci U S A, 102, 10478-10481.  
15583964 R.A.Ghiladi, H.W.Huang, P.Moënne-Loccoz, J.Stasser, N.J.Blackburn, A.S.Woods, R.J.Cotter, C.D.Incarvito, A.L.Rheingold, and K.D.Karlin (2005).
Heme-copper/dioxygen adduct formation relevant to cytochrome c oxidase: spectroscopic characterization of [(6L)FeIII-(O2(2-))-CuII]+.
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15868183 S.Hirota, H.Okumura, S.Kuroiwa, N.Funasaki, and Y.Watanabe (2005).
Reduction of ferricytochrome c by tyrosyltyrosylphenylalanine.
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15807657 S.Papa (2005).
Role of cooperative H(+)/e(-) linkage (redox bohr effect) at heme a/Cu(A) and heme a(3)/Cu(B) in the proton pump of cytochrome c oxidase.
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16163550 T.M.Bandeiras, M.M.Pereira, M.Teixeira, P.Moenne-Loccoz, and N.J.Blackburn (2005).
Structure and coordination of CuB in the Acidianus ambivalens aa3 quinol oxidase heme-copper center.
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15377522 B.L.Victor, A.M.Baptista, and C.M.Soares (2004).
Theoretical identification of proton channels in the quinol oxidase aa3 from Acidianus ambivalens.
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14747309 C.Kandt, J.Schlitter, and K.Gerwert (2004).
Dynamics of water molecules in the bacteriorhodopsin trimer in explicit lipid/water environment.
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15041681 C.Koutsoupakis, T.Soulimane, and C.Varotsis (2004).
Probing the Q-proton pathway of ba3-cytochrome c oxidase by time-resolved Fourier transform infrared spectroscopy.
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15240445 D.Flöck, and V.Helms (2004).
A Brownian dynamics study: the effect of a membrane environment on an electron transfer system.
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15041635 E.Olkhova, M.C.Hutter, M.A.Lill, V.Helms, and H.Michel (2004).
Dynamic water networks in cytochrome C oxidase from Paracoccus denitrificans investigated by molecular dynamics simulations.
  Biophys J, 86, 1873-1889.  
15317589 H.Danielsson Thorell, N.H.Beyer, N.H.Heegaard, M.Ohman, and T.Nilsson (2004).
Comparison of native and recombinant chlorite dismutase from Ideonella dechloratans.
  Eur J Biochem, 271, 3539-3546.  
15326290 H.J.Hwang, and Y.Lu (2004).
pH-dependent transition between delocalized and trapped valence states of a CuA center and its possible role in proton-coupled electron transfer.
  Proc Natl Acad Sci U S A, 101, 12842-12847.  
15386632 H.Katayama, T.Tabata, Y.Ishihama, T.Sato, Y.Oda, and T.Nagasu (2004).
Efficient in-gel digestion procedure using 5-cyclohexyl-1-pentyl-beta-D-maltoside as an additive for gel-based membrane proteomics.
  Rapid Commun Mass Spectrom, 18, 2388-2394.  
15111436 K.Bettinger, A.Prutsch, K.Vogtt, and M.Lübben (2004).
Noninvasive auto-photoreduction used as a tool for studying structural changes in heme-copper oxidases by FTIR spectroscopy.
  Biophys J, 86, 3230-3240.  
15236746 P.Brzezinski (2004).
Redox-driven membrane-bound proton pumps.
  Trends Biochem Sci, 29, 380-387.  
15454425 S.Braun-Sand, M.Strajbl, and A.Warshel (2004).
Studies of proton translocations in biological systems: simulating proton transport in carbonic anhydrase by EVB-based models.
  Biophys J, 87, 2221-2239.  
14732697 S.Yohannan, S.Faham, D.Yang, J.P.Whitelegge, and J.U.Bowie (2004).
The evolution of transmembrane helix kinks and the structural diversity of G protein-coupled receptors.
  Proc Natl Acad Sci U S A, 101, 959-963.
PDB codes: 1q5i 1q5j
14645061 A.Burykin, and A.Warshel (2003).
What really prevents proton transport through aquaporin? Charge self-energy versus proton wire proposals.
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A TyrCD1/TrpG8 hydrogen bond network and a TyrB10TyrCD1 covalent link shape the heme distal site of Mycobacterium tuberculosis hemoglobin O.
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Role of the pathway through K(I-362) in proton transfer in cytochrome c oxidase from R. sphaeroides.
  Biochemistry, 37, 2470-2476.  
9665692 P.H.Tsatsos, K.Reynolds, E.F.Nickels, D.Y.He, C.A.Yu, and R.B.Gennis (1998).
Using matrix-assisted laser desorption ionization mass spectrometry to map the quinol binding site of cytochrome bo3 from Escherichia coli.
  Biochemistry, 37, 9884-9888.  
9585553 P.Hellwig, J.Behr, C.Ostermeier, O.M.Richter, U.Pfitzner, A.Odenwald, B.Ludwig, H.Michel, and W.Mäntele (1998).
Involvement of glutamic acid 278 in the redox reaction of the cytochrome c oxidase from Paracoccus denitrificans investigated by FTIR spectroscopy.
  Biochemistry, 37, 7390-7399.  
9788983 R.B.Gennis (1998).
How does cytochrome oxidase pump protons?
  Proc Natl Acad Sci U S A, 95, 12747-12749.  
9751640 R.M.Garavito (1998).
Membrane protein structures: the known world expands.
  Curr Opin Biotechnol, 9, 344-349.  
9922138 S.Karlin, Z.Y.Zhu, and K.D.Karlin (1998).
Extended metal environments of cytochrome c oxidase structures.
  Biochemistry, 37, 17726-17734.  
9772174 T.K.Das, C.Pecoraro, F.L.Tomson, R.B.Gennis, and D.L.Rousseau (1998).
The post-translational modification in cytochrome c oxidase is required to establish a functional environment of the catalytic site.
  Biochemistry, 37, 14471-14476.  
9485458 T.V.Vygodina, C.Pecoraro, D.Mitchell, R.Gennis, and A.A.Konstantinov (1998).
Mechanism of inhibition of electron transfer by amino acid replacement K362M in a proton channel of Rhodobacter sphaeroides cytochrome c oxidase.
  Biochemistry, 37, 3053-3061.  
The most recent references are shown first. Citation data come partly from CiteXplore and partly from an automated harvesting procedure. Note that this is likely to be only a partial list as not all journals are covered by either method. However, we are continually building up the citation data so more and more references will be included with time. Where a reference describes a PDB structure, the PDB codes are shown on the right.