The cytochrome ba3 oxygen reductase from Thermus thermophilus uses a single input channel for proton delivery to the active site and for proton pumping

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 38, 2009, Pages 16169-16173

  Chang, Hsin Yang ^a   Hemp, James ^a   Chen, Ying ^b   Fee, James A ^b   Gennis, Robert B ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Cytochrome c oxidase; Respiratory enzymes

Indexed keywords

CYTOCHROME BA3 OXYGEN REDUCTASE; CYTOCHROME REDUCTASE; PROTON; PROTON PUMP; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CYTOCHROME B; CYTOCHROME BA3; CYTOCHROME C OXIDASE; OXYGEN;

ARTICLE; CHEMICAL REACTION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; STEADY STATE; THERMUS THERMOPHILUS; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PH; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

PROKARYOTA; THERMUS THERMOPHILUS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; CYTOCHROME B GROUP; CYTOCHROME REDUCTASES; ELECTRON TRANSPORT COMPLEX IV; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; OXIDATION-REDUCTION; OXYGEN; PROTEIN STRUCTURE, TERTIARY; PROTON PUMPS; PROTONS; SEQUENCE HOMOLOGY, AMINO ACID; THERMUS THERMOPHILUS;

EID: 70349493006     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0905264106     Document Type: Article

References (44)

1. Hosler JP, Ferguson-Miller S, Mills DA (2006) Energy transduction: Proton transfer through the respiratory complexes. Annu Rev Biochem 75:165-187. (Pubitemid 44118030)
2. Pereira MM, Santana M, Teixeira M (2001) A novel scenario for the evolution of haem-copper oxygen reductases. Biochim Biophys Acta 1505:185-208. (Pubitemid 32378771)
3. Hemp J, Gennis RB (2008) Diversity of the heme-copper superfamily in Archae: Insights from genomics and structural modeling. Results Problems Cell Differentiation 1-31.
4. Gennis RB (1998) Multiple proton-conducting pathways in cytochrome oxidase and a proposed role for active-site tyrosine. Biochim Biophy. Acta 1365:241-248.
5. Konstantinov AA, Siletky SA, Mitchell D, Kaulen A, Gennis RB (1997) The roles of the two proton input channels in cytochrome c oxidase from Rhodobacter sphaeroides probed by the effects of site-directed mutations on time-resolved electrogenic intraprotein proton transfer. Proc Natl Acad Sci USA 94:9085-9090. (Pubitemid 27357786)
6. Brzezinski P, Gennis RB (2008) Cytochrome c oxidase: Exciting progress and remaining mysteries. J Bionenerg Biomembr 40:521-531.
7. Durr KL, et al. (2008) A D-pathway mutation decouples the Paracoccus denitrificans cytochrome c oxidase by altering the side-chain orientation of a distant conserved glutamate. J Mol Biol 384:865-877.
8. Soulimane T, et al. (2000) Structure and mechanism of the aberrant ba3-cytochrome c oxidase from Thermus thermophilus. EMBO J 19:1766-1776.
9. Blomberg MRA, Siegbahn PEM, Babcock GT, Wikström M (2000) O-O bond splitting mechanism in cytochrome oxidase. J Inorg Biochem 80:261-269.
10. Popovic DM, Stuchebrukhov AA (2004) Proton pumping mechanism and catalytic cycle of cytochrome c oxidase: Coulombpumpmodel with kinetic gating. FEBS Lett 566:126-130.
11. Olsson MHM, Sharma PK, Warshel A (2005) Simulating redox coupled proton transfer in cytochrome c oxidase: Looking for the proton bottleneck. FEBS Lett 579:2026-2034.
12. Kaukonen M (2007) Calculated reaction cycle of cytochrome c oxidase. J Phys Chem 111:12543-12550.
13. Pisliakov AV, Sharma PK, Chu ZT, Haranczyk M, Warshel A (2008) Electrostatic basis for the unidirectionality of the primary proton transfer in cytochrome c oxidase. Proc Natl Acad Sci USA 105:7726-7731. (Pubitemid 351872706)
14. Xu J, Sharpe MA, Qin L, Ferguson-Miller S, Voth GA (2007) Storage of an excess proton in the hydrogen-bonded network of the D-pathway of cytochrome c oxidase: Identi- fication of a protonated water cluster. J Am Chem Soc 129:2910-2913. (Pubitemid 46417967)
15. Kamiya K, Boreo M, Tateno M, Shiraishi K, Oshiyama A (2007) Possible mechanism of proton transfer through peptide groups in the H-pathway of the bovine cytochrome c oxidase. J Am Chem Soc 129:9663-9673. (Pubitemid 47237480)
16. Kaila VRI, Johansson MP, Laakkonen L, Wikström M (2009) The chemistry of the CuB site in cytochrome c oxidase and the importance of its unique His-Tyr bond. Biochim Biophys Acta 1787:221-233.
17. Fee JA, Case DA, Noodleman L (2008) Toward a chemical mechanism of proton pumping by the B-type cytochrome c oxidases: Application of density functional theory to cytochrome ba3 of Thermus thermophilus. J Am Chem Soc 130:15002-15021.
18. 3-type quinol oxidase from Acidianus ambivalens: Implication for proton translocation. Proc Nat'l Acad Sci USA 96:9591-9596.
19. Agmon N (1995) The Grotthuss mechanism. Chem Phys Lett 244:456-462.
20. Farver O, Chen Y, Fee JA, Pecht I (2006) Electron transfer among the CuA-, heme b- and heme a3-centers of Thermus thermophilus cytochrome ba3. FEBS Lett 580:3417-3421.
21. Siletsky SA, et al. (2007) Time-resolved single-turnover of ba3 oxidase from Thermus thermophilus. Biochim Biophys Acta 1767:1383-1392.
22. Smirnova IA, Zaslavsky D, Fee JA, Gennis RB, Brzezinski P (2008) Electron and proton transfer in the ba3 oxidase from Thermus thermophilus. J Bionenerg Biomembr 40:281-287.
23. Hemp J, et al. (2006) Evolutionary migration of a post-translationally modified active-site residue in the proton-pumping heme-copper oxygen reductases. Biochemistry 45:15405-15410. (Pubitemid 46043109)
24. Rauhamaki V, Baumann M, Soliymani R, Puustinen A, Wikström M (2006) Identification of a histidine-tyrosine cross-link in the active site of the cbb3-type cytochrome c oxidase from Rhodobacter sphaeroides. Proc Natl Acad Sci USA 103:16135-16140.
25. Pereira MM, Sousa FL, Verissimo AF, Teixeira M (2008) Looking for the minimum common denominator in haem-copper oxygen reductases: Towards a unified catalytic mechanism. Biochim Biophys Acta 1777:929-934.
26. Siegbahn PEM, Blomberg MRA (2008) Proton pumping mechanism in cytochrome c oxidase. J Phys Chem A. 112:12772-12780.
27. Siegbahn PEM, Blomberg MRA (2007) Energy diagrams and mechanism for proton pumping in cytochrome c oxidase. Biochim Biophys Acta 1767:1143-1156. (Pubitemid 47313389)
28. Sugitani R, Medvedev DM, Stuchebrukhov AA (2008) Theoretical and computational analysis of the membrane potential generated by cytochrome c oxidase upon single electron injection into the enzyme. Biochim Biophys Acta 1777:1129-1139.
29. Wikström M, Verkhovsky MI (2007) Mechanism and energetics of proton translocation by the respiratory heme-copper oxidases. Biochim Biophys Acta 1767:1200-1214. (Pubitemid 47498307)
30. Michel H (1999) Cytochrome c oxidase: Catalytic cycle and mechanisms of proton pumping, a discussion. Biochemistry 38:15129-15140.
31. Sharpe MA, Ferguson-Miller S (2008) A chemically explicit model for the mechanism of proton pumping in heme-copper oxidases. J Bionenerg Biomembr 40:541-549.
32. Yoshikawa S, et al. (2006) Reaction mechanism of bovine heart cytochrome c oxidase. Biochim Biophys Acta 1757:395-400. (Pubitemid 43993867)
33. Heberle J (2004) A local area network of protonated water molecules. Biophys J 87:2105-2106. (Pubitemid 41071314)
34. Garczarek F, Gerwert K (2006) Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy. Nature 439:109-112. (Pubitemid 43053638)
35. Cukier RI (2005) A molecular dynamics study of water chain formation in the proton-conducting K channel of cytochrome c oxidase. Biochim Biophys Acta 1706:134-146.
36. Vendrel O, Meyer H-D (2005) Proton conduction along a chain of water molecules. Development of a linear model and quantum dynamical investigations using the multiconfiguration time-dependent Hartree method. J Chem Phys 122:104505-104515.
37. Hemp J, et al. (2007) Comparative genomics and site-directed mutagenesis support the existence of only one input channel for protons in the C-family (cbb3 oxidase) of heme-copper oxygen reductases. Biochemistry 46:9963-9972. (Pubitemid 47378586)
38. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797. (Pubitemid 38832724)
39. Chen Y, Hunsicker-Wang LM, Pacoma RL, Luna E, Fee JA (2005) A homologous expression system for obtaining engineered cytochrome ba3 from Thermus thermophilus HB8. Protein Expression Purif 40:299-318. (Pubitemid 40335913)
40. Fee JA, et al. (2000) Integrity of Thermus thermophilus cytochrome c552 synthesized by Escherichia coli cells expressing the host-specific cytochrome c maturation genes, ccmABCDEFGH: Biochemical, spectral and structural characterization of the recombinant protein. Protein Sci 9:2074-2084.
41. Keightey JA, et al. (1995) Molecular genetic and protein chemical characterization of the cytochrome ba3 from Thermus thermophilus HB8. J Biol Chem 270:20345-20358.
42. Kannt A, et al. (1998) Electrical current generation and proton pumping catalyzed by the ba3-type cytochrome c oxidase from Thermus thermophilus. FEBS Lett 434:17-22.
43. Hunsicker-Wang LM, Pacoma RL, Chen Y, Fee JA, Stout CD (2005) A novel cryoprotection scheme for enhancing the diffraction of crystals of the recombinant, integral-membrane cytochrome ba3 from Thermus thermophilus. Acta Crystallogr D 61:340-343.
44. Luna VMM, Chen Y, Fee JA, Stout CD (2008) Crystallographic studies of Xe and Kr binding within the large internal cavity of cytochrome ba3 from Thermus thermophilus: Structural analysis and role of oxygen transport channels in the heme-Cu oxidases. Biochemistry 47:4657-4665. (Pubitemid 351555486)