Exploring the proton pump and exit pathway for pumped protons in cytochrome ba 3 from Thermus thermophilus

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

Volumn 109, Issue 14, 2012, Pages 5259-5264

  Chang, Hsin Yang ^a   Choi, Sylvia K ^a   Vakkasoglu, Ahmet Selim ^a   Chen, Ying ^b   Hemp, James ^a   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

Bioenergetics; Cytochrome c oxidase; Exit channel; Respiratory chain

Indexed keywords

AMINO ACID; BACTERIAL ENZYME; CYTOCHOME BA3 OXIDASE; CYTOCHROME C OXIDASE; HEME; MUTANT PROTEIN; OXIDOREDUCTASE; PROPIONIC ACID; PROTON; PROTON PUMP; UNCLASSIFIED DRUG; WATER;

ARTICLE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ESCHERICHIA COLI; FOURIER TRANSFORMATION; HYDROGEN BOND; INFRARED SPECTROSCOPY; MOLECULE; MUTATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXYGEN TRANSPORT; PARACOCCUS DENITRIFICANS; PRIORITY JOURNAL; RHODOBACTER SPHAEROIDES; THERMUS THERMOPHILUS; ULTRAVIOLET SPECTROSCOPY;

CATALYTIC DOMAIN; CYTOCHROME B GROUP; ELECTRON TRANSPORT COMPLEX IV; HYDROGEN BONDING; MODELS, MOLECULAR; PROTON PUMPS; PROTONS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; THERMUS THERMOPHILUS;

THERMUS THERMOPHILUS;

EID: 84859446853     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1107345109     Document Type: Article

References (50)

1. Pereira MM, Sousa FL, Veríssimo 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.
2. Hemp J, Gennis RB (2008) Diversity of the heme-copper superfamily in archaea: Insights from genomics and structural modeling. Results Probl Cell Differ 45:1-31.
3. Belevich I, Bloch DA, Belevich N, Wikström M, Verkhovsky MI (2007) Exploring the proton pump mechanism of cytochrome c oxidase in real time. Proc Natl Acad Sci USA 104:2685-2690. (Pubitemid 46327940)
4. Brzezinski P, Gennis RB (2008) Cytochrome c oxidase: Exciting progress and remaining mysteries. J Bioenerg Biomembr 40:521-531.
5. 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)
6. 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)
7. 3-type cytochrome c oxidase from Thermus thermophilus. FEBS Lett 434:17-22.
8. 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)
9. 3-type cytochrome c oxidase from Rhodobacter sphaeroides, a proton-pumping heme-copper oxidase. Biochim Biophys Acta 1365:421-434.
10. Arslan E, Kannt A, Thöny-Meyer L, Hennecke H (2000) The symbiotically essential cbb(3)-type oxidase of Bradyrhizobium japonicum is a proton pump. FEBS Lett 470:7-10. (Pubitemid 30155613)
11. Han H, et al. (2011) Adaptation of aerobic respiration to low O2 environments. Proc Natl Acad Sci USA 108:14109-14114.
12. Belevich I, et al. (2010) Initiation of the proton pump of cytochrome c oxidase. Proc Natl Acad Sci USA 107:18469-18474.
13. Kaila VR, Verkhovsky M, Hummer G, Wikström M (2008) Prevention of leak in the proton pump of cytochrome c oxidase. Biochim Biophys Acta 1777:890-892.
14. Belevich I, Verkhovsky MI (2008) Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxid Redox Signal 10:1-29. (Pubitemid 350115984)
15. Yoshikawa S, et al. (2006) Proton pumping mechanism of bovine heart cytochrome c oxidase. Biochim Biophys Acta 1757:1110-1116. (Pubitemid 44442134)
16. Michel H (1998) The mechanism of proton pumping by cytochrome c oxidasex127e [comments]. Proc Natl Acad Sci USA 95:12819-12824.
17. Siegbahn PEM, Blomberg MRA (2008) Proton pumping mechanism in cytochrome c oxidase. J Phys Chem A 112:12772-12780.
18. Siegbahn PE, Blomberg MR (2007) Energy diagrams and mechanism for proton pumping in cytochrome c oxidase. Biochim Biophys Acta 1767:1143-1156. (Pubitemid 47313389)
19. Olsson MH, Siegbahn PE, Blomberg MR, Warshel A (2007) Exploring pathways and barriers for coupled ET/PT in cytochrome c oxidase: A general framework for examining energetics and mechanistic alternatives. Biochim Biophys Acta 1767:244-260. (Pubitemid 46420433)
20. Sugitani R, Medvedev ES, 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.
21. Kaila VR, Verkhovsky MI, Hummer G, Wikström M (2008) Glutamic acid 242 is a valve in the proton pump of cytochrome c oxidase. Proc Natl Acad Sci USA 105:6255-6259. (Pubitemid 351758333)
22. Daskalakis V, Farantos SC, Guallar V, Varotsis C (2011) Regulation of electron and proton transfer by the protein matrix of cytochrome c oxidase. J Phys Chem B 115:3648-3655.
23. Chang HY, Hemp J, Chen Y, Fee JA, Gennis RB (2009) The cytochrome ba3 oxygen reductase from Thermus thermophilus uses a single input channel for proton delivery to the active site and for proton pumping. Proc Natl Acad Sci USA 106:16169-16173.
24. Sharpe MA, Ferguson-Miller S (2008) A chemically explicit model for the mechanism of proton pumping in heme-copper oxidases. J Bioenerg Biomembr 40:541-549.
25. Popovic DM, Leontyev IV, Beech DG, Stuchebrukhov AA (2010) Similarity of cytochrome c oxidases in different organisms. Proteins 78:2691-2698.
26. Makhov DV, Popović DM, Stuchebrukhov AA (2006) Improved density functional theory/electrostatic calculation of the His291 protonation state in cytochrome C oxidase: Self-consistent charges for solvation energy calculation. J Phys Chem B 110:12162-12166. (Pubitemid 44024841)
27. Wikström M (2000) Mechanism of proton translocation by cytochrome c oxidase: A new four-stroke histidine cycle. Biochim Biophys Acta 1458:188-198.
28. 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.
29. Das TK, et al. (2004) Active site structure of the aa3 quinol oxidase of Acidianus ambivalens. Biochim Biophys Acta 1655:306-320. (Pubitemid 38526194)
30. Puustinen A, Wikström M (1999) Proton exit from the heme-copper oxidase of Escherichia coli. Proc Natl Acad Sci USA 96:35-37. (Pubitemid 29036048)
31. Buschmann S, et al. (2010) The structure of cbb3 cytochrome oxidase provides insights into proton pumping. Science 329:327-330.
32. Lee HJ, Ojemyr L, Vakkasoglu A, Brzezinski P, Gennis RB (2009) Properties of Arg481 mutants of the aa3-type cytochrome c oxidase from Rhodobacter sphaeroides suggest that neither R481 nor the nearby D-propionate of heme a3 is likely to be the proton loading site of the proton pump. Biochemistry 48:7123-7131.
33. Kaila VR, Sharma V, Wikström M (2011) The identity of the transient proton loading site of the proton-pumping mechanism of cytochrome c oxidase. Biochim Biophys Acta 1807:80-84.
34. Siegbahn PEM, Blomberg MRA, Blomberg ML (2003) A theoretical study of the energetics of proton pumping and oxygen reduction in cytochrome oxidase. J Phys Chem B 107:10946-10955.
35. 3-cytochrome c oxidase by time-resolved Fourier transform infrared spectroscopy. Biophys J 86:2438-2444.
36. Luna VM, 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)
37. Hunsicker-Wang LM, Pacoma RL, Chen Y, Fee JA, Stout CD (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. (Pubitemid 43965375)
38. Tiefenbrunn T, et al. (2011) High resolution structure of the ba3 cytochrome c oxidase from Thermus thermophilus in a lipidic environment. PLoS ONE 6:e22348.
39. Rich PR, Iwaki M (2007) Methods to probe protein transitions with ATR infrared spectroscopy. Mol Biosyst 3:398-407. (Pubitemid 46838788)
40. Hellwig P, Soulimane T, Buse G, Mäntele W (1999) Electrochemical, FTIR, and UV/VIS spectroscopic properties of the ba(3) oxidase from Thermus thermophilus. Biochemistry 38:9648-9658.
41. Pfitzner U, et al. (2000) Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 39:6756-6762. (Pubitemid 30390366)
42. Qian J, et al. (1997) Aspartate-407 in Rhodobacter sphaeroides cytochrome c oxidase is not required for proton pumping or manganese binding. Biochemistry 36: 2539-2543. (Pubitemid 27106646)
43. Thomas JW, Puustinen A, Alben JO, Gennis RB, Wikström M (1993) Substitution of asparagine for aspartate-135 in subunit I of the cytochrome bo ubiquinol oxidase of Escherichia coli eliminates proton-pumping activity. Biochemistry 32:10923-10928. (Pubitemid 23327830)
44. Thomas JW, Lemieux LJ, Alben JO, Gennis RB (1993) Site-directed mutagenesis of highly conserved residues in helix VIII of subunit I of the cytochrome bo ubiquinol oxidase from Escherichia coli: An amphipathic transmembrane helix that may be important in conveying protons to the binuclear center. Biochemistry 32:11173-11180. (Pubitemid 23332025)
45. Fetter JR, et al. (1995) Possible proton relay pathways in cytochrome c oxidase. Proc Natl Acad Sci USA 92:1604-1608.
46. Hosler JP, et al. (1996) Polar residues in helix VIII of subunit I of cytochrome c oxidase influence the activity and the structure of the active site. Biochemistry 35:10776-10783. (Pubitemid 26279658)
47. Pfitzner U, et al. (1998) Cytochrome c oxidase (heme aa3) from Paracoccus denitrificians: Analysis of mutations in putative proton channels of subunit I. J Bioenerg Biomembr 30:89-97. (Pubitemid 28262412)
48. Chen Y, Hunsicker-Wang L, Pacoma RL, Luna E, Fee JA (2005) A homologous expression system for obtaining engineered cytochrome ba3 from Thermus thermophilus HB8. Protein Expr Purif 40:299-318. (Pubitemid 40335913)
49. Vakkasoglu AS, Morgan JE, Han D, Pawate AS, Gennis RB (2006) Mutations which decouple the proton pump of the cytochrome c oxidase from Rhodobacter sphaeroides perturb the environment of glutamate 286. FEBS Lett 580:4613-4617. (Pubitemid 44189377)
50. Yang K, et al. (2007) Glutamate 107 in subunit I of the cytochrome bd quinol oxidase from Escherichia coli is protonated and near the heme d/heme b595 binuclear center. Biochemistry 46:3270-3278. (Pubitemid 46453727)