The chemistry of the CuB site in cytochrome c oxidase and the importance of its unique His-Tyr bond

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1787, Issue 4, 2009, Pages 221-233

  Kaila, Ville R I ^a   Johansson, Mikael P ^b   Sundholm, Dage ^c   Laakkonen, Liisa ^c   Wikström, Mårten ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

DFT; Oxygen reduction; Proton transfer; Quantum chemistry

Indexed keywords

COPPER; CYTOCHROME C OXIDASE; HISTONE; PROTON; TYROSINE; HISTIDINE; LIGAND; MUTANT PROTEIN;

ARTICLE; CATALYSIS; CHEMICAL BOND; CROSS LINKING; ELECTRON; ENERGY TRANSFER; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTUM CHEMISTRY; ANIMAL; BIOCATALYSIS; CATTLE; CHEMISTRY; ENZYME ACTIVE SITE; METABOLISM; OXIDATION REDUCTION REACTION; SPIN LABELING; STATIC ELECTRICITY; THERMODYNAMICS;

ANIMALS; BIOCATALYSIS; CATALYTIC DOMAIN; CATTLE; COPPER; ELECTRON TRANSPORT COMPLEX IV; ELECTRONS; HISTIDINE; LIGANDS; MUTANT PROTEINS; OXIDATION-REDUCTION; PROTONS; SPIN LABELS; STATIC ELECTRICITY; THERMODYNAMICS; TYROSINE;

EID: 61349155612     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.01.002     Document Type: Article

References (84)

1. Wikström M.K.F. Proton pump coupled to cytochrome c oxidase in mitochondria. Nature 266 (1977) 271-273
2. Babcock G.T., and Wikström M. Oxygen activation and the conservation of energy in cell respiration. Nature 356 (1992) 301-365
3. Wikström M. Cytochrome c oxidase: 25 years of the elusive proton pump. Biochim. Biophys. Acta 1655 (2004) 241-247
4. Iwata S., Ostermeier C., Ludwig B., and Michel H. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376 (1995) 660-669
5. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., and Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272 (1996) 1136-1144
6. Hosler J.P., Ferguson-Miller S., and Mills D.A. Energy transduction: proton transfer through the respiratory complexes. Annu. Rev. Biochem. 75 (2006) 165-187
7. Brändén G., Gennis R.B., and Brzezinski P. Transmembrane proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta 1757 (2006) 1052-1063
8. Belevich I., and Verkhovsky M.I. Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxid. Redox Signal 10 (2008) 1-29
9. Belevich I., Bloch D., Belevich N., Wikström M., and Verkhovsky M.I. Exploring the proton pump mechanism of cytochrome c oxidase in real time. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 2685-2690
10. Belevich I., Verkhovsky M.I., and Wikström M. Proton-coupled electron transfer drives the proton pump of cytochrome c oxidase. Nature 440 (2006) 829-832
11. Wikström M., Verkhovsky M.I., and Hummer G. Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta 1604 (2003) 61-65
12. Olsson M.H.M., and Warshel A. 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 (2006) 6500-6505
13. Blomberg M.R.A., and Siegbahn P.E.M. Quantum chemistry applied to the mechanisms of transition metal containing enzymes - cytochrome c oxidase, a particularly challenging case. J. Comput. Chem. 12 (2006) 1373-1384
14. Popovic D.M., Quenneville J., and Stuchebrukhov A.A. DFT/electrostatic calculations of pK(a) values in cytochrome c oxidase. J. Phys. Chem. B 109 (2005) 3616-3626
15. Xu J., Sharpe M.A., Qin L., Ferguson-Miller S., and Voth G.A. Storage of an excess proton in the hydrogen-bonded network of the d-pathway of cytochrome C oxidase: identification of a protonated water cluster. J. Am. Chem. Soc. 129 (2007) 2910-2913
16. Fadda E., Chakrabarti N., and Pomès R. Acidity of a Cu-bound histidine in the binuclear center of cytochrome C oxidase. J. Phys. Chem. B 109 (2005) 22629-22640
17. 3 with oxygen. Biochemistry 35 (1996) 13673-13680
18. 3 from Rhodobacter sphaeroides is involved in proton uptake during the reaction of the fully-reduced enzyme with dioxygen. Biochemistry 36 (1997) 13824-13829
19. 3 is involved in proton translocation. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10128-10131
20. Konstantinov A.A., Siletsky S., Mitchell D., Kaulen A., and Gennis R.B. 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. U. S. A. 94 (1997) 9085-9090
21. Kaila V.R.I., Verkhovsky M.I., Hummer G., and Wikström M. Glutamic acid 242 is a valve in the proton pump of cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 6255-6259
22. Kaila V.R.I., Verkhovsky M.I., Hummer G., and Wikström M. Prevention of leak in the proton pump of cytochrome c oxidase. Biochim. Biophys. Acta 1777 (2008) 890-892
23. Wikström M., and Verkhovsky M.I. Mechanism and energetics of proton translocation by the respiratory heme-copper oxidases. Biochim. Biophys. Acta 1767 (2007) 1200-1214
24. Siegbahn P.E.M., and Blomberg M.R.A. Energy diagrams and mechanism for proton pumping in cytochrome c oxidase. Biochim. Biophys. Acta 1767 (2007) 1143-1156
25. Buse G., Soulimane T., Dewor M., Meyer H.E., and Blüggel M. Evidence for a copper-coordinated histidine-tyrosine cross-link in the active site of cytochrome oxidase. Protein Sci. 8 (1999) 985-990
26. Yoshikawa S., Shinzawa-itoh K., Nakashima R., Yaono R., Yamashita E., Inoue N., Yao M., Fei M.J., Libeu C.P., Mizushima T., Yamaguchi H., Tomizaki T., and Tsukihara T. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280 (1998) 1723-1729
27. Babcock G.T. How oxygen is activated and reduced in respiration. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 12971-12973
28. Wiertz F.G., Richter O.M., Cherepanov A.V., MacMillan F., Ludwig B., and de Vries S. An oxo-ferryl tryptophan radical catalytic intermediate in cytochrome c and quinol oxidases trapped by microsecond freeze-hyperquenching (MHQ). FEBS Lett. 575 (2004) 127-130
29. MacMillan F., Budiman K., Angerer H., and Michel H. The role of tryptophan 272 in the Paracoccus denitrificans cytochrome c oxidase. FEBS Lett. 580 (2006) 1345-1349
30. 2. Biochemistry 40 (2001) 6882-6892
31. Gorbikova E.A., Belevich I., Wikström M., and Verkhovsky M.I. The proton donor for O-O bond scission by cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 10733-10737
32. Gennis R.B. Coupled proton and electron transfer reactions in cytochrome oxidase. Front. Biosci. 4 (2004) 581-591
33. Brzezinski P. Redox-driven membrane-bound proton pumps. TIBS 29 (2004) 380-387
34. Kannt A., Soulimane T., Buse G., Becker A., Bamberg E., and Michel H. Electrical current generation and proton pumping catalyzed by the ba3-type cytochrome c oxidase from Thermus thermophilus. FEBS Lett. 434 (1998) 17-22
35. 3 oxidase from Thermus thermophilus. Biochim. Biophys. Acta 1767 (2007) 1383-1392
36. I.A. Smirnova, D. Zaslavsky, J.A. Fee, R.B. Gennis, P. Brzezinski, Electron and proton transfer in the ba(3) oxidase from Thermus thermophilus, J. Bioenerg. Biomembr. (in press)
37. Mitchell R., Mitchell P., and Rich P.R. The assignment of the 655 nm spectral band of cytochrome oxidase. FEBS Lett. 280 (1991) 321-324
38. Solomon E.I., Szilagyi R.K., DeBeer George S., and Basumallick L. Electronic structures of metal sites in proteins and models: contributions to function in blue copper proteins. Chem. Rev. 104 (2004) 419-458
39. Kaim W., and Schwederski B. Biological Chemistry: Inorganic Elements in the Chemistry of Life - An Introduction and Guide (1994), John-Wiley and Sons 187-214
40. Proshlyakov D.A., Pressler M.A., DeMaso C., Leykam J.F., DeWitt D.L., and Babcock G.T. Oxygen activation and reduction in respiration: involvement of redox-active tyrosine 244. Science 290 (2000) 1588-1591
41. McCauley K.M., Vrtis J.M., Dupont J., and van der Donk W.A. Insights into the functional role of the tyrosine-histidine linkage in cytochrome c oxidase. J. Am. Chem. Soc. 122 (2000) 2403-2404
42. Bu Y., and Cukier R.I. Structural character and energetics of tyrosyl radical formation by electron/proton transfers of a covalently linked histidine-tyrosine: a model for cytochrome C oxidase. J. Phys. Chem. B 109 (2005) 22013-22026
43. Daskalakis V., Pinakoulaki E., Stavrakis S., and Varotsis C. Probing the environment of cu(b) in heme-copper oxidases. J. Phys. Chem. B 111 (2007) 10502-10509
44. Hohenberg P., and Kohn W. Inhomogeneous electron gas. Phys. Rev. 136 (1964) B864-B871
45. Kohn W., and Sham L.J. Self-consistent equations including exchange and correlation effects. Phys. Rev. 140 (1965) A1133-A1138
46. Siegbahn P.E.M. The performance of hybrid DFT for mechanisms involving transition metal complexes in enzymes. J. Biol. Inorg. Chem. 11 (2006) 695-701
47. Harris D., Loew G., and Waskell L. Structure and spectra of ferrous dioxygen and reduced ferrous dioxygen model cytochrome P450. J. Am. Chem. Soc. 120 (1998) 4308-4318
48. Siegbahn P.E.M., and Blomberg M.R.A. Transition-metal systems in biochemistry studied by high-accuracy quantum chemical methods. Chem. Rev. 100 (2000) 421-437
49. Ghosh A., Vangberg T., Gonzales E., and Taylor P. Molecular structures and electron distributions of higher-valent iron and manganese porphyrins. Density functional theory calculations and some preliminary open-shell coupled-cluster results. J. Porphyrins Phthalocyanines 5 (2001) 345-356
50. Johansson M.P., Blomberg M.R.A., Sundholm D., and Wikström M. Change in electron and spin density upon electron transfer to haem. Biochim. Biophys. Acta 1553 (2002) 183-187
51. Johansson M.P., Sundholm D., Gerfen G., and Wikström M. The spin distribution in low-spin iron porphyrins. J. Am. Chem. Soc. 124 (2002) 11771-11790
52. Johansson M.P., and Sundholm D. Spin and charge distribution in iron porphyrin models: a coupled cluster and density-functional study. J. Chem. Phys. 120 (2004) 3229-3236
53. Siegbahn P.E.M., and Borowski T. Modeling enzymatic reactions involving transition metals. Acc. Chem. Res. 39 (2006) 729-738
54. Becke A.D. Density-functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 98 (1993) 5648-5652
55. Lee C., Yang W., and Parr R.G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B 37 (1988) 785-789
56. Curtiss L.A., Raghavachari K., Redfern R.C., and Pople J.A. Assessment of Gaussian-3 and density functional theories for a larger experimental test set. J. Chem. Phys. 112 (2000) 7374-7383
57. Siegbahn P.E.M., and Blomberg M.R.A. Density functional theory of biologically relevant metal centers. Annu. Rev. Phys. Chem. 50 (1999) 221-249
58. Jensen K.P., and Ryde U. Theoretical prediction of the Co-C bond strength in cobalamins. J. Phys. Chem. B 107 (2003) 7539-7545
59. Ryde U., and Nilsson K. Quantum chemistry can locally improve protein crystal structures. J. Am. Chem. Soc. 125 (2003) 14232-14233
60. Jensen K.P., Roos B.O., and Ryde U. Performance of density functionals for first row transition metal systems. J. Chem. Phys. 126 (2007) 014103-1-14
61. Neese F. A critical evaluation of DFT, including time-dependent DFT, applied to bioinorganic chemistry. J. Biol. Inorg. Chem. 11 (2006) 702-711
62. Ghosh A. Transition metal spin state energetics and noninnocent systems: challenges for DFT in the bioinorganic arena. J. Biol. Inorg. Chem. 11 (2006) 712-724
63. Tsukihara T., Shimokata K., Katayama Y., Shimada H., Muramoto K., Aoyoma H., Mochizuki M., Shinzawa-Itoh K., Yamashita E., Yao M., Ishimura Y., and Yoshikawa S. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc.Natl. Acad. Sci. U. S. A. 100 (2003) 15304-15309
64. Johansson M.P., Kaila V.R.I., and Laakkonen L. Charge parameterization of the metal centers in cytochrome c oxidase. J. Comp. Chem. 29 (2008) 753-767
65. Schäfer A., Horn H., and Ahlrichs R. Fully optimized contracted Gaussian basis sets for atoms Li to Kr. J. Chem. Phys. 97 (1992) 2571-2577
66. Schäfer A., Huber C., and Ahlrichs R. Fully optimized contracted Gaussian basis sets of triple zeta valence quality for atoms Li to Kr. J. Chem. Phys. 100 (1994) 5829-5835
67. Klamt A., and Schüürmann G. COSMO: a new approach to dielectric screening in solvents with explicit expressions for the screening energy and its gradient. J. Chem. Soc. Perkin Trans. 2 (1993) 799-805
68. Gorbikova E.A., Vuorilehto K., Wikström M., and Verkhovsky M.I. Redox titration of all electron carriers of cytochrome c oxidase by Fourier transform infrared spectroscopy. Biochemistry 45 (2006) 5641-5649
69. +. J. Phys. Chem. A 108 (2004) 3692-3694
70. Ahlrichs R., Bär M., Häser M., Horn H., and Kölmel C. Electronic-structure calculations on workstation computers - the program system Turbomole. Chem. Phys. Lett. 162 (1989) 165-169
71. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Molec. Graphics 14 (1996) 33-38
72. Laaksonen L. A graphics program for the analysis and display of molecular dynamics trajectories. J. Mol. Graphics 10 (1992) 33-34
73. Bergman D.L., Laaksonen L., and Laaksonen A.J. Visualization of solvation structures in liquid mixtures. J. Mol. Graphics and Modelling 15 (1997) 301-306
74. Qin L., Hiser C., Mulichak A., Garavito R.M., and Ferguson-Miller S. 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 (2006) 16117-16122
75. v fragment. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10547-10553
76. Soulimane T., Buse G., Bourenkov G.P., Bartunik H.D., Huber R., and Than M.E. Structure and mechanism of the aberrant ba(3)-cytochrome c oxidase from Thermus thermophilus. EMBO J. 19 (2000) 1766-1776
77. C.E. Housecroft, A.G. Sharpe, Inorganic Chemistry 2005, 2nd ed., ISBN 0130-39913-2.
78. 3 from Escherichia coli. Is chloride ion a cofactor?. Biochemistry 38 (1999) 7185-7194
79. Remenyi C., Reviakine R., and Kaupp M. Density functional study of EPR parameters and spin-density distribution of azurin and other blue copper proteins. J. Phys. Chem. B 111 (2007) 8290-8304
80. Blomberg M.R.A., Siegbahn P.E.M., and Wikström M. Metal-bridging mechanism for O-O bond cleavage in cytochrome C oxidase. Inorg. Chem. 42 (2003) 5231-5243
81. Lepp H., Svahn E., Faxén K., and Brzezinski P. Charge transfer in the K proton pathway linked to electron transfer to the catalytic site in cytochrome c oxidase. Biochemistry 47 (2008) 4929-4935
82. Verkhovsky M.I., Jasaitis A., Verkhovskaya M.L., Morgan J.E., and Wikström M. Proton translocation by cytochrome c oxidase. Nature 400 (1999) 480-483
83. Bloch D., Belevich I., Jasaitis A., Ribacka C., Puustinen A., Verkhovsky M.I., and Wikström M. The catalytic cycle of cytochrome c oxidase is not the sum of its two halves. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 529-533
84. Jancura D., Berka V., Antalik M., Bagelova J., Gennis R.B., Palmer G., and Fabian M. Spectral and kinetic equivalence of oxidized cytochrome C oxidase as isolated and "activated" by reoxidation. J. Biol. Chem. 281 (2006) 30319-30325