Water chain formation and possible proton pumping routes in Rhodobacter sphaeroides cytochrome c oxidase: A molecular dynamics comparison of the wild type and R481K mutant

Biochemistry

Volumn 44, Issue 31, 2005, Pages 10475-10485

  Seibold, Steve A ^a   Mills, Denise A ^b   Ferguson Miller, Shelagh ^b   Cukier, Robert I ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; COMPUTER SIMULATION; HYDROGEN BONDS; MOLECULAR DYNAMICS; MUTAGENESIS; OXYGEN; PROTONS; REDOX REACTIONS; WATER;

CYTOCHROME C OXIDASE (CCO); MOLECULAR DYNAMICS (MD) SIMULATIONS; WATER CHAIN FORMATION;

ENZYMES;

ADENOSINE TRIPHOSPHATE; ARGININE; CYTOCHROME C OXIDASE; HEME DERIVATIVE; HISTIDINE; LYSINE; MAGNESIUM ION; PROPIONIC ACID DERIVATIVE; PROTON PUMP; WATER;

ALGORITHM; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; ELECTRON TRANSPORT; ENERGY CONVERSION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STRUCTURE; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; OXIDATION REDUCTION REACTION; PKA; PRIORITY JOURNAL; PROTON TRANSPORT; RHODOBACTER SPHAEROIDES; X RAY CRYSTALLOGRAPHY;

ARGININE; COMPUTER SIMULATION; ELECTRON TRANSPORT COMPLEX IV; GLUTAMIC ACID; HEME; HYDROGEN BONDING; LYSINE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROPIONIC ACIDS; PROTEIN STRUCTURE, SECONDARY; PROTON PUMPS; RHODOBACTER SPHAEROIDES; THERMODYNAMICS; WATER;

RHODOBACTER SPHAEROIDES;

EID: 23244450116     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0502902     Document Type: Article

References (52)

1. Qian, J., Mills, D. A., Geren, L., Wang, K. F., Hoganson, C. W., Schmidt, B., Hiser, C., Babcock, G. T., Durham, B., Millett, F., and Ferguson-Miller, S. (2004) Role of the conserved arginine pair in proton and electron transfer in cytochrome c oxidase, Biochemistry 43, 5748-5756.
2. Voet, D., and Voet, J. G. (1990) Biochemistry, John Wiley & Sons, New York.
3. Cukier, R. I. (2004) Quantum molecular dynamics simulation of proton transfer in cytochrome c oxidase, Biochim. Biophys. Acta 1656, 189-202.
4. Cukier, R. I. (2004) Theory and simulation of proton-coupled electron transfer, hydrogen-atom transfer, and proton translocation in proteins, Biochim. Biophys. Acta 1655, 37-44.
5. Mills, D. A., and Ferguson-Miller, S. (2003) Understanding the mechanism of proton movement linked to oxygen reduction in cytochrome c oxidase: Lessons from other proteins, FEBS Lett. 545, 47-51.
6. Zaslavsky, D., and Gennis, R. B. (2000) Proton pumping by cytochrome oxidase: Progress, problems and postulates, Biochim. Biophys. Acta 1458, 164-179.
7. Mitchell, R., and Rich, P. R. (1994) Proton Uptake by Cytochrome-C-Oxidase on Reduction and on Ligand-Binding, Biochim. Biophys. Acta 1186, 19-26.
8. Artzatbanov, V. Y., Konstantinov, A., and Skulachev, V. (1978) Involvement of intramitochondrial protons in redox reactions of cytochrome a, FEBS Lett. 87, 180-185.
9. Capitanio, N., Capitanio, G., Minuto, M., De Nitto, E., Palese, L. L., Nicholls, P., and Papa, S. (2000) Coupling of electron transfer with proton transfer at heme a and Cu(A) (redox Bohr effects) in cytochrome c oxidase. Studies with the carbon monoxide inhibited enzyme, Biochemistry 39, 6373-6379.
10. Michel, H. (1999) Cytochrome c Oxidase: Catalytic Cycle and Mechanisms of Proton Pumping-A Discussion, Biochemistry 38, 15129-15140.
11. Konstantinov, A. A., Siletsky, S., Mitchell, D., Kaulen, A., and Gennis, R. (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. U.S.A. 94, 9085-9090.
12. Branden, M., Sigurdson, H., Namslauer, A., Gennis, R., Adelroth, P., and Brzezinski, P. (2001) On the role of the K-proton-transfer pathway in cytochrome c oxidase, Proc. Natl. Acad. Sci. U.S.A. 98, 5013-5018.
13. Adelroth, P., Ek, M. S., Mitchell, D. M., Gennis, R. B., and Brzezinski, P. (1997) Glutamate 286 in cytochrome aa3 from Rhodobacter sphaeroides is involved in proton uptake during the reaction of the fully-reduced enzyme with dioxygen, Biochemistry 36, 13824-13829.
14. Svensson-Ek, M., Abramson, J., Larsson, G., Tornoth, S., Brzezinski, P., and Iwata, S. (2002) The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides, J. Mol. Biol. 321, 329-339.
15. Behr, J., Michel, H., Mäntele, W., and Hellwig, P. (2000) Functional Properties of the Heme Propionates in Cytochrome c Oxidase from Paracoccus denitrificans. Evidence from FTIR Difference Spectroscopy and Site-Directed Mutagenesis, Biochemistry 39, 1356-1363.
16. Puustinen, A., and Wikstrom, M. (1999) Proton exit from the heme-copper oxidase of Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 96, 35-37.
17. Nagle, J. F., and Tristam-Nagle, S. (1983) Hydrogen Bonded Chain Mechanisms for Proton Conduction and Proton Pumping, J. Membr. Biol. 74, 1-14.
18. Agmon, N. (1995) The Grotthuss Mechanism, Chem. Phys. Lett. 244, 456-462.
19. Iwata, S., Ostermeier, C., Ludwig, B., and Michel, H. (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans, Nature 376, 660-669.
20. + conduction along hydrogen-bonded chains of water molecules, Biophys. J. 75, 33-40.
21. Stuchebrukhov, A. A. (2003) Electron-transfer reactions coupled to proton translocation. Cytochrome oxidase, proton pumps, and biological energy transduction, J. Theor. Comput. Chem. 2, 91-118.
22. Wikstrom, M., Verkhovsky, M. I., and Hummer, G. (2003) Water-gated mechanism of proton translocation by cytochrome c oxidase, Biochim. Biophys. Acta 1604, 61-65.
23. Pomes, R., Hummer, G., and Wikstrom, M. (1998) Structure and dynamics of a proton shuttle in cytochrome c oxidase, Biochim. Biophys. Acta 1365, 255-260.
24. Zheng, X., Medvedev, D. M., Swanson, J., and Stuchebrukhov, A. A. (2003) Computer simulation of water in cytochrome c oxidase, Biochim. Biophys. Acta 1557, 99-107.
25. 13C labeling, Biochemistry 37, 7400-7406.
26. Behr, J., Michel, H., Mantele, W., and Hellwig, P. (2000) Functional properties of the heme propionates in cytochrome c oxidase from Paracoccus denitrificans. Evidence from FTIR difference spectroscopy and site-directed mutagenesis, Biochemistry 39, 1356-1363.
27. Yoshikawa, S. (2003) A cytochrome c oxidase proton pumping mechanism that excludes the O2 reduction site, FEBS Lett. 555, 8-12.
28. Ostermeier, C., Harrenga, A., Ermler, U., and Michel, H. (1997) Structure at 2.7 Å 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.
29. Cukier, R. I., and Seibold, S. A. (2002) Molecular Dynamics Simulations of Prostaglandin Endoperoxide II Synthase-1: Role of Water and the Mechanism of Compound I Formation from Hydrogen Peroxide, J. Phys. Chem. B 106, 12031-12044.
30. van Gunsteren, W. F., and Berendsen, H. J. C. (1987) GROMOS Manual, University of Groningen: Groningen.
31. Hockney, R. W., and Eastwood, J. W. (1981) Computer simulation using particles, McGraw-Hill, New York.
32. Allen, M. P., and Tildesley, D. J. (1987) Computer Simulation of Liquids, Clarendon Press, Oxford, U.K.
33. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical-Integration of Cartesian Equations of Motion of a System with Constraints: Molecular-Dynamics of N-Alkanes, J. Comput. Phys. 23, 327-341.
34. Berendsen, H. H. C., Postma, J. P. M., Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath, J. Chem. Phys. 81, 3684-3690.
35. Ferguson-Miller, S. (2003) Coordinates.
36. MOE (2003) Chemical Computing Co., Montreal, PQ.
37. MacKerell, A. D., Brooks, B. R., Brooks, C. L., III, Nilsson, L., Rous, B., Won, Y., and Karplus, M. (1998) The Encyclopedia of Computational Chemistry, Vol. 1, p 271, John Wiley & Sons, Chichester, U.K.
38. Hofacker, I., and Schulten, K. (1998) Oxygen and proton pathways in cytochrome c oxidase, Proteins 30, 100-107.
39. Solomon, E. I., Sundaram, U. M., and Machonkin, T. E. (1996) Multicopper Oxidases and Oxygenases, Chem. Rev. 96, 2563-2605.
40. Jasaitis, A., Backgren, C., Morgan, J., Puustinen, A., Verkhovsky, M. I., and Wikstrom, M. (2001) Electron and proton transfer in the arginine-54-wethionine mutant of cytochrome c oxidase from Paracoccus denitrificans, Biochemistry 40, 5269-5274.
41. 3 from Paracoccus denitrificans, Biochim. Biophys. Acta 1456, 1-4.
42. 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. (2003) 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, 15304-15309.
43. 1 complex, Science 281, 64-71.
44. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., and Yoshikawa, S. (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å, Science 272, 1136-1144.
45. 3 from Rhodobacter sphaeroides is Involved in Proton Uptake During the Reaction of the Fully-Reduced Enzyme with Dioxygen, Biochemistry 36, 13824-13829.
46. Adelroth, P., Karpefors, M., Gilderson, G., Tomson, F. L., Gennis, R., and Brzezinski, P. (2000) Proton transfer from glutamate 286 determines the transition rates between oxygen intermediates in cytochrome c oxidase, Biochim. Biophys. Acta 1459, 533-539.
47. Mills, D. A., and Ferguson-Miller, S. (2002) Influence of structure, pH and membrane potential on proton movement in cytochrome c oxidase, Biochim. Biophys. Acta 1555, 96-100.
48. Lanyi, J. K., and Luecke, H. (2001) Bacteriorhodopsin, Curr. Opin. Struct. Biol. 11, 415-419.
49. Hellwig, P., Rost, B., Kaiser, U., Ostermeier, C., Michel, H., and Mantele, W. (1996) Carboxyl group protonation upon reduction of the Paracoccus denitrificans cytochrome c oxidase: Direct evidence by FTIR, FEBS Lett. 385, 53-57.
50. Hellwig, P., Gryzbek, S., Behr, J., Ludwig, B., Michel, H., and Mantele, W. (1999) Electrochemical and ultraviolet/visible/infrared spectroscopic analysis of heme a and a3 redox reactions in the cytochrome c oxidase from Paracoccus denitrificans: Separation of heme a and a3 contributions and assignment of vibrational modes, Biochemistry 38, 1685-1694.
51. 1 Complex, Biophys. J. 77, 1753-1768.
52. Florens, L., Schmidt, B., McCracken, J., and Ferguson-Miller, S. (2001) Fast deuterium access to the buried magnesium/manganese site in cytochrome c oxidase, Biochemistry 40, 7491-7497.