Theory and simulation of proton-coupled electron transfer, hydrogen-atom transfer, and proton translocation in proteins

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1655, Issue 1-3, 2004, Pages 37-44

  Cukier, R I ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Cytcohrome c oxidase; Photosystem II oxygen evolving complex; Proton and electron transfer; Proton translocation

Indexed keywords

CYTOCHROME C OXIDASE; GLUTAMIC ACID; HYDROGEN; PROTEIN; PROTON; WATER;

ELECTRON TRANSPORT; HYDROGEN BOND; MOLECULAR DYNAMICS; PARTICLE SIZE; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN TRANSPORT; PROTON TRANSPORT; QUANTUM MECHANICS; REVIEW; THEORY;

ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; HYDROGEN; HYDROGEN BONDING; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PHOTOSYSTEM II PROTEIN COMPLEX; PROTON-MOTIVE FORCE; THERMODYNAMICS;

EID: 1942504857     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2003.06.011     Document Type: Review

References (56)

1. Tommos C., Babcock G.T. Proton and hydrogen currents in photosynthetic water oxidation. Biochim. Biophys. Acta. 1458:2000;199-219.
2. Ferguson-Miller S., Babcock G.T. Heme/copper terminal oxidases. Chem. Rev. 96:1996;2889-2908.
3. Westphal K.L., Tommos C., Cukier R.I., Babcock G.T. Concerted hydrogen-atom abstraction in photosynthetic water oxidation. Curr. Opin. Plant Biol. 3:2000;236-242.
4. ··in PSII membranes - evidence for concerted hydrogen-atom transfer in oxygen evolution. Biochemistry. 39:2000;16220-16229.
5. Cukier R., Nocera D. Proton-coupled electron transfer. Annu. Rev. Phys. Chem. 49:1998;337-369.
6. Cukier R.I. Wheeler R.A. Bioenergetics Simulations of Electron, Proton, and Energy Transfer, American Chemical Society Symposium Series. 2003;194.
7. Hoganson C.W., Babcock G.T. A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science. 277:1997;1953-1956.
8. Tommos C., Babcock G.T. Oxygen production in nature: a light-driven metalloradical enzyme process. Acc. Chem. Res. 31:1998;18-25.
9. +) nanosecond reduction kinetics in single flashes as a function of pH. Biochim. Biophys. Acta. 974:1989;36-43.
10. Z in photosystem II from multiple electron magnetic-resonance spectroscopies: implications for photosynthetic oxygen evolution. J. Am. Chem. Soc. 117:1995;10325-10335.
11. Chu H.-A., Nguyen A.P., Debus R. Amino acid residues that influence the binding of manganese or calcium to photosystem II: 1. The lumenal interhelical domains of the D1 polypeptide. Biochemistry. 34:1995;5839-5858.
12. Yocum C.F., Pecoraro V.L. Recent advances in the understanding of the biological chemistry of manganese. Curr. Opin. Struct. Biol. 3:1999;182-187.
13. Barber J., Kuhlbrandt W. Photosystem II. Curr. Opin. Struct. Biol. 9:1999;469-475.
14. Ulstrup J. Charge Transfer Processes in Condensed Media. 1979;Springer, Berlin.
15. Fain B. Lecture Notes in Chemistry: Theory of Rate Processes in Condensed Media. 1980;Springer-Verlag, Berlin/Heidelberg.
16. Krishtalik L.I. Charge Transfer Reactions in Electrochemical and Chemical Processes. 1979;Plenum, New York.
17. Cukier R.I. A theory that connects proton-coupled electron-transfer and hydrogen-atom transfer reactions. J. Phys. Chem., B. 106:2002;1746-1757.
18. Levich V.G., Dogonadze R.R., German E.D., Kuznetsov A.M., Kharkats Y.I. Theory of homogeneous reactions involving proton transfer. Electrochim. Acta. 15:1970;353-367.
19. Kuznetsov A.M., Ulstrup J. Proton and hydrogen atom tunnelling in hydrolytic and redox enzyme catalysis. Can. J. Chem. 77:1999;1085-1096.
20. Borgis D., Staib A. Quantum adiabatic umbrella sampling: the excited state free energy surface of an electron-atom pair in solution. J. Chem. Phys. 104:1996;4776-4783.
21. Cukier R.I., Zhu J. Simulation of proton transfer reaction rates: the role of solvent electronic polarization. J. Phys. Chem. 101:1997;7180-7190.
22. Decornez H., Hammes-Schiffer S. Model proton-coupled electron transfer reactions in solution: predictions of rates, mechanisms, and kinetic isotope effects. J. Phys. Chem., A. 104:2000;9370-9384.
23. Iordanova N., Decornez H., Hammes-Schiffer S. Theoretical study of electron, proton, and proton-coupled electron transfer in iron bi-imidazoline complexes. J. Am. Chem. Soc. 123:2001;3723-3733.
24. Georgievskii Y., Stuchebrukhov A.A. Concerted electron and proton transfer: transition from nonadiabatic to adiabatic proton tunneling. J. Chem. Phys. 113:2000;10438-10450.
25. Nikitin E.E., Umanskii S.Y. Theory of Slow Atomic Collisions. 1984;Springer-Verlag, Berlin.
26. Bell R.P. The Tunnel Effect in Chemistry. 1980;Chapman & Hall, London.
27. Tommos C., Hoganson C.W., DiValentin M., Lydakis-Simantiris N., Dorlet P., Westphal K., Chu H.-A., McCracken J., Babcock G.T. Manganese and tyrosyl radical function in photosynthetic oxygen evolution. Curr. Opin. Chem. Biol. 2:1998;244-252.
28. Karge M., Irrgang K.D., Renger G. Analysis of the reaction coordinate of photosynthetic water oxidation by kinetic measurements of 355 nm absorption changes at different temperatures in Photosystem II preparations suspended in either H2O or D2O. Biochemistry. 36:1997;8904-8913.
29. ··with its environment in acetate-treated Photosystem II membranes and reaction center cores. J. Phys. Chem., B. 102:1998;8239-8247.
30. Peloquin J.M., Campbell K.A., Britt R.D. 55Mn pulsed ENDOR demonstrates that the Photsystem II "split" EPR signal arises from a magnetically-coupled mangano-tyrosyl complex. J. Am. Chem. Soc. 120:1998;6840-6841.
31. Lakshmi K.V., Eaton S.S., Eaton G.R., Frank H.A., Brudvig G.W. Analysis of dipolar and exchange interactions between manganese and tyrosine Z in the S2YZ state of acetate-inhibited Photosystem II via EPR spectral simulations at X- and Q-bands. J. Phys. Chem., B. 102:1998;8327-8335.
32. Zouni A., Witt H.T., Kern J., Fromme P., Krauss N., Saenger W., Orth P. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 angstrom resolution. Nature. 409:2001;739-743.
33. Kamiya N., Shen J.R. Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-angstrom resolution. Proc. Natl. Acad. Sci. U. S. A. 100:2003;98-103.
34. Blomberg M.R.A., Siegbahn P.E.M., Styring S., Babcock G.T., Åkermark B., Korall P. A quantum chemical study of hydrogen abstraction from manganese coordinated water by a tyrosyl radical: a model for water oxidation in Photosystem II. J. Am. Chem. Soc. 119:1997;8285-8292.
35. Nagle J.F., Tristam-Nagle S. Hydrogen bonded chain mechanisms for proton conduction and proton pumping. J. Membr. Biol. 74:1983;1-14.
36. Selloni A., Carnevali P., Car R., Parrinello M. Localization, hopping, and diffusion of electrons in molten salts. Phys. Rev. Lett. 59:1987;823-826.
37. Barnett R.N., Landman U., Nitzan A. Dynamics and spectra of a solvated electron in water clusters. J. Chem. Phys. 89:1988;2242-2256.
38. Rossky P.J., Schnitker J. The hydrated electron: quantum simulation of structure, spectroscopy, and dynamics. J. Phys. Chem. 92:1988;4277-4285.
39. Zhu J., Cukier R.I. A quantum molecular dynamics simulation of an excess electron in methanol. J. Chem. Phys. 98:1993;5679-5693.
40. Cukier R.I., Seibold S.A. 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. 106:2002;12031-12044.
41. van Gunsteren W.F., Berendsen H.J.C. GROMOS Manual. 1987;Groningen University, Groningen.
42. S. Ferguson-Miller (2003). Coordinates kindly provided by Professor S. Ferguson-Miller.
43. Svensson-Ek M., Abramson J., Larsson G., Tornroth S., Brzezinski P., Iwata S. The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J. Mol. Biol. 321:2002;329-339.
44. 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., Tsukihara T. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science. 280:1998;1723-1729.
45. Iwata S., Ostermeier C., Ludwig B., Michel H. Structure at 2.8-angstrom resolution of Cytochrome-C-Oxidase from Paracoccus denitrificans. Nature. 376:1995;660-669.
46. Rost B., Behr J., Hellwig P., Richter O.M.H., Ludwig B., Michel H., Mantele W. Time-resolved FT-IR studies on the CO adduct of Paracoccus denitrificans cytochrome c oxidase: comparison of the fully reduced and the mixed valence form. Biochemistry. 38:1999;7565-7571.
47. 3 from Escherichia coli. Biochemistry. 36:1997;13195-13200.
48. 3 from Rhodobacter sphaeroides is involved in proton uptake during the reaction of the fully reduced enzyme with dioxygen. Biochemistry. 36:1997;13824-13829.
49. Meunier B., Ortwein C., Brandt U., Rich P.R. Effects of mutation of residue 167 on redox-liinked protonation processes in yeast cytochrome c oxidase. Biochem. J. 330:1998;1197-1200.
50. Junemann S., Meunier B., Fisher N., Rich P.R. Effects of mutation of the conserved glutamic acid-286 in subunit I of cytochrome c oxidase from Rhodobacter sphaeroides. Biochemistry. 38:1999;5248-5255.
51. Backgren C., Hummer G., Wikstrom M., Puustinen A. Proton translocation by cytochrome c oxidase can take place without the conserved glutamic acid in subunit I. Biochemistry. 39:2000;7863-7867.
52. Aagaard A., Gilderson G., Mills D.A., Ferguson-Miller S., Brzezinski P. Redesign of the proton-pumping machinery of cytochrome c oxidase: proton pumping does not require Glu(I-286). Biochemistry. 39:2000;15847-15850.
53. Adelroth P., Karpefors M., Gilderson G., Tomson F.L., Gennis R.B., Brzezinski P. Proton transfer from glutamate 286 determines the transition rates between oxygen intermediates in cytochrome c oxidase. Biochim. Biophys. Acta. 1459:2000;533-539.
54. Forsyth W.R., Antosiewiez J.M., Robertson A.D. Empirical relationships between protein structure and carboxyl pK(a) values in proteins. Proteins Struct. Funct. Genet. 48:2002;388-403.
55. Dwyer J.J., Gittis A.G., Karp D.A., Lattman E.E., Spencer D.S., Stites W.E., Garcia-Morena E B. High apparent dielectric constants in the interior of a protein reflect water penetration. Biophys. J. 79:2000;1610-1620.
56. Zheng X., Medvedev D.M., Swanson J., Stuchebrukhov A.A. Computer simulation of water in cytochrome c oxidase. Biochim. Biophys. Acta. 1557:2003;99-107.