Natural engineering principles of electron tunnelling in biological oxidation-reduction

Nature

Volumn 402, Issue 6757, 1999, Pages 47-52

  Page, Christopher C ^a   Moser, Christopher C ^a   Chen, Xiaoxi ^a   Dutton, P Leslie ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXIDOREDUCTASE; PROTEIN;

ARTICLE; BIOENGINEERING; CALCULATION; ELECTRON TRANSPORT; EVOLUTION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; TRANSPORT KINETICS;

CATALYSIS; ELECTROCHEMISTRY; ELECTRONS; EVOLUTION; MODELS, BIOLOGICAL; MODELS, CHEMICAL; OXIDATION-REDUCTION; OXIDOREDUCTASES;

EID: 0033523919     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/46972     Document Type: Article

References (50)

1. Michaelis, L. in The Enzymes, Chemistry and Mechanism of Action (eds Sumner, J. B. & Myrback, K.) 1-54 (Academic, New York, 1951).
2. Devault, D. Quantum mechanical tunnelling in biological systems. Quart. Rev. Biophys. 13, 387-564 (1980).
3. Marcus, R. A. & Sutin, N. Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811, 265-322 (1985).
4. Jortner, J. Temperature dependent activation energy for electron transfer between biological molecules. J. Chem. Phys. 64, 4860-4867 (1976).
5. Hopfield, J. J. Electron transfer between biological molecules by thermally activated tunneling. Proc. Natl Acad. Sci. USA 71, 3640-3644 (1974).
6. Moser, C. C., Keske, J. M., Warncke, K., Farid, R. S. & Dutton, P. L. Nature of biological electron-transfer. Nature 355, 796-802 (1992).
7. Smalley, J. F. et al. The kinetics of electron-transfer through ferrocene-terminated alkanethiol monolayers on gold. J. Phys. Chem. 99, 13141-13149 (1995).
8. Beratan, D. N., Onuchic, J. N., Winkler, J. R. & Gray, H. B. Electron-tunneling pathways in proteins. Science 258, 1740-1741 (1992).
9. Moser, C. C. & Dutton, P. L. Engineering protein structure for electron transfer function in photosynthetic reaction centers. Biochim. Biophys. Acta 1101, 171-176 (1992).
10. A. J. Am. Chem. Soc. 111, 3400-3412 (1989).
11. 2 to the photosynthetic reaction center of the purple bacterium Rhodobacter sphaeroides. Biophys. J. 74, 3226-3240 (1998).
12. Kuki, A. & Wolynes, P. G. Electron tunneling paths in proteins. Science 236, 1647-1652 (1987).
13. Kisker, C. et al. Molecular basis of sulfite oxidase deficiency from the structure of sulfite oxidase. Cell 91, 973-983 (1997).
14. 4 centre. J. Biol. Inorg. Chem. 2, 680-689 (1997).
15. Dutton, P. L. et al. in Biological Electron Transfer Chains: Genetics, Composition and Mode of Operation 3-8 (Kluwer Academic, Netherlands, 1998).
16. Gunner, M. R., Tiede, D. M., Prince, R. C. & Dutton, P. in Function of Quinones in Energy Conserving Systems (ed Trumpower, B. L.) 265-269 (Academic, New York, 1982).
17. Woodbury, N. W., Parson, W. W., Gunner, M. R., Prince, R. C. & Dutton, P. L. Radical-pair energetics and decay mechanisms in reaction centers containing anthraquinones, napthoquinones or benzoquinones in place of ubiquinone. Biochim. Biophys. Acta 851, 6-22 (1986).
18. Volbeda, A. et al. Crystal-structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373, 580-587 (1995).
19. Rousset, M. et al. [3Fe-4S] to [4Fe-4S] cluster conversion in Desulfovibrio fructosovorans [NiFe] hydrogenase by site-directed mutagenesis. Proc. Natl Acad. Sci. USA 95, 11625-11630 (1998).
20. Michel, H., Deisenhofer, J. & Epp, O. Pigment protein interactions in the photosynthetic reaction center from Rhodopseudomonas viridis. EMBO J. 5, 2445-2451 (1986).
21. 2 with photosynthetic reaction centers from Rhodopseudomonas viridis. Biochemistry 30, 1303-13010 (1991).
22. Shopes, R. J., Holten, D., Levine, L. M. A. & Wraight, C. A. Kinetics of oxidation of the bound cytochromes in reaction centers from Rhodopseudomonas viridis. Photosynth. Res. 12, 165-180 (1987).
23. Dohse, B. et al. Electron-transfer from the tetraheme cytochrome to the special pair in the Rhodopseudomonas viridis reaction-center - effect of mutations of tyrosine L162. Biochemistry 34, 11335-11343 (1995).
24. Meyer, T. E., Bartsch, R. G., Cusanovich, M. A. & Tollin, G. Kinetics of photooxidation of soluble cytochromes, hipip, and azurin by the photosynthetic reaction center of the purple phototrophic bacterium Rhodopseudomonas viridis. Biochemistry 32, 4719-4726 (1993).
25. 2 and the tetraheme cytochrome c in Rhodopseudomonas viridis. Photosyn. Res. 59, 147-157 (1999).
26. Proshlyakov, D. A., Pressler, M. A. & Babcock, G. T. Dioxygen activation and bond cleavage by mixed-valence cytochrome c oxidase. Proc. Natl Acad. Sci. USA 95, 8020-8025 (1998).
27. Stubbe, J. & van der Donk, W. A. Protein radicals in enzyme catalysis. Chem. Rev. 98, 705-762 (1998).
28. Hunt, J., Massey, V., Dunham, W. R. & Sands, R. H. Redox potentials of milk xanthine dehydrogenase - room-temperature measurement of the FAD and 2Fe/2S center potentials. J. Biol. Chem. 268, 18685-18691 (1993).
29. Farrington, J. A., Land, E. J. & Swallow, A. J. The one-electron reduction potentials of NAD. Biochim. Biophys. Acta 590, 273-276 (1980).
30. Romao, M. J. et al. Crystal-structure of the xanthine oxidase-related aldehyde oxidoreductase from D. gigas. Science 270, 1170-1176 (1995).
31. Huber, R. et al. A structure-based catalytic mechanism for the xanthine oxidase family of molybdenum enzymes. Proc. Natl Acad. Sci. USA 93, 8846-8851 (1996).
32. Powell, M. F., Wu, J. C. & Bruice, T. C. Ferricyanide oxidation of dihydropyridines and analogues. J. Am. Chem. Soc. 106, 3850-3856 (1984).
33. Eberson, L. Electron Transfer Reactions in Organic Chemistry 1-234 (Springer, New York, 1987).
34. Pross, A. The single electron shift as a fundamental process in organic chemistry: the relationship between polar and electron-transfer pathways. Acc. Chem. Res. 18, 212-219 (1985).
35. Gray, H. B. & Winkler J. R. Electron transfer in proteins. Annu. Rev. Biochem. 65, 537-561 (1996).
36. McLendon, G. Control of biological electron-transport via molecular recognition and binding - the velcro model. Struct. Bond. 75, 159-174 (1991).
37. Darwin, C. Origin of Species by Means of Natural Selection (Earlton House, New York, 1872).
38. Jortner, J., Bixon, M., Langenbacher, T. & Michel-Beyerle, M. E. Charge transfer and transport in DNA. Proc. Natl Acad. Sci. USA 95, 12759-12765 (1998).
39. Siegbahn, P. E. M., Blomberg, M. R. A. & Crabtree, R. H. Hydrogen transfer in the presence of amino acid radicals. Theor. Chem. Acc. 97, 289-300 (1997).
40. Ehrenberg, A. Protein dynamics, free radical transfer and reaction cycle of ribonucleotide reductase. Third International Symposium on Biological Physics 1, 1-10 (Springer, New York, 1998).
41. Mitchell, P. The protonmotive Q cycle: a general formulation. FEBS Lett. 59, 137-139 (1975).
42. Spee, J. H. et al. Redox properties and electron paramagnetic resonance spectroscopy of the transition state complex of Azotobacter vinelandii nitrogenase. FEBS Lett. 432, 55-58 (1998).
43. Siegbahn, P. E. M. Theoretical study of the substrate mechanism of ribonucleotide reductase. J. Am. Chem. Soc. 120, 8417-8439 (1998).
44. Bahnson, B. J., Colby, T. D., Chin, J. K., Goldstein, B. M. & Klinman, J. P. A link between protein structure and enzyme catalyzed hydrogen tunneling. Proc. Natl Acad. Sci. USA 94, 12797-12802 (1997).
45. Zinth, W., Arlt, T. & Wachtveitl, J. The primary processes of bacterial photosynthesis - ultrafast reactions for the optimum use of light energy. Ber. Bunsenges Phys. Chem. 100, 1962-1966 (1996).
46. Allen, J. P. et al. Free energy dependence of the direct charge recombination from the primary and secondary quinones in reaction centers from Rhodobacter sphaeroides. Photosyn. Res. 55, 227-233 (1998).
47. B- and the associated processes in Rhodobacter sphaeroides R-26 reaction centers. Biochemistry 37, 2818-2829 (1998).
48. 2 from Rhodopseudomonas viridis at 3.0 Å resolution. Photosyn. Res. 34, 154-154 (1992).
49. Alegria, G. & Dutton, P. L. Langmuir-Blodgett monolayer films of bacterial photosynthetic membranes and isolated reaction centers: preparation, spectrophotometric and electrochemical characterization. I. Biochim. Biophys. Acta 1057, 239-257 (1991).
50. Teixeira, M. et al. Redox intermediates of Desulfovibrio gigas [NiFe] hydrogenase generated under hydrogen. Mossbauer and EPR characterization of the metal centers. J. Biol. Chem. 264, 16435-16450 (1989).