Journal of Bioenergetics and Biomembranes

, Volume 27, Issue 3, pp 263–274 | Cite as

Biological electron transfer

  • Christopher C. Moser
  • Christopher C. Page
  • Ramy Farid
  • P. Leslie Dutton


Many oxidoreductases are constructed from (a) local sites of strongly coupled substrate-redox cofactor partners participating in exchange of electron pairs, (b) electron pair/single electron transducing redox centers, and (c) nonadiabatic, long-distance, single-electron tunneling between weakly coupled redox centers. The latter is the subject of an expanding experimental program that seeks to manipulate, test, and apply the parameters of theory. New results from the photosynthetic reaction center protein confirm that the electronic-tunneling medium appears relatively homogeneous, with any variances evident having no impact on function, and that control of intraprotein rates and directional specificity rests on a combination of distance, free energy, and reorganization energy. Interprotein electron transfer between cytochromec and the reaction center and in lactate dehydrogenase, a typical oxidoreductase from yeast, are examined. Rates of interprotein electron transfer appear to follow intraprotein guidelines with the added essential provision of binding forces to bring the cofactors of the reacting proteins into proximity.

Key words

Intra-protein and inter-protein electron transfer oxidoreductases enzyme mechanisms 


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  1. Allen, J. P., Feher, G., Yeates, T. O., Komiya, H., and Rees, D. C., (1987).Proc. Natl. Acad. Sci. USA 84, 5725–5729.PubMedGoogle Scholar
  2. Beitz, J. V., and Miller, J. R. (1979). InTunneling in Biological Systems (Chance, B., De Vault, D. C., Frauenfelder, H., Marcus, R. A., Schrieffer, J. R., and Sutin, N., eds.). Academic Press, New York.Google Scholar
  3. Beratan, D. N., Onuchic, J. N., Winkler, J. R., and Gray, H. B. (1992)Science 258, 1740–1741.PubMedGoogle Scholar
  4. Betts, J. N., Beratan, D. N., and Onuchic, J. N. (1992).J. Am. Chem. Soc. 114, 4043–4046.Google Scholar
  5. Casimiro, D. R., Richards, J. H., Winkler, J. R. and Gray, H. B. (1993a)J. Phys. Chem. 97, 13073–13077.Google Scholar
  6. Casimiro, D. R., Wong, L. L., Colon, J. L., Zewert, T. E., Richards, J. H., Chang, I. J., Winkler, J. R. and Gray, H. B. (1993b).J. Am. Chem. Soc. 115, 1485–1489.Google Scholar
  7. Cha, Y, Murray, C. J., and Klinman, J. P. (1989).Science 243, 1325–1330.PubMedGoogle Scholar
  8. Chang, C. H., Tiede, D., Tang, J., Smith, U., Norris, J., and Schiffer, M. (1986).FEBS Lett. 205, 82–6.PubMedGoogle Scholar
  9. Chapman, S. K., White, S. A., and Reid, G. A. (1991).Adv. Inorg. Chem. 36, 257–301.Google Scholar
  10. Chidsey, C. E. D., Kirmaier, C., Holten, D., and Boxer, S. G. (1985).Biochim. Biophys. Acta 766, 424–437.Google Scholar
  11. Devault, D. (1980).Q. Rev. Biophys. 13, 387–564.PubMedGoogle Scholar
  12. Devault, D., and Chance, B. (1966).Biophys. J. 6, 825–847.PubMedGoogle Scholar
  13. Dutton, P. L., and Moser, C. C. (1994).Proc. Natl. Acad. Sci. USA 91, 10247–10250.PubMedGoogle Scholar
  14. Edwards (1994).Biochemistry and Physiology of the Neutrophil, Cambridge University Press, Cambridge.Google Scholar
  15. Ermler, U., Fritzsch, G., Buchanan, S. K., and Michel, H. (1994).Structure 2, 925–936.PubMedGoogle Scholar
  16. Evenson, J. W., and Karplus, M. (1993).Science 262, 1247–1249.PubMedGoogle Scholar
  17. Farid, R. S., Moser, C. C., and Dutton, P. L. (1993).Curr. Opin. Struct. Biol. 3, 225–233.Google Scholar
  18. Farver, O., and Pecht, I. (1992).J. Am. Chem. Soc. 114, 5764–5767.Google Scholar
  19. Franzen, S., Goldstein, R. F., and Boxer, S. G. (1990).J. Phys. Chem. 94, 5135–5149.Google Scholar
  20. Friesner, R. A., and Monge, A. (1994).Structure 2, 339–43.PubMedGoogle Scholar
  21. Giangiacomo, K. M., and Dutton, P. L. (1989).Proc. Natl. Acad. Sci. USA 86, 2658–2662.PubMedGoogle Scholar
  22. Gruschus, J. M., and Kuki, A. (1993).J. Phys. Chem. 97, 5581–5593.Google Scholar
  23. Gunner, M. R., and Dutton, P. L. (1989).J. Am. Chem. Soc. 111, 3400–3412.Google Scholar
  24. Gunner, M. R., Robertson, D. E., and Dutton, P. L. (1986).J. Phys. Chem. 90, 3783–3795.Google Scholar
  25. Holten, D., Windsor, M. W., Parson, W. W., and Thornber, J. P. (1978).Biochim. Biophys. Acta 501, 112–126.PubMedGoogle Scholar
  26. Holzapfel, W., Finkele, U., Kaiser, W., Oesterhelt, D., Scheer, H., Stilz, H. U., and Zinth, W. (1990).Proc. Natl. Acad. Sci. USA 87, 5168–5172.PubMedGoogle Scholar
  27. Hopfield, J. J. (1974).Proc. Natl. Acad. Sci. USA 71, 3640–4.Google Scholar
  28. Jia, Y. W., Dimagno, T. J., Chan, C. K., Wang, Z. Y., Du, M., Hanson, D. K., Schiffer, M., Norris, J. R., Fleming, G. R., and Popov, M. S. (1993).J. Phys. Chem. 97, 13180–13191.Google Scholar
  29. Jortner, J. (1976).J. Chem. Phys. 64, 4860–4867.Google Scholar
  30. Karpishin, T. B., Grinstaff, M. W., Komarpanicucci, S., McLendon, G., and Gray, H. B. (1994).Structure 2, 415–422.PubMedGoogle Scholar
  31. Kuki, A., and Wolynes, P. G. (1987).Science 236, 1647–52.PubMedGoogle Scholar
  32. Labahn, A., Paddock, M. L., McPherson, P. H., Okamura, M. Y., and Feher, G. (1994).J. Chem. Phys. 98, 3417–3423.Google Scholar
  33. Levich, V. G., and Dogonadze, R. R. (1959).Dokl. Akad. Nauk SSSR 124, 123–6.Google Scholar
  34. Lin, X., Murchison, H. A., Nagarajan, V., Parson, W. W., Allen, J. P., and Williams, J. C. (1994a).Proc. Natl. Acad. Sci. USA 91, 10265–10269.PubMedGoogle Scholar
  35. Lin, X., Williams, J. C., Allen, J. P., and Mathis, P. (1994b).Biochemistry 33, 13517–13523.PubMedGoogle Scholar
  36. Marcus, R. A. (1956).J. Chem. Phys. 24, 966–978.Google Scholar
  37. Marcus, R. A., and Sutin, N. (1985).Biochim. Biophys. Acta 811, 265–322.Google Scholar
  38. McLendon, G., Zhang, Q., Wallin, S. A., Miller, R. M., Billstone, V., Spears, K. G., and Hoffman, B. M. (1993).J. Am. Chem. Soc. 115, 3665–3669.Google Scholar
  39. Michel, H., Deisenhofer, J., and Epp, O. (1986).EMBO J. 5, 2445–2451.Google Scholar
  40. Miller, J. R., Beitz, J. V., and Huddleston, R. K. (1984).J. Am. Chem. Soc. 106, 5057–5068.Google Scholar
  41. Mitchell, P. (1961).Nature (London) 191, 144–148.Google Scholar
  42. Moser, C. C., and Dutton, P. L. (1992).Biochim. Biophys. Acta 1101, 171–176.PubMedGoogle Scholar
  43. Moser, C. C., Keske, J. M., Warncke, K., Farid, R. S. and Dutton, P. L. (1992).Nature (London) 355, 796–802.Google Scholar
  44. Moser, C. C., Sension, R. J., Szarka, A. Z., Repinec, S. T., Hochstrasser, R. M., and Dutton, P. L. (1995).J. Chem. Phys., in press.Google Scholar
  45. Ohnishi, S. T., and Ohnishi, T., Eds. (1993).Cellular Membrane. A Key to Disease Processes, CRC Press, Boca Raton.Google Scholar
  46. Okamura, M. Y., and Feher, G. (1992).Annu. Rev. Biochem. 61, 861–96.PubMedGoogle Scholar
  47. Onuchic, J. N., Beratan, D. N., Winkler, J. R., and Gray, H. B. (1992).Annu. Rev. Biophys. Biomol. Struct. 21, 349–77.PubMedGoogle Scholar
  48. Padmanaban, G., Venkateswar, V., and Rangarajan, P. N. (1989).Trends Bio. Sci. 14, 492.Google Scholar
  49. Pan, L. P., Durham, B., Wolinska, J., and Millett, F. (1988).Biochemistry 27, 7180–7184.PubMedGoogle Scholar
  50. Parson, W. W., Clayton, R. K., and Cogdell, R. J. (1975).Biochim. Biophys. Acta 387, 265–277.PubMedGoogle Scholar
  51. Parson, W. W., Chu, Z. T., and Warshel, A. (1990).Biochim. Biophys. Acta 1017, 251–72.PubMedGoogle Scholar
  52. Pelletier, H., and Kraut, J. (1992).Science 258, 1748–1755.PubMedGoogle Scholar
  53. Schenck, C. C., Blankenship, R. E., and Parson, W. W. (1982).Biochim. Biophys. Acta 680, 44–59.Google Scholar
  54. Sharp, R. E., White, P., Chapman, S. K., and Reid, G. A. (1994).Biochemistry 33, 5515–5120.Google Scholar
  55. Shopes, R. J., and Wraight, C. A. (1985).Biochim. Biophys. Acta 806, 348–356.PubMedGoogle Scholar
  56. Siddarth, P., and Marcus, R. A. (1993).J. Phys. Chem. 97, 2400–2405.Google Scholar
  57. Stryer, L. (1995).Biochemistry, W. H. Freeman, New York.Google Scholar
  58. Tegoni, M., White, S. A., Roussel, A., Mathews, F. S., and Cambillau, C. (1993).Proteins: Struct. Funct. Gen. 16, 408–422.Google Scholar
  59. Tiede, D. M., and Dutton, P. L. (1993). InThe Photosynthetic Bacteria (Deisenhofer, J. and Norris, J. R., eds.), Academic Press, New York, pp. 257–288.Google Scholar
  60. Tiede, D. M., Vashishta, A.-C., and Gunner, M. R. (1993).Biochemistry 32, 4515–4531.PubMedGoogle Scholar
  61. Voet, D., and Voet, J. G. (1995).Biochemistry, Wiley, New York.Google Scholar
  62. Volk, M., Haberle, T., Feick, R., Ogrodnik, A., and Michel-Beyerle, M.-E. (1993).J. Phys. Chem. 97, 9831–9836.Google Scholar
  63. Warncke, K., Gunner, M. R., Braun, B. S., Gu, L., Yu, C.-A., Bruce, J. M., and Dutton, P. L. (1994).Biochemistry 33, 7830–41.PubMedGoogle Scholar
  64. Warshel, A. and Weiss, R. (1978). InFrontiers of Biological Energetics (Dutton, P. L., Leigh, J., and Scarpa, A. eds.), Academic Press, New York, pp. 30–36.Google Scholar
  65. Warshel, A., Chu, Z. T., and Parson, W. W. (1989).Science 246, 112–6.PubMedGoogle Scholar
  66. Warshel, A., Chu, Z. T., and Parson, W. W. (1994).J. Photochem. Photobiol. 82, 123–128.Google Scholar
  67. Willie, A., Stayton, P. S., Sligar, S. G., Durham, B., and Millett, F. (1992).Biochemistry 32, 7237–7242.Google Scholar
  68. Wuttke, D. S., Bjerrum, M. J., Winkler, J. R., and Gray, H. B. (1992a).Science 256, 1007–1009.Google Scholar
  69. Wuttke, D. S., Bjerrum, M. J., Chang, I., Winkler, J. R., and Gray, H. B. (1992b).Biochim. Biophys. Acta 1101, 168–170.Google Scholar
  70. Xia, Z. X., and Mathews, F. S. (1990).J. Mol. Biol. 212, 837–63.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1995

Authors and Affiliations

  • Christopher C. Moser
    • 1
  • Christopher C. Page
    • 1
  • Ramy Farid
    • 2
  • P. Leslie Dutton
    • 1
  1. 1.The Johnson Research Foundation and Department of Biochemistry and BiophysicsUniversity of PennsylvaniaPhiladelphia
  2. 2.Department of ChemistryRutgers University at NewarkNewark

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