Pressure Effects on the Intramolecular Electron Transfer Reactions in Hemoproteins

  • Yoshiaki Furukawa
  • Yoichi Sugiyama
  • Satoshi Takahashi
  • Koichiro Ishimori
  • Isao Morishima
Part of the Biological and Medical Physics Series book series (BIOMEDICAL)


The activation volumes (ΔV ) for intramolecular electron transfer (ET) reactions in Ru-modified cytochrome b 5 (Ru-cytb 5) and Zn-porphyrin substituted myoglobins (Ru-ZnMb) were determined to investigate the pressure effects on the ET pathway; this provided us with new insights into the fluctuation—controlled ET reaction mechanism in proteins. Ru-cytb 5, in which the Ru complex was attached at His26, exhibited a large negative activation volume for the ET reaction, although the ET reactions in previous Rucytb 5 mutants were almost insensitive to pressurization [14]. The pathway analysis revealed that our Ru-cytb 5 system has a long ‘through-space’ process on the electron pathway, while the pathway for the previous system consisted of only a ‘through-bond’ process with covalent bonds or included a single short ‘through-space’ process. The pressure effects on the ET reaction, therefore, depend highly on the flexibility of the pathway, a flexible ‘through-space’ or rigid ‘through-bond’ process, and the ET reaction mediated by the ‘through-space’ process would be more susceptible to pressurization, implying that the structural fluctuation would preferentially affect the ‘through-space’ ET reaction. To confirm the prominent effects of pressure on the ‘through-space’ ET reaction, we also examined the pressure dependence of Ru-ZnMbs, the ET pathways of which have some flexible and long ‘through-space’ processes. In spite of the same donor—acceptor (D—A) pair, three Ru-ZnMbs, for which D—A distances for the ET reactions are 12.7 (His48Mb), 15.5 (His83Mb) and 19.3 Å (His81Mb), showed different activation volumes for the ET reactions: —1.6 (His83Mb), +3.7 (His81Mb), +6.5 cm3 mol−1 (His48Mb). Since the Marcus theory indicates that the acceleration and deceleration of the ET reaction rates in RuZnMbs would correspond to the shortening and stretching of the D—A distance, respectively, some of the flexible ‘through-space’ processes in Ru-ZnMbs would reduce the D—A distance and the others would increase the distance by pressurization. In other words, the structural fluctuation affecting the ‘through-space’ ET process is not isotropic in protein, and local fluctuations count as one of the factors regulating the protein ET reactions.


Activation Volume Pressure Effect Pressure Dependence Reorganization Energy Dynamic Fluctuation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 9.1
    R.A. Marcus, N. Sutin: Biochim. Biophys. Acta 811, 265 (1985)CrossRefGoogle Scholar
  2. 9.2
    J.R. Winkler, H.B. Gray: Chem. Rev. 92, 369 (1992)CrossRefGoogle Scholar
  3. 9.3
    G. McLendon, R. Hake: Chem. Rev. 92, 481 (1992)CrossRefGoogle Scholar
  4. 9.4
    B.M. Hoffman, M.A. Ratner: J. Am. Chem. Soc. 109, 6237 (1987)CrossRefGoogle Scholar
  5. 9.5
    B.H. McMahon, J.D. Müller, C.A. Wraight, G.U. Nienhaus: Biophys. J. 74, 2567 (1998)Google Scholar
  6. 9.6
    E.S. Medvedev, A.A. Stuchebrukhov: J. Chem. Phys. 107, 3821 (1997)ADSCrossRefGoogle Scholar
  7. 9.7
    A.J.A. Aquino, P. Beroza, J. Reagan, J.N. Onuchic: Chem. Phys. Lett. 275, 181 (1997)ADSCrossRefGoogle Scholar
  8. 9.8
    I. Daizadeh, E.S. Medvedev, A.A. Stuchebrukhov: Proc. Natl. Acad. Sci. USA 94, 3703 (1997)ADSCrossRefGoogle Scholar
  9. 9.9
    H. Frauenfelder, F. Parak, R.D. Young: Annu. Rev. Biophys. Biochem. 17, 451 (1998)CrossRefGoogle Scholar
  10. 9.10
    A. Ansari, J. Berendzen, S.F. Bowne, H. Frauenfelder, I.E.T. Iben, T.B. Sauke, E. Shyamsunder, R.D. Young: Proc. Natl. Acad. Sci. USA 82, 5000 (1985)ADSCrossRefGoogle Scholar
  11. 9.11
    Y. Sugiyama, S. Takahashi, K. Ishimori, I. Morishima: J. Am. Chem. Soc. 119, 9582 (1997)CrossRefGoogle Scholar
  12. 9.12
    M. Meier, R. van Eldik, I.-J. Chang, G.A. Mines, D.S. Wuttke, H.B. Gray: J. Am. Chem. Soc. 116, 1577 (1994)CrossRefGoogle Scholar
  13. 9.13
    J.F. Wishart, R. van Eldik, J. Sun, C. Su, S.S. Isied: Inorg. Chem. 31, 3986 (1992)CrossRefGoogle Scholar
  14. 9.14
    J.R. Scott, J.L. Fairris, M. McLean, K. Wang, S.G. Sligar, B. Durham, F. Millets: Inorg. Chim. Acta 243, 193 (1996)CrossRefGoogle Scholar
  15. 9.15
    K. Heremans, L. Smeller: Biochim. Biophys. Acta 1386, 353 (1998)CrossRefGoogle Scholar
  16. 9.16
    H. Frauenfelder, N.A. Alberding, A. Ansari, D. Braunstein, B.R. Cowen, M.K. Hong, I.E.T. Iben, J.B. Johnson, S. Luck, M.C. Marden, J.R. Mourant, P. Ormos, L. Reinisch, R. Scholl, A. Schulte, E. Shyamsunder, L.B. Sorensen, P.J. Steinbach, A. Xie, R.D. Young, K.T. Yue: J. Phys. Chem. 94, 1024 (1990)CrossRefGoogle Scholar
  17. 9.17
    R. van Eldik, T. Asano, W. J. Le Noble: Chem. Rev. 89, 549 (1989)CrossRefGoogle Scholar
  18. 9.18
    F.S. Mathews, E.W. Czerwinski, P. Argos, in The Porphyrins,Vol.7 ed. by D. Dolphin ( Academic Press, New York 1979 ) p. 107Google Scholar
  19. 9.19
    E.C. Johnson, B.P. Sullivan, D.J. Salmon, S.A. Adeyemi, T.J. Meyer: Inorg. Chem. 17, 2211 (1978)CrossRefGoogle Scholar
  20. 9.20
    P. Ford, D.F.P. Rudd, R. Gaunder, H. Taube: J. Am. Chem. Soc. 90, 1187 (1968)CrossRefGoogle Scholar
  21. 9.21
    A.D. Adler, F.R. Longo, F. Kampas, J. Kim: J. Inorg. Nucl. Chem. 32, 2443 (1970)CrossRefGoogle Scholar
  22. 9.22
    S.B. von Bodman, M.A. Schuler, D.R. Jouie, S.G. Sligar: Proc. Natl. Acad. Sci. USA 83, 9443 (1986)ADSCrossRefGoogle Scholar
  23. 9.23
    B. Durham, L.P. Pan, S. Hahm, J. Long. Millett, in ACS Advances in Chemistry Series, Vol. 226 ed. by M.K. Johnson, R.B. King, D.M. Kurtz, C. Kutal, M.L. Norton, and R.A. Scott ( American Chemical Society, Washington DC 1990 ) p. 181Google Scholar
  24. 9.24
    M.P. Jackman, M. Lim, P. Osvath, D.G.A. Harshani de Silva, A.G. Sykes: Inorg. Chim. Acta 153, 205 (1988)Google Scholar
  25. 9.25
    J. Altman, J.J. Lipka, I. Kuntz, L. Waskell: Biochemistry 28, 7516 (1989)CrossRefGoogle Scholar
  26. 9.26
    C.D. Moore, O.N. Al-Misky, J.T.J. Lecomte: Biochemistry 30, 8357 (1991)CrossRefGoogle Scholar
  27. 9.27
    A. Willie, P.S. Stayton, S.G. Sligar, B. Durham, F. Millett: Biochemistry 31, 7237 (1992)CrossRefGoogle Scholar
  28. 9.28
    R. Varadarajan, A. Szabo, S.G. Boxer: Proc. Natl. Acad. Sci. USA 82, 5681, (1985)ADSCrossRefGoogle Scholar
  29. 9.29
    D.R. Casimiro, L. Wong, J.L. Colon, T.E. Zewert, J.H. Richards, I.-J. Chang, J. R. Winkler, H.B. Gray: J. Am. Chem. Soc. 115, 1485 (1993)CrossRefGoogle Scholar
  30. 9.30
    F.W.J. Teale: Biochim. Biophys. Acta 35, 543 (1959)CrossRefGoogle Scholar
  31. 9.31
    A.W. Axup, M. Albin, S.L. Mayo, R.J. Crutchley, H.B. Gray: J. Am. Chem. Soc. 110, 435 (1989)CrossRefGoogle Scholar
  32. 9.32
    J.A. Cowan, H.B. Gray: Inorg. Chem. 28, 2074 (1989)CrossRefGoogle Scholar
  33. 9.33
    K. Hara, I. Morishima: Rev. Sci. Instrum. 59, 2397 (1988)ADSCrossRefGoogle Scholar
  34. 9.34
    R.C. Newmann Jr., W. Kauzmann, A. Zipp: J. Phys. Chem. 77, 2687 (1973)CrossRefGoogle Scholar
  35. 9.35
    B. Durham, J.V. Casper, J.K. Nagle, T.J. Meyer: J. Am. Chem. Soc. 104, 4803 (1982)CrossRefGoogle Scholar
  36. 9.36
    P.S. Braterman, A. Harriman, G.A. Heath, L.J. Yellowlees: J. Chem. Soc. Dalton Trans. 1801 (1983)Google Scholar
  37. 9.37
    G.A. Heath, L.J. Yellowlees: J. Chem. Soc. Chem. Comm. 287 (1981)Google Scholar
  38. 9.38
    K. Sigfridsson, M. Sundahl, M.J. Bjerrum, O.J. Hansson: J. Bioinorg. Chem. 405 (1996)Google Scholar
  39. 9.39
    K. Sigfridsson, M. Ejdedaeck, M. Sundahl, O. Hansson: Arch. Biochem. Biophys. 351, 197 (1998)CrossRefGoogle Scholar
  40. 9.40
    L.K. Skov, T. Pascher, J.R. Winkler, H.B. Gray: J. Am. Chem. Soc. 120, 1102 (1998)CrossRefGoogle Scholar
  41. 9.41
    A.J. Di Bilio, M.G. Hill, N. Bonander, B.G. Karlsson, R.M. Villahermosa, B.G. Malmström, J.R. Winkler, H.B. Gray: J. Am. Chem. Soc. 119, 9921 (1997)CrossRefGoogle Scholar
  42. 9.42
    A.J. Di Bilio, C. Denninson, H.B. Gray, B.E. Ramirez, A.G. Sykes, J.R. Winkler: J. Am. Chem. Soc. 120, 7551 (1998)CrossRefGoogle Scholar
  43. 9.43
    D.H. Heacock II, M.R. Harris, B. Durham, F. Millett: Inorg. Chim. Acta 226, 129 (1994)CrossRefGoogle Scholar
  44. 9.44
    A. Freiberg, A. Ellervee, M. Tars, K. Timpmann, A. Laisaar: Biophys. Chem. 68, 189 (1997)CrossRefGoogle Scholar
  45. 9.45
    W. Chung, N.J. Turro, I.R. Gould, S. Farid: J. Phys. Chem. 95, 7752 (1991)CrossRefGoogle Scholar
  46. 9.46
    B. Bänsch, M. Meier, P. Martinez, R. van Eldik, C. Su, J. Sun, S.S. Isied, J.F. Wishart: Inorg. Chem 33, 4744 (1994)CrossRefGoogle Scholar
  47. 9.47
    B. Durham, L.P. Pan, J.E. Long, F. Millett: Biochemistry 28, 8659 (1989)CrossRefGoogle Scholar
  48. 9.48
    J.A. Cowan, R.K. Upmacis, D.N. Beratan, J.N. Onuchic, H.B. Gray: Ann. N. Y. Acad. Sci. 550, 68 (1989)ADSCrossRefGoogle Scholar
  49. 9.49
    H. Li, H. Yamada, K. Akasaka: Biochemistry 37, 1167 (1998)CrossRefGoogle Scholar
  50. 9.50
    K. Akasaka, T. Tezuka, H. Yamada: J. Mol. Biol. 271, 671 (1997)CrossRefGoogle Scholar
  51. 9.51
    Y. Furukawa, K. Ishimori, I. Morishima: J. Phys. Chem. B 104, 1817 (2000)CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • Yoshiaki Furukawa
    • 1
  • Yoichi Sugiyama
    • 1
  • Satoshi Takahashi
    • 1
  • Koichiro Ishimori
    • 1
  • Isao Morishima
    • 1
  1. 1.Department of Molecular Engineering, Graduate School of EngineeringKyoto UniversityKyotoJapan

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