Application of electron transfer theories to biological systems

  • Patrick Bertrand
Conference paper
Part of the Structure and Bonding book series (STRUCTURE, volume 75)

Abstract

In biological systems, the mechanisms of conversions and storage of energy involved sequences of oxido-reduction reactions in which electrons are transferred along a chain of redox centers embedded in a protein medium. The theoretical interpretation of the kinetics of these transfers pertains to Quamtum Mechanics, and was developed by chemists and physicists. However, owing to the fundamental importance of these processes, many biochemists are also concerned with these theories and their practical application to biological systems. This introductory chapter is an attempt to clarify the physical basis of current theoretical interpretations of biological electron transfers. It comprises an account of the standard formalism appropriate for non-adiabatic processes, and a analysis of kinetic data. Important advances in this field have resulted, on the one hand, from precise theoretial calculations based on molecular structures, and on the other hand, from implementation of elaborate experimental methods based on efficient chemical and biochemical techniques. This topic is illustrated by many examples taken from the recent literature which concern redox proteins as well as photosynthestic systems.

Keywords

Electron Transfer Chem Phys Electron Transfer Process Electron Transfer Rate Reorganization Energy 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Marcus RA (1956) J Chem Phys 24: 966Google Scholar
  2. 2.
    Marcus RA (1960) Disc Faraday Soc 29: 21Google Scholar
  3. 3.
    Marcus RA (1965) J Chem Phys 43: 679Google Scholar
  4. 4.
    Marcus RA, Sutin N (1985) Biochim Biophys Acta 811: 265Google Scholar
  5. 5.
    Levich VG (1966) Adv Electrochem Electochem Eng 4: 249Google Scholar
  6. 6.
    Dogonadze RR, Kuznetsov AM, Vorotyntsev MA (1972) Phys Stat Sol B 54: 125Google Scholar
  7. 7.
    Kestner NR, Logan J, Jortner J (1974) J Phys Chem 78: 2148Google Scholar
  8. 8.
    Hopfield JJ (1974) Proc Nat Acad Sci USA 71: 3640Google Scholar
  9. 9.
    Jortner, J (1976) J Chem Phys 64: 4860Google Scholar
  10. 10.
    Pierrot M, Haser R, Frey M, Payan F, Astier JP (1982) J Bio1 Chem 23: 14341Google Scholar
  11. 11.
    Higushi Y, Kusonoki M, Yasuoka N, Kakudo M, Yagi T (1984) J Mol Biol 172: 109Google Scholar
  12. 12.
    McRee DE, Richardson DC, Richardson JS, Siegel LM (1986) J Bio1 Chem 261: 10277Google Scholar
  13. 13.
    Verma AL, Kimura K, Nakamura A, Yagi T, Inokuchi H, Kitagawa T (1988) J Am Chem Soc 110: 6617Google Scholar
  14. 14.
    Chance B, Marcus RA, Devault DC, Schrieffer JR, Frauenfelder H, Stain N (eds) (1979) Tunnelling in biological systems, Academic, New York.Google Scholar
  15. 15.
    Deisenhofer J, Epp O, Miki K, Huber R, Michel H (1984) J Mol Biol 180: 385Google Scholar
  16. 16.
    Deisenhofer J, Epp O, Miki K, Huber R, Michel H (1985) Nature 318: 618Google Scholar
  17. 17.
    Michel H, Epp O, Deisenhofer J (1986) EMBO J 5: 2445Google Scholar
  18. 18.
    Allen JP, Feher G, Yeates TO, Komiya H, Rees DC (1987) Proc Nat Acad Sci USA 84: 5730Google Scholar
  19. 19.
    Allen JP, Feher G, Yeates TO, Komiya H, Rees DC (1987) Proc Nat Acad Sci USA 84: 6162Google Scholar
  20. 20.
    Allen JP, Feher G, Yeates TO, Komiya H, Rees DC (1988) Proc Nat Acad Sci USA 85: 8487Google Scholar
  21. 21.
    Feher G, Allen JP, Okamura MY, Rees DC (1989) Nature 339: 111Google Scholar
  22. 22.
    Devault D (1984) Quantum mechanical tunnelling in biological systems. Cambridge University Press, CambridgeGoogle Scholar
  23. 23.
    Bertrand P (1986) Biochimie 68: 619Google Scholar
  24. 24.
    McLendon G (1988) Acc Chem Res 21: 160Google Scholar
  25. 25.
    Newton MD (1982) ACS Sym Ser 198: 255Google Scholar
  26. 26.
    Newton MD, Sutin N (1984) Ann Rev Phys Chem 35: 437Google Scholar
  27. 27.
    Efrima S, Bixon M (1976) J Chem Phys 64: 3639Google Scholar
  28. 28.
    Wolfsberg M, Helmholz L (1952) J Chem Phys 20: 837Google Scholar
  29. 29.
    Siders P, Marcus RA (1981) J Am Chem Soc 103: 741Google Scholar
  30. 30.
    McCammon JA, Gelin BR, Karplus M (1977) Nature 267: 585Google Scholar
  31. 31.
    Go N, Noguti T, Nishikawa T (1983) Proc Nat Acad Sci USA 80: 3696Google Scholar
  32. 32.
    Doster W, Cusack S, Petry W (1989) Nature 337: 754Google Scholar
  33. 33.
    Marcus RA (1984) J Chem Phys 81: 4494Google Scholar
  34. 34.
    Zener C (1932) Proc Roy Soc Lond A 137: 696Google Scholar
  35. 35.
    Landau L (1932) Phys Z Sowjetunion 2: 46Google Scholar
  36. 36.
    Sailasuta N, Anson FC, Gray HB (1979) J Am Chem Soc 101: 455Google Scholar
  37. 37.
    Taniguchi VT, Sailasuta-Scott N, Anson FC, Gray HB (1980) Pure and Appl Chem 52: 2275Google Scholar
  38. 38.
    Huang YY, Kimura T (1983) Anal Biochem 133: 385Google Scholar
  39. 39.
    Huang YY, Kimura T (1984) Biochemistry 23: 2231Google Scholar
  40. 40.
    Huang YY, Hara T, Sligar S, Coon, MJ, Kimura T (1986) Biochemistry 25: 1390Google Scholar
  41. 41.
    Reid LS, Taniguchi VT, Gray HB, Mauk AG (1982) J Am Chem Soc 104: 7516Google Scholar
  42. 42.
    Blair DF, Ellis WR, Wang H, Gray HB, Chan SI (1986) J Biol Chem 261: 11524Google Scholar
  43. 43.
    Churg AK, Weiss RM, Warshel A, Takano T (1983) J Phys Chem 87: 1683Google Scholar
  44. 44.
    Warshel A, Huang JK (1986) J Chem Phys 84: 4938Google Scholar
  45. 45.
    Huang JK, Warshel A (1987) J Am Chem Soc 109: 715Google Scholar
  46. 46.
    Kuharski RA, Bader JS, Chandler D, Sprik M, Klein ML, Impey RW (1988) J Chem Phys 89: 3248Google Scholar
  47. 47.
    Hopfield JJ (1977) Biophys J 18: 311Google Scholar
  48. 48.
    Hopfield JJ (1977) In: Roux HF (ed) Electrical phenomena at the biological membrane level. Proc 29th Int Congr Chim Phys Elsevier, Amsterdam, p 471Google Scholar
  49. 49.
    Beratan DN, Hopfield JJ (1984) J Am Chem Soc 106: 1584Google Scholar
  50. 50.
    Bertrand, P (1985) Chem Phys Lett 113: 104Google Scholar
  51. 51.
    Okamura MY, Isaacson RA, Feher G (1979) Biophys Biochim Acta 546: 394Google Scholar
  52. 52.
    Siders P, Cave RJ, Marcus RA (1984) J Chem Phys 81: 5613Google Scholar
  53. 53.
    Cave RJ, Siders P, Marcus RA (1986) J Phys Chem 90: 1436Google Scholar
  54. 54.
    Halpern J, Orgel L (1960) Discuss Faraday Soc 29: 32Google Scholar
  55. 55.
    McConnell HM (1961) J Chem Phys 35: 508Google Scholar
  56. 56.
    Kramers (1934) Physica 1: 182Google Scholar
  57. 57.
    Beratan DN, Onuchic JN, Hopfield JJ (1987) J Chem Phys 86: 4488Google Scholar
  58. 58.
    Mayoh B, Day P (1974) J Chem Soc Dalton Trans 846Google Scholar
  59. 59.
    Mayoh B, Day P (1974) Inorg Chem 13: 2273Google Scholar
  60. 60.
    Richardson DE, Taube H (1983) J Am Chem Soc 105: 40Google Scholar
  61. 61.
    Larsson S (1981) J Am Chem Soc 103: 4034Google Scholar
  62. 62.
    Larsson S (1983) J Chem Soc, Faraday Trans 79: 1375Google Scholar
  63. 63.
    Beratan DN (1986) J Am Chem Soc 108: 4321Google Scholar
  64. 64.
    Bertrand P (1987) Chem Phys Lett 140: 57Google Scholar
  65. 65.
    Larsson S, Volosov A (1986) J Chem Phys 85: 2548Google Scholar
  66. 66.
    Larsson S, Volosov A (1987) J Chem Phys 87: 6623Google Scholar
  67. 67.
    Larsson S, Broo A, Kallebring, Volosov A (1988) Int J Quantum Chem Symp 15: 1Google Scholar
  68. 68.
    Newton MD (1980) Int J Quantum Chem Symp 14: 363Google Scholar
  69. 69.
    Logan J, Newton MD (1983) J Chem Phys 78: 4086Google Scholar
  70. 70.
    Newton MD (1986) J Phys Chem 90: 3734Google Scholar
  71. 71.
    Newton MD (1988) J Phys Chem 92: 3049Google Scholar
  72. 72.
    Kuki A, Wolynes PG (1987) Science 236: 1647Google Scholar
  73. 73.
    Miller JR, Beitz J (1981) J Chem Phys 74: 6746Google Scholar
  74. 74.
    Guarr T, McGuire ME, McLendon G (1985) J Am Chem Soc 107: 5104Google Scholar
  75. 75.
    Miller JR (1987) Nouv J Chim, 11: 83Google Scholar
  76. 76.
    Isied SS, Vassilian A, Wishart JF, Creutz C, Schwartz HA, Sutin N (1988) J Am Chem Soc 110: 635Google Scholar
  77. 77.
    Closs GL, Miller JJ (1988) Science 240: 440Google Scholar
  78. 78.
    Closs GL, Calcaterra LT, Green NJ, Penfield KW, Miller JR (1986) J Phys Chem 90: 3673Google Scholar
  79. 79.
    Johnson MD, Miller JR, Green NS, Closs GL (1989) J Phys Chem 93: 1173Google Scholar
  80. 80.
    Balaji V, Ng L, Jordan KD, Paddon-Row MN, Patney HK (1987) J Am Chem Soc 109: 6957Google Scholar
  81. 81.
    Oliver AM, Craig DC, Paddon-Row MN, Kroon J, Verhoeven JW (1988) Chem Phys Lett 150: 366Google Scholar
  82. 82.
    Ohta K, Closs GL, Morokuma K, Green NJ (1986) J Am Chem Soc 108: 1319Google Scholar
  83. 83.
    Heitele H, Michel-Beyerle ME (1985) J Am Chem Soc 107: 8286Google Scholar
  84. 84.
    Heitele H, Michel-Beyerle ME, Finckh P (1987) Chem Phys Lett 134: 273Google Scholar
  85. 85.
    Wasielewski MR (1988) In: Fox MA, Chanon M (eds) Photoinduced electron transfer, Elsevier, Amsterdam, Part A p 161Google Scholar
  86. 86.
    Gust D, Moore TA (1989) Science 244: 35Google Scholar
  87. 87.
    Beratan DN, Hopfield JJ, (1984) J Chem Phys 81: 5753Google Scholar
  88. 88.
    Freed KF (1986) J Chem Phys 84: 2108Google Scholar
  89. 89.
    Onudric JN, Beratan DN, Hopfield JJ (1986) J Phys Chem 90: 3707Google Scholar
  90. 90.
    Deumens E, Ohrn Y (1988) J Phys Chem 92: 3181Google Scholar
  91. 91.
    Kuznetsov AM, Ulstrup J (1982) Phys Stat Sol B 114: 673Google Scholar
  92. 92.
    Mikkelsen KV, Ulstrup J, Zakaraya MG (1989) J Am Chem Soc 111: 1315Google Scholar
  93. 93.
    Jortner, J (1980) J Am Chem Soc 102: 6676Google Scholar
  94. 94.
    Garg A, Onuchic JN (1985) J Am Chem Soc 83: 4491Google Scholar
  95. 95.
    Morillo M, Yang DY, Cukier RI (1989) J Chem Phys 90: 5711Google Scholar
  96. 96.
    Warshel A (1982) J Phys Chem 86: 2218Google Scholar
  97. 97.
    Creighton S, Hwang JK, Warshel A, Parson WW, Norris J (1988) Biochemistry 27: 774Google Scholar
  98. 98.
    Mikkelsen KV, Ratner MA (1989) J Phys Chem 93: 1759Google Scholar
  99. 99.
    Mikkelsen KV, Ratner MA (1989) J Chem Phys 90: 4237Google Scholar
  100. 100.
    Churg AK, Warshel A (1986) Biochemistry 25: 1675Google Scholar
  101. 101.
    Gray HB, Malmstrom BG (1983) Comments Inorg Chem 2: 203Google Scholar
  102. 102.
    Takano T, Dickerson RE (1981) J Mol Biol 153: 95Google Scholar
  103. 103.
    Argos P, Mathews FS (1975) J Biol Chem 250: 747Google Scholar
  104. 104.
    Teo BK, Shulman RG, Brown GS, Meixner AE (1979) J Am Chem Soc 101: 5624Google Scholar
  105. 105.
    Tsukahara K (1989) J Am Chem Soc 111: 2040Google Scholar
  106. 106.
    Trewhella J, Carlson VAP, Curtis EH, Heidorn DB (1988) Biochemistry 27: 1121Google Scholar
  107. 107.
    Levitt M, Sander C, Stern PS (1985) J Mol Biol 181: 423Google Scholar
  108. 108.
    Cusack S, Smith J, Finney J, Tidor B, Karplus M (1988) J Mol Biol 202: 903Google Scholar
  109. 109.
    Mishra KC, Mishra SK, Roy JN, Ahmad S, Das TP (1985) J Am Chem Soc 107: 7898Google Scholar
  110. 110.
    Nocera DG, Winkler JR, Yocom KM, Bordignon E, Gray HB (1984) J Am Chem Soc 106: 5145Google Scholar
  111. 111.
    Kostic NM, Margalit R, Che CM, Gray HB (1983) J Am Chem Soc 105: 7765Google Scholar
  112. 112.
    Margalit R, Kostic NM, Che CM, Blair DF, Chiang HJ, Pecht I, Shelton JB, Shelton JR, Schroeder WA, Gray HB (1984) Proc Nat Acad Sci USA 81: 6554Google Scholar
  113. 113.
    Crutchley RJ, Ellis WR, Gray HB (1985) J Am Chem Soc 107: 5002Google Scholar
  114. 114.
    Brown GM, Sutin N (1979) J Am Chem Soc 101: 883Google Scholar
  115. 115.
    Jackman MP, Mc Ginnis J, Powls R, Salmon GA, Sykes AG (1988) J Am Chem Soc 110: 5880Google Scholar
  116. 116.
    Osvath P, Salmon GA, Sykes AG (1988) J Am Chem Soc 110: 7114Google Scholar
  117. 117.
    Jackman MP, Lim MC, Salmon GA, Sykes AG (1988) J Chem Soc Dalton Trans 11: 2843Google Scholar
  118. 118.
    Farver O, Pecht I (1989) FEBS Lett 244: 379Google Scholar
  119. 119.
    Goldstein RA, Takiff L, Boxer SG (1988) Biochim Biophys Acta 934: 253Google Scholar
  120. 120.
    Buhks E, Bixon M, Jortner J (1981) Chem Phys 55: 41Google Scholar
  121. 121.
    Bixon M, Jortner J (1986) FEBS Lett 200: 303Google Scholar
  122. 122.
    Bixon M, Jortner J (1986) J Phys Chem 90: 3795Google Scholar
  123. 123.
    Knapp EW, Fischer SF (1987) J Chem Phys 87: 3880Google Scholar
  124. 124.
    Bertrand P, Gayda JP, Rao K (1982) J Chem Phys 76: 4715Google Scholar
  125. 125.
    Eden D, Matthew JB, Rosa JJ, Richards FM (1982) Proc Nat Acad Sci USA 79: 815Google Scholar
  126. 126.
    Mancino LJ, Dean DP, Blankenship RE (1984) Biochim Biophys Acta 764: 46Google Scholar
  127. 127.
    Peterson-Kennedy SE, McGourty JL, Hoffman BM (1984) J Am Chem Soc 106: 5010Google Scholar
  128. 128.
    McGourty JL, Peterson-Kennedy SE, Ruo WY, Hoffman BM (1987) Biochemistry 26: 8302Google Scholar
  129. 129.
    Miller JR, Beitz JV, Huddleston RK (1984) J Am Chem Soc 106: 5057Google Scholar
  130. 130.
    Joran AD, Leland BA, Felker PM, Zewail AH, Hopfield JJ, Dervan, PB (1987) Nature 327: 508Google Scholar
  131. 131.
    McLendon G, Miller JR (1985) J Am Chem Soc 107: 7811Google Scholar
  132. 132.
    Cheung E, Taylor K, Kornblatt JA, English AM, McLendon G, Miller JR (1986) Proc Nat Acad Sci USA 83: 1330Google Scholar
  133. 133.
    Taylor Conklin K, Mc Lendon G (1988) J Am Chem Soc 110: 3345Google Scholar
  134. 134.
    Salemne, FR (1976) J Mol Biol 102: 563Google Scholar
  135. 135.
    Wendolovski JJ, Matthew JB, Weber PC, Salemne FR (1987) Science 238: 719Google Scholar
  136. 136.
    Poulos TL, Kraut J (1980) J Biol Chem 255, 10322Google Scholar
  137. 137.
    Karas JL, Lieber CM, Gray HB (1988) J Am Chem Soc 110: 599Google Scholar
  138. 138.
    Meade TJ, Gray HB, Winkler JR (1989) J Am Chem Soc 111: 4353Google Scholar
  139. 139.
    Gunner MR, Robertson DE, Dutton PL (1986) J Phys Chem 90: 3783Google Scholar
  140. 140.
    Gunner MR, Dutton PL (1989) J Am Chem Soc 111: 3400Google Scholar
  141. 141.
    Popovic ZD, Kovacs GJ, Vincett PS, Alegria G, Dutton PL (1986) Chem Phys 110: 227Google Scholar
  142. 142.
    Bixon M, Jortner J (1988) J Phys Chem 92: 7148Google Scholar
  143. 143.
    Hazzard JT, McLendon G, Cusanovich MA, Das G, Sherman F, Tollin G (1988) Biochemistry 27: 4445Google Scholar
  144. 144.
    Mauro JM, Fishel LA, Hazzard JT, Meyer TE, Tollin G, Cusanovich MA, Kraut J (1988) Biochemistry 27: 6243Google Scholar
  145. 145.
    Miller MA, Hazzard JT, Mauro JM, Edwards SL, Simons PC, Tollin G, Kraut J (1988) Biochemistry 27: 9081Google Scholar
  146. 146.
    Liang N, Mauk AG, Pielak GJ, Johnson JA, Smith M, Hoffman BM (1988) Science 240: 311Google Scholar
  147. 147.
    Pielak GJ, Mauk AG, Smith M (1985) Nature 313: 152Google Scholar
  148. 148.
    Louie GV, Pielak GJ, Smith M, Brayer GD (1988) Biochemistry 27: 7870Google Scholar
  149. 149.
    Gingrich DJ, Noceck JM, Natan MJ, Hoffman BM (1987) J Am Chem Soc 109: 7533Google Scholar
  150. 150.
    Mayo SL, Ellis WR, Crutchley RJ, Gray HB (1986) Science 233: 948Google Scholar
  151. 151.
    Axup AW, Albin M, Mayo SL, Crutchley RJ, Gray HB (1988) J Am Chem Soc 110: 435Google Scholar
  152. 152.
    Jackman MP, McGinnis J, Powls R, Salmon GA, Sykes AG (1988) J Am Chem Soc 110: 5880Google Scholar
  153. 153.
    Hazzard JT, Moench SJ, Erman JE, Satterle JD, Tollin G (1988) Biochemistry 27: 2002Google Scholar
  154. 154.
    Hazzard JT, McLendon G, Cusanovich MA, Tollin G (1988) Biochem Biophys Res Comm 151: 429Google Scholar
  155. 155.
    Peerey LM, Kostic NM (1989) Biochemistry 28: 1861Google Scholar
  156. 156.
    Dolla A, Guerlesquin F, Bruschi M, Guigliarelli B, Asso M, Bertrand P, Gayda JP (1989) Biochim Biophys Acta 975: 395Google Scholar
  157. 157.
    Parrot P, Thiery J, Vermeglio A (1987) Biochim Biophys Acta 893: 534Google Scholar
  158. 158.
    Kleinfeld D, Okamura MY, Feher G (1984) Biochemistry 23: 5780Google Scholar
  159. 159.
    Sebban P, Wraight CA (1989) Biochim Biophys Acta 974: 54Google Scholar
  160. 160.
    Setif P, Mathis P, Wanngard TP (1984) Biochim Biophys Acta 767: 404Google Scholar
  161. 161.
    Vos MH, Van Gorkom HJ (1988) Biochim Biophys Acta 934: 293Google Scholar
  162. 162.
    Hoffman BM, Ratner MA (1987) J Am Chem Soc 109: 6237Google Scholar
  163. 163.
    Cartiing BO (1985) J Chem Phys 83: 5231Google Scholar
  164. 164.
    Brunschwig BS, Sutin N (1989) J Am Chem Soc 111: 7454Google Scholar
  165. 165.
    McLendon G, Pardue K, Bak P (1987) J Am Chem Soc 109: 7540Google Scholar
  166. 166.
    Xia ZX, Shamala N, Bethge PH, Lim LW, Bellamy HD, Xuong NH, Lederer F, Mathews FS (1987) Proc Nat Acad Sci USA 84: 2629Google Scholar
  167. 167.
    Fleming GR, Martin JL, Breton J (1988) Nature 333: 190Google Scholar
  168. 168.
    Bixon M, Jortner J (1989), Chem Phys Lett 159: 17Google Scholar
  169. 169.
    Michel-Beyerle ME, Plato M, Deisenhofer J, Michel H, Bixon M, Jortner J (1988) Biochim Biophys Acta 932: 52Google Scholar
  170. 170.
    Breton J, Martin JL, Fleming GR, Lambry JC (1988) Biochemistry 27: 8276Google Scholar
  171. 171.
    Marcus RA (1987) Chem Phys Lett 133: 471Google Scholar
  172. 172.
    Bixon M, Jortner J, Michel-Beyerle ME, Ogrodnik A, Lersch W (1987) Chem Phys Lett 140: 626Google Scholar
  173. 173.
    Marcus RA (1988) Chem Phys Lett 146: 13Google Scholar
  174. 174.
    Michel Beyerle ME, Bixon M, Jortner J (1988) Chem Phys Lett 151: 188Google Scholar
  175. 175.
    Won Y, Friesner RA (1988) Biochim Biophys Acta 935: 9Google Scholar
  176. 176.
    Holzapfel W, Finkele U, Kaiser W, Oesterhelt D, Scheer H, Stilz HU, Zinth W (1989) Chem Phys Lett 160: 1Google Scholar
  177. 177.
    Moehl KW, Lous EJ, Hoff AJ (1985) Chem Phys Lett 121: 22Google Scholar
  178. 178.
    Hunter DA, Hoff AJ, Hore PJ (1987) Chem Phys Lett 134: 6Google Scholar
  179. 179.
    Ogrodnik A, Remy-Richter N, Michel-Beyerle ME, Feick R (1987) Chem Phys Lett 135: 576Google Scholar
  180. 180.
    Joachim C (1987) Chem Phys 116: 339Google Scholar
  181. 181.
    Hu Y, Mukamel S (1989) Chem Phys Lett 160: 410Google Scholar
  182. 182.
    Reimers JR, Hush NS (1989) Chem Phys 134: 323Google Scholar
  183. 183.
    Scherer POJ, Fischer SF (1987) Chem Phys Lett 141: 179Google Scholar
  184. 184.
    Scherer POJ, Fischer SF (1989) Chem Phys 131: 115Google Scholar
  185. 185.
    Plato M, Mobius K, Michel-Beyerle ME, Bixon M, Jortner J (1988) J Am Chem Soc 110: 7279Google Scholar
  186. 186.
    Warshel A, Creighton S, Parson WW (1988) J Phys Chem 92: 2696Google Scholar
  187. 187.
    Yeates TO, Komiya H, Chirino A, Rees DC, Allen JP, Feher G (1988) Proc Natl Acad Sci USA 85: 7993Google Scholar
  188. 188.
    Plato M, Michel-Beyerle ME, Bixon M, Jortner J (1989) FEBS Lett 249: 70Google Scholar
  189. 189.
    Gupte SS, Hackenbrock CR (1988) J Biol Chem 263: 5241Google Scholar
  190. 190.
    Gupte SS, Hackenbrock CR (1988) J Biol Chem 263: 5248Google Scholar
  191. 191.
    Chazotte B, Hackenbrock CR (1989) J Biol Chem 264: 4978Google Scholar
  192. 192.
    Northrup SH, Boles JO, Reynolds JCL (1987) J Phys Chem 91: 5991Google Scholar
  193. 193.
    Wikstrom M (1989) Nature 338: 776Google Scholar
  194. 194.
    Brzezinski P, Malmstrom BG (1987) Biochim Biophys Acta 894: 29Google Scholar
  195. 195.
    Malmstrom BG (1989) FEBS Lett 250: 9Google Scholar
  196. 196.
    Williams RJP (1987) FEBS Lett 226: 1Google Scholar
  197. 197.
    Hopfield JJ, Onuchic JN, Beratan DN (1989) J Phys Chem 93: 6350Google Scholar
  198. 198.
    Gayda JP, Benosman H, Bertrand P, More C, Asso M (1988) Europ J Biochem 177: 199Google Scholar
  199. 199.
    Benosman H, Asso M, Bertrand P, Yagi T, Gayda JP (1989) Eur J Biochem 182: 51Google Scholar
  200. 200.
    Santos H, Moura JJG, Moura I, Legall J, Xavier AV (1984) Eur J Biochem 141: 283Google Scholar
  201. 201.
    Hintz MJ, Mock DM, Peterson LL, Tuttle K, Peterson JA (1982) J Biol Chem 257: 14324Google Scholar
  202. 202.
    Woodbury NWT, Parson WW (1984) Biochim Biophys Acta 767: 345Google Scholar
  203. 203.
    Booth PJ, Crystall B, Giorgi LB, Barber J, King DR, Porter G (1990) Biochim Biophys Acta 1016: 141Google Scholar

Copyright information

© Spring-Verlag 1991

Authors and Affiliations

  • Patrick Bertrand
    • 1
  1. 1.Laboratoire d'Electronique des Milieux Condensés URA CNRS 784Université de Provence, Centre de St JérômeMARSEILLE Cedex 13France

Personalised recommendations