Kinetics and mechanism of redox-coupled, long-range proton transfer in an iron-sulfur protein. Investigation by fast-scan protein-film voltammetry

Journal of the American Chemical Society

Volumn 120, Issue 28, 1998, Pages 7085-7094

  Hirst, Judy ^a   Duff, Jillian L C ^a   Jameson, Guy N L ^a   Kemper, Mary A ^b   Burgess, Barbara K ^b   Armstrong, Fraser A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; ASPARTIC ACID; CARBOXYLIC ACID DERIVATIVE; FERREDOXIN; IRON SULFUR PROTEIN; PROTON;

ARTICLE; CRYSTALLOGRAPHY; ELECTROCHEMISTRY; ELECTRON; ELECTRON TRANSPORT; KINETICS; OXIDATION REDUCTION REACTION; POTENTIOMETRY; PROTON TRANSPORT; SPECTROPHOTOMETRY;

EID: 0032558152     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja980380c     Document Type: Article

References (77)

1. Mitchell, P. Nature 1961, 191, 144-148: Williams, R. J. P. Biochim. Biophys. Acta 1991, 1058, 71-74.
2. Mitchell, P. Nature 1961, 191, 144-148: Williams, R. J. P. Biochim. Biophys. Acta 1991, 1058, 71-74.
3. Babcock, G. T.; Wikström, M. Nature 1992, 356, 301-309. Malmström, B. G. Acc. Chem. Res. 1993, 26, 332-338: Ramirez, B. E.; Malmström, B. G.; Winkler, J. R.; Gray, H. B. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 11949-11951. Rich, P. R.; Meunier, B.; Mitchell, R.; Moody, A. J. Biochim. Biophys. Acta 1996, 1275, 91-95.
4. Babcock, G. T.; Wikström, M. Nature 1992, 356, 301-309. Malmström, B. G. Acc. Chem. Res. 1993, 26, 332-338: Ramirez, B. E.; Malmström, B. G.; Winkler, J. R.; Gray, H. B. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 11949-11951. Rich, P. R.; Meunier, B.; Mitchell, R.; Moody, A. J. Biochim. Biophys. Acta 1996, 1275, 91-95.
5. Babcock, G. T.; Wikström, M. Nature 1992, 356, 301-309. Malmström, B. G. Acc. Chem. Res. 1993, 26, 332-338: Ramirez, B. E.; Malmström, B. G.; Winkler, J. R.; Gray, H. B. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 11949-11951. Rich, P. R.; Meunier, B.; Mitchell, R.; Moody, A. J. Biochim. Biophys. Acta 1996, 1275, 91-95.
6. Babcock, G. T.; Wikström, M. Nature 1992, 356, 301-309. Malmström, B. G. Acc. Chem. Res. 1993, 26, 332-338: Ramirez, B. E.; Malmström, B. G.; Winkler, J. R.; Gray, H. B. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 11949-11951. Rich, P. R.; Meunier, B.; Mitchell, R.; Moody, A. J. Biochim. Biophys. Acta 1996, 1275, 91-95.
7. Clark, W. M. Oxidation Reduction Potentials of Organic Systems; Williams and Wilkins: Baltimore, 1960.
8. Verkhovsky, M. I.; Morgan, J. E.; Wikström, M. Biochemistry 1995, 34, 7483-7491. Brzezinski, P. Biochemistry 1996, 35, 5611-5615: Ädelroth, P.; Sigurdson, H.; Hallén, S.; Brzezinski, P. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 12292-12297.
9. Verkhovsky, M. I.; Morgan, J. E.; Wikström, M. Biochemistry 1995, 34, 7483-7491. Brzezinski, P. Biochemistry 1996, 35, 5611-5615: Ädelroth, P.; Sigurdson, H.; Hallén, S.; Brzezinski, P. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 12292-12297.
10. Verkhovsky, M. I.; Morgan, J. E.; Wikström, M. Biochemistry 1995, 34, 7483-7491. Brzezinski, P. Biochemistry 1996, 35, 5611-5615: Ädelroth, P.; Sigurdson, H.; Hallén, S.; Brzezinski, P. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 12292-12297.
11. Graige, M. S.; Paddock, M. L.; Bruce, J. M.; Feher, G.; Okamura, M. Y. J. Am. Chem. Soc. 1996, 118, 9005-9016.
12. Sarai, A.; DeVault, D. Methods Enzymol. 1986, 127, 79-91. Bahnson, B. J.; Klinman, J. P. Methods Enzymol. 1995, 249, 373-397.
13. Sarai, A.; DeVault, D. Methods Enzymol. 1986, 127, 79-91. Bahnson, B. J.; Klinman, J. P. Methods Enzymol. 1995, 249, 373-397.
14. Nagle, J. F.; Morowitz, H. J. Proc. Natl. Acad. Sci. U.S.A. 1978, 75, 298-302: Nagle, J. F.; Tristam-Nagle, S. J. Membr. Biol. 1983, 74, 1-14. Schulten, Z.; Schulten, K. Methods Enzymol. 1986, 127, 419-438.
15. Nagle, J. F.; Morowitz, H. J. Proc. Natl. Acad. Sci. U.S.A. 1978, 75, 298-302: Nagle, J. F.; Tristam-Nagle, S. J. Membr. Biol. 1983, 74, 1-14. Schulten, Z.; Schulten, K. Methods Enzymol. 1986, 127, 419-438.
16. Nagle, J. F.; Morowitz, H. J. Proc. Natl. Acad. Sci. U.S.A. 1978, 75, 298-302: Nagle, J. F.; Tristam-Nagle, S. J. Membr. Biol. 1983, 74, 1-14. Schulten, Z.; Schulten, K. Methods Enzymol. 1986, 127, 419-438.
17. Baciou, L.; Michel, H. Biochemistry 1995, 34, 7967-7972.
18. Williams, R. J. P. Annu. Rev. Biophys. Biophys. Chem. 1988, 17, 71-97.
19. Warshel, A. Methods Enzymol. 1986, 127, 578-587.
20. Lanyi, J. K. Nature 1995, 375, 461-463.
21. Fetter, J. R.; Qian, J.; Shapleigh, J.; Thomas, J. W.; García-Horsman, A.; Schmidt, E.; Hosler, J.; Babcock, G. T.; Gennis, R. B.; Ferguson-Miller, S. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 1604-1608.
22. Iwata, S.; Ostermeier, C.; Ludwig, B.; Michel, H. Nature 1995, 376, 660-669. Ostermeier, C.; Iwata, S.; Michel, H. Curr. Opin. Struct. Biol. 1996, 6, 460-466.
23. Iwata, S.; Ostermeier, C.; Ludwig, B.; Michel, H. Nature 1995, 376, 660-669. Ostermeier, C.; Iwata, S.; Michel, H. Curr. Opin. Struct. Biol. 1996, 6, 460-466.
24. Morgan, J. E.; Verkhovsky, M. I.; Wikström, M. J. Bioenerg. Biomembr. 1994, 26, 599-608.
25. Okamura, M. Y.; Feher, G. Annu. Rev. Biochem. 1992, 61, 861-896.
26. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. Paddock, M. L.; Rongey, S. H.; McPherson, P. H.; Juth, A.; Feher, G.; Okamura, M. Y. Biochemistry 1994, 33, 734-745. McPherson, P. H.; Schönfeld, M.; Paddock, M. L.; Okamura, M. Y.; Feher, G. Biochemistry 1994, 33, 1181-1193.
27. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. Paddock, M. L.; Rongey, S. H.; McPherson, P. H.; Juth, A.; Feher, G.; Okamura, M. Y. Biochemistry 1994, 33, 734-745. McPherson, P. H.; Schönfeld, M.; Paddock, M. L.; Okamura, M. Y.; Feher, G. Biochemistry 1994, 33, 1181-1193.
28. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. Paddock, M. L.; Rongey, S. H.; McPherson, P. H.; Juth, A.; Feher, G.; Okamura, M. Y. Biochemistry 1994, 33, 734-745. McPherson, P. H.; Schönfeld, M.; Paddock, M. L.; Okamura, M. Y.; Feher, G. Biochemistry 1994, 33, 1181-1193.
29. Takahashi, E.; Wraight, C. A. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 2640-2645. Takahashi, E.; Wraight, C. A. Biochemistry 1992, 31, 855-866. Takahashi, E.; Wraight, C. A. Biochim. Biophys. Acta 1990, 1020, 107-111.
30. Takahashi, E.; Wraight, C. A. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 2640-2645. Takahashi, E.; Wraight, C. A. Biochemistry 1992, 31, 855-866. Takahashi, E.; Wraight, C. A. Biochim. Biophys. Acta 1990, 1020, 107-111.
31. Takahashi, E.; Wraight, C. A. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 2640-2645. Takahashi, E.; Wraight, C. A. Biochemistry 1992, 31, 855-866. Takahashi, E.; Wraight, C. A. Biochim. Biophys. Acta 1990, 1020, 107-111.
32. (a) Burgess, B. K.; Lowe, D. J. Chem. Rev. 1996, 96, 2983-3011.
33. (b) Peters, J. W.; Stowed, M. H. B.; Soltis, S. M.; Finnegan, M. G.; Johnson, M. K.; Rees, D. G. Biochemistry 1997, 36, 1181-1187. See also: Rohlfs, R. J.; Huang, L.; Hille, R. J. Biol. Chem. 1995, 270, 22196-22207, for a recent example of a study of proton-gated electron transfer in an Fe-S flavoenzyme.
34. (b) Peters, J. W.; Stowed, M. H. B.; Soltis, S. M.; Finnegan, M. G.; Johnson, M. K.; Rees, D. G. Biochemistry 1997, 36, 1181-1187. See also: Rohlfs, R. J.; Huang, L.; Hille, R. J. Biol. Chem. 1995, 270, 22196-22207, for a recent example of a study of proton-gated electron transfer in an Fe-S flavoenzyme.
35. Cukier, R. I. J. Phys. Chem. 1994, 98, 2377-2381; 1995, 99, 16101-16115; 1996, 100, 15428-15433. Kirby, J. P.; Roberts, J. A.; Nocera, D. G. J. Am. Chem. Soc. 1996, 119, 9230-9236.
36. Cukier, R. I. J. Phys. Chem. 1994, 98, 2377-2381; 1995, 99, 16101-16115; 1996, 100, 15428-15433. Kirby, J. P.; Roberts, J. A.; Nocera, D. G. J. Am. Chem. Soc. 1996, 119, 9230-9236.
37. Cukier, R. I. J. Phys. Chem. 1994, 98, 2377-2381; 1995, 99, 16101-16115; 1996, 100, 15428-15433. Kirby, J. P.; Roberts, J. A.; Nocera, D. G. J. Am. Chem. Soc. 1996, 119, 9230-9236.
38. Cukier, R. I. J. Phys. Chem. 1994, 98, 2377-2381; 1995, 99, 16101-16115; 1996, 100, 15428-15433. Kirby, J. P.; Roberts, J. A.; Nocera, D. G. J. Am. Chem. Soc. 1996, 119, 9230-9236.
39. Armstrong, F. A.; Heering, H. A.; Hirst, J. Chem. Soc. Rev. 1997, 26, 169-179.
40. Hirst, J.; Armstrong, F. A. Submitted for publication.
41. Cammack, R. Adv. Inorg. Chem. 1992, 38, 281-322. Johnson, M. K. Encyclopedia of Inorganic Chemistry; King, R. B., Ed.; Wiley: Chichester, 1994; pp 1896-1915. Beinert, H.; Holm, R. H.; Münck, E. Science 1997, 277, 653-659.
42. Cammack, R. Adv. Inorg. Chem. 1992, 38, 281-322. Johnson, M. K. Encyclopedia of Inorganic Chemistry; King, R. B., Ed.; Wiley: Chichester, 1994; pp 1896-1915. Beinert, H.; Holm, R. H.; Münck, E. Science 1997, 277, 653-659.
43. Cammack, R. Adv. Inorg. Chem. 1992, 38, 281-322. Johnson, M. K. Encyclopedia of Inorganic Chemistry; King, R. B., Ed.; Wiley: Chichester, 1994; pp 1896-1915. Beinert, H.; Holm, R. H.; Münck, E. Science 1997, 277, 653-659.
44. The Rieske center is an example of an Fe-S cluster in which electron transfer is linked to ligand (imidazole)-based proton transfer. See: Link, T. A.; Hagen, W. R.; Pierik, A. J.; von Jagow, G. Eur. J. Biochem. 1992, 208, 685-691.
45. Duff, J. L. C.; Breton, J. L. J.; Butt, J. N.; Armstrong, F. A.; Thomson, A. J. J. Am. Chem. Soc. 1996, 118, 8593-8603.
46. Butt, J. N.; Sucheta, A.; Martin, L. L.; Shen, B.; Burgess, B. K.; Armstrong, F. A. J. Am. Chem. Soc. 1993, 115, 12587-12588.
47. Shen, B.; Martin, L. L.; Butt, J. N.; Armstrong, F. A.; Stout, C. D.; Jensen, G. M.; Stephens, P. J.; La Mar, G. N.; Gorst, C. M.; Burgess, B. K. J. Biol. Chem. 1993, 268, 25928-25939.
48. (a) Breton, J. L.; Duff, J. L. C.; Butt, J. N.; Armstrong, F. A.; George, S. J.; Pétillot, Y.; Forest, E.; Schäfer, G.; Thomson, A. J. Eur. J. Biochem. 1995, 233, 937-946:
49. (b) Fawcett, S. E. J.; Davis, D. E.; Breton, J. L. J.; Thomson, A. J.; Armstrong, F. A. submitted for publication.
50. George, S. J.; Richards, A. J. M.; Thomson, A. J.; Yates, M. G. Biochem. J. 1984, 224, 247-251. Armstrong, F. A.; George, S. J.; Thomson, A. J.; Yates, M. G. FEBS Lett. 1988, 234, 107-110.
51. George, S. J.; Richards, A. J. M.; Thomson, A. J.; Yates, M. G. Biochem. J. 1984, 224, 247-251. Armstrong, F. A.; George, S. J.; Thomson, A. J.; Yates, M. G. FEBS Lett. 1988, 234, 107-110.
52. Johnson, M. K.; Bennett, D. E.; Fee, J. A.; Sweeney, W. V. Biochim. Biophys. Acta 1987, 911, 81-94.
53. Stephens, P. J.; Jensen, G. M.; Devlin, F.; Morgan, T. V.; Stout, C. D.; Burgess, B. K. Biochemistry 1991, 30, 3200-3209.
54. Iismaa, S. E.; Vázquez, A. E.; Jensen, G. M.; Stephens, P. J.; Butt, J. N.; Armstrong, F. A.; Burgess, B. K. J. Biol. Chem. 1991, 266, 21563-21571.
55. Hu, Z. G.; Jollie, D.; Burgess, B. K.; Stephens, P. J.; Münck, E. Biochemistry 1994, 33, 14475-14485.
56. Stout, C. D. J. Biol. Chem. 1988, 263, 9256-9260; J. Mol. Biol. 1989, 205, 545-555.
57. Stout, C. D. J. Biol. Chem. 1988, 263, 9256-9260; J. Mol. Biol. 1989, 205, 545-555.
58. Stout, C. D. J. Biol. Chem. 1993, 268, 25920-25927.
59. Cheng, H.; Grohmann, K.; Sweeney, W. V. J. Biol. Chem. 1990, 265, 12388-12392.
60. Bond, A. M.; Oldham, K. B. J. Phys. Chem. 1983, 87, 2492-2502: Evans, D. H.; O'Connell, K. M. Electroanal. Chem. 1986, 14, 113-207.
61. Bond, A. M.; Oldham, K. B. J. Phys. Chem. 1983, 87, 2492-2502: Evans, D. H.; O'Connell, K. M. Electroanal. Chem. 1986, 14, 113-207.
62. Hoffman, B. M.; Ratner, M. R. J. Am. Chem. Soc. 1987, 109, 6237-6243. Brunschwig, B. S.; Sutin, N. J. Am. Chem. Soc. 1989, 111, 7454-7465.
63. Hoffman, B. M.; Ratner, M. R. J. Am. Chem. Soc. 1987, 109, 6237-6243. Brunschwig, B. S.; Sutin, N. J. Am. Chem. Soc. 1989, 111, 7454-7465.
64. Bard, A. J.; Faulkner, L. R. Electrochemical Methods: Fundamentals and Applications; Wiley: New York, 1980.
65. Armstrong, F. A. In Bioelectrochemistry of Biomacromolecules: Bioelectrochemistry: Principles and Practice; Lenaz, G., Milazzo, G., Eds.; Birkhauser Verlag: Basel, 1997; pp 205-255. Armstrong, F. A.; Butt, J. N.; Sucheta, A. Methods Enzymol. 1993, 227, 479-500. Armstrong, F. A. Adv. Inorg. Chem. 1992, 38, 117-163.
66. Armstrong, F. A. In Bioelectrochemistry of Biomacromolecules: Bioelectrochemistry: Principles and Practice; Lenaz, G., Milazzo, G., Eds.; Birkhauser Verlag: Basel, 1997; pp 205-255. Armstrong, F. A.; Butt, J. N.; Sucheta, A. Methods Enzymol. 1993, 227, 479-500. Armstrong, F. A. Adv. Inorg. Chem. 1992, 38, 117-163.
67. Armstrong, F. A. In Bioelectrochemistry of Biomacromolecules: Bioelectrochemistry: Principles and Practice; Lenaz, G., Milazzo, G., Eds.; Birkhauser Verlag: Basel, 1997; pp 205-255. Armstrong, F. A.; Butt, J. N.; Sucheta, A. Methods Enzymol. 1993, 227, 479-500. Armstrong, F. A. Adv. Inorg. Chem. 1992, 38, 117-163.
68. Britz, D. J. Electroanal. Chem. 1978, 88, 309-352.
69. Press, W. H.; Flannery, B. P.; Teukolsky, S. A.; Vetterling, W. T. Numerical Recipes in Pascal; Cambridge University Press: New York, 1989.
70. Britz, D. Digital Simulation in Electrochemistry, 2nd ed.; Springer-Verlag: Berlin, 1988.
71. Pladziewicz, J. R.; Meyer, T. J.; Broomhead, J. A.; Taube, H. Inorg. Chem. 1973, 12, 639-643.
72. Wilkins, R. G. In Kinetics and Mechanism of Reactions of Transition Metal Complexes; VCH: Weinheim, 1991; pp 15 and 16.
73. Lappin, A. G. Redox Mechanisms in Inorganic Chemistry; Ellis Horwood: Chichester, 1994.
74. An example of a complete ECEC cycle as analyzed by protein-film voltammetry is given in a study of the redox-dependent binding of a thiolate ligand to a [4Fe-4S] cluster. See: Butt, J. N.; Sucheta, A.; Armstrong, F. A.; Breton, J.; Thomson, A. J.; Hatchikian, E. C. J. Am. Chem. Soc. 1993, 115, 1413-1421.
75. Armstrong, F. A. J. Biol. Inorg. Chem. 1997, 2, 139-142.
76. Huheey, J. E.; Keiter, E. A.; Keiter, R. L. Inorganic Chemistry: Principles of Structure and Reactivity, 4th ed.; Harper Collins: New York, 1993.
77. We have assumed that the salt bridge between D15 and K84 is weak and does not restrict the function of D15. Our results support this proposal since, if the integrity of the salt bridge was a key factor in mediating proton transfer, rates of both protonation and deprotonation would fall off at low pH; instead, only deprotonation slows down, while the rate of protonation approaches a maximum value.