Global observation of hydrogen/deuterium isotope effects on bidirectional catalytic electron transport in an enzyme: Direct measurement by protein-film voltammetry

Journal of the American Chemical Society

Volumn 119, Issue 32, 1997, Pages 7434-7439

  Hirst, Judy ^a   Ackrell, Brian A C ^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

DEUTERIUM; SUCCINATE DEHYDROGENASE;

ARTICLE; ELECTRON TRANSPORT; ENZYME KINETICS; ENZYME MECHANISM; IN VITRO STUDY; ISOTOPE LABELING; MITOCHONDRIAL RESPIRATION; POTENTIOMETRY; THERMODYNAMICS;

EID: 0030817887     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja9631413     Document Type: Article

References (58)

1. Ideas of the scope of protein-film voltammetry are given in the following publications: (a) Armstrong, F. A. Adv. Inorg. Chem. 1992, 38, 117-163. (b) Armstrong, F. A.; Butt, J. N.; Sucheta, A. Methods Enzymol. 1993, 227, 479-500. (c) Armstrong, F. A. Bioelectrochemistry of Biomacromolecules. In Bioelectrochemistry: Principles and Practice, Vol. 5, Lenaz, G., Milazzo, G., Eds.; Birkhauser Verlag: Basel, 1997, Vol. 5, pp 205-255. (d) Armstrong, F. A.; Heering, H. A.; Hirst, J. Chem. Soc. Rev., in press.
2. Ideas of the scope of protein-film voltammetry are given in the following publications: (a) Armstrong, F. A. Adv. Inorg. Chem. 1992, 38, 117-163. (b) Armstrong, F. A.; Butt, J. N.; Sucheta, A. Methods Enzymol. 1993, 227, 479-500. (c) Armstrong, F. A. Bioelectrochemistry of Biomacromolecules. In Bioelectrochemistry: Principles and Practice, Vol. 5, Lenaz, G., Milazzo, G., Eds.; Birkhauser Verlag: Basel, 1997, Vol. 5, pp 205-255. (d) Armstrong, F. A.; Heering, H. A.; Hirst, J. Chem. Soc. Rev., in press.
3. Ideas of the scope of protein-film voltammetry are given in the following publications: (a) Armstrong, F. A. Adv. Inorg. Chem. 1992, 38, 117-163. (b) Armstrong, F. A.; Butt, J. N.; Sucheta, A. Methods Enzymol. 1993, 227, 479-500. (c) Armstrong, F. A. Bioelectrochemistry of Biomacromolecules. In Bioelectrochemistry: Principles and Practice, Vol. 5, Lenaz, G., Milazzo, G., Eds.; Birkhauser Verlag: Basel, 1997, Vol. 5, pp 205-255. (d) Armstrong, F. A.; Heering, H. A.; Hirst, J. Chem. Soc. Rev., in press.
4. Ideas of the scope of protein-film voltammetry are given in the following publications: (a) Armstrong, F. A. Adv. Inorg. Chem. 1992, 38, 117-163. (b) Armstrong, F. A.; Butt, J. N.; Sucheta, A. Methods Enzymol. 1993, 227, 479-500. (c) Armstrong, F. A. Bioelectrochemistry of Biomacromolecules. In Bioelectrochemistry: Principles and Practice, Vol. 5, Lenaz, G., Milazzo, G., Eds.; Birkhauser Verlag: Basel, 1997, Vol. 5, pp 205-255. (d) Armstrong, F. A.; Heering, H. A.; Hirst, J. Chem. Soc. Rev., in press.
5. Examples of endeavors to obtain structurally defined electroactive protein monolayers: Song, S.; Clark, R. A.; Bowden, E. F.; Tarlov, M. J. J. Phys. Chem. 1993, 97, 6564-6572. Feng, Z. Q.; Imabayashi, S.; Kakiuchi, T.; Niki, K. J. Electroanal. Chem. 1995, 394, 149-154.
6. Examples of endeavors to obtain structurally defined electroactive protein monolayers: Song, S.; Clark, R. A.; Bowden, E. F.; Tarlov, M. J. J. Phys. Chem. 1993, 97, 6564-6572. Feng, Z. Q.; Imabayashi, S.; Kakiuchi, T.; Niki, K. J. Electroanal. Chem. 1995, 394, 149-154.
7. For examples of applications of protein-film voltammetry to study labile active sites, see: Butt, J. N.; Sucheta, A.; Martin, L. L.; Shen, B. H.; Burgess, B. K.; Armstrong, F. A. J. Am. Chem. Soc. 1993, 115, 12587-12588. Butt, J. N.; Niles, J.; Armstrong, F. A.; Breton, J.; Thomson, A. J. Nat. Struct. Biol. 1994, 1, 427-433. 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.
8. For examples of applications of protein-film voltammetry to study labile active sites, see: Butt, J. N.; Sucheta, A.; Martin, L. L.; Shen, B. H.; Burgess, B. K.; Armstrong, F. A. J. Am. Chem. Soc. 1993, 115, 12587-12588. Butt, J. N.; Niles, J.; Armstrong, F. A.; Breton, J.; Thomson, A. J. Nat. Struct. Biol. 1994, 1, 427-433. 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.
9. For examples of applications of protein-film voltammetry to study labile active sites, see: Butt, J. N.; Sucheta, A.; Martin, L. L.; Shen, B. H.; Burgess, B. K.; Armstrong, F. A. J. Am. Chem. Soc. 1993, 115, 12587-12588. Butt, J. N.; Niles, J.; Armstrong, F. A.; Breton, J.; Thomson, A. J. Nat. Struct. Biol. 1994, 1, 427-433. 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.
10. Sucheta, A.; Cammack, R.; Weiner, J.; Armstrong, F. A. Biochemistry 1993, 32, 5455-5465. Mondal, M. S.; Fuller, H. A.; Armstrong, F. A. J. Am. Chem. Soc. 1996, 118, 263-264.
11. Sucheta, A.; Cammack, R.; Weiner, J.; Armstrong, F. A. Biochemistry 1993, 32, 5455-5465. Mondal, M. S.; Fuller, H. A.; Armstrong, F. A. J. Am. Chem. Soc. 1996, 118, 263-264.
12. Sucheta, A.; Ackrell, B. A. C.; Cochran, B.; Armstrong, F. A. Nature 1992, 356, 361-362. Ackrell, B. A. C.; Armstrong, F. A.; Cochran, B.; Sucheta, A.; Yu, T. FEBS Lett. 1993, 326, 92-94.
13. Sucheta, A.; Ackrell, B. A. C.; Cochran, B.; Armstrong, F. A. Nature 1992, 356, 361-362. Ackrell, B. A. C.; Armstrong, F. A.; Cochran, B.; Sucheta, A.; Yu, T. FEBS Lett. 1993, 326, 92-94.
14. Hirst J.; Sucheta, A.; Ackrell, B. A. C.; Armstrong, F. A. J. Am. Chem. Soc. 1996, 118, 5031-5038.
15. Ackrell, B. A. C.; Johnson, M. K.; Gunsalus, R. P.; Cecchini, G. In Chemistry & Biochemistry of Flavoenzymes; Müller, F., Ed.; CRC Press: Boca Raton, FL, 1992. Hederstedt, L.; Ohnishi, T. In Molecular Mechanisms in Bioenergetics; Ernster, L., Ed.; Elsevier: New York, 1992; pp 163-198.
16. Ackrell, B. A. C.; Johnson, M. K.; Gunsalus, R. P.; Cecchini, G. In Chemistry & Biochemistry of Flavoenzymes; Müller, F., Ed.; CRC Press: Boca Raton, FL, 1992. Hederstedt, L.; Ohnishi, T. In Molecular Mechanisms in Bioenergetics; Ernster, L., Ed.; Elsevier: New York, 1992; pp 163-198.
17. Catalytic electron transport in bacterial photoreaction centers is limited by the rate of proton transfer to a buried quinone group. Away from conductive water channels, proton transfers are restricted (see ref 9) by the proximity of suitable bases. See: Okamura, M. Y.; Feher, G. Annu. Rev. Biochem. 1992, 61, 861-896. Takahashi, E.; Wraight, C. A. Biochemistry 1992, 31, 855-866.
18. Catalytic electron transport in bacterial photoreaction centers is limited by the rate of proton transfer to a buried quinone group. Away from conductive water channels, proton transfers are restricted (see ref 9) by the proximity of suitable bases. See: Okamura, M. Y.; Feher, G. Annu. Rev. Biochem. 1992, 61, 861-896. Takahashi, E.; Wraight, C. A. Biochemistry 1992, 31, 855-866.
19. The much lower tunneling capability of hydrogen nuclei compared to electrons is an interesting concept, having obvious relevance to complex electron-transport enzymes and is described in articles by Klinman. A convenient comparison uses the de Broglie wavelengths of the two species, that of the electron being approximately 43 times greater than that of the proton, reflecting its much higher ability to tunnel through energy barriers and over larger distances. See for example: Klinman, J. P. Trends Biochem. Sci. 1989, 14, 368-377. Rucker, J., Cha, Y.; Jonsson, T.; Grant, K. L.; Klinman, J. P. Biochemistry 1992, 31, 11489-11499. Bahnson, B. J.; Park, D.-H.; Kim, K.; Plapp, B. V.; Klinman, J. P. Biochemistry 1993, 32, 5503-5507. Jonsson, T.; Edmondson, D. E.; Klinman, J. P. Biochemistry 1994, 33, 14871-14878. Bahnson, B. J.; Klinman, J. P. Methods Enzymol. 1995, 249, 373-397.
20. The much lower tunneling capability of hydrogen nuclei compared to electrons is an interesting concept, having obvious relevance to complex electron-transport enzymes and is described in articles by Klinman. A convenient comparison uses the de Broglie wavelengths of the two species, that of the electron being approximately 43 times greater than that of the proton, reflecting its much higher ability to tunnel through energy barriers and over larger distances. See for example: Klinman, J. P. Trends Biochem. Sci. 1989, 14, 368-377. Rucker, J., Cha, Y.; Jonsson, T.; Grant, K. L.; Klinman, J. P. Biochemistry 1992, 31, 11489-11499. Bahnson, B. J.; Park, D.-H.; Kim, K.; Plapp, B. V.; Klinman, J. P. Biochemistry 1993, 32, 5503-5507. Jonsson, T.; Edmondson, D. E.; Klinman, J. P. Biochemistry 1994, 33, 14871-14878. Bahnson, B. J.; Klinman, J. P. Methods Enzymol. 1995, 249, 373-397.
21. The much lower tunneling capability of hydrogen nuclei compared to electrons is an interesting concept, having obvious relevance to complex electron-transport enzymes and is described in articles by Klinman. A convenient comparison uses the de Broglie wavelengths of the two species, that of the electron being approximately 43 times greater than that of the proton, reflecting its much higher ability to tunnel through energy barriers and over larger distances. See for example: Klinman, J. P. Trends Biochem. Sci. 1989, 14, 368-377. Rucker, J., Cha, Y.; Jonsson, T.; Grant, K. L.; Klinman, J. P. Biochemistry 1992, 31, 11489-11499. Bahnson, B. J.; Park, D.-H.; Kim, K.; Plapp, B. V.; Klinman, J. P. Biochemistry 1993, 32, 5503-5507. Jonsson, T.; Edmondson, D. E.; Klinman, J. P. Biochemistry 1994, 33, 14871-14878. Bahnson, B. J.; Klinman, J. P. Methods Enzymol. 1995, 249, 373-397.
22. The much lower tunneling capability of hydrogen nuclei compared to electrons is an interesting concept, having obvious relevance to complex electron-transport enzymes and is described in articles by Klinman. A convenient comparison uses the de Broglie wavelengths of the two species, that of the electron being approximately 43 times greater than that of the proton, reflecting its much higher ability to tunnel through energy barriers and over larger distances. See for example: Klinman, J. P. Trends Biochem. Sci. 1989, 14, 368-377. Rucker, J., Cha, Y.; Jonsson, T.; Grant, K. L.; Klinman, J. P. Biochemistry 1992, 31, 11489-11499. Bahnson, B. J.; Park, D.-H.; Kim, K.; Plapp, B. V.; Klinman, J. P. Biochemistry 1993, 32, 5503-5507. Jonsson, T.; Edmondson, D. E.; Klinman, J. P. Biochemistry 1994, 33, 14871-14878. Bahnson, B. J.; Klinman, J. P. Methods Enzymol. 1995, 249, 373-397.
23. The much lower tunneling capability of hydrogen nuclei compared to electrons is an interesting concept, having obvious relevance to complex electron-transport enzymes and is described in articles by Klinman. A convenient comparison uses the de Broglie wavelengths of the two species, that of the electron being approximately 43 times greater than that of the proton, reflecting its much higher ability to tunnel through energy barriers and over larger distances. See for example: Klinman, J. P. Trends Biochem. Sci. 1989, 14, 368-377. Rucker, J., Cha, Y.; Jonsson, T.; Grant, K. L.; Klinman, J. P. Biochemistry 1992, 31, 11489-11499. Bahnson, B. J.; Park, D.-H.; Kim, K.; Plapp, B. V.; Klinman, J. P. Biochemistry 1993, 32, 5503-5507. Jonsson, T.; Edmondson, D. E.; Klinman, J. P. Biochemistry 1994, 33, 14871-14878. Bahnson, B. J.; Klinman, J. P. Methods Enzymol. 1995, 249, 373-397.
24. For general books and articles dealing with isotope effects, see, for example: Bell, R. P. The Proton in Chemistry, 2nd ed.; Chapman and Hall: London, 1973. Cleland, W. W. Acc. Chem. Res. 1975, 8, 145-151. More O'Ferrall, R. A. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Albery, W. J. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Isotope Effects on Enzyme-Catalyzed Reactions; Cleland, W. W., O'Leary, M. H., Northrop, D. B., Eds.; University Park Press: Baltimore, 1977. Transition States of Biochemical Processes, Candour, R. D., Schowen, R. L., Eds.; Plenum Press: New York, 1978. Schowen, K. B.; Schowen, R. L. Methods Enzymol. 1982, 87, 551-606. Enzyme Mechanism from Isotope Effects; Cook, P. F., Ed.; CRC Press: Boca Raton, 1991.
25. For general books and articles dealing with isotope effects, see, for example: Bell, R. P. The Proton in Chemistry, 2nd ed.; Chapman and Hall: London, 1973. Cleland, W. W. Acc. Chem. Res. 1975, 8, 145-151. More O'Ferrall, R. A. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Albery, W. J. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Isotope Effects on Enzyme-Catalyzed Reactions; Cleland, W. W., O'Leary, M. H., Northrop, D. B., Eds.; University Park Press: Baltimore, 1977. Transition States of Biochemical Processes, Candour, R. D., Schowen, R. L., Eds.; Plenum Press: New York, 1978. Schowen, K. B.; Schowen, R. L. Methods Enzymol. 1982, 87, 551-606. Enzyme Mechanism from Isotope Effects; Cook, P. F., Ed.; CRC Press: Boca Raton, 1991.
26. For general books and articles dealing with isotope effects, see, for example: Bell, R. P. The Proton in Chemistry, 2nd ed.; Chapman and Hall: London, 1973. Cleland, W. W. Acc. Chem. Res. 1975, 8, 145-151. More O'Ferrall, R. A. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Albery, W. J. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Isotope Effects on Enzyme-Catalyzed Reactions; Cleland, W. W., O'Leary, M. H., Northrop, D. B., Eds.; University Park Press: Baltimore, 1977. Transition States of Biochemical Processes, Candour, R. D., Schowen, R. L., Eds.; Plenum Press: New York, 1978. Schowen, K. B.; Schowen, R. L. Methods Enzymol. 1982, 87, 551-606. Enzyme Mechanism from Isotope Effects; Cook, P. F., Ed.; CRC Press: Boca Raton, 1991.
27. For general books and articles dealing with isotope effects, see, for example: Bell, R. P. The Proton in Chemistry, 2nd ed.; Chapman and Hall: London, 1973. Cleland, W. W. Acc. Chem. Res. 1975, 8, 145-151. More O'Ferrall, R. A. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Albery, W. J. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Isotope Effects on Enzyme-Catalyzed Reactions; Cleland, W. W., O'Leary, M. H., Northrop, D. B., Eds.; University Park Press: Baltimore, 1977. Transition States of Biochemical Processes, Candour, R. D., Schowen, R. L., Eds.; Plenum Press: New York, 1978. Schowen, K. B.; Schowen, R. L. Methods Enzymol. 1982, 87, 551-606. Enzyme Mechanism from Isotope Effects; Cook, P. F., Ed.; CRC Press: Boca Raton, 1991.
28. For general books and articles dealing with isotope effects, see, for example: Bell, R. P. The Proton in Chemistry, 2nd ed.; Chapman and Hall: London, 1973. Cleland, W. W. Acc. Chem. Res. 1975, 8, 145-151. More O'Ferrall, R. A. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Albery, W. J. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Isotope Effects on Enzyme-Catalyzed Reactions; Cleland, W. W., O'Leary, M. H., Northrop, D. B., Eds.; University Park Press: Baltimore, 1977. Transition States of Biochemical Processes, Candour, R. D., Schowen, R. L., Eds.; Plenum Press: New York, 1978. Schowen, K. B.; Schowen, R. L. Methods Enzymol. 1982, 87, 551-606. Enzyme Mechanism from Isotope Effects; Cook, P. F., Ed.; CRC Press: Boca Raton, 1991.
29. For general books and articles dealing with isotope effects, see, for example: Bell, R. P. The Proton in Chemistry, 2nd ed.; Chapman and Hall: London, 1973. Cleland, W. W. Acc. Chem. Res. 1975, 8, 145-151. More O'Ferrall, R. A. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Albery, W. J. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Isotope Effects on Enzyme-Catalyzed Reactions; Cleland, W. W., O'Leary, M. H., Northrop, D. B., Eds.; University Park Press: Baltimore, 1977. Transition States of Biochemical Processes, Candour, R. D., Schowen, R. L., Eds.; Plenum Press: New York, 1978. Schowen, K. B.; Schowen, R. L. Methods Enzymol. 1982, 87, 551-606. Enzyme Mechanism from Isotope Effects; Cook, P. F., Ed.; CRC Press: Boca Raton, 1991.
30. For general books and articles dealing with isotope effects, see, for example: Bell, R. P. The Proton in Chemistry, 2nd ed.; Chapman and Hall: London, 1973. Cleland, W. W. Acc. Chem. Res. 1975, 8, 145-151. More O'Ferrall, R. A. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Albery, W. J. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Isotope Effects on Enzyme-Catalyzed Reactions; Cleland, W. W., O'Leary, M. H., Northrop, D. B., Eds.; University Park Press: Baltimore, 1977. Transition States of Biochemical Processes, Candour, R. D., Schowen, R. L., Eds.; Plenum Press: New York, 1978. Schowen, K. B.; Schowen, R. L. Methods Enzymol. 1982, 87, 551-606. Enzyme Mechanism from Isotope Effects; Cook, P. F., Ed.; CRC Press: Boca Raton, 1991.
31. For general books and articles dealing with isotope effects, see, for example: Bell, R. P. The Proton in Chemistry, 2nd ed.; Chapman and Hall: London, 1973. Cleland, W. W. Acc. Chem. Res. 1975, 8, 145-151. More O'Ferrall, R. A. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Albery, W. J. In Proton Transfer Reactions, Caldin, E. F., Gold, V., Eds.; Chapman and Hall: London, 1975. Isotope Effects on Enzyme-Catalyzed Reactions; Cleland, W. W., O'Leary, M. H., Northrop, D. B., Eds.; University Park Press: Baltimore, 1977. Transition States of Biochemical Processes, Candour, R. D., Schowen, R. L., Eds.; Plenum Press: New York, 1978. Schowen, K. B.; Schowen, R. L. Methods Enzymol. 1982, 87, 551-606. Enzyme Mechanism from Isotope Effects; Cook, P. F., Ed.; CRC Press: Boca Raton, 1991.
32. 2O isotope effects on intramolecular ET in a multicentered flavoenzyme, xanthine oxidase, is described in: Hille, R. Biochemistry 1991, 30, 8522-8529.
33. For further examples of H/D isotope effects on catalysis by complex ET enzymes, see: Batie, C. J.; Kamin, H. J. Biol. Chem. 1984, 259, 11976-11985. Beckmann, J. D.; Frerman, F. E. Biochemistry 1985, 24, 3922-3925. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. D'Ardenne, S. C.; Edmondson, D. E. Biochemistry 1990, 29, 9046-9052. Döring, O.; Böttger, M. Biochem. Biophys. Res. Commun. 1992, 182, 870-876. Aikens, J.; Sligar, S. G. J. Am. Chem. Soc. 1994, 116, 1143-1144. Bishop, G. R.; Davidson, V. L. Biochemistry 1995, 34, 12082-12086. Proshlyakov, D. A.; Ogura, T.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. Biochemistry 1996, 35, 8580-8586. Ogura, T.; Hirota, S.; Proshlyakov, D. A.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. J. Am. Chem. Soc. 1996, 118, 5443-5449.
34. For further examples of H/D isotope effects on catalysis by complex ET enzymes, see: Batie, C. J.; Kamin, H. J. Biol. Chem. 1984, 259, 11976-11985. Beckmann, J. D.; Frerman, F. E. Biochemistry 1985, 24, 3922-3925. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. D'Ardenne, S. C.; Edmondson, D. E. Biochemistry 1990, 29, 9046-9052. Döring, O.; Böttger, M. Biochem. Biophys. Res. Commun. 1992, 182, 870-876. Aikens, J.; Sligar, S. G. J. Am. Chem. Soc. 1994, 116, 1143-1144. Bishop, G. R.; Davidson, V. L. Biochemistry 1995, 34, 12082-12086. Proshlyakov, D. A.; Ogura, T.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. Biochemistry 1996, 35, 8580-8586. Ogura, T.; Hirota, S.; Proshlyakov, D. A.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. J. Am. Chem. Soc. 1996, 118, 5443-5449.
35. For further examples of H/D isotope effects on catalysis by complex ET enzymes, see: Batie, C. J.; Kamin, H. J. Biol. Chem. 1984, 259, 11976-11985. Beckmann, J. D.; Frerman, F. E. Biochemistry 1985, 24, 3922-3925. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. D'Ardenne, S. C.; Edmondson, D. E. Biochemistry 1990, 29, 9046-9052. Döring, O.; Böttger, M. Biochem. Biophys. Res. Commun. 1992, 182, 870-876. Aikens, J.; Sligar, S. G. J. Am. Chem. Soc. 1994, 116, 1143-1144. Bishop, G. R.; Davidson, V. L. Biochemistry 1995, 34, 12082-12086. Proshlyakov, D. A.; Ogura, T.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. Biochemistry 1996, 35, 8580-8586. Ogura, T.; Hirota, S.; Proshlyakov, D. A.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. J. Am. Chem. Soc. 1996, 118, 5443-5449.
36. For further examples of H/D isotope effects on catalysis by complex ET enzymes, see: Batie, C. J.; Kamin, H. J. Biol. Chem. 1984, 259, 11976-11985. Beckmann, J. D.; Frerman, F. E. Biochemistry 1985, 24, 3922-3925. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. D'Ardenne, S. C.; Edmondson, D. E. Biochemistry 1990, 29, 9046-9052. Döring, O.; Böttger, M. Biochem. Biophys. Res. Commun. 1992, 182, 870-876. Aikens, J.; Sligar, S. G. J. Am. Chem. Soc. 1994, 116, 1143-1144. Bishop, G. R.; Davidson, V. L. Biochemistry 1995, 34, 12082-12086. Proshlyakov, D. A.; Ogura, T.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. Biochemistry 1996, 35, 8580-8586. Ogura, T.; Hirota, S.; Proshlyakov, D. A.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. J. Am. Chem. Soc. 1996, 118, 5443-5449.
37. For further examples of H/D isotope effects on catalysis by complex ET enzymes, see: Batie, C. J.; Kamin, H. J. Biol. Chem. 1984, 259, 11976-11985. Beckmann, J. D.; Frerman, F. E. Biochemistry 1985, 24, 3922-3925. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. D'Ardenne, S. C.; Edmondson, D. E. Biochemistry 1990, 29, 9046-9052. Döring, O.; Böttger, M. Biochem. Biophys. Res. Commun. 1992, 182, 870-876. Aikens, J.; Sligar, S. G. J. Am. Chem. Soc. 1994, 116, 1143-1144. Bishop, G. R.; Davidson, V. L. Biochemistry 1995, 34, 12082-12086. Proshlyakov, D. A.; Ogura, T.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. Biochemistry 1996, 35, 8580-8586. Ogura, T.; Hirota, S.; Proshlyakov, D. A.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. J. Am. Chem. Soc. 1996, 118, 5443-5449.
38. For further examples of H/D isotope effects on catalysis by complex ET enzymes, see: Batie, C. J.; Kamin, H. J. Biol. Chem. 1984, 259, 11976-11985. Beckmann, J. D.; Frerman, F. E. Biochemistry 1985, 24, 3922-3925. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. D'Ardenne, S. C.; Edmondson, D. E. Biochemistry 1990, 29, 9046-9052. Döring, O.; Böttger, M. Biochem. Biophys. Res. Commun. 1992, 182, 870-876. Aikens, J.; Sligar, S. G. J. Am. Chem. Soc. 1994, 116, 1143-1144. Bishop, G. R.; Davidson, V. L. Biochemistry 1995, 34, 12082-12086. Proshlyakov, D. A.; Ogura, T.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. Biochemistry 1996, 35, 8580-8586. Ogura, T.; Hirota, S.; Proshlyakov, D. A.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. J. Am. Chem. Soc. 1996, 118, 5443-5449.
39. For further examples of H/D isotope effects on catalysis by complex ET enzymes, see: Batie, C. J.; Kamin, H. J. Biol. Chem. 1984, 259, 11976-11985. Beckmann, J. D.; Frerman, F. E. Biochemistry 1985, 24, 3922-3925. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. D'Ardenne, S. C.; Edmondson, D. E. Biochemistry 1990, 29, 9046-9052. Döring, O.; Böttger, M. Biochem. Biophys. Res. Commun. 1992, 182, 870-876. Aikens, J.; Sligar, S. G. J. Am. Chem. Soc. 1994, 116, 1143-1144. Bishop, G. R.; Davidson, V. L. Biochemistry 1995, 34, 12082-12086. Proshlyakov, D. A.; Ogura, T.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. Biochemistry 1996, 35, 8580-8586. Ogura, T.; Hirota, S.; Proshlyakov, D. A.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. J. Am. Chem. Soc. 1996, 118, 5443-5449.
40. For further examples of H/D isotope effects on catalysis by complex ET enzymes, see: Batie, C. J.; Kamin, H. J. Biol. Chem. 1984, 259, 11976-11985. Beckmann, J. D.; Frerman, F. E. Biochemistry 1985, 24, 3922-3925. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. D'Ardenne, S. C.; Edmondson, D. E. Biochemistry 1990, 29, 9046-9052. Döring, O.; Böttger, M. Biochem. Biophys. Res. Commun. 1992, 182, 870-876. Aikens, J.; Sligar, S. G. J. Am. Chem. Soc. 1994, 116, 1143-1144. Bishop, G. R.; Davidson, V. L. Biochemistry 1995, 34, 12082-12086. Proshlyakov, D. A.; Ogura, T.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. Biochemistry 1996, 35, 8580-8586. Ogura, T.; Hirota, S.; Proshlyakov, D. A.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. J. Am. Chem. Soc. 1996, 118, 5443-5449.
41. For further examples of H/D isotope effects on catalysis by complex ET enzymes, see: Batie, C. J.; Kamin, H. J. Biol. Chem. 1984, 259, 11976-11985. Beckmann, J. D.; Frerman, F. E. Biochemistry 1985, 24, 3922-3925. Okamura, M. Y.; Feher, G. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 8152-8156. D'Ardenne, S. C.; Edmondson, D. E. Biochemistry 1990, 29, 9046-9052. Döring, O.; Böttger, M. Biochem. Biophys. Res. Commun. 1992, 182, 870-876. Aikens, J.; Sligar, S. G. J. Am. Chem. Soc. 1994, 116, 1143-1144. Bishop, G. R.; Davidson, V. L. Biochemistry 1995, 34, 12082-12086. Proshlyakov, D. A.; Ogura, T.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. Biochemistry 1996, 35, 8580-8586. Ogura, T.; Hirota, S.; Proshlyakov, D. A.; Shinzawa-Itoh, K.; Yoshikawa, S.; Kitagawa, T. J. Am. Chem. Soc. 1996, 118, 5443-5449.
42. Studies of organic substrate isotope effects on catalysis by SDH are described in: Vitale, L.; Rittenberg, D. Biochemistry 1967, 6, 690-699. Hollocher, T. C., You, K., Conjalka, M. J. Am. Chem. Soc. 1970, 92, 1032-1035. Kaczorowski, G. J.; Cheung, Y.-F.; Walsh, C. Biochemistry 1977, 16, 2619-2628.
43. Studies of organic substrate isotope effects on catalysis by SDH are described in: Vitale, L.; Rittenberg, D. Biochemistry 1967, 6, 690-699. Hollocher, T. C., You, K., Conjalka, M. J. Am. Chem. Soc. 1970, 92, 1032-1035. Kaczorowski, G. J.; Cheung, Y.-F.; Walsh, C. Biochemistry 1977, 16, 2619-2628.
44. Studies of organic substrate isotope effects on catalysis by SDH are described in: Vitale, L.; Rittenberg, D. Biochemistry 1967, 6, 690-699. Hollocher, T. C., You, K., Conjalka, M. J. Am. Chem. Soc. 1970, 92, 1032-1035. Kaczorowski, G. J.; Cheung, Y.-F.; Walsh, C. Biochemistry 1977, 16, 2619-2628.
45. Glasoe, P. K.; Long, F. A. J. Phys. Chem. 1960, 64, 188-190.
46. 3.
47. Williamson, J. R.; Corkey, B. E. Methods Enzymol. 1969, 13, 463-466.
48. 2O. A linear relationship is expected for the involvement of a single exchangeable proton, a quadratic relationship for two protons etc. (Klinman, J. P. Adv. Enzymol. Relat. Areas Mol. Biol. 1978, 46, 415-494; see also ref 10). The results obtained indicated the possibility of using the voltammetric technique in such a way; however, although the data showed an approximately linear trend the errors were sufficiently significant that curvature could not be excluded.
49. 2O. The basis for this hysteresis is under investigation.
50. lim, 2.00 ± 0.50 (pL 7.4) and 1.90 ± 0.50 (pL 7.8).
51. peak measured for the 100% H system are 18 mV more negative than reported recently in ref 6. This figure lies outside of experimental error and at present we have no satisfactory explanation. The conclusions of these experiments, which directly compare H/D effects in the same system, are not affected.
52. La Mer, V. K.; Korman, S. J. Am. Chem. Soc. 1935, 57, 1511.
53. McDougall, A. O.; Long, F. A. J. Phys. Chem. 1962, 66, 429-433.
54. La Mer, V. K.; Korman, S. Science 1936, 83, 624-626. La Mer, V. K. Chem. Rev. 1936, 19, 363-374.
55. La Mer, V. K.; Korman, S. Science 1936, 83, 624-626. La Mer, V. K. Chem. Rev. 1936, 19, 363-374.
56. 2O). We would however expect this to be a relatively small contribution (<5 mV); see: La Mer, V. K.; Noonan, E. J. Am. Chem. Soc. 1939, 61, 1487-1491. Salomaa, P. Acta Chem. Scand. 1971, 25, 365-366.
57. 2O). We would however expect this to be a relatively small contribution (<5 mV); see: La Mer, V. K.; Noonan, E. J. Am. Chem. Soc. 1939, 61, 1487-1491. Salomaa, P. Acta Chem. Scand. 1971, 25, 365-366.
58. Enzyme Structure and Mechanism; Fersht, A.; W. H. Freeman and Co.: New York, 1985.