Direct immobilization of native yeast iso-1 cytochrome c on bare gold: Fast electron relay to redox enzymes and zeptomole protein-film voltammetry

Journal of the American Chemical Society

Volumn 126, Issue 35, 2004, Pages 11103-11112

  Heering, Hendrik A ^a,b   Wiertz, Frank G M ^a   Dekker, Cees ^b   De Vries, Simon ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON TRANSFER; GOLD ELECTRODES;

CHEMISORPTION; DENITRIFICATION; ELECTRODES; ENZYMES; GOLD; YEAST;

ENZYME IMMOBILIZATION;

CYTOCHROME C; CYTOCHROME C PEROXIDASE; CYTOCHROME CD1; GOLD; ISOCYTOCHROME C1; NITRIC OXIDE REDUCTASE; NITRITE; NITRITE REDUCTASE; UNCLASSIFIED DRUG;

ADSORPTION; ARTICLE; ATOMIC FORCE MICROSCOPY; CATALYSIS; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; ELECTROCHEMISTRY; ELECTRON TRANSPORT; ENZYME IMMOBILIZATION; MICROELECTRODE; NONHUMAN; OXIDATION REDUCTION REACTION; PARACOCCUS DENITRIFICANS; SACCHAROMYCES CEREVISIAE;

CATALYSIS; CYTOCHROMES C; ELECTROCHEMISTRY; ENZYMES, IMMOBILIZED; GOLD; KINETICS; MICROSCOPY, ATOMIC FORCE; OXIDATION-REDUCTION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPECTROSCOPY, NEAR-INFRARED;

EID: 4444287592     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja046737w     Document Type: Article

References (114)

1. (a) Arsmtrong, F. A.; Wilson, G. S. Electrochim. Acta 2000, 45, 2623-2645.
2. (b) Fedurco, M. Coord. Chem. Rev. 2000, 209, 263-331.
3. (c) Willner, I.; Katz, E. Angew. Chem., Int. Ed. 2000, 39, 1180-1218.
4. (d) Chaki, N. K.; Vijayamohanan, K. Biosens. Bioelectron. 2002, 17, 1-12.
5. (e) Zu, Y. B.; Shannon, R. J.; Hirst, J. J. Am. Chem. Soc. 2003, 125, 6020-6021.
6. (a) Armstrong, F. A.; Heering, H. A.; Hirst, J. Chem. Soc. Rev. 1997, 26, 169-179.
7. (b) Anderson, L. J.; Richardson, D. J.; Butt, J. N. Faraday Discuss. 2000, 116, 155-169.
8. (c) Angove, H. C.; Cole, J. A.; Richardson, D. J.; Butt, J. N. J. Biol. Chem. 2002, 277, 23374-23381.
9. (d) Armstrong, F. A. J. Chem. Soc., Dalton Trans. 2002, 661-671.
10. (e) Elliott, S. J.; Léger, C.; Pershad, H. R.; Hirst, J.; Heffron, K.; Ginet, N.; Blasco, F.; Rothery, R. A.; Weiner, J. H.; Armstrong, F. A. Biochim. Biophys. Acta 2002, 1555, 54-59.
11. (f) Leger, C.; Elliott, S. J.; Hoke, K. R.; Jeuken, L. J. C.; Jones, A. K.; Armstrong, F. A. Biochemistry 2003; 42, 8653-8662.
12. (g) Liu, H. H.; Pang, D. W. Prog. Chem. 2002, 14, 425-432.
13. (h) Elliott, S. J.; Hoke, K. R.; Heffron, K.; Palak, M.; Rothery, R. A.; Weiner, J. H.; Armstrong, F. A. Biochemistry 2004, 43, 799-807.
14. (i) Frangioni, B.; Arnoux, P.; Sabaty, M.; Pignol, D.; Bertrand, P.; Guigliarelli, B.; Léger, C. J. Am. Chem. Soc. 2004, 126, 1328-1329.
15. Heering, H. A.; Hirst, J.; Armstrong, F. A. J. Phys. Chem. B 1998, 102, 6889-6902.
16. Scott, D. L.; Paddock, R. M.; Bowden, E. F. J. Electroanal. Chem. 1992, 341, 307-321.
17. Mondal, M. S.; Fuller, H. A.; Armstrong, F. A. J. Am. Chem. Soc. 1996, 118, 263-264.
18. Mondal, M. S.; Goodin, D. B.; Armstrong, F. A. J. Am. Chem. Soc. 1998, 120, 6270-6276.
19. (a) Moreno, C.; Franco, R.; Moura, I.; Legall, J.; Moura, J. J. G. Eur. J. Biochem. 1993, 217, 981-989.
20. (b) Amine, A.; Deni, J.; Kauffmann, J. M. Bioelectrochem. Bioenerg. 1994, 34, 123-128.
21. (c) Verhagen, M. F. J. M.; Wolbert, R. B. G.; Hagen, W. R. Eur. J. Biochem. 1994, 221, 821-829.
22. (d) Willner, I.; Katz, E.; Willner, B.; Blonder, R.; HelegShabtai, V.; Buckmann, A. F. Biosens. Bioelectron. 1997, 12, 337-356.
23. (e) Jin, W.; Wollenberger, U.; Kärgel, E.; Schunck, W.-H.; Scheller, F. W. J. Electroanal. Chem. 1997, 433, 135-139.
24. (f) Abass, A. K.; Hart, J. P.; Cowell, D. Sens. Actuators, B 2000, 62, 148-153.
25. (g) Fridman, V.; Wollenberger, U.; Bogdanovskaya, V.; Lisdat, F.; Ruzgas, T.; Lindgren, A.; Gorton, L.; Scheller, F. W. Biochem. Soc. Trans. 2000, 28, 63-70.
26. (h) Wirtz, M.; Klucik, J.; Rivera, M. J. Am. Chem. Soc. 2000, 122, 1047-1056.
27. (i) Liu, H.; Hill, H. A. O.; Chapman, S. K. J. Electroanal. Chem. 2001, 500, 598-603.
28. (j) Lopes, H.; Besson, S.; Moura, I.; Moura, J. J. G. J. Biol. Inorg. Chem. 2001, 6, 55-62.
29. (k) Takagi, K.; Yamamoto, K.; Kano, K.; Ikeda, T. Eur. J. Biochem. 2001, 268, 470-476.
30. (l) Lojou, E.; Cutruzzola, F.; Tegoni, M.; Bianco, P. Electrochim. Acta 2003, 48, 1055-1064.
31. (m) Okuda, J.; Wakai, J.; Yuhashi, N.; Sode, K. Biosens. Bioelectron. 2003, 18, 699-704.
32. Pardo-Yissar, V.; Katz, E.; Willner, I.; Kotlyar, A. B.; Sanders, C.; Lill, H. Faraday Discuss. 2000, 116, 119-134.
33. Haas, A. S.; Pilloud, D. L.; Reddy, K. S.; Babcock, G. T.; Moser, C. C.; Blasie, J. K.; Dutton, P. L. J. Phys. Chem. B 2001, 105, 11351-11362.
34. (a) Döpner, S.; Hildebrandt, P.; Rosell, F. I.; Mauk, A. G. J. Am. Chem. Soc. 1998, 120, 11246-11255.
35. (b) Chen, X. X.; Ferrigno, R.; Yang, J.; Whitesides, G. A. Langmuir 2002, 18, 7009-7015.
36. (c) Wackerbarth, H.; Hildebrandt, P. ChemPhysChem 2003, 4, 714-724.
37. (a) Hirota, S.; Hayamizu, K.; Endo, M.; Hibino, T.; Takabe, T.; Kohzuma, T.; Yamauchi, O. J. Am. Chem. Soc. 1998, 120, 8177-8183.
38. (b) Rivera, M.; Seetharaman, R.; Girdhar, D.; Wirtz, M.; Zhang, X. J.; Wang, X. Q.; White, S. Biochemistry 1998, 37, 1485-1494.
39. (c) Johnson, D. L.; Maxwell, C. J.; Losic, D.; Shapter, J. G.; Martin, L. L. Bioelectrochem. 2002, 58, 137-147.
40. Baymann, F.; Barlow, N. L.; Aubert, C.; Schoepp-Cothenet, B.; Leroy, G.; Armstrong, F. A. FEES Lett. 2003, 539, 91-94.
41. Louie, G. V.; Brayer, G. D. J. Mol. Biol. 1990, 214, 527-555.
42. Moench, S. J.; Satterlee, J. D. J. Biol. Chem. 1989, 264, 9923-9931.
43. Pelletier, H.; Kraut, J. Science 1992, 258, 1748-1755.
44. Worrall, J. A. R.; Kolczak, U.; Canters, G. W.; Ubbink, M. Biochemistry 2001, 40, 7069-7076.
45. (a) Hunte, C.; Solmaz, S.; Lange, C. Biochim. Biophys. Acta 2002, 1555, 21-28.
46. (b) Lange, C.; Hunte, C. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 2800-2805.
47. Döpner, S.; Hildebrandt, P.; Rosell, F. I.; Mauk, A. G.; von Walter, M.; Buse, G.; Soulimane, T. Eur. J. Biochem. 1999, 261, 379-391.
48. (a) Roberts, V. A.; Pique, M. E. J. Biol. Chem. 1999, 274, 38051-38060.
49. (b) Flöck, D.; Helms, V. Proteins 2002, 47, 75-85.
50. Kotlyar, A.; Borovok, N.; Hazani, M.; Szundi, I.; Einarsdóttir, Ó. Eur. J. Biochem. 2000, 267, 5805-5809.
51. (a) Wood, L. L.; Cheng, S.-S.; Edmiston, P. L.; Saavedra, S. S. J. Am. Chem. Soc. 1997, 119, 571-576.
52. (b) Edmiston, P. L.; Saavedra, S. S. Biophys. J. 1998, 74, 999-1006.
53. (c) Edwards, A. M.; Zhang, K.; Nordgren, C. E.; Blasie, J. K. Biophys. J. 2000, 79, 3105-3117.
54. (d) Tronin, A.; Edwards, A. M.; Wright, W. W.; Vanderkooi, J. M.; Blasie, J. K. Biophys. J. 2002, 52, 996-1003.
55. Taking 1YCC (ref 13) as the starting point, reorientation of the three C-terminal amino acids Ala101, Cys102, and Glu103, avoiding overlapping van der Waals radii, results in a surface-exposed thiol at a distance of ∼1.6 nm from the burned heme edge. Experimentally, a distance >1.5 nm between the heme and a spin label attached to Cys102 has been found: Qu, K. B.; Vaughn, J. L.; Sienkiewicz, A.; Scholes, C. P.; Fetrow, J. S. Biochemistry 1997, 36, 2884-2897.
56. Page, C. C.; Moser, C. C.; Chen, X.; Dutton, P. L. Nature 1999, 402, 47-51.
57. (a) Hansen, A. G.; Boisen, A.; Nielsen, J. U.; Wackerbarth, H.; Chorkendorff, I.; Andersen, J. E. T.; Zhang, J. D.; Ulstrup, J. Langmuir 2003, 19, 3419-3427.
58. (b) Zhang, J. D.; Grubb, M.; Hansen, A. G.; Kuznetsov, A. M.; Boisen, A.; Wackerbarth, H.; Ulstrup, J. J. Phys.: Condens. Matter 2003, 15, S1873-S1890.
59. Bonanni, B.; Alliata, D.; Bizzarri, A. R.; Cannistraro, S. ChemPhysChem 2003, 4, 1183-1188.
60. Girsch, P.; de Vries, S. Biochim. Biophys. Acta 1997, 1318, 202-216.
61. Moir, J. W. B.; Baratta, D.; Richardson, D. J.; Ferguson, S. J. Eur. J. Biochem. 1993, 212, 377-385.
62. Lide, D. L., Ed. Handbook of Chemistry and Physics, 81st ed.; CRC Press LLC: Boca Raton, FL, 2000.
63. Hagen, W. R. Eur. J. Biochem. 1989, 182, 523-530.
64. Heering, H. A.; Mondal, M. S.; Armstrong, F. A. Anal. Chem. 1999, 71, 174-182.
65. Press, W. H.; Flannery, B. P.; Teukolsky, S. A.; Vetterling, W. T. Numerical Recipes in Pascal; Cambridge University Press: New York, 1989.
66. Eddowes, M. J.; Hill, H. A. O. J. Chem. Soc., Chem. Commun. 1977, 771-772.
67. Terrettaz, S.; Chun, J.; Miller, C. J. J. Am. Chem. Soc. 1996, 118, 7857-7858.
68. (a) Rafferty, S. P.; Pearce, L. L.; Barker, P. D.; Guillemette, J. G.; Kay, C. M.; Smith, M.; Mauk, A. G. Biochemistry 1990, 29, 9365-9369.
69. (b) Davies, A. M.; Guillemette, J. G.; Smith, M.; Greenwood, C.; Thurgood, A. G. P.; Mauk, A. G.; Moore, G. R. Biochemistry 1993, 32, 5431-5435.
70. (c) Pollock, W. B. R.; Resell, F. I.; Twitchett, M. B.; Dumont, M. E.; Mauk, A. G. Biochemistry 1998, 37, 6124-6131.
71. (d) Lett, C. M.; Guillemette, J. G. Biochem. J. 2002, 362, 281-287.
72. El Kasmi, A.; Leopold, M. C.; Galligan, R.; Robertson, R. T.; Saavedra, S. S.; El Kacemi, K.; Bowden, E. F. Electrochem. Commun. 2002, 4, 177-181.
73. Feldberg, S. W.; Rubinstein, I. J. Electroanal. Chem. 1988, 240, 1-15.
74. Armstrong, F. A.; Camba, R.; Heering, H. A.; Hirst, J.; Jeuken, L. J. C.; Jones, A. K.; Léger, C.; McEvoy, J. P. Faraday Discuss. 2000, 116, 191-203.
75. Jeuken, L. J. C. Biochim. Biophys. Acta 2003, 1604, 67-76.
76. Bard, A. J.; Faulkner, L. R. Electrochemical Methods: Fundamentals and Applications, 2nd ed.; John Wiley & Sons: New York, 2001.
77. Battistuzzi, G.; Borsari, M.; Sola, M. Eur. J. Inorg. Chem. 2001, 2989-3004.
78. Delauder, S. F.; Mauro, J. M.; Poulos, T. L.; Williams, J. C.; Schwarz, F. P. Biochem. J. 1994, 302, 437-442.
79. Goodin, D. B.; Davidson, M. G.; Roe, J. A.; Mauk, A. G.; Smith, M. Biochemistry 1991, 30, 4953-4962.
80. Villegas, J. A.; Mauk, A. G.; Vazquez-Duhalt, R. Chem. Biol. 2000, 7, 237-244.
81. Baker, S. C.; Saunders, N. F. W.; Willis, A. C.; Ferguson, S. J.; Hajdu, J.; Fülöp, V. J. Mol. Biol. 1997, 269, 440-455.
82. Richter, C. D.; Allen, J. W. A.; Higham, C. W.; Koppenhöfer, A.; Zajicek, R. S.; Watmough, N. J.; Ferguson S. J. J. Biol. Chem. 2002, 277, 3093-3100.
83. Wasser, I. M.; de Vries, S.; Moënne-Loccoz, P.; Schröder, I.; Karlin K. D. Chem. Rev. 2002, 102, 1201-1234.
84. Zumft, W. G. Microbiol. Mol. Biol. Rev. 1997, 61, 533-616.
85. (a) Subtraction of a bare gold electrode blank is not sufficient for analysis because slight differences after polishing and cleaning yield differences in the background current that are relatively small, yet many times larger than the YCC peaks.
86. (b) The voltammograms in the presence of enzyme and substrate are noisier as compared to the background. In part, this is expected because of the difference in the number of averaged traces (3 versus 10). Additional noise is probably generated by small fluctuations in the diffusion profile due to the long time-scale of the measurement.
87. Barker, P. D.; Bertini, I.; Del Conte, R.; Ferguson, S. J.; Hajieva, P.; Tomlinson, E.; Turano, P.; Viezzoli, M. S. Eur. J. Biochem. 2001, 268, 4468-4476.
88. Pyka, J.; Osyczka, A.; Turyna, B.; Blicharski, W.; Froncisz, W. Eur. Biophys. J. 2001, 30, 367-373.
89. Marcus, R. A.; Sutin, N. Biochim. Biophys. Acta 1985, 811, 265-322.
90. Gray, H. B.; Winkler, J. R. J. Electroanal. Chem. 1997, 438, 43-47.
91. (a) Moser, C. C.; Keske, J. M.; Warncke, K.; Farid, R. S.; Dutton, P. L. Nature 1992, 355, 796-802.
92. (b) Gray, H. B.; Winkler, J. R. Annu. Rev. Biochem. 1996, 65, 537-561.
93. (c) Moser, C. C.; Page, C. C.; Chen, X.; Dutton, P. L. J. Biol. Inorg. Chem. 1997, 2, 393-398.
94. (d) Winkler, J. R.; Gray, H. B. J. Biol. Inorg. Chem. 1997, 2, 399-404.
95. (a) Chidsey, C. E. D. Science 1991, 251, 919-922.
96. (b) Chidsey, C. E. D. Science 1991, 252, 631.
97. Honeychurch, M. J. Langmuir 1999, 15, 5158-5163.
98. Adams, D. M.; Brus, L.; Chidsey, C. E. D.; Creager, S.; Creutz, C.; Kagan, C. R.; Kamat, P. V.; Lieberman, M.; Lindsay, S.; Marcus, R. A.; Metzger, R. M.; Michel-Beyerle, M. E.; Miller, J. R.; Newton, M. D.; Rolison, D. R.; Sankey, O.; Schanze, K. S.; Yardley, J.; Zhu, X. J. Phys. Chem. B 2003, 107, 6668-6697.
99. Two major differences with the single donor-acceptor model are noted: because all levels contribute, the inverted regions of the individual levels are compensated and do not appear in the total rate constant. Furthermore, the reorganization energy is associated with the half-reaction of the redox center only, because the electrode does not contribute to it.
100. For equine cytochrome c, electrostatically adsorbed with the heme cleft towards a carboxyl-terminated self-assembled monolayer on gold, Murgida and Hildebrandt reported that the reorganization energy is 0.22 eV, which is substantially lower as compared to that in solution due to exclusion of water: (a) Murgida, D. H.; Hildebrandt, P. J. Phys. Chem. B 2002, 106, 12814-12819.
101. (b) Hildebrandt, P.; Murgida, D. H. Bioelectrochem. 2002, 55, 139-143. However, because in our system the heme cleft is facing the solution, we assume that the reorganization energy is equal to that of YCC in solution.
102. -1 for ferrocene-terminated alkanethiols studied by Chidsey (ref 54).
103. -1 for ferrocene-terminated alkanethiols studied by Chidsey (ref 54).
104. (a) Xie, A.; van der Meer, L.; Austin, R. H. J. Biol. Phys. 2002, 28, 147-154.
105. (b) Morita, T.; Kimura, S. J. Am. Chem. Soc. 2003, 125, 8732-8733.
106. Zheng, J. W.; Ye, S. Y.; Lu, T. H.; Cotton, T. M.; Chumanov, G. Biopolymers 2000, 57, 77-84.
107. Fulop, V.; Moir, J. W. B.; Ferguson, S. J.; Hajdu, J. Cell 1995, 81, 369-377.
108. Koppenhöfer, A.; Turner, K. L.; Allen, J. W. A.; Chapman, S. K.; Ferguson, S. J. Biochemistry 2000, 39, 4243-4249.
109. Blatt, Y.; Pecht, I. Biochemistry 1979, 18, 2917-2922.
110. Farver, O.; Kroneck, P. M. H.; Zumft, W. G.; Pecht, I. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 7622-7625.
111. (a) Grönberg, K. L. C.; Roldán, M. D.; Prior, L.; Butland, G.; Cheesman, M. R.; Richardson, D. J.; Spiro, S.; Thomson, A. J.; Watmough, N. J. Biochemistry 1999, 38, 13780-13786.
112. (b) Field, S. J.; Prior, L.; Roldan, M. D.; Cheesman, M. R.; Thomson, A. J.; Spiro, S.; Butt, J. N.; Watmought, N. J.; Richardson, D. J. J. Biol. Chem. 2002, 277, 20146-20150.
113. (a) Moënne-Loccoz, P.; de Vries, S. J. Am. Chem. Soc. 1998, 120, 5147-5152.
114. (b) Moënne-Loccoz, P.; Richter, O. M. H.; Huang, H. W.; Wasser, I. M.; Ghiladi, R. A.; Karlin, K. D.; de Vries, S. J. Am. Chem. Soc. 2000, 122, 9344-9345.