Spectroscopy of mixed-valence Cu(A)-type centers: Ligand-field control of ground-state properties related to electron transfer

Journal of the American Chemical Society

Volumn 120, Issue 21, 1998, Pages 5246-5263

  Gamelin, Daniel R ^a   Randall, David W ^a   Hay, Michael T ^b   Houser, Robert P ^c   Mulder, Ton C ^d   Canters, Gerard W ^e   De Vries, Simon ^d   Tolman, William B ^c   Lu, Yi ^b   Solomon, Edward I ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c University of Minnesota ^*  (United States)

^d DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^e LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMICYANIN; AZURIN; DIMER; PROTEIN;

ARTICLE; BACILLUS SUBTILIS; CIRCULAR DICHROISM; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; MODEL; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PSEUDOMONAS AERUGINOSA; RAMAN SPECTROMETRY; SPECTROSCOPY; THIOBACILLUS;

EID: 0032479015     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja973161k     Document Type: Article

References (99)

1. Babcock, G. T.; Wikström, M. Nature 1992, 356, 301-307.
2. Chan, S. I.; Li, P. M. Biochemistry 1990, 29, 1-12.
3. Kroneck, P. M. H.; Antholine, W. E.; Riester, J.; Zumft, W. G. FEBS Lett. 1988, 242, 70-74.
4. Scott, R. A.; Zumft, W. G.; Coyle, C. L.; Dooley, D. M. Proc. Natl. Acad. Sci. U.S.A. 1989, 86, 4082-4086.
5. Antholine, W. E.; Kastrau, D. H. W.; Steffens, G. C. M.; Buse, G.; Zumft W. G.; Kroneck, P. M. H. Eur. J. Biochem 1992, 209, 875-881.
6. Zumft, W. G.; Dreusch, A.; Loechelt, S.; Cuypers, H.; Friedrich, B.; Schneider, B. Eur. J. Biochem. 1992, 208, 31-40.
7. Vängård, T. In Copper Proteins; Swartz, H. M., Bolton, J. R., Borg, D. C., Eds.; Wiley & Sons: New York, 1972; pp 411-447.
8. Peisach, J.; Blumberg, W. E. Arch. Biochim. Biophys. 1974, 165, 691-708.
9. Greenwood, C.; Hill, B. C.; Barber, D.; Eglinton, D. G.; Thomson, A. J. Biochem. J. 1983, 215, 303-316.
10. Hoffman, B. M.; Roberts, J. E.; Swanson, M.; Speck, S. H.; Margoliash, E. Proc. Natl. Acad. Sci. U.S.A. 1980, 77, 1452-1456.
11. Stevens, T. H.; Martin, C. T.; Wang, H.; Brudvig, G. W.; Scholes, C. P.; Chan, S. I. J. Biol. Chem. 1982, 257, 12106-12113.
12. Blackburn, N. J.; Barr, M. E.; Woodruff, W. H.; van der Oost, J.; de Vries, S. Biochemistry 1994, 33, 10401-10407.
13. Blackburn, N. J.; de Vries, S.; Barr, M. E.; Houser, R. P.; Tolman, W. B.; Sanders, D.; Fee, J. A. J. Am. Chem. Soc. 1997, 119, 6135-6143.
14. Iwata, S.; Ostermeier, C.; Ludwig, B.; Michel, H. Nature 1995, 376, 660-669.
15. Tsukihara, T.; Aoyama, H.; Yamashita, E.; Tomizaki, T.; Yamaguchi, H.; Shinzawa-Itoh, K.; Nakashima, R.; Yaono, R.; Yoshikawa, S. Science 1996, 272, 1136-1144.
16. Tsukihara, T.; Aoyama, H.; Yamashita, E.; Tomizaki, T.; Yamaguchi H.; Shinzawa-Itoh, K.; Nakashima, R.; Yaono, R.; Yoshikawa, S. Science 1995, 269, 1069-1074.
17. Andrew, C. R.; Fraczkiewicz, R.; Czemuszewicz, R. S.; Lappalainen, P.; Saraste, M.; Sanders-Loehr, J. J. Am. Chem. Soc. 1996, 118, 10436-10445.
18. Speno, H.; Taheri, M. R., Sieburth, D.; Martin, C. T. J. Biol. Chem. 1995, 270, 25363-25369.
19. Zickermann, V.; Verkhovsky, M.; Morgan, J.; Wikström M.; Anemueller, S.; Bill, E.; Steffens, G. C. M.; Ludwig, B. Eur. J. Biochem. 1995, 234, 686-693.
20. Zickermann, V.; Wittershagen, A.; Kolbesen, B. O.; Ludwig, B. Biochemists 1997, 36, 3232-3236.
21. Kelly, M.; Lappalainen, P.; Talbo, G.; Haltia, T.; van der Oost, J.; Saraste, M. J. Biol. Chem. 1993, 268, 16781-16787.
22. Farrar, J. A.; Lappalainen, P.; Zumft, W. G.; Saraste, M.; Thomson, A. J. Eur. J. Biochem. 1995, 232, 294-303.
23. Andrew, C. R.; Lappalainen, P.; Saraste, M.; Hay, M. T.; Lu, Y.; Dennison, C.; Canters, G. W.; Fee, J. A.; Nakamura, N.; Sanders-Loehr, J. J. Am. Chem. Soc. 1995, 117, 10759-10760.
24. Andrew, C. R.; Han, J.; de Vries, S.; van der Oost, J.; Averill, B. A.; Loehr, T. M.; Sanders-Loehr, J. J. Am. Chem. Soc. 1994, 116, 10805-10806.
25. Martin, C. T.; Scholes, C. P.; Chan, S. I. J. Biol. Chem. 1988, 263, 8420-8429.
26. Fan, C.; Bank, J. F.; Dorr, R. G.; Scholes, C. P. J. Biol. Chem. 1988, 263, 3588-3591.
27. Hansen, A. P.; Britt, R. D.; Klein, M. P.; Bender, C. J.; Babcock, G. T. Biochemistry 1993, 32, 13718-13724.
28. Gurbiel, R. J.; Fann, Y. C.; Surerus, K. K.; Werst, M. M.; Musser, S. M.; Doan, P. E.; Chan, S. I.; Fee, J. A.; Hoffman, B. M. J. Am. Chem. Soc. 1993, 115, 10888-10894.
29. Bertini, I.; Bren, K. L.; Clemente, A.; Fee, J. A.; Gray H. B.; Luchinat, C.; Malmström, B. G.; Richards, J. H.; Sanders, D.; Slutter, C. E. J. Am. Chem. Soc. 1996, 118, 11658-11659.
30. Dennison, C.; Berg, A.; Canters, G. W. Biochemistry 1997, 36, 3262-3269.
31. Kroneck, P. M. H.; Antholine, W. A.; Riester, J.; Zumft, W. G. FEBS Lett. 1989, 248, 212-213.
32. Neese, F.; Zumft, W. G.; Antholine, W. E.; Kroneck, P. M. H. J. Am. Chem. Soc. 1996, 118, 8692-8699.
33. Karpefors, M.; Slutter, C. E.; Fee, J. A.; Aasa, R.; Ksellebring, B.; Larsson, S.; Vaenngaard, T. Biophys. J. 1996, 71, 2823-2829.
34. Farrar, J. A.; Neese, F.; Lappalainen, P.; Kroneck, P. M. H.; Saraste, M.; Zumft, W. G.; Thomson, A. J. J. Am. Chem. Soc. 1996, 118, 11501-11514.
35. Williams, K. R., Gamelin, D. R.; LaCroix, L. B.; Houser, R. P.; Tolman, W. B.; Mulder, T. C.; de Vries, S.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1997, 119, 613-614.
36. Larsson, S.; Kaellebring, B.; Wittung, P.; Malmström, B. G. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 7167-7171.
37. Neese, F.; Kappl, R.; Zumft, W. G.; Hüttermann, J.; Kroneck, P. M. H. J. Biol. Inorg. Chem. 1998, 3, 53-67.
38. von Wachenfeldt, C.; de Vries, S.; van der Oost, J. FEBS Lett. 1994, 340, 109-113.
39. Lappalainen, P.; Aasa, R.; Malmström, B. G.; Saraste, M. J. Biol. Chem. 1993, 268, 26416-26421.
40. Slutter, C. E.; Sanders, D.; Wittung, P.; Malmström, B. G.; Aasa, R.; Richards, J. H.; Gray, H. B.; Fee, J. A. Biochemistry 1996, 35, 3387-3395.
41. Zumft, W. G.; Viebrock-Sambale, A.; Braun, C. Eur. J. Biochem. 1990, 192, 591-599.
42. Houser, R. P.; Young, V. G., Jr.; Tolman, W. B. J. Am. Chem. Soc. 1996, 118, 2101-2102.
43. Hay, M.; Richards, J.; Lu, Y. Proc Natl. Acad. Sci. U.S.A. 1996, 93, 461-464.
44. Dennison, C.; Vijgenboom, E.; de Vries, S.; van der Oost, J.; Canters, G. W. FEBS Lett. 1995, 365, 92-94.
45. van der Oost, J.; Lappalainen, P.; Musacchio, A.; Warne, A.; Lemieux, L.; Rumbley, J.; Gennis, J. B.; Aasa, R.; Pascher, T.; Malmström, B. G.; Saraste, M. EMBO J. 1992, 11, 3209.
46. Wilmanns, M.; Lappalainen, P.; Kelly, M.; Sauer-Eriksson, E.; Saraste, M. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 11955-11959.
47. Houser, R. P.; Halfen, J. A.; Young, V. G., Jr.; Blackburn, N. J.; Tolman, W. B. J. Am. Chem. Soc. 1995, 117, 10745-10746.
48. (a) Cook, M.; Case, D. A. QCPE 1991, 23 465.
49. (b) Schwartz, K. Phys. Rev. B 1972, 5, 2466-2468.
50. Gewirth, A. A.; Solomon, E. I. J. Am. Chem. Soc. 1988. 110, 3811-3819.
51. Abola, E. E.; Bernstein, F. C.; Bryant, S. H.; Koetzle, T. F.; Weng, J. In Crystallographic Databases - Information Content, Software Systems, Scientific Applications; Allen, F. H., Bergerhoff, G., Sievers, R., Eds.; Data Commission of the International Union of Crystallography: Bonn, 1987; pp 107-132.
52. Bernstein, F. C.; Koetzle, T. F.; Williams, G. J. B.; E. F. Meyer, J.; Brice, M. D.; Rodgers, J. R.; Kennard, O.; Shimanouchi, T.; Tasumi, M. J. Mol. Biol. 1977, 112, 535-542.
53. Average metrical parameters of the two crystallographically distinct MV structures were used.
54. Gamelin, D. R.; Randall, D. W.; Hay, M. T.; Houser, R. P.; Mulder, T. C.; Canters, G. W.; de Vries, S.; Tolman, W. B.; Lu, Y.; Solomon, E. I., unpublished results.
55. Albright, T. A.; Burdett, J. K.; Whangbo, M.-H. Orbital Interactions in Chemistry; Wiley & Sons: New York, 1985.
56. Hay, P. J.; Thibeault, J. C.; Hoffmann, R. J. Am. Chem. Soc. 1975, 97, 4884-4899.
57. Gamelin, D. R.; Bominaar, E. L.; Mathomère, C.; Kirk, M. L.; Wieghardt, K.; Girerd, J.-J.; Solomon, E. I. Inorg. Chem. 1996, 35, 4323-4335.
58. Gamelin, D. R.; Bominaar, E. L.; Kirk, M. L.; Wieghardt, K.; Solomon, E. I. J. Am. Chem. Soc. 1996, 118, 8085-8097.
59. Wallace-Williams, S. E.; James, C. A.; de Vries S.; Saraste M.; Lappalainen, P.; van der Oost, J.; Fabian, M.; Palmer, G.; Woodruff, W. H. J. Am. Chem. Soc. 1996, 118, 3986-3987.
60. Hughey, J. L. I.; Fawcett, T. G.; Rudich, S. M.; Lalancette, R. A.; Potenza, J. A.; Schugar, H. J. J. Am. Chem. Soc. 1979, 101, 2617-2623.
61. Shadle, S. E.; Penner-Hahn, J. E.; Schugar, H. J.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1993, 115, 767-776.
62. Solomon, E. I.; Baldwin, M. J.; Lowery, M. D. Chem. Rev. 1992, 92, 521-542.
63. Reister, J.; Kroneck, P. M. H.; Zumft, W. G. Eur. J. Biochem. 1989, 178, 751-762.
64. Morgan, J. E.; Wilkström, M. Biochemistry 1991, 30, 948-958.
65. Sequence numbering scheme from bovine heart CcO (refs 15 and 16, PDB 1OCC).
66. Ramirez, B. E.; Malmström, B. G.; Winkler, J. R.; Gray, H. B. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 11949-11951.
67. Schugar, H. J. In Copper Coordination Chemistry: Biochemical and Inorganic Perspectives; Karlin, K. D., Zubieta, J., Eds.; Adenine Press: New York, 1982; pp 43-74.
68. Mulliken, R. S.; Person, W. B. Molecular Complexes; Wiley-Interscience: New York, 1969.
69. Metal-metal overlap is not considered to contribute the majority of intensity to these bands. The metal-metal contribution to the CT intensity is estimated to be less than half of the intensity of band 3 in Figure 1.
70. 74 although other structural changes may also contribute (vide infra).
71. 43
72. Piepho, S. B.; Schatz, P. N. Group Theory in Spectroscopy; Wiley-Interscience: New York, 1983.
73. Rivoal, J. C.; Briat, B. Mol. Phys. 1974, 27, 1081-1108.
74. Gerstman, B. S.; Brill, A. S. J. Chem. Phys. 1985, 82, 1212-1230.
75. Hay, M. T.; Ang, M. C.; Gamelin, D. R.; Solomon, E. I.; Antholine, W. T.; Blackburn, N. J.; Massey, P. D.; Kwon, A. H.; Lu, Y. Inorg. Chem. 1998, 37, 191-198.
76. Warshel, A. Annu. Rev. Biophys. Bioeng. 1977, 6, 273-300.
77. Warshel, A.; Dauber, P. J. Chem. Phys. 1977, 66, 5477-5488.
78. Blazej, D. C.; Peticolas, W. L. Proc. Natl. Acad. Sci. U.S.A. 1977, 74, 2639-2643.
79. Heller, E. J.; Sundberg, R. L.; Tannor, D. J. Phys. Chem. 1982, 86, 1822-1833.
80. Heller, E. J. Acc. Chem. Res. 1981, 14, 368-375.
81. Schachtschneider, J. H. Technical Report Nos. 231-264 and 57-65; Shell Development Co.: Emeryville, CA, 1964-1965.
82. Wilson, E. B., Jr.; Decius, J. C.; Cross, P. C. Molecular Vibrations; Dover Publications: New York, 1980.
83. 17
84. u HOMOs typical of wild-type CUA sites, and that this HOMO is fully delocalized in PCyoA as in the MV model.
85. Guckert, J. A.; Lowery, M. D.; Solomon, E. I. J. Am. Chem. Soc. 1995, 117, 2817-2844.
86. 2 plane should allow some flexibility in the positions of the S(Cys) atoms.
87. Blondin, G.; Girerd, J.-J. Chem. Rev. 1990, 90, 1359-1376.
88. Girerd, J.-J. J. Chem. Phys. 1983, 79, 1766-1775.
89. Piepho, S. B.; Krausz, E. R.; Schatz, P. N. J. Am. Chem. Soc. 1978, 100, 2996-3005.
90. Abrahamson, H. B.; Frazier, C. C.; Ginley D. S.; Gray, H. B.; Lilienthal, J.; Tyler, D. R.; Wrighton, M. S. Inorg. Chem. 1977, 16, 1554-1556.
91. AB diminished.
92. Beratan, J. N.; Betts, J. N.; Onuchic, J. N. Science 1991, 252, 1285-1288.
93. Marcus, R. A.; Sutin, N. Biochim. Biophys. Acta 1985, 811, 265-322.
94. Newton, M. D. Chem. Rev. 1991, 91, 767-792.
95. Dennison, C.; Berg, A.; de Vries, S.; Canters, G. W. FEBS Lett. 1996, 394, 340-344.
96. The ∼6-fold greater covalency of S(Cys) relative to N(His)gives the W104/C200 path a ∼13-fold overall advantage over a D158/H161 path, assuming equal ET rates from cytochrome c to D158 or W104.
97. Brzezinski, P. Biochemistry 1996, 35, 5611-5615.
98. Bominaar, E. L.; Achim, C.; Borshch, S. A.; Girerd, J. J.; Münck, E. Inorg. Chem. 1997, 36, 3689-3701.
99. Hupp, J. T.; Zhang, X. L. J. Phys. Chem. 1995, 99, 853-855.