Copper A of cytochrome c oxidase, a novel, long-embattled, biological electron-transfer site

European Journal of Biochemistry

Volumn 245, Issue 3, 1997, Pages 521-532

  Beinert, Helmut ^a,b  

^a UNIVERSITY OF WISCONSIN   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

copper thiolate complex; Cu hyperfine structure; CuA site; cytochrome c oxidase; mixed valence complex; nitrous oxide reductase; polynuclear metal cluster

Indexed keywords

COPPER; CYTOCHROME C OXIDASE;

BINDING SITE; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME BINDING; METAL BINDING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; REVIEW;

EID: 0030982183     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.t01-1-00521.x     Document Type: Review

References (113)

1. Beinert, H., Griffiths, D. E., Wharton, D. C. & Sands, R. H. (1962) Properties of the copper associated with cytochrome oxidase as studied by paramagnetic resonance spectroscopy, J. Biol. Chem. 237, 2337-2346.
2. Beinert, H. & Palmer, G. (1965) in Oxidases and related redox systems (King, T. E., Mason, H. S. & Morrison, M., eds) pp. 567-590, John Wiley & Sons, New York.
3. Beinert, H. (1966) in The biochemistry of copper (Peisach, J., Aisen, P. & Blumberg, W. E., eds) pp. 213-234, Academic Press, New York.
4. 3 in cytochrome c oxidase, Biochim. Biophys. Acta 81, 405-407.
5. Morrison, M., Horie, S. & Mason, H. S. (1963) Cytochrome c oxidase components: II. A study of the copper in cytochrome c oxidase, J. Biol. Chem. 238, 2220-2224.
6. Van Gelder, B. F. & Beinert, H. (1969) Studies of the heme components of cytochrome c oxidase by EPR spectroscopy, Biochim. Biophys. Acta 189, 1-24.
7. Palmer, G., Babcock, G. T. & Vickery, L. E. (1976) A model for cytochrome oxidase, Proc. Natl Acad. Sci USA 73, 2206-2210.
8. Elvehjem, C. A. (1931) The role of iron and copper in the growth and metabolism of yeast, J. Biol. Chem. 90, 111-132.
9. Cohen, E. & Elvehjem, C. A. (1934) The relation of iron and copper to the cytochrome and oxidase content of animal tissues, J. Biol. Chem. 107, 97-105.
10. Keilin, D. & Hartree, E. F. (1939) Cytochrome and cytochrome oxidase, Proc. R. Soc. (Lond.) B127, 167-191.
11. Slater, E. C., Van Gelder, B. F. & Minnaert, K. (1964) in Oxidases and related redox systems (King, T. E., Mason, H. S. & Morrison, M., eds) pp. 667-706, John Wiley & Sons, New York.
12. Lemberg, M. R. (1969) Cytochrome oxidase, Physiol. Rev. 49, 48-121.
13. Eichel, B., Wainio, W. W. & Person, P. (1950) A partial separation and characterization of cytochrome oxidase and cytochrome b, J. Biol. Chem. 183, 89-103.
14. Kubowitz, F. (1937) Über die chemische Zusammensetzung der Kartoffeloxydase, Biochem. Z. 292, 221-229.
15. Keilin, D. & Mann, T. (1938) Polyphenol oxidase: Purification, nature and properties, Proc. R. Soc. (Lond.) B125, 187-204.
16. Malmström, B. G. & Neilands, J. B. (1964) Metalloproteins, Annu. Rev. Biochem. 33, 331-354.
17. Beinert, H. & Palmer, G. (1965) Contributions of EPR spectroscopy to our knowledge of oxidative enzymes, Adv. Enzymol. 27, 105-198.
18. Malmström, B. G. (1974) Cytochrome c oxidase: Some current biochemical and biophysical problems, Q. Rev. Biophys. 6, 389-431.
19. Chan, S. I., Brudvig, G. W., Martin, C. T. & Stevens, T. H. (1982) in Electron transport and oxygen utilization (Ho, C., ed.) pp. 171-177, Elsevier/North-Holland, Amsterdam.
20. Blair, D. F., Martin, C. T., Gelles, J., Wang, H., Brudvig, G. W., Stevens, T. H. & Chan, S. I. (1983) The metal centers of cytochrome c oxidase: Structures and interactions, Chem. Scr. 21, 43-53.
21. C?) ZnMg, Chem. Scr. 28A, 35-40.
22. A center in cytochrome c oxidase, FEBS Lett. 325, 49-52.
23. Fee, J. A., Antholine, W. E., Fan, C., Gurbiel, R. J., Surerus, K., Werst, M. & Hoffman, B. M. (1993) in Bioinorganic chemistry of copper (Karlin, K. D. & Tyeklár, Z., eds) pp. 485-500, Chapman & Hall, New York.
24. A: A novel mixed-valence dinuclear copper electron-transfer center, J. Am. Chem. Soc. 18, 11 501-11 514.
25. Massey, V. & Veeger, C. (1963) Biological oxidations, Annu. Rev. Biochem. 32, 579-638.
26. Peisach, J. (1966) in The biochemistry of copper (Peisach, J., Aisen, P. & Blumberg, W. E., eds) p. 211, Academic Press, New York.
27. Beinert, H. & Palmer, G. (1964) Oxidation-reduction of the copper component of cytochrome oxidase, J. Biol. Chem. 239, 1221-1227.
28. Griffiths, D. E. & Wharton, D. C. (1961) Studies of the electron transport system, XXXV, J. Biol. Chem. 236, 1850-1856.
29. Wharton, D. C. & Tzagoloff, A. (1964) Studies on the electron transfer system, LVII, J. Biol. Chem. 239, 2036-2041.
30. A in bovine cytochrome c oxidase determined by low-temperature magnetic-circular-dichroism spectroscopy, Biochem. J. 215, 303-316.
31. A(II) in bovine cytochrome c oxidase using magnetic circular dichroism as an optical detector of paramagnetic resonance, J. Inorg. Biochem. 28, 195-205.
32. A site in cytochrome c oxidase preparations, Ann. N.Y. Acad. Sci. 550, 47-52.
33. Griffiths, D. E. & Wharton, D. C. (1961) Studies of the electron transport system, XXXVI. J. Biol. Chem. 236, 1857-1862.
34. Gibson, Q. H. & Greenwood, C. (1963) Reactions of cytochrome oxidase with oxygen and carbon monoxide, Biochem. J. 86, 541-554.
35. Gibson, Q. H. & Greenwood, C. (1965) Kinetic observations on the near infrared band of cytochrome c oxidase, J. Biol. Chem. 240, 2694-2698.
36. Atherton, N. M., Gibson, Q. H. & Greenwood, C. (1963) Electron-spin-resonance changes on oxidation of cytochrome oxidase, Biochem. J. 86, 554-555.
37. Warburg, O. (1924) Über Eisen, den sauerstoffübertragenden Bestandteil des Atmungsferments, Biochem. Z. 152, 479-494.
38. Person, P., Wainio, W. W. & Eichel, B. (1953) The prosthetic groups of cytochrome oxidase and cytochrome b, J. Biol. Chem. 202, 369-381.
39. Zhang, Y.-Z. & Capaldi, R. A. (1988) Subunit composition of the transmembrane parts of beef heart cytochrome c oxidase, Ann. N.Y. Acad. Sci. 550, 3-7.
40. Buse, G. & Steffens, G. C. M. (1991) Cytochrome c oxidase in Paracoccus denitrificans. Protein, chemical, structural, and evolutionary aspects, J. Bioenerg. Biomembr. 23, 269-288.
41. [1-3] Primary structure and function of subunit II. Hoppe-Seyler's Z. Physiol. Chem. 360, 613-619.
42. Buse, G., Steffens, G. C. M., Biewald, R., Bruch, B. & Hensel, S. (1987) in Cytochrome systems: Molecular biology and bioenergetics (Papa, S., Chance, B. & Ernster, L., eds) pp. 261-270, Plenum Press, New York.
43. Steffens, G. C. M., Soulimane, T., Wolff, G. & Buse, G. (1993) Stoichiometry and redox behaviour of metals in cytochrome-c oxidase, Eur. J. Biochem. 213, 1149-1157.
44. Öblad, M., Selin, E., Malmström, B., Strid, L., Aasa, R. & Malmström, B. G. (1989) Analytical characterization of cytochrome oxidase preparations with regard to metal and phospholipid contents, peptide composition and catalytic activity, Biochim. Biophys. Acta 975, 267-270.
45. Bombelka, E., Richter, F.-W., Stroh, A. & Kadenbach, B. (1986) Analysis of the Cu, Fe, and Zn contents in cytochrome c oxidases from different species and tissues by proton-induced X-ray emission (pixe), Biochim. Biophys. Res. Commun. 140, 1007-1014.
46. Vänngård, T. (1972) in Copper proteins (Swartz, H. M., Bolton, J. R. & Borg, D. C., eds) pp. 411-447, John Wiley & Sons, New York.
47. Peisach, J. & Blumberg, W. E. (1974) Structural implications derived from the analysis of electron paramagnetic resonance spectra of natural and artificial copper proteins, Arch. Biochim. Biophys. 165, 691-708.
48. 15N-histidine-enriched enzyme and a molecular orbital interpretation, J. Am. Chem. Soc. 118, 8692-8699.
49. Minis, W. B., Peisach, J., Shaw, R. W. & Beinert, H. (1980) Electron spin echo studies of cytochrome c oxidase, J. Biol. Chem. 255, 6843-6846.
50. A in cytochrome c oxidase, J. Biol. Chem. 257, 12 106-12 113.
51. Chan, S. I. & Li, P. M. (1990) Cytochrome c oxidase: Understanding nature's design of a proton pump, Biochemistry 29, 1-12.
52. 3 from Thermus thermophilus, J. Am. Chem. Soc. 115, 10 888-10 894.
53. A in cytochrome c oxidase, Israel J. Chem. 25, 56-65.
54. Farrar, J. A., Formicka, G., Zeppezauer, M. & Thomson, A. J. (1996) Magnetic and optical properties of copper-substituted alcohol dehydrogenase: A bisthiolate copper (II) complex, Biochem. J. 317, 447-456.
55. Scott, R. A. (1989) X-ray absorption spectroscopic investigations of cytochrome c oxidase structure and function, Annu. Rev. Biophys. Biophys. Chem. 18, 137-158.
56. 2+ EPR spectra, J. Chem. Phys. 73, 3123-3131.
57. Froncisz, W., Scholes, C. P., Hyde, J. S., Wei, Y.-H., King, T. E., Shaw, R. W. & Beinert, H. (1979) Hyperfine structure resolved by 2 to 4 GHz EPR of cytochrome c oxidase, J. Biol. Chem. 254, 7482-7484.
58. Hoffman, B. M., Roberts, J. E., Swanson, M., Speck, S. H. & Margoliash, E. (1980) Copper electron-nuclear double resonance of cytochrome c oxidase, Proc. Natl Acad. Sci. USA 77, 1452-1456.
59. 3 and cytochrome bo, J. Bioenerg. Biomembr. 25, 121-136.
60. Saraste, M. (1990) Structural features of cytochrome oxidase. Q. Rev. Biophys. 23, 331-366.
61. van der Oost, J., Lappalainen, P., Musacchio, A., Warne, A., Lemieux, L., Rumbley, J., Gennis, R. B., Aasa, R., Pascher, T., Malmström, B. G. & Saraste, M. (1992) Restoration of a lost metal-binding site: Construction of two different copper sites into u subunit of the E. coli cytochrome o quinol oxidase complex, EMRO J. 11, 3209-3217.
62. van der Oost, J., Musacchio, A., Pauptit, R. A., Ceska, T. A., Wierenga, R. K. & Saraste, M. (1993) Crystallization and preliminary X-ray analysis of the periplasmic fragment of CyoA-a subunit of the Excherichia coli cytochrome o complex, J. Mol. Biol. 229, 794-796.
63. Wilmanns, M., Lappalainen, P., Kelly, M., Sauer-Eriksson, E. & Saraste, M. (1995) Crystal structure of the membrane-exposed domain from a respiratory quinol oxidase complex with an engineered dinuclear copper center, Proc. Natl Acad. Sci. USA 92, 11955-11959.
64. A domains, Proc. Natl Acad. Sci. USA 92, 7167-7171.
65. 3-type oxidase of Bacillus subtilis is a mixed-valence binuclear copper centre, FEBS Lett. 340, 109-113.
66. 3 subunit II from Thermus thermophilus, Biochemistry 35, 3387-3395.
67. A site into the blue copper protein amicyanin from Thiobacillus versutus, FEBS Lett. 365, 92-94.
68. Hay, M., Richards, J. H. & Lu, Y. (1996) Construction and characterization of an azurin analog for the purple copper site in cytochrome c oxidase, Proc. Natl Acad. Sci. USA 93, 461-464.
69. Coyle, C. L., Zumft, W. G., Kroneck, P. M. H., Körner, H. & Jakob, W. (1985) Nitrous oxide reductase from denitrifying Pseudomonas perfectomarina: Purification and properties of a novel multicopper enzyme, Eur. J. Biochem. 153, 459-467.
70. Kroneck, P. M. H., Antholine, W. E., Riester, J. & Zumft, W. G. (1988) The cupric site in nitrous oxide reductase contains a mixed-valence [Cu(II), Cu(I)] binuclear center: A multifrequency electron paramagnetic resonance investigation, FEBS Lett. 242, 70-74.
71. 2O reductase and in an inactive protein isolated from a mutant deficient in copper-site biosynthesis, Inorg. Chem. 30, 3006-3011.
72. Farrar, J. A., Thomson, A. J., Cheesman, M. R., Dooley, D. M. & Zumft, W. G. (1991) A model of the copper centres of nitrous oxide reductase (Pseudomonas stutzeri): Evidence from optical, EPR and MCD spectroscopy, FEBS Lett. 294, 11-15.
73. Jin, H., Thomann, H., Coyle, C. L. & Zumft, W. G. (1989) Copper coordination in nitrous oxide reductase from Pseudomonas stutzeri, J. Am. Chem. Soc. 111, 4262-4269.
74. Antholine, W. E., Kastrau, D. H. W., Steffens, G. C. M., Buse, G., Zumft, W. G. & Kroneck, P. M. H. (1992) A comparative EPR investigation of the multicopper proteins nitrous-oxide reductase and cytochrome c oxidase, Eur. J. Biochem. 209, 875-881.
75. Li, P. M., Malmström, B. G. & Chan, S. I. (1989) The nature of CuA in cytochrome c oxidase, FEBS Lett. 248, 210-211.
76. 2O reductase and cytochrome-c oxidase, Eur. J. Biochem. 208, 31-40.
77. Yoshikawa, S., Tera, T., Takahashi, Y., Tsukihara, T. & Caughey, W. S. (1988) Crystalline cytochrome c oxidase of bovine heart mitochondrial membrane: Composition and X-ray diffraction studies. Proc. Natl Acad. Sci. USA 85, 1354-1358.
78. A center of cytochrome oxidase, Biochemistry 33, 10401-10407.
79. B center, Angew. Chem. Int. Ed. Engl. 34, 1488-1492.
80. 3+, Inorg. Chem. 34, 1302-1303.
81. 2O reductase are tetrahedrally distorted type 1 Cu cysteinates, J. Am. Chem. Soc. 116, 10 805-10 806.
82. A centre from the cytochrome-c oxidase complex of Paracoccus denitrificans, Eur. J. Biochem. 232, 294-303.
83. A sites: Evidence from resonance Raman spectroscopy, J. Am. Chem. Soc. 117, 10759-10760.
84. A site of cytochrome c oxidase, J. Am. Chem. Soc. 118, 10436-10445.
85. 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. (1996) Far-red resonance Raman study of copper A in subunit II of cytochrome c oxidase, J. Am. Chem. Soc. 118, 3986-3987.
86. Iwata, S., Ostermeier, C., Ludwig, B. & Michel, H. (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans, Nature 376, 660-669.
87. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R. & Yoshikawa, S. (1995) Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å, Science 269, 1069-1074.
88. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T. Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R. & Yoshikawa, S. (1996) The whole structure of the 13 subunit oxidized cytochrome c oxidase at 2.8 Å, Science 272, 1136-1144.
89. 3 of Thermus thermophilus, Biophys. J. 71, 2823-2829.
90. Schatz, P. N. (1980) in Mixed valence compounds (Brown, D. B., ed.) pp. 115-150, D. Reidel Publishing Co., Dordrecht.
91. Houser, R. P., Halfen, J. A., Young, V. G. Jr. Blackburn, N. J. & Tolman, W. B. (1995) Structural characterization of the first example of a bis(μ-thiolato)dicopper(II) complex. Relevance to proposals for the electron transfer sites in cytochrome c oxidase and nitrous oxide reductase, J. Am. Chem. Soc. 117, 10745-10746.
92. A biological electron-transfer site. J. Am. Chem. Soc. 118, 2101-2102.
93. A site in cytochrome-c oxidase of Paracoccus denitrificans by replacement of Met227 with isoleucine, Eur. J. Biochem. 234, 686-693.
94. Hay, M. T., Milberg, R. M. & Lu, Y. (1996) Preparation and characterization of mercury and silver derivatives of an engineered purple copper center in azurin, J. Am. Chem. Soc. 118, 11 976-11977.
95. 3, J. Biol. Inorg. Chem. 1, 529-531.
96. Hemmerich, P. (1966) in The biochemistry of copper (Peisach, J., Aisen, P. & Blumberg, W. E., eds) pp. 15-34 and 269-270, Academic Press, New York.
97. Weintraub, S. T. & Wharton, D. C. (1981) The effects of copper depletion on cytochrome c oxidase, J. Biol. Chem. 256, 1669-1676.
98. Beinert, H., Hartzell, C. R., Van Gelder, B. F., Ganapathy, K., Mason, H. S. & Wharton, D. C. (1970) A reappraisal of copper depletion from cytochrome c oxidase, J. Biol. Chem. 245, 225-229.
99. Gennis, R. & Ferguson-Miller, S. (1995) Structure of cytochrome c oxidase, energy generator of aerobic life. Science 269, 1063-1064.
100. Hartzell, C. R. & Beinert, H. (1976) Oxido-reductive titrations of cytochrome c oxidase followed by EPR spectroscopy, Biochim. Biophys. Acta 423, 323-338.
101. A and cytochrome a in cytochrome c oxidase: Comparison to heme, copper, and sulfur radical complexes, J. Biol. Chem. 259, 11 001- 11 009.
102. Hill, B. C. (1991) The reaction of the electrostatic cytochrome c-cytochrome oxidase complex with oxygen, J. Biol. Chem. 266, 2219-2226.
103. Beinert, H., Meinen, W. & Palmer, G. (1962) Enzyme models and enzyme structure, Brookhaven Symp. Biol. 15, 229-265.
104. Gibson, J. F., Hall, D. O., Thornley, J. H. M. & Whatley, F. R. (1966) The iron complex in spinach ferredoxin, Proc. Natl Acad. Sci. USA 56, 987-990.
105. Farver, O., Wherland, S. & Pecht, I. (1994) Intramolecular electron transfer in ascorbate oxidase is enhanced in the presence of oxygen. J. Biol. Chem. 269, 22933-22936.
106. Solomon, E. I., Penfield, K. W., Gewirth, A. A., Lowery, M. D., Shadle, S. E., Guckert, J. A. & Lacroix, L. B. (1996) Electronic-structure of the oxidized and reduced blue copper sites: Contributions to the electron transfer pathway, reduction potential, and geometry, Inorg. Chim. Acta 243, 67-78.
107. Ramirez, B. E., Malmström, B. G., Winkler, J. R. & Gray, H. B. (1995) The currents of life: The terminal electron-transfer complex of respiration, Proc. Natl Acad. Sci. USA 92, 11 949-11 951.
108. Winkler, J. R., Malmström, B. G. & Gray, H. B. (1995) Rapid electron injection into multi-site metal proteins: Intramolecular electron transfer in cytochrome oxidase, Biophys. Chem. 54, 199-209.
109. 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. (1996) The CuA center of a soluble domain from Thermits cytochrome ba3. An NMR investigation of the paramagnetic protein. J. Am. Chem. Soc. 118, 11 658-11 659.
110. A domain, Biophys. Chem. 54, 191-197.
111. Chan, M. K., Kim, J. & Rees, D. C. (1993) The nitrogenase FeMo-cofactor and P-cluster pair: 2.2 Å resolution structures, Science 260, 792-794.
112. Johnson, M. K. (1994) in Encyclopedia of inorganic chemistry (King, R. B., ed.) pp. 1896-1915, John Wiley & Sons, Chichester.
113. 1 complex determined by MAD phasing at 1.5 Å resolution, Structure 4, 567-579.