Rates and equilibrium of CuA to heme a electron transfer in Paracoccus denitrificans cytochrome c oxidase

Biophysical Journal

Volumn 90, Issue 6, 2006, Pages 2131-2137

  Farver, Ole ^a   Grell, Ernst ^b   Ludwig, Bernd ^c   Michel, Hartmut ^b   Pecht, Israel ^d  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^c GOETHE UNIVERSITY   (Germany)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYLNICOTINAMIDE; CYTOCHROME C OXIDASE; HEME A; HEME DERIVATIVE; RADICAL; UNCLASSIFIED DRUG; COPPER; DRUG DERIVATIVE; HEME;

ANALYTICAL ERROR; ARTICLE; DIFFUSION COEFFICIENT; ELECTRON TRANSPORT; ENZYME DEGRADATION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME STRUCTURE; HEME SYNTHESIS; OXIDATION KINETICS; PARACOCCUS DENITRIFICANS; RADIOLYSIS; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; ENZYME ACTIVATION; ENZYMOLOGY; KINETICS; PULSE RADIOLYSIS;

BACTERIA (MICROORGANISMS); PARACOCCUS DENITRIFICANS;

COMPUTER SIMULATION; COPPER; ELECTRON TRANSPORT; ENZYME ACTIVATION; HEME; KINETICS; MODELS, CHEMICAL; MODELS, MOLECULAR; PARACOCCUS DENITRIFICANS; PULSE RADIOLYSIS;

EID: 33645984884     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.075440     Document Type: Article

References (68)

1. Richter, O.-M. H., and B. Ludwig. 2003. Cytochrome c oxidase: structure, function, and physiology of a redox-driven molecular machine. Rev. Physiol. Biochem. Pharmacol. 147:47-74.
2. Wikström, M. 2004. Cytochrome c oxidase: 25 years of the elusive proton pump. Biochim. Biophys. Acta. 1655:241-247.
3. Wikström, M. K. F. 1977. Proton pump coupled to cytochrome c oxidase in mitochondria. Nature. 266:271-273.
4. Babcock, G. T., and M. Wikström. 1992. Oxygen activation and the conservation of energy in cell respiration. Nature. 356:301-309.
5. Michel, H., J. Behr, A. Harrenga, and A. Kannt. 1998. Cytochrome c oxidase: structure and spectroscopy. Annu. Rev. Biophys. Biomol. Struct. 27:329-356.
6. Paula, S., A. Sucheta, I. Szundi, and Ó. Einarsdóttir. 1999. Proton and electron transfer during the reduction of molecular oxygen by fully reduced cytochrome c oxidase: a flow-flash investigation. Biochemistry. 38:3025-3033.
7. Wikström, M. 2000. Mechanism of proton translocation by cytochrome c oxidase: a new four-stroke histidine cycle. Biochim. Biophys. Acta. 1458:188-198.
8. Ruitenberg, M., A. Kannt, E. Bamberg, B. Ludwig, H. Michel, and K. Fendler. 2000. Single-electron reduction of the oxidized state is coupled to proton uptake via the K pathway in Paracoccus denitrificans cytochrome c oxidase. Proc. Natl. Acad. Sci. USA. 97:4632-4636.
9. Wikström, M., and M. I. Verkhovski. 2002. Proton translocation by cytochrome c oxidase in different phases of the catalytic cycle. Biochim. Biophys. Acta. 1555:128-132.
10. Michel, H. 1998. The mechanism of proton pumping by cytochrome c oxidase. Proc. Natl. Acad. Sci. USA. 95:12819-12824.
11. Backgren, C., G. Hummer, M. Wikström, and A. Puustinen. 2000. Proton translocation by cytochrome c oxidase can take place without the conserved glutamic acid in subunit I. Biochemistry. 39:7863-7867.
12. Bloch, D., I. Belevich, A. Jasaitis, C. Ribacka, A. Puustinen, M. I. Verkhovsky, and M. Wikström. 2004. The catalytic cycle of cytochrome c oxidase is not the sum of its two halves. Proc. Natl. Acad. Sci. USA. 101:529-533.
13. Olkhova, E., M. C. Hutter, M. A. Lill, V. Helms, and H. Michel. 2004. Dynamic water networks in cytochrome c oxidase from Paracoccus denitrificans investigated by molecular dynamics simulations. Biophys. J. 86:1873-1889.
14. Greenwood, C., and Q. H. Gibson. 1967. The reaction of reduced cytochrome c oxidase with oxygen. J. Biol. Chem. 242:1782-1787.
15. Wilson, M. T., C. Greenwood, M. Brunori, and E. Antonini. 1975. Kinetic studies on the reaction between cytochrome c oxidase and ferrocytochrome c. Biochem. J. 147:145-153.
16. Ferguson-Miller, S., D. Brautigam, and E. Margoliash. 1976. Correlation of the kinetics of electron transfer activity of various eukariotic cytochromes c with binding to mitochondrial cytochrome c oxidase. J. Biol. Chem. 251:1104-1115.
17. 1. Differential acetylation of lysyl residues in free and complexed cytochrome c. J. Biol. Chem. 255:4732-4739.
18. Ludwig, B., and Q. H. Gibson. 1981. Reactions of oxygen with cytochrome c oxidase from Paracoccus denitrificans. J. Biol. Chem. 256:10092-10098.
19. Antalis, T. M., and G. Palmer. 1982. Kinetic characterization of the interaction between cytochrome oxidase and cytochrome c. J. Biol. Chem. 257:6194-6206.
20. Bisson, R., G. C. M. Steffens, R. A. Capaldi, and G. Buse. 1982. Mapping the cytochrome c binding site on cytochrome c oxidase. FEBS Lett. 144:359-363.
21. Einarsdóttir, Ó., M. G. Choc, S. Weldon, and W. S. Caughey. 1988. The site and mechanism of dioxygen reduction in bovine heart cytochtrome c oxidase. J. Biol. Chem. 263:13641-13654.
22. 3 oxidase. Eur. J. Biochem. 269:2980-2988.
23. Hill, B. C. 1991. The reaction of the electrostatic cytochrome c-cytochrome oxidase complex with oxygen. J. Biol. Chem. 266:2219-2226.
24. Hill, B. C. 1994. Modeling the sequence of electron transfer reactions in the single turnover of reduced, mammalian cyrochrome c oxidase with oxygen. J. Biol. Chem. 269:2419-2425.
25. Morgan, J. E., P. M. Li, D.-J. Jang, M. Q. A. El-Sayed, and S. I. Chan. 1989. Electron transfer between cytochrome a and copper A in cytochrome c oxidase: a perturbed equilibrium study. Biochemistry. 28:6975-6983.
26. Nilsson, T. 1992. Photoinduced electron transfer from tris(2,2′-bipyridyl)ruthenium to cytochrome c oxidase. Proc. Natl. Acad. Sci. USA. 89:6497-6501.
27. Brzezinski, P., and M. T. Wilson. 1997. Photochemical electron injection into redox-active proteins. Proc. Natl. Acad. Sci. USA. 94:6176-6179.
28. Konstantinov, A. A., S. Siletsky, D. Mitchell, A. Kaulen, and R. B. Gennis. 1997. The roles of the two proton input channels in cytochrome c oxidase from Rhodobacter sphaeroides probed by the effects of site-directed mutations on time-resolved electrogenic intraprotein proton transfer. Proc. Natl. Acad. Sci. USA. 94:9085-9090.
29. Zaslavsky, D., R. C. Sadoski, K. Wang, B. Durham, R. B. Gennis, and F. Millett. 1998. Single electron reduction of cytochrome c oxidase compound F: resolution of partial steps by transient spectroscopy. Biochemistry. 37:14910-14916.
30. Geren, L. M., J. R. Beasley, B. R. Fine, A. J. Saunders, S. Hibdon, G. J. Pielak, B. Durham, and F. Millett. 1995. Design of a ruthenium-cytochrome c derivative to measure electron transfer to the initial acceptor in cytochrome c oxidase. J. Biol. Chem. 270:2466-2472.
31. Wang, K., Y. Zhen, R. Sadoski, S. Grinnell, L. Geren, S. Ferguson-Miller, B. Durham, and F. Millett. 1999. Definition of the interaction domain for cytochrome c on cytochrome c oxidase. J. Biol. Chem. 274:38042-38050.
32. Szundi, I., J. A. Cappucino, N. Borovok, B. Kotlyar, and Ó. Einarsdóttir. 2001. Photoinduced electron transfer in the cytochrome c/cytochrome c oxidase complex using thiouredopyrenetrisulfonate-labeled cytochrome c. Optical multichannel detection. Biochemistry. 40:2186-2193.
33. Farver, O., and I. Pecht. 1992. Low activation barriers characterize intramolecular electron transfer in ascorbate oxidase. Proc. Natl. Acad. Sci. USA. 89:8283-8287.
34. Farver, O., S. Wherland, and I. Pecht. 1994. 1994. Intramolecular electron transfer in ascorbate oxidase is enhanced in the presence of oxygen. J. Biol. Chem. 269:22933-22936.
35. Farver, O., L. Bendahl, L. K. Skov, and I. Pecht. 1999. Human ceruloplasmin. Intramolecular electron transfer kinetics and equilibration. J. Biol. Chem. 274:26135-26140.
36. Suzuki, S., T. Kohzuma, A. Deligeer, K. Yamagushi, N. Nakamura, S. Shidara, K. Kobayashi, and T. Tagawa. 1994. Pulse radiolysis studies on nitrite reductase from Achromobacter cycloclastes IAM 1013: evidence for intramolecular electron transfer from type 1 Cu to type 2 Cu. J. Am. Chem. Soc. 116:11145-11446.
37. Farver, O., R. R. Eady, G. Sawers, M. Prudencio, and I. Pecht. 2004. Met144ala mutation of the copper-containing nitrite reductase from Alcaligenes xylosoxidans reverses the intramolecular electron transfer. FEBS Lett. 561:173-176.
38. Kobayashi, K., S. Tagawa, and S. Suzuki. 1999. The pH-dependent changes of intramolecular electron transfer on copper-containing nitrite reductase. J. Biochem. (Tokyo). 126:408-412.
39. Farver, O., R. R. Eady, and I. Pecht. 2004. Reorganization energies of the individual copper centers in dissimilatory nitrite reductases. J. Phys. Chem. Ser. A. 108:9005-9007.
40. Suzuki, S., T. Maetani, K. Yamagushi, K. Kobayashi, and S. Tagawa. 2005. The intramolecular electron transfer between the type 1 Cu and the type 2 Cu in a mutant of Hyphomicrobium nitrite reductase. Chem. Lett. (Jpn.). 34:36-37.
41. 1-heme. Biochemistry. 36:13611-13616.
42. 1 nitrite reductase occurs over the same distances at very different rates depending on the source of the enzyme. Biochemistry. 40:8542-8547.
43. 1 nitrite reductase from Pseudomonas stutzeri; kinetics and thermodynamics. Biophys. Chem. 98:27-34.
44. 1 nitrite reductase. Proc. Natl. Acad. Sci. USA. 100:7622-7625.
45. Anderson, R. F., R. Hille, and V. Massey. 1986. The radical chemistry of milk xanthine oxidase as studied by radiation chemistry techniques. J. Biol. Chem. 261:15870-15876.
46. Hille, R., and R. F. Anderson. 1991. Electron transfer in milk xanthine oxidase as studied by pulse radiolysis. J. Biol. Chem. 266:5608-5615.
47. Kobayashi, K., M. Miki, K. Okamoto, and N. Nishino. 1993. Electron transfer process in milk xanthine dehydrogenase as studied by pulse radiolysis. J. Biol. Chem. 268:24642-24646.
48. Kobayashi, K., H. Une, and K. Hayashi. 1989. Electron transfer process in cytochrome oxidase after pulse radiolysis. J. Biol. Chem. 264:7976-7980.
49. Farver, O., O. Einarsdottir, and I. Pecht. 2000. Electron transfer rates and equilibrium within cytochrome c oxidase. Eur. J. Biochem. 267:950-954.
50. Iwata, S., C. Ostermeier, B. Ludwig, and H. Michel. 1995. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature. 376:660-669.
51. Tsukihara, T., H. Aoyama, E. Yamashita, T. Tomizaki, H. Yamaguchi, K. Shinzawa-Itoh, R. Nakashima, R. Yaono, and S. Yoshikawa. 1995. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å. Science. 269:1069-1074.
52. Tsukihara, T., H. Aoyama, E. Yamashita, T. Tomizaki, H. Yamaguchi, K. Shinzawa-Itoh, R. Nakashima, R. Yaono, and S. Yoshikawa. 1996. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science. 272:1136-1144.
53. V fragment. Proc. Natl. Acad. Sci. USA. 94:10547-10553.
54. Yoshikawa, S., K. Shinzawa-Itoh, R. Nakashima, R. Yaono, E. Yamashita, N. Inoue, M. Yao, M. J. Fei, C. Peters-Libeu, T. Mizushima, H. Yamaguchi, T. Tomizaki, and T. Tsukihara. 1998. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science. 280:1723-1729.
55. Harrenga, A., and H. Michel. 1999. The cytochrome c oxidase from Paracoccus denitrificans does not change the metal center ligation upon reduction. J. Biol. Chem. 274:33296-33299.
56. 3-cytochrome c oxidase from Thermus thermophilus. EMBO J. 19:1766-1776.
57. Svensson-Ek, M., J. Abramson, G. Larsson, S. Törnroth, P. Brzezinski, and S. Iwata. 2002. The X-ray crystal structures of wild-type and EQ (I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J. Mol. Biol. 321:329-339.
58. 3 from Paracoccus denitrificans and the 13-subunit beef heart enzyme. Biophys. J. 60:415-423.
59. 3 contributions and assignment of vibrational modes. Biochemistry. 38:1685-1694.
60. Pan, L. P., S. Hibdon, R.-Q. Liu, B. Durham, and F. Millett. 1993. Intracomplex electron transfer between ruthenium-cytochrome c derivatives and cytochrome c oxidase. Biochemistry. 32:8492-8498.
61. Richter, O.-M. H., K. L. Dürr, A. Kannt, B. Ludwig, F. M. Scandurra, A. Giuffrèe, P. Sarti, and P. Hellwig. 2005. Probing the access of protons to the K pathway in the Paracoccus denitrificans cytochrome c oxidase. FEBS J. 272:404-412.
62. Verkhovsky, M. I., J. E. Morgan, and M. Wikström. 1995. Control of electron delivery to the oxygen reduction site of cytochrome c oxidase: a role of protons. Biochemistry. 34:7483-7491.
63. Wikström, M., M. I. Verkhovsky, and G. Hummer. 2003. Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta. 1604:61-65.
64. Marcus, R. A., and N. Sutin. 1985. Electron transfers in chemistry and biology. Biochim. Biophys. Acta. 811:265-322.
65. Beratan, D. N., J. N. Onuchic, J. R. Winkler, and H. B. Gray. 1992. Electron-tunneling pathways in proteins. Science. 258:1740-1741.
66. Kurnikov, I. V., and D. N. Beratan. 1996. Ab initio based effective Hamiltonians for long-range electron transfer: Hartree-Fock analysis. J. Chem. Phys. 105:9561-9573.
67. Brzezinski, P. 1996. Internal electron-transfer reactions in cytochrome c oxidase. Biochemistry. 35:5611-5615.
68. Ramirez, B. E., B. G. Malmström, J. R. Winkler, and H. B. Gray. 1995. The currents of life: the terminal electron-transfer complex of respiration. Proc. Natl. Acad. Sci. USA. 92:11949-11951.