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. 1999 May;8(5):985–990. doi: 10.1110/ps.8.5.985

Evidence for a copper-coordinated histidine-tyrosine cross-link in the active site of cytochrome oxidase.

G Buse 1, T Soulimane 1, M Dewor 1, H E Meyer 1, M Blüggel 1
PMCID: PMC2144334  PMID: 10338009

Abstract

Following hints from X-ray data (Ostermeier C et al., 1997, Proc Natl Acad Sci USA 94:10547-10553; Yoshikawa S et al., 1998, Science 280: 1723-1729), chemical evidence is presented from four distantly related cytochrome-c oxidases for the existence of a copperB-coordinated His240-Tyr244) cross-link at the O2-activating Heme Fea3-CuB center in the catalytic subunit 1 of the enzyme. The early evolutionary invention of this unusual structure may have prevented damaging *OH-radical release at e(-)-transfer to dioxygen and thus have enabled O2 respiration.

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Selected References

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  1. Anderson S., de Bruijn M. H., Coulson A. R., Eperon I. C., Sanger F., Young I. G. Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol. 1982 Apr 25;156(4):683–717. doi: 10.1016/0022-2836(82)90137-1. [DOI] [PubMed] [Google Scholar]
  2. Babcock G. T., Wikström M. Oxygen activation and the conservation of energy in cell respiration. Nature. 1992 Mar 26;356(6367):301–309. doi: 10.1038/356301a0. [DOI] [PubMed] [Google Scholar]
  3. Buse G., Hensel S., Fee J. A. Evidence for cytochrome oxidase subunit I and a cytochrome c--subunit II fused protein in the cytochrome 'c1aa3' of Thermus thermophilus. How old is cytochrome oxidase? Eur J Biochem. 1989 Apr 15;181(1):261–268. doi: 10.1111/j.1432-1033.1989.tb14720.x. [DOI] [PubMed] [Google Scholar]
  4. Davies K. J., Delsignore M. E., Lin S. W. Protein damage and degradation by oxygen radicals. II. Modification of amino acids. J Biol Chem. 1987 Jul 15;262(20):9902–9907. [PubMed] [Google Scholar]
  5. Deckert G., Warren P. V., Gaasterland T., Young W. G., Lenox A. L., Graham D. E., Overbeek R., Snead M. A., Keller M., Aujay M. The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature. 1998 Mar 26;392(6674):353–358. doi: 10.1038/32831. [DOI] [PubMed] [Google Scholar]
  6. Ferguson-Miller Shelagh, Babcock Gerald T. Heme/Copper Terminal Oxidases. Chem Rev. 1996 Nov 7;96(7):2889–2908. doi: 10.1021/cr950051s. [DOI] [PubMed] [Google Scholar]
  7. Hensel S., Buse G. Studies on cytochrome-c oxidase, XIV. The amino-acid sequence of subunit I--proteinchemical methods for the analysis of a large hydrophobic membrane protein. Biol Chem Hoppe Seyler. 1990 May;371(5):411–422. doi: 10.1515/bchm3.1990.371.1.411. [DOI] [PubMed] [Google Scholar]
  8. Ito N., Phillips S. E., Yadav K. D., Knowles P. F. Crystal structure of a free radical enzyme, galactose oxidase. J Mol Biol. 1994 May 20;238(5):794–814. doi: 10.1006/jmbi.1994.1335. [DOI] [PubMed] [Google Scholar]
  9. Iwata S., Ostermeier C., Ludwig B., Michel H. Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature. 1995 Aug 24;376(6542):660–669. doi: 10.1038/376660a0. [DOI] [PubMed] [Google Scholar]
  10. Kannt A., Soulimane T., Buse G., Becker A., Bamberg E., Michel H. Electrical current generation and proton pumping catalyzed by the ba3-type cytochrome c oxidase from Thermus thermophilus. FEBS Lett. 1998 Aug 28;434(1-2):17–22. doi: 10.1016/s0014-5793(98)00942-9. [DOI] [PubMed] [Google Scholar]
  11. Keightley J. A., Zimmermann B. H., Mather M. W., Springer P., Pastuszyn A., Lawrence D. M., Fee J. A. Molecular genetic and protein chemical characterization of the cytochrome ba3 from Thermus thermophilus HB8. J Biol Chem. 1995 Sep 1;270(35):20345–20358. doi: 10.1074/jbc.270.35.20345. [DOI] [PubMed] [Google Scholar]
  12. Musser S. M., Chan S. I. Evolution of the cytochrome c oxidase proton pump. J Mol Evol. 1998 May;46(5):508–520. doi: 10.1007/pl00006332. [DOI] [PubMed] [Google Scholar]
  13. Ostermeier C., Harrenga A., Ermler U., Michel H. Structure at 2.7 A resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment. Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):10547–10553. doi: 10.1073/pnas.94.20.10547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Parsons M. R., Convery M. A., Wilmot C. M., Yadav K. D., Blakeley V., Corner A. S., Phillips S. E., McPherson M. J., Knowles P. F. Crystal structure of a quinoenzyme: copper amine oxidase of Escherichia coli at 2 A resolution. Structure. 1995 Nov 15;3(11):1171–1184. doi: 10.1016/s0969-2126(01)00253-2. [DOI] [PubMed] [Google Scholar]
  15. Preisig O., Anthamatten D., Hennecke H. Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3309–3313. doi: 10.1073/pnas.90.8.3309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Proshlyakov D. A., Pressler M. A., Babcock G. T. Dioxygen activation and bond cleavage by mixed-valence cytochrome c oxidase. Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8020–8025. doi: 10.1073/pnas.95.14.8020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Soulimane T., Buse G. Integral cytochrome-c oxidase. Preparation and progress towards a three-dimensional crystallization. Eur J Biochem. 1995 Jan 15;227(1-2):588–595. doi: 10.1111/j.1432-1033.1995.tb20429.x. [DOI] [PubMed] [Google Scholar]
  18. Soulimane T., Gohlke U., Huber R., Buse G. Three-dimensional crystals of cytochrome-c oxidase from Thermus thermophilus diffracting to 3.8 A resolution. FEBS Lett. 1995 Jul 10;368(1):132–134. doi: 10.1016/0014-5793(95)00623-h. [DOI] [PubMed] [Google Scholar]
  19. Steffens G. C., Soulimane T., Wolff G., Buse G. Stoichiometry and redox behaviour of metals in cytochrome-c oxidase. Eur J Biochem. 1993 May 1;213(3):1149–1157. doi: 10.1111/j.1432-1033.1993.tb17865.x. [DOI] [PubMed] [Google Scholar]
  20. Stetter K. O. Hyperthermophiles in the history of life. Ciba Found Symp. 1996;202:1–18. [PubMed] [Google Scholar]
  21. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., Yoshikawa S. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 A. Science. 1995 Aug 25;269(5227):1069–1074. doi: 10.1126/science.7652554. [DOI] [PubMed] [Google Scholar]
  22. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science. 1996 May 24;272(5265):1136–1144. doi: 10.1126/science.272.5265.1136. [DOI] [PubMed] [Google Scholar]
  23. Wikström M. Identification of the electron transfers in cytochrome oxidase that are coupled to proton-pumping. Nature. 1989 Apr 27;338(6218):776–778. doi: 10.1038/338776a0. [DOI] [PubMed] [Google Scholar]
  24. Yoshikawa S., Shinzawa-Itoh K., Nakashima R., Yaono R., Yamashita E., Inoue N., Yao M., Fei M. J., Libeu C. P., Mizushima T. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science. 1998 Jun 12;280(5370):1723–1729. doi: 10.1126/science.280.5370.1723. [DOI] [PubMed] [Google Scholar]
  25. Zumft W. G. The biological role of nitric oxide in bacteria. Arch Microbiol. 1993;160(4):253–264. doi: 10.1007/BF00292074. [DOI] [PubMed] [Google Scholar]
  26. van der Oost J., Haltia T., Raitio M., Saraste M. Genes coding for cytochrome c oxidase in Paracoccus denitrificans. J Bioenerg Biomembr. 1991 Apr;23(2):257–267. doi: 10.1007/BF00762221. [DOI] [PubMed] [Google Scholar]

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