Skip to main content
SpringerLink
Log in

Peculiarities of cyanide binding to the ba 3-type cytochrome oxidase from the thermophilic bacterium Thermus thermophilus

  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Cytochrome c oxidase of the ba 3-type from Thermus thermophilus does not interact with cyanide in the oxidized state and acquires the ability to bind heme iron ligands only upon reduction. Cyanide complexes of the reduced heme a 3 in cytochrome ba 3 and in mitochondrial aa 3-type cytochrome oxidase are similar spectroscopically, but the a 2+3 -CN complex of cytochrome ba 3 is strikingly tight. Experiments have shown that the K d value of the cytochrome ba 3 complex with cyanide in the presence of reductants of the enzyme binuclear center does not exceed 10−8 M, which is four to five orders of magnitude less than the K d of the cyanide complex of the reduced heme a 3 of mitochondrial cytochrome oxidase. The tightness of the cytochrome ba 3 complex with cyanide is mainly associated with an extremely slow rate of the ligand dissociation (k off ≤ 10−7 sec−1), while the rate of binding (k on ∼ 102 M−1·sec−1) is similar to the rate observed for the mitochondrial cytochrome oxidase. It is proposed that cyanide dissociation from the cytochrome ba 3 binuclear center might be hindered sterically by the presence of the second ligand molecule in the coordination sphere of Cu 2+B . The rate of cyanide binding with the reduced heme a 3 does not depend on pH in the neutral area, but it approaches linear dependence on H+ activity in the alkaline region. Cyanide binding appears to be controlled by protonation of an enzyme group with pK a = 8.75.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

DAD:

diaminodurene

DM:

dodecyl maltoside

References

  1. Ferguson-Miller, S., and Babcock, G. T. (1996) Chem. Rev., 7, 2889–2907.

    Article  Google Scholar 

  2. Abramson, J., Riistama, S., Larsson, G., Jasaitis, A., Svensson-Ek, M., Laakkonen, L., Puuustinen, A., Iwata, S., and Wikstrom, M. (2000) Nat. Struct. Biol., 7, 910–917.

    Article  CAS  PubMed  Google Scholar 

  3. Abramson, J., Svensson-Ek, M., Byrne, B., and Iwata, S. (2001) Biochim. Biophys. Acta, 1544, 1–9.

    CAS  PubMed  Google Scholar 

  4. Liberman, E. A. (1977) Biofizika, 22, 1115–1128.

    CAS  PubMed  Google Scholar 

  5. Konstantinov, A. A. (1977) Dokl. Akad. Nauk SSSR, 237, 713–716.

    CAS  PubMed  Google Scholar 

  6. Artzatbanov, V. Y., Konstantinov, A. A., and Skulachev, V. P. (1978) FEBS Lett., 87, 180–185.

    Article  CAS  PubMed  Google Scholar 

  7. Iwata, S., Ostermeier, C., Ludwig, B., and Michel, H. (1995) Nature, 376, 660–669.

    Article  CAS  PubMed  Google Scholar 

  8. Tsukihara, T., Aoyama, H., Yamashita, E. I., Takashi, T., Yamaguichi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., and Yoshikawa, S. (1996) Science, 272, 1136–1144.

    Article  CAS  PubMed  Google Scholar 

  9. Soulimane, T., Buse, G., Bourenkov, G. P., Bartunik, H. D., Huber, R., and Than, M. E. (2000) EMBO J., 19, 1766–1776.

    Article  CAS  PubMed  Google Scholar 

  10. Pereira, M. M., Santana, M., and Teixeira, M. (2001) Biochim. Biophys. Acta, 1505, 185–208.

    Article  CAS  PubMed  Google Scholar 

  11. Pereira, M. M., Gomes, C. M., and Teixeira, M. (2002) FEBS Lett., 522, 14–18.

    Article  CAS  PubMed  Google Scholar 

  12. Pereira, M. M., and Teixeira, M. (2004) Biochim. Biophys. Acta, 1655, 340–346.

    Article  CAS  PubMed  Google Scholar 

  13. Svensson-Ek, M., Abramson, J., Larsson, G., Tornroth, S., Brzezinski, P., and Iwata, S. (2002) J. Mol. Biol., 321, 329–339.

    Article  CAS  PubMed  Google Scholar 

  14. Hunsicker-Wang, L. M., Pacoma, R. L., Chen, Y., Fee, J. A., and Stout, C. D. (2005) Acta Cryst., D61, 340–343.

    CAS  Google Scholar 

  15. Liu, B., Chen, Y., Doukov, T., Soltis, S. M., Stout, C. D., and Fee, J. A. (2009) Biochemistry, 48, 820–826.

    Article  CAS  PubMed  Google Scholar 

  16. Sousa, F. L., Verissimo, A. F., Baptista, A. M., Soulimane, T., Teixeira, M., and Pereira, M. M. (2008) Biophys. J., 94, 2434–2441.

    Article  CAS  PubMed  Google Scholar 

  17. Nicholls, P., and Soulimane, T. (2004) Biochim. Biophys. Acta, 1655, 381–387.

    Article  CAS  PubMed  Google Scholar 

  18. Siletskiy, S., Soulimane, T., Azarkina, N., Vygodina, T. V., Buse, G., Kaulen, A., and Konstantinov, A. (1999) FEBS Lett., 457, 98–102.

    Article  CAS  PubMed  Google Scholar 

  19. Fowler, L. R., Richardson, S. H., and Hatefi, Y. (1962) Biochim. Biophys. Acta, 64, 170–173.

    Article  CAS  PubMed  Google Scholar 

  20. Giuffre, A., Forte, E., Antonini, G., D’Itri, E., Brunori, M., Soulimane, T., and Buse, G. (1999) Biochemistry, 38, 1057–1065.

    Article  CAS  PubMed  Google Scholar 

  21. Nicholls, P., Petersen, L. C., Miller, M., and Hansen, F. B. (1976) Biochim. Biophys. Acta, 449, 188–196.

    Article  CAS  PubMed  Google Scholar 

  22. Farver, O., Chen, Y., Fee, J. A., and Pecht, I. (2006) FEBS Lett., 580, 3417–3421.

    Article  CAS  PubMed  Google Scholar 

  23. Tofani, L., Feis, A., Snoke, R. E., Berti, D., Baglioni, P., and Smulevich, G. (2004) Biophys. J., 87, 1186–1195.

    Article  CAS  PubMed  Google Scholar 

  24. Hill, B. C., and Marmor, S. (1991) Biochem. J., 279, 355–360.

    CAS  PubMed  Google Scholar 

  25. Antonini, E., Brunori, M., Greenwood, C., Malmstrom, B. G., and Rotilio, G. C. (1971) Eur. J. Biochem., 23, 396–400.

    Article  CAS  PubMed  Google Scholar 

  26. Van Buuren, K. J., Nicholis, P., and van Gelder, B. F. (1972) Biochim. Biophys. Acta, 256, 258–276.

    Article  PubMed  Google Scholar 

  27. Clark, W. M. (1960) Oxidation-Reduction Potentials of Organic Systems, Williams and Wilkins, Baltimore, MD.

    Google Scholar 

  28. Nikol’skii, B. P. (1964) Handbook of Chemistry [in Russian], Khimiya, Moscow.

    Google Scholar 

  29. Andreev, I. M., Myakotina, O. L., Popova, E. Y., and Konstantinov, A. A. (1983) Biokhimiya, 48, 219–223.

    CAS  Google Scholar 

  30. Ver Ploeg, D. A., and Alberty, R. A. (1968) J. Biol. Chem., 243, 435–440.

    Google Scholar 

  31. Shiro, Y., Iwata, T., Makino, R., Fujii, M., Isogai, Y., and Iizuka, T. (1993) J. Biol. Chem., 268, 19983–19990.

    CAS  PubMed  Google Scholar 

  32. Bolli, A., Ciaccio, C., Coletta, M., Nardini, M., Bolognesi, M., Pesce, A., Guertin, M., Visca, P., and Ascenzi, P. (2008) FEBS J., 275, 633–645.

    Article  CAS  PubMed  Google Scholar 

  33. Kim, Y., Babcock, G. T., Surerus, K. K., Fee, J. A., Dyer, B., Woodruff, W., and Oertling, A. (1998) Biospectroscopy, 4, 1–15.

    Article  PubMed  Google Scholar 

  34. Yoshikawa, S., and Caughey, W. S. (1990) J. Biol. Chem., 265, 7945–7958.

    CAS  PubMed  Google Scholar 

  35. Yoshikawa, S., Shinzawa-Itoh, K., and Tsukihara, T. (2000) J. Inorg. Biochem., 82, 1–7.

    Article  CAS  PubMed  Google Scholar 

  36. Qin, L., Liu, J., Mills, D. A., Proshlyakov, D. A., Hiser, C., and Ferguson-Miller, S. (2009) Biochemistry, 48, 5121–5130.

    Article  CAS  PubMed  Google Scholar 

  37. Surerus, K. K., Oertling, W. A., Fan, C., Gurbiel, R. J., Einarsdottir, O., Antholine, W. E., Dyer, R. B., Hoffman, B. M., Woodruff, W. H., and Fee, J. A. (1992) Proc. Natl. Acad. Sci. USA, 89, 3195–3199.

    Article  CAS  PubMed  Google Scholar 

  38. Oertling, W. A., Surerus, K. K., Einarsdyttir, O., Fee, J. A., Dyer, R. B., and Woodruff, W. H. (1994) Biochemistry, 33, 3128–3141.

    Article  CAS  PubMed  Google Scholar 

  39. Wilson, D. F., Erecinska, M., and Brocklehurst, E. S. (1972) Arch. Biochem. Biophys., 151, 180–187.

    Article  CAS  PubMed  Google Scholar 

  40. Andreev, I. M., Artzatbanov, V. Y., Konstantinov, A. A., and Skulachev, V. P. (1979) Dokl. Akad. Nauk SSSR, 244, 1013–1017.

    CAS  PubMed  Google Scholar 

  41. Andreev, I. M., and Konstantinov, A. A. (1983) Bioorg. Chem. (Moscow), 9, 216–227.

    CAS  Google Scholar 

  42. Konstantinov, A. A., Vygodina, T. V., and Andreev, I. M. (1986) FEBS Lett., 202, 229–234.

    Article  CAS  PubMed  Google Scholar 

  43. Jones, M. G., Bickar, D., Wilson, M. T., Brunori, M., Colisimo, A., and Sarti, P. (1984) Biochem. J., 220, 57–66.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119992, Moscow, Russia

    A. V. Kalinovich, N. V. Azarkina, T. V. Vygodina & A. A. Konstantinov

  2. Materials and Surface Science Institute, University of Limerick, Limerick, Ireland

    T. Soulimane

Authors
  1. A. V. Kalinovich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. V. Azarkina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. V. Vygodina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. Soulimane
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. A. Konstantinov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. A. Konstantinov.

Additional information

Original Russian Text © A. V. Kalinovich, N. V. Azarkina, T. V. Vygodina, T. Soulimane, A. A. Konstantinov, 2010, published in Biokhimiya, 2010, Vol. 75, No. 3, pp. 418–430.

Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM09-267, February 14, 2010.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kalinovich, A.V., Azarkina, N.V., Vygodina, T.V. et al. Peculiarities of cyanide binding to the ba 3-type cytochrome oxidase from the thermophilic bacterium Thermus thermophilus . Biochemistry Moscow 75, 342–352 (2010). https://doi.org/10.1134/S0006297910030119

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297910030119

Key words

Search

Navigation