Skip to main content
SpringerLink
Log in

EPR Analysis of Imidazole Binding to Methanosarcina acetivorans Protoglobin

  • Published:
Applied Magnetic Resonance Aims and scope Submit manuscript

Abstract

Protoglobins form an unusual class of globin proteins with surprising structural features, such as a highly ruffled heme. Electron paramagnetic resonance spectra of the frozen solution of the ferric imidazole complex of Methanosarcina acetivorans protoglobin reveal the existence of two low-spin ferric heme complexes. Hyperfine sublevel correlation spectroscopy was used to study the imidazole complex of this protoglobin as well as the imidazole complex of horse heart myoglobin for comparison. The spin Hamiltonian values obtained for the dominant contribution of the imidazole-ligated protoglobin agree with a heme conformation in which the plane of the exogenous imidazole is turned more than 30° versus the imidazole plane of the proximal histidine ligand. In turn, the electron paramagnetic resonance data of the minority complex indicate a second conformer, in which the two ligand planes are aligned almost parallel to each other with a lengthened iron–nitrogen bond for the exogenous imidazole ligand.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. S. Hou, T. Freitas, R.W. Larsen, M. Piatibratov, V. Sivozhelezov, A. Yamamoto, E.A. Melshkevitch, M. Zimmer, G.W. Ordal, M. Alam, Proc. Natl. Acad. Sci. USA 98, 9353 (2001)

    Article  ADS  Google Scholar 

  2. S.N. Vinogradov, D. Hoogewijs, X. Bailly, K. Mizuguchi, S. Dewilde, L. Moens, J.R. Vanfleteren, Gene 398, 132 (2007)

    Article  Google Scholar 

  3. T.A.K. Freitas, S. Hou, E.M. Dioum, J.A. Saito, J. Newhouse, G. Gonzalez, M.A. Gilles-Gonzalez, Proc. Natl. Acad. Sci. USA 101, 6675 (2004)

    Article  ADS  Google Scholar 

  4. T.A.K. Freitas, J.A. Saito, S. Hou, M. Alam, J. Inorg. Biochem. 99, 23 (2004)

    Article  Google Scholar 

  5. M. Nardini, A. Pesce, L. Thijs, J.A. Saito, S. Dewilde, M. Alam, P. Ascenzi, M. Coletta, C. Ciaccio, L. Moens, M. Bolognesi, EMBO Rep. 9, 157 (2008)

    Article  Google Scholar 

  6. J.E. Galagan, C. Nusbaum, A. Roy, M.G. Endrizzi, P. Macdonald, W. FitzHugh, S. Calvo, R. Engels, S. Smirnov, D. Anoor, A. Brown, N. Allen, J. Naylor, N. Stange-Thomann, J. Talamas, A. Tirrell, W. Ye, A. Zimmer, R.D. Barber, I. Cann, D.E. Graham, D.A. Grahame, A.M. Guss, R. Hedderich, C. Ingram-Smith, H.C. Kuettner, J.A. Krzycki, J.A. Leigh, W. Li, J. Liu, B. Mukhopadhyay, J.N. Reeve, K. Smith, T.A. Springer, L.A. Umayam, O. White, R.H. White, E.C. de Macario, J.G. Ferry, K.F. Jarrell, H. Jing, A.J.L. Macario, I. Paulsen, M. Pritchett, K.R. Sowers, R.V. Swanson, S.H. Zinder, E. Lander, W.W. Metcalf, B. Birren, Genome Res. 12, 532 (2002)

    Article  Google Scholar 

  7. A. Pesce, L. Tilleman, S. Dewilde, P. Ascenzi, M. Coletta, C. Ciaccio, L. Moens, M. Bolognesi, M. Nardini, IUBMB Life 63, 287 (2011)

    Article  Google Scholar 

  8. A. Pesce, L. Tilleman, J. Donné, E. Aste, P. Ascenzi, C. Ciaccio, M. Coletta, L. Moens, C. Viappiani, S. Dewilde, M. Bolognesi, M. Nardini, PLoS One 8, e66144 (2013)

    Article  ADS  Google Scholar 

  9. C. Lionetti, M.G. Guanziroli, F. Frigerio, P. Ascenzi, M. Bolognesi, J. Mol. Biol. 217, 409 (1991)

    Article  Google Scholar 

  10. S. Van Doorslaer, L. Tilleman, B. Verrept, F. Desmet, S. Maurelli, F. Trandafir, L. Moens, S. Dewilde, Inorg. Chem. 51, 8834 (2012)

    Article  Google Scholar 

  11. P. Höfer, A. Grupp, H. Nebenführ, M. Mehring, Chem. Phys. Lett. 132, 279 (1986)

    Article  ADS  Google Scholar 

  12. S. Stoll, A. Schweiger, J. Magn. Reson. 178, 42 (2006)

    Article  ADS  Google Scholar 

  13. F.A. Walker, Coord. Chem. Rev. 185–186, 471–534 (1999)

    Article  Google Scholar 

  14. C.P. Scholes, K.M. Falkowski, S. Chen, J. Bank, J. Am. Chem. Soc. 108, 1660 (1986)

    Article  Google Scholar 

  15. Y. Yamamoto, T. Suzuki, H. Hori, Biochim. Biophys. Acta 1248, 149 (1995)

    Article  Google Scholar 

  16. P.L. Hagedoorn, D.C. de Geus, W.R. Hagen, Eur. J. Biochem. 269, 4905 (2002)

    Article  Google Scholar 

  17. M. Ikeda-Saito, T. Iizuka, Biochim. Biophys. Acta 393, 335 (1975)

    Article  Google Scholar 

  18. R.E. Berry, X.D. Ding, TKh Shokhireva, A. Weichsel, W.R. Montfort, F.A. Walker, J. Biol. Inorg. Chem. 9, 135 (2004)

    Article  Google Scholar 

  19. L.A. Yatsunyk, A. Dawson, M.D. Carducci, G.S. Nichol, F.A. Walker, Inorg. Chem. 45, 5417 (2006)

    Article  Google Scholar 

  20. L.A. Yatsunyk, M.D. Carducci, F.A. Walker, J. Am. Chem. Soc. 125, 15986 (2003)

    Article  Google Scholar 

  21. I. García-Rubio, G. Mitrikas, J. Biol. Inog. Chem. 15, 929 (2010)

    Article  Google Scholar 

  22. E. Vinck, S. Van Doorslaer, S. Dewilde, L. Moens, J. Am. Chem. Soc. 126, 4516 (2004)

    Article  Google Scholar 

  23. J.S. Griffith, Nature 180, 30 (1957)

    Article  ADS  Google Scholar 

  24. C.P.S. Taylor, Biochim. Biophys. Acta 491, 137 (1977)

    Article  Google Scholar 

  25. P.J. Alonso, J.I. Martínez, I. García-Rubio, Coord. Chem. Rev. 251, 12 (2007)

    Article  Google Scholar 

  26. H. Sugimoto, M. Makino, H. Sawai, N. Kawada, K. Yosizato, Y.J. Shiro, Mol. Biol. 339, 873 (2004)

    Article  Google Scholar 

  27. R. Quinn, J. Selverstone Valentine, M.P. Byrn, C.E. Strouse, J. Am. Chem. Soc. 109, 3301 (1987)

    Article  Google Scholar 

  28. S.A. Dikanov, Yu. Tsvetkov, M.K. Bowman, A. Astashkin, Chem. Phys. Lett. 90, 149 (1982)

    Article  ADS  Google Scholar 

  29. A.I. Ioanitescu, S. Van Doorslaer, S. Dewilde, B. Endeward, L. Moens, Mol. Phys. 105, 2073 (2007)

    Article  ADS  Google Scholar 

  30. E. Vinck, S. Van Doorslaer, Phys. Chem. Chem. Phys. 6, 5324 (2004)

    Article  Google Scholar 

  31. M.J. Hunt, A.L. MacKay, D.T. Edmonds, Chem. Phys. Lett. 34, 473 (1975)

    Article  ADS  Google Scholar 

  32. Y.-N. Hsieh, G.V. Rubenacker, C.P. Cheng, T.L. Brown, J. Am. Chem. Soc. 99, 1384 (1977)

    Article  Google Scholar 

Download references

Acknowledgments

S. Van Doorslaer acknowledges the support from the Hercules Foundation, Flanders (Contract AUHA013). S. Van Doorslaer and S. Dewilde thank the Fund for Scientific Research–Flanders (FWO) for financial support (Grant G.0687.13).

Author information

Authors and Affiliations

  1. BIMEF Laboratory, Department of Physics, University of Antwerp, Universiteitsplein 1, 2610, Antwerp, Belgium

    Sabine Van Doorslaer & Martje van den Bosch

  2. PPES Laboratory, Department of Biomedical Sciences, University of Antwerp, Universiteitsplein 1, 2610, Antwerp, Belgium

    Lesley Tilleman & Sylvia Dewilde

Authors
  1. Sabine Van Doorslaer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martje van den Bosch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lesley Tilleman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sylvia Dewilde
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sabine Van Doorslaer.

Additional information

This paper is in honor of Giovanni Giacometti on the occasion of his 85th birthday.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 325 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Van Doorslaer, S., van den Bosch, M., Tilleman, L. et al. EPR Analysis of Imidazole Binding to Methanosarcina acetivorans Protoglobin. Appl Magn Reson 46, 421–433 (2015). https://doi.org/10.1007/s00723-014-0638-z

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00723-014-0638-z

Keywords

Search

Navigation