Skip to main content
Log in

Structural evidence for a proton transfer pathway coupled with haem reduction of cytochrome c″ from Methylophilus methylotrophus

  • Original Article
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

Abstract

The crystal structures of the oxidized and reduced forms of cytochrome c″ from Methylophilus methylotrophus were solved from X-ray synchrotron data to atomic resolution. The overall fold of the molecule in the two redox states is very similar and is comparable to that of the oxygen-binding protein from the purple phototrophic bacterium Rhodobacter sphaeroides. However, significant modifications occur near the haem group, in particular the detachment from axial binding of His95 observed upon reduction as well as the adoption of different conformations of some protonatable residues that form a possible proton path from the haem pocket to the protein surface. These changes are associated with the previously well characterized redox-Bohr behaviour of this protein. Furthermore they provide a model for one of the presently proposed mechanisms of proton translocation in the much more complex protein cytochrome c oxidase.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Costa HS, Santos H, Turner DL (1994) Eur J Biochem 223:783–789

    Article  PubMed  CAS  Google Scholar 

  2. Santos H, Turner DL (1988) Biochim Biophys Acta 954:277–286

    CAS  Google Scholar 

  3. Berry MJ, George SJ, Thomson AJ, Santos H, Turner DL (1990) Biochem J 270:413–417

    PubMed  CAS  Google Scholar 

  4. Costa HS, Santos H, Turner DL, Xavier AV (1992) Eur J Biochem 208:427–433

    Article  PubMed  CAS  Google Scholar 

  5. Costa H, Santos H, Turner DL (1996) Eur J Biophys 25:19–24

    Article  CAS  Google Scholar 

  6. Costa HS, Santos H, Turner DL (1993) Eur J Biochem 215:817–824

    Article  PubMed  CAS  Google Scholar 

  7. Indiani C, de Sanctis G, Neri F, Santos H, Smulevich G, Coletta M (2000) Biochemistry 39:8234–8242

    Article  PubMed  CAS  Google Scholar 

  8. Leys D, Backers K, Meyer TE, Hagen WR, Cusanovich MA, Van Beeumen JJ (2000) J Biol Chem 275:16050–16056

    Article  PubMed  CAS  Google Scholar 

  9. Papa S, Guerrieri F, Izzo G (1986) Methods Enzymol 126:331–343

    PubMed  CAS  Google Scholar 

  10. Xavier AV (2004) Biochim Biophys Acta 1658:23–30

    Article  PubMed  CAS  Google Scholar 

  11. Wikstrom M (2004) Biochim Biophys Acta 1655:241–247

    Article  PubMed  CAS  Google Scholar 

  12. Enguita FJ, Rodrigues L, Archer M, Sieker L, Rodrigues A, Pohl E, Turner DL, Santos H, Carrondo MA (2003) Acta Crystallogr D Biol Crystallogr 59:580–583

    Article  PubMed  CAS  Google Scholar 

  13. Pohl E, Gonzalez A, Hermes C, van Silfhout RG (2001) J Synchrotron Rad 8:1113–1120

    Article  CAS  Google Scholar 

  14. Collaborative Computational Project N (1994) Acta Crystallogr D Biol Crystallogr 50:760–763

    Article  Google Scholar 

  15. Vagin A, Teplyakov A (2000) Acta Crystallogr D Biol Crystallogr 56 (Pt 12):1622–1624

    Article  PubMed  CAS  Google Scholar 

  16. Terwilliger TC (2003) Methods Enzymol 374:22–37

    Article  PubMed  CAS  Google Scholar 

  17. Cowtan KD (1996) Acta Crystallogr D Biol Crystallogr 52:43–48

    Article  PubMed  CAS  Google Scholar 

  18. Morris RJ, Perrakis A, Lamzin VS (2003) Methods Enzymol 374:229–244

    PubMed  CAS  Google Scholar 

  19. McRee DE (1999) J Struct Biol 125:156–165

    Article  PubMed  CAS  Google Scholar 

  20. Sheldrick GM, Sheneider TR (1997) In: Sweet RM, Carter CW Jr (eds) Methods in enzymology. Academic, Orlando, pp 319–343

  21. Murshudov GN, Vagin AA, Lebedev A, Wilson KS, Dodson EJ (1999) Acta Crystallogr D Biol Crystallogr 55 (Pt 1):247–255

    Article  PubMed  CAS  Google Scholar 

  22. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) J Appl Cryst 26:283–291

    Article  CAS  Google Scholar 

  23. Fiser A, Sali A (2003) Methods Enzymol 374:461–491

    PubMed  CAS  Google Scholar 

  24. DeLano WL (2002) The PyMOL molecular graphics system. Delano Scientific, San Carlos

    Google Scholar 

  25. Brennan L, Turner DL, Fareleira P, Santos H (2001) J Mol Biol 308:353–365

    Article  PubMed  CAS  Google Scholar 

  26. Frazao C, Enguita FJ, Coelho R, Sheldrick GM, Navarro JA, Hervas M, De la Rosa MA, Carrondo MA (2001) J Biol Inorg Chem 6:324–332

    Article  PubMed  CAS  Google Scholar 

  27. Allen JW, Daltrop O, Stevens JM, Ferguson SJ (2003) Philos Trans R Soc Lond B Biol Sci 358:255–266

    Article  PubMed  CAS  Google Scholar 

  28. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Proc Natl Acad Sci USA 98:10037–10041

    Article  PubMed  CAS  Google Scholar 

  29. Fulop V, Ridout CJ, Greenwood C, Hajdu J (1995) Structure 3:1225–1233

    Article  PubMed  CAS  Google Scholar 

  30. Williams PA, Fulop V, Garman EF, Saunders NF, Ferguson SJ, Hajdu J (1997) Nature 389:406–412

    Article  PubMed  CAS  Google Scholar 

  31. Dias JM, Alves T, Bonifacio C, Pereira AS, Trincao J, Bourgeois D, Moura I, Romao MJ (2004) Structure (Camb) 12:961–973

    Article  CAS  Google Scholar 

  32. Wikstrom M, Verkhovsky MI (2002) Biochim Biophys Acta 1555:128–132

    Article  PubMed  CAS  Google Scholar 

  33. Wikstrom M, Verkhovsky MI, Hummer G (2003) Biochim Biophys Acta 1604:61–65

    Article  PubMed  CAS  Google Scholar 

  34. Bento I, Matias PM, Baptista AM, da Costa PN, van Dongen WM, Saraiva LM, Schneider TR, Soares CM, Carrondo MA (2004) Proteins 54:135–152

    Article  PubMed  CAS  Google Scholar 

  35. Michel H (1998) Proc Natl Acad Sci USA 95:12819–12824

    Article  PubMed  CAS  Google Scholar 

  36. Wikstrom M (2000) Biochim Biophys Acta 1458:188–198

    Article  PubMed  CAS  Google Scholar 

  37. Wikstrom M (2000) Biochemistry 39:3515–3519

    Article  PubMed  CAS  Google Scholar 

  38. Xavier AV (2002) FEBS Lett 532:261–266

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

Access to the European Molecular Biology Laboratory–Deutsche Elektronen Synchrotron (EMBL-DESY) Hamburg Facility was supported through the European Commission program “Access to Research Infrastructure Action of the Improving Human Potential” grant HPRI-1999-CT-00017.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria Arménia Carrondo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Enguita, F.J., Pohl, E., Turner, D.L. et al. Structural evidence for a proton transfer pathway coupled with haem reduction of cytochrome c″ from Methylophilus methylotrophus . J Biol Inorg Chem 11, 189–196 (2006). https://doi.org/10.1007/s00775-005-0065-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-005-0065-6

Keywords

Navigation