Reinvestigation of the method used to map the electronic structure of blue copper proteins by NMR relaxation

  • D. Flemming Hansen
  • Serge I. Gorelsky
  • Ritimukta Sarangi
  • Keith O. Hodgson
  • Britt Hedman
  • Hans E. M. Christensen
  • Edward I. Solomon
  • Jens J. Led
Original Paper

Abstract

A previous method for mapping the electron spin distribution in blue copper proteins by paramagnetic nuclear magnetic resonance (NMR) relaxation (Hansen DF, Led JJ, 2004, J Am Chem Soc 126:1247–1253) suggested that the blue copper site of plastocyanin from Anabaena variabilis (A.v.) is less covalent than those found for other plastocyanins by other experimental methods, such as X-ray absorption spectroscopy. Here, a detailed spectroscopic study revealed that the electronic structure of A.v. plastocyanin is similar to those of other plastocyanins. Therefore, the NMR approach was reinvestigated using a more accurate geometric structure as the basis for the mapping, in contrast to the previous approach, as well as a more complete spin distribution model including Gaussian-type natural atomic orbitals instead of Slater-type hydrogen-like atomic orbitals. The refinement results in a good agreement between the electron spin density derived from paramagnetic NMR and the electronic structure description obtained by the other experimental methods. The refined approach was evaluated against density functional theory (DFT) calculations on a model complex of the metal site of plastocyanin in the crystal phase. In general, the agreement between the experimental paramagnetic relaxation rates and the corresponding rates obtained by the DFT calculations is good. Small deviations are attributed to minor differences between the solution structure and the crystal structure outside the first coordination sphere. Overall, the refined approach provides a complementary experimental method for determining the electronic structure of paramagnetic metalloproteins, provided that an accurate geometric structure is available.

Keywords

Electronic structure Blue copper proteins Plastocyanin NMR Paramagnetic nuclear relaxation DFT 

Abbreviations

A.v.

Anabaena variabilis

DFT

Density functional theory

ENDOR

Electron–nuclear double resonance

EPR

Electron paramagnetic resonance

EXAFS

Extended X-ray absorption fine structure

LUMO

Lowest unoccupied molecular orbital

MCD

Magnetic circular dichroism

NMR

Nuclear magnetic resonance

SERF

Signal eliminating relaxation filter

XAS

X-ray absorption spectroscopy

Supplementary material

775_2005_70_MOESM1_ESM.pdf (174 kb)
Supplementary material

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Copyright information

© SBIC 2006

Authors and Affiliations

  • D. Flemming Hansen
    • 1
  • Serge I. Gorelsky
    • 2
  • Ritimukta Sarangi
    • 2
  • Keith O. Hodgson
    • 2
    • 3
  • Britt Hedman
    • 3
  • Hans E. M. Christensen
    • 4
  • Edward I. Solomon
    • 2
  • Jens J. Led
    • 1
  1. 1.Department of ChemistryUniversity of CopenhagenCopenhagenDenmark
  2. 2.Department of ChemistryStanford UniversityStanfordUSA
  3. 3.Stanford Synchrotron Radiation Laboratory, Stanford Linear Accelerator CenterStanford UniversityStanfordUSA
  4. 4.Department of ChemistryThe Technical University of DenmarkKgs. LyngbyDenmark

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