Resonance Raman spectral properties of FMN of bovine heart NADH:ubiquinone oxidoreductase suggesting a mechanism for the prevention of spontaneous production of reactive oxygen species

Biochemistry. 2013 Jan 8;52(1):98-104. doi: 10.1021/bi3011972. Epub 2012 Dec 20.

Abstract

A highly improved method for obtaining resonance Raman (RR) spectra provided spectra comparable to the best known flavoprotein spectra when the method was tested using bovine heart NADH:ubiquinone oxidoreductase (Complex I), a protein with a molecular mass of 1000 kDa, which causes the level of RR noise to be 1 order of magnitude higher than for most flavoproteins. The FMN RR band shift (1631/1633 cm(-1)) and the increase in the magnitude of the band at 1252 cm(-1) upon binding to Complex I suggest hydrogen bond formation involving one of the C=O groups [C(2)=O] of isoalloxazine to stabilize its quinoid form. This lowers the redox potential of FMN and the electron density of the O(2) binding site [a carbon atom, C(4a)] in the reduced form. Thus, spontaneous production of reactive oxygen species at the FMN site is prevented by minimizing the duration of the fully reduced state by accelerating the FMN oxidation and by weakening the O(2) affinity of C(4a). Other band shifts (1258/1252 cm(-1) and 1161/1158 cm(-1)) suggest a significantly weaker hydrogen bond to the NH group [N(3)-H] of isoalloxazine. This result, together with the reported X-ray structure in which N(3)-H is surrounded by negatively charged surface without hydrogen bond formation, suggests that N(3)-H is weakly but significantly polarized. The polarized N(3)-H, adjacent to the C(2)=O group, stabilizes the polarized state of C(2)=O to strengthen the hydrogen bond to C(2)=O. This could fine-tune the hydrogen bond strength. Other results show a high-dielectric constant environment and weak hydrogen bonds to the isoalloxazine, suggesting adaptability for various functional controls.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Binding Sites
  • Cattle
  • Electron Transport Complex I / chemistry
  • Electron Transport Complex I / metabolism*
  • Flavin Mononucleotide / chemistry
  • Flavin Mononucleotide / metabolism*
  • Flavins / chemistry
  • Flavins / metabolism
  • Hydrogen Bonding
  • Myocardium / chemistry
  • Myocardium / enzymology*
  • Myocardium / metabolism
  • Oxidation-Reduction
  • Oxygen / metabolism
  • Reactive Oxygen Species / metabolism*
  • Spectrum Analysis, Raman

Substances

  • Flavins
  • Reactive Oxygen Species
  • isoalloxazine
  • Flavin Mononucleotide
  • Electron Transport Complex I
  • Oxygen