Bis-histidine-coordinated hemes in four-helix bundles: how the geometry of the bundle controls the axial imidazole plane orientations in transmembrane cytochromes of mitochondrial complexes II and III and related proteins

J Biol Inorg Chem. 2008 May;13(4):481-98. doi: 10.1007/s00775-008-0372-9.

Abstract

Early investigation of the electron paramagnetic resonance spectra of bis-histidine-coordinated membrane-bound ferriheme proteins led to the description of a spectral signal that had only one resolved feature. These became known as "highly anisotropic low-spin" or "large g(max)" ferriheme centers. Extensive work with small-molecule model heme complexes showed that this spectroscopic signature occurs in bis-imidazole ferrihemes in which the planes of the imidazole ligands are nearly perpendicular, deltaphi = 57-90 degrees. In the last decade protein crystallographic studies have revealed the atomic structures of a number of examples of bis-histidine heme proteins. A frequent characteristic of these large g(max) ferrihemes in membrane-bound proteins is the occurrence of the heme within a four-helix bundle with a left-handed twist. The histidine ligands occur at the same level on two diametrically opposed helices of the bundle. These ligands have the same side-chain conformation and ligate heme iron on the bundle axis, resulting in a quasi-twofold symmetric structure. The two non-ligand-bearing helices also obey this symmetry, and have a conserved small residue, usually glycine, where the edge of the heme ring makes contact with the helix backbones. In many cases this small residue is preceded by a threonine or serine residue whose side-chain hydroxyl oxygen acts as a hydrogen-bond acceptor from the N(delta1) atom of the heme-ligating histidine. The deltaphi angle is thus determined by the common histidine side-chain conformation and the crossing angle of the ligand-bearing helices, in some cases constrained by hydrogen bonds to the serine/threonine residues on the non-ligand-bearing helices.

Publication types

  • Research Support, N.I.H., Extramural
  • Review

MeSH terms

  • Cell Membrane / chemistry
  • Cell Membrane / enzymology*
  • Cytochromes / chemistry*
  • Cytochromes / metabolism*
  • Heme / chemistry*
  • Heme / metabolism*
  • Histidine / chemistry
  • Histidine / metabolism
  • Imidazoles / chemistry*
  • Mitochondria / chemistry
  • Mitochondria / enzymology*

Substances

  • Cytochromes
  • Imidazoles
  • Heme
  • Histidine
  • imidazole