Structural changes in the heme proximal pocket induced by nitric oxide binding to soluble guanylate cyclase

Biochemistry. 1998 Sep 8;37(36):12458-64. doi: 10.1021/bi9811563.

Abstract

When expressed in Escherichia coli, the heme domain [beta1(1-385)] of rat lung soluble guanylate cyclase (sGC) is isolated with a stoichiometric amount of bound heme [Zhao, Y., and Marletta, M. A. (1997) Biochemistry 36, 15959-15964]. Nitric oxide (NO) binding to the heme in beta1(1-385) leads to cleavage of the Fe-His bond and formation of a five-coordinate NO-heme complex. Addition of imidazole to the five-coordinate NO complex shifts the Soret peak from 399 to 420 nm, which appears to result from the formation of a six-coordinate NO complex. Removal of the added imidazole by gel filtration results in formation of the five-coordinate NO complex once again. The EPR spectrum of the putative six-coordinate NO complex has nine distinct derivative-shaped lines (a triplet of triplets), which is the signature spectrum of a six-coordinate NO complex with two nitrogen atoms as the axial ligands. [15N]Imidazole simplifies the six-coordinate NO complex EPR spectrum to six distinct derivative-shaped lines (a triplet of doublets), indicating that the other axial ligand in the six-coordinate NO complex is an imidazole molecule. These results show that NO binding to sGC not only leads to the cleavage of the Fe-His bond but also induces a conformational change which opens the heme proximal pocket large enough to accommodate an exogenous imidazole molecule. These observations have important implications for determining the NO activation mechanism of sGC.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Binding Sites
  • Electron Spin Resonance Spectroscopy
  • Guanylate Cyclase / chemistry
  • Guanylate Cyclase / metabolism*
  • Heme / chemistry*
  • Heme / metabolism*
  • Imidazoles / metabolism
  • Macromolecular Substances
  • Nitric Oxide / chemistry
  • Nitric Oxide / metabolism*
  • Peptide Fragments / chemistry
  • Peptide Fragments / metabolism
  • Rats
  • Solubility

Substances

  • Imidazoles
  • Macromolecular Substances
  • Peptide Fragments
  • Nitric Oxide
  • Heme
  • imidazole
  • Guanylate Cyclase
  • 1-methylimidazole
  • 4-methylimidazole