Distinct roles of a tyrosine-associated hydrogen-bond network in fine-tuning the structure and function of heme proteins: two cases designed for myoglobin

Mol Biosyst. 2016 Oct 20;12(10):3139-45. doi: 10.1039/c6mb00537c. Epub 2016 Aug 1.

Abstract

A hydrogen-bond (H-bond) network, specifically a Tyr-associated H-bond network, plays key roles in regulating the structure and function of proteins, as exemplified by abundant heme proteins in nature. To explore an approach for fine-tuning the structure and function of artificial heme proteins, we herein used myoglobin (Mb) as a model protein and introduced a Tyr residue in the secondary sphere of the heme active site at two different positions (107 and 138). We performed X-ray crystallography, UV-Vis spectroscopy, stopped-flow kinetics, and electron paramagnetic resonance (EPR) studies for the two single mutants, I107Y Mb and F138Y Mb, and compared to that of wild-type Mb under the same conditions. The results showed that both Tyr107 and Tyr138 form a distinct H-bond network involving water molecules and neighboring residues, which fine-tunes ligand binding to the heme iron and enhances the protein stability, respectively. Moreover, the Tyr107-associated H-bond network was shown to fine-tune both H2O2 binding and activation. With two cases demonstrated for Mb, this study suggests that the Tyr-associated H-bond network has distinct roles in regulating the protein structure, properties and functions, depending on its location in the protein scaffold. Therefore, it is possible to design a Tyr-associated H-bond network in general to create other artificial heme proteins with improved properties and functions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Crystallography, X-Ray
  • Heme / chemistry*
  • Hydrogen Bonding*
  • Hydrogen Peroxide / chemistry
  • Hydrogen Peroxide / metabolism
  • Ligands
  • Models, Molecular*
  • Mutation
  • Myoglobin / chemistry*
  • Myoglobin / metabolism*
  • Protein Conformation*
  • Protein Unfolding
  • Spectrum Analysis
  • Structure-Activity Relationship
  • Tyrosine / chemistry*

Substances

  • Ligands
  • Myoglobin
  • Tyrosine
  • Heme
  • Hydrogen Peroxide