Locating Hydrogen Atoms in a Protein Using Neutron Crystallography

Approximately one-half of all atoms in a protein are hydrogen (H) atoms.

The Science

Hydrogen atoms are notoriously difficult to locate in proteins, yet they are key atoms in many of the chemical reactions of life and comprise one-half of a protein’s atoms. X-ray crystallography has been used to determine the atomic structure of many proteins and macromolecular complexes, but only a small fraction of the hydrogen atoms in these molecules can be located using this technique. In contrast, neutrons are scattered by hydrogen atoms, enabling determination of the position of these atoms in a protein molecule, though usually only to a medium resolution of about 2Å. Now, scientists at the Los Alamos Neutron Science Center have used the Protein Crystallography Station to determine the structure of a protein with the positions of its hydrogen atoms defined to an ultrahigh resolution of 1.1Å, the highest resolution ever for a neutron structure of a protein. They were able not only to locate nearly 95% of the hydrogen atoms in the protein at this resolution, but could determine the location of the hydrogen bonds that help determine the three-dimensional structure of the folded protein, and in some cases see how individual hydrogen atoms vibrate about their position in the protein. This new capability will improve understanding of the activity of many proteins, as well as guide computational modeling of systems such as protein-substrate and protein-drug complexes. The research was a collaboration of scientists at the University of Toledo, Los Alamos National Laboratory, and Oak Ridge National Laboratory.

Summary

H atoms play a variety of critical roles in proteins, including hydrogen bonding, electrostatic interactions, and catalysis. Unfortunately, H atoms are difficult to visualize in a three-dimensional context, and for the vast majority of crystal structures, their locations are inferred from the position of their neighboring heavy atom (C, N, O, S). These locations are based on atomic positions in databases of previously solved structures, general chemical knowledge, quantum mechanical calculations, or potential hydrogen bonding interactions. Together with the hydrophobic effect, H bonds are one of the primary interactions contributing to the formation of secondary and tertiary structural motifs and are crucial for protein–ligand recognition. For almost all X-ray crystal structures, including those solved at atomic resolution, H bonds are normally inferred from the heavy atom positions of the donor–acceptor pair, and their distances. In this structure, H atom positions have been experimentally determined, and the high resolution of the neutron diffraction data and the accuracy of the model allow researchers to analyze the observed H bonds within the protein and the water network in more detail.

Principal Investigator

Julian Chen
University of Toledo

BER Program Manager

Amy Swain

U.S. Department of Energy, Biological and Environmental Research (SC-33)
Biological Systems Science Division
[email protected]

References

Chen, J. C.-H., B.L. Hanson, S.Z. Fisher, P. Langan, and A.Y. Kovalevsky. 2012. “Direct Observation of Hydrogen Atom Dynamics and Interactions by Ultrahigh Resolution Neutron Protein Crystallography,” Proceedings of the National Academy of Sciences (USA) 109(38), 15301–306. DOI:10.1073/pnas.1208341109.