Coulombic interactions between partially charged main-chain atoms not hydrogen-bonded to each other influence the conformations of α-helices and antiparallel β-sheet. A new method for analysing the forces between hydrogen bonding groups in proteins includes all the Coulombic interactions

Abstract

An angle named γ has been employed to describe the geometry at a hydrogen bond between main-chain atoms of polypeptides. In antiparallel β-sheet, γ is normally positive, whereas, in parallel β-sheet and α-helices, it is negative. Although intriguing, no particular explanation has been offered to explain this result. We provide evidence that, in each case, the angular preference maximises the favourable Coulombic interaction between the partial negative charge on the carbonyl oxygen atom and the partial positive charge on the carbonyl carbon atom adjacent to the NH group to which it is hydrogen-bonded. Analyses of helices and β-sheets in native proteins using Lennard-Jones potentials suggest that these carbonyl-carbonyl interactions are significant components of the attractive forces holding main-chain CONH groups together and are even in some cases larger than the hydrogen bonds themselves.

A novel technique for analysing the forces holding together hydrogen bonding groups in proteins is presented. It can be regarded as a development of the Kabsch and Sander method of calculating the energy of hydrogen bonds between main-chain atoms. In their program, electrostatic interactions are calculated between appropriate pairs of atoms, i.e. NH binding to CO. Instead, in our method, the four N, H, C, and O atoms, in a peptide bond are taken as a unit and the interaction between two NHCO groups calculated. We also use a Lennard-Jones potential, rather than just measuring the Coulombic interaction. With this approach, account is taken of all types of interactions between partially charged atoms, not only the hydrogen bonds.