A tensegrity model for hydrogen bond networks in proteins.

Robert P Bywater

doi:10.1016/j.heliyon.2017.e00307

Abstract

Hydrogen-bonding networks in proteins considered as structural tensile elements are in balance separately from any other stabilising interactions that may be in operation. The hydrogen bond arrangement in the network is reminiscent of tensegrity structures in architecture and sculpture. Tensegrity has been discussed before in cells and tissues and in proteins. In contrast to previous work only hydrogen bonds are studied here. The other interactions within proteins are either much stronger − covalent bonds connecting the atoms in the molecular skeleton or weaker forces like the so-called hydrophobic interactions. It has been demonstrated that the latter operate independently from hydrogen bonds. Each category of interaction must, if the protein is to have a stable structure, balance out. The hypothesis here is that the entire hydrogen bond network is in balance without any compensating contributions from other types of interaction. For sidechain-sidechain, sidechain-backbone and backbone-backbone hydrogen bonds in proteins, tensegrity balance (“closure”) is required over the entire length of the polypeptide chain that defines individually folding units in globular proteins (“domains”) as well as within the repeating elements in fibrous proteins that consist of extended chain structures. There is no closure to be found in extended structures that do not have repeating elements. This suggests an explanation as to why globular domains, as well as the repeat units in fibrous proteins, have to have a defined number of residues. Apart from networks of sidechain-sidechain hydrogen bonds there are certain key points at which this closure is achieved in the sidechain-backbone hydrogen bonds and these are associated with demarcation points at the start or end of stretches of secondary structure. Together, these three categories of hydrogen bond achieve the closure that is necessary for the stability of globular protein domains as well as repeating elements in fibrous proteins.

Highlights

Over a least a half a century, there has been an ongoing debate about the nature of the stabilizing forces that maintain the integrity of the 3D structure of proteins (Dill, 1990; Cooper, 2006; Bywater, 2013a, b; Ben-Naim, 1990; 2011)
There is one further difference that needs to be clarified at the outset: the “tendons” as defined by hydrogen bonding in proteins differ from those in architectural or sculptural constructs is the sense that the latter consist of tensile elements which are internally symmetrical, while hydrogen bonding is by its very nature polarized meaning that the tension in the structural element has a sense in one direction or another
Three main conclusions emerge from this work: 1. The proposed tensegrity model is upheld

Summary

Introduction

Over a least a half a century, there has been an ongoing debate about the nature of the stabilizing forces that maintain the integrity of the 3D structure of proteins (Dill, 1990; Cooper, 2006; Bywater, 2013a, b; Ben-Naim, 1990; 2011). The two that are said to play the most prominent role are so-called “hydrophobic interactions” (the lipophilic effect) and hydrogen bonding The latter are important as, in addition to providing a necessary cohesive force, they confer directionality (defined below). It is important to include hydrogen bonds linking atoms within the polypeptide backbone (BB), linking backbone atoms to atoms in the sidechains (BS) and those between sidechains and other sidechains (SS) When all these are taken into account the network of hydrogen bonds can be said to resemble a “tensegrity” structure as found in the architecture of Buckminster Fuller (1961) and the sculptures of Snelson (Heartney, 1971). As to the issue of directionality: the underlying mechanism of hydrogen bonding is both electrostatic (a strong dipolar interaction) and quantum mechanical (overlap between n and σ* or π* orbitals) These forces restrict bending and torsion around the “bond” which dictate the planar and rotational angles formed by the atoms participating in the bond

Methods

Results

Conclusion