Parallels between DNA and collagen \u2013 comparing elastic models of the double and triple helix

Fei Xu,Vikas Nanda,Hongning Zheng,Nicolas Clauvelin,Xiang-Jun Lu,Wilma K Olson

doi:10.1038/s41598-017-12878-3

Abstract

Multi-stranded helices are widespread in nature. The interplay of polymeric properties with biological function is seldom discussed. This study probes analogies between structural and mechanical properties of collagen and DNA. We modeled collagen with Eulerian rotational and translational parameters of adjacent rungs in the triple-helix ladder and developed statistical potentials by extracting the dispersion of the parameters from a database of atomic-resolution structures. The resulting elastic model provides a common quantitative way to describe collagen deformations upon interacting with integrins or matrix metalloproteinase and DNA deformations upon protein binding. On a larger scale, deformations in Type I collagen vary with a periodicity consistent with the D-periodic banding of higher-order fibers assemblies. This indicates that morphologies of natural higher-order collagen packing might be rooted in the characteristic deformation patterns.

Highlights

Biomacromolecules often adopt multi-stranded helical structures, such as the DNA double helix and the collagen triple helix
Individual chains adopt an extended, left-handed poly-proline type II (PPII) local helix, which supercoils upon formation of the triple-helix
In addition to providing insight into peptide models of collagen, the parameterization can be used to examine the in situ structure of type I collagen microfibrils, the major form of natural collagen, obtained by X-ray fiber diffraction[19]

Summary

Introduction

Biomacromolecules often adopt multi-stranded helical structures, such as the DNA double helix and the collagen triple helix. The degrees of freedom between two adjacent base pairs in DNA are reduced to three translational and three rotational parameters[3,4] Variation in these parameters observed across a dataset of high-resolution nucleic acid structures can be transformed into a set of empirical elastic functions that describe DNA deformability. This deformability underlies mechanical aspects of processes such as protein-induced DNA looping, DNA cyclization, and genomic nucleosome positioning that require effective modeling of hundreds of bases[5,6,7,8]. The elastic model developed in this study adapts the El Hassan-Calladine description of nucleic acid base-pair step parameters[18] to characterize the Gly/X/Y layers in the triple helix, appropriately modeling bending and shearing and eliminating the need for a rigid-rod approximation. Various correlations between triple helix conformations, ligand binding sites, and fibrillar packing have been noted[21,22]

Methods

Results

Conclusion