Stabilization and Anomalous Hydration of Collagen Fibril under Heating

Abstract

BackgroundType I collagen is the most common protein among higher vertebrates. It forms the basis of fibrous connective tissues (tendon, chord, skin, bones) and ensures mechanical stability and strength of these tissues. It is known, however, that separate triple-helical collagen macromolecules are unstable at physiological temperatures. We want to understand the mechanism of collagen stability at the intermolecular level. To this end, we study the collagen fibril, an intermediate level in the collagen hierarchy between triple-helical macromolecule and tendon.Methodology/Principal FindingWhen heating a native fibril sample, its Young’s modulus decreases in temperature range 20–58°C due to partial denaturation of triple-helices, but it is approximately constant at 58–75°C, because of stabilization by inter-molecular interactions. The stabilization temperature range 58–75°C has two further important features: here the fibril absorbs water under heating and the internal friction displays a peak. We relate these experimental findings to restructuring of collagen triple-helices in fibril. A theoretical description of the experimental results is provided via a generalization of the standard Zimm-Bragg model for the helix-coil transition. It takes into account intermolecular interactions of collagen triple-helices in fibril and describes water adsorption via the Langmuir mechanism.Conclusion/SignificanceWe uncovered an inter-molecular mechanism that stabilizes the fibril made of unstable collagen macromolecules. This mechanism can be relevant for explaining stability of collagen.

Physical mechanism for biopolymers to aggregate and maintain in non-equilibrium states

“…The non-equilibrium behaviors of peptide chains have also been observed in native collagen fibril 69, 70 and oxyhemoglobin crystals 71 . When one increase the temperature of native collagen fibril, the measured curves for Young’s modulus and logarithmic decrement are very different for different rates to increase the temperature, i.e.…”

Thermal and vibrational characterization of human skin

“…Usually, about 0.3-0.7 kg of unfreezable water remains associated per kilogram of a 'dry' protein [58]. Assuming that the average molar mass of one amino acid in collagen is 0.1 kg mol -1 , a roughly approximation leads to a value of 4 mol of water per moles of amino acid of collagen, which is slightly higher than the value determined by DVS [59] or X-ray diffraction for adsorbed multilayer water in collagen and collagen peptides [60], certainly because of the presence of HA in dermis.…”

Does knee joint cooling change in vivo patellar tendon mechanical properties?

“…A more plausible explanation for the increased tendon stiffness may lie in changes of the material properties of collagen fibrils. Recent research by Gevorkian and colleagues ( 2009 , 2013 ) has demonstrated that the collagen triple-helix constituting the microfibrils of collagen type I fibers (i.e., the by far most prevalent type of collagen in tendons) is thermally unstable at physiological temperatures. Studying collagenous material obtained from rat Achilles tendons, the authors found the Young’s modulus of collagen fibrils to be higher by ~14 % at 20 °C as compared to 40 °C (Gevorkian et al 2009 ).…”