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Protein elasticity based on conformations of sequential polypeptides: The biological elastic fiber

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Abstract

Fibrous elastin of the biological elastic fiber is a cross-linked condensed state in which there is roughly one-half polypeptide and one-half water. The precursor protein tropoelastin, a chemical fragmentation product α-elastin, and a sequential polypeptide (l·Val1-l·Pro2-Gly3-l·Val4-Gly5)n, which is a prominent primary structural feature of tropoelastin, are each soluble in all proportions in water at 20°C. On heating to physiological temperatures, each undergoes aggregation and forms a dense viscoelastic phase, which as the fiber itself, is about 60% water. This reversible heat-elicited condensed phase is called the coacervate. Circular dichroism studies show coacervation to be a process of increasing intramolecular order. Electron microscopy (light, scanning, and transmission) shows coacervation to be a process of increasing order intermolecularly. Thus a rise in temperature between 20 and 40°C results in an increase in order of the polypeptide. Coacervation is an inverse temperature transition, and the condensed state is anisotropic at the molecular level. Thermoelasticity studies in water on bovine ligamentum nuchae fibrous elastin and on γ-irradiation cross-linked polypentapeptide coacervates show increases in elastomeric force,f, over the same 20–40°C temperature range in which the inverse temperature transition gives rise to the coacervate, and the constancy off/T with temperature, once the transition is effectively completed, suggests a high-entropy component to the elastomeric force. Thus the data argue for an anisotropic-entropic elastomer.

Detailed conformational studies on the polypentapeptide result in the development of a β-spiral conformation in which there are regularly recurring β-turns in loose helical array (a structure that forms on raising the temperature) and in which there are recurring dynamic suspended segments that are the focal point of large, low-energy oscillatory motions called librations. The structure gives rise to a librational entropy mechanism of elasticity wherein the amplitudes of the rocking motions become damped on stretching. This perspective is substantiated by dielectric relaxation studies on the coacervate state and by characterization of synthetic analogs of the polypentapeptide. Dielectric relaxation studies on a concentrated state of about 60% water show the development of a regular structure over the same temperature range as for the development of the coacervate state, and the development of the regular structure with increasing temperature is seen to parallel the development of elastomeric force with increasing temperature. Increasing elastomeric force coincides with increasing regularity of structure! Synthetic analogs of the polypentapeptide, designed to interfere with the librational processes of the suspended segment, impair elastic function, and an analog that makes the β-turn more rigid results in increased elastic modulus. This development of a librational entropy mechanism for protein elasticity is a departure from the kinetic theory of rubber elasticity, the random network perspective that has dominated the traditional view of biological elasticity for the past several decades. The new perspective opens the way to insightful consideration of new elastomeric biomaterials with numerous biomedical applications.

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    Dan W. Urry

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Urry, D.W. Protein elasticity based on conformations of sequential polypeptides: The biological elastic fiber. J Protein Chem 3, 403–436 (1984). https://doi.org/10.1007/BF01025061

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