Molecular Origin of Piezo- and Pyroelectric Properties in Collagen Investigated by Molecular Dynamics Simulations

Abstract

Molecular dynamics simulations were used to study the effect of mechanical and thermal stimuli on the electrostatic properties of collagen model helices. Our model sequences were based on glycine proline and hydroxyproline amino acids. We find that longitudinal mechanical strain induces significant variation of the polarization of the collagen fibril. Such a phenomenon is determined by reorientation of the backbone polar groups, which are free to respond to the mechanical solicitation. This non-negligible effect is facilitated by the peculiar folding structure of the collagen helix, which is characterized by the absence of an extended hydrogen-bond network. The stretching/compression of the helix requires a concomitant winding/unwinding motion of the global structure; therefore, the shear components of the stress tensor are the components that most effectively induce structural modification associated to the piezoelectric response. The present calculations also report a pyroelectric response to thermal activation. Model calculations indicate that the pyroelectric effect is dominated by secondary components associated with the piezoelectric tensor.

Biomolecular Piezoelectric Materials: From Amino Acids to Living Tissues

“…The intensity of the polarization in the longitudinal direction changes due to the winding/unwinding motion of the structure when the physical force of compression/tension is applied, which is a piezoelectric effect. [129] In 2016, Zhu et al reported the piezoelectric effect on the "supertwisted" collagen structure using atomistic simulation of supertwisted collagen, and verified the piezoelectric mechanism. [130] The result shows that collagen represents unidirectional polarization along the longitudinal axis of collagen fibril, and the magnitude of polarization is varied when mechanical stress is applied on the collagen due to the reorientation and magnitude change of the permanent dipoles.…”

“…Each polypeptide chain possesses a characteristic major tripeptide repeat (GPX) sequence with glycine (G), proline (P), and several different amino acids (X) ( Figure a) 120–125. It was found that the piezoelectricity of collagen is due to this particular helical structure 13,126–129. The static polarization in the longitudinal direction of collagen is due to helically aligned peptide bonding and the hydroxyl group present at the side chain of hydroxyprolines.…”

“…The static polarization in the longitudinal direction of collagen is due to helically aligned peptide bonding and the hydroxyl group present at the side chain of hydroxyprolines. The intensity of the polarization in the longitudinal direction changes due to the winding/unwinding motion of the structure when the physical force of compression/tension is applied, which is a piezoelectric effect 129. In 2016, Zhu et al reported the piezoelectric effect on the “super‐twisted” collagen structure using atomistic simulation of super‐twisted collagen, and verified the piezoelectric mechanism 130.…”

“…[120][121][122][123][124][125] It was found that the piezoelectricity of collagen is due to this particular helical structure. [13,[126][127][128][129] The static polarization in the longitudinal direction of collagen is due to helically aligned peptide bonding and the hydroxyl group present at the side chain of hydroxyprolines. The intensity of the polarization in the longitudinal direction changes due to the winding/unwinding motion of the structure when the physical force of compression/tension is applied, which is a piezoelectric effect.…”

“…[5,8,9,17,21,23,24,148,[162][163][164] One of the reason why living cells exhibit piezoelectric properties is that their structures consist of piezoelectric proteins. [12,126,129,144,165] In 1957, Fukada investigated the quantitative piezoelectric property of bone by means of both direct and converse piezoelectric effects, and found that the value of the piezoelectric constant is about one-tenth that of quartz. [5] In addition, it was found that the piezoelectric property of bone disappeared after decollagenation, but still had piezoelectricity after demineralization.…”