High-resolution ¹³C NMR indicates that changes in the dynamics of polyproline II conformations induce collagen I...

Collagen I is a 300 nm long fibrous protein that plays an important role in maintaining the structure of several tissues, such as the dermis, bone, enamel and cornea. In these tissues, collagen is found in the form of fibrils, which can be several microns in length and have different diameters. Collagen-collagen interactions rely mainly on the hydrogen bond (H-bond) network and display a very strong sensitivity to temperature; at the physiological temperature, it forms micro to macro fibrils but tends to be dissolved into a triple helix at 5 °C. It has been argued that the temperature-dependent structural transformation of the more flexible regions of collagen is mainly responsible for this transition. In the present work, we used ¹³C nuclear magnetic resonance (NMR) spectroscopy with magic angle spinning (MAS) technique to acquire local and unusual high-resolution information on the conformations and dynamics of collagen in the microfibril form (at the physiological temperature) and dissolved form (at 5 °C). The obtained data showed that at physiological temperatures, about 60% of the dihedral angles in the collagen are in the polyproline II (PII) conformation, which resulted in higher dynamics than the other residues. These residues displayed chemical shifts in previously assigned regions close to amino acids. Alternatively, the regions assigned to imino acid-rich regions displayed the strongest decrease in dynamics in contrast to the remaining conformations. Although the resolution remained relatively good at 5 °C, no strong shift was observed in the NMR spectrum for the other residues, indicating that the temperature affected mainly the PII residues. These results support the previous hypothesis that the PII regions are mainly responsible for the temperature-dependent tunability of collagen into fibrils. These data bring new insights into collagen mechanics and may help understand the impact of collagen defects in related diseases.