The Magic-Angle effect1 is observed in MRI of ordered collagenous tissues such as articular cartilage. It is traditionally attributed to the formation of ice-like water-molecule bridges within the collagen fibrils forming part of the extracellular matrix (ECM) of those tissues. This effect reports on the microstructure of the collagen scaffold of the ECM. Its quantitative interpretation requires an understanding of the dynamics of water molecules in the hydration shell of the aligned collagen fibres in the tissue ECM.
Recent molecular dynamics (MD) simulations2 have demonstrated that, at least in isolated tropocollagen molecules, the collagen water bridges are short-lived rather than ice-like. We attribute this to the fact that the melting temperature of individual tropocollagen molecules is significantly lower than that of an assembled collagen fibre, resulting in high backbone mobility and consequently short (<1 ns) water bridge lifetimes. We hypothesise that the tropocollagen backbone in MD simulations can be rendered relatively immobile by using lower temperature and higher pressure, and that this could promote the formation of ice-like water bridges. This would enable MD simulations to emulate the hydration state of massive collagen fibres without the need for a significant increase in the size of the simulation.
1H spin relaxation rates and the dynamics of intramolecular proton-proton vectors of water molecules in the vicinity of an oriented tropocollagen molecule was investigated using all-atom molecular dynamics simulations. Residence times of water molecules near the collagen molecule were measured, and their histogram was constructed. The time evolution of the proton-proton vectors of the water molecules that exhibited long residence times was analysed, and the intra-molecular contribution to the 1H spin relaxation rate constant in the collagen-bound water was calculated. Spin relaxation rates were similarly calculated for different hydration layers. The results will inform quantitative interpretation of spin-relaxation measurements in collagenous tissues.