Function of the connective tissues such as articular cartilage and tendon, which are vital for the quality of life, is highly dependent on the tissue microstructure. Magnetic resonance imaging remains a promising noninvasive technique to image early-stage degradation of such tissues. It has long been known that NMR spin relaxation rates in ordered collagenous tissues are dependent upon the orientation of the tissue relative to the magnetic field. This phenomenon, known as the Magic Angle effect, complicates the interpretation of the MR images of these tissues and simultaneously serves as a biomarker of tissue microstructure. Therefore, quantifying the relationship between molecular-level tissue-water interactions and measurable MRI parameters such as transverse relaxation time T2 bears clinical importance.
Our objective was to study anisotropic spin relaxation of water interacting with collagen, which is the major macromolecular component in tendon. Molecular dynamics simulations of water were carried out in the presence of a single tropocollagen fragment and a collagen microfibril structure constructed by assembling seven tropocollagen fragments in a minimum-energy configuration. The structures were solvated in boxes of TIP4P/2005 water, and the simulations were carried out for 20 ns. The water boxes were divided into hydration shells representing the proximity of water molecules to the collagen; the thicknesses of the shells were determined by the radial distribution function of water. Time evolution of the water H-H vectors in each hydration shell was obtained from the MD simulation trajectories; ensemble-averaged spectral density functions of motion were obtained as the Fourier transforms of the autocorrelation functions of the random functions describing the rotational motion of water molecules. The transverse spin-relaxation rates were then calculated using the equations derived from the Redfield relaxation theory. Our results allow quantifying the spin relaxation rates in different hydration shells with the binding patterns of water molecules with collagen structures.