Radial packing, order, and disorder in collagen fibrils

Abstract

Collagen fibrils resemble smectic, liquid crystals in being highly ordered axially but relatively disordered laterally. In some connective tissues, x-ray diffraction reveals three-dimensional crystallinity in the molecular packing within fibrils, although the continued presence of diffuse scatter indicates significant underlying disorder. In addition, several observations from electron microscopy suggest that the molecular packing is organized concentrically about the fibril core. In the present work, theoretical equatorial x-ray diffraction patterns for a number of models for collagen molecular packing are calculated and compared with the experimental data from tendon fibrils. None of the models suggested previously can account for both the crystalline Bragg peaks and the underlying diffuse scatter. In addition, models in which any of the nearest-neighbor, intermolecular vectors are perpendicular to the radial direction are inconsistent with the observed radial orientation of the principal approximately 4 nm Bragg spacing. Both multiple-start spiral and concentric ring models are devised in which one of the nearest-neighbor vectors is along the radial direction. These models are consistent with the radial orientation of the approximately 4 nm spacing, and energy minimization results in radially oriented crystalline domains separated by disordered grain boundaries. Theoretical x-ray diffraction patterns show a combination of sharp Bragg peaks and underlying diffuse scatter. Close agreement with the observed equatorial diffraction pattern is obtained. The concentric ring model is consistent with the observation that the diameters of collagen fibrils are restricted to discrete values.

Imaging the Nonlinear Susceptibility Tensor of Collagen by Nonlinear Optical Stokes Ellipsometry

“…The next simplest distribution was a constrained bimodal distribution, in which prior knowledge of fibril arrangement in collagen was explicitly incorporated. The inhomogeneity of the fibril distribution has been suggested in previous studies using an atomic force microscope, where collagen fibrils with different packing densities were observed in the fiber bundle (58,59). Fibrous collagen domains of opposite orientation were observed in the tail tendon by Han et al (60).…”

“…From previous measurements performed using SEM, NMR, and electron tomography, the most probable helix tilt angle was reported to be~17 . From the fiber diffraction studies, collagenous material was observed to be comprised of both a well-ordered fraction and a relatively disordered fraction (59). If it is reasonably assumed that the less-ordered fraction exhibits a broad distribution in orientations (corresponding to an effective c ð2Þ l;zzz =c ð2Þ l;zxx ¼ 3), the net distribution can be modeled as a sum of a normal distribution centered about zero with a mode at 17 and a broadly distributed antiparallel component.…”

Hierarchical Structure and Nanomechanics of Collagen Microfibrils from the Atomistic Scale Up

“…The equilibration of the hydrated (wet) collagen microfibril (Fig. 3c) leads to a density of ≈1.19 g/cm 3 , a value that is halfway between the density of water and the density of dehydrated (dry) collagen, which has been estimated at 1.34 g/cm 3 [49]. A Ramachandran analysis of the solvated system (Fig.…”

“…Since pioneering experimental works by Fraser, Hulmes, Hess, Orgel, Fratzl and others it is known that virtually all collagen-based tissues are organized into hierarchical structures, where the lowest hierarchical level consists of triple helical collagen molecules (Fig. 1) [2][3][4][5][6][7][8]. Collagen fibrils consist of high-aspect-ratio polypeptides, tropocollagen molecules, with a length of ≈300 nm and a diameter of about 1.5 nm, which are laterally staggered.…”

Emergence of Collagen Orientation Heterogeneity in Healing Infarcts and an Agent-Based Model

“…However, it may be possible that the local orientation of collagen monomers or fibrils produced by a cell could help determine the orientation of larger collagen fibers that form by aggregation of those smaller subunits, influencing collagen orientation over distances of hundreds of microns. Thus, although we did not think that enough is known about the control of orientation during fibrillogenesis to explicitly include these effects in our model, our results suggest that the role of fibrillogenesis in controlling collagen fiber alignment and heterogeneity warrants further study and modeling (e.g., (29)(30)(31)(32)). …”